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Skctiox  TI. 


Part  II. 


An 

Intkodlhtion 
To 


NEMATOLOGY 


J.  R.  CHRISTIE 

Editor 


nail' 


ALBERT  HASSALL 

Born  in  Woolwich,  Kent,  England.  M.  R.  C.  V.  S.,  Royal  College  of  Veter- 
inary  Surgeons  London,  1886.  Inspector,  1887-1905;  Assistant  in  Zoology,  1905- 
1910;  Assistant  Zoologist,  1910-1922;  Associate  Zoologist,  1922-1924;  Zoologist, 
1924-1925;   Senior   Zoologist   and   Assistant   Chief   of   Zoological    Division,    1925- 

1932;  Collaborator,  1934- ;  Bureau  of  Animal  Industry,  U.  S.  Department  of 

Agriculture. 

Zoologist,  biblographer,  author  of  numerous  papers  in  parasitology,  compiler 
of  Index  Catalogue  of  Medical  and  Veterinary  Zoology  published  in  collaboration 
with  Stiles.     Nematologists'  best   friend  and  severest  critic. 


Section  II. 


Part  II. 


An 

Introduction 
To 


NEMATOLOGY 


J.  R.  CHRISTIE 
Editor 


y 


ALBERT  HASSALL 

Born  in  Woolwich,  Kent,  England.  M.  R.  C.  V.  S.,  Royal  College  of  Veter- 
inary Surgeons  London,  1886.  Inspector,  1887-1905;  Assistant  in  Zoology,  1905- 
1910;  Assistant  Zoologist,  1910-1922;  Associate  Zoologist,  1922-1924;  Zoologist, 
1924-1925;  Senior  Zoologist  and  Assistant  Chief  of  Zoological  Division,  1925- 
1932;  Collaborator,  1934-  ;  Bureau  of  Animal  Industry,  U.  S.  Department  of 

Agriculture. 

Zoologist,  biblographer,  author  of  numerous  papers  in  parasitology,  compiler 
of  Index  Catalogue  of  Medical  and  Veterinary  Zoology  published  in  collaboration 
with  Stiles.     Nematologists'  best   friend  and  severest  critic. 


PREFACE 

In  IIk'  preparation  of  Section  11,  Parts  II  and 
III,  it  lias  been  necessary  to  deviate  from  the 
arrangement  proposed  in  the  original  annomice- 
ment.  J)iiring  the  course  of  preparation  it  be- 
came evident  that  the  treatment  of  the  subject, 
as  developed  by  the  various  authors,  would  re- 
sult in  more  pages  than  can  be  saddle  stitched 
into  one  cover.  It  also  became  evident  that  it 
^  would  be  impossible  to  complete  some  of  the 

chapters   dealing  with   free-living   and  plant- 
parasitic  nematodes  until  long  after  most  of 
the  others  were  ready  for  printing.    Hence  it 
g  r^  seemed  advisable  to  so  change  the^rrangement 

of  the  chapters  as  to  permit  the  inunediate  pub- 
lication of  completed  manuscripts  even  though 
it  was  necessary  to  modify  what  might  seem  the 
most  logical  sequence. 

The  various  authors  are  responsible  for  the 
facts  presented  and  the  opinions  expressed  in 
the  parts  accredited  to  them  with  the  one  ex- 
ception of  taxonomic  nomenclature,  for  which 
Dr.  B.  G.  C'hitwood  assumes  responsibility. 

To  the  contributors  I  wish  to  express  my  ap- 
preciation and  thanks  for  their  sympathetic  co- 
operation as  well  as  for  the  excellence  of  their 
contributions  and  the  care  and  thoroughness 
with  wliich  these  were  prepared. 

J.  R.  Christie. 


i  1-^ 


CD 


;  a 

i  rn 

a 

o 


CHAPTER  IV 
LIFE  HISTORY.     GENERAL  DISCUSSION 

B.  G.  CHITWOOD 


The  dovclopmoiit  of  iioiiiiitodos  in  its  sim|)lost  form  is  diroct, 
or  not  marked  liy  a  motamorpliosis  siu'li  as  occurs  in  tlio  in 
sects.  In  Ronoral  tlio  newly  hatched  nematode  rosenil)les  tlie 
adult  in  all  gross  morpholoRic  characters  with  the  exception  of 
the  reproductive  system  and  secondary  sexual  characters.  The 
various  growth  stages,  except  the  adult  stage,  are  teruiinated 
liy  molts  (or  ecdysesi,  the  nunil>er  of  nuilts  lieing  four,  the  uum 
her  of  stages  five.  Internal  changes  do  not  occur  to  any  marked 
extent  in  the  simplest  form  of  life  history.  We  should,  there- 
fore, speak  of  the  stages  previous  to  the  adult  as  nynijihs,  if  a 
terminology  were  used  similar  to  that  emi)loyed  in  the  Arthro 
poda,  but  usage  has  made  larva,  as  applied  to  such  stages,  the 
accepted  term. 

The  number  of  uuilts  occurring  in  the  course  of  develojiment  is 
common  for  nearly  all  nematodes,  and  it  ajipears  to  be  the  gen 
eralized  or  primitive  number  for  the  class.  I>evelopment  may 
be  outlined  as  follows: 

First  stage  (larva) 

(molt) 

Second  stage  (larva) 

(molt) 

Third  stage  (larva) 

(molt) 

Fourth  stage  (larva) 

(molf) 

Fifth  stage  (adult) 
Correlated  with  mode  of  life,  various  adaptations  or  modifi- 
cations h,ive  taken  place  in  the  life  history,  these  adaptations 
having  arisen  through  the  need  for  food  and  a  means  of  dis 
semination.  With  free-living  nematodes,  living  either  upon 
decaying  matter  or  preying  upon  other  microscopic  organisms, 
these  factors  seem  to  have  played  a  smaller  part  than  with 
those  living  as  parasites. 

Probably  need  for  dissemination  was  the  earlier  influence; 
at  any  rate,  it  has  caused  the  simplest  modifications  of  life 
history.  The  action  of  this  factor  on  some  free-living  nema- 
todes is  evidenced  by  the  occurrence  of  a  persistent  stage,  the 
cuticle  of  one  of  the  larval  molts  being  retained  as  a  protec- 
tive sheath  or  "cyst."  It  is  not  uncommon  for  such  species  to 
have  two  types  of  larva,  environmental  conditions  determining 
whether  or  not  larvae  will  be  of  the  persistent  type.  The  sig 
nifieance  of  these  persistent  larvae  is  indicated  by  their  nega- 
tively geotropic  tendencies,  for  tlie.v  craw!  to  the  highest  sur- 
face available  and  "standing"  on  their  tails  swing  about, 
catching  upon  any  moving  ob,iect.  The  climax  of  this  type  of 
development  is  found  in  species  where  an  encysted  stage  on 
some  arthropod  (Rhabditis  coarctata,  see  cover  page,  see.  1,  part 
1),  or  annelid  is  obligatory  before  the  adult  stage  can  be 
reached. 

The  need  for  obtaining  food  plays  a  much  more  striking 
role,  being  evidenced  by  all  conceivable  degrees  of  parasitism 
both  on  and  in  plants  and  animals.  In  the  group  of  "herbi- 
vors"  life  c.vcles  may  be  of  numerous  t.vpes,  depending  on 
whether  tlie  nematodes  are  "grazers,"  passing  from  host  to 
host,  or  sedentary  forms,  entering  the  host  and  there  under- 
going all  or  most  of  the  stages  of  development.  Life  histories 
may  be  further  modified  by  the  factor  of  dissemination  and 
the  growth  habits  of  the  host.  Among  the  jiarasitcs  of  animals 
the  factors  of  dissemination  and  nourishment  also  play  their 
roles.  We  have  forms  that  are  parasitic  only  during  a  par 
ticular  larval  stage,  the  third,  which,  incidentally,  is  usually 
sheathed  or  "encysted."  Certain  parasites  of  annelids  (i.e., 
Rhabditis  pellio)  pass  the  third  stage  in  the  nejihridia  of  their 
host  and  can  only  develop  to  adults  in  the  decomposing  tissues 
of  their  host.  Other  species  (mermithids)  enter  their  hosts 
either  as  eggs  or  larvae  and  develop  to  ])readults  (fourth  stage) 
within  the  body  cavity,  finally  leaving  their  host  before  matur- 
ing. In  such  instances  the  nourishment  necessary  for  the  entire 
life  cycle  is  obtained  from  the  host  and  stored  during  the  para- 
sitic stages. 

The  type  of  life  history  in  parasitic  nematodes  being  entirely 
correlated  with  the  degree  of  parasitism,  we  find,  with  more 
ndvanced  parasitism,  more  complicated  life  cycles  and  more 
morphologic  changes  taking  place  during  the  course  of  devel- 
opment. Seurat  (Ullfi;  1920),  recognizing  this,  proposed  a  ter- 
minology for  the  different  types  of  life  cycles  based  on  the 
mode  of  development. 

Some  forms  have  an  alternation  of  generations,  one  genera- 
tion being  free  living,  the  other  parasitic.      This   type   of   life 


cycle  is  termed  hctnopenonx.  In  such  forms  we  find  free-living 
adults  giving  rise  to  larvae  which  enter  the  host  and  develop 
to  i)arasitic  adults.  These  larvae  may  or  may  not  be  ensheatlied 
(third  stage),  i.e.,  the  cuticle  of  one  or  more  larval  molts  re- 
tained though  separated  from  the  body.  The  stage  ready  to 
enter  the  host  is  ti'rnied  the  infrclivc  stage.  Nematodes  with 
no  alteration  of  generations  are  termed  monogcnous.  These 
are  by  far  the  most  common, 

l'arasit<'s  of  animals  may  also  be  classified  according  to  the 
number  of  hosts  necessary  for  completion  of  the  life  cycle. 
Species  in  which  there  is  a  single  host  are  termed  monoxcnous, 
those  in  which  there  are  two  or  more  hosts,  hclcroxcnous. 

Some  nematodes  have  both  free-living  and  parasitic  stages, 
the  free-living  st;iges  being  larvae,  the  parasitic  stages  late 
larvae  and  adults.  In  these  we  find  young  larval  stages  (the 
first  and  second)  feeding  U|)on  bacteria  and  similar  organic 
matter,  the  third  stage  usually  ensheathed  or  persistent,  this 
commonly  being  the  infective  stage.  Upon  entering  the  host 
these  species  develop  through  the  fourth  stage  to  the  sexually 
mature  adult. 

A  further  development  of  parasitism  is  indicated  by  the  ab- 
sence of  the  free-living  stages.  Eggs  of  the  parasite  pass  out 
of  the  host  and,  outside,  undergo  only  embryonic  development 
within  the  egg  shell.  In  such  instances  the  egg  shell  is  often 
covered  by  a  protein  layer  (p.  178),  and  the  embryo  often  con- 
tains more  yolk  than  forms  in  which  the  eggs  hatch  before  en- 
tering the  host.  With  such  a  completely  parasitic  mode  of 
existence,  the  factor  of  dissemination  again  becomes  manifest 
and  we  find  still  other  modifications  in  the  life  cycle. 

Some  nematode  parasites  of  vertebrates  pass  through  larval 
stages  in  invertebrates,  this  course  of  development  being  either 
obligatory  or  facultative;  still  others  undergo  larval  develop- 
ment in  other  vertebrates,  such  development  usually  being  obli- 
gatory, rarely  facultative.  The  host  in  which  such  a  parasite 
develops  to  infeetivity  is  termed  the  intermediate  or  secondary 
host  while  that  in  which  it  develops  to  sexual  maturity  is  called 
the  terminal,  definitive  or  primary  host.  Sometimes  the  inter- 
mediate host  is  eaten  by  another  animal  (secondary  interme- 
diate host)  in  which  the  parasite  can  continue  its  existence  but 
cannot  reach  maturity.  When  this  second  animal  is,  in  turn, 
eaten  by  the  primary  host  the  life  cycle  is  completed.  If  the 
parasite  neither  feeds  nor  undergoes  growth  within  an  animal, 
that  host  is  termed  a  transport  Itost.  This  type  of  intermediate 
host  serves  chiefly  as  a  means  of  dissemination  and  is  faculta- 
tive rather  than  obligatory. 

We  have  attempted  to  extend  Seurat 's  outline  to  include  all 
nematodes.  With  the  recent  and  extensive  increase  in  informa- 
tion on  the  life  histories  of  vertebrate  parasites  it  has  become 
very  difficult  to  adjust  Seurat 's  classification  to  the  many 
variations  in  life  cycles.  For  example  it  is  hardly  proper  to 
speak  of  a  form  as  being  heteroxenous  when  the  use  of  an  in- 
termediate host  is  facultative  {DictyocauUis  filaria)  yet  other 
nematodes  in  the  same  taxonomic  group  may  be  truly  heteroxe- 
nous requiring  an  intermediate  host  (Metastrone/i/his  clonffa- 
tus).  In  general  one  can  say  that  the  Spiruroidea,  Filarioidea, 
Camallanoidea,  Draeunculoidca  and  Dioctophymatoidea  are 
heteroxenous.  The  Strongyloidea,  Trichostrongyloidea  and 
Oxyuroidea  are  monoxenous  while  the  Metastrongyloidea  and 
Ascaridoidea  contain  forms  with  both  monoxcnous  and  heteroxe- 
nous life  cycles.  Some  e.xceptioiml  forms  do  not  fit  into  any 
part  of  the  classification.  Ncoaplectana  glaseri  (Rhabditoidea) 
and  Probsimayria  vivipara  (Oxyuroidea)  reproduce  through 
several  consecutive  generations  within  the  host.  Some  strains 
of  a  SIronpyloidcs  species  may  reproduce  without  an  alternation 
of  generations  while  other  strains  of  the  same  species  may  be 
predominantly  heterogenctic.  The  diiBculty  in  fitting  life  his- 
tories into  a  well  defined  classification  appears  to  be  due  to  the 
adaptation  of  each  species  to  its  host  which  entails  a  means  of 
dissemination  suitable  to  the  host's  environment  and  habits. 

A  large  assembly  of  nematodes  have  been  found  in  more  or 
less  close  association  with  vertebrates  or  invertebrates.  Some 
of  these  merely  use  the  "host"  as  a  means  of  transportation 
{Ehabditis  coarctata  which  may  pass  an  encysted  stage  on  the 
surface  of  dung  beetles).  Such  nematodes  are  not  considered 
parasitic  unless  the.v  actually  penetrate  the  host.  Some  well 
known  free-living  nematodes  have  been  reported  also  existing 
under  parasitic  conditions.  Thus  Rhabditis  strongyjoides  has 
been  repeatedly  taken,  in  the  larval  stage,  from  diseased  skin 
of  dogs  and  Diploscapter  coronata  from  the  ahydrochloric  acid 
stomaches  of  human   beings.     Yet  these  forms  are  free-living 


243 


nematodes  and  it  would  not  he  proper  to  classify  them  other- 
wise. If  it  happens  that  they  are  adaptable  to  unusual  environ- 
ments it  is  but  an  evidence  of  the  nature  of  the  group  to  which 
they  belong. 

Because  of  the  numerous  difficulties  and  inconsistencies  ap- 
parent in  any  classification  of  nematode  life  histories,  each  of 
the  authors  has  followed  the  system  which  seemed  most  logical 
to  himself.  Thus,  the  nematode  parasites  of  invertebrates  are 
grouped  according  to  the  manner  and  site  of  parasitism,  be- 
ginning with  the  semiparasitic  forms  that  mature  at  the  death 
of  their  host  and  feed  upon  the  carcass,  then  taking  up  the  in- 
testinal parasites  and  finally  the  parasites  of  the  body  cavity. 
Most  of  the  invertebrate  parasites  belong  to  the  Rhabditoidea 
and  Tylenchoidea  in  which  groups  parasitism  has  arisen  so 
many  times  and  adaptations  are  so  numerous  that  life  cycles 
have  little  in  common  with  systematics.  The  vertebrate  para- 
sites are  taken  up  according  to  their  systematic  position  since 
the  large  groups  show  some  consistency  within  themselves  and 
distinct  trends  are  apparent. 

For  those  who  desire  an  outline  after  the  manner  of  Seurat, 
we  have  revised  his  system  to  include  groups  with  which  he  did 
not  deal.  The  classification  is  entirely  artificial.  Nematodes 
are  divided  into  the  Vagantia  or  wanderers  and  the  Parasitica. 
The  Vagantia  includes  members  of  the  Rhabditoidea,  Tylen- 
choidea, Monhysteriua,  Chromadorina,  Enoplina  and  Dorylai- 
moidea.  Some  representatives  of  most,  if  not  all,  of  these 
groups  have  been  found  in  more  or  less  close  asspciation  as 
semiparasites  or  parasites  of  plants  or  animals  but  the  groups 
are  basically  free  living.  The  only  known  modification  in  the 
life  history  of  such  free  living  forms  is  the  existence  of  n 
persistent  stage.  Thus  far,  this  stage  is  known  only  in  ter- 
restrial  and   semiterrestrial   forms. 

The  Parasitica  is  subdivided  into  Phytoparasitica  and  Zoo- 
parasitica.  All  the  known  nematode  parasites  of  plants  belong 
to  the  Tylenchoidea  though  certain  members  of  the  Rhabditoidea 
and  Dorylaimoidea  are  commonly  found  in  close  association 
with  plants.  In  the  Zooparasitica  the  heteroxenous  group  con- 
sists exclusively  of  parasites  of  vertebrates  including  all  mem- 
bers of  the  order  Spirurida,  the  suborder  Dioctophymatina,  and 
representatives  of  the  Triehuroidea,  Ascaridoidea  and  Meta- 
strongyloidea.  Those  monoxenous  nematodes  in  which  the  adult 
is  wholly  or  partially  free  living  belong  to  the  Rhabditoidea, 
Tylenchoidea  and  Mermithoidea  and  are  all  parasites  of  in- 
vertebrates. The  monoxenous  nematodes  in  which  the  adult  is 
wholly  parasitic  include  the  Strongyloidea,  Trichostrongyloidea, 
Oxyuroidea  and  representatives  of  tlie  Rhabditoidea,  Meta- 
strongyloidea,  Ascaridoidea  and  Monhysteroidea.  One  com- 
monly thinks  of  the  groups  with  this  type  of  life  cycle  as  ver- 
tebrate parasites  yet  NeoapJectana.  and  Ccphalobiiim  viicvo- 
bivorum  are  rhabditoid  parasites  of  invertebrates,  the  Thelasto 
matidae  (Leidiincma,  Psciidonymons),  Rhigonematidae  and 
Ransomnematiiiae  are  oxyuroid  parasites  of  invertebrates  while 
Longihncca,  Rlmbdias,  and  Sfrontiyloidcs  are  rhabditoid  para- 
sites of  vertebrates  and  Oiloiifobiii.i  is  the  lone  monhysterid 
parasite  of  vertebrates. 

CLASSIFRATIOX    OF    NEMATODES    ACCORDIN'G   TO   LIFE   HISTORY* 

I.  Vagantia  (Free-living  nematodes). 

1.  Without  persistent  stage. 
Enoplidae 

(1)   Ejwplus  commnnis  (Marine) 

2.  With  persistent  stage. 
Rhabditidae 

(1)  Eliabditis  strongyloidcs  (Soil,  sometimes  causing  der- 
matitis in  dogs). 

(2)  Rhabditis     coarctnta      (Dung,     encysting     on     dung 
beetles). 

II.  Parasitica     (Nematodes    deriving    nourishment    from    their 
host). 
1.  Phytoparasitica   (Nematode  parasites  of  plants). 

A.  Vagrant  parasites.  More  or  less  migratory,  often  feed 
externally,  do  not  permanently  localize  in  part  of  plant. 
Tylenehidae 

(1)  Criconemoides   mutabile — Tagetes   erecta    (Exter- 
nal, roots). 

(2)  Pratylenchus  praicnsis — Cowpea  (Internal,  roots). 

(3)  Aphelenchoides   ritzema-bosi   —  Chrysanthemums 
(Leaf  and  bud). 

(4)  Ditylenchus     dipsaci — Narcissus,     onions,     clover 
(Stem,  leaf,  and  bulb). 

B.  Semivagrant  parasites.  (Localize  during  definite  pe- 
riod of  life  history.) 

Tylenehidae 

(1)   Angnina  (ritici — wheat  (Stem  and  seed). 

*In  this  outline  no  attempt  is  made  to  supply  all  hosts  or  to  include 
all   nematode  life  histories.      Only   examples   are   given. 


C.  Sedentary  parasites.    (Female  does  not  migrate  after 
maturity.) 
Tvlenchidae 


(1) 


-Tomatoes,  potatoes,  tobacco 
Sugar     beets,     potatoes 


(3) 
(4) 


b. 


Uctcrodcra   maiioiii- 
(Roots  and  tubers). 
(2)   Heterodera     schachtii 
(Roots  and  tubers). 

Tylenchulus  scmipcnetrans — Citrus  plants  (Roots). 
Botylencliulus  reniformis — Cowpea  (Roots). 
2.  ZooparasUica    (Nematode  parasites  of   animals). 
A.   Monoxenous  (Only  1  animal  host  in  life  cycle). 
AA.  Adult  stage  wholly  or  partially  free-living. 

a.  Only  larval  stages  parasitic  or  semiparasitic. 

aa.  Feed  in  adult  stage  usually  on  carcass  of  host. 
Rhabditidae 

(1)  Rhabditis  pellio — Earthworms    (Nephridia). 
Diplogasteridae 

(2)  Piisiionchus  aerivora — Termites   (Head). 

(3)  Alloionema      appendicidatum — Limax      aler 
(Foot,  alternation  of  generations  reported). 

Steinernematidae 

(4)  Keoaplectana  bibionis — flies   (Intestine), 
bb.  Do  not  feed  in  adult  stage. 

Mermithidae 

(1)  Agamermis  dccaudata — Grasshoppers  (Body 
cavity). 

(2)  Hermit  subnigrescens — Grasshoppers  (Body 
cavity). 

(3)  AUomerinis  myrmecophila  —  Lasius  spp. 
(Body  cavity). 

AUantonematidae 

(4)  Choiidronema  passali — Popiliu.s  interriipiiis 
(Body  cavity). 

Tetradonematidae 

(.1)    Trtradoneiiia       plicanx — Sciara       coprophila 

(Body  cavity). 
.\dult  stage  partially  parasitic,  partially  free-living. 
aa.  Monogenetic     (Without    alternation    of    genera- 
tions). 
AUantonematidae 

AUanlonema       mirabilc — Hylobiiis      abicliis 

(Body  cavity). 

Tylenchinema   oscindlae  —   Frit-iiy    (Body 

cavity). 

Howardula  bcnigna — Cucumber  beetle  (Body 

cavity). 
(4)   Scatoncma  wiillceri — Scatupsc  ftiscipes  (Body 

cavity,    sometimes    reproduces    several    gen- 
erations in  host). 
(.5)    Aphelciichulus  diplogaalcr — Ips  typographiis 

(Body  cavity). 

PdiaxiU/lrncliii.i     ditipar  —  Ips     typographiis 

(Body  cavity). 

Sphacriilaria     bombi  —  Bumbiis     tcrrestris 

(Body  cavity). 

Tripius    gibbosus — Cecidomyia    pini    (Body 

cavity), 
bb.  Heterogenetie     (With     alternation     of     genera- 
tions). 
AUantonematidae 

(1)  Fergusobia  curriei — One  generation  in  plant, 
Eiicah/ptiis  macrorrhynchia  (Leaf  and  flow- 
er) other  in  fly  Feriisonina  nicholsonia 
(Body  cavity). 

(2)  Heterotylenchus  abberaiis — One  generation 
bisexual,  other  parthenogenetic,  both  in 
body  cavity  Hylcmyia  antiqiia. 

BB.  Adult  stage  wholly  parasitic. 

a.  Heterogenetie     (Free-living    generation    sometimes 
suppressed). 

Strongyloididae 

(1)  Strongyloides  stercoralis — Man  (Small  in- 
testine). 

Rhabdiasidae 

(2)  Rhabdias  biifonis — Biifo  amrricanus  (Luug). 

b.  Monogenetic. 
aa.  Reproduce  in  the  host. 

Atraetidae 

(1)  Probst mayria  vivipara — Efjuines  (Intestine). 
Steinernematidae 

(2)  Neoaplectana  glaseri — Japanese  beetle  (Body 
cavity). 

Cylindrogasteridae 

(3)  Longibucca  lasiura  —  Lasiurus  borealis 
(Small  intestine). 

Diplogasteridae 

(4)  Cephalobium  microbivorum — Grylhis  assimi- 


(1) 
(2) 
(3) 


(7) 
(8) 


244 


lis  (Intestine). 
Monliysteridae. 
(.I)   f>(/i)ii^ibi«,s-  crti — Wliiilo  (Baleen)- 

(0)  Monhi/stira  cambari — Crawfish  (Gills). 

(7)    Tripiilium  carcinicoliim — OBcnrcinii.i  lalntilis 

(Gills). 
Myenoliidac 

(5)  iljifiichiis  6o^■f/l(ll— l.eocliea  (MiiscU-  i!c  con- 
iioctivo  tissue). 

I'll,  Ho   not   repioduoo  in   linst. 

aaa.  First  tliree  larval  stages  fror  liviiiK. 
.\iieylostoniatidae 

(1)  ".•lnc.i//(wft)Hi(i   (luodcnale — M.ui    ^Snlall   intes- 

tine). 
Triehostrongylidae 

(2)  IIuimoncliKS  cniitortiis — Sheep  (Abomasum). 

(3)  Osiraltiocru:ia  fitiformis — .\mplul)ians  (In- 
testine). 

Syngamidae 

(4)  Si/tinaiiiiiK  Irachra — Poult ly  (Broiulii  or 
trachea)  [Invertebrate,  annelid,  mollusc  nr 
insect   transport  host  facultative]. 

(5)  OUulanim  tricuspid — Cats    (Stomach), 
fist  moult  in  parent  worm.] 

Metastron^ylidae 

(6)  Dicli/ocdiilitu  filaria — Sheep   (Bronchi). 
(.Vnnelid   transport    host    facultative;    1st    - 
larval  stages  do  not  feed.] 

Cosmocercidae 

(7)  Cosnwccrcoidr.i  <hilui  —  .\m])hibians  and 
snails   (Intestine). 

l)bb.  Eggs  infective  to  host. 
Thelastomatidae 

(1)  I.iidijtirma  appendicutattim  —  Pfiiplaiicia 
amcricana    (Intestine). 

(2)  Psrniloni/mnus  spirotheca — HtidrnphUiis  pic- 
ens    (Intestine). 

Oxyuridae 

(3)  Enierobiiis  r^ermicularix  —  >ran  (Appendix, 
caecum). 

(4)  Oxyuris  eqtii — Equines   (Colon). 
Heterakidae 

(n)   Hctcralis  paUinae — Poultry   (Intestine), 
(fi)   Ascaridia  galli — Poultry  (Intestine). 
Ascarididae 

(7)  Ascaris  himbricoidcs — Man   (Intestine). 
Trichuridae 

(8)  CapiUaria  columbae — Pigeons   (Small  intes- 
tine). 

(9)  Trichnris  Irichiura — Man  (Caecum). 

B   Heteroxenous   (Two  or  more  animal  hosts  in  life  cycle). 
a.  Eggs  infective  to  intermediate  host. 
Metastrongylidae 

(1)  iletaxtronfjyhis  clntigafiix  —  Earthworms  — 
Swine   (Lung). 

Heterakidae 

(2)  Subulura  brumpti — Various  insects — Poul- 
try  (Cecum). 

Ascarididae 

(3)  Haphidnsrnri-a  canadrnxis — Ernf/otr  nymphs 
— Minnows — Eunx  liiciiin  (Intestine).  2  in- 
termediate hosts,  mandatory. 

Thelaziidae 

(4)  Gongi/Ionema  pulclinim — Beetles,  roaches — 
Pig,  sheep,  deer  (Esophagus  and  mouth). 

('))  Spirocerca  liipi — Dung  beetles — Dog  (Esoph- 
agus). 

(6)  Ascarnps  strongylina — Dung  beetles — Swine 
(Stomach). 

(7)  Physocrphalux  srxnlatus  —  Dung  beetles — 
Swine  (Stomach). 

Spiruridae 

(8)  Tetramercs  crami — Araphipods — Duck  (Pro- 
ventriculus). 

Acuariidae 


('.0  ChrUospnma  hamulosa  —  Grasshoppers  — 
Poultry  (Gizzard). 

(10)  Krhiniiria  nncinala — Cladocera  (Daphnia)  — 
Duck   (Fore  and  mid-gut). 

(11)  Disphoiiinr  .npiralis  —  Isopods  —  Poultry 
(  Esophagus  iind  crop). 

(inathostomatidae 

(12)  Ilarlirlia  (inUiiianim  — Termites —  Poultry 
(  Sni.'ill  intestine). 

Trichuridae 

(13)  CapiUaria  annulala — .\nnelid  transport  host 
obligatory — Chickens    (Crop). 

Cystoopsidae 

(14)  Ci/stoopsis-  acipcnxeri  —  .\mphii)ods — Stur- 
geons  (Skin). 

Eustrongylididae 

(1."))  Jitistrotifnilides  ignotu.i — .'  Crustacean — Fun- 
diilii.s  diaplianus — Ardea  herodiax  (Gizzard). 
Dioctophymatidae 

(16)  Dioctophyma  renale — ?  Crustacean — ?     fish 
— Man,  dogs,  mink   (Kidney). 
.  Larvae  infective  to  intermediate  host, 
aa.  Enter  final  host  per  os. 
Dracunculidae 

(1)  Dracunculiis  medinensis  —  Cyclops  —  Man 
(Under  skin). 

Philometridae 

(2)  Philnmclra  nodulosa — Cyclops — Catostomus 
cnmmrrsoilii   (Lip). 

(3)  Philometra  fujimotoi — Cyclops — Ophicepha- 
hts  argils  (Fin). 

Camallanidae 

(4)  CamaHaniis  sxoeeti — Cyclops — Ophicephahis 
gachiia  (Intestine).  Second  intermediate 
host,  small  fish?  obligatory. 

Pseudaliidae 

(5)  Murllrrius  capillaris — Molluscs — Sheep  and 
goats  (Lung). 

Spiruridae 

(6)  Habronema  mitscac  —  Munca  domestica  — 
Equines   (Stomach). 

(7)  Habronema  microstoma  —  Stomoxys  spp. 
— Equines    (Stomach). 

(8)  Draschia  megastoma — 3[ii.ica  domestica — 
Equines   (Stomach). 

Gnathostomatidae 

(9)  Spiroxys  contorta- 
Turtles  (Stomach), 
host  not  mandatory. 

(10)  Gnathostoma  spinigerum — Cyclops — Fish  or 
snakes — Felidae  (Stomach).  Second  inter- 
mediate host  mandatory. 

Ascarididae 

(11)  Conlracaecum  spiculigerum — Minnows — Car- 
nivorous fish — Cormorant  (Proventriculus). 
Second  intermediate  host  mandatory. 

(12)  Eaphidascaris  canadensis — Erogon  nymphs — 
Minnows — Esox   iitciiis    (Intestine).      Second 

intermediate  host?  mandatory. 
Trichincllidae 

(13)  Trichinella  spiralis — Eat,  pig,  man  (Intes- 
tine). Hosts  serve  both  as  intermediate 
and  final  host. 

bb.  Enter  final  host  through  skin. 
Dipetalonematidae 

(1)  Wuchercria  bancrofti  —  Mosquitoes  —  Man 
(Lymphatic  system). 

(2)  Onchocerca  volvnlus — Sinuilium  damnosiim — 
Man  (Subcutaneous). 

(3)  Onchocerca  ceriicalis — Ciilicoides  nebcculo- 
sis — Equines  (Cervical  ligament). 

(4)  Dirofilaria  immitis  —  Mosquitoes  —  Dogs 
(Heart). 


Cyclops  —  Minnows  — 
Second    intermediate 


245 


CHAPTER  V 

LIFE  HISTORY  (ZOOPARASITICA) 

Parasites  of  Invertebrates 

J.  R.  CHRISTIE,  U.  S.  Horticultural  Station,  Beltsville,  Md. 


Introduction 


There  are  many  different  types  of  association  between  nema- 
todes and  other  invertebrates  and  it  is  difficult  to  draw  a  line 
between  what  should  and  what  should  not  be  regarded  as  para- 
sitism. Most  of  the  nematodes  that  live  within  the  bodies  of 
invertebrates  are  customarily  referred  to  as  parasites  though 
there  is  little  evidence  that  some  of  them  interfere  materially 
vpith  the  well-being  of  their  "hosts."  We  know  very  little, 
however,  about  the  effects  of  these  nematodes  on  the  animals 
that  harbor  them  unless  the  manifestations  are  pronounced  and 
obvious.  The  only  feasible  procedure  is  to  regard  as  eligible  for 
inclusion  in  this  chapter  all  nematodes  that  regularly  spend 
part  of  the  life  cycle  within  the  bodies  of  invertebrates  regard- 
less of  the  precise  character  of  the  association.  Species  for 
which  vertebrates  serve  as  definitive  hosts  and  invertebrates 
only  as  intermediate  hosts  are  dealt  with  in  the  following 
chapter. 

In  general  the  parasites  of  invertebrates  and  those  of  verte- 
brates are  not  found  in  the  same  phylogenetie  groups  and  in 
those  cases  where  both  belong  to  the  same  group  the  vertebrates 
involved  are  almost  always  amphibians  and  reptiles.  However, 
the  Thelastomatidae  and  the  Oxyuridae  have  very  close  affini- 
ties. 

Arthropods,  annelids  and  mollusks  are  the  invertebrates  most 
commonly  parasitized  by  nematodes  though  scattered  cases  have 
been  reported  where  other  invertebrates,  even  nematodes  them- 
selves, serve  as  hosts.  There  are  surprisingly  few  records  of 
marine  invertebrates  harboring  nematodes  and  most  of  these 
apparently  deal  with  cases  where  the  association  is  erratic  or 
accidental  or  where  some  vertebrate  serves  as  definitive  host. 

Included  among  the  nematodes  harbored  by  invertebrates  are 
species  where  a  parasitic  mode  of  life  is  only  now  being  ac- 
quired and  others  where  it  is  of  great  antiquity.  There  is  great 
diversity  in  the  types  of  life  cycles  and  to  simplify  discussion 
and  facilitate  comparison  the  nematodes  are  divided  into  three 
groups. 

The  first  of  these  groups  is  made  up  of  nematodes  that  are 
more  or  less  closely  related  to  free-living  species  and  in  the  life 
cycles  we  often  find  a  combination  of  saprophagous  and  "para- 
sitic" habits.  In  one  line  of  evolutionary  development  the 
nematodes  live  and  reproduce  in  the  carcass  of  the  "host,"  to 
the  death  of  which  they  may  or  may  not  have  contributed.  Life 
cycles  are  simple,  perhaps  the  most  outstanding  feature  being 
the  frequent  occurrence  of  dauer  larvae,*  a  characteristic  that 
has  been  carried  over  from  a  free-living  to  a  parasitic  mode  of 
life.  Another  line  of  evolutionary  development  seems  to  have 
culminated  in  a  life  cycle  where  the  nematode  may  pass  through 
one  or  more  free-living  generations,  then  gain  entrance  to  the 
host  and  pass  through  one  or  more  parasitic  generations. 

The  second  group  comprises  tliose  nematodes,  not  included  in 
the  first  group,  that  inhabit  the  alimentary  tract.  Life  cycles, 
so  far  as  known,  are  simple.  With  perhaps  an  occasional  ex- 
ception (i.  g.,  Ccphalobium  microbivoriim) ,  only  the  egg  stage 
occurs  outside  the  host,  a  characteristic  shared  by  verj'  few 
species  in  the  otlier  two  groups. 

The  third  group  includes  the  body-cavity  and  tissue  para- 
sites. In  contrast  to  the  fir.st  group,  these  nematodes  are  highly 
specialized,  obligate  parasites  and,  in  contrast  to  the  second 
group,  they  pass,  at  the  most,  only  a  transitory  period  in  the 
alimentary  tract  of  the  host.  Five  families  are  included  in 
this  group.  The  Drilonematidae  and  Mycnchidae  have  received 
little  attention  and  our  knowledge  regarding  life  cycles  is  very 
meager.  The  Tetradoneraatidac,  Mermithidae  and  Allantone- 
matidae  have  been  somewhat  more  adequately  studied.  The 
nematodes  belonging  to  these  three  families  have  been  parasites 
for  a  very  long  time  and  many  of  them  have  complicated  life 
cycles  that  are  highly  adapted  to  individual  requirements.     Of 


*'nie  term  dauer  larva  is  used  in  tliis  te-\t  to  designate  a  larva,  in  a 
particular  stage  of  development,  that  is  especially  adapted  to  withstand 
adverse  conditions  and,  when  a  dauer  stage  is  not  obligatory,  that  differs 
from  a  larva  of  the  same  stage  that  develops  when  conditions  are  favor- 
able and  food  is  abundant.  The  term  is  not  new,  having  been  used  by 
Fuchs  and  others  with  approximately  this  same  meaning  and,  while  not 
of  classic  origin,  it  is  short,  expressive,  appropriate  and  useful.  Dauer 
larvae  are  of  common  occurrence  in  the  Rhabditidae  and  Diplogasteridae 
and  are  more  characteristic  of  free-living  than  of  parasitic  species,  hence 
the  term  is  not  synonymous  with  "infective  larva." 


the  various  factors  that  have  influenced  these  life  cycles,  two 
stand  out  as  being  of  great  importance. 

One  of  these  factors  is  the  necessity  for  the  infective  stage 
to  reach  and  gain  entrance  to  the  host.  This,  of  course,  is  a 
requisite  in  the  life  cycle  of  every  parasite  but  for  the  allan- 
tonematids  and  merraitliids  there  are  certain  restricting  condi- 
tions with  which  many  of  the  others  do  not  have  to  contend,  at 
least  not  to  an  equal  extent.  Some  of  the  hosts  are  insects  that 
develop  in  seasonal  cycles  and  where  the  total  life  span  of  the 
individual  may  be  only  a  few  months.  It  is  frequently  neces- 
sary that  the  parasite  enter  when  the  host  is  in  a  particular 
stage  and  this  stage  may  be  available  only  at  restricted  times 
of  the  year.  As  a  result  the  life  cycles  of  many  of  these  para- 
sites have  become  closely  correlated  with  the  life  cycles  of  their 
respective  hosts. 

The  other  factor  is  the  ability  of  the  nematode  to  take  food 
only  during  restricted  periods.  The  fact  that  for  many  of  these 
parasites  the  free-living  stage  may  be  of  considerable  duration 
and  that  during  this  period  the  nematodes  take  no  food,  but, 
nevertheless,  pass  through  important  phases  of  the  life  cycle, 
has  had  a  profound  effect  on  development.  In  many  cases  the 
larval  mermithid,  during  a  comparatively  short  period  of  para- 
sitic life,  must  make  a  phenomenal  growth  and  store  sufficient 
nutrient  materials  to  carry  the  adult  through  its  relatively 
long,  free-living  period  of  sexual  activity  and  reproduction.  The 
larval  allantonematid  that  develops  to  maturity  outside  the  host 
after  only  a  very  brief  period  of  parasitic  life,  must  exercise 
the  strictest  economy  in  the  utilization  of  its  limited  supply  of 
stored  nutrients.  Since,  as  a  rule,  only  the  female  again  be- 
comes parasitic,  the  male  must  produce  and  mature  its  sperma- 
tozoa though  the  production  and  maturation  of  the  eggs  by  the 
female  is  postponed.  There  can  be  little  or  no  increase  in 
l)ody  size  during  this  free-living  period,  hence  the  adult,  im- 
pregnated female,  after  entering  a  new  host,  undergoes  a  pe- 
riod of  rapid  growth.  In  the  Sphaerulariinae  a  prolap.sus  of 
the  uterus  has  resulted  through  the  inability  of  the  small,  un- 
derdeveloped bodj'  of  the  young  female  to  keep  pace  with  the 
rapidly  growing  reproductive  organs. 

Novitious  Parasites  and  Semiparasites 

Among  these  nematodes  two  lines  of  evolutionary  develop- 
ment seem  to  stand  out  more  or  less  distinctly  though  it  is  ob- 
viously improbable  tliat  they  account  for  the  origin  of  all  the 
different  types  of  parasitism  or  semiparasitism  encountered  in 
tills  heterogeneous  group. 

One  line  of  evolutionary  development  appears  to  have  been 
initiated  when  certain  saprophagous  nematodes  utilized  other 
invertebrates,  frequently  saprophagous  insects,  as  vehicles  for 
transportation.  These  "hitchhikers,"  first  seeking  protection 
from  desiccation  in  crevices  on  the  external  surface,  eventually 
entered  the  bodies  of  their  "hosts."  In  the  life  histories  of 
species  representing  an  intermediate  step  in  this  line  of  develop- 
ment, larval  nematodes,  after  gaining  entrance  to  the  body  of 
the  "host"  and  becoming  established  therein,  do  not  at  once 
grow  to  maturit3'  and  reproduce  but  remain  in  a  more  or  less 
quiescent  condition.  These  larvae  do  not  appear  to  interfere 
materially  with  the  life  processes  of  the  animal  that  harbors 
them  but  when  the  animal  dies  from  otlier  causes  the  nematodes 
immediately  resume  development  and  reproduce  in  the  carcass. 

In  some  cases,  however,  this  type  of  relationship  has  evolved 
to  a  point  where  it  is  no  longer  passive  but  where  the  nema- 
todes are  an  important  factor  in  bringing  about  the  death  of 
the  animal  whose  body  they  enter.  Even  though  present  in 
small  numbers,  some  species  of  NeoapJectana  are  said  to  kill 
their  insect  hosts  in  a  very  short  time. 

The  parasitic  or  semiparasitic  relationship  between  these 
nematodes  and  tlicir  respective  "hosts"  is  not  always  obliga- 
tory. Johnson  (101,3)  concluded  that  entrance  into  the  body 
of  an  earthworm  is  not  necessary  in  the  life  cycle  of  Rhahditis 
maupasi  but  if  larvae,  during  their  sojourn  in  the  soil,  find  suit- 
able decaying  organic  matter  they  will  develop  and  reproduce 
therein.  Neither  is  Pristionchus  acrivora  dependent  on  en- 
trance into  a  termite  or  some  other  insect  to  complete  its  de- 
velopment as  it  has  been  found  reproducing  in  a  number  of  dif- 
ferent habitats  including  decaying  plant  tissues.  Neoaplectana 
fliaseri,  on  the  other  hand,  appears  to  be  an  obligate  parasite 
that,  in  nature,  develops  only  after  entering  the  living  body  of 
its  insect  host. 


246 


Most  of  llu'SO  iioiiiatoilos  :uo  liisrwwil  :iiul  l'i'in;iU'.s  inodiici' 
fertile  I'KKS  only  after  eopulntioii.  Males  are  usually  somewhat 
loss  numerous  than  females,  reaeh  maturity  a  little  quicker, 
ami  do  not  live  quite  so  \o\\g.  Aeeordiug  to  Johnson,  females 
of  KhabdiU.i  maiiimni  usually,  thouRh  not  always,  reproduee 
without  males.  In  nmny  speeies  of  this  uroup  a  female  may  be 
oviparous  when  young  but  toward  the  end  of  life  sonio  of  the 
last  ecds  produced  may  be  retained  and  hatch  in  the  uterus. 
'Pile  resultiiiR  larvae  may  not  escape  thr(iii);h  the  vulva  but  un- 
diTRo  part  of  their  development  within  the  mother  nematode, 
eonsumiuf;  her  internal  orjrans  and  convertint;  her  into  a  brood 
sac.  Incidentally,  this  same  mode  of  reproduction  is  character 
istic  of  many  free-living  species  of  Diplogastcr,  Rhabdilix  and 
related  genera. 

The  sec(uid  line  of  evolutionary  development  referred  to  above 
may  have  been  initiated  when,  during  periods  of  adversity,  cer- 
tain sai'rophagous  nematodes,  seeking  refuge  and  succor,  en- 
tered and  temporarily  dwelt  within  the  bodies  of  other  inver- 
tebrates. In  the  case  of  nematodes  in  this  category  parasitism 
apparently  does  not  ordinarily  result  in  the  death  of  the  host 
nor  are  the  parasites  able  to  live  in  a  decaying  carcass.  Usually 
these  nematodes  either  inhabit  the  alimentary  tract  of  the  host 
(e.  g.,  Aiuiiostoma  limacis)  or  arc  associated  with  its  reproduc- 
tive organs  (e.  g.,  " Angiostoma"  hclicis).  For  at  least  one 
species  (i.  e.,  AUoioncma  appcndiciiJaUi)  an  alternation  of  one 
or  more  parasitic  generations  with  one  or  more  free-living  gen- 
erations has  become  a  more  or  less  regiilar  procedure. 

Rii.\BmTis  M.\irpAsi  Caullery  and  Seurat,  1919  (Syn.  R.  iiclUo 
Butschli,  1S73;  not  Schneider,  ISOG).  Larvae  of  Shabtlitis 
maiipasi  are  found  in  the  nophridia  and  coelom  of  living  earth- 
worms. For  Liimbricus  terrcfitri.i  L.  the  incidence  of  infection 
is  frequently  very  high  and  at  least  several  and  perhaps  many 
other  species  harbor  these  nematodes  more  or  less  frequently. 

Larvae  are  found  near  the  uephridiopore  in  the  dilated,  muscu- 
lar termination  or  "bladder"  of  the  neiihridial  tube.  Often 
nearly  every  tube  is  inhabited,  the  number  of  worms  in  each 
varying  from  2  or  3  to  12  or  more.  Also  larvae  may  occasion- 
ally be  found  in  the  seminal  vesicles.  When  in  these  above 
mentioned  locations  larvae  are  in  an  active  condition  and  not 
ensheathed.  Johnson  concluded  that  these  inhabitants  of  the 
neiihridia  are  not  necessarily  confined  to  this  location  through 
out  the  life  of  the  earthworm  but  may  move  out  into  the  soil 
and  later  go  back  through  the  nepluidiopores  into  the  same  or  a 
different  earthworm. 

Larvae  occur  also  in  the  coelom  and  these  are  usually  en- 
sheathed and  inactive  (Fig.  165C).  Occasionally  a  larva  may 
be  embedded  in  the  muscles  of  the  body  wall  or  encysted  on  a 
septum.  Frequently  several  larvae  are  embedded  in  a  brown, 
oval  body  composed  of  cysts  of  the  sporozoan.  Monocystus,  and 
various  earthworm  tissues.  Such  bodies  are  most  common  at 
the  posterior  end  of  the  coelom. 

There  is  no  evidence  that  the  presence  of  these  larval  nema- 
todes is  detrimental  to  the  annelid.  So  long  as  the  earthworm 
is  alive  the  nematodes  remain  in  a  larval  stage  but  when  the 
earthworm  dies  they  quickly  grow  to  adults  (Fig.  165  A  &  B) 
and  reproduce  in  the  carcass.  Otter  (1933)  concluded  that  a 
female  lives  from  7  to  10  days  after  reaching  maturity  and  lays 
from  150  to  300  eggs.  Males,  in  his  opinion,  live  about  a  third 
as  long  as  females.  No  doubt  several  generations  occur  before 
the  food  supply  is  exhausted  though  Johnson  was  uncertain  on 
this  point.  After  the  body  of  the  earthworm  is  consumed  large 
numbers  of  larvae  move  out  into  the  soil  where  they  live  await- 
ing the  opportunity  to  enter  another  earthworm.  Larvae  from 
the  soil  are  said  to  be  in  the  same  .stage  as  those  from  the 
nephridia,  but  what  this  stage  is  has  not  been  stated. 

With  regard  to  the  method  of  entering  the  earthworm,  John- 
son writes:  "Those  that  enter  by  the  nephridiopores  take  up 
their  position  in  the  terminal,  bladder-like  part  of  the  nephridia. 
Those  that  use  the  spermiducal  apertures  travel  up  the  vasa 
deferentia  and  occupy  the  seminal  vesicles.  Lastly,  those  that 
pass  in  by  the  dorsal  pores  and  the  oviducal  apertures  find  them- 
selves in  the  coelom,  where,  being  attacked  by  the  amoebocytes, 
they  encyst.  These  encysted  larvae  coated  with  amoebocytes  are 
worked  backward  by  the  movement  of  the  worm  till  they  come 
to  rest  in  the  tail  end  of  the  worm,  where,  together  with  other 
foreign  bodies,  such  as  cysts  of  Monocjistix  and  discarded  setae, 
and  with  masses  of  dead  brown-colored  amoebocytes,  they  are 
compressed  and  cemented  into  the  brown  bodies  which  are  found 
there." 

According  to  Keilin  (1925)  the  accumulation  of  foreign  bod- 
ies in  the  posterior  segment  of  an  earthworm  may  induce  the 
development  of  a  stricture  that  will  sever  this  distended  ter- 
minal i)ortion  from  the  rest  of  the  body.  The  detached  portion 
then  decomj)oses  and  in  this  manner  M.  maupnsi  and  other 
coelomic    j)arasites   of   the   earthworm    may    be    liberated. 

Males  of  E.  maupasi  are  much  fewer  in  number  than  females. 
Although  Johnson  did  not  observe  copulation,  his  rearing  ex- 


periments lead  him  tu  ccincluiii'  that  most  females  are  lier- 
ma))hro(litic  but  that  occasionally  females  occur  that  are  able 
to  reproduce  only  after  being  fertilized  by  males.  Otter,  who 
observed  co]>ulaticin  and  agrees,  in  the  main,  with  Johnson, 
writes  that  li.  maupa.ii  "may  thus  be  considered  to  be  one  of 
those  species  of  Rliabdilis  in  which  hermaphroditism  is  in  a 
very  early  stage,  and  in  which  funetion.al  males,  females,  and 
hermaiihrodite  females,  exist  side  by  side  in  fluctuating  pro 
jiortions. ' ' 

I'Eu.sTiONCiiu.s  AKRIV0K.\  (Cobb,  1916),  was  first  found  by 
Merrill  and  Ford  in  the  heads  of  termites, /.rHro/criiif.s- /»ci/».r/».s' 
Rossi,*  collected  ne.ar  Manhattan,  Kansas.  Under  natural  con- 
ditions the  nematodes  varied  from  0  to  about  75  per  insect. 
After  experimental  termites  had  been  kept  for  4  days  in  soil 
heavily  infested  with  P.  acrivora,  the  average  number  of  nema- 
todes per  insect  was  46.0  while  termites  used  as  controls 
averaged  about  3  nematodes  per  insect.  IIow  the  nematodes 
enter  or  why,  in  living  termites,  they  are  found  only  in  the 
head  are  points  that  have  not  been  determined.  The  parasites 
do  not  reach  nuiturity  in  living  hosts  but  when  the  termites 
are  heavily  infected  they  become  sluggish  and  die,  whereupon 
the  nematodes  reproduce  in  the  carcass.  Hence,  in  this  instance, 
the  relationship  is  not  purely  passive. 

Merrill  and  Ford  were  able  to  rear  this  nematode  in  water 
cultures  with  various  substances  supplied  for  food,  preferably 
the  macerated  bodies  of  insects.  Eggs  hatched  in  about  18 
hours  and  the  adult  stage  (Fig.  165  .T)  was  reached  in  about 
2  days.  The  complete  life  cycle  from  egg  to  egg  required  about 
4  to  5  days  but  after  beginning  to  lay  eggs  an  adult  female 
usually  lived  for  12  to  13  days.  During  a  period  of  13  days 
one  female,  while  under  observation,  copulated  with  7  males  and 
deposited  317  fertile  eggs  and  14  infertile  eggs.  Males  were 
somewhat  less  numerous  than  females.  They  lived  for  about  19 
days  and  one  male,  while  under  observation,  copulated  with  10 
different  females. 

Toward  the  end  of  life  a  female  becomes  sluggish  and  eggs 
are  not  extruded  but  hatch  in  the  uterus.  W'hile  the  resulting 
larvae  may  sometimes  escape  through  the  vulva  they  usually 
remain  in  the  mother  nematode,  feeding  on  her  internal  organs. 

Since  Merrill  and  Ford's  investigations  nematodes  identified 
as  P.  aerivora  have  been  reported  from  various  other  habitats. 
They  have  been  found  in  other  termites,  usually  located  in  the 
head  while  the  insect  is  alive.  They  have  been  found  in  dead 
pupae  of  the  corn  ear  worm,  Hcliotliis  armigcra  (Hiibn.),  and 
in  dead  pupae  of  the  rose  leaf  beetle,  Kodonota  puncticoUia 
(Say).  They  have  been  found  in  grasshopper  egg  masses  where 
they  were  reported  to  have  been  destroying  the  eggs.  On  sev- 
eral occasions  they  have  been  found  in  decaying  plant  tissues. 
However,  the  populations  from  these  different  habitats  may 
represent  different  strains  or,  perhaps,  even  different,  though 
closely  related,  speeies. 

The  peculiar  habit  of  swallowing  air,  to  which  this  nema- 
tode owes  its  specific  name,  is  shared  by  several  species  of  Dip- 
Jogastcr  and  Khabditis.  When  mounted  in  water  on  a  micro- 
scope slide,  one  of  these  nematodes  may  place  its  head  against 
the  surface  of  an  entrapped  air  bubble  and  air  can  be  seen  as 
it  passes  down  the  esophagus  to  the  anterior  end  of  the  intes- 
tine where  it  is  quickly  absorbed.  According  to  Cobb  (1915) 
some  of  these  nematodes  can  ingest  their  own  volume  of  air 
in  the  course  of  an  hour  or  two.  The  swallowing  of  air  is  ac- 
complished by  the  usual  rhythmic  muscular  movements  of  the 
esophagus.  During  the  first  muscular  movement  a  small  bubble 
of  air  passes  quickly  from  the  mouth  to  the  median  pseudobulb 
where  it  stops.  At  the  next  muscular  movement  the  bubble 
passes  on  into  the  intestine  while  another  simultaneously  passes 
from  the  mouth  to  the  median  pseudobulb.  This  may  continue 
uninterrupted  for  a  considerable  period  of  time. 

Neo.\plectan"a  bibionis  Bovien,  1937,  was  studied  by  Bovien 
(1937)  who  found  it  in  Denmark  associated  with  the  dipterous 
insects  Bibio  ferruginatns  (L.),  B.  hortidaniis  (L.)  and  Dilo- 
phim  rtdgari.i  Meig. 

An  interesting  and  significant  point  in  the  life  cycle  of  this 
nematode  is  the  occurrence  of  dauer  larvae  (Fig.  165  G).  These, 
according  to  Bovien,  are  in  the  third  stage.  A  dauer  stage  is 
not  obligatory  but  occurs  only  when  environmental  conditions 
arc  unfavorable  to  enable  the  nematode  to  persist  through  pe- 
riods of  adversity.  Dauer  larvae  are  relatively  sluggish  and 
are  usually  enclosed  in  a  partly  separated  cuticle  though  this 
may  be  lost  before  the  end  of  the  dauer  stage.  These  larvae 
are  easily  distinguished  from  third-stage  larvae  that  develop 
under  favorable  conditions  being  slenderer  and  differing  in 
other  morphological  details.  Bovien  found  dauer  larvae  cling- 
ing to  the  surface  of  adult  flies  and  being  transported  by  them. 

The  various  host  insects  become  infected  by  swallowing  these 
dauer  larvae  which,  on  reaching  the  alimentary  tract,  remain 

*Regarded  by  Snyder,  according  to  Van  Zwaluwenburg  (1928,  p.  9), 
as  either  Keliruliternie/t  tibiaUjt  Banks  or  R.  claripennia  Banks. 


247 


Fig.  165.      NOVITIOrS   PARASITES  AND   SEMIPARASITES 


A-C — Rhabditw  maupasi  (A — Adult  female;  B — Adult  male;  C — 
Larva  escaping  from  *'cyst").  D-H — NeoapUctana  bibinni.^  (D — Adult 
male;  E — Adult  female;  F — Larva  that  developed  under  favorable  con- 
ditions; G — Dauer  larva  of  same  stage  as  F;  H — Pigmy  female).  I-J — 
Pristioiu'hiis  aerirora    (1 — Newly  hjitehed  larva;  J — Adult  female).    K — 


Diptoffaster  labiata,  dauer  larva.  L  &  JI — AU-oionema  appendicuUitum 
( L — Adult  female  of  parasitic  generation ;  M — Adult  female  of  free- 
living  generation).  A-C.  after  Johnson.  1913;  D-H,  after  Bovien, 
1937;  I-K,  after  Merrill  and  Ford,  1916;   L  &  M,  after  Claus,  1868. 


;24« 


iiiiclmiiKcd,  :i|>))aii'iitly  liaviiiK  iio  adverse  effeot  on  the  inswt. 
WIu'ii  rvt'iitnally  the  insect  dies,  presunmlily  from  otlier  causes, 
the  larvae  move  into  its  tissues  and  jiroceed  in  development, 
IiassiuK  tlmiUKli  several  penerations  and  <|nickly  IniildiiiK  uji  a 
large  iiopulation.  When  the  carcass  has  lieeii  consumed  youug 
nematodes  move  out  into  the  soil  and  develop  into  dauer  larvae. 

Although  Hies  become  infected  while  in  the  larval  stage,  if 
the  nenuitodes,  on  reaching  the  intestine,  are  wholly  innocuous, 
many  of  the  insects  must  carry  their  infection  on  into  the  adult 
stage.  Rovien  is  not  very  lucid  on  this  jioint  Init  he  merifioTis 
finding  nematodes  in  living  1]\  i)upae,  on  one  occasion  in  tlu' 
tiody  cavity. 

Bovien  concluded  that  development  from  egg  to  egg  laying 
female  requires  about  4  days.  A  young  female  is  oviparous  but 
some  of  the  last  eggs  laid  by  an  old  fcm.'ile  liatch  within  the 
uterus.  Kach  female  usually  produces  somewhat  in  excess  of 
-""  eKRS. 

It  is  not  strictly  necessary  that  N.  bibioni.i  enter  living  in- 
sects as  Rovien  was  able  to  rear  several  generations  on  dead 
insects  of  different  sjiecies  if  fresh  cadavers  were  periodically 
provided.  Several  generations  could  sometimes  be  reared  on 
egg   albumen. 

Gravid  fenuiles  (Fig.  IG.')  E")  usually  attain  a  length  of  up 
to  ■>  mm.  but  Rovien  reports  finding  mature,  rci)roducing  fe- 
males that  failed  to  reach  a  length  of  1  mm.  (Fig.  IG.l  H),  per- 
haps due  to  some  nutritional  deficiency.  Between  these  dwarfs 
and  females  of  maximum  stature  numerous  intermediate  sizes 
were  found. 

NEO.\PI,E(.-r.\NA  GLASERI  Steiner,  lili!!1,  was  first  fovind  in  dead 
larvae  of  the  .Japanese  beetle,  ropillid  japonica  Newni.,  col- 
lected in  New  Jersey  and  is  best  known  as  a  jiarasite  of  this 
insect.  However  it  has  been  demonstrated  that  this  nematode 
will  infect  larvae  of  the  Enrojiean  corn  borer,  Purausta  nu- 
bilalis  (Hiibn.)  and  coleopterous  larvae  belonging  to  at  least 
nine  genera  including  the  white  fringed  beetle,  Pnntomorus  tcu- 
colnma   (Boh.). 

The  life  historv  of  .V.  glascri  has  been  investigated  by  Glaser 
(1932)  and  by  Glaser,  McCoy  and  Girth  (l',t40).  The  following 
account  is  based  on  their  results  that  were  secured,  in  part  by 
using  Japanese  beetle  larvae  as  experimental  hosts  and  in  part 
by  rearing  on  culture  media.  It  is  lielieved  that  the  behavior 
of  this  nematode  is  not  materially  different  whether  growing  on 
culture  media   or   in   the   various  susceptible   insect   hosts. 

Japanese  beetle  grubs  acquire  their  infection  by  ingesting 
third  stage,  infective  larvae  of  the  parasite.  On  reaching  the 
alimentary  tract  the  larvae  immediately  develop  to  maturity 
and  copulate.  A  female  will  not  produce  offspring  unless  fer- 
tilized by  a  male.  The  female  is  ovoviviparous,  eggs  hatching 
within  the  uterus.  Larvae  may  remain  within  the  uterus  and 
move  about  for  a  considerable  period  but  eventually  pass  out 
through  the  vulva  one  at  a  time.  If  a  female  dies  before  all 
larvae  are  l)orn  those  remaining  may  undergo  partial  develop- 
ment within  the  dead  body.  Each  normal-sized  female  produces 
a  total  of  aliout  1-"  offspring  and  a  generation  under  optimum 
conditions  requires  about  ■)  to  7  days.  By  the  time  the  first 
generation  of  offspring  liave  matured  the  insect  is  usually 
dead  whereupon  its  entire  body  is  invaded.  The  nematodes 
usuall.v  pass  through  two  more  generations  consuming  the  car- 
cass and  leaving  only  a  sac  formed  by  the  skin  and  head  cap- 
sule and  filled  with  a  thin  fluid  swarming  with  larval  parasites. 
In  a  few  cases  Glaser  was  able  to  infect  newlj'  killed  beetle 
grubs  but  he  concluded  that  the  nematodes  do  not  enter  and 
multijily  as  readily  in  cadavers  as  in  living  insects. 

With  regard  to  the  virulence  of  this  parasite,  Glaser,  McCoy 
and  Girth  (lit-tO)  write  that  "occasionally  an  insect  Iiost  be- 
comes parasitized  very  lightly,  so  that  only  one  nematode  be- 
comes successfully  established.  This  individual  may  be  of  either 
sex,  and  while  if  frequently  (if  not  always)  causes  the  death 
of  the  host,  there  is  no  reproduction." 

McCoy,  Girth  and  Glaser  (19.38)  report  that  exceptionally 
large  females  of  X.  glaseri  are  occasionally  found  in  beetle  lar- 
vae though  never  on  cultures.  Such  individuals  may  develop 
an  enormous  number  of  eggs,  one  giant  female  producing  1,420 
larvae.  When  offsprings  of  a  giant  are  reared  to  maturity  on 
cultures  only  normal  sized  females  are  obtained.  >rcCoy,  Girth 
and  Glaser  concluded  that  fecundation  at  a  late  period  in  de- 
velopment and  abundant  food  are  factors  contriliuting  to  the 
production  of  these  giant   females. 

So  long  as  conditions  are  favorable  and  abundant  food  is 
availalile,  the  life  cycle  of  N.  glanni,  according  to  Glaser,  McCoy 
and  Girth  (1940),  is  completed  in  three  molts  the  third  stage 
being  omitted.  When  conditions  are  unfavorable,  as  when  the 
carcass  of  the  beetle  larva  has  l)een  consumed  and  food  is  ex- 
hausted, the  young  parasites  develop  into  third  stage,  dauer 
larvae.  At  the  end  of  the  second  stage  growth  ceases,  the  ali- 
mentary tract  is  emptied,  and,  as  a  result  of  certain  niorphologi 
cal  changes,  the  body  becomes  more  slender.    The  second  molted 


(Utide  is  retained  hcru'c  the  d.aui  r  Ijirva  is  ensheathed  though 
the  sheath  is  not  very  tenaci(ni8  and  may  soon  be  lost.  These 
dauer  larvae  escape  into  the  soil  where  they  are  able  to  persist, 
in  a  more  or  less  .'ictive  condition,  for  at  host  S'i  years. 

•  ■l.'L.si'r  and  his  coworkers  have  reared  this  lU'inatode  success- 
fully on  Petri  dish  jilates  of  veal  infusion  agar  flooded  with 
living  yeast,  on  jiofato  culture  medium,  and  on  veal  l>ulp 
medium.  These  investigators  found  that  "distiiu't  cultural 
characteristics  occur  in  nematodes  from  different  insect  cada- 
vers, .  .  .  There  is  a  slow  decline  in  fecundity  of  the  cultured 
nematodes,  some  'strains'  dying  out  after  .I  or  6  transfers, 
while  others  continue  to  yield  good  cultures  after  20  or  more 
ti.-insfers. "  If  beetle  larvae  are  infected  with  nematodes  from 
cultures  that  are  dying  out  .and  several  generations  are  passed 
in  the  natural  host,  the  nematodes  can  again  be  reared  success- 
fully on  cultures,  the  length  of  time  before  the  cultures  again 
die  out  depending,  to  some  extent,  on  the  number  of  genera- 
tions  iiassed   in   beetle  larvae. 

Am.oionkma  afpkndicui-atum  Schneider,  Is.'ill,  has  on  sev- 
eral occasions  been  found  within  the  bodies  of  slugs.  Schneider 
found  it  originally  in  Arioii  atrr  (L.)  and  Clans  (1890),  who 
investigated  its  life  history,  secured  his  material  from  the  same 
host.  The  life  cycle  of  this  nematode  appears  to  represent  a 
somewhat  different  line  of  evolutionary  development  than  the 
life  cycles  already  discussed.  According  to  Claus  (1890),  one 
or  more  free-living  generations  alternate  with  one  or  more 
jiarasitic  generations,  both  males  and  females  (Fig.  Ifi.'i  L  &  M) 
developing  in  each  instance.  Individuals  of  the  parasitic  gener- 
ations leave  the  host  .inst  before  reaching  maturity  by  boring 
their  way  out  through  the  foot.  On  reaching  the  exterior  they 
nuifure,  copulate  and  produce  progeny  that  usually  develop  as 
free-living  individuals.  Maupas  (1899)  found  that  larvae  of 
the  free-living  generation  undergo  the  usual  four  molts  and 
reach  maturity   in  about   3'4   days. 

A  regular  alternation  of  a  free-living  with  a  parasitic  gen- 
eration does  not  necessarily  follow,  however,  as  there  may  be 
several  consecutive  free-living  or  several  consecutive  parasitic 
generations.  There  are  usually  consecutive  free-living  genera- 
tions as  long  as  conditions  are  favorable  but  when  conditions 
become  unfavorable  the  nematodes  "encyst"  and  these  "en- 
cysted" larvae  will  continue  development  only  when  taken  into 
the  bod.v  of  a  slug.  According  to  Maupas,  "encysted"  larvae 
that  fail  to  gain  entrance  to  a  slug  become  exhausted  and  die 
in  about  4  months.  Precisely  how  the  nematodes  enter  the  slugs 
and  wlietlier  or  not,  in  event  of  consecutive  parasitic  genera- 
tions, females  mature  without  leaving  the  host,  are  points  that 
seem  to  need  further  elucidation. 

Claus  found  certain  morphological  differences  between  corre- 
sponding stages  of  the  two  generations.  Adults  of  the  parasitic 
generations  are  much  larger  than  adults  of  the  free-living  gen- 
erations and  parasitic  larvae,  in  the  later  stages  of  develop- 
ment, are  said  to  possess  two  long,  ribbon-like,  caudal  append- 
ages not  present  on  free-living  larvae  of  the  corresponding 
stage. 

Other  Species.  Diplogaster  labiala  Cobb  (in  Merrill  and 
Ford,  1916)  was  found  in  the  elm  borer,  Saperda  tridciitala 
Oliv.,  collected  near  Manhattan,  Kansas.  This  nematode  repro- 
duces in  the  intestine  of  the  living,  adult  liorer  and  may  ac- 
cumulate in  sufficient  numbers  to  rupture  the  gut  and  kill  the 
insect.  Infected  female  beetles  are  usuall.v  sterile.  When  reared 
on  cultures,  Merrill  and  Ford  (1916)  found  that  eggs  hatched 
in  from  30  to  32  hours  and  the  nematodes  matured  in  7  to  10 
days.  Oviposition  began  from  2  to  4  hours  after  copulation  and 
lasted  for  about  2  days  with  an  average  output  of^  seven  eggs 
per  female.  Only  a  few  individuals  were  seen  copulating  a  sec- 
ond time.  Apparently  dauer  larvae  (Fig.  lO."!  K)  develop  when 
conditions  are  unfavorable. 

Xcoaplectana  affinis,  Bovien,  1937,  was  found  in  Denmark 
where  it  infects  larvae  of  the  same  insects  that  harbor  Neoaplrc- 
lann  bibinni.s,  i.e.,  Bibio  fcrnif/iiiatii.s,  B.  hort iilanifs  and  VUo- 
pitus  vuli/aris.  These  two  nematodes  were  differentiated  mor- 
phologically by  Bovien  (1937)  only  on  the  basis  of  males  and 
dauer  larvae,  the  life  cycles  and  behavior  of  the  two  being  al- 
most identical.  Bovien  made  one  observation,  however,  that  de- 
serves mention.  When  in  the  intestine  of  any  of  its  three  nat- 
ural hosts  mentioned  above,  .V.  affinifi  remained  in  the  dauer 
stage  and  was  apparently  innocuous  so  long  as  the  insect  re- 
mained alive.  When  two  larvae  of  a  beetle,  Tcirplwru.i  sp., 
were  experimcntall.v  infected,  they  became  moribund  in  a  few 
days  and  dissection  revealed  several  adult  and  prcadult  nema- 
todes in  the  body  cavity  of  each  beetle.  This  observation  sug- 
gests that  whether  or  not  A',  affinis  remains  passively  in  the 
intestines    depends   on    the    insect    involved. 

A  mode  of  life  on  the  border  line  between  saprophagous  and 
parasitic  is  characteristic  of  other  nematodes,  probably  of  a 
considerable  number.  Other  species  of  Neoapleclana  are  known 
to  exist  but  life  cycles  have  not  been  investigated.   Steincrncvxa 


249 


hravssei  (Steiiier,  1923),  found  in  the  intestine  of  the  wasp, 
Cephalcia  abictis  (L.),  is  so  closely  related  to  the  genua  Neo- 
aplectana  that  a  similar  mode  of  life  is  suggested  but  verify- 
ing information  is  lacking. 

Among  the  rather  numerous  and  diverse  nematodes  that  have 
been  reported  from  snails  and  slugs  are  representatives  of  the 
Angiostomatidae  and  Cosmoeercidae,  two  families  that  include 
also  parasites  of  Amphibia.  The  four  species  mentioned  below 
will  serve  as  examples  but  very  little  information  is  available 
about  life  cycles.  Angiostoma  limacis  belongs  to  the  Angiosto- 
matidae while  the  other  three,  according  to  Chitwood  and  Chit- 
wood   (1937),  probably  belong  to  the  Cosmoeercidae. 

Angiosioma  limacis  Dujardin,  184.5,  has,  on  at  least  two  oc- 
casions, been  found  in  the  intestine  of  Arion  ater  (L.)  (Syn. 
Limax  rufa)  where,  apparently,  it  reaches  maturity.  Chitwood 
and  Chitwood  (1937)  report  finding  a  very  closely  related  spe- 
cies in  the  intestine  of  a  salamander,  Plctliodon  cinerens. 

Ascaroides  limacis  Barthelemy,  18.38,  was  found  in  eggs  of 
Deroceras  agrestis  var.  cincracea  Moq.  Tand.  (Syn.  Limax 
griseas),  each  infected  egg  containing  one  to  four  larval  para- 
sites. Barthelemy  (18.">6)  determined  that  the  nematodes  were 
already  present  when  the  eggs  were  deposited.  Apparently  the 
adult  of  this  parasite  has  not  j'et  been  studied. 

"Angiostoma"  helicis  Conte  and  Bonnet,  1903,  was  secured 
by  its  discoverers  from  the  slug,  Helix  aspersa  (Miill.),  where 
it  occurred  in  the  genital  organs,  especially  the  oviducts  and 
seminal  vesicle,  but  not  elsewhere  in  the  body.  Conte  and  Bon- 
net (1903)  concluded  that  the  parasite  is  passed  from  host  to 
host  during  copulation. 

Trionchonema  riisticum  Kreis,  1932,  was  secured  from  the 
land  snail,  Folygyra  espwola  Bland.  Presumably  this  parasite 
is  an  inhabitant  of  the  alimentary  tract  though  the  location 
\\-ithin  the  host  was  not  specified.  Kreis  (1932)  refers  to  the 
development  of  a  "filariform"  larva  and  suggests  the  possibil- 
ity "that  there  is  still  another  stage  of  development,  perhaps 
a  rhabditiform  larva,  which  could  not  be  found  and  which  may 
perhaps  be  free-living. ' ' 

Parasites  of  the  Alimentary  Tract 

All  nematodes  belonging  to  the  families  Thelastomatidae  and 
Rhigonematidae  and  to  the  subfamily  Ransomnematinae  are 
parasites  of  the  alimentary  tract  and  one  finds  an  occasional 
species  of  the  family  Diplogasteridae  that  has  acquired  this 
mode  of  life. 

The  thelastomatids  are  parasites  of  insects  and  myriapods  and 
scattered  through  the  literature  are  descriptions  of  between  60 
and  70  species  but  usually  not  much  other  information.  How- 
ever, studies  by  Galeb  (1878),  Dobrovolny  and  Ackert  (1934), 
and  others  indicate  that  most  of  these  species  probably  have 
about  the  same  tj-pe  of  life  cycle  and  that  it  is  comparatively 
simple.  Eggs  pass  out  of  the  host  with  the  feces.  Eggs  do  not 
hatch  in  the  intestine  to  reinfect  the  same  host  but  must  first 
undergo  some  development  on  the  outside  to  reach  an  infective 
stage.  The  various  arthropod  hosts  acquire  their  parasites  by 
swallowing  these  infective  eggs. 

In  the  genus  Pseudonymous,  the  species  of  which  are  parasites 
of  aquatic  beetles,  the  egg  is  provided  with  two  entangling  ap- 
pendages, the  so-called  spiral  filament  (Fig.  13.")  R,  p.  176) 
which,  presumably,  enables  the  egg  to  hang  on  aquatic  vegeta- 
tion thus  increasing  its  chance  of  lieing  ingested.  From  two  to 
four  eggs  of  Biiicma  biiirma  and  B.  ornaia  (Fig.  166G)  are  en- 
closed in  an  outer  capsule  or  case  of  loose  texture  formed,  ap- 
parently, by  the  entangling  and  anastomosing  of  polar  fila- 
ments.   The  purpose  of  this  adaptation  is  obscure. 

The  Rhigonematidae  and  Ransomnematinae  are  small  groups 
with  only  a  few  species  each.  It  seems  proliable  that  life  cycles 
of  these  nematodes  are  not  materially  different  from  the  type 
of  life  cycle  characteristic  of  many  thelastomatids  though,  ad- 
mittedly, such  a  statement  is  wholly  conjectural. 

Cephalobium  microbivorum  Cobb,  1920,  a  member  of  the 
Diplogasteridae,  inhabits  the  intestine  of  the  black  field  cricket, 
Gryllns  assimilis  (Fab.),  Avliere  it  may  occur  in  numbers  up  to 
30  or  more.  Infected  crickets  have  been  collected  in  Virginia 
and  Kansas.  In  the  region  of  Manhattan,  Kansas,  according 
to  Ackert  and  Wadley  (1921),  there  are  two  races  of  this  in- 
sect each  having  one  brood  a  year.  One  race  matures  during 
April  and  May  and  overwinters  in  the  nymph  stage  while  the 
other  race  matures  during  August  and  September  and  over- 
winters in  the  egg  stage.  These  investigators  found  that  in 
autumn  over  85  per  cent  of  the  adults  of  the  latter  generation 
were  infected,  the  incidence  being  somewhat  higher  in  female 
(about  90  percent)   than  in  male  crickets   (about  70  percent). 

Eggs  of  C.  microbivorum  are  usually  deposited  in  a  four-cell 
stage  and  pass  out  of  the  host  with  the  feces.  Ackert  and  Wad- 
ley  concluded  that  probably  eggs  hatch  after  being  voided  and 
that  a  cricket  becomes  infected  by  ingesting  larval  nematodes 


perhaps  after  these  have  undergone  a  brief  period  of  free-living 
development.  The  two  races  of  crickets  provide  the  parasite 
with  suitable  hosts  throughout  most  of  the  year  and,  no  doubt, 
some  of  the  nematodes  pass  the  cold  season  in  overwintering 
nymphs.  The  presence  of  this  nematode  has  no  obvious  effect 
on  the  well-being  of  the  cricket. 

Leidynema  appendiculatum  (Leidy,  18.50)  Chitwood,  1932. 
— The  life  history  of  Leidynema  appendiculatum,  which  was  in- 
vestigated by  Dobrovolny  and  Ackert  (1934),  is  probably  more 
or  less  typical  of  many  thelastomatids  and  will  serve  as  an 
example  of  the  family.  This  nematode  is  a  parasite  of  the 
cockroaches,  Blatta  orientalis  (L.)  and  Feriplaneta  americana 
(L.).  Out  of  259  individuals  of  P.  americana  collected  by 
Dobrovolny  and  Ackert  at  Manhattan,  Kansas,  90  harbored  this 
parasite  in  numbers  of  from  1  to  36  per  host. 

The  egg,  deposited  in  a  one  to  a  four-cell  stage,  passes  out 
of  the  insect  with  the  feces.  After  extrusion  it  undergoes  a 
short  period  of  development  and  a  tadpole-like  larva  (Fig. 
166  A)  is  formed.  The  larva  is  at  first  motile,  wiggling  and 
squirming  about,  but  becomes  inactive  as  the  infective  stage 
(Fig.  166  B)  is  reached.  Dobrovolny  and  Ackert  found  that 
at  37°   C.  eggs  reach  this  infective  stage  in  3  to   7   days  and 


Fig.  166.  PARASITES  OF  THE  INTESTINE 

A-F — Leidynema  appendiculatum  (A — -Egg  with  active  embryo;  B — 
Egg  with  larva  in  resting  stage;  C — An  early  stage  larva,  presumably 
second  stage;  D — Larval  female  showing  intestinal  diverticulum  be- 
ginning to  form;  E — Adult  male;  F — Adult  female).  G — Binema  or- 
naia, egg  capsule.      A-P,   after  Dobrovolny  and  Ackert,    1934. 


250 


that  I'KK"  iMiiitsiiiiinp  motile  laivm-  :iro  not  infective.  Alieala 
(1!<34)  found  tliat  tlio  larva  of  IlUillirola  bhiltar,  a  closely 
rolatod  llielastoniatid,  molts  in  the  okr  before  reaeliins  the  in 
feetive  since  and  while  Dotirovolny  and  Aekort  do  not  men- 
tion the  matter  their  liRnres  indieate  that  L.  (ipixniliciilalum 
undergoes  a  similar  molt.  If  kept  moist  at  room  temperatnre 
and  in  sniidned  lifrht  infeetive  vjxiix  remain  viable  for  a  eonsid 
erable  time  bnt  are  killed  by  jiroloiiK'ed  exposnre  to  direct  snn 
light.  Infective  egRs  are  inRcsted  by  the  insects  and  li.itih  in 
the  posterior  part  of  the  midgnt. 

Dobrovolny  and  .\ckert  kept  heavily  infected  cockroaches  in 
enptivity  for  more  than  a  year  and  -saw  no  evidence  that  tlu' 
insects  were  markedly  affected  by  the  parasites. 

Body  Cavity  and  Tissue  Parasites 

This  (jroup  imindes  wh.it  are,  i)erluiiis,  our  oldest  jiarasitic 
nematodes  in  the  sense  that  their  ])riiKenitors  w<'i'e  t\w  first  to 
assume  a  parasitic  mode  of  life  and  throuKli  the  aRcs  they  have 
become  very  highly  adapted  to  this  way  of  living.  Some  of  the 
allantonematids  have  become  almost  incrednlously  si)eciali/.ed  in 
morplK)logy,  liehavior  and  host  parasite  relationships  and  among 
them  are  to  be  found  some  of  the  most  unusual  nematodes 
known. 

MVEXCIlin.VE 

This  is  a  small  and  comparatively  little  known  group  of  nema- 
todes that  are  parasites  of  amphibians  and  leeches.  The  sys- 
tematic position  of  the  family  is  somewhat  questionable  but 
investigators  who  have  studied  the  group  regard  it  as  probably 
related  to  the  Tylenchidae.  Both  se.xes  arc  characterized  by  a 
medium  sized  stylet  without  basal  swellings  and  by  a  peculiar, 
sucker-like  organ  situated  on  the  mid  ventral  surface  about  one- 
fifth  of  the  distance  from  head  to  tail,  this  latter  presumably 
marking  the  position  of  the  excretory  pore.  Two  species  have 
been  reported  from  leeches. 

MvENClirs  BOTHRVOPHORUS  Schuberg,  1004,  was  found  in 
iTcrnuiny  ]>arasitizing  the  leech,  KnipobthUit  ortocuIaUt  (L.) 
(Syn.  S'cpliclix  viilgari.s  (Miiller)  iloi).  Tand.).  Different  stages 
of  the  nematode,  including  sexually  mature  individuals  (Fig. 
107  .-V  &  B),  occurred  in  the  connective  tissues  and  larvae  were 
found  within  the  muscle  cells  (Fig.  167  C).  Adults  were  also 
found  in  the  cocoons  of  the  leech.  All  the  details  of  the  life 
cycle  are  not  known  with  certainty  but  Schuberg  and  Schroder 
(1904)  concluded  that  larvae  undergo  the  first  part  of  their 
development  within  the  muscle  cells,  then  leave  this  location 
and  enter  the  connective  tissues  where  they  continue  develop- 
ment to  sexual  maturity.  From  this  point  on  the  life  cycle 
is  apparently  continued  outside  the  Iiost,  presumably  in  the 
cocoons.  Schuberg  and  Schroder  suggest  that  the  nematodes 
reach  the  cocoons  either  by  penetrating  into  the  gonads  and 
passing  out  with  the  reproduction  products  or  b3'  penetrating 
directly  through  the  body  wall  and  entering  the  cocoon  while 
this  structure  still  encompasses  the  body  of  the  leech.  The  fact 
that  the  i>arasites  are  frequently  found  in  the  connective  tissues 
immediately  underlying  the  epidermis  of  the  leech  seems 
to  make  the  latter  alternative  all  the  more  probable.  Schuberg 
and  .Schriider  concluded  that  the  females  lay  their  eggs  within 
the  cocoons  and  that  the  resulting  larvae  infect  the  young 
leeches.  How  the  parasite  enters  the  host  has  not  been  deter- 
mined. 

Myen-cius  botelhoi  Pereira,  1931,  is  a  parasite  of  the  leech, 
Limnobdella  bra.'iiUensi.s  Pinto,  and  was  found  and  studied  in 
Brasil.  According  to  Pereira  (1931),  infected  leeches  harbored 
the  nematode  in  all  stages  of  development.  The  epididymus  was 
a  favored  location  but  the  parasite  was  found  in  other  connec- 
tive tissues  tliimgh  rarely  in  the  muscles  and  never  in  the  ali- 
mentary tract.  Apparently  the  worms  occurred  between  but 
not  within  the  cells.  The  outstanding  point  of  interest  regard- 
ing this  nematode  is  the  fact  that  Pereira  found  it  regularly 
within  the  sjiermatophores  of  the  leech.  It  would  appear,  there- 
fore, that  the  parasite  enters  the  spermatophores  at  some  time 
during  their  formation  or  passage  out  of  the  leech  and  uses 
them  as  a  vehicle  for  transmission  from  host  to  host. 

DRlLONEMATrD-IE 

This  is  a  small  family  of  about  a  dozen  genera  that  arc  cither 
monotypic  or  contain  only  a  few  species  each.  These  nema- 
todes are  parasites  of  earthworms  and  occur  in  the  coelomic 
cavities,  in  or  associated  with  the  reproductive  organs  or  em- 
bedded in  the  muscles.  Many  of  the  species  are  characterized 
by  large,  sometimes  almost  sucker-like,  phasmids  and  some  of 
the  species  by  large  cephalic  hooks.  Very  little  is  known  about 
life  cycles. 

DiCELis  FiLARi.\  Dujardin,  184.i. — Of  the  specimens  of  Liim- 
bricus  rubelluit  Hoff.,  collected  by  Wiilker  (1926)  in  Germany 
near  Frankfort  a.  M.,  about  2.^  percent  harbored  this  parasite 


(Fig.  1(17  10  \-  F)  but  other  species  of  earthworms  collected  in 
the  .s.ime  region  were  not  infected.  The  usual  number  of  nema- 
todes per  host  was  6  to  H  with  a  maximum  of  22,  females  gen 
erally  outnumbering  nmles.  The  parasites  occurred  in  the  body 
cavity  of  the  host  in  the  region  of  the  reproductive  organs  but 
not  in  the  nephridi.-i. 

The  covering  of  the  egg  (Pig.  ]()7  D)  is  thick  with  a  rough 
outer  surface  indicating  that  the  shell  proper  is  probably  cov- 
ered by  an  external  coat  and  suggesting  that  the  egg  is 
e(iuipped  to  resist  adverse  conditions  and  jiersist  in  the  soil  for 
.1  considerable  period.  lOggs  are  laid  in  the  body  cavity  of  the 
host  but  do  not  continue  development  in  this  location.  Wiilker 
did  nut  (iinl  larv;il  stages  either  in  earthworms  or  in  surround 
ing  soil  and  was  unable  to  follow  the  life  cycle.  It  is  not 
known  how  eggs  are  expelled  from  the  host,  or  in  what  stage, 
the  p;irasites  enter.  Wiilker  demonstrated  that  if  the  earth 
worm  dies  these  nematodes  are  unalile  to  reproduce  in  the  car- 
cass but  perish  with  the  host. 

■1  l-:TKM)ONKM.\Tin.\E    .\XD    MKR.MITHIDAE 

To  the  family  Tetradonematidae  there  have,  as  yet,  been  as- 
signed only  two  sjiecies,  Tetradoncma  pUcan.i  and  Aproctonema 
rntomophaiinm.  These,  essentially,  are  primitive  mermithids 
and  must  be  included  in  any  general  consideration  of  life 
cycles  in  this  group. 


Fig.   107.     .MYENCHIDAE  AND   DRILOXEMATIDAE 

A-C — Miienchuit  bothryophorus  (A — Adult  female;  B — Adult  male; 
C — Larva  in  muscle  cell).  D-F — Dicelis  filaria  (D — Eggs;  E — Adult 
male;  F — Adult  female).  A-C,  after  Schuberg  and  Schroder,  1904: 
D-F,    after    Wiilker,    1926. 


251 


The  mermithids  are  preeminentl.v  insect  parasites  although 
crustaceans,  spiders,  snails,  and  some  other  invertebrates  are 
included  among  their  hosts.  Most  of  our  knowledge  regarding 
life  cycles  and  habits  has  beeu  derived  from  a  study  of  species 
that  infect  insects  and  the  following  discussion  has,  of  necessity, 
been  written  with  these  hosts  in  mind. 

Eggs  may  hatch  outside  the  host  and  larvae  reach  the  body 
cavity  of  the  young  insect  by  penetrating  its  body  wall  or  eggs 
may  be  ingested  and  larvae  reach  the  body  cavity  by  penetrat 
ing  the  wall  of  the  gut.  In  the  former  type  of  life  cycle  there 
is  a  tendency  for  larvae  to  enter  while  their  hosts  are  young 
and  for  each  host  to  harbor  a  small  number  of  parasites.  In 
the  latter  type  of  life  cycle  the  chances  of  the  host  becoming 
infected  are  likely  to  increase  with  its  age  and  food  consump- 
tion and  the  number  of  parasites  per  host  is  likely  to  be  greater. 
Tetradonema  plicans,  after  reaching  the  body  cavity  of  its 
dipterous  host,  develops  to  maturity,  copulates  and  lays  its  eggs 
as  an  internal  parasite.  This  is  a  simpler  and  probably  a  more 
primitive  life  cycle  than  that  known  for  any  mermithid.  Most 
mermithids,  after  completing  growth,  force  their  way  out  of  the 
host  and  are  free  living  during  the  adult  stage.  For  Ae/amer- 
mis  decaiulata,  Mcrmis  subnigrcsccns,  and  probably  some  other 
species,  the  free  living  period  is  of  two  years'  duration  and 
during  it  the  worms  undergo  their  last  molt,  copulate,  and  fe- 
males lay  their  eggs.  Aproctotiema  entomophagum  develops  to 
maturity  and  copulates  within  its  host  but  females  emerge  to 
lay  eggs,  while  Paramermis  contorta  undergoes  its  final  molt 
within  the  host  but  emerges  before  copulation.  For  both  these 
species  the  free-living  stage  is  of  very  short  duration  and  these 
life  cycles  seem  to  represent  intermediate  steps  between  the 
life  cycle  of  Tetradonema  pUean.i  and  that  of  such  species  as 
Agamermis  decaudata. 

If  a  species  enters  its  host  by  penetrating  the  body  wall  the 
posterior  portion  of  the  larva  is  often  modified  to  serve  as  a 
propelling  organ.  In  some  cases,  as  for  example  species  of 
Agamermis,  this  modified  posterior  portion,  which  may  consti- 
tute as  much  as  four-fifths  of  the  total  body  length,  is  de- 
tached during  the  act  of  penetration  and  remains  on  the  out- 
side. In  other  species  this  modified  portion  is  relatively  shorter 
and  persists  to  form  a  horn-like  appendage  at  the  posterior  ter- 
minus of  the  fully  grown  larva. 

In  most  mermithids,  especially  those  having  an  adult,  free- 
living  stage  of  considerable  duration,  the  intestine  grows  rap- 
idly during  parasitic  development  until  it  fills  nearly  all  the 
space  in  the  body  not  occupied  by  other  organs.  This  modified 
intestine,  filled  with  reserve  nutrient  materials  and  frequently 
referred  to  as  the  "fat  body,"  is  largely  responsible  for  the 
opaqueness  of  the  fully  grown  larva.  The  adult  becomes  in- 
creasingly transparent  as  these  stored  nutrients  are  consumed 
and  life  ends  when  they  are  exhausted. 

Most  mermithids  are  represented  by  both  sexes  but  the  sex 
ratio  is  subject  to  a  good  deal  of  variation,  not  only  as  between 
different  species  but  in  the  same  species.  Males  of  Amphimer- 
mis  suimiislii  and  of  Agamermis  deeandata  considerably  out- 
number females  while  males  of  Mermis  vigrescens  and  M.  sub- 
riigrescens  are  rarely  found.  The  sex  ratio  of  some  species  is 
influenced  by  environmental  conditions  during  parasitic  develop- 
ment. One  or  a  few  parasites  per  host  results  in  a  prepon- 
derance of  the  larvae  developing  into  females  while  a  large 
number  of  parasites  per  host  results  in  all,  or  nearly  all,  devel- 
oping into  males.  Convincing  data  demonstrating  this  environ- 
mental influence  on  sex  ratios  have  been  presented  by  Caullery 
and  Comas  (1928)  for  Parainermis  contorta,  by  Christie  (1929") 
for  Mermis  subnigreseens,  and  by  Kaburaki  and  Ij'atomi  (1933) 
for  Amphimermis  zuimusM.  There  is  evidence  suggesting  that 
some  other  species  behave  in  a  similar  manner. 

Functional  females  that  possess  such  male  characters  as  cau- 
dal papillae,  male  copulatory  muscles,  and  even  rudimentary 
spicules  have  been  reported  from  numerous  species.  It  seems 
probable  that  there  is  some  correlation,  as  yet  not  understood, 
between  the  influence  of  environment  on  sex  and  the  occurrence 
of  these  so-called  "intersexes." 

Females  of  Hexamermis  sp.  (parasite  of  the  ant,  Fheidoie 
pallidula)  and  of  Agamermis  decaudata  lay  eggs  only  after 
copulation.  Females  of  AUomermis  myrmecophilia  and  of  Mer- 
mis subnigreseens  produce  viable  eggs  in  the  absence  of  males 
though  individuals  of  the  latter  species  have  been  observed  in 
copula. 

The  presence  of  mermithid  parasites  affects  insects  in  various 
ways;  development  of  the  gonads,  especially  the  ovaries,  is 
usually  suppressed  resulting  in  sterility;  wing  muscles  are  some- 
times weakly  developed  reducing  ability  to  fly ;  internal  fat  de- 
posits are  largely  consumed;  development  of  the  body  as  a 
whole  may  be  retarded  and  metamorphosis  delayed ;  and  infected 
individuals  may  be  .sluggish  or,  in  the  case  of  ants,  have  a 
voracious  appetite.  As  a  rule  external  morphological  characters 
are  not  appreciably  modified  but  there  are  exceptions,  that  of 


ants  being  the  most  outstanding.     The  emergence  of  the  para- 
site usually  results  in  the  death  of  the  host. 

Numerous  species  of  ants  are  rather  commonly  infected  with 
mermithids.  Males,  females,  workers  and  soldiers  have  been 
reported  as  harboring  these  parasites  and  there  is  wide  varia- 
tion in  the  effects  of  the  mermithids  on  the  external  anatomy 
of  the  hosts.  In  some  instances  infected  ants  show  little  recog- 
nizable difference  from  normal  individuals  of  the  same  sex  or 
caste,  except,  perhaps,  a  somewhat  more  distended  gaster  and 
slight  variations  in  color.  This  seems  frequently  to  be  the 
case  with  infected  males  but  sometimes,  according  to  Gosswald 
(1930)  and  Vandel  (1934),  infected  females,  workers  or  sol- 
diers are  not  materially  modified.  In  some  instances,  on  the 
other  hand,  the  external  anatomy  is  greatly  modified  (Fig.  169 
C-G)  and  infected  ants  are  not  identical  to  any  normal  caste 
but  show  female,  worker  and  soldier  characters  in  varying  de- 
grees.    Such  individuals  are  called  intercastes. 

In  the  genus  Lasius  infected  females  resemble  normal  females 
but  are  easily  recognized,  at  least  in  many  instances,  by  a 
smaller  head,  shorter  wings,  and  a  somewhat  more  distended 
gaster.  Intercastes  of  this  type  have  been  designated  mer- 
mithogj/nes. 

In  the  genus  Pheidole,  Wheeler  (192S)  found  a  variety  of 
different  intercastes  with  mixtures  of  soldier,  worker  and  female 
characters.  He  recognized  five  more  or  less  distinct  types 
lias'.'d  on  thn  degree  of  resemblance  to  one  or  another  of  these 
three  normal  castes.  In  all  these  types  the  resemblance  was 
more  especially  to  woikers  and  soldiers  and  for  these  intercastes 
Wheeler  proposed  the  term  mermithergates. 

To  Vandel  (1930),  working  with  Pheidole  pallidula,  the  sit- 
uation was  somewhat  simpler  as  he  was  able  to  recognize  only 
two  types  of  intercastes.  One  type  showed  no  very  pronounced 
difference  from  normal  workers  except  a  somewhat  more  dis- 
tended gaster.  The  other  type  he  believed  to  be  modified  sol- 
diers and  for  these  he  proposed  the  term  mermithostratiotes  re- 
serving the  term  mermithergates  for  those  intercastes  where 
resemblance  to  workers  predominates. 

Gosswald  (1930)  found  young  mermithid  larvae  in  ants  at 
various  times  of  the  year  and  concluded  that  there  may  be  con- 
siderable variation  in  the  time  when  these  insects  acquire  their 
parasites.  Although  mermithids  have  been  found  in  larval  ants, 
only  a  few  such  cases  have  been  reported,  and  Vandel  concluded 
that  the  infection  is  usually  acquired  during  or  just  prior  to 
the  pupal  stage.  Based  on  the  size  and  development  of  larval 
mermithids  from  young  ants,  Gosswald  concluded  that  the  para- 
sites may  be  acquired  when  the  immature  insects  are  in  differ- 
ent stages  of  development  and  that  the  stage  when  the  parasites 
nre  acquired  determines,  in  a  large  measure,  the  degree  to  which 
the  adult  host  will  be  modified. 

How  ants  acquire  these  parasites  is  a  question  that  has 
aroused  considerable  interest  but  stimulated  little  actual  inves- 
tigation. Gosswald  (1930)  conducted  infection  experiments 
with  Lnsius  alienus  and  used  eggs  of  what  was,  presumably, 
AUomermis  myrmecophilia.  His  results  indicate  that  the  ant 
acquires  this  parasite  by  Ingesting  the  eggs.  As  ant-infecting 
mermithids  belong  to  several  genera  (Agamermis,  He.ramermis, 
Allomerinis,  etc.)  life  cycles  and  behavior  undoubtedly  differ 
and  all  may  not  necessarily  enter  the  host  at  the  same  time  or 
in  the  same  manner.  It  would  be  surprising  if  an  ant  became 
infected  with  a  species  of  Agamermis  by  ingesting  its  eggs. 

Tetradonema  plicans  Cobb,  1919,  is  a  parasite  of  the  dip- 
terous insect,  Sciara  coprophila  Lint.  It  has  been  found  in  only 
one  collection  of  these  insects  made  by  Hungerford  (1919)  at 
Manhattan,  Kansas,  in  which  every  individual  was  infected.  It 
occurred  in  larval,  pupal,  and  adult  flies  each  insect  harboring 
from  2  to  20  parasites  with  an  average  of  about  10,  the  number 
of  males  slightly  exceeding  the  number  of  females.  T.  plicans 
passes  its  adult  stage  and  lays  eggs  within  its  host,  differing  in 
this  respect  from  any  mermithid  of  which  the  life  history  is 
known. 

How  the  insects  acquire  their  infection  has  not  been  deter- 
mined. Eggs  (Fig.  108  G)  secured  by  Hungerford  from  around 
females  dissected  out  of  fly  maggots  hatched  in  a  few  hours 
when  placed  in  water  and  the  larvae  that  emerged  seemed  to  be 
identical  with  the  youngest  larvae  found  within  the  insects. 
These  larvae  were  of  two  types,  a  slender  type  about  12.')M  long 
with  a  curved  caudal  end  and  a  plumper  type  about  90/^  long. 
This  difference,  presumably,  is  sexual  dimorphism.  Hungerford 
found  eggs  of  the  parasite  in  the  digestive  tract  of  small  Sciara 
larvae  and  concluded  that  eggs  are  probably  swallowed  and 
nematode  larvae,  after  hatching,  penetrate  through  the  wall  of 
the  gut  into  the  body  cavity.  He  noted,  however,  that  "the 
older  maggots  are  much  less  susceptible  to  infestation  than  the 
younger  ones"  and  he  figures  the  tail  of  the  adult  parasite  with 
a  horn-like  projection  whicli  suggests  that  the  larva  has  a  cau- 
dal propelling  organ,  two  characteristics  that  one  is  inclined 


2.52 


Fig.    168.      TETRADOXEMATIDAE    AXD    MERMITHIDAE 


A-F — Api  ortonemn  fntotiiofihagxim  (A — Fertilized  ese:  B — Egg  con- 
t»ining  ovic  larva:  C — Very  young  larval  female;  D — Older  larval  fe- 
male; E — Larvnl  male;  F — Spermati^ed  female).  G  &  H^ — Tftrndonpiun 
plirnnn  ( G — Egg  ;  H — Egg-laying  female  with  male*  attached  } .  I — 
AUomermiit  mermifOphyUi,  egg.  J-M — Apamfrmiit  dpratidatn  (J — Xewly 
deposited  egg;  K — Egg  containing  ovit-  larva;  L — Infective,  preparasitic 


larva;  M — Grasshopper  nymph  containing  one  fully  grown  para*<itic 
female).  N — Mermis  suhnigrescens,  females  depositing  eggs  on  vege- 
tation. (All  eggs.  A.  B.  G.  I,  .7.  &  K,  drawn  to  snme  scale).  .\-F, 
after  Keilin  and  Robinson.  19^3  (C-F,  drawn  from  compressed  speci- 
mens) ;  G  &  H.  after  Hungerford,  1919;  I.  after  Crawley  and  Baylis. 
1921:  J,  K  &  M.  after  Christie,  19^6;  L,  after  Christie.  1929;  N.  after 
Christie,  1937. 


253 


to  associate  with  a  species  that  enters  its  host  by  penetrating 
the  body  wall. 

After  arriving  in  the  body  cavity  of  the  host  the  larval  nema- 
todes grow  rapidly  and  development  is  usually  so  timed  that 
females  copulate  and  deposit  eggs  before  the  fly  pupates. 
Adult  flies  were  found  that  contained  egg-laying  female  nema- 
todes and  also  small  larvae  that  approximated  the  size  usually 
reached  after  a  few  daj-s  of  parasitic  life.  Hungerford  believed 
these  small  individuals  had  been  arrested  in  development  by 
the  growth  and  maturity  of  the  other  worms. 

Eggs  pass  through  the  vulva  and  are  retained  within  the 
separated  but  unshed  cuticle  of  the  final  molt  which,  near  the 
middle  region  of  the  body,  becomes  distended  to  form  a  more 
or  less  spindle-shaped  egg  capsule  (Fig.  1(58  H).  Eggs  are  not 
normally  discharged  from  this  capsule  prior  to  the  death  of  the 
female.  This  final  molt  of  the  female  is  the  only  one  men- 
tioned by  Hungerford.  How  the  males  circumvent  this  encom- 
passing cuticle  and  effect  coition  is  not  explained.  The  host 
insect  is  eventually  killed  and  the  body  disintegrates  to  set  free 
a  residual  mass  of  nematode  eggs. 

Hungerford  found  that  the  internal  fat  deposits  of  infected 
fly  larvae  were  largelj'  consumed  leaving  the  body  much  more 
transparent  than  that  of  a  normal  individual.  Most  infected 
fly  larvae  died  before  pupating  but  where  the  infection  was 
acquired  late  or  the  parasites  were  few  in  number  the  fly  might 
endeavor  to  pupate.  Many  such  pupae  died  being  little  more 
than  nematode-filled  shells  but  some  succeeded  in  casting  off 
the  larval  skins.  The  emerging,  infected  adults  were  able  to 
fly  and  differed  very  little  in  appearance  from  normal  indi- 
viduals but  they  lacked  functional  reproductive  organs. 

Aproctonema  entomophagum  Keilin,  1917,  was  found  in 
England  where  it  is  a  parasite  of  the  dipterous  insect,  Sciara 
pulhda  Winn.,  the  larval  stages  of  which  inhabit  decaying  wood. 
The  morphology  and  life  history  of  the  nematode  are  discussed 
in  a  paper  by  Keilin  and  Robinson  (1933)  upon  which  the  fol- 
lowing account  is  based.  It  will  be  noted  that  the  host  of  this 
parasite  belongs  to  the  same  genus  as  the  host  of  Tctradonema 
plicans  and  the  two  nematodes  have  many  points  in  common. 

Each  infected  larval  fly  usually  harbors  several  females  of  A. 
entomophagum  (Fig.  168  F)  and  a  varying  number  of  smaller 
males  (Fig.  168  E).  Mention  is  made  of  one  larval  fly  that 
contained  2  females  and  10  males.  The  parasites  reach  ma- 
turity in  the  body  cavity  of  the  host  and  copulate  whereupon 
the  males  die  and  the  females  emerge  forcing  their  way  out  of 
the  host  in  the  manner  of  most  mermithids.  Egg  laying  begins 
almost  immediately  after  emergence.  Each  female  deposits 
somewhat  over  200  eggs  and  when  egg  laying  is  completed  the 
female  dies.  Hence  only  the  female  has  a  free-living,  post- 
parasitic  stage  and  it  is  of  very  short  duration. 

The  egg  (Fig.  168  A)  is  laid  before  cleavage  but  develops 
rapidly  and  in  a  few  days  contains  a  coiled  larva  (Fig.  168B) 
that  molts  before  hatching.  There  seems  little  reason  to  doubt 
that  the  larval  mermithids  enter  the  young  fly  larvae  by  pene- 
trating the  body  wall  though  actual  penetration  was  not  ob- 
served. 

If  infection  occurs  late  in  the  development  of  the  fly  larva 
the  parasites  may  be  carried  through  the  pupal  stage  and  in- 
fected adult  female  flies  were  found  though  not  infected  adult 
males.  The  parasites  delay  the  metamorphosis  of  the  insects 
and  infected  adult  female  flies  lack  functional  reproductive 
organs. 

Paramermis  contorta  (Linstow,  1889)  Kohn,  1913,  is  one 
of  the  aquatic  mermithids  of  which  there  are  a  considerable 
number.  It  is  a  parasite  of  Chironomus  larvae  and  was  dis- 
covered and  studied  in  Europe.  Each  host  usually  harbors  one 
parasite  but  sometimes  two  to  three  or  more.  The  sex  ratio, 
as  reported  by  different  investigators,  varies  a  great  deal  but 
in  most  cases  females  have  considerably  outnumbered  males. 

According  to  Kohn  (190.5),  P.  contorta  molts  before  leaving 
its  host.  This,  undoubtedly,  is  the  last  molt  and  the  uteri  are 
already  filled  with  eggs.  The  parasite  may  issue  through  the 
anus  or  force  its  way  directly  through  the  body  wall,  the  ma 
.iority  emerging  just  before  their  insect  hosts  would  normally 
pupate.  The  worms  settle  into  the  mud  at  the  bottom  of  the 
pool  and  copulation  soon  takes  place  tg  be  followed  immediately 
by  egg  laying.  According  to  Comas  (1927),  the  uteri  are  emp- 
tied and  egg  laying  completed  in  4  or  5  days  whereupon  the 
female  dies. 

Eggs  are  laid  before  cleavage  but  develop  immediately  and 
hatch  in  the  course  of  a  few  weeks.  The  mermithid  larvae  swim 
in  the  water  and  seek  young  Chironomus  larvae  which  they  en- 
ter by  penetrating  the  body  wall.  Comas  states  that  these 
mermithid  larvae  do  not  appear  capable  of  living  long  in 
water  and,  if  unable  to  find  and  enter  a  host,  will  die  in  a  few 
hours.  Comas  recounts  that  if  a  mermithid  larva  attempts  to 
penetrate  between  the  more  posterior  abdominal  segments  of 
its  prospective  host,  the  Chironomus  larva  may  reach  back  and 


with  its  mandibles  pull  the  nematode  away  or  bite  it  in  two. 
If  penetration  is  attempted  nearer  the  middle  of  the  body  the 
insect  will  be  unable  to  reach  the  nematode  and  penetration  is 
more  likely  to  take  place. 

Allomermis  myrmecophilia  (Crawley  and  Baylis,  1921) 
Steiner,  1924,  was  named  and  described  by  Baylis  and  its  life 
history  was  studied  by  Crawley  (Crawley  and  Baylis,  1921). 
The  specimens  were  from  two  species  of  ants  collected  in  Eng- 
land, Lasius  alienus  (Fijrst),  and  L.  flavus  (F.)  and  a  third 
ant,  L.  niger  (L.),  was  reported  as  a  host.  Observations  on  a 
mermithid  identified  as  this  species  and  secured  from  the  same 
ants  were  made  in  Germany  by  Gosswald  (1929;  1930). 

After  completing  its  parasitic  development  this  mermithid; 
according  to  Craw-ley,  emerges  from  the  ant,  sometimes  through 
the  anus  and  sometimes  between  two  of  the  ventral  plates  of 
the  gaster,  whereupon  it  enters  the  soil.  As  with  many  other 
mermithids,  emergence  apparently  occurs  over  a  considerable 
period  during  summer  and  autumn ;  Baylis  mentions  specimens 
that  emerged  during  July.  Crawley  first  saw  eggs  in  the  uteri 
of  experimentally  reared  females  on  December  .5.  Egg  laying 
begins  before  completion  of  the  final  molt  and  many  eggs  are 
retained  within  the  separated  but  uncast  cuticle  after  the  man- 
ner of  Tetradoncma  plicans.  As  mention  is  made  of  four  ex- 
perimental females  that  had  molted  by  November  20,  one  might 
infer  that  two  molts  take  place  after  emergence  but  Crawley 
and  Baylis  are  not  explicit  on  this  point.  Some  of  Gosswald 's 
(1930)  ant-infecting  mermithids  molted  twice  after  emergence 
Init  presumably  these  were  not  A.  myrmecophilia.  Bj'  actual 
count  Crawley  found  that  one  cast  cuticle  contained  6,560  eggs 
and  another  5,900  eggs.  Oviposition  continues  after  the  cuticle 
is  cast  off  and  probably  at  least  as  many  more  eggs  are  laid 
making  a  total  egg  output  of  12,000  or  more.  Eggs  (Fig. 
16S  I)  are  embedded  in  a  "gelatinous"  matrix  that  causes 
them  to  collect  in  masses  around  the  vulva  or  sometimes  to  be 
extruded  in  tlie  form  of  a  ribbon.  Crawley  and  Baylis  failed 
to  find  males  of  this  mermithid  and  Gosswald  demonstrated  that 
females  develop  and  lay  viable  eggs  without  copulation. 

Crawley  believed  that  ants  become  infected  while  in  the  larval 
stage  and  Gosswald 's  infection  experiments  seem  to  indicate 
that  eggs  of  the  parasite  are  ingested.  Crawley  and  Baylis  re- 
ported finding  only  mermithogynes  which,  when  present  in  a 
colony,  rarely  exceeded  the  normal  females  in  number  and  usual- 
l.y  were  much  fewer.  One  series  of  colonies  showed  an  average 
proportion  of  about  1  to  12.  Gosswald  found  infected  males 
and  workers  of  Lasius  alienus  and  L.  flavus  and  one  infected 
male  of  L.  niger.  Each  infected  ant  usually  harbors  one  mer- 
mithid though  sometimes  as  many  as  three. 

Infected  males  and  workers,  according  to  Gosswald,  show,  at 
the  most,  only  very  slight  external  differences  from  normal  ants. 
The  ovaries  and  wing  muscles  of  mermithogj-nes  fail  to  de- 
velop normally,  according  to  Crawley  and  Baylis,  but,  except 
for  a  marked  reduction  in  the  size  of  the  wings  and  a  more 
distended  gaster,  the  external  characters  show  no  pronounced 
dift'erence  from  those  of  normal  females  (Fig.  169  C  &  D). 

Hbxamermis  sp.  This  unidentified  species  of  the  genus 
Hexamermis  is  a  parasite  of  the  ant,  Pheidole  pallidula  (Nyl.), 
and  its  life  history  was  studied  in  France  by  Vandel  (1934). 
Most  individuals  complete  parasitic  development  by  late  summer 
or  autumn  and  emerge  from  the  ant  by  forcing  their  way  out 
through  the  anus.  They  do  not  remain  in  the  ant  galleries  but 
penetrate  a  short  distance  into  surrounding  soil  where  they  oc- 
cupy small  cavities.  The  final  molt  occurs  about  a  month  after 
emergence  and  is  followed,  within  the  next  month,  by  copula- 
tion and  egg  laying.  One  of  Vandel 's  experimental  females  had 
begun  to  lay  eggs  by  December  23  and  was  still  laying  eggs  on 
March  15.  Females  exhaust  their  reserve  nutrient  materials, 
stop  laying  eggs,  and  die  by  the  end  of  March  or  soon  there- 
after. Hence  there  is  one  generation  each  season  with  no  post- 
parasitic  individuals  in  the  soil  during  late  spring  and  early 
summer. 

The  infected  individuals  of  this  ant  are  mermithergates  and 
mermithostratiotes  and,  with  at  most  very  few  exceptions,  each 
harbors  one  parasite.  It  is  not  known  how  the  parasite  enters 
the  host.  Vandel  concluded  that  the  infection  is  acquired  either 
immediately  prior  to,  or  during  the  pupal  stage.  The  location 
where  eggs  are  laid,  the  small  number  of  parasites  per  host,  and 
the  vestigeal  caudal  appendage  of  the  adult  is  circumstantial 
evidence  suggesting  that  the  larva  penetrates  the  body  wall  of 
the  young  ant. 

Copulation  is  necessary  in  the  reproduction  of  this  mermithid. 
Experimental  females  reared  in  the  absence  of  males  by  Van- 
del  failed  to  lay  eggs.  These  females  lost  their  opaque  appear- 
ance very  slowly  and  some  lived  for  from  22  to  33  months  after 
emergence  whereas  females  that  were  allowed  to  copulate  and 
that  layed  eggs  lost  their  opaque  appearance  much  more  quickly 
and  lived  for  only  about  5  months  after  emergence. 

Agamermis  dbcadbata  Cobb,  Steiner  and  Christie,  1923,  oc- 


254 


curs  ill  the  north  i-oiitrnl  and  northoastorii  Uiiitod  States  wiicrc 
it  is  a  common  parasite  of  grasshoppers  inoUidinR  both  Acridi- 
dae  and  TotliKouiidae.  It  sometinioa  iiifeets  crickets  (drylli- 
dae)  and  has  been  found,  occasionally,  in  leaf  hoppers  and 
beetles.  The  life  history  of  this  merinithid  was  studied  by 
Christie  (I'.KiG)  upon  whose  work  tlie  following  account  is  based 
and  which  applies  to  the  soil  and  climatic  conditions  of  north- 
eastern Virginia. 

The  free  living  stages  of  this  nematode  occnjiy  small  cavities 
in  the  soil  usually  from  .">  to  15  cm.  below  the  surface  (proliably 
deeper  in  sandy  or  loose  soil).  When  inhabited  by  .'idults  each 
cavity,  almost  without  exception,  contains  one  female  aiul  sov 
eral  males,  generally  two  or  three,  sometimes  as  many  as  eight, 
coiled  and  intertwined  to  form  a  "knot."  Copulation  is  neces- 
sary and  females  reared  in  the  absence  of  males  fail  to  lay 
eggs.  Egg  laying  begins  about  the  first  of  July,  continues  until 
interrupted  by  the  advent  of  cold  weather,  and  eggs  (Fig. 
108  ,1  &  K)  accumulate  over  the  surface  of  the  soil  cavities  and 
over  the  parent  nematodes.  For  the  most  part  eggs  laid  during 
a  given  summer  do  not  hatch  until  the  following  spring.  Cleav 
ago  and  embryonic  development  take  place  after  deposition  and 
the  first  molt  occurs  within  the  egg  shell. 

At  the  time  of  hatching  the  second  stage  larva  is  immediately 
infective.  The  body,  which  shows  a  high  degree  of  organiza- 
tion and  development,  is  divided  into  two  parts  by  the  node 
(Fig.  1()8  LV  In  the  anterior  part,  which  constitutes  about 
one  fifth  of  the  total  length,  one  finds  most  of  the  organs  com- 
mon to  nematodes  including  esophagus  and  esophageal  glands, 
intestine,  nerve  ring,  and  excretory  pore.  The  posterior  part 
of  the  body  serves  as  a  propelling  and  food  storage  organ  and 
contains  a  row  of  cylindrical  cells,  probably  modified  intestinal 
cells.     An  anus  is  apparently  lacking. 

During  late  fall  and  winter  a  female  is  surrounded  by  her 
total  egg  output  of  the  season.  Egg  counts  on  six  females 
made  during  the  winter  showed  the  total  number  of  eggs  present 
to  vary  from  L!,(>2."i  to  6,.530.  As  will  be  noted  later,  a  female 
lays  eggs  during  two  summers  hence  these  figures  represent 
roughl.v  about  half  the  total  egg  output. 

Although  some  larvae  may  begin  to  emerge  from  the  eggs 
fairly  early  in  spring,  a  greater  part  of  them  hatch  during  a 
short  period  at  about  the  middle  to  the  latter  part  of  June.  The 
species  of  grasshoppers  that  mo.st  commonly  serve  as  hosts 
(Mclanoplus  fcmurrtibrum  and  Conoccphalns  brcvipennis  (Scud- 
der)  in  northeastern  Virginia)  also  hatch  at  about  this  time. 
The  larval  nematodes  migrate  to  the  surface  of  the  soil  and 
climb  grass  and  other  low  vegetation  when  it  is  wet  with  dew 
or  rain.  They  seek  newly  hatched  grasshopper  nymphs  and 
enter  their  body  cavity  by  penetrating  the  body  wall.  Pene- 
tration takes  place  under  the  edges  of  the  pronotum,  between 
the  abdominal  segments,  or  at  other  places  where  the  chitinous 
covering  is  thin.  Penetration  is  effected  by  the  use  of  the 
stylet  probably  aided  by  the  dissolving  action  of  a  chitin  sol- 
vent secreted  by  one  or  more  of  the  most  anterior  esophageal 
glands. 

After  the  anterior  end  is  inserted  into  the  host  the  body  of 
the  larva  breaks  at  the  node  and  the  postnodal  portion  is  left 
on  the  outside.  If  the  body  fails  to  break,  as  occasionally  hap- 
pens, the  postnodal  part  undergoes  no  development  in  the  host 
but  remains  as  a  vestigeal  appendage  that  eventually  sloughs 
off.  The  nodal  scar  (Fig.  93,  p.  89)  persists  throughout  the 
parasitic  stage  as  convincing  evidence  that  no  molt  takes  place 
during  this  period.  The  number  of  parasites  per  host  is 
usually  one  (Fig.  168  M),  sometimes  two,  rarely  three  or  more. 

Ouee  inside  the  body  cavity  of  the  host  the  parasite  under- 
goes a  period  of  phenomenal  growth  accompanied  by  pro- 
nounced morphological  changes.  The  stychocytes  (see  p.  92) 
arc  a  conspicuous  anatomical  feature  of  larvae  that  have  been 
in  the  host  from  4  to  10  days  (Fig.  93,  p.  89).  As  the  body 
increases  rapidly  in  length  it  becomes  filled  by  the  intestine, 
in  fact  intestinal  tissue  eventually  fills  all  available  space  not 
occupied  by  other  organs  even  growing  past  the  base  of  the 
esophagus  and  extending  into  the  neck  region.  Apparently 
this  modified  intestine  performs  no  digestive  function  but  serves 
as  a  reservoir  for  nutrient  materials.  Males  remain  in  the 
host  for  from  1  to  1V>  months  and  females  from  2  to  3 
months.  The  mermithids  emerge  head  foremost  forcing  their 
way  through  the  body  wall  between  the  segments,  fall  to  the 
surface  of  the  ground,  and  enter  the  soil. 

During  the  first  winter  in  the  soil  males  and  females  remain 
isolated  each  individual  forming  a  separate  "knot."  The  final 
molt  takes  place  the  following  spring  about  the  latter  part  of 
June  and  at  this  time  males  seek  the  females.  It  will  be  noted 
that  only  two  molts  have  been  observed.  Egg  laying  begins 
soon  after  the  final  molt,  usually  about  the  first  of  .Tuly,  and 
continues  until  interrupted  by  cold  weather.  The  following 
spring  a  year-old  female  begins  laying  eggs  slightly  earlier 
than  one  that  has  just  molted.     By  the  end  of  the  second  sum- 


mer of  egg  laying  the  reserve  food  has  become  exhausted  and 
the  transparency  of  the  body  is  in  sharp  contrast  to  its 
opaqueness  at  the  time  of  emergence  from  the  host.  Most  fe- 
males probably  fail  to  survive  a  third  winter  in  the  soil.  In- 
formation regarding  the  longevity  of  males  is  not  very  satis- 
factory but  it  seems  probable  that  they  live  for  about  the  same 
length  of  time  as  females. 

.1.  ilccaudala  causes  no  noticeable  change  in  the  external 
anatiiMiy  of  grasshoppers.  Infected  individuals  sometimes  have 
distended  abdonu'us  and  are  likely  to  apjicar  sluggish,  adults 
being  incapable  of  suslaimnl  flight.  The  most  pronounced  ef- 
fect of  this  parasite  is  on  the  gonads  of  the  host  (Fig.  109  A 
&  B).  It  is  doubtful  if  infected  female  grasshoppers  are  capa- 
ble of  laying  eggs  as  the  ovaries  are  always  greatly  reduced  in 
size.  The  effect  on  the  testes  is  less  pronounced  and  infected 
male  grasshoppers  have  been  observed  in  copula.  The  cme>-g- 
gence  of  the  parasite  invariably  results  in  the  death  of  the  host. 

Mekmis  siJHNiORKSCf;NS  Cobb,  1930,  appears  to  be  strictly  a 
grasshopper  parasite.  It  occurs  in  the  United  States  over  about 
the  same  range  as  Affajnermis  drcaudala  where  it  has  been 
found  infecting  nine  different  species  of  grasshoppers  including 
both   Acrididae  and   Teltigoniidae.     Several  other  species  have 


H  -~-      ^^^-x^  ^—    G 

Fig.   169.      EFFECTS   OF   MERMITHIDS   ON  THEIR   HOSTS 

A  &  B — Dissections  of  adult  female  grasshoppers,  Melanoplus  femur- 
rub  rum,  showing  reproductive  organs  (A — Normal  grasshopper;  B — 
Grasshopper  parasitized  by  Agamennis  decaudata) .  gas  cne,  gastric 
caeca ;  int,  intestine ;  o  i%  ovary ;  ovd,  oviduct ;  spthc,  spermatheca.  0 
&  D — Females  of  the  ant.  Lasius  alienus  (C — Normal  female:  D — Fe- 
male parasitized  by  Allomermis  mermicophyla,  i.e.,  a  mermithogyne). 
E-G — The  ant,  Pheidole  absurda  (E — Individual  parasitized  by  a  mer- 
mithid,  i.e.,  a  mermithergate;  F — Normal  worker;  G — Normal  soldier). 
H — The  ant,  Pheidole  f/auldi,  a  mermithergate.  A  &  B,  after  Christie, 
1936;  C  &  D.  after  Crawley  and  Baylis.  1921;  E-G,  from  Wheeler, 
1928,  after  Emery;  H^  after  Wheeler.  1928. 


2.15 


Au^usr  September 

Fig.    170a.      LIFE    CYCLE    OF   AGAilERillfi    DECAUDATA 

Diagram  illustrating  12-month  period,  August  to  July,  inclusive.  ". 
"knot"  composed  of  one  female  and  several  males  that  emerged  froni 
hosts  2  years  previous  to  beginning  of  period  represented,  b.  "knot" 
composed  of  one  female  and  several  males  that  emerged  from  hosts  1 
year  previous  to  period  represented.  Mermithids  that  would  emerge 
during  September  and  October  of  period  represented  are  omitted  for 
simplicity.  Female  in  "knot"  a  has,  by  October,  completed  its  second 
summer  "of  egg  laying  and  dies  during  ensuing  winter  but  the  accumu- 
lated eggs,  deposited  during  previous  summer,  hatch  May  to  June.  Fe- 
male in  "knot"  ii  has,  by  October,  completed  its  first  summer  of  egg 
laying  and  the  accumulated  eggs  hatch  May  to  June  while  the  second 
summer  of  egg  laying  is  begun  during  May. 


been  experimentally  infected.  Attempts  to  infect  other  insects 
including  crickets  (Gryllidae),  mole  crickets  (Gryllotalpinae), 
and  larvae  of  several  species  of  Lepidoptera  have  been  unsuc- 
cessful. The  following  account  of  the  life  history  is  based  on 
investigations  by  Christie  (1937)  conducted,  for  the  most  part, 
in  Massachusetts. 

Grasshoppers  become  infected  with  .1/.  siibnigrescens  by  swal- 
lowing the  eggs.  In  order  to  bring  this  about  the  egg-laying 
habits  of  this  nematode  are  radically  different  from  those  of 
Againer7nis  decaudata,  otherwise  the  two  life  cycles  are  some- 
what similar.  Eggs  of  .V.  siibnigrescens  are  never  laid  in  the 
soil.  Gravid  females  climb  low  vegetation  on  which  they  lay 
their  eggs  (Fig.  168  N)  and  to  which  the  eggs  cling  l)y  means 
of  the  entangling  appendages  or  bissi. 

The  egg,  when  deposited,  contains  a  fully  developed  infec- 
tive larva  (Fig.  140  B,  p.  ISl).  The  shell  proper  is  protected 
by  an  outer  covering  that  is  divided  into  two  cup-like  halves 
by  a  groove  at  the  equator  (Fig.  14(1  A,  p.  ISl).  At  each  pole 
there  is  a  raised  or  thickened  area  formed  by  the  attachment 
of  the  entangling  appendages  (Fig.  139,  p.  181).  The  outer 
covering  breaks  apart  along  the  groove  at  the  equator  and  the 
two  cup-like  halves  are  easily  removed.  In  the  shell  proper 
there  are  two  opposite  areas  at  the  equator  where  the  color  is 
lighter  than  elsewhere  and  these  areas  are  partly  dissolved  by 
the  digestive  action  of  the  host  thus  facilitating  the  escape  of 
the  larva.  Botli  the  outer  covering  and  the  shell  proper  con- 
tain brown  pigment,  presumably  to  protect  the  larva  from  the 
action  of  sunlight.  Eggs  deposited  on  foliage  remain  viable 
throughout  the  summer.  When  eggs  were  kept  experimentally 
in  a  moist  chamber  sonic  remained  viable  for  a  year. 

When  an  egg  reaches  the  alimentary  tract  of  its  host  the 
outer  covering  has  usually  been  rubbed  off.  The  two  opposite 
areas  of  the  shell  at  the  equator  gradually  become  clearer  and 
begin  to  protrude  until  they  appear  as  colorless  hemispherical 
projections  (Fig.  140  C,  p.  181)  that  finally  rupture  and  pro- 
vide openings  for  the  escape  of  the  larva.  The  larva  itself  does 
not  appear  to  aid  in  its  own  liberation.  Wlien  first  freed  it  is 
rather  sluggish  but  soon  becomes  active,  penetrates  the  wall  of 
the  gut  and  enters  the  body  cavity.  Penetration  through  the 
intestinal  wall  is  aided  by  the  stylet  which  is  rhythmically  pro- 
truded. 

From  1  to  5  parasites  per  host  is  the  number  most  frequently 
encountered  but  there  is  great  variation  and  grasshoppers  har- 
boring 100  or  more  parasites  of  widely  different  ages  are  not 
uncommon  in  some  localities.  As  a  nymph  grows  older  and  its 
food  consumption  increases,  its  chance  of  becoming  infected 
is  correspondingly  greater.  The  sex  ratio  of  M.  siibnigrescens 
is  intluenced  by  the  number  of  parasites  per  host.  When  a 
grasshopper  harbors  a  large  number,  all  develop  into  males  but 
when  a  grasshopper  harbors  only  1  or  2  these  usually  develop 
into  females  (Christie,  1929). 

The  parasitic  development  of  M.  siibiiignscens  is  essentially 
the  same  as  that  of  Agamcrmis  decaudata.  There  is  the  same 
rapid  increase  in  size  and  the  same  extensive  proliferation  of 
intestinal  tissue.  Males  remain  in  the  host  from  4  to  6  weeks 
and  females  from  8  to  10  weeks.  At  the  end  of  this  time  the 
parasites  force  their  way  through  the  body  wall  of  the  host 
and  enter  the  soil.  When  a  grasshopper  harbors  parasites  of 
different  ages,  all  that  are  too  immature  to  escape  and  survive 
in  the  soil  perish  with  the  host  when  the  older  ones  emerge. 


June 

Postparasitic  individuals  of  M.  siibnigrescens  are  found  in  the 
soil  down  to  about  60  cm.,  the  majority  occurring  from  15  to  4.1 
cm.  below  the  surface.  They  usually  remain  isolated  and  one 
larely  finds  a  "knot''  composed  of  a  female  and  one  or  more 
males  as  is  characteristic  of  Againerniis  decaudata.  Most  in- 
dividuals emerge  from  the  host  during  summer  and  autumn 
and  molt  the  following  April.  This  is  the  final  molt  and  the 
only  one  that  has  been  observed.  Copulation  may  take  place 
and  has  been  seen  on  several  occasions  but  copulation  is  not 
necessary  as  females  reared  in  the  absence  of  males  produce 
viable  eggs.  By  July  females  begin  to  exhibit  a  brownish  color 
due  to  accumulating  eggs  and  by  September  they  are  nearly 
Iilack  except  for  a  short  region  at  each  extremity  of  the  body. 
At  this  time  most  of  the  eggs  are  viable  but  they  are  not  laid 
until  the  following  spring.  Before  ovipositing,  a  gravid  female 
8")  mm.  long  contains  about  14,000  eggs. 

Egg  laying  usually  begins  in  May  and  may  continue  through- 
out July  or  even  into  August,  depending  on  weather  condi- 
tions. Eggs  are  laid  during  rain  and  should  the  early  summer 
months  be  dry  egg  laying  will  be  delayed.  Gravid  females 
climb  grass  and  other  low  vegetation  over  which  they  con- 
stantly move  while  eggs  are  being  laid.  If  rain  continues  egg 
deposition  goes  on  throughout  the  day  but  if  the  rain  stops 
and  the  foliage  becomes  dry  females  coil  up,  fall  to  the  sur- 
face of  the  ground  and  enter  the  soil,  presumalily  to  resume  egg 
laying   during   the   next   rain. 

It  is  not  known  how  long  females  live  after  the  uteri  are 
emptied  of  eggs  but  by  this  time  their  stored  food  is  nearly 
exhausted  and  it  seems  highly  improbable  that  the.v  are  able  to 
survive  a  third  winter  or  to  develop  more  eggs.  However,  if 
prevented  from  coming  to  the  surface  to  deposit  eggs  they  are 
able  to  survive  a  third  winter  and  to  lay  eggs  the  following 
spring.  Females  that  normally  would  have  deposited  eggs  in 
1932  were  buried  in  containers  and  prevented  from  coming  to 
the  surface  (Christie,  1937).  When  examined  during  May, 
1933,  many  of  these  females  were  alive,  in  good  condition,  and 
filled  with  eggs.  There  was  no  evidence  tliat  eggs  had  Ijeen 
deposited,  although  these  females  promptly  began  laying  eggs 
when  brought  to  the  surface  and  placed  in   the  light. 

Apparently  eggs  are  not  laid  at  night.  Egg  laying  is  con- 
trolled, at  least  in  part,  by  light  stimuli.  When  an  ovipositing 
female  is  placed  in  the  dark,  egg  laying  promptly  stops,  but  is 
resumed  just  as  promptly  when  the  female  is  again  placed  in 
the  light.  The  head  of  the  adult  female  is  colored  with  areas 
of  reddish  brown  pigment  which,  presumably,  is  an  organ  for 
light  perception.  The  male,  which  never  comes  to  the  surface, 
lacks  this  pigment. 

Merniis  siibnigrescens  has  about  the  same  effects  on  its  host 
as  does  Agamcrmis  decaudata.  These  effects  are  suppression 
of  the  gonads,  especially  the  ovaries,  and  death  of  the  host 
when  the  parasite  emerges.  With  If.  subnigresccns  the  effect 
on  the  gonads  of  the  host  is  much  more  variable  than  with  A. 
decaudata  due  to  variations  in  the  nnmlier  of  parasites  per  host 
and  the  time  the  parasites  are  acquired. 

.-VLLANTONEMATIDAE 

The  Allantonematidae  is  a  group  of  insect  parasites  that  are 
closely  related  to  the  preeminently  plant-infecting  Tylenchidae. 
The  species  that  have  been  studied  and  named  jnobably  con- 
stitute but  a  small  part  of  the  number  that  exist  but  in  nearly 
every  instance  where  the  life  cycle  is  known  it  follows  the  same 
genera!  plan  and  differs  from  that  found  in  any  other  group  of 
nematodes. 

Adult  gravid  females  occupy  the  body  cavity  (haemocoel)  of 
the  insect,  frequently  in  small  numbers,  often  one  per  host. 
Here  larvae  accumulate  and  develop  to  a  certain  stage,  molting 
at  least  once  (probably  twice  in  most  species)  ;  then  they  escape 
from  the  host  either  by  entering  the  alimentary  tract  and  pass- 
ing out  through  the  anus  or  by  entering  the  female  reproductive 
system  and  passing  out  thi'ough  the  genital  aperture.  Most 
species  infect  both  males  and  females  of  their  host  insect.  In 
some  eases  the  only  known  way  by  which  larvae  are  able  to 


Aug  list 


September 


Octtbrr 


huv.  -Alir 


Hay 


Ju  n  e 


July 


Fig.   170b.  I.IKK  rYCl.E  OF  AGAilKltMlS  DECAVDiTi — Continued 

Disgram  ilhislraling  fnsuiiig  rj-nionth  piTioii.  August  to  July,  in- 
clusive, c,  nierniilhids  einerKtiig  from  hosts  SejiteinlxT  to  October.  Fe- 
nmle  and  miiies  remain  in  separnte  cavities  until  latter  iiart  of  May 
when  males  seek  female,  copulation  takes  place,  and.  ilurins;  .luiie,  the 
(emnle  begins  it-s  first  summer  of  egg  laying.  Female  in  "knot"  h  has. 
by  October,  completed  its  second  summer  of  egg  laying  and  dies  during 
the  ensuing  winter  but  the  accumulated  eggs  hatch  May  to  .June.  (While 
the  above  diagram  is  essentially  correct  for  a  nia.iority  of  individuals 
where  grasshoppers  serve  as  hosts,  the  various  life-cycle  changes  are 
actually  spread  out  over  somewhat  greater  periods  of  time  than  the 
diagram  indicates.  A  few  eggs  hatch  before  May  and  June.  A  few 
prcparasitic  larvae  enter  hosts  as  early  as  .\pril  and  as  late  a.s  August 
and  the  time  of  emergence  is  correspondingly  affected.  A  few  individuals. 
especially  males,  emerge  from  hosts  at  least  as  early  as  July.) 


leave  the  host  is  via  the  female  reprtiduetive  system  ami  the 
fate  of  Uirvae  that  iiilialiit  the  beily  cavity  of  male  insects  is 
not   yet    fully    understood. 

A  free  living  stiige  is  passed  wheievor  the  liost  in.scct  umlef- 
goes  its  early  development  and  during  tliis  period  the  nema- 
todes molt  at  least  once  (as  a  rule  prohalily  twice)  and  Ijccome 
adults.  In  the  adult  male  the  stylet  is  usually  either  ahseiit  or 
weakly  developed  and  the  esophageal  glands  are  ineonspicuous 
ami  apparently  lacking.  In  the  preparasitie  adult  female  the 
stylet  is  usually  well  developed  and  at  least  one  of  the  esopha- 
geal glands  is  large  and  conspicuous.  E.xeeptions  to  these  mor- 
phological differences  between  the  sexe.s  are  usually  correlated 
with  deviations  from  the  more  typical  life  cycle.  The  apparent 
absence  of  esophageal  glands  and  the  somewhat  more  rapid  de- 
velopment of  the  genital  primordiuni  in  the  male  usually  make 
it  possible  to  distinguish  sex  at  an  early  stage  sometimes  while 
a  larva  is  still  within  the  egg. 

The  ovary  of  the  adult  preparasitie  female  is  small  and  com- 
posed of  only  a  few  cells  the  extent  of  its  development  differ- 
ing somewhat  with  different  species.  When  copulation  takes 
place  the  uterus  is  packed  with  small,  more  or  less  spherical 
spermatozoa.  After  copulation  males  usually  die  and  impreg- 
nated females  enter  their  respective  hosts,  usually  by  penetrat- 
ing the  body  wall  while  the  insect  is  still  in  the  larval  stage. 
The  fact  that  in  most  species  only  the  female  possesses  an  effec- 
tive stylet  and  at  least  one  well-developed  esophageal  gland  has 
been  regarded  as  evidence  that  these  structures  function  in 
connection  with  penetration  into  the  host.  There  is  little  reason 
to  doubt  that  the  stylet  is  employed  for  this  purpose.  It  has 
been  suggested  that  penetration  is  further  facilitated  by  a 
secretion  of  the  esojihageal  glands  which  may  serve  as  a  cliitin 
solvent.  The  validity  of  this  suggestion  does  not  rest  entirely 
on  morphological  evidence  for  Bovien  (1S)32)  demonstrated  that 
ScntDtirma  wiill'cri  does,  in  fact,  exude  a  rather  copious  secre- 
tion  through   the  stylet  at  the  time  of  penetration. 

The  free-living  stage  is  usually  of  short  duration.  There  is 
no  evidence  that  the  nematodes  feed  during  this  period  (with 
the  exception  of  Fergusobia  citrrici)  and  larvae,  at  the  time 
they  leave  the  host,  are  at  least  nearly  as  large  as  young 
adults.  However,  after  entering  a  new  host,  the  female  under- 
goes a  very  great  increase  in  size.  The  fully  grown  gravid  fe- 
male of  most  species  is  curved  ventrad  ;ind  assumes  a  form 
usually  referred  to  as  "sausage-shaped."  There  are  exceptions, 
however,  and,  for  example,  AUantonrma  miriiblr  is  oval  while 
in  many  species  of  A  ph  clench  id  us  the  body  is  bent  dorsad  with 
the  vulva  on  the  outside  of  the  curve. 

Some  species  deposit  eggs  in  the  body  cavity  of  the  host  but 
in  many  species  eggs  hatch  before  deposition  and  the  uterus  be 
comes  distended  with  developing  eggs  and  larvae  that  gradually 
fill  the  greater  part  of  the  body  and  push  the  ovary  into  the 
anterior  end.  As  a  rule  larvae  eventually  pass  through  the 
vulva  into  the  body  cavity  of  the  host.  There  is  a  tendency  for 
the  other  internal  organs  of  the  female  to  degenerate,  the  ex- 
tent  of   this   degeneration   differing   in   different    species. 

In  most  species  the  rapid  increase  in  the  size  of  the  female 
after  becoming  parasitic  provides  space  for  the  rei)roductive  or- 
gans. In  one  group,  the  Sphaerulariinae,  adequate  s|iace  for  the 
developing    reproductive    organs    is    not    provided    by    a    corre- 


sponding increase  in  body  size.  The  uterus  of  Si>li(ini(laria 
hombi  is  everted  through  the  vulva  and  the  entire  reproductive 
system  develops  outside  the  body  jiroper.  This  prolapsed  uterus 
increases  enormously  in  size  and  the  body  proper  remains  at- 
tached to  otu^  end  :is  a  vestigial  and  apparently  fiinctionless 
structure.  'I'ripiu.i  i/ibbusut!  (Syn.  Alractoncma  iiibbumim)  rep- 
resents an  intermediate  stage  in  the  evolutionary  developnuMit 
of  this  peculiar  adaptation  and  the  size  of  the  body  and  of  the 
jMolapsed  uterus  is  le.ss  disproportionate.  In  both  these  species 
the  life  c.vele,  so  far  as  known,  is  essentially  the  same  as  that 
of  most  allantonematids. 

There  are,  nevertheless,  several  deviations  from  this  typical 
life  cycle.  Young  adult  males,  as  well  as  young  adult  females, 
of  Par(i.iiti/lciicliii.s  di.ipar  typograpki  enter  the  body  cavity  of 
their  host  insect  where  they  are  found  in  large  numbers,  while 
neither  adult  males  nor  adult  females  of  Chondronema  passali 
become  parasitic,  only  larval  stages  being  found  in  the  host 
insect.  Chnndronevia  pansali  enters  its  host,  not  as  young 
adults,   but   as   young   larvae,   probably   by    being   ingested. 

Two  species  of  this  family  have  heterogeneous  life  cycles. 
There  is  interpolated  into  the  life  cycle  of  Heteroli/lcncliiis  aber- 
rans  a  parasitic,  parthenogenetic  generation  and  into  the  life 
cycle  of  Fergusobia  ciirriei  several,  consecutive,  "free-living," 
parthenogenetic  generations.  The  parthenogenetic  females  of 
Fergusobia  currici  occur,  associated  with  their  "host"  insect,  in 
plant  galls  where  they  feed  on  plant  cells  and  are,  in  fact, 
plant  parasites.  In  each  of  these  heterogeneous  species,  how- 
ever, the  gamogenetic  generation  still  follows  the  typical  allan- 
tonematid  plan  of  development. 

Tylenchinbma  oscinellab  Goodey,  1030,  is  a  body-cavity 
parasite  of  the  frit-fly,  Oscinclla  frit.  (L.).  The  life  history  of 
this  nematode  was  studied  in  England  by  Goodey  (1930,  1931). 

The  frit-fly  has  three  generations  a  year.  Eggs  are  laid  on 
small  oat  plants  generally  during  May  and  fly  larvae  penetrate 
the  shoots,  destroying  the  central  tissues.  This  is  the  first  or 
stem  generation.  Adult  flies  appear  by  mid-July  and  deposit 
eggs  on  the  panicles  of  oats  where  the  larvae  attack  the  tissues 
of  the  inflorescence.  This  is  the  second  or  panicle  generation. 
Adult  flies  again  appear  during  August  or  early  September  and 
lay  eggs  on  various  species  of  wild  grasses.  This  is  the  third 
or  grass  generation;  also  it  is  the  overwintering  generation  and 
winter  is  passed  in  the  larval  stage.  The  life  cycle  of  the  nema- 
tode is,  of  necessity,  closely  correlated  with  that  of  the  frit- 
fly  and  like  it,  undergoes  three  generations  a  year  (Fig.  17.5). 

Infected  flies  hariior  usually  one,  sometimes  two  or  three, 
more  rarely  four  to  eight,  adult  female  nematodes  that  give 
birth  to  living  young.  Eggs  pass  into  the  uterus  of  the  mother 
nematode  where  they  undergo  development.  As  more  and  more 
eggs  are  produced  the  uterus  becomes  distended,  pushing  the 
ovary  into  the  anterior  end  and  finally  occupying  most  of  the 
space  within  the  body.  Larvae  (Fig.  171  A  &  C),  escaping 
from  the  egg  membranes,  pack  the  posterior  etui  of  the  uterus 
and  finally  pass  through  the  vulva  into  the  body  cavity  of  the 
host.  Here  they  accumulate  and  continue  development.  Goodey 
observed  one  molt  that  takes  place  when  a  larva  is  about  4G0/i 
long  and  which  he  believed  to  be  the  second  suspecting  that  the 
first  molt  takes  place  while  the  larva  is  still  within  the  uterus  of 
the  mother.  The  gonads  undergo  considerable  development  and 
show  differences  that  make  it  possible  to  distinguish  sex.  The 
wall  of  the  intestine  becomes  well  stocked  with  reserve  food 
globules. 

After  attaining  a  size  nearly  as  large  as  free-living  adults, 
the  larvae  escape  from  the  host.  To  accomplish  this  they  pene- 
trate the  food  reservoir  of  the  fly's  digestive  system  from  which 
they  migrate  through  the  intestine  to  the  rectum  and  are  e.iected 
through  the  anus.  With  regard  to  this  escape  of  larvae,  Goodey 
writes  as  follows:  "Parasitized  flies  of  both  sexes,  having 
failed  to  develop  their  sex  cells,  fly  about  and  instead  of  taking 
part  in  the  normal  process  of  reproduction  are  able  only  to 
deposit  larvae  of  the  nematode  parasite.  Normal  females  go  to 
oat  panicles  and  there  lay  eggs;  similarly,  the  parasitized  fliea 
responding  to  the  same  urge  of  the  life-cycle  rhythm  also  fly 


2o7 


to  oat  panicles,  but,  instead  of  eggs,  deposit  larvae  of  the  nema- 
tode parasite.  These  find  their  way,  possibly  in  response  to 
some  ehemotactic  stimulus,  into  the  plant  tissues  surrounding 
the  fly  larvae."  In  this  environment  the  nematode  larvae  con- 
tinue development  and  two  final  molts  take  place,  the  last 
cuticle  separating  while  the  larva  is  still  within  the  cuticle  of 
the  preceding  molt. 

Larvae  that  Goodey  removed  fi'om  the  gut  of  infected  flies 
and  kept  in  tap  water  completed  their  final  molt  in  about  41 
hours.  Males  remained  alive  for  about  14  days  and  females  for 
about  29  days  but  copulation  did  not  take  place  while  the  worms 
remained  in  water.  In  nature  copulation  follows  the  final  molt 
and  the  uterus  of  the  female  is  distended  with  spermatozoa. 
The  preparasitic  female  (Pig.  171  F  &  G)  has  a  well  devel- 
oped stylet  with  basal  swellings  and  a  large  dorsal  esophageal 
gland.  These  structures  are  inconspicuous  or  lacking  in  the 
male.    (Fig.  171  E). 

Tlie  male  does  not  again  beconu-  parasitic  but  the  impreg- 
nated, precocious  female  enters  the  body  cavity  of  a  frit-fly 
larva.  Goodey  did  not  actually  observe  the  entrance  but  as- 
sumed, no  doubt  correctly,  that  it  is  accomplished  by  penetrat- 
ing the  body  wall.  The  incidence  of  infection  is  about  the 
same  for  male  and  female  flies  except  possibly  in  the  grass  or 


overwintering  generation,  where  Goodey  found  that  about  two- 
thirds  of  the  infected  flies  were  females. 

After  becoming  parasitic  the  female  nematode  increases  very 
greatly  in  size  and  is  about  fully  grown  when  the  host  emerges 
from  its  pupal  ease.  Tlie  body  has  assumed  the  characteristic 
"sausage  shape"  and  the  ovary  has  completed  its  development 
(Fig.  11.')  J,  p.  136).  The  stylet  is  retained  and  Goodey  be- 
lieves that  probably  the  parasite  continues  to  take  food  via  the 
alimentary   canal. 

Tylenchhicma  oscincUae  produces  no  noticeable  effect  on  the 
external  characters  of  its  host  but  it  prevents  the  normal  de- 
velopment of  the  gonads  and  both  male  and  female  flies  are 
sterilized.  Occasionally,  however,  parasitized  flies  of  both  sexes 
develop  normal  sex  organs  and  when  this  happens  the  parasite 
fails  to  undergo  normal  development.  In  regard  to  this  Goodey 
(1931)  writes:  "In  the  great  majority  of  cases  the  worm  man- 
ages to  get  the  upper  liand  and  grows  to  sexual  maturity  within 
the  host,  but  occasionally  the  fly,  during  its  final  metamorpho- 
sis, is  able,  by  some  means,  to  Imild  up  its  gonads  in  the  nor- 
mal manner.  When  this  happens  the  worm  fails  to  grow,  re- 
mains non-functional  and  becomes  degenerate.  .  .  .  These  rela- 
tionships may  possibly  be  explained  on  the  supposition  that  the 
worm  secretes  or  excretes  something,  perhaps  from  the  intesti- 


rig.  171.     ALLANTONEMATIDAE 


A-G — Tylenchinema  oscinellne  (A — Very  young  male  larva  and,  B, 
genital  primordium  of  same;  C — Very  young  female  and,  D,  genital 
primordium  and  esophageal  gland  of  same;  E — Adult  male;  F — Adult, 
preparasitic   female    and,    G,    anterior    end   of    same.      For   fully    grown. 


adult,  parasitic  female,  see  Fig,  115  J,  p.  136).  H-J — Allantonema 
mil-able  (H — Adult  male;  I — Adult,  preparasitic  female  after  copula- 
tion ;  J — Fully  grown,  adult,  parasitic  female.  For  stage  intermediate 
between  I  and  J,  see  Fig.  115  I,  p.  136).  A-G,  after  Goodey,  1930; 
H-J,  after  Wulker,  1923. 


il58 


FiK.  172.     ALLANTONEMATIDAE 


Al — yScatonemn  wulkeri.  (A — Newly  hatched  female  larva;  B — New- 
ly hatched  male  larva;  C — Partly  grown  male  larva;  D — Female  just 
before  final  molt;  E — Adult  preparasitic  female  after  copulation;  F — 
Male  just  before  final  molt;  G — Adult  male;  H — Adult  parasitic  female 
a  few  days  after  entering  host;  I — Fully  grown  gravid  female).  J-0 — 
BelerotyUnehuH  aberrans  (J — Egg  laid  by  female  of  gamogenetic  gen- 
eration; K — Egg  laid  by  female  of  parthenogenetic  generation;  Lr — New- 
ly   hatched    larva    of    gamogenetic    generation;    M — Adult    preparasitic 


female  of  gamogenetic  generation;  () — Fully  jjruwii  female  of  par- 
thenogenetic generation).  P — Aphplenrhnhm  tliplopajtter,  adult  para- 
sitic female.  Q-S — FerguHohiu  curriei  Hi  &  R — Adult  male  and  adult 
female,  respectively,  of  "free-living"  generation,  i.e.,  from  EttcalyptiiH 
galls;  S — Gravid  female  of  "parasitic"  generation,  i.e.,  from  body  cavity 
of  gall  fly).  T  &  U — Parasitylenrliux  dinpar  ti/pographi,  adult  parasitic 
male  and  adult  parasitic  female,  respectivelv.  A-I.  after  Bovien,  1932; 
J-0,  after  Bovien,  1937;  P,  T  &  U.  after  Fnchs.  1915;  Q-S,  after  Car- 
rie,  1937. 


259 


Fig.   173 

Diagram  illustrating  life  cycle  of  Scatotienui  iriilkeri.  The  adult  para- 
sitic female  (a)  produces  offspring  (b)  that  eventually  enter  the  female 
fly  s  reproductive  organs  and  are  extruded  with  the  eggs  (c).  Outside 
the  host  these  larvae  develop  into  adults  (rf)  and  copulate  whereupon 
males  die  and  impregnated  females  (e)  enter  flv  larvae.  These  females 
then  undergo  a  period  of  growth  (/)  and  mav  begin  producing  off- 
spring (n«)  while  the  fly  is  still  in  the  larval  stage  or  females  mav  be 
only  partly  grown  (though  adult)  (p)  when  the  flv  pupates  and  begin 
flaying  eggs   (a)    when  the  fly  becomes  adult.     After  Bovien,  1937. 


Fig.  174.     CnONDROXEMA  PASSALI 

A — Oldest  larva  found  within  body  cavity  of  host:  B — Youngest  larva 
found  within  body  cavity  of  host:  C-E — Portions  of  body  of  adult  fe- 
male filled  with  eggs  or  larvae  and  serving  as  brood  sac;  P — Eggs. 
All  figures  after  Christie  and  Chitwood.  1931. 


nal  [esophageal]  gland,  nliieli  prevents  tlie  normal  growth  of 
the  host's  sex-eells.  At  the  same  time  it. is  quite  likel.v  that  the 
same  may  be  true  of  the  host;  if  once  its  reproductive  organs 
become  sufficiently  developed,  then  it  is  able  to  pour  out  some 
substance  which  definitely  inhibits  the  growth  of  the  worm." 
Allantonema  mirable  Leuckart,  1884,  is  a  bodv  cavitv 
parasite  of  the  pine  weevil,  Eylohius  ahirtis  (L.)  and  occurs 
in  Europe  but  has  not  been  found  elsewhere.  This  nematode 
differs  from  TylencMnema  oscinellae,  not  so  much  in  its  life 
cycle,  which  is  essentially  the  same,  as  in  the  form  and  degen- 
eration of  the  gravid  female.  Unlike  most  allantoiiematids,  the 
fully  grown  female  (Fig.  171  J)  is  oval,  some  L.T  to  2  mm. 
in  length  and  about  half  as  wide  as  long.  Its  bodv  is  virtually 
a  sac  largely  filled  by  the  uterus  as  it  becomes  di.stended  witii 
eggs  and  larvae.  The  other  internal  organs  degenerate  to  such 
an  extent  that  if  vestiges  persist  their  identitv  has  not  liecn 
recognized. 

Eggs  hatch  in  the  uterus  where  they  begin  to  accumulate 
during  late  summer  and  where  they  remain  during  the  winter 
undergoing  little  development.  In  "the  spring  larvae  begin  to 
pass  through  the  vulva  into  the  body  cavity  of  the  weevil 
where  they  undergo  two  molts.  Larvae  finally  leave  the  host  by 
penetrating  its  alimentary  tract  and  passing  out  thiougli  tlie 
anus. 

The  adult  female  of  Hylnbins  abiFfix  eats  small  holes  in  the 
bark  on  the  trunk  and  roots  of  fir  and  certain  other  coniferous 
trees.  In  this  cavity  eggs  are  laid  and  hatch,  the  young  weevils 
tuiineling  into  adjacent  tissues.  In  order  to  pass  their  free- 
living  stages  in  the  immediate  vicinity  of  newly  hatched  weevils, 
the  larval  nematodes  must  escape  when  and  where  female 
weevils  are  laying  eggs,  albeit  not  through  the  genital  aperture 
of  the  insect.  Wiilker  (1923)  observed  only  one  molt  during 
free-living  development  which  took  place  after  8  to  10  days. 
Bovien  (1937)  found  that  larvae,  taken  from  the  rectum  of 
adult   weevils  and   placed   in  hanging  drops  of  water,  became 


adult  in  5  to  6  da3'S.  The  final  molt  is  followed  very  soon  by 
copulation  after  which  males  die  and  impregnated  females  enter 
the  body  cavity  of  weevil  larvae  that,  in  the  meantime,  have 
hatched. 

The  adult  preparasitic  female  of  A.  mirable  (Fig.  171  I)  has 
a  well  developed  stylet  and  Bovien  (1937)  figures  two  esopha- 
geal glands,  one  opening  into  the  esophagus  on  the  dorsal  side 
near  the  base  of  the  stylet  and  the  other  on  the  ventral  side 
farther  back.  In  the  adult  male  (Fig.  171  H)  a  stylet  is  pres- 
ent though  somewhat  more  weakly  developed  than  in  the  female 
but  the  esophageal  glands  are  inconspicuous  or  lacking. 

By  about  July,  when  the  weevils  are  pupating,  the  parasitic 
female  nematode  is  producing  ova.  Fuchs  (1915)  states  that 
ni/lohiiif:  abii'tis  lives  for  at  least  31  months  and,  finding  fe- 
males of  A.  mirable  in  2-yearold  weevils,  he  concludes  that  the 
nematode  lives  for  at  least  2  years. 

SrATOXEM.4.  wuLKERi  Bovien,  1932,  is  a  liody  cavity  parasite 
of  the  dipterous  insect,  Scatopse  fiiscipes  Meig.,  the  immature 
stages  of  which  develop  in  manure  and  other  putrescent  mate- 
rial. Eggs  of  this  nematode  hatch  in  the  uterus  where  larvae 
(Fig.  172  A  &  B)  undergo  early  development,  the  extent  of 
this  development  varying  considerably.  In  some  cases,  which 
Bovien  (1932)  regards  as  exceptional,  an  individual,  while  still 
within  the  uterus,  ma.y  reach  maturity  and,  in  turn,  develop 
larvae  within  its  uterus,  thus  creating  three  generations,  one 
within  another.  Most  of  the  progeny,  however,  pass  through 
the  vulva  into  the  body  cavity  of  the  host  as  partly  grown 
larvae.  These  larvae  enter  the  reproductive  system  of  the  in- 
sect and  pass  out  with  the  eggs.  When  an  infected  fly  dies 
not  all  the  harbored  parasites  necessarily  perish  but  some 
larvae  may  complete  development,  molt,  and  copulate  after 
which  impregnated  females  escape  from  the  dead  body.  As 
male  flies  die  soon  after  copulation  Bovien  concludes  that,  in 
moist    surroundings,    part    of    the    nematodes    may    be    able    to 


260 


^V-J 


Fig.   173.      TTLEXCHINEilA   OSCINELLAE 

Schematic  drawing  illustrating  life  history  of  frit-fl.v  in  its  three 
^easonal  generations,  and  the  approximate  time  occupied  by  each,  linked 
with  that  of  its  parasite.  Tylenchinema  oscin^llae.  The  various  stages 
of  the  rty  and  worm  are  greatly  enlarged  whilst  the  outs  and  gr.Tss  are 
smaller  than  natural  size.  Although  the  female  fly  only  is  shown  it  is 
to  be  understood  that  the  male  also  carries  the  parasite.  The  dotted 
circles  contain  stages  of  the  parasite  related  to  the  corresponding  stage 
of  the  host.  The  circles  cut  into  the  pupa  and  imago  hut  not  into  the 
fly  larva  in  each  case,  thus  showing  that  the  parasite  is  within  the  pupa 
and  fly  hut  not  within  the  larvae,  c  I,  ensheathed  larvae;  /  r,  food 
reservoir  of  fly  with  larvae  passing  in:  g  f,  growing  female  worms;  7»  /. 
mature  female  worms,    .^fter  Goodey,  1931.  explanation  quoted  verbatim. 

escape  from  the  decaying  insects.    Otherwise  tlie  fate  of  larvae 
harbored  by  male  fiies  is  unknown. 

Bovien  observed  only  one  molt,  the  last,  which  may  occur 
liefore,  but  usually  not  until  after,  emergence  from  the  host. 
As  this  molt  takes  place  not  later  than  24  hours  after  emer- 
gence and  is  followed  immediately  b.v  copulation,  the  free  living 
stage  is  of  short  duration.  In  the  adult,  preparasitic  female 
(Fig.  172  F)  the  stylet  and  esophageal  glands  (Bovien  figures 
two)  are  well  developed  while  in  the  adult  male  (Fig,  172  G) 
these  structures  arc  inconspicuous  or  absent.  By  the  less  well- 
developed  genital  primordium  and  the  presence  of  esophageal 
glands  one  can  distinguish  female  larvae  while  they  are  still 
within   the  egg. 

Regarding  penetration  of  preparasitic  females  into  the  body 
cavity  of  a  fly  larva  Bovien  (1932)  writes  as  follows:  "In 
many  cases  I  found  the  nematodes  in  the  act  of  entering  the 
body  of  the  larva.  In  a  few  cases  I  saw  dead  nematodes,  which 
had  not  succeeded  in  penetrating  the  body  wall,  held  fast  by  it. 
Tlie  jienetration  may  take  place  through  all  parts  of  the  surface 
of  the  larva  and  no  preference  seems  to  be  given  to  any  ])ar 
ticular  region.  The  very  beginning  of  this  act,  however,  was 
not  observed.  I  placed  female  worms  in  hanging  drops 
together  with  Scatopse-\aT\ae,  the  presence  of  which  had  an 
unmistakably  attractive  influence  on  the  nemas.  The 
nematodes  slung  themselves  around  the  body  of  the  larva, 
pressing  their  mouths  against  the  skin  without  being  able  to 
puncture  it,  I  suppose  this  failure  may  be  :iscril)ed  to  the  lack 
of  supporting  surfaces.  On  the  third  day  the  worms  were  dead. 
,\n  oblong,  somewhat  spiral-wound,  coagulated  ma.ss  of  secre- 
tion had  been  ejected  from  the  aperture  of  the  buccal  stylet, 
and  the  salivary  [esophageal]  glands  apjieared  to  be  empty.'' 
The  jjrcscnce  of  the  parasite  does  not  result  in  sterility  of  thi' 
host. 

Chondronema  PASSALi  (Lcidy,  18.')2)  Christie  and  Chitwood, 
Ifl.Sl,  is  a  body  cavity  parasite  of  the  beetle  PopiliiiK  ivlrrr\ip- 


Fig.  176.      HETEROTYLENCHUS  ABERRANS 

Diagram  illustrating  life  cycle  of  Heterotylenchua  aberran.t.  The 
adult  parasitic  female  of  the  gamogenetic  generation  («)  lays  eggs  (6) 
that  develop  into  females  of  the  parthenogenetic  generation  (c).  These 
females  lay  eggs  (rf)  and  the  resulting  larvae  (e)  enter  the  reproductive 
organs  of  the  female  fly  and  pass  out  through  the  genital  aperture. 
Outside  the  host  these  larvae  develop  into  adults  of  the  gamogenetic 
generation  (/)  and  copulate  whereupon  males  die  and  impregnated  fe- 
males (ff)  enter  fly  larvae.  While  the  fly  matures  and  pupates  the  fe- 
male grows  (/i)  to  reach  full  stature  (a)  and  lav  eggs  (b) .  After  Bo- 
vien.   1937. 


tits  (L.)  (Syn.  Pasxalus  cnrnutns  Fab.).  This  beetle  occupies 
galleries  in  decaying  stumps  and  logs  where  eggs  are  laid  and 
where  larvae  develop  and  pupate.  Leidy  (18.52)  found  90  per- 
cent of  the  adult  beetles  infected  and  Christie  and  Chitwood 
(1931)  estimated  that  each  beetle  usually  harbors  from  .")00 
to  1,000  parasites.  In  the  body  cavity  of  the  insect  one  finds 
larvae  in  all  stages  of  development  from  young,  newly  hatched 
individuals  (Fig.  174  B)  to  those  that  are  fully  grown  (Fig. 
174  A)   but  never  adults. 

Larval  nematodes  of  both  sexes  taken  from  the  body  cavity 
of  a  beetle  have  a  minute  stylet,  a  moderately  large  esophageal 
gland  (presumably  the  dorsal),  and  exceptionally  large  and 
conspicuous  phasmids.  Sex  can  be  distinguished  at  a  rather 
early  stage  partl.y  through  differences  in  the  genital  primordia 
but  more  especially  through  differences  in  the  general  appear- 
ance of  the  body,  females  being  more  opaque  than  males.  Move- 
ment  is  sluggish. 

The  mode  of  exit  from  the  host  has  not  been  determined. 
Once  the  nematodes  have  escaped  neither  males  nor  females 
again  become  parasitic  but  remain  in  the  beetle  galleries 
throughout  the  remainder  of  their  lives.  The  mouth,  anus,  and 
vulva  of  the  female  become  vestigeal.  If  the  vulva  functions 
it  is  only  during  copulation.  Eggs  (Fig.  174  F)  are  retained 
within  the  body  where  they  accumulate  and  hatch  pushing  aside 
the  internal  organs  and  converting  the  female  into  a  brood 
sac   (Fig.  174  C-E). 

C.  passali  enters  its  host  as  a  very  young  larva  but  it  is  not 
known  how  this  is  accomplished.  Larvae  of  all  sizes  may  be 
found  in  old  beetles  at  any  time  of  the  year  when  the  insects 
can  be  collected.  The  incidence  of  infection  seems  to  be  very 
much  lower  in  larval  beetles  and  pupae  than  in  adults.  These 
circumstances,  together  with  the  exceedingly  large  number  of 
parasites  usually  harbored  by  a  beetle,  caused  Christie  and 
Chitwood  (1931)  to  suggest  that  the  larval  nematodes  enter 
per  0.1,  possibly  the  gravid  female  and  her  entire  progeny  being 
swallowed. 


261 


Heterotylenchus  aberrans  Bovien,  1937,  is  a  body  eavity 
parasite  of  the  onion  fly,  Hylemya  antiqiia  (Moig.),  and  its 
life  history  was  studied  by  Bovien  (1937)  at  Lyngby,  Den- 
mark. Tlie  onion  fly  hibernates  in  the  pupal  stage  and  emerges 
in  May  to  lay  eggs  on  onion  plants  or  in  nearby  cracks  in  the 
soil.  The  young  fly  larvae  move  down  the  plant  usually  inside 
the  sheath  and  finally  burrow  into  the  bulb.  Pupation  takes 
place  in  the  soil  or  occasionally  in  the  bulb.  There  are  two  or 
perhaps,  occasionally,  three  broods  a  year  with  considerable 
overlapping. 

In  the  body  cavity  of  infected  flies  one  finds  from  one  to 
four  large,  adult  females  of  B.  aberrans  (Fig.  172  N)  and  a 
greater  number  of  smaller,  adult  females  (Fig.  172  O).  The 
larger  individuals  are  females  of  the  gamogenetic  generation 
and  the  smaller  ones  are  females  of  the  parthenogenetic  gener- 
ation. The  reproductive  organs  of  a  gamogenetic  female,  as 
compared   with   these   structures   in   most   allantoneraatids,   are 


exceptionally  small.  Much  of  the  space  within  the  body  is 
occupied  by  the  intestine  which,  according  to  Bovien,  is  with- 
out a  lumen.  A  small  stylet  is  present  and  the  three  esophageal 
glands,  empty  and  reduced  in  size,  are  grouped  around  the  base 
of  the  esophagus.  Eggs  (Fig.  172  J)  are  deposited  in  the  body 
cavity  of  the  host  where  they  hatch  and  whore  the  larvae  de- 
velop into  parthenogenetic  females. 

The  outstretched  reproductive  organs  of  a  parthenogenetic 
female  are  relatively  much  larger  than  those  of  a  gamogenetic 
female.  The  esophagus  and  esophageal  glands  have  almost  com- 
pletely degenerated  but  a  small  stylet  is  present  and,  according 
to  Bovien,  the  intestine  is  represented  by  a  single  row  of 
large,  binuclear  cells.  Eggs  (Fig.  172  K),  which  are  smaller 
than  those  of  the  preceding  generation,  are  deposited  in  the 
body  cavity  of  the  host  and  from  them  develop  larvae  of  both 
sexes.  These  larvae  remain  in  the  host  until  they  are  ready  to 
undergo  their  final  molt  when  they  penetrate  the  fly's  ovaries. 


Fig.   177.      SPH.VEKULARIINAE 


.  A-D — Sphaerularia  bombi   (A — Fully  grown  lavva;  B-D — Adult  para- 
sitic   females   showing   progressive    stages    in    prolapsus    of    uterus.      For 

fully   grown   adult   parasitic   female,    see   Fig.    115    A,   p.    136).      E-I 

Tripius  gibbosus   (E — Newly  born  larva;  F — Young  but  sexually  mature 
fomale;    Ci — Sexually  mature  male;    H — Adult   parasitic   female' showing 


early  stage  in  prolapsus  of  uterus;  I — Adult  parasitic  female  showing 
late  stage  in  prolapsus  of  uterus.  For  stage  intermediate  between  H 
and  I.  see  Fig.  115  K,  p.  136).  J — "Ti/lerwlius  sulphureus  piceae." 
adult  parasitic  female.     A-I.  after  Leuckart.  1887;  J,  after  Fuchs.  1929 


262 


mi(irnto  to  ami  assiiiiMr  in  llu'  dvidiuls  and  osiaiu'  tl[i(in;;h  tlif 
gonititl  aiH'itiiro. 

Both  miilo  ami  foiiialf  tliis  an'  iiarasiti/.i'd.  liovicn  t'uniul  no 
cvidoiico  that  male  tlios  arc  romliTod  sterile  lint  the  ovaries 
of  iiifeeted  females  fail  to  develop  and  heeause  of  this  the 
nematode  larvae  ean  seareely  he  transferred  to  onion  )dants 
with  the  OKKs  of  their  host.  However,  Rovien  noted  that  in 
feeted  female  tlies  "strelehed  ont  the  ovipositor,  as  if  thev 
wanted  to  lav  eRRS-"  As  in  tlie  life  eyele  of  Ttilt  iirliiiit  ma  ii.i 
ciiiilhK.  infeeted  female  Hies  prol>;ilily  .•leccnnpaiiy  normal  fe 
males  to  the  plaee  where  eRgs  are  laid  Imt  deposit  there,  not 
ogRS,  bat  larval  nematodes.  Hovien  fouiul  no  evidenee  that  the 
genitalia  of  male  tlies  are  invaded  ami  he  eonelnded  tlial  larvae 
■liave  no  way  of  eseaping  from  male  tlies. 

The  free  living  stages  of  the  nematode  arc  passed  in  elose 
assoeiation  with  the  larval  insects,  cither  in  the  onion  i)lant  or 
in  nearby  soil.  The  nematodes  reach  maturity,  copulate  and  the 
males  die.  Impregnated  females  (Fig.  171!  M)  enter  larval 
Hies  presumably  by  penetrating  the  body  wall  though  the  act 
of  penetration  was  not  observed.  The  adult  male  has  a  stylet 
with  basal  swellings  comparable  to  that  of  the  female  but 
somewhat  more  slender.  .\11  tlirei'  esophageal  glands  are  well 
developed  in  the  preparasitic  female  but  inconspicuous  or  lack 
ing  in  the  male.  After  entering  the  host  a  female  develops  into 
the  large,  parasitic  individual  of  the  gamogenetic  generation. 

The  life  cycle  of  //.  abirrans  (Kig.  I7(iK  therefore,  consi.sts 
of  a  parthenogenetic  generation,  passed  entirely  within  the  host, 
alternating  with  a  gamogenetic  generation  that  has  both  para 
sitic  and  free-living  stages.  If  the  parthenogenetic  generation 
was  omitted  the  life  cycle  would  be  es.sentially  the  same  as 
that  of  most  other  members  of  this  family. 

Ferousobi.v  cfRRlEl  (Currie,  IH.'fT)  n.  comb.  [Synonyms: 
Anguilhilina  (Fcrflii.sobia)  tiimifacii  nx  Carrie,  1937;  Anguilhi' 
Una  (Fcrijiixobia)  curriei  (Currie,  l!t37)  Johnston,  103S;  not 
AnpuilluUna  Uimtfacirns  (Cobb,  l!i.'!2)  |. 

Fcrfjusobia  curriri  occurs  in  Australia  where,  in  association 
with  flies  of  the  genus  Fergtisonhm,  it  produces  galls  on  Eiica 
lyptus  trees.  This  association  was  discovered  by  Morgan  (lii;^3) 
and  later  investigated  by  Currie  (1937),  the  following  ae 
count  being  based  on  the  hitter's  observations.  There  are  many 
species  of  Ffrgiisoiiiiia  that  attack  Fiirnliiptiix  trees  in  Aus- 
tralia and,  according  to  Currie,  all  are  probabl.y  associated 
with  a  nematode.  Several  species  of  Eiirah/ptiif:  are  attacked 
and  galls  may  be  formed  on  leaf  buds,  axil  buds,  stem  tips, 
and  flower  buds,  depending  on  the  species  involved.  The  fol 
lowing  account  of  the  life  history  of  FcriivKnbia  curriei  is  based 
on  a  study  of  flower  galls  on  Euciiliiptii.i  tnacrorrhynchia  and 
of  the  associated  fly,  Frrffusoyiiiia  iiirholxonia.  Currie  regards 
the  stages  of  the  nematode  found  in  the  galls  as  true  plant 
para.sites  but  is  inclined  to  regard  the  relationship  with  the  gall 
flies   as   symbiosis    rather    than    parasitism. 

Each  female  fly  harbors  two  gravid  female  nematodes  (Fig. 
172  S).  These  nematodes  deposit  eggs  and  the  resulting  larvae, 
on  reaching  the  proper  stage,  leave  the  body  cavity  and  enter 
the  reproductive  system  of  the  "host."  Adult  flics  emerge 
during  summer  and  females,  after  mating,  lay  eggs  in  young 
flower  buds,  depositing  with  each  egg  from  1  to  ."lO  nematode 
larvae.  The  same  fly  or  different  flics  may  lay  numerous  eggs 
in  a  single  bud  as  many  as  74  eggs  and  227  nematode  larvae 
having  been  found.  The  larval  nematodes  immediately  start  to 
feed  on  the  anther  primordial  cells  that  form  a  ring  around 
the  inner  wall  of  the  bud  cavity  and  under  this  stimulus  the  tis 
sue  proliferates  rapidly  forming  masses  of  large,  thin-walled 
parenchymatous  cells  full  of  mucilagious  cell  sap.  The  fly  eggs 
hatch  in  about  6  weeks  and  by  this  time  masses  of  gall  tissue 
are  already  i)resent  in  the  bud.  On  hatching  a  fly  larva  moves 
in  between  two  of  these  cell  masses  and  tears  out  a  small  crypt 
in  which  to  lie.  The  larval  nematodes  migrate  into  this  crypt 
and  quickly  develop  into  adults  all  of  which  are  parthenogenetic 
females  (Fig.  172  R).  Apparently  the  nematode  passes  through 
several  parthenogenetic  generations  feeding  on  surrounding 
plant  cells  and  in  no  way  injuring  the  insect.  During  its  first 
two  instars  the  fly  larva  feeds  on  the  viscous  cell  sap  which 
oozes  from  surrounding  cells  that  have  been  punctured  by  nem 
atode  stylets.  During  its  last  larval  instar  the  fly  larva  tears 
down  the  walls  of  the  cavity  and  feeds  on  the  ruptured  cells. 
In  autumn  both  male  (Fig.  172  Q)  and  female  nematodes 
appear  that  become  the  adults  of  the  gamogenetic  generation. 
This  "preparasitic"  female  does  not  differ  materially  from  the 
female  of  the  preceding  parthenogenetic  generations  (Fig.  172 
R).  Both  the  adult  male  and  the  adult  "preparasitic"  female 
have  a  stylet  and  three  well  developed  esophageal  glands.  As  in 
most  other  allantonematids,  the  male  does  not  become  parasitic. 
Jnst  before  pupating,  if  the  fly  larva  is  a  female  two  adult,  for 
tilized  female  nematodes  enter  its  body  cavity,  presumably  by 
penetrating  the  body  wall.  Male  flies  are  never  infected,  female 
flies  invariably  so.    Once  in  the  body  cavity  of  the  "host"  the 


feniah'  ui'malodes  iiruceed  in  their  di'VelopmeMl  and,  li\  tlie 
time  the  fly  has  emerged  as  an  adult,  they  :ire  dipositing  eggs. 
The  life  cycle  of  Fcrriusohia  curriri,  therefore,  consists  of 
several  i);irthenogi'nelic  gener.ations  passed  entirely  outsid<'  the 
"host"  alternating  with  a  gamog<Mietic  geru'ration  that  has 
lioth  a  "freeliving"  and  a  "parasitic"  stage.  If  the  parthe 
migenetic  generations  were  omitted  the  life  I'ycle  would  be  es- 
sentially the  sanu'  as  that  of  uu)st  allantonematids. 

In  the  case  of  Frriiiixoliia  curriri  associated  with  FerfjusoiiiiKi 
iiicliDl.ioiiia  in  galls  of  Fiicnlnptiis  macrorrlninchia,  only  two 
gr.ivid  "parasites"  are  normally  found  in  each  female  fly  but 
in  souu'  other  species  of  Frrnu.soiiiua,  usually  those  of  larger 
size,  a  female  fly  may  harbor  a  gre.-iter  number.  As  Currie  sug 
gests,  further  work  may  demonstrate  that  the  nematodes  asso 
ciated  with  difTcrent  species  of  flies  are  themselves  specifically 
distinct. 

Tripius  (Jinnosus  (Lcuckart,  1886)  Chitwood,  1!135  |Syno 
iium,  Atr<icl<i)\<ma  (jibhoxum  (Leuckart,  ]8S())1  is  a  parasite  of 
the  dipterous  insect  Cccidomjiia  pini  (Degeer).  Since  the  in- 
vestigations by  l-enckart  (18S7'),  following  its  original  discov 
cry  in  (jermauy,  this  nematode  has  not  been  reported  else 
where  or  received  further  study.  Each  infected  larva  of  C. 
pini  usually  harbors  a  dozen  or  more,  sometimes  as  many  as 
.'lO,  adult  female  parasites  showing  diffi'rent  degrees  of  de 
velopment. 

Eggs  are  laid  in  the  body  cavity  of  the  host  where  they 
hatch  and  where  larvae  (Fig.  177  E)  accumulate  in  great  num 
bers.  Leuckart  could  never  find  larvae  in  the  alimentary  tract 
or  secure  other  evidence  that  they  pass  out  through  the  anus 
and  he  was  inclined  to  believe  that  they  are  liberated  by  the 
death  and  decomposition  of  the  insect.  The  extrusion  of  larvae 
along  with  the  eggs  of  the  host  when  adult  flies  are  ovipositing 
seems  to  be  an  uninvestigated  possibility. 

The  free  living  period,  passed  in  the  soil,  is  of  short  duration 
and  in  a  few  days  after  leaving  the  host  the  larval  nematodes 
have  developed  to  adult  males  and  females  (Fig.  177  F  &  G). 
Ijcuckart  mentions  one  molt,  apparently  the  last,  but  noted 
that  sometimes  the  cuticle  shed  by  the  male  is  double.  After 
copulation  males  die  and  females  enter  new  hosts.  Leuckart 
did  not  determine  how  the  young  females  reach  the  body  cav 
ity  of  larval  flies  but  suggests  entrance  through  the  mouth  or 
anus  as  a  possibility.  In  the  light  of  our  present  knowledge  of 
this  group,  penetration  directly  through  the  body  wall  seems 
more  proliable.  Fly  larvae  are  su.sceptible  to  infection  from 
the  time  they  hatch  until  they  go  into  the  pupal  stage. 

During  parasitic  development  of  the  female  the  uterus  is 
gradually  everted  through  the  vulva  (Fig.  177  H)  and  develops 
on  the  outside  eventually  forming  an  oval  structure,  somewhat 
exceeding  in  size,  but  always  firmly  attached  to,  the  body 
proper  that,  in  the  meantime,  has  become  greatly  foreshortened. 
The  remainder  of  the  reproductive  system  and  part  of  the 
modified  intestine  occupy  this  prolapsed  uterus   (Fig.  177  I). 

The  effect  on  the  host  is  not  pronounced  and  when  the  nem- 
atodes are  present  in  moderate  numbers  fly  larvae  are  able  to 
pupate  and  become  adults.  However.  Leuckart  concluded  that 
this  parasite  is  not  harmless  and  that  heavily  infected  flies 
frequently   die  in   the  pupal   stage. 

Spn.*.ERUL.VRl.\  BOMBi  Dufour,  1S37.  This  remarkable  nema- 
tode is  a  parasite  of  queen  bumble  bees.  It  has  been  reported 
from  several  species  of  Bomhiis,  each  host  usually  harboring  on(> 
or,  at  the  most,  only  a  few  adult  female  parasites  though 
Leuckart  (1887)  found  32  in  one  bee.  Vespa  rufa  and  V.  viil- 
f/arix  have  also  been  reported  as  hosts.  This  parasite  has  been 
found  in  several  localities  in  Europe  and  North  America  and  is 
apparently  widesjiread. 

S.  bombi,  in  so  far  as  information  is  available,  has  the  typi- 
cal allantonematid  life  cycle.  Eggs  are  laid  and  hatch  in  the 
body  cavity  of  the  host  and  larvae,  after  a  period  of  parasitic 
development,  pass  out  by  way  of  the  anus  and  enter  the  soil. 
Here  the  nematodes  reach  maturity  and  cojiulate  whereupon  the 
males  die  and  the  impregnated  females  enter  their  new  hosts. 
The  free-living  period,  according  to  Leuckart,  is  of  several 
months'    duration. 

Queen  bees  hibernate  in  the  soil  and  Leuckart  found  that 
under  coniferous  trees  where  the  soil  is  moist  and  covered  with 
humus  and  moss  is  a  favored  place.  Leuckart  concluded  that 
the  bees  become  infected  in  autumn  when  they  are  penetrating 
the  soil  preparatory  to  hibernation  and  that  this  explains  why 
only  queens  are  parasitized.  Infected  queens,  due  to  retarded 
development  of  the  ovaries,  are  either  unable  to  produce  eggs 
or  produce  only  a  few  and  both  Schneider  (188."))  and  Leuckart 
were  convinced  that  such  queens  never  found  colonies. 

The  interesting  and  unusual  feature  about  this  nematode  is 
not  its  life  cycle  but  the  morphological  development  of  the 
parasitic  female.  After  entrance  into  the  new  host  the  body 
of  the  young  female  undergoes  little  or  no  increase  in  size. 
Instead  "the  uterus  is  everted  through  the  vulva,  carries  within 


263 


it  tlic  other  reproductive  organs  as  well  as  the  modified  intes- 
tine or  "fat  body,"  and  develops  outside  the  body  proper  (Fig. 
177  BD).  This  prolapsed  uterus  increases  enormously  in  size 
while  the  body  proper  remains  a  relatively  minute,  functionless 
structure  that  may  sometimes  become  detached  (Fig.  11. "i  A,  p. 
13G). 

Other  Species.  In  addition  to  the  species  already  discussed, 
the  number  of  allantonematids  that  have  as  yet  been  named 
and  described  is  not  great  and  for  most  of  these  information 
about  life  cycles,  especially  regarding  free-living  stages,  is 
meager  or  lacking.  A  few  exceptions,  however,  may  be  noted 
briefly. 

Bradynema  rigldnm  (v.  Siebold,  1836)  zur  Strassen,  LS92,  is  a 
parasite  of  the  dung  beetle,  Aphodiiis  fimetarius  (L.)  and 
Bradynema  strasseni  Wiilker,  1921,  is  a  parasite  of  the  wood- 
boring  beetle,  Spondylis  biiprcsloidcs  (L.).  These  two  nema 
todes  have  been  rather  extensively  investigated  in  Europe  (zur 
Strassen,  1892;  Wulker,  1923)  though  the  free-living  stages  of 
B.  rigldnm  are  still  imperfectly  known.  Both  have  the  typical 
allentonematid  life  cycle,  larvae  passing  out  of  the  hosts  by 
way  of  the  anus. 

Souardula  benifftia  Cobb,  1921,  is  a  parasite  of  the  cucumber 
beetle,  Diahrotica  vittata  (Fab.)  and,  less  commonly,  of  the 
related  beetles,  D.  trivittata  (Mann)  and  D.  di(odcciinpuncta1a 
(Fab.).  This  nematode  has  the  typical  allantoiiematid  life  cy- 
cle, larvae  passing  out  with  the  eggs  of  the  host  (Fig.  178). 
Beetles  of  both  sexes  are  infected  and  the  fate  of  larvae  that 
find  themselves  in  male  beetles  is  not  known.  Cobb  (1928)  was 
of  the  opinion  that  these  larvae  may  be  transferred  to  female 
beetles  during  copulation.  He  found  considerable  numbers  of 
larvae  in  the  proximal  end  of  the  male  genitalia  but  was  un- 
able to  demonstrate  experimentally  that  such  larvae  are  ac- 
tually transferred  to  female  beetles. 

In  the  genus  Aphclenchuliis  the  adult,  parasitic  female  is 
usually  characterized  by  being  curved  dorsad  with  the  vulva 
on  the  outside  of  the  curve.  A.  diplogaster  (Linstow,  1890), 
Filipjev,  1934  (Fig.  172  P)  is  a  parasite  of  the  bark  beetle, 
Ips  typographus  (L.)  and  A.  tomici  Bovien,  1937,  is  a  parasite 
of  the  bark  beetle,  Pityogenes  bidenlalus  (Hbst.)  (Syn.  Tomi- 
ciis  bidens  (F.)).  These  two  nematodes  are  very  closely  related 
and  both  have  the  typical  allantonematid  life  cycle,  larvae  pass- 
ing out  of  the  host  by  way  of  the  anus  (Fuchs,  1915;  Bovien, 
1937)  to  undergo  free-living  development  in  the  frass  of  the 
beetle  galleries. 

■'  Tylenchus"  aptini  Sharga,  1932,  was  found  in  Scotland, 
where  it  is  a  parasite  of  the  thrips,  Aptinothrips  rufiis  (Gme- 
lin).  Eggs  of  this  parasite  are  deposited  in  the  body  cavity 
of  the  host  and  larvae  leave  by  way  of  the  anus.  Males  remain 
in  the  host  until  bursa,  spicules  and  gubernaculum  arc  formed 
and  Sharga  (1932),  finding  no  evidence  that  males  enter  the 
gut  or  pass  out  through  the  anus,  suggests  that  copulation 
takes  place  before  the  parasites  leave  the  host.  Furtliermore, 
Sharga  states  that  "after  several  ecdyses  the  mature  female 
stage  is  reached"  and  his  discussion  and  drawings  seem  to  in- 
dicate that  one  or  more  of  these  ecdyses  take  place  after  the 
female  has  passed  through  the  free-living  stage  and  entered  a 
new  host.  If  copulation  takes  place  before  this  parasite  leaves 
the  first  host  and  the  female  molts  after  entering  the  second 
host,  the  life  cycle  is,  indeed,  a  departure  from  that  known  for 
any   other  allantonematid. 

Parasitylenchtis  dif:par  (Fuchs,  191:1)  Mieoletzky,  1922,  sub- 
species, typographi  (Fuchs,  1915)  is  a  parasite  "of  the  bark 
beetle,  Ips  1  ypographiis  (L.).  In  general  this  nematode  has  the 
typical  allantonematid  life  cycle.  The  adult,  parasitic  female 
gives  birth  to  larvae,  large  numbers  of  which  accumulate  in 
the  body  cavity  of  the  host  to  eventually  enter  the  gut  and 
pass  out  through  the  anus.  In  one  respect,  however,  the  life 
cycle  differs  from  that  of  most  allantonematids.  After  com 
pleting  free-living  development  young  adults  of  both  sexes  enter 
the  new  host.  One  finds  in  the  body  cavity  of  infected  beetles 
200  to  300  adult  parasitic  females  (Fig.  i72  U)  and  an  even 
greater  number  of  adult  jiarasitic  males   (Fig.  172  T). 

Fuchs  (1915)  did  not  observe  copulation  or  determine 
whether  it  takes  place  before  or  after  entering  the  new  host. 
However,  he  was  able  to  rear  to  maturity  larvae  taken  from 
the  rectum  of  a  beetle,  the  adult  stage  being  reached  in  7  to 
10  days.  The  experimentally  reared  females  did  not  lay  eggs 
and  it  seems  probable  that  eggs  are  not  laid  until  after  en- 
trance into  a  new  host.  If  this  is  true  we  have,  not  a  free- 
living  generation,  as  Fuehs  called  it,  but  a  free-living  stage. 

Ostensibly,  Tripiii.\  gibbositf:  and  Sphaenilaria  hombi  are  the 
only  members  of  the  Sphaerulariinae  that  have  as  yet  been  re- 
ported. It  may  be  noted,  however,  that  Fuchs  (1929)  has  de- 
scribed two  very  unusual  nematodes  from  bark  beetles,  viz., 
"Tylenchus  sulplnirriis  picear"  and  "Tylenchus  siilphiireiis 
pini."  Fuchs  maintained  that  in  the  case  of  these  two  nema- 
todes the  gravid   female  is  not  a  prolapsed  uterus  basing  his 


contention,  in  part,  on  a  failure  to  find  any  vestige  of  the  body 
proper  or  transitional  stages  showing  the  uterus  in  the  process 
of  prolapsus.  But  in  (he  case  of  Sphaenilaria  bombi,  as  Leuck- 
art  points  out,  the  body  proper  is  sometimes  detached  and  one 
wonders  if  Fuehs'  material  included  a  sufficiently  complete 
series  of  developmental  stages.  If  the  gravid  female  of  ' '  Ty- 
lenchus siiiphnreiis  picear"  (Fig.  177  J)  is  not  a  prolapsed 
uterus  its  resemblance  to  the  gravid  female  of  Sphaerularia 
hiinibi  is,  to  say  the  least,  very  renuirkable. 


Fig.   178.      EOWARDVLA    BESHI.\S 

Showing  relative  size  of  beetle.  Diabrotvja  vittattt,  and  of  its  par.i- 
?'ites  (line  XY  indicates  actual  length  of  beetle)  :  also  egg  of  beetle  and 
larval  nematodes  deposited  with  it.      After  Cobb,    1921. 


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2Go 


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1926. — t)ber  geschleehtsreife  Nematoden  im  Regen- 
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1-6. 


266 


CHAPTER  VI 

LIFE  HISTORY  (ZOOPARASITICA) 

II     I'AKASI'I'KS  OK  VKirrKI'.KATKS 

ASA  C.  CHANDLER.  Rico  Institute,  Houston,  Texas;  J.  E.  ALICATA,  University  of  Hawaii, 
Honolulu,  T.  H.;  and  M.  B.  CHITWOOD.  Babylon,  N.  Y. 


In:roductIon 

The  life  cycles  of  tlie  nematodes  piiriisitic  in  veitelii:itis 
differ  in  no  essential  from  those  of  free  livinj;  nematodes,  hnt 
are  subject  to  a  numl)er  of  modifications  which  enable  the 
parasites  to  train  access  to  new  hosts  with  more  facility  and 
greater  certainty.  With  a  few  exceptions  these  nematodes 
have  tive  stages  of  development  separated  by  four  moults  as 
do  most  free  living  nematodes,  but  in  a  few  forms  (e.g..  Con 
tracacciim  and  Trivhiiullo)  the  number  of  molts  is  said  to  be 
increased,  and  in  some  forms  one  or  more  of  them  is  sujipressed 
to  the  extent  of  being  passed  through  rapidly  in  the  egg, 
or   in    hatched   larvae    with    no    intervening   period    of    growth. 

The  outstanding  feature  in  the  life  cycle  of  parasitic  nema 
todes  is  a  cessation  of  develoi)ment  of  the  young  worms  aftei 
reaching  an  infective  stage,  while  they  await  an  opjiortunity 
to  gain  access  to  a  new  delinitive  host.  In  most  eases  the  or 
ganisms  pass  through  this  jieriod  of  w.'iiting  outside  the  body 
of  the  original  host,  either  (1)  as  embryos  inside  the  egg 
shells  (oxyurjds,  ascaridids,  trichurids)  ;  (2)  as  free  living  but 
nonfeeding  third  stage  larvae,  often  enclosed  in  the  .shed 
cuticle  of  stage  two  (Stroii(iijlui<l< s,  many  strong.vlins)  ;  or 
(3)  as  third  stage  larvae,  usually  encysted,  in  the  bod.y  of  an 
intermediate  host,  which  in  some  cases  is  obligatory  (e.g., 
spiruroids,  eamallanins,  some  metastrongylids)  but  in  other 
cases  is  optional  (e.g.,  CapUlaria  aiiiiiilain,  Si/iinamiix  Iraclira). 
In  many  cases  such  larvae  are  capable  of  re-encystment,  some- 
times over  and  over  again,  in  other  hosts — transport  hosts — 
in  which  development  to  maturity  does  not  occur.  In  a  few 
cases  such  secondary  intermediate  hosts  have  become  neces- 
sary parts  of  the  life  cycle  (e.g.,  Gnalhostoma  spinigeriim). 
In  the  filariae  and  a  few  other  nematodes  (e.g.,  Hahronima) 
the  infective  larvae  do  not  become  encysted,  and  habitually 
emerge  through  a  break  in  the  labium  of  the  vector  as  a  re 
suit  of  their  own  activities.  A  striking  exception  to  the  usual 
waiting  period  outside  the  body  of  the  host  occurs  in  the  case 
of  TrichiniUa  spiralis,  which  passes  its  waiting  period  en 
cysted  in  the  flesh  of  the  parental  host. 

In  considering  the  life  cycles  of  parasitic  nematodes  from 
an  evolutionary  standpoint  it  is  necessary  to  consider  possible 
ways  in  which  the  nematodes  may  have  developed  into  para 
sites    of    vertebrates.      One    method    was    presumably    the    re 
suit  of  ingestion  by  the  host,  followed  by  adaptation  to  the 
environment     encountered     inside     the    alimentary     canal.       It 
seems  probable  that  the  Oxyuridae,  for  instance,  became  para 
sitic   in   this   manner.      Such   nematodes   might   lie   expected   to 
have    the    simplest    possible    type    of    life    cycle,    reproducing 
generation  after  generation  in  the  lumen  of  some  part   of  the 
alimentary   canal,   with    enough   eggs    or   larvae   escaping   witli 
the  feces  to  allow  for  spread  to  other  hosts  through  the  me 
dium   of   contaminated   food   or   water.      It   seems    remarkable 
that  only  a  single  instance   (Probst mayria  viripara)    is  known 
of  a  parasite  which  has  unequivocally  adapted   itself  to   this 
type   of   life.      The   nearest   approach,   with   the   exception    of 
Probstmayria,    is   the    facultative   parasitism    of    a    number    of 
species   whose   congeners   are   saprozoic   free-living   forms,   e.g., 
a  species  of  Longibucca  in  the  stomach  of  a  snake   (Chitwood, 
1933),  and  another  species  of  Longibucca  in  the  stomach  and 
intestines   of   a   bat    (Mcintosh   and   Chitwood,   1934)  ;    Diplo 
scapter  coronata  in   ahydrochloric  human   stomachs    (Chandler. 
1!>38)  ;    and    Ccphalobiis    parasiticus    in    the    stomachs    and    in 
testines  of  monkeys   (Sandgronnd,  1'.I39).     In  addition  to  these 
cases,   it    is   claimed    by   a    number   of   writers    (Koch,    1925; 
Penso,    193:;)     that    Evlcrobius    vrntiicufaris.    Passalunis    atn- 
biguus   and    other    oxyurids   are    callable    of    reproducing,    gen 
eration  after  generation,  in  the  lumen  aiul   walls  of  the  intcs 
tine.     This  is  denied  by  others    (Zowadowsky  and  Schalimov, 
1929;    Lentze,    193.5)    because    of    the    demonstrated    need    of 
oxygen   by   the   embryos   before   they   can   complete   their    de 
velopment.      Even    if   the   larvae   can    occasionally   develop   to 
maturity   in   the   gut   walls,   such   an    occurrence   can    certainly 
be  considered  the  exception  rather  than  the  rule.     One  other  in 
stance    of    repeated    generations    in    a    single    host    has    been 
claimed  for  Strongyluidcs  stcrcoralis   (Nishigori,  1928;    Faust, 
1931)    but   this   is   a   case   of   short  circuited   rather   than    con 
tinuous  development,  and   occurs  only   under  exceptional  con 
ditions.      The    offspring    of    wonns    in    the    intestine    do    not 
grow  to  maturity  directly  in  the  intestinal  lumen,  but  migrate 


through    the    body    as    they    wouhl    if    Ihcy    h.-iii    infected    from 
outside. 

With  the  few  exceptions  mentioned  above,  the  simplest  type 
of  life  cycle  in  the  case  of  obligatory  parasites  is  that  ex- 
hibited by  most  species  of  oxyurids,  in  which  the  eggs  fail 
to  develoi)  beyond  a  certain  point  (morula  stage  in  some, 
"tadpole"  in  others)  until  exposure  to  oxygen  outside  the 
body  of  the  host,  followed  by  reentrance  of  the  embryonated 
eggs  or  hatched  larvae  into  the  same  or  another  host  with 
food  or  water  contaminated  by  them.  In  many  cases,  jiossibly 
in  all.  this  simple  cycle  is  modified  further  by  a  stage  in 
with  the  larvae  attach  themselves  to  the  mucous  membnuie, 
liury  their  heads  in  it,  or  actually  burrow  into  the  walls  of 
the  gut  before  they  take  up  their  residence  in  the  lumen  as 
adults. 

Few  parasites  other  than  the  Oxyuroidea  have  as  simjile  a 
life  cycle  as  that  described  in  the  last  paragraph.  Most  of 
them  have  an  instinct  for  burrowing  at  some  time  during  the 
course  of  their  development  and  exercise  it  either  (1)  by  bur- 
rowing through  the  skin  and  going  on  a  tour  of  the  body 
via  the  circulatory  system,  lungs  and  throat  before  reaching 
the  intestine;  (2)  by  burrowing  into  the  mucous  membranes 
of  the  alimentary  canal,  either  being  content  to  live  buried 
in  the  gut  wall  for  a  few  days,  or  entering  the  circulatory 
system  and  going  on  a  tour  of  the  body  similar  to  that  of  the 
skin  penetrators  or,  in  some  eases,  burrowing  directly  through 
into  the  body  cavity  or  through  mesenteries,  parenteral  tis 
sues,  etc.;  or  (3)  by  burrowing  into  the  body  cavity  or  tissues 
of  an  intermediate  host,  either  through  the  surface  or  through 
the  walls  of  the  gut  after  being  ingested. 

Two  possible  origins  of  this  burrowing  habit  suggest  them- 
selves. One  possible  origin  is  as  a  useful  instinct  on  the  part 
of  gut  parasites  to  serve  either  one  or  both  of  two  purposes, 
(1)  to  protect  the  young  worms  from  being  swept  out  of  the 
intestine  with  the  feces,  and  (2)  to  provide  a  better  type  of 
nourishment  for  the  period  of  rapid  growth  and  development. 
There  can  be  little  doubt  but  that  the  burying  of  the  head  of 
fourth-stage  larvae  of  Dermatoxys  vcligera  (Wetzel,  1931) 
and  the  use  of  the  "corpus"  of  the  esophagus  of  Oxyuris  eqiii 
as  a  mouth  capsule  (Wetzel,  1930)  are  steps  in  this  direction. 
One  could  then  visualize  as  further  developments  complete 
burrowing  into  the  gut  wall,  penetration  into  the  circulatory 
system,  and  the  circuit  through  the  body  that  would  neces- 
sarily be  entailed. 

Tlie  alternative  explanation  is  that  the  worms  which  mi- 
grate through  the  body  originally  became  vertebrate  parasites 
by  burrowing  through  the  skin.  An  initial  step  in  this  direc- 
tion can  be  observed  today  in  the  occasional  invasion  of  the 
skin  of  dogs  and  sometimes  of  other  animals  by  Ehabditis 
strongyloides,  the  adults  of  which  live  in  soiled  straw  bed 
ding.  Successful  development  of  adult  parasitism  by  this 
method  would  necessitate  an  ultimate  location  in  the  body 
whence  the  eggs  or  embryos  could  escape  in  order  to  reach 
new  hosts.  This  condition  would  be  fulfilled  in  the  case  of 
those  parasites  which,  after  penetration  of  the  skin,  reach 
the  circulatory  system  and  eventually  arrive  in  the  lungs, 
where,  still  imbued  with  an  instinct  for  burrowing,  they 
would  escape  into  the  air  spaces.  Here  they  could  successfully 
reach  maturity  and  reproduce  (e.g.,  Metastrongylidae)  or 
they  could  be  carried  passively,  via  trachea  and  throat,  to  the 
alimentary  canal.  Successful  parasitism  would,  of  course,  be 
dependent  upon  loss  of  the  burrowing  instinct  after  the  third 
moult,  which  actually  occurs. 

The  temporary  burrowing  into  the  intestinal  mucosa  of  the 
larvae  of  such  worms  as  Ascaridia,  Hacmonchus  and  Oesopha- 
gostomum  might,  then,  be  construed  either  as  a  step  in  the 
direction  of  a  more  extended  migration,  as  practiced  by  re- 
lated worms,  or  as  a  step  in  the  direction  of  the  simple 
oxyurid  type  of  life  cycle,  with  abandonment  of  a  primitive 
but  no  longer  necessary  migration  from  skin  to  intestine.  In 
those  species  which  usually  perform  the  entire  migration,  the 
failure  of  some  individuals  to  do  so  (e.g.,  Ascaris.  hookworms) 
could  be  either  atavistic  or  progressive.  The  fact  that  the 
curtailed  migration  is  more  likely  to  occur  in  the  normal  than 
in  abnormal  hosts  is  of  little  help  in  the  matter,  for  it  could 
be  argued  either  that  the  reason  for  the  failure  of  migra- 
tion in  normal  hosts  is  due  to  less  restlessness  in  such  hosts 
and  a  consequent  slipping  back  to  ancestral  ways,  or  that  it  is 


267 


duo  to  more  perfect  adaptatio.i  and  therefore  more  advanced 
evolution. 

It  is,  as  a  matter  of  fact,  probable  that  the  migration  is 
primitive  for  some  worms  and  secondarily  acquired  for  others. 
Worms  which  may  be  assumed  normally  to  develop  directly  in 
the  intestine  are  at  least  occasionally  able  to  reach  the  in 
testine  even  if  injected  under  the  skin.  This  was  demon- 
strated by  Harwood  (1930)  in  tlie  case  Cosiiioccrcoidcs  diikac, 
for  although  he  found  the  larvae  of  this  worm  to  be  incapable 
of  skin  penetration,  he  succeeded  in  recovering  a  few  worms 
from  lungs  and  intestine  after  subcutaneous  injection.  There 
is  some  reason  to  believe  that  the  Strongyloididae  and  Rhab- 
diasidae,  the  latter  of  which  never  establish  themselves  in  the 
intestine  at  all,  may  be  primitively  skin  penetrators,  whereas 
it  is  very  unlikely  that  the  ascarids  are.  Whether  parenteral 
migration  is  primitive  or  secondary  among  the  Strongylina  is 
not  so  easy  to  guess. 

An  interesting  derivative  of  the  migratory  type  of  life  cycle 
is  the  course  of  develoi)ment  of  TricliinclUi.  Th?  unique  life 
cycle  of  this  worm  has  apparently  resulted  from  a  precocious 
development  and  hatching  of  the  eggs  in  the  uterus  of  the 
mother,  accompanied  by  early  acquisition  of  the  burrowing 
instinct,  the  result  being  the  invasion  of  the  parental  host  in- 
stead of  a  new  host.  The  Strongylokles  life  cycle  is  another 
derivative  in  which  the  parasitic  worms  have  become  partheno- 
genetic  and  a  free-living  sexually-reproducing  generation  may 
be  interpolated  in  the  course  of  a  cycle  of  development  whicli 
is  otherwise  similar  to  that  of  hookworms. 

In  the  case  of  nematodes  whose  larvae  hatch  outside  the 
body  and  have  an  instinct  for  burrowing  it  is  easy  to  conceive 
of  the  accidental  or,  in  time,  routine  invasion  of  intermediate 
or  transport  hosts.  This  might  come  about  by  invasion  from 
the  outside  (e.g.,  Protostrongylinae),  or  by  penetration  through 
the  gut  wall  after  being  swallowed  (e.g.,  Anisakinae).  Such 
penetration  of  hosts  other  than  the  definitive  one,  and  subse- 
quent encapsulation  in  parenteral  tissues,  is  an  extremely  com- 
mon phenomenon,  and  occurs  in  all  the  major  groups  of  para- 
sitic nematodes.  In  some  instances  it  is  a  more  or  less  ex- 
ceptional phenomenon,  e.g.,  the  encystment  of  Tojcocuia  larvae 
in  mice  (Fiilleborn,  IH21)  ;  in  others  it  constitutes  an  im- 
portant but  not  absolutely  essential  factor  in  the  epidemiology, 
e.g.,  Syngamun  trachea;  and  in  still  others  it  has  become  ob- 
ligatory, the  invaded  hosts  then  becoming  true  intermediate 
hosts   rather   than   transport    hosts,   e.g.,   spiruroids. 

The  frequent  encapsulation  of  some  nematodes  in  transport 
hosts  and  its  non -occurrence  in  others  is  i)robably  dependent 
upon  the  behavior  of  the  larvae  in  the  hosts  concerned.  Larvae 
that  keep  on  the  move  do  not  become  encapsulated.  It  is 
for  this  reason  that  most  spiruroids  are  encapsulated,  whereas 
Habioncma  and  filariae  are  not.  No  encapsulation  of  hook- 
worm or  Ascaris  liimbricoides  larvae  occurs  when  these  enter 
rodents  since  the  larvae  complete  the  migration  to  the  intes- 
tine, and  are  then  evacuated  because  the  environment  is  un- 
suitable for  growth  to  maturity.  On  the  other  hand,  since 
Toxocara  is  encapsulated  in  mice,  it  must  be  assumed  that  this 
worm  loses  its  burrowing  instinct  before  it  has  regained  the 
alimentary  canal,  and  then  becomes  quiet  enough  to  be  en- 
capsulated by  the  host. 

In  the  Metastrongylidae  alone  all  gradations  can  be  found 
from  more  or  less  accidental  and  unnecessary  penetration  of 
an  intermediate  host  (e.g.,  Dictyocaulus  filaria)  to  obligatory 
development  in  specific  invertebrates  (e.g.,  Aleta.stroiipyhiK. 
Protostrongylus  and  Muellerius).  Similar  obligatory  depend- 
ence upon  specific  intermediate  hosts  has  become  the  lot  of 
the  entire  group  of  spiruroids,  the  C'amallanina,  the  Diocto- 
phymatina,  and  apparently  at  least  one  ascaridoid,  SiibiiUira 
hrumpti  (Alieata,  1939). 

A  clue  to  the  origin  of  the  iilarioid  type  of  life  cycle,  in 
which  the  microfilariae  are  withdrawn  from  blood  or  skin 
by  blood  sucking  arthropods,  and  are  eventually  given  an 
opportunity  for  reinvasion  of  the  skin  by  these  same  arthro- 
pods, after  development  within  them,  is  afforded  by  the 
habronemas  (see  p.  286).  In  these  the  larvae  show  a  definite 
step  towards  the  filarial  type  in  that  they  fail  to  become 
encapsulated  in  the  intermediate  host,  there  to  await  passive 
transfer  to  the  definite  host,  but  instead  remain  free  and 
active,  and  leave  the  intermediate  host,  under  suitable  con- 
ditions, of  their  own  volition.  The  further  steps  to  a  filarial 
life  cycle  are  merely  (1)  substitution  of  a  parenteral  for  a 
gastrointestinal  habitat  for  the  adult  worms,  and  consequent 
liberation  of  the  embryos  into  the  blood  or  tissues  whence 
blood-sucking  insects  can  withdraw  them;  and  (2)  successful 
penetration  of  the  skin  by  the  infective  larvae  to  reach  their 
deiinitive  location. 

It  will  be  seen  that  in  no  case  is  there  reason  to  believe 
that  intermediate  hosts  of  nematodes  are  ancestral  hosts,  as  is 
the  case  with  intermediate  hosts  of  flukes. 

The  same  modifications  in  life  cycle  have  a  tendency  to  re- 
appear  over   and   over   again   in   the   various   groups   of   para- 


sitic nematodes,  and  sometimes  several  of  the  principal  types 
may  occur  within  a  group  of  closely  related  genera.  In  the 
genus  Habroncma,  for  instance,  the  species  parasitic  in  the 
stomachs  of  horses  are  deposited  by  the  intermediate  hosts 
on  the  lips  or  skin  and  they  reach  their  destination  by  way 
of  the  mouth,  either  by  direct  migration  into  it  or  by  being 
licked  from  the  skin.  In  the  habronemas  parasitic  in  insec- 
tivorous birds,  on  the  other  hand,  there  can  be  little  doubt 
but  that  they  reach  their  destination  in  the  orthodox  spiruroid 
fashion,  by  the  intermediate  hosts  harboring  them  being 
swallowed.  In  the  species  found  in  raptorial  birds,  however, 
a  secondary  transport  host  is  usually  if  not  always  involved. 
Because  of  this  lack  of  uniformity  within  even  nearly  related 
forms,  and  because  of  the  endless  number  of  minor  varia- 
tions by  which  one  type  of  life  cycle  grades  into  another, 
we  believe  that  a  clearer  picture  of  the  life  cycles  of  parasitic 
nematodes  can  be  given  by  discussing  the  outstanding  types 
and  principal  variations  in  each  natural  group,  than  by  dis- 
cussing types  of  life  cycles  irrespective  of  the  natural  groups 
in  which  they  occur.  By  way  of  summary,  however,  we  sug- 
gest the  following  classification  of  the  principal  life  cycle 
types : 

A.  Monoxenous  or  Direct    (no   intermediate  host   required). 

1.  Continuous  reproduction  within  host,  generation  after 
generation ;  various  stages  of  worms  occasionally  carried 
out  of  bod.v  and  infect  other  hosts  through  contaminated 
food.  Ex.,  Probstmayiia ;  facultative  rhabditoid  para- 
sites. 

2.  Discontinuous,  eggs  or  embryos  escaping  habitat  of 
adults,  and  usuall.v  leaving  parental  host. 

(1)  Without   free-living  phase. 

a.  Simple.  Eggs  leave  body  of  host,  usually  l)Ccoming 
embryonated  outside,  reenter  via  the  mouth  usually 
before  hatching,  and  grow  to  maturity  in  the  ali- 
mentary canal.     Ex.,  Enterobius,  Trichiirin. 

h.  With  temporary  burrowing  into  mucosa.  Ex., 
A  scar  id  ia. 

c.  With  parenteral  migration  via  blood  system  to  heart 
and  lungs,  returning  to  intestine  via  throat.  Ex., 
Ascaris    laiiibricoidcs. 

d.  With  parenteral  migration  via  blood  system  to 
definitive  locations  elsewhere  in  body.  Ex.,  Capil- 
laria   hepatica. 

(2)  With  free-living  phase.  Eggs  usually  hatch  out- 
side body  of  host  into  first-stage  larvae  which  grow  to 
third  (infective)  stage  while  free,  but  in  some  forms 
may  develop  to  third  stage  before  hatching. 

a.  With  skin  ])enctration  and  migration  to  intestinal 
tract  via  heart  and  lungs. 

(a)  Free-living   forms   larvae  only.   Ex.,  Necator. 

(b)  With  possilile  development  of  an  alternative 
generation  of  free-living  adult  males  and  fe- 
males.    Ex.,  Strongyloides. 

b.  Without    skin     penetration;     infection     by     mouth. 

(a)  With  temporary  burrowing  of  larvae  into 
mucosa.     Ex.,  Ilaeinonchiis. 

(b)  With  more  extended  burrowing  and  forma- 
tion of  nodules  in  intestinal  wall.  Ex., 
Oesophagoslomii  III. 

(c)  Migration  through  intestinal  wall  and  for- 
mation of  nodules  in  parenteral  locations. 
Ex.,  Strongyhis. 

c.  With  optional  use  of  transport  host.  Infective 
larvae  when  ingested  by  various  invertebrates  be- 
come enc.vsted  and  reach  final  host  when  trans- 
port host   is   eaten.     Ex.,  Syngamus ;   Dictyocaulus. 

B.  Heteroxenous    or    Indirect    (development    occurs    only   in 

an  intermediate  host) 

1.  Passive  Indirect.  Embryonated  eggs  or  larvae  enter 
an  intermediate  host  and  become  infective  upon  reach- 
ing third  stage.  Pinal  host  reached  when  intermediate 
host  is  eaten.  Migration  in  definitive  host,  if  any,  via 
tissues  or  natural  passages,  not  via  blood  system. 

(1)  Eggs  cr  larvae  leave  host  with  feces. 

a.  Embryonated  eggs  or  larvae  are  swallowed  by 
intermediate  host.     Ex.,  MetasiroiigyUis,  spiruroids. 

b.  Larvae  superficially  penetrate  foot  of  molluscs.  Ex., 
Protostrongylinae. 

(2)  Larvae  leave  host  through  skin  or  by  other  paren- 
teral routes.  Develop  after  being  swallowed  by  in 
termediate   host.      Ex.,   Dracunculoidea. 

2.  Active  Indirect.  Larvae  actively  leave  intermediate  host 
to  reach  skin  of  definitive  host. 

(1)  Larvae  reach  intermediate  host  by  eggs  being  eaten. 
Ex.,  Habroncma. 

(2)  Larvae  reach  intermediate  host  by  being  sucked 
from  blood  or  skin.     Ex.,  Filariae. 

3.  Double  Indirect.  Larvae  utilize  two  or  more  succes- 
sive intermediate  hosts. 


268 


(1)  Swoiul  niiil  siilisf(nicnl  iiiti'iiiu'ilinli'  liosis  <i|ilii)ii:il, 
I'ossililo  Yai'iatioii  in  nmiiy  siilnlivisions  aliovo. 

(2)  Two  snccfssivo  inlormodiali'  hosts  (ililiRatorv :  deli- 
iiitivi'  host  roHchoil  t)V  ciitiiiK  <•'  second  inti'inu"- 
diiito  host.     Kx.,  (liiutlio.itoma. 


RHABDITOIDEA 

As  noted  on  p.  2li7,  thi'io  iiro  a  consideialilo  nnnilur  iif  mnui 
todes  IirlonKini;  fo  this  pi-oiip  whieh  are  faenltative  parasites 
of  verteliiates,  but  only  the  Klialidiasidae  and  StioiiKyloididae 
have  heeonie  obliflator;/  parasites  of  vertelrrates.  In  Imtli  oC 
these  families  there  is  a  tendeney  for  an  alternation  between 
f  ree  liviiiB  and  parasitic  Renerations,  and  in  both,  e.xeept  in 
Olio  species,  I'ara.i't ronni/loitlts  itiiichesi,  there  is  a  sn|)pre.ssion 
of  males  in  the  parasitic  H''">''''''io"-  The  larvae  of  most  sjie 
cies  pellet r;ite  the  skin  or  mucous  membranes  and  iiiinrate  to 
the  luntis  before  trrowiiin  to  maturity.  The  Rliabdiasidae  nia 
ture  in  the  luiiKs.  and  this  is  probably  the  mure  ]iiimitive 
condition;  the  StrouKyb'ididae  only  exceptionally  mature  in 
the  luiiKs,  ordinarily  returiiiiiK  to  the  intestine  before  ma- 
turinj;. 

Stronuvi,oidii).\k 

The  life  cycle  of  Stronmiloidis  stercoral iv  of  man.  the  main 
features  of  which  were  first  elucidated  by  Grassi  (1S78)  and 
I>euckart  (1S.S:;),  has  been  studied  by  a  large  number  of 
proniiiient  parasitologists,  yet  even  today  there  is  no  unanimi 
ty  of  opinion  about  some  jihases  of  it.  Grassi  observed  di 
roct  development  into  filariform*  larvae;  Leuckait  discov 
ered  that  an  alternation  of  gener.-itioiis  might  occur;  van 
Dunne  (ISH):;)  first  demonstrated  that  infection  resulted  from 
skin  iH-netration ;  and  Looss  (liH)"))  showed  that  the  migrntimi 
of  the  larvae  after  penetration  paralleled  that  of  Ancylo.iloiixi. 
Important  additional  details  or  interpretations  w^itli  resjiect 
to  this  or  related  species  have  been  added  by  Leiclitensteni 
(lS9i>.  190.-)),  Fiilleborn  (1!>14),  Sandground  (lltiii).  Xislii- 
gori  (1!»2S),  Kreis  (1>»32),  Faust  dilHS"),  Liicker  (l!t.S4), 
Graham  (1!).'?6-I03i1),  Beach.  T.  1).,  n!l3.5  193(i)  and  Chitwood 
and  Graham    (liHO). 

The  parasitic  females  live  more  or  less  deeply  imbedded  in 
the  mucous  membrane  of  the  small  intestine  where  they  pro 
duce  embryonated  eggs  which  in  this  species  hatch  promptly 
within  the  host.  The  embryos  are  rhabditiform,  and  resemble 
those  of  hookworms  except  for  the  very  sliort  stoma.  They  nor 
mally  pass  out  of  the  body  with  the  feces  of  the  host,  and 
then  begin  to  feed  and  grow.  From  this  point  on  they  may 
follow  either  o  le  of  two  courses  of  development,  known  re 
spectively  as  the  direct  or  liomogonie  type,  and  the  indirect 
or  heterogoiiic   type. 

In  the  homogonic  type  of  development  the  rhabditiform 
larvae  grow  and  transform  into  filariform  larvae,  sometimes 
in  24  hours  or  less.  Looss  reported  two  molts  in  the  course  of 
the  develoiunent  of  rhabditiform  to  filariform  larvae  in  the 
human  and  other  species,  and  Lucker  (1934)  observed  two 
molts  in  the  larvae  of  S.  ranxoiiii  of  pigs,  but  other  observers 
have  not  mentioned  more  than  one  molt.  The  -second  stage 
larva,  according  to  Lucker.  does  not  at  first  differ  in  any 
morphological  characters  from  the  first  stage  larva,  but  transi- 
tion to  the  filariform  type  of  larva  begins  soon  afterwards. 
The  first  molt  occurs  12  to  18  hours  after  hatching,  the  sec- 
ond within  48  hours,  at  room  temperatures.  The  filariform 
larvae  are  unsheathed  and  constitute  the  infective  stage.  They 
creep  up  on  points  of  vantage  in  the  soil  or  culture,  often 
clustering  together  in  brush  like  groups  to  await  an  opportu- 
nity to  burrow  through  the  skin  of  a   host. 

In  the  heterogoiiic  type  of  ilevelo])meiit  the  rhabditiform 
larvae,  instead  of  developing  into  filariform  larvae,  change 
into  adult  free  living  males  and  females.  With  the  exceptimi 
of  Lucker  (1934),  no  observer  has  mentioned  or  suggested  more 
than  a  single  molt  in  the  course  of  this  development,  but 
Lucker  has  been  able  to  trace  the  usual  four  molts  and  five 
stages.  The  only  morphological  changes  are  in  size  and  in 
growth  of  the  genital  primordiiim  until  the  fourth  stage  is 
reached,  when  the  structure  of  the  head  simulates  that  of  the 
adult,  and  the  male  and  female  characters  are  gradually  as 
sunied.  At  the  time  of  the  final  molt  the  ovaries  of  the  females 
and  spicules  of  the  males  are  fully  formed.  Adults  may  be 
found  after  36  to  48  hours  at  room  temperature. 

The  impregnated  females  produce  eggs  soon  after  they 
reach  maturity,  and  these  hatch  soon  after  being  deposited. 
These  first-stage  rhabditiform  larvae  are  morphologically  simi 
lar  to  those  hatching  from  eggs  deposited  by  the  iiarasitic  fe 
males,  although   a   few  small   differences   have   been   mentioned 

*The  term  "filariform**  is  used  here  to  denote  the  third  stage  larva  of 
Stronffyloitles  to  distinguiKh  it  from  the  third  stage  larva  of  strongyliiis 
which  is  called  "slrongyliform**  larva.  Its  use  in  no  way  signifies  a 
similarity  to  any  slage  of  tilariids.  Actually,  the  esophagus  is  very 
similar  to  that  of  an  infective  strongyl  larva. — B.  O.  C. 


by  Kreis  (1932).  AIIIi.mikIi  Kieis.  like  all  ollicis  lirfure  him, 
fails  to  niention  luore  than  a  single  molt,  l.ucker  was  able  to 
trace  the  orthodox  two  molts  before  the  infective  filariform 
larva  was  iirodnced,  .just  as  in  the  case  of  filariform  larvae  of 
direct  devi'lopmeiit.  No  dilTercnce  between  the  two  types  of 
infective  larvae  has  been   noted. 

Heacli  (193r)  193(i)  showed  that  under  particularly  favorable 
conditions  there  may  be  several  generations  of  free  living 
bisexual  forms.  Kouri,  Hasnuevo  and  .Xrenas  (1930)  reported 
that  .S*.  sicrciirnli.s,  after  numerous  free  living  generations,  be- 
comes entirely  free  living;  the  females  become  iiarthenogenetic 
and  there  are  no  males,  but  the  fecundity  of  the  females  gradu- 
ally  decreases  until   the  cultures   become   sterile. 

.Nishigori  ( 1928)  first  demonstrated  the  opposite  extreme  in  the 
life  cycle  of  .S*.  sti-rroriiliK — internal  auto  infection  (called  hyper- 
infection  by  Faust),  with  complete  eliinination  of  a  free  liv- 
ing stage.  Nishigori  also  suggested  circumstances  under  which 
this  might  occur.  Faust  (1931)  and  Faust  and  Kagy  (1933) 
continued  Nishigori 's  observations,  but  the  evidence  was  in- 
conclusive for  many  until  Faust  and  detiroat  (1940)  made  ob- 
servations at  autoiisy  of  a  case  which  left  no  room  for  doubt 
but  that  under  exceptional  conditions  in  human  beings  auto- 
infection  by  filariform  larvae  of  S.  nlircoralis  through  the  walls 
of  the  colon  can  occur.  There  is  no  certainty,  however,  that 
it   occurs   in   other   siiecies   or   hosts. 

The  filariform  larvae  of  S.  .stfrc(ir<ili«  and  most  other  sjiecies 
normally  jienetrate  the  skin.  If  swallowed  they  burrow  through 
the  mucous  niembranes  of  mouth,  esojihagns  or  stomach.  Miiii- 
nig  (1930),  however,  states  that  sheep  are  usually  infected 
with  S.  papilloxiiK  by  mouth,  this  species  being  a  poor  skin-penc- 
trator,  and  that  larvae  administered  by  month  do  not  migrate 
to  the  lungs.  Lucker 's  (1934)  experiments  with  .S.  ransiimi 
suggest  that  in  this  species  also  migration  to  the  lungs  may 
not  take  place  after  oral  infection. 

The  larvae  of  .S*.  xhrcorallx,  after  penetrating  skin  or  mu- 
cous membranes,  enter  the  circulatory  system  and  are  carried 
to  the  lungs.  Faust  (1933)  states  that  they  reach  the  lungs 
unchanged;  they  are  sometimes  recovered  as  earl.v  as  the  third 
day,  and  sometimes  as  late  as  the  thirtieth  day.  Although  no 
molts  are  mentioned,  Faust  distinguishes  iiost-filariform,  pre- 
adolescent,  adolescent,  aid  mature  female  mid  male  forms.  The 
post-filariform  type  of  larvae  is  found  most  commonly  in  the 
lungs  about  the  fifth  day;  if  carried  to  the  digestive  tract 
they  seem  unable  to  establish  themselves.  These  larvae  are 
slenderer  than  infective  larvae,  with  longer  esophagus,  and 
are  more  plastic.  The  preadolescent  forms  also  occur  princi- 
pally ill  the  lung  tissue  and  bronchioles,  and  are  believed  to  be 
too  immature  to  establish  themselves  in  the  intestine.  At  this 
stage,  according  to  Faust,  sexual  differences  are  observable 
for  the  first  time,  the  female  being  still  more  slender  than  the 
post  filariform  type  and  with  a  longer  esophagus,  whereas  the 
male  shows  decided  resemblances  to  the  rhabditiform  larva. 
The  adolescent  forms  are  migratory,  and  are  commonly  found 
not  only  ill  the  lungs  but  also  in  the  upper  parts  of  the  respira- 
tory ti-ee,  e.sophagus  and  intestines.  Both  mature  females 
and  males  were  reported  from  lung  tissue  and  bronchioles,  but 
only  mature  females  from  the  intestine,  where  they  burrow 
into  the  walls.  Lucker  (1934),  studying  S.  ransomi,  ob.servcd 
only  a  single  molt  after  entering  the  body  of  an  animal,  this 
occurring  in  the  intestine  about  6  days  after  infection  ;  Looss 
(1911)  also  reported  only  a  single  molt,  but  Fiilleborn  (1914) 
apparently  considers  that  two  molts  occur.  By  analogy  with 
other  nematodes,  and  with  the  development  of  the  free  living 
adults  of  atrongyloidcs  itself,  it  would  seem  more  probable  that 
two  molts  do  occur  in  the  course  of  the  development  in  the 
host. 

There  has  been  much  difference  of  opinion  on  several  points 
in  connection  with  the  life  cycle  of  Strimt/yloides,  particularly 
(1)  the  factors  determining  whether  the  development  is  homo- 
gonic or  heterogoiiic;  (2)  the  reproduction  status  of  the  jjara- 
sitie  females,  and  (3),  since  the  work  of  Kreis  (1932)  and 
Faust   (1933),  the  occurrence  and  function   of  parasitic  males. 

Sandground  (1926)  gave  a  brief  but  valuable  summary  of 
views  up  to  the  time  of  his  writing  on  the  factors  determining 
direct  or  indirect  development.  Environmental  factors  were 
first  thought  to  be  the  cause,  but  Braun  (1S99)  and  others 
showed  that  such  was  not  the  case;  Sandground  felt  that  there 
remained  no  substantial  rea.soii  for  questioning  the  gener- 
ally accepted  idea  that  the  direction  of  development  was  fixed 
before  the  larvae  entered  their  period  of  free  life.  Leichten- 
stern  (190.-|)  advanced  the  view  that  there  were  two  genetically 
different  varieties  of  the  human  species,  differing  in  their  life 
cycles,  the  indirectly  developing  variety  being  confined  to  the 
tropics,  the  directly  developing  one  being  especially  character- 
istic of  the  temperate  zone.  Leichtenstern  considered  the 
heterogonic  type  to  be  the  more  primitive  and  gave  a  very 
jilausilile  explanation  for  the  evolution  of  the  homogonic  type. 
Darling  (1911)  suggested  as  a  cause  environmental  effects  on 
the  rhabditifonn  larvae  jirior  to  leaving  the  host,  and  Brumpt 


269 


Fig.    179.     DEVELOPMENT    Ob'    STJi'OMiY LOI UKS    AND    h'HAJilJJAS 


A-L — Strongyloides  ransomi  (A-B — Direct  cycle,  A — First  stage  larva. 
newly  hatched;  B — Larva  in  first  molt;  C-J — Indirect  cycle:  C — 
First  stage  larva,  newly  hatched ;  D — Larva  in  first  molt ;  E — Larva 
in  second  molt ;  F — Larva  in  third  molt ;  G — Larval  female  in  fourth 
molt,  H — Fiist  stage  larva  from  free-living  female,  newly  hatched;  I — 
Second  stage  larva,  immediately  after  first  molt;  J — "Filariform"  larva 
undergoing  second  molt;  K-Lr — Parasitic  generation,  K — Larva  from 
suiall  intestine  of  pig  about  4  days  after  percutaneous  infection;  L — 
Larva  fi  om  pig,  showing  early  final  molt) .  M-0 — Rhabdios  fulleborjii 
(M — Free-living  female  with  larva,  the  genital  organs  already  destroyed: 
N — Cuticular  hull  of  female  with  only  one  filariform  larva,  115  hr.  old 
culture;    O — Filariform    larva    (Same   as    N)    from    which    ruticle   of    fe- 


male has  been  carefully  removed) .  P-Q — Rhnhdia^  fuscovenosa  (P — 
Infective  rhabditiform  larva  72  hours  after  hatching  from  egg  of  para- 
sitic generation;  Q — Filariform  larva  (infective  larva)  from  free-living 
generation) .  R — Parastrongyloides  winckesi  male,  S-W — Rkabdias  fua- 
corenosa,  direct  development  {S— Rhabditiform  larva ;  T — Ensheathed 
infective  larva;  U — Anterior  end ;  V — Anterior  end  during  third  and 
fourth  molts;  \V — Posterior  end  of  same).  A-L,  after  Lucker,  J,  T.. 
1934,  U.  S.  D.  A.  Bull.  no.  437.  M-0.  after  Travassos,  L.,  1926. 
Arch.  Schiffs.  u.  Tropen-Hyg.  v.  30.  P-Q.  after  Chu.  T.  C.  1936,  J. 
Parasit.  v.  22  (2).  R,  after  Morgan,  D.  O..  1928,  J.  Helm.  (6). 
S-W,  after  Goodey.  T.,   1924,  J.  Helm.  2. 


270 


<I!I21>  piishfd  till'  i.ott'niiinatioii  ;i:ifK  still  r'lirtliii',  l»  ilu-  dc 
velopiiift  OKRS.  Siiiidttrouinl  (lil'JO),  wlio  ro|ioitiMl  tlio  nndliiR 
of  sperins  in  frmali'  worms  jinil  romUiili'd  that  the  worms 
wore  liermapliroditic,  sii(;K>'sti'd  that  tlio  diri'ition  of  drvrlop 
mont  is  dotormiiiod  Ivv  tlio  cliioinosoiiial  constitiilioii  of  tlio 
ORRS  siibsi>(iU(Mit  to  firtilizatioii.  Kaust  (l!i:!3),  liaviiiK  found 
what  he  inti'rprotod  as  parasitic  niaU's.  suntri'stcd  that  fntilizi'il 
*'BBS  givo  risi"  to  hotoioKoiiic  and  iitifi'rtili/.ed  orks  to  lionio 
gonic  progeny.  Snlisecpiontly  Beacli  (,  1!I,'!.">1  ".).'!(>'),  working  in 
Faust's  laboratory,  showed  conelusively  that  the  course  of 
development  can  l>e  iiitluenccd  by  nutritional  conditions;  as 
these  become  less  favorable  more  and  more  of  the  rhabditi 
form  larvae  undergo  direct  development  to  filariform  larvae 
instead  of  becominu  males  and  females.  The  evidence  indi 
catcd  that  the  potential  females  are  intluenced  in  this  way 
more    readily    than    the    potential    males. 

Meanwhile  Graham   (ISKUi  l'.)3il)   started  two  pure  lines  of  .S. 
rata  of  rats  from  original  single  larva  infections  of  the  homo 
gonic    and    heterogonic    type,    respectively,    and    found    marked 
inherent  dilTerenees  between   them.     In   each  line  over  85  per- 
cent of  the  total  progeny  were  of  its  own  type,  with  an  ex- 
treme   difference    in    the    number    of    males    produced.    Graham 
also  observed  that  there  was  .-i  falling  off  in  heterogonic  larvae 
in  winter  as  comjiared  with  summer,  brought  about  b.v  climatic 
effects  on  the  host,  not  on  the  develojiing  larvai'.     Tlie  conclu 
sion    seems   warranted,   therefore,   that    the   course   of   develop 
ment  is  dependent  upon   nutrition  or  other  cnvirontuental  con 
ditious  and  not  upon  genetic  constitution,  but  that  there  are 
genetic    differences    in    the    e.\tent    to    which    different    strains 
are  influenced  towards  homogony  by  a  given  degree  of  unfavor 
ableness  in  the  environment. 

The  reproductive  status  of  the  parasitic  females  was  brought 
into  question  by  Sandground  (lilifi^  ;  prior  to  that  time  it 
had  been  generally  accejited  that  they  were  partheuogenetic, 
although  Leuckart  ai>parently  suspected  that  they  were  hernia 
phroditie,  by  analogy  with  the  condition  in  the  parasitic  genera- 
tion of  Rhabdia.i.  Satulground  believed  them  to  be  protandrous 
hermaphrodites;  he  described  what  he  interpreted  as  sperms 
and  observed  what  seemed  to  be  fertilization  in  specimens  of 
S.  ratti.  Faust  (1933),  having  found  male  worms  in  the  lungs, 
concluded  that  the  sperms  observed  by  Sandground  luobably 
were  the  result  of  copulation.  He  considered  the  worms  to 
be  bisexual  early  in  life,  later  becoming  parthenogenetic.  Chit- 
wood  and  Graham  (1940)  concluded  that  -S.  ratti  was  parthe- 
nogenetic since  they  were  unable  to  find  sperms  and  also  un- 
able to  find  fertilization  membranes.  The  weight  of  evidence 
is  therefore  in  favor  of  parthenogenesis. 

The  occurrence  of  parasitic  males  described  by  Kreis  (1932) 
and  Faust  (1933)  has  not  been  confirmed  by  others.  In  an 
unpublished  observation,  one  of  us  (J.  E.  A.)  has  noted  adult 
rhabditiform  males  in  the  fresh  feces  from  a  ease  of  human 
strongyloidiasis  but  it  was  unknown  whether  these  were  para- 
sitic males  or  males  developing  from  eggs  of  parasitic  females. 
The  fact  that  the  supposed  parasitic  males  of  Kreis  and  of 
Faust  were  rhabditiform  and  practically  identical  with  free- 
living  males  is  sufficient  cause  for  doubt  that  they  are  really 
males  of  the  parasitic  generation,  for  in  the  one  other  mem- 
ber of  the  Strongyloididae  in  which  males  have  been  found — 
Parastronffyloidcs  uinchcsi,  Morgan  1928 — the  parasitic  males 
are  filariform  like  the  females.  We  suggest  that,  since  Faust 
not  only  observed  eggs  and  rhabditiform  larvae,  but  also 
filariform  larvae  which  he  interpreted  as  the  progeny  of 
the  parasitic  worms,  in  the  lungs  and  bronchioles  of  infected 
hosts,  the  males  observed  were  free  living  males  produced 
precociously  in  the  lungs.  The  observations  of  Beach  (1.  c.) 
that  males  will  develop  more  readily  than  females  under  subop- 
timal  conditions  would  account  for  the  failure  to  find  free- 
living  females.  Graham's  work  with  single-larva  infections 
has  shown  clearly  that  males  are  at  least  unnecessary  in  S.  ratti, 
though  no  conclusions  can  be  drawn  from  this,  for  it  is,  of 
course,  possible  that  there  might  be  differences  between  spe- 
cies in  this  respect.  For  the  present  the  occurrence  of  rhab- 
ditiform parasitic  males  in  members  of  the  genus  Strongy- 
loides  must  certainly  be  considered  sub  jtidice. 


Fig.  180.  DEVELOPMENT  OF  STRONGTLOIDKS 

A-G — StTontryloiileg  stercorals  (A — Parasitic  female;  B — Free  living 
male;  C — Free  living  female;  D — Filariform  larva  (human  strain  A), 
from  lung  tissue  of  experimental  dog  three  days  after  skin  inoculation; 
E — Post-filariform  larva  from  same:  F — I'readolescent  female  from  lung 
of  experimental  dog  11  days  after  skin  inoculation,  note  developing 
genital  primordium;  G — Adult  male  from  lung  tissue  of  experimental 
dog  57  days  after  skin  inoculation).  H-M — Strongyloitle/t  sp.  from  dog. 
free  living  generation  (H — First  stage  larva;  I — Infective  larva:  J — 
Tail  of  infective  larva;  K — Head,  adult  female;  L — Adult  female;  M — 
Tail,  male).  A-C.  after  Faust.  E.  C,  Human  Helminthology.  1939. 
D-G.  after  Faust.  E.  (',.  1933.  Am.  J.  Hyg.  v.  18  (1).  Remainder 
original  drawings  by  M.  B.  C. 


271 


Ehabdiasidae 

The  niembers  uf  tlio  genera  EJiabdian  and  Entoinclat:,  now 
separated  into  a  separate  family  from  Strunyyloides,  resemble 
Strongyloididae  in  having  an  alternation  of  generations,  at 
least  in  some  species.  This  double  life  cycle  was  tirst  demon- 
strated by  Meczuikov  (18G.j)  in  the  case  of  M.  btifonis.  Unlike 
StrongyluidcK,  the  parasitic  generation,  at  least  of  some  species 
of  Sliabdias,  consists  of  hermaphroditic  females,  possessing  a 
well  developed  seminal  receptacle.  Seurat  (1920a),  however, 
thinks  that  the  parasitic  forms  of  Entumdas  dujardini  and 
E.  entomclux  from  Anguis  fragilis  are  parthenogenetic  rather 
than  protandrous  hermaphrodites,  since  he  was  unable  to  find 
seminal   receptacles  or  to  detect   sperms. 

As  in  Strongyloides,  l)oth  homogonic  and  lieterogonic  types  of 
development  may  occur  in  the  free-living  phase  of  the  life  cycle 
of  Sliabdia.i.  In  most  of  the  species  one  type  or  the  otiier 
strongly  predominates  or  may  even  occur  exclusively,  though 
in  some  of  the  forms  in  which  one  type  of  development  was 
long  thought  to  occur  exclusively,  the  alternative  type  has 
more  recently  been  observed.  Travassos  (i;i2())  called  atten- 
tion to  the  fact  that  the  species  found  in  Amphibia  and  La- 
certilia  have  indirect  development,  while  those  found  iji  snakes 
liave  direct  development.  Chu  (iy3(i),  however,  reported  some 
unpublished  observations  of  Chitwood  's,  and  also  some  of  his 
own,  in  which  both  types  of  development  were  found  in  sev- 
eral amphibian  and  reptilian  species,  (ranac,  eustreiitus,  fulle- 
borni,  and  fuscovenosa  var.  caUtiicnfiin).  In  the  last-named  spe- 
cies Chu  observed  only  homogonic  development  except  wlien 
an  especially  favorable  culture  medium  was  used,  whereupon 
a  small  percentage  of  free-living  adults,  predominantly  males, 
were  usually  found.  The  oflspring  of  these  adults  failed,  how- 
ever, to  infect  snakes.  It  seems  evident  from  this  data  that  the 
course  of  development  of  Bluibdia!<  is  determined  by  factors 
similar   to   those   operating   in   the   case   of   Utroiigijloidcs. 

Whereas  in  SI niiigiituidc s  both  direct  and  indirect  infective 
larvae  are  filariform,  in  the  Rhabdiasidae  the  direct  huvae  are 
rhabditiform  while  the  indirect  ones  are  filariform  (cf.  Figs. 
17ii,  P-Q).  The  free-living  adults  of  different  species  vary  con- 
siderably in  their  mode  of  reproduction.  Travassos  describes  the 
free-living  female  of  S.  fiiUcborni  of  frogs  as  producing  only 
one  or  two  larvae,  which  may  become  fully  developed  within  the 
mother,  destroying  her  tissues,  whereas  Chu  (lit.^G)  describes 
K.  fuscovenona  var.  cataiiciiin  as  having  a  few  eggs  in  each  horn 
of  the  uterus,  which  are  usually  laid  when  little  or  no  develop- 
ment has  occurred. 

According  to  Goodey  (,l!t24)  the  homogonic  larvae  of  S. 
fuscovenosa  undergo  two  ecdyses  outside  the  body  of  the  host, 
the  second  shed  cuticle  being  retained  as  a  tight-fitting  sheath 
for  the  infective  larvae.  The  sheath  is  shed'  upon  gaining 
entry  to  the  host.  The  larvae  molt  twice  more  during  de- 
velopment in  the  host's  parenteral  tissues,  but  both  shed 
cuticles  are  retained  as  sheaths.  Although  the  infective  larvae 
of  S.  bufoiiis  were  reported  by  FuUeborn  (1920)  to  penetrate 
the  skin,  and  by  the  same  writer  (1928)  to  migrate  to  the 
lungs  via  the  circulatory  system,  Goodey  (1924)  failed  to 
get  the  infective  larvae  of  R.  fuscovenosa  to  penetrate  skin, 
although  their  behavior  outside  the  body  was  like  that  of 
skin-penetrating  larvae,  and  he  also  thought  it  probable,  from 
their  distribution  in  the  body,  that  they  migrated  to  the  lungs, 
after  penetrating  the  gut  wall,  by  direct  migration  through 
the  mesentery  and  not  via  the  blood  stream.  Fiilleborn  (192S) 
called  attention  to  the  fact  that  larvae  of  E.  bufoiiis  would 
also  penetrate  snails  and  possibly  other  invertebrates,  where 
they  rcmaiu  unchanged  for  weeks,  capable  of  infecting  a  frog 
when  the  snail  is  eaten.  Similarly  the  larvae  may  sometimes 
became  encapsulated  parenterally  in  frogs  which  may  then 
act  as  "transport  hosts"  for  infection  of  larger  frogs  which 
eat  them.  Fulleborn  suggests  that  since  the  skin  of  snakes  is 
hard  to  penetrate  transport  hosts  may  constitute  the  principal 
method  of  infection  for  these  hosts. 


STRONGYLINA 
I.    STRONGYLOIDEA  AND  TRICHOSTRONGYLOIDEA 

Three  geneial  types  of  life  cycles,  which  more  or  less  merge 
into  each  other,  occur  in  the  superfamilies  Strongyloidca  and 
Triehostrongyloidea  of  the  suborder  Strongyliua.  One  of  these, 
characteristic  of  the  Ancylostomatidae  and  a  few  other  forms 
in  the  Strongyloidca  and  Triehostrongyloidea,  is  essentially 
the  same  as  the  homogonic  cycle  of  Ehahdias,  except  that  the 
parasitic  worms  are  bisexual.  It  involves  development  to  the 
third  (infective)  stage  outside  the  body  of  the  host,  skin  pene 
tration,  and  parenteral  migration  via  the  circulatory  system 
after    infection.      The    second,    characteristic    of    most    of    the 


Triehostrongyloidea  and  many  of  the  Strongyloidca,  differs 
in  that  there  is  no  skin  penetration,  and  no  migration  in  the 
host  beyond  the  walls  of  the  alimentary  canal.  The  third, 
characteristic  of  the  Syngamidae  in  the  Strongyloidca,  in- 
volves development  and  molting  within  the  egg,  w^ithout  feed- 
ing or  growth,  with  at  least  optional  establishment  in  an  in- 
vertebrate transport  host,  and  a  parenteral  migration  which 
leads  to  the  respiratory  system  but  not  lieyond.  We  think  it 
probable  that  both  types  2  and  3  were  derived  from  type  1, 
although  it  is  also  possible  that  type  2  is  the  most  primi- 
tive, and  that  types  1  and  ?>  were  both  derived  from  this. 

1.  Ancylostoma  spp. 
The  genus  Ancylostoma  will  serve  as  a  typical  example  of  the 
first  type,  involving  skin  penetration  and  parenteral  migration. 
The  eggs  of  these  worms  are  deposited  by  the  adult  females 
in  the  lumen  of  the  small  intestine,  whence  they  make  their 
exit  with  the  feces;  at  the  time  of  leaving  the  body  of  the 
host  they  are  nearly  always  in  the  four-celled  stage  of  devel- 
opment, normally  being  unable  to  progress  beyond  this  point 
without  free  oxygen.  Under  optimum  conditions  of  oxygen, 
moisture  and   warmth    (7.1°   to   8.')°   F.)    the   eggs  proceed  with 


Fig.   181.    DEVELOPMENT  OF   HOOKWORMS 

Ani-ylostonui  dtindenale.  A — First  stage  larva  ;  B — Second  stage;  C — 
'I'liird  stage.  D-H — Development  of  primitive  and  definitive  capsules; 
(  1) — Bladder-like  structures  forming  around  the  larval  oral  cavity,  with 
heginning  of  formation  of  the  primitive  larval  teeth;  E — Nearly  com- 
pleted primitive  capsule,  with  triangular  teeth  at  base,  and  old  larval 
oral  cavity  still  running  through  center  of  primitive  capsule;  F — Fully 
developed  primitive  capsule  with  beginning  of  formation  of  bladders  at 
its  base;  G — Later  stage  in  development  of  dorsal  and  ventral  bladders 
which  will  eventually  form  the  definitive  capsule;  H — Later  stage  in 
development  of  definitive  capsule,  with  primitive  capsule  still  connected 
with  esophagus  by  a  strand  of  tissue;  I — Female  larva  with  definitive 
capsule  formed  but  primitive  capsule  still  attached ;  J — -Male  after  final 
moult  but  last  cuticle  still  enclosing  it;  K — Male  larva  with  primitive- 
capsule.     After  Looss.  Chandler.  A.  C.   1929,   Hookworm   Disease. 


272 


thoir    (U'voli)|)niiMif     laiiidly,    :iii<l    :i     rliiiliilitifi)iiii     liirvji     iiiav 
liatih  witliin  :;4  lunirs.     This  larva  is  aliout  •_'."!()  ^  loiiR,  with  nii 
iMonuali'il   liiiccal  cavity  ami  a   typical   rhahilitiform  csophaKiis 
IKisscssiiiK  csoiihaiioal  valves.     Tlu'so  larvae  were  shown  l>y  Mc 
Coy  (IJIJill   to  (icvclop  normally  with  oTily  pnrc  cultures  of  cer 
tain  species  of   living  bacteria  as  food.      Tniler   favorable  con 
(litions   the   larvae  underKo   the   first   ecdysis  or  molt   within   4S 
li.niis  atter  liatchinj;,  bnl   second  sta(;e  larvae  show  very  slight 
niorpholoKical  difTeronccs  from  first  sta^e  larvae,  although  they 
arc  about  400  to  4:U)  A"  long,     .\ftor  a  niiniuiuni  of  about  2  more 
d.-iys   the   larvae  cease   fecdiuK.   undergo   a   second   ecdysis,  and 
enter   the   third   or   infective   staRO.      The   cuticle   shod   at    this 
molt  is  normally  retaiiu'd  as  a  protective  sheath,  though  it  may 
occasionally  be  lost.    The  most  important  inori)holo^rical  changes 
in  the  infective  larva  are  noted  in  the  shape  of  the  tail  and  the 
structure  of  the  esophaRUs.   The  tail  is  shorter  and  more  stumi)y 
than   that   of  the   prccediuK  stages.     The  esojihaKus   is   "lilari 
form,"   or    preferably    "strouByliform,"    i.e.,   it   is   more   uni 
form  ill  width  with  tapering  anterior  portion,  and  the  esoplia 
seal  valves  are  lacking.     The  anterior  portion  of  the  lumen  of 
the  stoma  is  closed  and  the  reuuiining  posterior  portion  remains 
open   in   a   characteristic   shape.     According   to   .\licata    (l!>.'i.")) 
the   various    third  stage   larvae   of   strongylid    nematodes    para 
sitic  m  swine  can   be  differentiated,  among  other  ways,  by  the 
form   of   the  stoma;    there   is  a   jiossibility   that   this  character 
istic  may  hold  true  for  other  members  of  the  Strongylina. 

The  infective  larvae  climb  up  on  ob.jects  as  high  as  a  film  of 
moisture  extends,  and  show  positive  thermotropism  and  thig- 
motropism.  They  retire  from  excessive  warmth  in  direct  sun- 
light. They  migrate  vertically  if  buried  in  soil,  but  migrate 
laterally  to  a  very  slight  extent  (Chandler,  1925). 

.Mthough  Leuckart  (ISOO  showed  that  .(.  caiiiiiiim  of  dogs 
could  1)0  transmitted  per  n.i,  and  Leicliteustern  (ISS(i)  proved 
the  same  thing  for  .1.  iltuHlciiali'  of  man,  the  usual  mode  of  in- 
fection is  by  iienetration  of  the  skin;  this  method  of  infection 
was  first  demonstrated  by  Looss  (ISiiS).  In  subser|uent  work 
Looss  (190."))  established  the  course  which  the  larvae  follow 
in  the  body  to  reach  the  intestine.  Skin  penetration  is  accom 
plishcd  in  a  few  minutes  when  the  larvae  are  able  to  obtain 
leverage,  as  in  mud,  to  help  them  in  their  burrowing,  but  they 
are  nimble  to  penetrate  when  submerged  iu  water.  Within  3.") 
to  40  minutes  the  larvae,  having  left  their  sheaths  behind  them. 
have  reached  the  dermis  and  within  a  few  hours  are  in  the  sub 
cutaneous  tissue.  Many  find  their  way  into  superficial  lym 
phatic  capillaries,  and  a  few  directly  enter  blood  vessels.  Some 
larvae  are  slow  in  entering  the  circulation,  and  may  be  en- 
capsulated in  the  .skin,  especially  in  hosts  sensitized  by  previous 
exposure.  Certain  "foreign"  species  of  hookworms,  e.g. 
Aiicnlo.'ttoma  braziUense  and  Uncinaria' stowccplmla  in  man, 
commonly  fail  to  enter  the  circulation  at  all  but  wander  aim- 
lessly in  the  skin,  causing  "creeping  eruption."  Although  the 
larvae  may  remain  in  the  skin  for  considerable  periods  no  de- 
velopment takes  place  there  (Fiilleborn,  1927). 

When  larvae  enter  the  lymphatics  they  are  carried  first  to 
the  regional  lymph  glands,  and  then  to  the  main  lymph  chan- 
nels leading  to  the  thoracic  duct,  through  which  they  enter  the 
circulation.  Such  larvae,  as  well  as  those  which  entered  the 
blood  system  directly,  eventually  reach  the  right  heart,  whence 
they  are  pumped  out  to  the  lungs.  Here  the  ma.iority  burrow 
into  the  air  spaces  (Fiilleborn,  192.')),  and  are  then  mechani- 
cally carried  in  mucus,  helped  by  epithelial  cilia,  to  the  trachea 
and  throat.  If  .swallowed  they  now  pass  to  the  alimentary 
canal,  and  grow  to  maturity  in  the  intestine. 

Although  .skin  penetration  is  undoubtedly  the  usual  mode  of 
infection,  infection  by  mouth  can  also  occur.  There  has  been 
considerable  controversy  as  to  whether  swallowed  larvae  had 
of  necessity  to  penetrate  the  mucosa  and  migrate  to  the  lungs 
before  growing  to  maturity,  or  whether  they  could  develop  to 
maturity  without  such  migration.  Yokogawa  (192(5)  investi- 
gated the  matter  and  found  that  when  A.  canhnim  larvae  are 
fed  to  puppies  a  few  penetrate  the  walls  of  the  alimentary 
oanal  and  enter  the  circulation,  but  the  great  ma.iority  of  those 
which  develop  at  all  do  so  directly,  without  migration.  In  ab- 
normal hosts,  however,  such  as  rodents,  most  of  them  perform 
the  usual  migration  via  the  circulatory  s.vstem,  and  a  few  mi- 
grate through  the  tissues  to  the  body  cavity  whence  they  enter 
the  liver,  or  go  through  the  diaphragm  to  the  ])leural  cavity, 
whence  thev  enter  the  lungs.  This  work  was  confirmed  In- 
Scott  (1928).  Fiilleborn  (1926-1927)  showed  that  the  larvae 
of  Uncinaria  strnociphala  of  dogs  also  develop  directly  after 
oral  infection,  few  migrating  even  in  abnormal  hosts.  Several 
Japanese  workers,  however,  (Myiagawa,  191fi;  Myiagawa  and 
Okada,  liiSO,  19H1;  Okada  ig.'Sl)  have  persisted  in  the  belief 
that  lung  migration  is  a  biological  necessity  for  hookworms. 
Foster  and  Cross  (1934)  carried  through  some  further  cxjjeri- 
ments  which  conclusively  confirm  the  earlier  work,  showing  that 
the  lung  .journey  is  not  a  biological  necessity  for  these  worms 
(though  it  apparently  is  for  Strongyloidex  sfrrcoraUn.)  Swal 
lowed    larvae    rarely   migrate   in   su.sceptible   normal    hosts,   but 


coniinonly  do  so  in  abriormal  hosts  and  in  resistant  normal  ones. 
I.oo.ss  (1911)  and  S'okogawa  (192(i)  observed  that  sw;illowed 
hookworm  larvae  remain  in  the  stomach  at  least  2  days,  and 
I'illleborn  (1927)  found  tin'y  could  remain  there  at  least  ") 
(l.iys,  partly  in  the  lumen,  jiartly  deep  in  the  mucous  glaruls. 
Ill'  demonstrated  that  the  larvae  have  an  initial  tendency  to 
burrow  into  the  glands,  later  to  return  to  the  lumen,  as  is  the 
case  with  Asroriiiia.  lie  thinks  that  something  in  the  secretion 
of  the  mucous  glands  causes  the  larvae  to  lose  their  mobility; 
possibly  the  .same  mech.'inism  is  responsible  for  the  loss  of  the 
burrowing  instinct  in  the  l;irvae  reaching  the  intestine  from  the 
Inngs  after  skin  penetration   (see  below). 

The  minimum  time  rc(|uired  for  the  larvae  to  reach  the 
trachea  after  skin  penetration  is  usually  about  3  days,  but  the 
ma.iority  re(|uire  4  or  ."i  days,  and  some  still  longer.  By  the 
time  the  larvae  appear  in  the  bronchioles  and  tr;ichea  they  have 
grown  slightly  in  length,  have  developed  a  provisional  mouth 
capsule,  and  are  ready  for  the  third  molt,  although  there  is  no 
evidence  tli:it  the.v  ever  complete  it  before  reaching  the  diges- 
tive tract.  The  formation  of  the  provisional,  and  subsefiuently 
of  the  definitive,  month  capsules  is  accomplished  by  the  devel- 
opment of  dorsal  and  ventral  bladder  like  structures  posterior 
to  the  already  existing  mouth.  These  spread  around  tin'  sides 
and    finally    unite    (Looss,    1905)     (Figs.    181). 

Up  to  the  time  of  the  third  molt  the  larvae  grow  very  little 
in  length,  but  increase  from  about  20  m  to  30  M  in  diameter. 
The  molt  usually  occurs  very  soon  after  the  larvae  reach  the 
intestine,  and  the  larvae  at  this  time  lose  their  tendency  to 
burrow,  so  remain  in  the  intestine.  There  is  no  evidence  that 
they  temporarily  burrow  into  the  glands  of  the  stomach  as  do 
larvae  that  are  directly  swallowed.  The  young  worms  now 
grow  very  rapidly.  They  may  reach  a  length  of  2.5  to  3  mm 
within  a  few  days.  Sexual  differentiation  now  begins,  and  in 
from  4  to  6  days  after  the  third  molt  the  definitive  mouth  cap 
sule  is  developed.  By  the  time  the  worms  have  reached  a 
length  of  from  3  to  5  mm.  the  fourth  molt  takes  place.  There- 
after the  worms  grow  to  maturity,  copulate,  and  begin  egg  pro- 
duction. In  the  case  of  Aitcylostoma  dnodeiiale  in  man  the 
eggs  first  appear  in  the  feces  5  to  6  weeks  after  infection, 
whereas  in  A  caiiiinim  of  dogs,  eggs  may  appear  as  early  as  15 
d;iys  (Herrick,  192S). 

2.     IIaemonchus  contortus 

The  life  cycle  of  this  worm  as  worked  out  by  Ran.soni  (1906), 
Veglia  (1916)  and  others  is  essentially  the  same  as  that  of  the 
ancylostomas  in  its  free-living  phase.  The  infective,  ensheathed 
third  stage  larvae,  however,  are  not  skin-penetrators,  but  have 
a  tendency  to  climb  up  on  vegetation  or  other  ob.iects  where 
they  are  in  a  favorable  position  to  be  ingested  by  their  herbiv- 
orous definitive  hosts.  Here  they  curl  up,  and  are  remarkably 
resistant  to  cold  and  to  moderate  desiccation.  Upon  being  in- 
gested by  the  final  host  the  larvae  bury  themselves  in  the  mu- 
cous glands  and  crypts  of  the  abomasum,  where  they  undergo 
the  third  and  fourth  molts;  the  sdult  stage  is  reached  after 
about  the  9th  to  11th  days,  and  the  worms  emerge  to  live  in  the 
lumen  of  the  organ,  beginning  egg  production  about  3  weeks 
after  infection.  Although  there  is  no  evidence  that  the  worms 
perform  a  parenteral  migration  in  sheep,  Ransom  (1920) 
showed  that  they  do  migrate  to  the  lungs  in  guinea  pigs. 

3.     Syngamus  trachea 

The  life  cycle  of  this  worm  was  first  experimentally  worked 
out  by  Ortlepp  (1923).  The  eggs  of  the  worm  are  laid  in  the 
bronchi  or  trachea  of  the  host  in  an  advanced  stage  of  seg- 
mentation. Under  favorable  conditions  the  first-stage  larva  is 
developed  in  about  3  days,  but  the  egg  does  not  become  infec- 
tive until  after  1  to  2  weeks,  whereupon  they  may  or  may  not 
hatch.  Ortlepp  observed  only  a  single  molt  during  the  course 
of  development  and  interpreted  the  infective  larva  as  a  second- 
stage  larva  but  Wehr  (1937)  demonstrated  that  the  develop- 
ing larva  undergoes  two  molts  within  the  egg.  Buckley  (1934), 
studying  5.  ierci  of  cats,  also  observed  the  usual  two  molts. 
Yokogawa  (1922)  also  missed  the  first  molt  in  the  case  of 
Xippostrongylus  muris,  and  in  spite  of  the  large  amount  of 
experimental  work  done  with  that  worm  the  missed  molt  was 
not  discovered  until  1936,  when  Lucker  demonstrated  it.  The 
first  cuticle  in  both  these  worms  is  extremely  thin,  and  the 
second  ecdysis  may  be  in  progress  before  it   is  coinpletely  shed. 

Infective  larvae,  whether  hatched  or  .still  in  the  eggs,  are 
infective  when  directly  swallowed  by  susceptible  hosts,  but 
very  often  they  are  swallowed  by  various  invertebrates;  when 
this  happens  they  penetrate  the  gut  wall  and  become  encap- 
sulated in  the  body  cavity.  Walker  (1.SS6)  and  Waite  (1920) 
both  called  attention,  on  epidemiological  grounds,  to  the  impor- 
tance of  earthworms  in  the  dissemination  of  this  parasite,  but 
Clapham  (1934)  first  experimentally  worked  out  the  role  played 
by  these  annelids.     Subsequently   Taylor    (1935)    showed  that 


273 


Fig.  182.  DEVELOPMENT  OF  THE  STRONGYLINA 


A-C — Syngamus  tracheaii^.  (A — Ensheathed  second  stage  larva;  B — 
Third  stage  larval  female;  C — Ensheathed  young  fourth  stage  larval 
male).  D-F — Syngamus  ierei  (D — Third  stage  larva;  E — .\nterior  end 
of  third  stage  larva;  F — Tail  of  third  stage  larva).  G — Haemonchus 
contortus  on  blade  of  grass.  H-N — OUulanus  ti'icuspis  (H — First  stage 
larva;  I — Second  stage  larva;  J — Tail  between  first  and  second  stage: 
K — Third  stage   (infective)    larva;   L — Fourth  stage  female;    M — Fourth 


stage  male;  N — Gravid  female).  0-U — Dictyocaulus  arnfieldi  (0-^Egg 
from  the  feces;  P-Q — First  stage;  R — Second  stage;  S — Third  stage;  T 
— Fourth  stage  male;  U — Fourth  stage  female).  A-C,  after  Ortlepp. 
1923,  J.  Helm.  v.  11.  D-F,  after  Buckley,  1934,  J.  Helm.  v.  72.  G, 
after  Ransom,  1906,  U.  S.  Bur.  An.  Ind.  Circ.  93.  H-N,  after  Cameron, 
1927,  J.  Helm.  v.  f>.  O-II.  after  Wetzel  and  Enigk,  1938,  Arch.  Wiss. 
u.  prakt.  Tierheilk.  73(2). 


274 


siiiiils  iiiul  sliiRS  wuiild  also  si'ivo  as  transport  liosts,  ami  later 
found  that  tlio  pneystod  larvae  would  remain  viable  in  these 
niolUises  for  several  years.  More  reeeiitly  Clnpham  (l!>Sila, 
l!).!i>h"l  showed  that  niaRBots.  erane  tiy  larvae,  spring  tails  ami 
eentipedes  would  serve  in  a  similar  eapaeity,  and  that  the 
worms  were  alile  to  survive  metamorphosis  in  the  tissues  of 
tlies. 

When  iiiKesteil  liy  these  hosts  the  infeetive  larvae  lialih  fnini 
the  eRKS  if  they  have  luit  already  done  so,  penetrate  the  gut 
wall,  and  enter  the  body  eavity,  where  they  are  eventually  en 
eapsulated  by  the  host  tissues,  t'lapliani  has  shown  that  the  life 
eycle  is  eompleted  somewhat  nuire  readily  with  the  aid  of  a 
vector  than  without,  and  was  able  to  infect  chickens  readily 
with  a  starlint;  strain  when  an  earthworm  vector  was  used, 
whereas  Taylor  (  1!>11S^  had  had  difficulty  in  doinjr  so  by  direct 
infection.  I'lapham  calls  attention  to  the  fact  that  Siiii'li'miix 
trachea  is  evidently  nndergoinK  evolution  in  its  life  cycle;  at 
present  it  can  still  develop  without  an  intermediate  host,  and 
iuis  not  as  yet  adapted  its  requirements  to  any  imiliciilar  inter 
mediate  host,  Init  can  use  almost  any  that  happens  to  swallow 
it.  She  makes  the  reasonable  suggestion,  however,  that  in  time 
difTerent  strains  may  adapt  themselves  to  different  intermedi 
ate  hosts,  as  determined  by  the  food  habits  of  the  final  hosts. 
and  thus  i>erhaps  give  rise  to  new  species.  At  present,  however, 
the  effect  of  living  in  a  transport  host  seems  to  be  to  rliiiiiiiair 
physiological  differences;  for  example,  in  the  case  of  starling 
strains  developing  in  chickens.  Tt  is  ]>ossible  that  some  species 
of  StjiiDamiis  may  already  have  reached  the  stage  of  reciiiirixn 
an  intermediate  host,  since  Buckley  (1S134)  was  unable  to  ii\ 
feet  cats  with  eggs  containing  third  stage  larvae  of  S.  irrci. 

After  infection  by  swallowing  eggs,  free  larvae,  or  larvae 
contained  in  invertebrate  transport  hosts,  .S".  trachra  appar 
ently  reaches  the  lungs  via  the  circulatory  .system.  Orflepp 
(1923)  found  the  larvae  in  the  lung  tissues  within  24  hours 
and  Wehr  as  early  as  17  hours  after  infection.  Welir  found 
fourth  stage  larvae  after  3  days  and  immature  adults  after  7 
days;  some  of  the  latter  were  already  in  cDpiila  even  before 
entering  the  trachea. 

Variatioks  in  the  Life  Cycle  in  Other  Stroncyi-oide.v 

AND  TrICHOSTRONGYLOIDEA 

The  preparasitic  stages  of  nearly  all  the  members  of  the 
Strongyloidea  and  Trichostrongyloidea,  except  the  Syngamidae, 
are  remarkably  similar,  involving  two  free  living  rhabditiform 
stages  separated  liy  a  molt,  and  a  strongyliform  third  stage,  in 
which  the  shed  cuticle  is  usually  retained  as  a  sheath.  The 
time  intervals  between  the  molts  and  the  total  time  required  to 
reach  maturity  vary  considerably;  in  some  species,  e.g.  Ornitlio- 
strongi/lus  quaflrirndiatiis,  the  infective  third  stage  may  lie 
reached  within  3  days.  The  infective  larvae  are  distinguish 
able  by  characters  of  the  mouth,  buccal  cavity,  esophagus, 
shape  of  tail,  length  of  sheath,  etc.,  and  also,  as  Lucker  has 
shown  in  a  series  of  papers  (e.g.,  I^ucker,  1938)  by  the  num 
ber  and  arrangement  of  cells  in  the  intestine. 

The  only  important  variation  from  this  formula  is  the  molt- 
ing of  some  species  within  the  egg,  thus  eliminating  a  period 
of  feeding  and  growth  outside  the  host ;  this,  as  already  noted, 
occurs  in  Synfiamim  and  it  also  occurs  in  XcmatoiUnis  spp. 
(Ransom,  1911;  Maupas  and  Seurat,  1913)  and  in  OsuaUlo 
cruzia  fijiformis  (Slrongyhis  auriciilari.t,  Zeder)  (Maupas  and 
Seurat,  1913  >.  According  to  the  latter  authors,  Ostcrtagio 
marshalli  hatches  as  a  second  stage  larva  and  undergoes  its 
second  molt  2  or  3  days  later  without  feeding.  This  is  not 
true,  however,  of  0.  circumcincia.  When  botli  molts  occur 
inside  the  egg  the  infective  embryos  may  or  may  not  hatch 
prior  to  being  swallowed  by  a  host,  eggs  containing  infeetive 
third-stage  larvae  being  infective  as  well  as  the  free  larvae. 

Strong ylacantha  glycirrhi^a,  according  to  Seurat  (1920b), 
hatches  at  the  end  of  48  hours  but  the  larvae  fail  to  feed,  and 
at  the  end  of  a  month  hare  molted  twice  and  are  ensheathed 
in  both  shed  cuticles,  .just  as  in  the  case  of  Dictyncaiiliis  (see 
below). 

A  striking  exception  to  the  usual  course  of  events  occurs  in 
the  case  of  Olliilaniis  iricuspis,  according  to  Cameron  (1927). 
This  parasite  of  the  stomach  of  eats  is  viviparous.  The  eggs 
hatch  in  the  uterus  of  the  mother,  and  the  larva  undergoes  its 
first  molt  before  it  is  born,  acquiring  the  typical  tri  cuspid 
tail.  Third  stage  larvae  are  found  free  in  the  stomach  of  the 
cat,  but  it  is  not  certain  whether  the  second  molt  occurs  before 
or  after  birth.  This  form  is  believed  by  Cameron  to  leave  the 
stomach  with  the  vomitus  of  the  eat.  When  eaten  by  another 
cat  with  the  vomitus  the  larvae  change  to  fourth-stage  larvae 
and  finally  adults.  Some  part  of  this  development  is  believed 
to  take  place  in  the  depths  of  the  mucous  membrane.  No  other 
method  of  exit  from  the  cat  has  yet  been  found ;  no  larvae  were 
ever  seen  in  the  intestine,  nor  were  mice  infected  when  fed  on 
cat  stomach  or  infected  vomitus.  Continuous  auto  infection  is 
believed   possitde   but   improbable;    Cameron   suggests   the   pos- 


sible production  of  a  substance  inhibiting  complete  larval  de- 
velojiment,  as  postulate<i  by  Fiilleborn  in  tin'  case  of  UhitlxUas 
hiifonis  in  the  lungs  of  frogs. 

The  mode  of  access  of  the  infective  l:nvae  to  the  final  host 
varies  in  different  species,  even,  sonietinu's,  within  the  same 
genus.  There  arc  three  possibilities:  (1)  pcTwtration  of  the 
skin;  (2)  ingestion  with  food  or  water;  (3;  ingestion  with  a 
transport  host.  Skin  penetration  is  characteristic  of  most  of 
the  hookworms  (l*'amily  Aucylostomatidae) — Avrylontoma, 
Xecalor,  i'ncinaria  iind  (laigerin — but  Iliiiioslomiiiii  seems  to 
be  an  exception  in  that,  althinigh  the  larvae,  at  least  of  B. 
Irigonncrplialiim,  seem  to  be  capable  of  penetrating  under  cer- 
tain conditions  (Ortlepp,  1937,  p.  2(17),  they  do  not  clo  so  as 
re.idily  as  other  hookworm  larvae  (Cameron,  1923;  Schwartz, 
192.'>),  and  normally  infect  by  mouth.  Although  most  of  the 
hookworms  ;ire  able  to  infect  the  host  by  mouth  as  well  as 
through  the  skin,  and  may  even  be  able  to  dispense  with  the 
parenteral  migration  (see  above),  Ortlepp  (1937)  was  unable 
to  cause  infection  in  sheep  by  the  oral  route  with  larvae  of 
Caigeria  pacliy.scrli.i.  Most  other  members  of  the  Strongy- 
loidea and  Trichostrongyloidea  fail  to  i)enetrate  the  skin  al- 
though a  few  {Slcphaiiiiriis  deniattis,  Nippostrongylux  miirix, 
Langixlriata  mii.seiili,  Trichostrongyliin  caJcaralus)  are  able  to 
do  so.  Other  species  of  Trirhostrongylux  apparently  do  not 
penetrate  the  skin.  Xippo.ilroiigyhix  miirix  is  almost  wholly 
dependent  upon  skin  penetration  ( Vokogawa,  1922),  whereas 
for  Langiatriaia  miisciili  oral  infection  is  probably  more  impor- 
tant in  nature   (Schwartz  and  Alicata,  1936). 

The  great  majority  of  the  worms  belonging  to  the  groups  we 
are  considering  normally  enter  the  host  by  mouth,  with  con- 
taminated water  or  food.  In  most  cases  the  larvae  climb  up  on 
living  vegetation  and  are  more  or  less  resistant  to  desiccation. 
This  is  true  of  all  the  Strongylidae  so  far  as  known  (except 
Stephaniinix),  and  all  of  the  Trichostrongyloidea  with  the  ex- 
ception of  the  few  mentioned  in  the  preceding  paragraph,  and 
OUiiIanus. 

The  development  within  the  host  involves  varying  degrees 
and  types  of  migiation.  Skin-penetrating  larvae  usually  follow 
the  route  described  above  for  ancylostoraes,  but  Schwartz  and 
Alicata  (1936)  showed  that  the  larvae  of  Longislriata  muscnU 
do  not  normally  do  so;  they  appear  in  the  stomach  within  a 
few  hours  after  skin  penetration,  and  in  the  intestine  soon  after 
that,  but  they  were  not  found  in  the  liver,  lungs  or  stomach 
walls.  Their  actual  route  was  not  determined.  In  the  case  of 
this  worm,  whether  infection  is  by  skin  or  mouth,  the  entire 
development  takes  |)lace  in  the  intestine,  contrary  to  what 
happens  in  other  skin-penetrating  £orms,  even  in  the  nearly 
related  Xippo.itrongyliis. 

Nematodes  infecting  by  mouth  may  or  may  not  migrate  via 
the  blood  stream.  Most  of  the  Trichostrongyloidea  (e.g. 
Cooperia,  OrnithoxtroiigyJiis,  Ostcrtagia,  Obeliscoidcs,  Graphid- 
iiiin.  Eacmonchu.^,  Hyoxtrougyliis,  most  species  of  Trichostrong- 
his,  Xematodinis)  perform  no  migration  at  all  beyond  a  more 
or  less  temporary  invasion  of  the  glands  or  crypts  of  the 
stomach  or  duodenum.  Some  forms,  e.g.,  Ornilhostrongybis 
qiiadriradiatiia,  may  reach  the  adult  stage  of  development  as 
carlv  as  the  third"  or  fourth  day  after  infection  (Curillier, 
1937). 

The  Strongylidae  show  various  gradations  from  invasion 
of  the  circulatory  system  and  transportation  with  the  blood,  to 
mere  temporary  invasion  of  the  glands.  Of  the  three  common 
species  of  Strongylus  in  horses  each  shows  characteristic  fea- 
tures in  its  migration,  the  larvae  of  S.  vulgaris  being  found  in 
aneurisms  in  the  anterior  mesenteric  vein,  those  of  S.  ideniatus 
under  the  peritoneal  walls  of  the  abdominal  cavity,  and  those 
of  S.  equinus  in  liver  and  pancreas.  According  to  the  usually 
accepted  view  (see,  for  example,  Xeveu-Lemaire,  19.36)  .S.  vtil 
garis  penetrates  the  walls  of  the  jntestine  and  migrates  through 
the  body  via  the  circulatory  system,  passing  through  the  capil- 
laries of  both  liver  and  lungs  to  be  distributed  all  over  the  body 
by  the  systemic  arterial  circulation.  Ninety  percent  stop  in  the 
anterior' mesenteric  artery,  to  the  walls  of  which  they  adhere 
by  using  the  mouth  as  a  sucker.  The  resulting  irritation  leads 
to  the  formation  of  an  aneurysm  and  thromboses.  Here  they 
remain  for  .")  months,  meanwhile  growing  and  passing  through 
two  molts;  one  at  a  length  of  3  to  4  mm,  the  other  at  a  length 
of  7  to  10  mm.  Having  jiassed  the  final  molt  they  release  their 
holds  and  are  carried  by  the  blood  stream  to  the  walls  of  the 
cecum  or  colon.  They  remain  imbedded  in  the  walls  in  little 
nodules  under  the  mucosa  for  about  a  month,  and  finally  make 
their  exit  into  the  lumen.  Olt  (1932)  thinks  that  the  normal 
migration  is  via  the  lungs  and  trachea  as  in  the  case  of  hook- 
worms, but  that  some  larvae  burrow  through  the  intestinal 
walls  and  l)etween  the  laminae  of  the  mesenteries  until  they 
reach  a  large  bloodvessel.  If  this  is  a  large,  heavy-walled 
vessel  the  slow  jiassage  through  it  leads  to  inflammation  and 
the  characteristic  aneurysms.  Wetzel  and  Enigk  (1938a),  on 
the  other  hand,  believe  they  have  convincing  evidence  that   no 


Fig.   18,!.     STROiVOTLUS  TULGARIt: 

Verminous  aneuvvstns  jiffecting  the  anterior  mesentei'ic 
Foster  &  Clark,  1937.  .\i>i.  J.  Tniii.  Med.  v.  17   (1). 


artery.     After 


Strongj/lus  larvae  migrate  via  the  hiiigs  and  trachea,  but  under- 
go tlieir  whole  dfveloptueut  within  tlic  abdominal  cavity. 

S.  edentatus  larvae  penetrate  the  walls  of  the  intestine  and 
the  majority  come  to  rest  under  the  peritoneum,  though  the 
route  followed  in  reaching  this  location  has  not  been  traced. 
Some,  probably  carried  by  the  blood  stream,  reach  the  liver 
and  lungs.  After  about  3  months,  during  which  they  grow 
much  larger,  the  larvae  migrate  to  the  roots  of  the  mesenteries 
and  travel  between  the  laminae  to  the  walls  of  the  cecum  and 
colon.  Here  they  become  lodged  for  about  a  month  in  large 
subserous  liemorrliagic  nodules  wliich  eventually  open  into  the 
lumen  of  the  intestine. 

S.  equiniis  larvae  penetrate  the  walls  of  the  intestine  and 
make  their  way  to  the  liver  and  pancreas.  It  has  generally 
been  assumed  that  they  arrive  in  these  places  via  the  blood 
stream,  but  Wetzel's  observations  (I.e.)  throw  doubt  on  this. 
After  development  to  the  fourth  larval  stage  they  return  to  the 
walls  of  colon  and  cecum,  again  by  an  undetermined  route,  and 
continue  their  growth  in  nodules  in  the  walls  of  these  organs. 
After  reaching  the  final  stage  of  development  by  a  fourtli  molt 
they  pass  into  the  lumen. 

The  Trichoneminae  of  horses  are  believed  not  to  migrate  out 
of  the  intestine  at  all.  Many  of  them,  jierliaps  all,  penetrate 
into  the  walls  of  the  mucosa  where  they  develop  in  nodules.  They 
undergo  the  tliird  molt  when  about  1  mm  long,  becoming  what 
Ihle  and  Ocirdt  (1923)  call  "Triehonema"  larvae,  provided 
witli  a  provisional  moutli  capsule.  Tlie  final  molt  occurs  in  the 
lumen  of  the  intestine. 

Trioilontopliorus  tcnuicolUs-  is  believed  by  Ortlepp  (102.T)  to 
develop  directly  in  the  lumen  of  the  cecum  and  colon,  without 
even  temporarily  burying  itself  in  the  mucosa.  He  was  never 
able  to  find  larvae  of  this  species  in  nodules.  However,  only 
fourtli  stage  larvae  were  found,  and  there  is  nothing  in  Ort- 
lepp's  observations  to  preclude  a  hookworm-like  migration  via 
lungs  and  trachea  on  the  part  of  the  third-stage  larvae. 

The  Oesoidiagostomiuae  have  a  life  cycle  in  the  host  essen- 
tially the  same  as  that  of  the  Trichoneminae,  the  young  worms 
tending  to  Ijuvy  themselves  in  the  mucosa,  where  tliey  cause  the 
formation  of  cysts  or  nodules.  Here  thej-  undergo  their  devel- 
opment to  the  final  stage,  emerging  into  the  lumen  of  the  intes- 
tine at  about  the  time  of  the  final  molt,  or  in  some  cases  even 
later,  when  they  have  grown  to  a  length  of  4  or  5  mm. 

According  to  Spindler  (1933),  Oexophagostomnm  quadrix- 
plmilatum  (=  loiigicaudiim)  of  pigs  produces  inflamed  liipiefy 
ing  cysts  within  4.S  hours  after  infection,  and  the  larvae  begin 
escaping  into  the  Inmen  after  aliout  17  days.  Similar  inflamed 
cysts  are  produced  by  most  other  species  of  oesophagostomes, 
but  Goodey  (1924)  failed  to  observe  tlieiu  in  experimental  in 
feetions  with  0.  dcntatiim  and  Schwartz  (1931)  saw  onl}'  small 
noninflamcd  nodules  at  the  site  of  attachment  of  adult  worms 
of  this  species  in  contrast  to  the  inflamed  lesions  caused  by 
quadrispiniilatum.  Chabcrtia  oviniis,  though  nearly  related  to 
Oesophagostotniim,  also  fails  to  develop  in  submucous  nodules. 

Stephaiturus  diniatiis,  (see  Schwartz  and  Price,  1932;  Ross 
and  Kauzal,  1932)  whether  entering  by  skin  or  mouth,  migrates 


Fig.    184.     OESOPHAGOSTOMVU    BIFVKCUM    AND 
METASTRONaTLUS  S'ALMI 

A — Nodules  of  Oesophagoatomum.  bifurcum  in  the  large  intestine  of 
an  African  (after  Brunipt).  B-E — Metnstrongylns  salvii  (B — Egg  with 
fully  developed  embryo;  C — Newly  hatched  first  stage  larva;  D — First 
stage  larva  undergoing  first  molt;  E — Second  stage  larva  undergoing 
second  molt  while  still  enclosed  within  the  cuticle  of  first  molt).  A.  after 
Chandler.  1940  (fig.  146)  Int.  to  Parasit.  B-E,  after  Alicata,  1!):!5, 
U.S.D.A.  Tech.    Bull.   489. 


to  the  liver  via  the  blood  stream.  The  third  molt  occurs  about 
70  hours  after  infection,  and  the  larvae  have  a  provisional 
mouth  capsule.  Normally  such  larvae  escape  from  the  capil- 
laries in  the  liver  and  wander  in  the  hepatic  parenchyma  until 
they  reach  the  surface  capsule.  They  wander  under  this  for  a 
time  but  eventually,  3  months  or  more  after  infection,  break 
free  into  the  body  cavity  and  make  their  way  to  the  perirenal 
fat  tissue,  perforating  the  walls  of  the  ureters  to  establish  con- 
nection with  the  outside  world.  They  tliemselves  become  en- 
closed in  capsules  of  host  tissue. 


II.    METASTRONGYLOIDEA 

In  this  supeifamily  of  the  Strongylina  the  early  development 
follows  somewhat  different  patterns  from  that  of  the  other 
members  of  the  suborder,  except  in  a  few  instances  (e.g., 
Strongijlacaniha  resembles  Dictyocaidus  in  hatching  and  then 
reaching  the  infective  stage  without  feeding  or  growing,  and 
the  Sj'ugamidae  also  resemble  Dicti/ocaulus  in  having  optiiuial 
transport  hosts). 

Three  principal  types  of  development  occur  among  the  Mcta- 
strongyloidea :  (1)  the  Dicfi/ocaidus  type,  in  which  the  larvae 
go  through  two  molts  and  reach  the  infective  stage,  surrounded 
by  one  or  both  shed  cuticles,  without  feeding  or  growing;  (2) 
the  Metastrongylus  type,  in  which  the  first-stage  larvae  con- 
tinue their  development  after  ingestion  by  earthworms,  and 
(3)  the  Prutostrongylus  type,  in  which  the  first  stage  larvae, 
attracted  by  the  mucus  of  snails  or  slugs,  continue  their  devel- 
opment after  entering  the  slime  glands  in  the  foot  of  these 
molluscs,  and  becoming  encapsulated  in  the  muscular  connec- 
tive tissue  under  the  epithelium. 


I.     Du-i'YOrwi.is  si'P, 

Tho  ogRS  of  /'.  filiiriii  iiiiil  l>.  rni/xin/.v  Iwitcli  in  tlie  Inoiulii. 
or  at  least  in  tlic  iiitostino,  as  tlii'v  aro  loaviiiR  the  body  of  tin' 
dotiiiitivo  liost,  Imt  tliosi-  of  />.  nrnfiilili,  aiTiiidiiiu  to  Wi't/.il  ,inii 
Kiiigk  (IS'.'tS)  fail  to  liatoli  in  ttio  UinRS,  anil  iisually  do  mil 
liati-li  nntil  a  few  lionrs  after  leavinR  tlie  body.  The  first  nioll 
nsiially  takes  plaee  at  room  temperature  in  from  1  to  ;;  days, 
anil  the  seeond  in  from  3  days  (in  />.  anifii'lili)  to  aliimt  I'J 
days  (P.  filaria)  later,  t'snally  both  sheaths  are  present  in 
early  third  stage  larvae,  but  the  lirst  eutiele  is  eventually  lusl. 
These  infeetive  larvae  live  a  long  time  in  moist  soil  or  water, 
and  .-ire  able  to  survive  in  earthworms  if  eaten  by  them,  al 
though  they  do  not  depend  upon  the  earthworm  as  an  inter 
mediate  host.  The  use  of  earthworms  as  transport  hosts  seems 
to  be  of  less  importnnee  in  the  e.iso  of  Dictiincaidiis  than  in  the 
oa.se  of  Si/nflamux  (see  aboveK  However,  there  is  no  evidenee 
as  yet  that  DirlnoftDiliix  ean  use  as  large  a  variety  of  transiiorl 
hosts  as  ean  Siinonmiis. 


'2.      Mbri'ASTKON'CVI.US 

Mi'taslroiiffjiiu.i  ilontiatiui  (=  apri),  M.  .salmi,  and  Chornt 
.ilrotiffiilii.t  pudcndotictii.i.  The  eggs  of  these  worms  eontain 
fully  developed  embryos  when  deposited.  .\lthinigh  usn.-illy 
stated  to  liateh  in  the  bronchi  or  intestinal  tract  during  passage 
out  of  the  definitive  host,  Alieata  (10.S.">)  found  that  they  are 
usually  passed  in  the  feces  unhatched,  and  remain  unhntehed 
until  taken  into  the  bod.v  of  a  susceptible  intermediate  host. 
The  eggs  or  embryos  nia.v,  however,  remain  viable  for  '.i  months 
in  moist  soil. 

When  ingested  by  earthworms  (species  of  Jlrloilriliis  ,iiul 
I.iimbricus)  the  larvae  burrow  into  the  walls  of  the  esophagus 
and  proventriculus  of  these  hosts.  Alieata  has  found  them  there 
K!  hours  after  exposure  to  infection.  They  also  enter  the 
circulatory  system  and  may  be  found  in  the  hearts,  but 
Schwartz  and  Alieata  (1!)2!0  showed  that  migration  via  the 
blood  stream  was  not  an  essential  part  of  the  life  cycle  of  this 
worm  in  its  intermediate  host.  In  the  earthworm  the  first  molt 
occurs  about  8  to  10  days  or  more  after  infection,  and  the 
second  one  a  few  days  later,  this  molt  beginning  before  the 
first  cuticle  has  been  shed.  The  seeond  cuticle  is  retained  by 
the  third  .stage  larvae,  which  are  now  infective.  The  larvae  do 
not  si)ontaneou.sly  leave  the  host,  and  an  earthworm  may  re 
main  infective  over  winter,  and  probably  at  times  for  several 
years.  Upon  death  of  the  earthworms  the  larvae  are  able  to 
survive  for  2  weeks  in  moist  soil.  Pigs  become  infected  by 
eating  infected  earthworms  or  liberated  infective  larvae.  After 
ingestion,  according  to  Hobmaier  and  Hobmaier  (li)29),  they 
migrate  via  the  lymphatics  or  blood  stream,  und  rgoing  the  third 
molt  in  mesenteric  lymph  glands,  and  then  proceed  via  the 
lymjihatic  and  blood  .systems  to  the  lungs,  where  they  become 
mature  after  a  fourth  .■ind  final  molt. 


?,.     Pkotostrongvi.inak 

.Ml  the  members  of  the  family  Protostrongylinae  resemble 
one  another  in  requiring  molluscs  as  intermediate  hosts.  In 
all  cases  the  embryonated  eggs  hatch  before  leaving  the  body, 
or  soon  after,  and  the  first  stage  larvae  may  live  in  soil  or 
water  for  several  weeks,  but  without  further  development.  The 
larvae  are  attracted  by  the  slime  of  molluscs,  and  upon  coming 
in  contact  with  a  mollusc  they  creep  into  furrows  in  the  foot, 
whence  they  penetrate  into  mucous  glands,  burying  themselves 
in  the  muscular  connective  tissue  under  the  e])itheluni.  Here 
they  coil  up  and  soon  become  enclosed  in  a  tubercle  resulting 
from  encapsulation  by  the  host.  The  fir.st  molt  usually  takes 
place  after  a  week  to  10  days  at  room  temperature,  the  larvae 
having  grown  comparatively  little  in  length,  but  having  become 
thicker.  The  second  molt  usually  takes  place  in  from  10  or 
12  days  (Aelurostrongylux,  MiicUcriti.s,  Crenosoma)  to  4  or  .t 
weeks  (Elaphostrongylus),  after  which  the  larvae  are  infective 
when  molluscs  containing  them  are  eaten.  In  most  cases  little 
specificity  is  shown  with  respect  to  the  species  of  molluscs 
utilized  as  intermediate  hosts,  although,  possibly  because  of 
the  habits  of  the  snails,  certain  species  seem  to  be  of  prime 
imjiortance.  I'mtdstroiij/i/liis  riifisccns  develops  primarily  in 
Ilelicella  (Hobmaier  and  Hobmaier,  1930)  ;  Miiellfriiis  capil- 
larix  can  utilize  a  great  variety  of  snails  and  slugs,  :ilthuug]i 
Pavlov    (1937)   found   only   Ilelicella  obxia  to  be   important    in 


Fig:.    IH.-,      DEVELOPMENT    OV     l'R(  ITOSTKdXi;  Yl.I  X  AE     IN 
MOLLU.S(.'S 

Larvjte  of  MueUerUi^  capiUnris  in  AgrUtlimtix  aurfittiH.  X — Larvae  in 
furrow  of  foot  of  mollusk  a  few  hours  after  infection;  B — On  first 
day  of  infection  (sagittal  section);  C — Coiled  larva  in  foot  on  second 
day  of  infection  (horizontal  section)  ;  D — I^arvae  in  sole  of  foot  on  16th 
(liiv  of  infection.     .After  Hobmaier,   1934,  Ztschr.  f.   Parasitenk,  v.  6   (5). 


.Jugoslavia;  Aelumstrongyliis  abstriistis,  reported  by  Cameron 
(1927)  to  utilize  mice  as  intermediate  hosts,  apparently  er- 
roneously, according  to  Hobmaier  and  Hobmaier  (1935)  devel- 
ops in  a  variety  of  snails  and  slugs,  but  Epiphragviophora 
proved  most  suitable.  Other  forms  in  which  a  variety  of  mol- 
luscs have  been  shown  to  serve  as  hosts  are  Aelurostrongi/liis 
fatcifonnis  (Wetzel,  1938),  Crcnonoma  viilpis  (Wetzel  and 
Miiller,  1935),  and  Elaphostrongylus  odocoilei  (Hobmaier  and 
Hobmaier,  1934). 

Hobmaier  (1934)  believes  that  the  utilization  of  molluscs  as 
intermediate  hosts  by  the  Protostrongylinae  grew  out  of  the 
habit  of  the  larvae  of  seeking  protection  from  desiccation  in 
the  slime  of  the  molluscs.  This  predilection  for  slime  extends 
to  the  period  of  passage  through  the  colon  of  the  definitive 
host,  for  the  larvae  are  commonly  found  burying  themselves 
in  the  intestinal  mucus  and  thus  becoming  located  on  the  sur- 
face of  fecal  pellets  instead  of  iuside.  In  this  position  those 
larvae  which  were  not  protected  from  desiccation  by  the  mucus, 
and  subsequently  the  ti.ssues,  of  snails  would  fail  to  survive. 
The  larvae,  as  Hobmaier  points  out,  differ  widely  in  their 
habitat  in  the  snail  from  the  parthenitae  of  flukes,  which  prob- 
ably develop  in  snails  because  these  were  ancestral  hosts. 
Whereas  fluke  parthenitae  are  true  internal  parasites  of  mol- 
luscs, lungworm  larvae  are  scarcel.v  more  than  external  para- 
sites. Larvae  ingested  by  snails  usually  pass  all  the  way 
through  the  alimentary  canal  and  fail  to  develop. 


277 


ASCARIDINA 
OXYUROIDEA 

1.     Enterobius  vermicularis 

111  spite  of  the  fact  that  the  oxyurid  type  of  life  cycle  is 
the  simplest  and  probably  the  most  primitive  of  any  found 
among  nematodes  parasitic  in  vertebrates,  a  search  of  the 
literature  has  failed  to  reveal  a  single  instance  in  Avhich  a  de- 
tailed molt  by  molt  account  of  the  life  cycle  has  been  descrilied. 
The  life  C3'cle  of  Entcrobiuf:  vennicidaris,  so  far  as  it  is  knoivn, 
will  serve  as  an  example  of  its  type. 

The  adult  female  worms,  with  the  uteri  filled  with  develop- 
ing eggs,  live  in  the  lower  part  of  the  large  intestine  and  par- 
ticularlj'  in  the  rectum.  They  do  not  ordinarily  deposit  their 
eggs  in  the  lumen  of  the  intestine,  but  crawl  out  of  the  anus 
and  deposit  them  in  the  perianal  region,  leaving  trails  of  eggs 
as  the}'  creep  about.  Contact  with  air  is  apparently  a  stimulus 
to  oviposition  (Philpot,  1!>24).  Although  they  frequently  re- 
main outside  the  anus  and  release  the  eggs  in  showers  when  the 
body  ruptures,  MacArthur  (1930)  and  others  state  that  they 
commonly  retreat  into  the  rectum,  to  repeat  their  egg-laying 
expeditions  out  of  the  anus  over  and  over  again,  particularly 
at  night. 

The  eggs  when  deposited  by  the  females,  or  contained  in  the 
uterus  of  females  which  have  voluntarily  migrated  out  of  the 
intestine,  are  fairly  uniformly  in  the  "tadpole"  stage  of  de- 
velopment, apparently  being  unable  to  progress  beyond  this 
point  without  free  oxygen.  Within  6  hours  after  leaving  the 
body  they  develop  a  coiled  larva  (ring  and-a-half  embryo) 
which  is  infective.  According  to  Brumiit  (1922)  the  larva 
undergoes  no  molt  before  hatching  nor,  according  to  Philpot 
(1924),  as  a  free  larva  in  water.  However,  Alicata  (1934)  sug- 
gested that  a  molt  within  the  egg  shell  might  be  general  for 
the  Asearidina,  and  Entcrohin.i  might  well  be  reexamined. 
Chitwood  (personal  communication)  believes  he  has  seen  a 
molt  in  the  egg,  and  thinks  there  may  be  two. 

Development  of  the  larva  in  the  egg  will  occur  in  oxygenated 
water,  and  in  this  medium  the  larvae  commonly  emerge  in 
from  9  to  24  hours  at  37°  C,  but  they  only  live  for  a  few  days, 
so  it  is  evident  that  water  cannot  be  an  important  vehicle  of 
infection.  Exposed  to  air  a  considerable  proportion  of  the 
eggs  survive  for  at  least  6  days  at  humidities  above  62  percent 
(Jones  and  Jacobs,  1939). 

When  ingested  the  eggs  hatch  in  the  stomach  or  intestine, 
and  the  worms  live  during  the  early  part  of  their  development 
in  the  lower  part  of  the  small  intestine,  cecum  and  upper  por- 
tions of  the  colon,  not  infrequently  invading  the  appendix. 
Heller  (1903)  states  that  there  definitely  are  two  molts  in  the 
small  intestine,  and  probably  three.  Chitwood,  (personal  com 
munication)  reports  having  seen  a  molt  in  the  epithelium  of  the 
appendix.  By  analogy  with  other  nematodes  there  is  probably 
a  total  of  four  molts. 

Although  the  worms  have  repeatedly  lieen  reported  as  bur- 
rowing into  the  mucous  membranes,  especially  of  the  appendix 
(Penso,  1932),  it  seems  probable  that  this  is  a  habit  only  of  the 
fourth-stage  larvae.  Chitwood  (personal  communication)  re- 
ports having  found  the  fourth-stage  larvae  in  sections  of  the 
appendix.  He  has  observed  a  definite  period  6  to  9  days  after 
infection  when  symptoms  of  invasion  appeared,  followed  4  to  7 
days  later  by  migration  of  the  worms  from  the  anus.  Exposure 
to  air  after  operation  would  account  for  the  deposits  of  eggs 
which  Penso  reports  and  figures  deep  in  the  walls  of  the  ap 
pendix. 

There  has  been  a  large  amount  of  discussion  as  to  whether 
internal  autoinfeetion  by  the  worms  can  occur.  The  fact  that 
infections  persist  even  for  many  years  in  spite  of  the  most  care- 
ful efforts  to  prevent  reinfection  from  the  anus  via  the  hands 
has  lent  support  to  this  idea.  However,  the  demonstration  by 
Lentze  (193.5),  and  Nolan  and  Reardon  (1939)  of  the  ease 
with  which  airborne  infectious  can  occur  seems  sufficient  to 
account  for  the  persistence  of  infections.  On  the  other  hand, 
Zawadowsky  and  Schalimov  (1929),  Lentze  (193.5)  and  others 
have  called  attention  to  the  failure  of  development  and  infec 
tion  of  eggs  or  embryos  left  under  conditions  such  as  exist  in 
the  lumen  of  the  large  intestine.  It  would  be  difficult  to  say 
that  internal  auto-infection  could  never  occur,  but  the  evidence 
is  all  in  favor  of  the  view  that  if  it  does  occur  it  is  an  abnormal 
and  exceptional  condition. 

Copulation  of  the  young  adult  worms  usually  takes  place  in 
the  upper  parts  of  the  colon  or  in  the  cecum,  where  the  males 
live  for  some  time.  The  females  do  not  migrate  to  the  rectum 
until  they  contain  developing  eggs.  Eipe  females  begin  to  ap- 
pear about  15  days  after  infection. 


2.  Other  Oxvuroide.v 

The  life  cycles  of  other  Oxyuridae  are  the  same  in  essential 
features,  but  differ  in  details.  Oxyuris  eqiii  differs  in  that  the 
fourth-stage  larva  has  a  special  structural  development  of  the 
anterior  portion  or  "corpus"  of  the  esophagus  which 
enables  the  larva  to  use  it  as  a  highly  developed  buccal 
capsule  for  adhering  to  the  mucosa  (Wetzel,  1931).  The  ripe 
females  of  this  species  creej)  out  of  the  anus  as  do  those  of 
fJntcrobiua.  but  this  is  probably  not  true  of  forms  parasitic  in 
rodents.  The  fourth  stage  larva  of  Dfnnatoxys  vcUgera  is  also 
provided  with  a  special  structure  for  adhering  to  the  mucosa, 
but  in  this  case  the  end  is  accomplished  by  the  development  of 
four  conspicuous  hooks  on  the  head  (Fig.  156,  X,  Y)  (Dikmans, 
1931),  which  is  buried  in  the  mucosa  (Wetzel,  1932).  These 
specializations  for  maintaining  a  position  in  the  colon  are  of 
interest  as  indicative  of  a  need  for  some  sort  of  protection 
against  expulsion  from  the  body  before  maturity  is  reached,  a 
need  which  may  perhaps,  as  has  already  been  suggested,  have 
led  to  a  deeper  burrowing  into  the  mucosa  and  ultimately  to  a 
parenteral  migration. 

According  to  Philpot  (1924),  Aspiculuris  ictraptcra  has  a 
life  cycle  strikingly  like  that  of  Eiitrrobitix,  differing  only  in 
the  earlier  stage  at  which  the  eggs  cease  development  before 
expulsion,  and  their  failure  to  hatch  outside  the  body.  Sypliacia 
obvelata  differs  in  that  the  eggs  have  developed  embryos  when 
they  leave  the  host.  All  stages  of  development  from  the  young- 
est larva  to  adult  can  be  found  in  the  cecum  of  naturally  in- 
fected mice,  and  are  strikingly  similar  to  those  described  and 
figured  for  Aspiculuris.  Tachygnnctria  loju/icoUis  and  T.  ilcn- 
laia  definitely  undergo  a  molt  before  hatching  from  the  egg. 
PassaJunis  cimbiniius,  according  to  Penso  (1932),  is  capable  of 
internal  auto-infection;  the  gravid  females  burrow  into  the 
mucosa  to  deposit  their  eggs,  and  the  larvae  subsequently 
emerge  to  continue  their  development.  Penso,  however,  postu- 
lates a  similar  behavior  on  the  part  of  Entcrobitis  vermicularis, 
and  thinks  that  Wetzel's  observations  on  Dcrmatoxys  vcUycra 
were  in  error,  the  larvae  with  buried  heads  being  emerging 
from,  not  entering,  the  mucosa,  .\lthough  Piissalurus  ambigiins 
may  sometimes  deposit  its  eggs  in  the  mucosa,  Penso 's  observa- 
tions need  to  be  extended  before  this  can  be  accepted  as  a 
normal  or  usual  procedure. 

Probstmayria  rivipara  (Atractidae)  is,  so  far  as  known  at 
present,  unique  among  nematodes  that  arc  known  to  be  obliga- 
tory parasites  of  vertebrates  in  reproducing  continuously  gen- 
eration after  generation  in  a  single  host.  It  is  among  the. 
nematodes  what  the  Pupipara  are  among  the  Diptera,  or  Tiiiiga 
among  fleas.  Its  larvae  hatch  in  the  uterus  and  grow  almost 
to  the  size  of  the  parents  before  being  born  (vide  Ransom, 
1907).  They  resemble  the  parents  except  for  lack  of  develop- 
ment of  the  genital  organs.  No  stage  of  development  is  known 
outside  the  body  of  the  host.  Transfer  to  new  hosts  is  believed 
by  Jerke  (1902)  to  be  accomplished  by  contamination  of  food 
or  water  by  worms  jiassed  in  the  feces;  such  worms,  he  says, 
remain  alive  in  feces  for  several  days. 


ASCARIDOIDEA 

In  the  Asearidoidca  there  are  ahvays  one  or  more  molts  be- 
fore the  embryos  leave  the  eggs  and,  with  few  if  any  excep- 
tions, there  is  a  phase  of  burrowing  into  the  mucosa,  and  in 
many  cases  more  extensive  migration  from  the  lumen  of  the  in- 
testine to  the  body  cavity,  liver,  lungs  or  other  tissues  of  the 
definitive  or  of  an  alternating  host. 

Heter.\kidae 

The  members  of  this  family  bridge  the  gap  between  the  typi- 
cal oxyurid  life  cycle  and  that  of  the  ascaridids.  At  least  one 
sjiecies,  Subulura  brumpti  (see  below),  has  become  dependent 
upon  an  intermediate  host. 

The  life  cycle  of  Hetcrakis  gallinac,  according  to  Clapham 
(1933),  is  of  the  typical  oxyurid  type  except  that  the  females 
do  not  migrate  out  of  the  anus  to  deposit  eggs,  but  oviposit  in 
the  ceca.  Earlier  writers  have  reported  burrowing  and  encyst- 
nieiit  in  the  cecal  walls,  or  penetration  into  cecal  glands,  but 
Clapham  was  unable  to  find  any  evidence  of  migration  or  bur- 
rowing, the  larvae  passing  directly  to  the  ceca  within  48  hours 
and  maturing  in  the  lumen.  The  first  molt  occurs  in  the  egg 
(Alicata,  1934),  the  third  not  until  10  days  after  infection. 

Other  species  of  Heterahis  {isolonche,  beramporia)  burrow 
into  the  intestinal  mucosa  at  some  time  during  development 
and  reach  maturity  in  tumors  which  form  around  them.  This 
possibly  is  the  first  step  in  the  direction  of  the  Ascaris  type  of 
life  cycle. 


DEVELOPMENT  OF  THE  ASCARIDIXA 


A — PuJtsaiuruK  nmbiguuit.  B — "0.ri/uri»"  brer-icnudn  showing  emer- 
gence area  and  embryo  in  outline  after  inculmtinn  for  64  hours  at  22° 
C.  C-il — Aitpictiluris  tetraptera  (C — EgK  incubated  in  water  24  hours; 
D — 43  hours;  E — 08  hours;  F — Larva  from  intestine  4  hours  after  feed- 
ing; G— Larva  from  cecum  4  hours  after  feeding;  H — After  18  hours; 
I — After  44  hours;  J-K — 10  days  after  feeding;  J,  male.  K.  female; 
L-M — 18  day*;  after  feeding.  L.  female.  M.  male).  N-Q — Supfiarin 
obvelata  (N — Uterine  egg  containing  mature  emt>ryo ;  O — Hatched  em- 
brj"o;  P — Youngest  larva  found  in  cecum ;  Q — Male  measuring  .8 1 
mm.).  R — EnierohiuM  vermiculariM,  larva  three  days  after  hatdiing  in 
Ringer's  solution.  S-T — Derma  toxi/s  vpUgern  (S — Head.  T- — ^Head. 
fourth  stage).  U — Probstmayria  riripara,  lateral  view  of  female  am- 
taining  a  well  developed  embr>'o.  a  second  less  developed  and  two  eggs. 
V-Y — Aficaridia  gaUi  ( V — cephalic  extremity  of  second  stage  larva 
showing  oral  prominence;  W — Second  stage,  newly  hatched;  X — Tail  of 
third    stage  female   showing   preanal    swelling;    Y — Tail   of   fourth    stage 


male).  Z-CC — Ancurin       himbrwoides        (Z — Second       stage        (newly 

hatched);  AA — Third  stage;  BB — Fourth  stage  (21  days);  CC — Fifth 
stage  (29  days  old).  I)I>-EE — Cosmocercoides  dukae  (DD — Newly 
hatched  larva;'  EE — Infective  larva).  FF-II — Contracaecum  aduncuni 
(FF-GG — Hatched  larvae;  HH — Anterior  end  of  larva  armed  with 
boring  tooth;  I1-— Larva  from  body  cavity  of  Ascartui  bifilonu).  JJ — 
Subulura  brt/wpti,  encysted  infective  larva  recovered  from  body  cavity 
of  the  beetle  Alphitobtufi  diaperinus.  KK — Hetarakis  guUinae,  infec 
tive  larva  found  newlv  hatched  in  the  small  intestine.  A-R.  after  Phil- 
pot.  J.  Helminth.,  v.  2  (5),  pp.  239-252.  S-T.  after  Dikmans.  1931. 
Trans.  Amer.  ilic.  Soc.  v.  50  (4).  U,  after  Ransom,  1907,  Trans. 
Amer.  Mic.  Soc.  v.  27.  V-Y,  after  Roberts.  19^7.  Bull.  2  An.  H.  Sta. 
Queensland.  Z-CC.  after  Roberts.  1934,  Bull.  1.  An.  H.  Sta.  Queens- 
land. DD-EE.  after  Harwood.  1930,  J.  Parasit.  17.  FF-II,  after 
Markowski,  1937,  Hull.  Acad.  Polon.  Ser.  B.  J.7.  after  Alicata,  1939. 
J.  Parasit.  25.     KK,  after  Ctapham,  1933,  J.  Helminth,  v.  11    (2). 


279 


V-^^r^:  :■" 


Dermtttoxys    veliffern,      Phofnmicrograph    of    fourth    stage   larva    pene- 
trating mucous  membrane.     After  Wetzel.   li>31.  J.  Para.sit.  v.   18. 


Asrnriilia  finjli. 
erts.   1H:i7.   Bull. 


Fig.  188. 

Section  nf  small  intestine  showing  larva.     After  Rob- 
.\'fi.  2.      Animal  Health  Sta.  Yeerongpilly.   Queensland. 


The  life  cycle  of  Ascaridia  galli  ma.v  well  be  a  second  step 
towards  that  of  Ascaris.  As  elucidated  bj-  Ackert  (1931), 
Alieata  (1934)  and  Roberts  (1937)  this  worm  undergoes  one 
molt  in  the  egg  and  then  normally  remains  enclosed  in  the  egg 
until  infection.  There  are  three  molts  in  the  host,  the  tirst  of 
these  (second  molt)  occurring  about  (3  days  after  infection  and 
the  others  at  about  6-day  intervals  thereafter.  After  reaching 
the  third  stage,  on  about  the  ninth  or  tenth  days,  the  larvae 
Inirrow  down  between  the  villi  and  penetrate  into  the  glands  of 
Lieberkuhn,  the  posterior  ends  of  the  bodies  remaining  free  in 
the  lumen.  Itagaki  (1927)  observed  that  at  certain  seasons  in 
Japan  (midsummer  and  midwinter)  the  larvae  habitually  pene- 
trated into  the  mucosa,  about  as  described  by  Ackert  and  by 
Roberts,  causing  fibrous  nodules,  but  that  in  spring  and  autumn 
they  remain  in  the  lumen.  Roberts  reported  less  tendency  for 
the  larvae  to  burrow  into  the  mucosa  in  April  and  May  than 
in  November.  Although  on  rare  occasions  the  larvae  penetrate 
too  deeply  and  enter  the  peritoneal  cavity,  mesenteries,  liver. 
or  even  the  lungs  (Ackert,  1923;  Guberlet,  1924),  it  is  clear 
that  this  is  purely  accidental. 

Svbuhira  iriimpti.  according  to  Alieata  (1939),  has  depart- 
ed from  the  usual  heterakid  life  cycle  pattern  in  requiring  an 
intermediate  host.  This  is  the  only  member  of  the  subfamily 
Subulurinae  in  which  the  life  cycle  has  been  investigated,  and 
it  is  possible  that  the  use  of  an  intermediate  host  has  become 
general  in  this  group  as  it  has  in  the  Anisakinac. 

Alieata  was  unable  to  infect  chickens  by  feeding  embryonated 
eggs,  either  just  recovered  from  the  uteri  of  gravid  females,  or 
incubated  in  \vater  at  about  24°  C.  for  1  week,  but  succeeded 
in  producing  infection  by  feeding  naturally  infected  arthro- 
pods harboring  the  cysts  in  the  body  cavity.  The  cysts  contain 
coiled  nematodes  having  bulbed  esophagi  and  conspicuous 
esophageal  valves  as  in  the  adults  (Fig.  1S6,  JJ).  High  inci- 
dences of  natural  infection  were  found  in  the  following  arthro- 
pods collected  on  poultry  farms  in  Hawaii:  (Coleoptera)  Der- 
mestes  vulpinus,  Gojioccphalus  scriatum,  Ammoplwnis  insiilaris, 
Alphit  oh  hits    diapcriniis ;    and    (.Dermaptera)    EiibonlJia    ainin- 


lipes.     Encysted  larvae  were  also  found  in  grasshoppers   (Con- 
ocephalns  aallalor)  l.'i  days  after  experimental  infection. 

CoSJIOt'ERCIDAE 

At  least  some  of  the  members  of  this  family  resemble  the 
typical  Ascarididae  in  that  the  larvae,  burrowing  into  the 
mucosa,  enter  the  circulatory  system  and  reach  the  lungs,  where 
they  escape  into  the  air  spaces  and  eventually  make  their  way 
back  to  the  intestine  via  trachea  and  esophagus.  They  differ, 
however,  in  having  a  free  living  phase  outside  the  body.  Cos- 
mocerca  trispinosa  (=  Nematoxys  longicaiida)  has  long  been 
known  to  occur  in  the  lungs  of  salamanders  in  an  immature 
form,  and  in  the  intestine  as  an  adult.  Von  Linstow  considers 
its  growth  in  the  lungs  as  analogous  to  the  growth  of  Ani- 
sakinae  in  an  intermediate  host.  Harwood  (1930)  found  that 
Cosmocercoides  dukac  (his  Oxi/somatium  variabilis)  undergoes 
a  molt  after  5  days  of  free  life  outside  the  bod.v  and,  although 
his  observations  on  development  after  infection  are  inconclu- 
sive, that  the  larvae  are  found  in  the  lungs  not  only  after  sub- 
cutaneous inoculation,  but  also  after  infection  by  mouth.  They 
do  not,  however,  penetrate  the  skin. 

Ascarididae 

The  ma.)ority  of  the  Ascarididae  have  a  migratory  phase  lie- 
fore  becoming  adult  in  the  intestine.  The  larvae,  burrowing 
into  the  mucosa,  enter  the  circulatory  system  and  are  cariiod 
via  liver  or  lymphatic  system  to  the  heart,  thence  to  the  lungs 
where  they  become  free  in  the  air  spaces,  and  thence  via  trachea 
and  throat  back  to  the  alimentary  canal.  Toxascaris  leonina, 
according  to  Wright  (1935),  does  not  perform  this  migration; 
the  life  cycle  is  similar  to  that  of  Ascaridia  except  that  the  sec- 
ond-stage larvae  burrow  into  the  mucous  membranes  almost 
immediately  after  hatching,  and  return  to  the  lumen  of  tlie 
intestine  after  the  third  molt,  on  the  9th  or  10th  day.  As 
shown  by  Fiilleborn  (1922)  and  others,  some  larvae  penetrate 
all  the  way  through  into  the  liody  cavity  and  enter  viscera  by 


280 


tie.  ixa. 

Aitcnris  tttitnn.     Liirva  in  sfctinn  of  iiinu.-t'  lung   1    VM-t'k  iiflt'i"  iiifei'tiori. 
AftiT  ISansoiii.   1!)20,  U.S. 11. A.  Yeailiook. 


this    louto,   :iiiil    souu'   aio    luolmlil.v    ]pii-kc'il    \ii>    :ni(l    cniicd    h.v 
the  circulatoiv  system. 

Axcarus  Iinnbricoide.s.  Long:  tlimij^lit  Ui  liave  a  liireet  devel- 
opment in  the  intestine,  Ascari.s  Iiiiiibricoidi's  was  fiist  shown  to 
undergo  a  preliniiiiaiy  migration  tluough  the  body  by  Stewart 
(1914)  ;  Stewart  found  that  eggs  fed  to  rats  migrated  to  the 
lung.s,  and  erroneously  concluded  that  rats  served  as  intcrmedi 
ate  hosts.  Shortly  thereafter  Ran.som  and  Poster  (1917)  and 
Chandler  (1918)  called  attention  to  the  probability  that  the 
migration  through  the  body  was  a  part  of  the  normal  develop- 
ment in  the  definitive  host;  experimental  proof,  with  details 
of  the  development,  was  supplied  by  Hansom  and  Foster  in 
llliO.  Details  of  the  course  of  the  migration  were  worked  out 
and  reported  by  Ransom  and  Cram  in  I'.l'Jl,  and  further  details 
were  supplied  by  Roberts    (lil34). 

The  first-stage  larva  appears  in  the  egg  on  about  the  eighth 
day  at  the  optimum  temperature  of  HO  to  33°  C,  and  the  first 
molt  occurs  in  the  egg  on  about  the  ISth  day.  Ransom  and 
Foster  (lifJO)  fir.st  observed  that  the  embryo  underwent  a  molt 
in  the  egg.  Later  Alicata  (1934)  reported  that  the  egg  is  not 
infective  until  after  this  molt;  he  also  pointed  out  that  the 
embryos  of  A-'scaridia  lineata,  Parascaris  cqiionnn,  Toxocara 
canis,  Toxa.scuris  leonina,  Heleral'is  gaUinae  and  the  roach 
oxyurid  Blatticola  blattac  also  underwent  a  molt,  a  feature 
which  may  be  common  in  the  Ascaridina  and  which  determines 
when  the  egg  has  reached  the  infective  stage. 

Normally  the  eggs  of  Ascarii  Inmbricoidcs  hatch  in  the  small 
intestine  after  lieing  swallowed,  but  they  will  sometimes  hatch 
when  implanted  subcutaneously  or  intraperitoneally  (Ransom 
and  Foster,  lfl20;  Yoshida  and  Toyoda,  1038)  or  in  artificial 
media  containing  glucose  or  various  nitrogenous  substances 
(Voshida  and  Toyoda,  I.e.). 

The  second-stage  larva  has  a  small,  sclerotized,  knob-like 
structure  at  the  anterior  end,  called  the  "boring  tooth."  The 
larvae  bore  into  the  intestinal  wall,  mainly  in  the  duodenum 
and  upper  part  of  the  .je.iunum,  after  hatching;  the  ma.jorit.v 
have  disappeared  within  2  hours.  The  ma.iorit3'  enter  the  blood 
stream  after  some  hours  and  are  found  in  the  liver  in  from  IS 
hours  to  several  days  after  infection.  A  few  apparently  enter 
lymphatics  since  they  are  sometimes  found  in  mesenteric  lymph 
glands,  but  from  here  they  seem  to  go  via  mesenteric  venules 
to  the  liver  rather  than  directly  to  the  lungs.  Within  .t  or  6 
days  all  have  left  the  liver  and  have  gone  to  the  lungs  via  the 
blood  stream;  some  appear  in  the  lungs  within  18  hours,  and 
they  may  continue  to  be  found  there  for  10  or  12  days,  al- 
though most  numerous  on  about  the  third  to  fifth  days.  Dur- 
ing the  first  2  days  of  this  migration  the  larvae  grow  consider- 
ably. About  the  fifth  or  si.^th  day  the  larvae  in  the  lungs, 
measuring  about  0.8  to  1  mm  in  length,  undergo  the  second 
molt.  The  third  stage  larva  has  three  lips  with  papillae,  l:icks 
the  boring  tooth,  has  a  highly  developed  muscular  esojihagus, 
has  the  intestiiuil  cells  packed  with  granules,  has  a  distinct 
nerve  ring  and  oval  genital  primordium,  and  a  conical  tail 
turned  dorsad  at  the  tip. 


On   the   tenth   to   twelttli   days   llie    llni<l    It    occins,  also    in 

till'  lungs.  In  the  <ipinion  of  Roberts,  althotigli  second  and 
Ihiril  stage  larvae  m.'iy  be  found  in  the  intestine  prior  to  the 
tenth  day  (Ransom  recovered  larvae  from  the  trachea  as 
early  ;is  the  third  day),  these  larvae  have  not  completed  their 
development  in  the  bmgs  an<l  probably  fail  to  I'slablisli  them- 
selves in  the  intestine  The  suggesticui  is  made  that  the  oc- 
currence of  such  l;irvae  in  the  intestine  may  indicate  unfavor- 
able conditions  in  the  lungs  resulting  from  excessive  infections. 
Roberts  found  some  hundreds  of  fourth  stage  larvae  in  the  in- 
testine on  the  14lh  aiul  21st  days,  but  no  molting  third-stage 
larvae  were  fcnmd  between  the  11th  and  14tli  days.  Fourth 
stage  larvae  are  1.4  mm  or  more  in  length.  The  cuticle  begins 
to  show  striations,  fin  like  lateral  alae  are  present,  the  lips 
resemble  those  of  the  adult,  the  esoyihagus  is  less  bulbous,  and 
the  sexes  can  be  diflCrentiated  by  a  difference  in  U'ngth  of  tail. 
Rudimentary  geiiilal  tubules  are  present  in  the  body  cavity. 

.\fter  arri\al  in  the  intestine  the  larva  grows  enormously, 
reaching  a  length  of  l(i  to  2.")  mm  2!)  days  after  infection.  Lar- 
vae undergoing  the  fourth  nudt  measure  17.3  to  22.5  mm  (Rob- 
erts). The  lateral  alae  have  become  inconspicuous,  the  genital 
tubules  and  body  wall  muscles  are  comparatively  well  devel- 
oped, and  the  cliaracteristic  features  of  the  tail  of  the  two 
sexes  are  present,  (irowth  to  maturity  and  beginning  of  reju-o- 
duction  takes  several  weeks. 

It  is  obvious  that  the  only  striking  difference  between  this 
life  cycle  and  that  of  the  heterakids  is  the  entrance  into  the 
circulatory  system  when  burrowing  into  the  intestinal  wall,  the 
consequence  of  which  is  the  migration  through  the  body  via 
liver,  heart  .and  lungs.  The  determining  factor  seems  to  be  the 
age  at  which  the  larvae  do  their  burrowing.  Eiitcrobiiis  and 
Dermatoxys,  as  we  saw,  burrow  as  fourth-stage  larvae,  and 
some  species  of  Ilclnakis  do  likewise  and  live  as  adults  in  the 
burrows;  Ascaridia  burrows  while  in  the  third  stage;  but  As- 
cari.i  burrows  immediatel.v  after  hatching  as  a  second-stage 
larva.  The  burrowing  heterakid  larvae  are  too  large  to  enter 
or  be  sucked  into  blood  vessels,  whereas  the  Asearis  larvae  can 
easily  do  so.  The  failure  of  T()xa!icari.<i  larvae  to  enter  the 
circulatory  system  except  rarely  ma.v  be  found  to  be  due  to  a 
difference  in  size,  particularly  in  the  diameter  of  the  larvae. 

Toxocara  canis  has  essentially  the  same  life  cycle  as  Ascaris 
himbriroidrs,  and  the  same  is  true  of  Neoascaris  vitulorum 
{vide  Schwartz,  1922),  of  Parascaris  equorum  (vide  Baylis, 
1923),  of  A.'icaris  coliimnaris  (vide  Goodey  and  Cameron,  1923), 
and  probably  of  all  other  A.scaridinae.  According  to  Fiilleborn 
(1921),  Toxocara  canis  is  frequently  encapsulated  in  the  tis- 
sues of  mice  or  other  abnormal  hosts,  which  thereby  become 
transport   hosts. 

Anisakin.\e 

It  has  long  been  known  that  various  members  of  this  sub- 
family occur  as  immature  worms  in  the  body  cavity,  mesen- 
teries and  other  organs  of  various  vertebrates,  and  sometimes 
invertebrates,  whereas  the  adults  occur  in  vertebrates  which 
prey  upon  these  hosts.  Although  morphological  characters 
often  suggested  affinities  between  larvae  and  adults  there 
was  little  experimental  evidence  in  support  of  them.  More- 
over the  various  larval  forms  were  not  clearly  differentiated 
from  each  other.  Baylis  (1916)  for  instance,  showed  that  a 
number  of  larval  forms  were  confused  under  the  iianu'  "Ascaris 
capsnlaria,"  which  he  believed  on  moriihological  and  distri- 
butional evidence  to  be  the  larval  form  of  "Ascaris  dccipicns" 
(now  Porrocaeciim  tircipiens).  The  same  confusion  probably 
holds  for  other  species. 

Thomas  (1937a,  1937b)  experimentally  worked  out  the  life 
cycle  of  Coiitracaccum  spiciiligcriim.  Eggs  obtained  from  the 
proventriculus  of  a  cormorant  contained  active  molted  larvae 
with  a  boring  tooth  after  being  incubated  in  water  for  5 
days,  and  on  the  sixth  day  they  molted  a  second  time  and  then 
hatched.  Many  attached  themselves  by  the  anterior  end  of  the 
sheaths,  which  seemed  adhesive,  but  the.v  swam  freely  when 
detached.  On  the  thirfi-eiith  day  a  third  molt  was  in  progress, 
with  a  cuticular  tooth  still  present.  When  swallowed  b.v  tad- 
poles or  guppies  (.Lahislis  rctici(hilits)  the  larvae  shed  their 
sheaths  and  were  found  free  in  the  intestine  or  in  the  body 
cavity.  About  3  months  later  larvae  were  found  encysted  in 
the  mesenteries;  they  had  grown  to  1.3  mm  in  length  (from 
less  than  400  m).  In  cysts  developed  by  the  host  tissues  they 
continue  to  grow  until  nearly  adult  size  is  reached.  Unlike 
most  nematodes  the  number  of  molts  is  not  limited  to  four; 
as  many  as  eight  molted  cuticles  have  lieen  removed  from  en- 
cj'sted    worms    from    a    natural    infection. 

There  is  evidence  that  when  ;in  infected  fish  is  eaten  by 
another    fish    the    larv.-ie    penetrate    the    intestinal   wall    and    re 


281 


encyst  in  the  mesentery.  This  was  observed  to  occur  when 
a  parasitized  guppy  was  fed  to  a  black  bass.  In  all  cases 
the  worms  retain  the  cuticular  "lioring  tooth"  until  the  defin- 
itive host  is  reached,  although  three  lips  can  be  seen  under 
the  cuticles  in  older  larvae.  Natural  infections  with  similar 
worms  were  found  in  several  species  of  fish  in  Illinois.  Sexual 
maturity  is  reached  only  in  birds.  Fledgling  cormorants  be- 
come infected  when  fed  on  infected  guppies.  The  larvae  at 
first  penetrate  into  the  glands  of  Lieberkuhn,  and  when 
fish  are  present  in  the  ventriculus  the.y  leave  the  glands  and 
l)enetrate  into  the  food  during  its  digestion. 

Kahl,  1936,  investigated  the  life  cycle  of  Contracaecum 
clavatum  and  concluded  that  it  can  undergo  partial  develop- 
ment in  a  great  variety  of  intermediate  hosts,  including  Sagitta, 
Calanidae,  amphipods  and  medusae  among  invertebrates,  and 
in  Ammodytcs  and  Mcrangiis  among  fishes.  Wiilker,  1!)29, 
thought  there  was  a  succession  of  three  hosts, — plankton,  plank- 
ton-eating fish,  and  piscivorous  fish,  but  Kahl  thinks  that  all 
three  hosts  are  not  necessary;  development  to  the  stage  in- 
fective for  the  definitive  hosts  can  take  place  directly  in  such 
fish  as  Merlangux  merlangus.  Merlangiis  can  also  serve  as  a 
definitive  host,  if  infective  larvae  are  swallowed  Avith  the 
flesh  of  smaller  intermediate  hosts. 

Markowski  (1937),  influenced  by  Wiilker's  work,  found 
that  certain  species  of  eopepods  served  as  first  intermediate 
hosts  for  C.  adinicum,  and  presented  evidence  for  the  view  that 
a  variety  of  plankton-eating  or  carnivorous  fish  might  serve 
as  second  intermediate  hosts,  although  he  expressed  doubt 
that  the  larvae  developing  in  the  parenteral  organs  of  a  fish 
would  develop  to  maturity  in  the  intestine  of  tlie  same  fish, 
even  if  it  were  a  suitable  host.  Markowski  did  not  con- 
sider the  possibility  of  a  plankton  host  being  unnecessary.  Ac- 
cording to  Kahl  the  larvae  undergo  their  early  development 
in  the  intestine  of  the  intermediate  hosts,  and  then,  when 
about  5  mm  long,  acquire  a  boring  tooth  and  penetrate  into  the 
body  cavity  where  they  molt  again,  but  retain  the  sheath 
with  tooth  and  posterior  spine  until  eaten  by  the  final  host. 
Essentially  then,  the  life  cycle  of  this  species  is  similar  to  that 
of  C.  spicidigeriim,  although  according  to  Kahl  the  eggs  de- 
velop embryos  only  after  being  swallowed  by  a  host.  For  a 
species  living  in  marine  hosts  this  might  be  necessary.  It  is 
probable  that  all  the  species  of  Contracaecum  conform  very 
closely  to  the  same  pattern. 

Thomas  (1937c)  worked  out  the  life  cycle  of  Ehaphidascaris 
canadensis.  The  eggs  of  the  species  may  become  embryonated 
after  8  hours  outside  the  host  and  are  infective  within  24 
hours,  after  one  molt  within  the  egg.  When  eaten  by  nymphs 
of  dragonflies,  these  eggs  hatch,  the  first  cuticle  is  shed,  and 
the  larvae  penetrate  into  the  body  cavity.  Infected  nymphs 
caused  infection  in  guppies,  which  in  turn  caused  infection 
in  fingerling  muskelunge.  In  Douglas  Lake  the  livers  of  all 
yearling  Perca  ftavesccns  are  full  of  Bhaphidaxcaris  cysts, 
whereas  the  plankton-feeding  fingerlings  are  free  of  infection. 
Guppies  can  be  infected  directly  by  the  embryonated  eggs, 
the  intervention  of  an  invertebrate  host  apparently  being 
unnecessary,  as  in  the  ease  of  Contracaecum  adiincnm.  In 
small  bottom-feeding  or  nymph-eating  fish,  then,  they  become 
encapsulated  in  the  mesenteries  and  liver  and  continue  growth 
until  eaten  by  species  of  Esox,  in  which  the  cycle  is  completed. 
R.  acus  of  Europe  presumably  has  a  similar  cycle,  since  the 
larvae  are  found  in  the  inner  organs  of  various  cyprinoid, 
salmonid  and  pereid  fishes,  whereas  the  adults  are  found  in 
Esox,  Perca,  Alosa   and   AnguiUa. 

The  observation  of  Baylis  on  the  probable  relation  between 
Porrocaecum  decipiens  of  seals  and  walruses  and  encapsulated 
larvae  in  various  fishes  have  already  been  mentioned.  A  num- 
ber of  European  writers  have  reported  encysted  larvae  of 
Porrocaecum  in  insectivores  (moles,  shrews,  desman)  and 
Schwartz  (1925)  has  reported  them  from  under  the  skin  of 
moles  and  shrews  in  the  United  States;  he,  and  also  Solonit- 
zine,  who  has  found  the  larvae  of  a  Porrocaecum  on  the  serous 
surface  of  the  stomach  of  a  desman  (Dcsmana  moschata), 
tliink  the  adult  stage  is  probably  reached  in  a  bird  of  prey. 

Walton  (1936a)  found  evidence  for  a  similar  life  cycle  for 
Multicaecnm  tenuicolle.  Encysted  larvae  were  found  in  spe- 
cies of  Sana  and  in  Siren;  3  weeks  after  being  fed  to  a  young 
alligator,  presumably  parasite-free,  several  immature  males 
and  females  were  found.  A  similar  cycle  was  found  by  Wal- 
ton (1936b)  for  Ophidascaris  labialopapUIosa;  the  larvae  were 
encysted  in  mesenteries  and  muscles  of  Sana  spp.,  the  adults 
developing  in  Natrix  spp.  Similar  larvae  encysted  in  mus- 
cles of  Amphiuma,  however,  failed  to  develop  in  Natrix.  Ort- 
lepp  (1922)  failed  to  get  larvae  of  O.  filaria  to  penetrate  the 
mucous  membranes  when  the  ripe  eggs  were  fed  to  a  mouse, 
although  those  of  Polijdelphis  anoura  migrated  to  liver  and 
lungs  like  typical   Ascaridinae. 


SPIRURINA 

Spiruroidea 

The  members  of  this  snperfamily,  with  a  few  exceptions, 
show  a  striking  degree  of  uniformity  in  the  general  features 
of  their  life  cycles.  Although  many  species  tend  to  live  in 
tlie  walls  of  the  alimentary  canal  or  in  more  distant  locations 
in  the  body,  the  eggs,  usuallj-  embryonated,  escape  with  the 
feces,  and  usually  hatch  only  after  being  eaten  by  an  inter- 
mediate host.  The  embryos  of  Habronema,  however,  hatch  be- 
fore escaping  from  the  body.  In  most  cases  there  is  some 
degree  of  specificity  with  respect  to  the  intermediate  host, 
but  usually  it  is  not  very  close.  After  ingestion  by  the  inter- 
mediate host  the  first-stage  larvae  emerge  from  the  egg,  pene- 
trate into  the  bodj'  cavity  or  tissues,  undergo  two  molts,  and 
become  encapsulated  as  third-stage  larvae.  These  larvae  are 
usually  not  sheathed,  as  are  the  larvae  of  metastrongyles; 
the  second  cuticle  is  not  needed  as  a  protection,  since  this  is 
provided  by  a  capsule  produced  by  the  host,  so  is  completely 
shed. 

Infection  of  the  definitive  host  is  nearly  always  by  ingestion 
of  the  infected  intermediate  host,  although  an  alternative 
method  occurs  in  the  ease  of  Habronema  (see  below).  Not  in- 
frequently transport  hosts  may  intervene  between  the  true 
intermediate  host  and  the  definitive  host,  and  it  is  possible 
that  this  can  occur  in  all  spiruroids.  When  the  larvae  are 
eaten  by  a  host  in  which  the  worm  is  unable  to  reach  ma- 
turity they  burrow  through  the  walls  of  the  alimentary  canal 
and  become  reencysted.  In  most  cases  this  seems  to  be  an 
optional  course  of  development  which  is  frequently  favorable 
to  ultimate  access  to  a  definitive  host  (e.g.,  Spirocerca,  Habro- 
nema mansioni)  but  in  the  case  of  at  least  one  species,  Gnatho- 
stoma  spinigerum,  a  second  intermediate  host  has  apparently 
become  indispensable  in  the  life  cycle.  After  reaching  the  final 
host  the  worms  undergo  two  more  molts  before  reaching 
maturity.  Being  too  large  to  enter  blood  vessels  in  the  in- 
testinal wall,  they  usually  reach  their  destination,  if  this 
is  outside  the  alimentary  canal,  by  direct  migration  through 
tissues  or  along  natural  passageways. 

Gongylonema  pulctirum  will  serve  as  an  example  of  a  typical 
spiruroid  life  cycle.  Gnatliostoma  spinigerum  and  Draschia 
megastoma  will  serve  to  exemplify  two  important  variations. 

GONGYLONEM.\  PULCHRUM 

The  adult  worms  live  imbedded  in  the  mucous  membranes 
of  the  esophagus,  tongue  and  oral  cavity.  The  eggs  escape 
into  the  lumen  and  leave  the  body  with  the  feces  in  a  fully 
embryonated  condition.  No  further  development  takes  place 
until  the  eggs  are  ingested  by  a  suitable  intermediate  host. 
This  may  be  anj'  of  a  large  number  of  beetles,  particularly 
scarabaeids,  or  cockroaches.  Twenty-four  hours  after  inges- 
tion by  Btatrlla  germanica,  according  to  Alicata  (193.5),  empty 
egg  shells  are  found  in  the  crop  and  intestine.  The  absence 
of  larvae  in  the  lumen  or  wall  of  the  intestine  and  the  pres- 
ence of  a  few  still  adhering  to  the  wall  of  the  crop,  apparently 
ready  to  invade  the  body  cavity,  suggests  that  hatching  takes 
place  in  the  crop,  and  that  the  larvae  find  their  way  into 
the  body  cavity  by  piercing  the  wall  cf  the  crop.  Forty-eight 
hours  after  ingestion  of  eggs,  first-stage  larvae  are  found 
in  the  body  cavity,  especially  in  the  thoracic  region. 

The  newly  hatched  first-stage  larva  is  cylindrical  with  a 
spine  and  a  small  hook  near  the  anterior  end  on  the  ventral 
side,  behind  which  about  20  rings  of  minute  spines  encircle 
the  anterior  end  of  the  body  (Fig  190B)  ;  the  tip  of  the  blunt 
tail  is  encircled  by  8  to  10  small  refringent  points,  a  character 
which  is  diagnostic  of  the  first-stage  lai'va.  The  filariform 
esophagus  and  intestine  are  about  equal  in  length.  l)oth  trans- 
parent. The  larvae  wander  about  in  the  body  cavity  and  grow 
to  double  their  original  length  in  about  2  weeks,  and  at  this 
time  are  preparing  for  the  first  molt  (Ransom  and  Hall, 
1916;  Alicata,  1935).  The  actual  molt,  according  to  Alicata, 
does  not  occur  until  about  the  19th  day. 

The  second-stage  larvae  lose  the  cuticular  armature  at  the 
anterior  and  posterior  ends,  which  are  bluntly  rounded.  The 
slender  esophagus  occupies  about  one-half  the  body  length, 
and  in  older  larvae  becomes  differentiated  into  an  anterior 
muscular  portion  and  a  posterior  glandular  portion.  These 
larvae  increase  in  size  to  a  length  of  1.5  to  2  mm  by  the 
end  of  the  fourth  week,  when  they  liegin  the  second  molt. 
At  about  this  time  they  usually  penetrate  the  muscles  of  the 
body  wall,  and  sometimes,  in  heavy  infections,  other  muscles, 
and  they  may  become  partially  encysted  prior  to  the  second 
molt. 

Third  stage  larvae  are  found  encysted  at  the  end  of  about 
a  month.  This  stage  is  distinguished  by  a  raised  lateral  bor- 


282 


Fig.    190. 


Develoimient  of  Ctonmilonpin/i  putchrum.  A — Egg  with  fully  devel- 
oped embryo;  B — Fir.st  stuKe  larva,  anterior  end;  C — First  stage  larva 
from  intermediate  host,  four  days  ;iftcr  experimental  infection;  D — Tail, 
lateral  view;  E — First  stage  1jiiv;i  undergoing  first  molt;  F — Second 
stage  larva;  G — Third  stage  larva  encysted  in  niuseulature  of  roach 
[BUttella   gerrnanirit)  ,    H — Third    stage,    hiteial    view;    I — Posterior    end 


showing  four  digltiform  prncesKes  ;  J — Posterior  end  of  male  undergoing 
third  molt;  K — Posterior  end  of  female  undergoing  third  molt,  h— 
Fourth  stage  larva,  anterior  end;  M — Posterior  part  of  male  in  fourth 
molt;  N — ^Region  of  vulva  of  larva  undergoing  fourtli  molt.  After 
Alicata.    19^5.    D.S.D.A.   Tech.    Bull.    489. 


283 


(liT  of  the  mouth  and  by  four,  occiisioiuilly  only  two,  small 
fligitiform  processes  on  the  tail.  The  larvae  are  found  imbedded 
within  the  sarcoplasm  suriounding  a  niusfle  fiber.  As  the 
cysts  become  well  formed  they  are  sometimes  pushed  out  into 
the  body  cavity,  remaining  attached  to  the  muscle  by  a  thin 
strand,  or  eventually  falling  free.  Baylis  (192(i)  found  that 
the  larvae  would  eseajie  from  disintegrating  cockroaches  into 
water,  and  could  be  kejit  alive  for  a  number  of  days,  Imt 
since  the  larvae  settle  to  the  bottom  he  concluded  that  drinking 
water  was  not  an  important  means  of  infection.  Freed  larvae 
were  found  to  be  incapable  of  skin  penetration.  The  possibility 
exists,  of  course,  that  larvae,  either  in  or  out  of  their  inter- 
mediate hosts,  might  reencyst  in  some  transport  host;  Alicata 
(I.e.)  cites  the  finding  of  third  stage  larvae  in  the  stomach 
wall  of  a  mole. 

Upon  ingestion  by  a  definitive  host  (Alicata  used  guinea 
pigs  for  experimental  infections)  the  larvae  are  liberated 
in  the  stomach  and  may  invade  the  esophagus  within  one-half 
hour  after  feeding,  entering  through  the  tissue  at  the  gastro- 
esophageal junction.  They  migrate  ujiward  througli  the  epithe- 
lium of  the  esophagus  and  may  roach  the  tongue  as  early 
as  the  third  day.  Larvae  begin  the  third  molt  on  the  ninth 
day  after  ingestion,  and  many  fourth-stage  larvae  are  pres- 
ent by  the  twelfth  day.  These  larvae  are  characterized  by 
development  of  the  reproductive  organs,  gradual  develop- 
ment of  the  characteristic  cuticular  bosses  at  the  anterior 
end,  and  loss  of  the  caudal  appendages.  The  final  molt  oc- 
curs about  a  month  after  infection ;  the  minimum  time  re- 
quired for  growth  to  maturity  seems  not  to  have  been  de- 
termined definitely,  but  Ransom  and  Hall  (I.e.)  report  the 
finding  of  egg-bearing  females  in  a  sheep  about  3  months 
after  infection,  and  Alicata  (lilS-'i)  obtained  an  adult  male 
70   days   after   infection. 

Gnathostoma    spiniuekum 

The  adult  worms  live  in  tumors  in  the  wall  of  the  stomach 
of  Felidae,  or  of  the  esophagus  of  mink,  the  eggs  escaping 
into  the  alimentary  canal  through  ojienings  which  eventually 
develop  from  the  tumors  into  the  lumen.  The  eggs  escape 
from  the  body  in  an  early  stage  of  development  (one  to  two- 
celled  stage  according  to  Pronimas  and  IJaengsvang,  1933; 
one  to  many-celled  according  to  Refuerzo  and  Garcia  (1938). 
In  aerated  water  they  become  embryonated  in  a  minimum 
of  about  4  or  o  days,  and  in  2  days  or  more  thereafter  the 
embryos  emerge  from  the  egg  in  an  onsheathed  condition, 
being,  therefore,  in  the  second  stage.  These  larvae  have 
smooth  cuticles  devoid  of  spines  or  striations,  and  are  armed 
with  a  spine  at  the  anterior  end. 

The  larvae  usually  live  for  only  a  few  days  in  tapwater 
(Prommas  and  Doengsvang,  1933)  although  sometimes  they 
may  live  for  a  month  or  more  (Yoshida,  1934).  Further  de- 
velopment is  known  to  occur  only  when  the  larvae  are  ingested 
by  Cyclops.  Attempts  to  infect  mammals,  fish,  frogs,  fleas 
and  Cladocera  have  all  been  negative.  The  development  of  the 
larvae  in  Cyclops  was  independently  discovered  by  Prommas 
and  Daengsvang  (I.e.)  in  Siam  and  by  Yoshida  (1934)  in 
Japan.  These  workers  showed  that  sheathless  motile  larvae 
were  found  in  the  stomachs  of  Cyclops  soon  after  experimental 
exposure,  and  that  by  the  following  day  they  could  be  found 
in  the  body  cavity.  According  to  Refuerzo  and  Garcia  (1938), 
the  larvae  in  the  liody  cavity  1  day  after  infection  lose  the 
sclerotized  oral  spine,  and  a  tieshy  enlargement  representing 
the  future  lips  develops  at  the  anterior  end.  Three  days  later 
the  cuticle  becomes  striated,  its  armature  of  spines  develops, 
and  a  head  bulb  armed  with  four  rows  of  spines,  and  con- 
nected with  cervical  sacs,  is  also  present.  The  larvae  seem 
to  have  completed  their  development  to  the  infective  stage 
by  the  sixth  day. 

Attempts  to  infect  cats  by  feeding  them  infected  Cyclops 
have  been  uniformly  negative  (Yoshida,  1934;  Prommas  and 
Daengsvang,  1936)  but  Prommas  and  Daengsvang  succeeded 
in  infecting  a  catfish,  Clarias  batrachus.  The  larvae  were 
found  in  the  muscles  of  the  stomach  or  intestine  of  the  fish 
2  to  6  days  after  infection  and  after  6  days  or  more  they 
were  found,  some  free  and  some  encysted,  in  body  muscles. 
Chandler  (1925a)  had  reported  the  presence  of  numerous 
gnathostome  cysts  in  the  mesenteries  of  Indian  snakes,  which 
he  found  to  undergo  further  development  in  cats  (1925a) 
until  the  adult  morphology  of  Gnathostoma  spinigerum  was 
reached  (1925b)  ;  Chandler  also  called  attention  to  reports 
of  probably  identical  larvae  in  pelicans  and  eagles.  Subsequent 
to  the  work  of  Prommas  and  Daengsvang  many  other  interme- 
diate hosts,  natural  and  experimental,  have  been  added,  in- 
cluding a  considerable  variety  of  fresh-water  fishes,  frogs, 
and  snakes.  In  all  of  these  the  larva  undergoes  considerable 
growth,  but  does  not  develop  more  than  4  rows  of  spines  on 
the  head  bulbs,  in  contrast  to  the  8  to  11  found  in  the  adults 


of  Gnathostoma  sphif/rnim.  It  is  probable  that  the  larvae  al- 
w^ays  become  encysted   ultimately. 

Chandler  (1925a)  showed  that  when  gnathostome  cysts  in 
snakes  are  fed  to  cats  they  penetrate  through  the  alimentary 
canal  and  can  be  found  parenterally  within  2  days  after  in- 
fection. Some  are  found  free  in  the  abdominal  cavity,  under 
the  parietal  peritoneum,  or  in  the  capsules  of  the  kidneys, 
but  the  majority,  and  nearly  all  later  in  the  infection,  are 
found  burrowing  in  the  liver.  A  single  larva  was  also  found 
in  the  liver  of  an  experimentally  infected  guinea  pig.  The 
larvae  in  the  livers  of  cats  grow  somewhat,  and  a  vulva 
and  rudimentary  genital  tubes  develop  within  (3  days.  No 
further  development  was  observed  in  cats  infected  for  as  long 
as  4  weeks,  although  in  the  meantime  there  was  extensive 
damage  done  to  the  liver.  Subsequently  (1925b)  Chandler 
found,  in  naturally  infected  cats,  all  stages  of  development 
from  (presumably)  fourth-stage  larvae  burrowing  in  tine 
liver,  exactly  like  those  obtained  from  exjierimental  infectious, 
to  forms,  still  sexually  immature,  which  had  undergone  the 
final  transformation  to  the  adult  morphology,  and  had  8  to 
11  rows  of  hooks  on  tlie  liead  bulb,  arid  comiilcx  spines  on  the 
liody.  Some  of  the  worms  which  had  undergone  the  final  molt 
were  found  still  in  the  liver,  but  others  were  evidently  migrat- 
ing out  of  the  liver;  a  few  were  found  in  the  mesentery  or 
in  the  diaphragm,  and  several  were  in  the  stomach  wall; 
one  was  free  in  the  .stomach.  The  worms  in  the  stomach  wall 
were  not  yet  enclosed  in  hard-walled  tumors,  Imt  occurred 
in  submucous  purulent  cavities.  It  was  evident  from  these 
observations  that  the  worms,  upon  gaining  access  to  a  defini- 
tive host,  migrate  through  the  walls  of  the  stomach  or  in- 
testiiu>  to  the  abdominal  cavity  and  enter  the  liver,  where 
they  burrow  and  feed  actively  for  several  weeks.  They  finally 
enter  the  wall  of  the  stomach  from  the  peritoneal  side,  and 
grow  to  maturitj'. 

Africa  et  al  (193(ia)  fed  rats  with  encysted  larvae  and 
found  the  larvae  in  the  liver  and  body  muscles  8  to  25  days 
later.  Infection  of  cats  fed  on  gnathostome  cysts  from 
cold-blooded  hosts  has  been  confirmed  by  Prommas  and  Daeng- 
svang (1937),  the  prepatent  period  being  28  to  32  weeks, 
and  l)y  Africa  et  al  (193()b),  who  found  semi  mature  worms 
in  tlie  diaphragm  and  in  nodules  in  the  stomach  wall  nearly 
4  months  after  infection.  It  is  clear  that  the  formation 
of  a  tumor  about  the  worms  in  the  wall  of  stomach  or  esopha- 
gus, which  finally  opens  into  the  lumen,  is  a  late  stage  of 
development.  It  also  seems  evident  from  observations  made 
by  the  writer  (1925b)  that  these  tumors,  when  in  the  stomach 
of  cats,  frequently  become  perforated  into  the  peritoneum 
and  are  then  fatal.  Yoshida 's  observation  that  in  luink  the 
tumors  form  on  the  esophagus  in  the  lower  part  of  the 
thoracic  cavity  suggests  that  this  may  be  the  normal  host  and 
habitat,  and  that  in  these  circumstances  there  is  less  danger 
of  fatal  parenteral  perforation. 

Draschia  meqastoma 

The  life  cycle  of  this  worm  is  of  particular  interest  since 
it  represents  an  intermediate  evolutionarj-  step  from  that 
of  the  typical  spiruroids  to  the  filariae.  It  was  first  worked 
out   in   detail   by  Eoubaud   and   Descazeanx    (1921). 

The  female  deposits  embryonated  eggs  in  the  alimentary 
canal  which,  according  to  Roubaud  and  Descazeaux,  hatch  be- 
fore leaving  the  body  of  the  host.  The  first-stage  larvae 
possess  a  hooklike  structure  similar  to  the  hook  of  Gongy- 
loiiema,  but  the  larvae  are  in  a  very  immature  state,  the  con- 
tents of  the  body  being  granular  in  appearance,  with  no  dif- 
ferentiation. These  larvae  are  ingested  by  young  nuiggots  of 
flies,  and  there  seems  to  be  a  fairly  high  degree  of  specificity. 
Draschia  megastoma  and  Habronema  miiscae  have  been  found 
to  be  capable  of  development  in  a  number  of  species  of 
Musca  and  also  in  Miisciim  stabiilaiis  and  in  Fannia,  but  ac- 
tual transmission  has  been  observed  only  in  Musca  domestica, 
and  was  definitely  found  by  Eoubaud  and  Descazeaux  to  fail 
in  the  case  of  Muscina  stabulans  because  of  inability  of  the 
larvae  to  escape  from  the  proboscis  of  that  species.  H.  micro- 
stoma, on  the  other  hand,  develops  primarily  in  Stomoxys, 
but  has  been  reijorted  as  developing  in  Sarcophaga,  Lyperosia 
and  }[tisca  as  well,  though  Roubaud  and  Descazeaux  (1922b) 
state  that  it  does  not  reach  the  infective  stage  in  Musca 
flomcstica.  Development  of  Eabroncma  larvae  has  also  been 
reported    from    Drosophila. 

The  ingested  larvae  bore  through  the  walls  of  the  ali- 
mentary canal  of  the  maggots  and  enter  the  body  cavity. 
They  live  free  in  the  body  cavity  for  only  a  brief  time, 
and  about  the  third  day  they  penetrate  into  the  Malpighian 
tubules.  Here  they  become  quiet,  and  undergo  the  first  molt 
on  the  third  or  fourth  day  after  ingestion.  They  lose  the 
oral  hook,  become  immobile,  and  grow  very  thick  and  aausage- 


284 


Fig.    191.      DEVELOPMENT   OF    SPIRUKOlOKA 


AJ — ~0 nathostoma  spinifferum  (A — Larva  emerging  from  egg  through 
opercular  t^nd ;  B — Newly  hatched  larva  with  loose  enveloping  sheath, 
anterior  spine :  C — Anterior  end  of  larva  dissected  from  oy clops  on 
first  day  of  infection,  no  anterior  spine  but  large  fleshy  lip.  two  pairs 
of  contractile  cervical  sats;  D— Larva  from  Cyclops  on  fourth  day  of 
infection,  cephalic  bulb  with  four  rows  of  miuut€  spines,  lip  smaller ; 
F — Larva  in  body  cavity  of  ryclops;  E — Same  larva;  O — ^Larva  from 
cyst  in  mesentery  of  cobra;  H- — -Head,  bulb  and  lips  of  larva  from  liver 
of  artificially  infected  cat;  I — Gnathostoiue  from  liver  of  artificially  in- 
fected cat;  J — Section  of  liver  of  cat  showing  riddling  of  tissue  by 
burrowing  gnathostomes) .  K-M — Stages  in  the  development  of  Habro- 
nema  mimcae.  (K — Egg  with  embryo;  L — Second  stage  larva;  M— 
Third  stage  larva  before  the  molt).  N-O — Sections  pointing  out  the 
histological  reaction  of  the  fat  cells  parasitized  by  Uabronema  inunca^- 
(N — Fat  cells  at  the  beginning  of  the  infection  showing  peripherial 
Uiickening  and  hypertrophy  of  parasitized  cell  in  relation  to  normal; 
O — Section   of   a   fat    sac   enclosing   many   parasites).      P — Fragment   of 


fat  tissue  of  larva  of  Slu^ca  dom-fstica  showing  aciculate  larva  of  H. 
muHcae  in  hypertrophied  and  transformed  fat  cell.  Q-S — Development 
of  H.  microatomurn  in  Stomoicys.  (Q — Group  of  adipose  cells  of  the  larva 
of  Stomoxyti  of  which  three  are  infested  with  a  young  larva  of  H. 
tnicrostamum  ;  R — Sausage  shaped  larva;  S — Older  second  stage  larva). 
T-CC — Draachia  nie{jastoiua.  (T — Embryonated  egg;  U — Aciculate  larva 
emerging  from  egg  shell;  V — Aciculate  larva  in  intestine  of  fly;  W — 
Second  stage  larva  immediately  after  molt  in  malpigbian  tubules  of  fly 
larva;  X-Y — Second  stage  larvae  recovered  from  larva  (X)  and  pupa 
(Y)  of  fly;  Z — Full  grown  second  stage  larva;  AA — Second  stage  larva 
about  to  molt;  BB — Second  stage  larva,  full  grown  and  about  to  molt, 
removed  from  malpigbian  cyst;  CC — Posterior  end  of  same).  A-D, 
after  Refuerzo  &  Garcia.  1938.  Philip.  J.  An.  Ind.  (5  (4)).  E  F, 
after  Prommas  and  Daengsvang,  1933,  J.  Parasit.  G-J,  after  Chandler, 
1925,  Parasit.  v.  17.  KCC.  after  Roubaud  and  Descazeaux,  Bull.  Soc. 
Path.'  Exot.,  V.   14,   15. 


285 


like.  An  outline  of  the  stoma  appears  at  the  head  end,  and  a 
conspicuous  caudal  vesicle  and  outline  of  the  pyriform  rec- 
tum at  the  posterior  end,  but  throughout  the  rest  of  the  body 
the  nuclei  are  still  scattered  without  definite  order.  Gradually 
during  the  next  few  days  the  worm  elongates,  and  the  alimen- 
tary canal,  nerve  ring,  and  rectum  become  well  developed. 
Meanwhile  the  tissue  of  the  wall  of  the  Malpighian  tubule 
surrounding  the  larva  degenerates  and  is  finally  reduced  to  a 
mere  membrane,  which  serves  as  a  sheath.  On  the  eighth 
day,  at  about  the  time  of  emergence  of  the  adult  fly,  the 
larvae  begin  to  break  loose  into  the  abdominal  cavity,  still 
enclosed  in  the  membrane,  but  they  now  molt  a  second  time 
and  their  movements  become  very  active,  resulting  in  their 
soon  freeing  themselves. 

These  third-stage  larvae,  the  infective  forms,  may  appear 
as  early  as  the  ninth  day.  They  migrate  forward  to  the 
head  of  the  fly,  and  collect  in  the  interior  of  the  labium. 
Attracted  by  warmth  and  moisture  they  move  down  into  the 
labellum,  and  escape  through  the  delicate  membrane  between 
the  lobes  of  this  structure  when  the  fly  is  resting  on  a  warm 
wet  surface,  e.g.,  the  lips,  nostrils  or  wounds  of  an  animal. 
If  on  the  lips,  the  larvae  have  an  opportunity  to  reach  the 
stomach  via  the  mouth,  and  grow  to  maturity  in  a  normal 
manner,  but  from  the  nostrils  they  reach  the  lungs,  and  from 
the  skin  the  subcutaneous  tissues,  and  in  either  case  fail  to 
grow  to  maturity.  There  is  no  doubt  but  that  animals 
could  also  be  infected  by  swallowing  flies  harboring  infective 
larvae,  but  in  the  case  of  habronemiasis  of  horses  this  would 
probably  not  be  a  common  method  in  nature.  On  the  other 
hand  it  would  probably  be  the  principal  if  not  the  exclusive 
method  in  the  case  of  habronemiasis  of  insectivorous  birds. 
Still  another  possibility — ingestion  by  a  transport  host — is 
suggested  in  the  case  of  habronemiasis  in  birds  of  prey ; 
this  is  supported  by  the  finding  of  abundant  larvae  of  H. 
mansioni  encysted  in  the  stomach  walls  of  toads  by  Hsii  and 
Chow  (1938).  Tliis  species  had  previously  been  recorded 
from  the  bearded  vulture,  Gypaeiii.'i  barbatiis,  but  several  spe- 
cies of  falcons  were  experimentally  infected  by  feeding  them 
larvae   from    toads. 

Habroneina  muscac  and  H.  micrn.ttomiim  have  similar  life 
cycles  {vide  Roubaud  and  Descazeaux,  lB22a),  but  different 
in  details.  These  two  species,  instead  of  undergoing  devel- 
opment in  the  Malpighian  tubes,  develop  in  cells  of  the  fat 
body,  the  thickened  walls  of  the  cells  serving  ns  temporary 
"cyst"  walls.  H.  micro.stomum.  which  develops  in  the  blood- 
sucking Stomoxys,  might  be  expected  to  be  introduced  into  the 
tissues  when  the  insect  pierces  the  skin,  and  be  forced  to 
find  its  way  to  the  stomach  by  some  roundabout  parenteral 
route,  but  Roubaud  and  Descazeaux  (1922b)  point  out  an  in- 
teresting biological  adjustment  which  makes  this  unnecessary. 
They  point  out  that,  as  a  result  of  interference  by  the  worms 
in  its  proboscis,  the  fly  is  unable  to  rasp  a  hole  in  the  skin 
to  suck  blood,  and  is  forced  to  revert  to  the  habits  of  its  an- 
cestors and  non-blood-sucking  relatives,  and  obtain  moisture 
and  nourishment  from  the  lips  or  other  exposed  moist  sur- 
faces. 

The  failure  of  the  larvae  of  Habroneina  to  become  encysted 
in  the  intermediate  host,  there  to  remain  until  eaten  by  a 
definitive  host,  and  the  substitution  of  a  voluntary  exit  from 
this  host  in  response  to  warmth  and  moisture,  are  definite 
steps  in  the  direction  of  a  filarial  life  cycle.  As  remarked 
by  Roubaud  and  Descazeaux  (1922b),  however,  the  habrone- 
mas  are  imperfectly  adapted  for  parenteral  parasitic  life.  Their 
larvae,  in  spite  of  the  fact  that  they  leave  the  body  of  the 
intermediate  host  on  the  surface  of  the  body  of  the  definitive 
host,  are  unable  to  penetrate  the  tissues,  and  are  unable  to 
reach  maturity  outside  the  alimentary  canal.  With  (1)  de- 
velopment of  a  parenteral  adult  habitat  (already  attempted 
by  many  spiruroids  but  always  hampered  by  the  necessity  for 
the  eggs  to  reach  the  alimentary  canal),  and  (2)  develop- 
ment of  ability  to  enter  the  skin  on  the  part  of  the  infecting 
larvae,  the  only  important  change  necessary  to  bring  about 
a  filarial  life  cycle  is  the  substitution  of  the  blood  or  skin  for 
the  alimentary  canal  as  a  means  of  exit  for  the  larvae.  Such 
a  development  could  hardly  fail  to  occur  in  the  case  of  a 
parenteral  parasite  with  a  blood-sucking  intermediate  host. 

Other,  Spiruroidea 

The  life  cycle  of  the  ma,iority  of  the  Spiruroidea  in  which 
it  has  been  determined  conforms  in  general  pattern  to  that  of 
Gongylonema,  except  for  the  intermediate  hosts  involved.  In 
some  cases  there  seems  to  be  far  less  specificity  with  respect 
to  intermediate  hosts  than  in  others,  but  some  instances  of 
apparent  specificity  are  probably  due  to  incomplete  data. 
Thus  Cheilospirura  hamulosa  was  not  known  to  develop  in  any- 
thing but  grasshoppers  until  Alieata  (1937)  showed  that  an 
amphipod  and   10   species  of  beetles  belonging  to   7   different 


families,  as  well  as  several  grasshoppers,  could  b?  utilized  as 
intermediate  hosts  by  this  worm.  On  the  other  hand,  Cram 
(1931)  got  negative  results  from  feeding  eggs  of  C.  spinosa 
to  cockroaches,  ground  beetles,  sowbugs  and  crickets,  but  ob- 
tained development  in  two  species  of  grasshoppers.  Again, 
whereas  Telramercs  fissispina  is  reported  as  capable  of  devel- 
opment in  grasshoppers,  roaches,  Daphnia,  Gainmariis  and  earth- 
worms. Swales  (1936)  found  that  the  eggs  of  T.  crami  failed 
to  hatch  in  various  species  of  Cladocera,  but  developed  read- 
ily in  two  species  of  amphipods.  Members  of  the  genera 
Ascarops,  Physocepltaliis  and  Spirocerca  seem  to  develop  pri- 
marily in  dung  beetles ;  Spirura,  Protospirura  and  Gongy- 
lonema in  beetles  or  roaches;  Oxyspirura  in  roaches;  Seurocyr- 
nea  in  roaches  and  grasshopper  nymphs;  Acnaria  in  grass- 
hoppers; Tetrameres  in  various  Orthoptera  and  Entomostraca ; 
Eartertia  in  termites  (workers);  Echinuria  in  Cladocera, 
Dispharynx  and  Hedrnris  in  isopods ;  Cystidicola  in  amphipods, 
and  Spiroxys  in  eopepods.  Spiruroid  larvae,  possibly  Protos- 
pirura,  have  been  found  in  fleas  also.  Under  experimental  con- 
ditions Physaloptera  iurgida,  according  to  Alieata  (1938),  is 
able  to  develop  in  cockroaches,  but  there  is  a  possibility  that 
other  arthropods  are  utilized  under  natural  conditions. 

Spiroxys  contorta,  as  reported  by  Hedrick  (193.5),  differs 
from  the  majority  of  the  Spiruroidea  but  resembles  Gnatho- 
stoma  in  that  the  eggs  become  embryonated  in  water  after 
leaving  the  body  of  the  host.  It  differs  from  Gnathostoma, 
however,  in  that  the  definitive  host  can  be  infected  directly 
by  the  third-stage  larvae  in  Cyclops,  without  requiring  a 
second  intermediate  host.  In  nature,  however,  transport  hosts 
— fish,  tadpoles,  frogs,  newts  and  dragonfly  nymphs,  and  fre- 
quently turtles  as  well — are  commonly  made  use  of.  The 
lar%-ae  of  this  worm  are  further  peculiar  in  that  they  continue 
to  grow  after  they  reach  the  infective  stage,  both  in  Cyclops 
and  in  the  various  transport  hosts.  The  development  of  a 
"sausage"  form  by  the  late  first-stage  larva  of  Oxyspirura 
mansoni,  as  figured  by  Kobayashi,  is  highly  suggestive  of 
Habroncma  or  the  filariae. 

As  far  as  known  at  present  Giialkostoma  spiiiigenim  is  the 
only  spiruroid  which  requires  a  second  intermediate  host,  but 
it  is  quite  possible  that  this  will  be  found  to  be  true  of  other 
Gnathostomatidae  as  well,  and  perhaps  of  still  other  spiruroids. 
The  larvae  of  Echiiiocepliahis  (family  Gnathostomatidae)  have 
been  found  encysted  in  the  tissues  of  a  bivalve,  Margaritifera 
vulgaris,  which  is  presumably  the  first  intermediate  host.  Simi- 
lar larvae  have  been  found  in  a  sea  urchin.  Since  the  adults 
occur  in  oyster-eating  fishes  no  second  intermediate  host  may 
be  necessary. 

The  course  of  migration  in  the  definitive  host  is  usually, 
as  noted  above,  by  burrowing  directly  through  tissues  or 
natural  cavities,  or  by  migration  along  natural  passageways. 
The  path  of  Oxyspirura  mansoni  to  the  eye,  according  to 
Fielding  (1926),  is  by  way  of  esophagus,  mouth  and  lachrymal 
duct,  the  larvae  sometimes  arriving  in  the  eye  20  minutes  after 
infected  roaches  are  fed  to  chicks. 

The  migration  route  of  Spirocerca  hipi  (—sanguinolenta) 
is  not  so  clearly  known.  Faust  (1927)  thought  that  the  larvae, 
after  ingestion  with  the  flesh  of  a  transport  host  (hedgehog), 
reach  the  aorta  via  the  portal  system  and  lungs,  but  does  not 


Fig.  192. 

Development  of  Ascaropsiniie  larvae.  A-E — Ascarops  strons^ylina 
(A — First  st.age  larva,  anterior  end,  lateral  view;  B — Larva  recovered 
from  an  intermediate  ho.st  three  days  after  e.xperiinental  infection;  C — 
Larva  undergoing  first  molt:  D — Third  stage  larva,  lateral  view;  E — 
Encysted  larva,  third  stage).  F-K — Fhysocephtilus  sexakttus  (F — An- 
terior end.  lateral  view;  G — Larva  from  intermediate  host  2  days  after 
experimental  infection;  H — Larva  from  intermediate  host  12  days  after 
experimental  infection;  I — Larva  undergoing  first  molt;  J — Encysted 
third  stage  larva  (from  Hobmaier,  1925);  K — Third  stage,  tail).  After 
Alieata,   1935,  U.S.D.A.,  Tech.  Bull.  489. 

Fig.   193. 

A-G  &  G — Spiroirtjs  contortus;  (A — Free-living  larva  with  sheath; 
B — Five-day  old  larva  from  cyclops;  C — Ci/clops  leucknrti  with  three 
larval  nematodes:  G — Fully  developed  larva  from  body  cavity  of  cyclops. 
showing  genital  primordium).  O-E — Disphnrtni.r  spiriilis  (D — Head; 
E — Tail).  F — Tetrampres  atuerirana,  tail  of  third  stage  larva.  H-I — 
Tetrameres  crami  <H — Third  stage  larva  from  Oammarus  fa-scintus  32 
days  after  infection:  I — Diagrammatic  illustration  of  papillae  ^on 
tail  of  third  stage  larva).  J — Larval  spirurid  larva  from  cat  flea.  K-M 
— Protospirura.  muricnla  (K — Lateral  view  of  anterior  extremity  of  in- 
fective larva;  L — Lateral  view  of  tail  of  3.5  mm.  specimen;  M — Free- 
had  sketch  of  rosette  of  papillae  on  tail  of  same).  N-P — Oxyspirura 
mansoni  (N — Larva  just  after  hatching;  O — Larva  at  end  of  first  lar- 
val stage;  P — Mature  larva).  Q — Habronema  mansioni,  larva.  A-C,  & 
G,  after  Hedrick.  L.  A.,  1935,  Tr.  Am.  Mic,  Soc.  v.  54(4).  D-F,  after 
Cram,  E.  B.,  1931,  U.S.D.A.  Tech.  Bull.  227  H,  I,  after  Swales,  1936, 
Canad.  J.  Ees.  D.  14.  J,  after  Alieata,  J.  E.,  1935,  J.  Parasit.  v.  21 
(3).  K-M,  after  Foster,  A.  0.,  and  Johnson,  C.  M..  1939,  Am.  J. 
Trop  Med.  v.  19  (3).  N-P,  after  Kobayashi,  H.,  1928,  Taiwan  Igakk. 
Zasshi  Formosa,  No.  280.  Q.  after  Hsu,  H.  P.,  and  Chow.  C.  Y.,  1938, 
China  Med.  J.   Suppl.   II. 


286 


Fig.   192.      DEVELOPMENT  OF  ASCAROPSINAE    LARVAE 


Kig.   19.3.      DEVELOPMENT  OP  Sl'IRUROIDEA 


287 


make  it  clear  how  a  worm  l.iO  M  in  diameter  is  able  to  pass 
througli  capillaries,  or  why  the  worms  appear  iu  the  ab- 
dominal aorta  before  the  thoracic,  and  never  cause  lesions 
in  vessels  anterior  to  the  aortic  arch.  It  seems  far  more  likely 
that  the  larvae  follow^  the  route  indicated  by  Hu  and  Hoeppli 
(1936)  ;  after  penetrating  the  gastric  wall  they  proceed  to  the 
coronary,  gastroepiploic  and  coeliac  arteries,  and  via  these 
to  the  upper  abdominal  and  lower  thoracic  portions  of  the 
aorta,  eventually  reaching  the  upjier  thoracic  aorta  from  below. 
In  the  aorta  the  worms  attach  themselves  to  the  wall  and 
cause  the  formation  of  characteristic  nodules.  Some  worms 
remain  iu  this  position  but  many  migrate  outward  through 
the  aortic  wall  and  through  the  intervening  tissue  until  they 
reach  the  esophageal  wall,  iii  which  they  find  a  favorable  habi- 
tat in  which  to  reach  maturity  and  reproduce.  The  eggs  reach 
the  lumen  of  the  esophagus  through  a  secondary  opening 
from  the  tumor  in  its  wall. 


FILARIOIDEA 

The  Filarioidea  are  unique  among  nematodes,  so  far  as  is 
known  at  present,  in  having  perfected  a  mechanism  by  which 
bott  exit  from  and  entrance  to  a  host  takes  place  through  the 
skin.  The  larvae  of  Dracuueuloidea  escape  through  the  skin, 
though  by  a  different  mechanism,  and  the  habronemas  suc- 
ceed in  infecting  a  host  when  deposited  on  certain  areas 
of  skin  (the  lips)  but  in  neither  case  is  both  exit  and  entrance 
accomplished  by  way  of  the  skin.  As  noted  under  the  discus- 
sion of  Spiruroidea,  the  evolutionary  process  by  which  the  life 
cycle  of  iilariae  developed  is  clearly  foreshadowed  by  the 
course  of  events  in  the  case  of  Eabronema. 

WUCHEMailA    BANCBOFTI 

Hanson's  (1878)  discovery  of  the  ingestion  of  filarial  em- 
bryos by  mosquitoes  and  their  development  in  these  insects  set 
a  landmark  in  the  history  of  medical  entomology,  since  it  was 
the  first  instance  of  a  human  blood  infection  being  transmit- 
ted by  an  insect.  Low  (1900)  first  demonstrated  the  mechanism 
by  which  the  larvae  were  returned  from  mosquitoes  to  man, 
and  Annett,  Dutton  and  Elliott  (1901),  Lebredo  (1905), 
and  Bahr    (1912)    added  further  details. 

The  adult  worms  live  iu  the  lymphatic  system  and  liberate 
their  larvae,  known  as  microfilariae,  into  this  system,  whence 
they  eventually,  unless  blocked,  make  their  way  into  the  blood 
stream.  Their  presence  in  the  peripheral  blood  is  periodic  in 
most  parts  of  the  world,  being  present  at  night,  but  not  in 
the  daytime.  Similar  periodicity,  though  often  less  complete, 
is  observed  in  many  other  filarial  infections;  in  some  spe- 
cies, however,  e.g.,  Loa  loa,  there  is  a  diurnal  periodicity,  and 
in  others,  e.g.,  Dipetaloncma  perstans,  no  periodicity  has  been 
observed.  Two  principal  theories  have  been  proposed  to  ac- 
count for  the  periodicity:  one,  originally  advanced  by  Man 
son,  is  that  the  larvae  retire  to  internal  organs  during  the 
day  and  enter  the  peripheral  circulation  only  at  night ;  the 
other,  advanced  by  Lane  (1929),  is  that  the  worms  have  cycli- 
cal parturition,  producing  their  entire  day's  output  of  larvae 
at  the  same  time  each  day,  and  that  these  worms  are  all 
destroyed  in  the  host  within  12  hours  after  they  appear  in 
the  blood  stream.  Some  support  is  given  to  this  theory  by 
O'Connor's  (1931)  observation  at  autopsies  that  at  certain 
hours  all  the  adult  female  filariae  have  their  uteri  crowded 
with  embryos,  while  at  other  hours  they  are  uniformly  spent. 
On  the  other  hand,  the  persistence  for  a  year  or  more  of  mi- 
crofilariae transferred  to  an  uninfected  host  (Underwood  and 
Harwood,  1939)  is  against  this  theory,  though  the  fate  of 
microfilariae  in  infected  and  nou-iufected  hosts  may  not  be  at 
all  comparable.  As  yet  there  is  no  unanimity  of  opinion  as 
to  the  reason  for  microfilarial  periodicity. 

The  microfilariae  of  Wuchereria  bancrofti  as  seen  iu  blood 
smears  are  covered  by  a  sheath  which  has  very  generally  been 
thought  to  be  not  a  shed  cuticle  but  a  delicate,  stretched  vitel- 
line membrane.  Augustine  (1937)  questioned  this,  since  he 
observed  that  developing  microfilariae  in  the  uterus  of  Vagri- 
filaria  columbigallinae  clearly  show  the  vitelline  membrane  sur- 
rounding eggs  containing  coiled  larvae,  but  none  of  the  micro- 
filariae from  the  vaginal  region  show  any  evidence  of  a  sheath, 
and  accumulations  of  crumpled  hyaliue  ob.iccts  interpreted  as 
the  remains  of  discarded  vitelline  membranes  were  found  at  a 
higher  level  in  the  uterus,  .lugustine  was  able  to  see  no  evi- 
dence of  a  sheath  on  the  microfilariae  of  this  species  while  they 
were  in  capillaries  but  was  able  to  follow  its  formation  on  dry- 
ing slides.  He  concludes,  therefore,  that  the  sheath  is,  as  in 
other  sheathed  nematode  larvae,  the  loosened  but  unshed  cuti- 
cle from  an  incomplete  ecdysis.  This  conclusion  seems  to  us, 
however,  to  be  very  doubtful,  since  no  other  nematode  larvae 
are  known  to  molt  at  such  an  early  stage  in  development,  and 


since  two  other  molts  have  been  observed  during  the  course  of 
development  of  the  larvae  in  their  mosquito  hosts;  this  would 
bring  them  to  the  third  stage,  which  is  usual  for  infective  lar- 
vae in  intermediate  hosts  (see  p.  237).  Some  species  of 
filariae  are  not  provided  with  sheaths. 

The  larvae  are  in  a  very  immature  state  of  development. 
They  are  covered  by  a  layer  of  sub  cuticular  cells,  and  within 
the  body  have  a  column  of  nuclei  which  subsequently  develop 
into  the  esophagus  and  intestine. 

This  column  of  cells  is  broken  at  certain  definite  spots  rep- 
resenting the  future  position  of  the  nerve  ring,  the  excretory 
pore  and  cell,  and  the  anus.  There  are  also  a  few  large  cells: 
an  excretory  cell  just  posterior  to  the  excretory  pore,  a  genital 
cell  well  behind  the  middle  of  the  body,  and  a  group  of  three 
cells  previously  reported  as  genital  cells  2  to  4,  but  which 
Feng  (1936)  says  give  rise  to  the  anus  and  rectum,  and  which 
Abe  (1937)  says  belong  to  the  sphincter  between  intestine  and 
rectum,  and  are  ultimately  lost.  There  is  a  difference  of  opin- 
ion as  to  the  existence  of  a  stylet  at  the  anterior  end  of  the 
worm.  The  structure  so  called  appears  to  be  a  rudimentary 
mouth    cavity. 

Upon  ingestion  by  suitable  species  of  mosquitoes  the  larvae 
become  unsheathed  iu  the  stomach  and  penetrate  into  the  body 
cavity,  whence  the  majority  migrate  at  once  to  the  thoracic 
muscles,  where  development  to  the  infective  stage  takes  place. 
The  factors  which  determine  the  suitability  of  particular  mos- 
quitoes have  not  been  elucidated.  Development  takes  place 
readily  in  mosquitoes  of  a  variety  of  genera,  including  Ano- 
pheles, Culex  and  Aedes,  but  sometimes  nearly  related  species 
within  these  genera  differ  widely  in  their  ability  to  serve  as 
nurses.  For  example,  Culex  quitiquefasciatus  and  C.  pipiens 
are  good  hosts,  whereas  C.  vexans  is  not ;  and  Aedes  variegatns 
is  a  very  good  host  whereas  A.  aepi/pti  and  A.  albopictus  are 
not.  As  yet  nobody  has  succeeded  in  obtaining  development 
in  any  arthropods  other  than  mosquitoes. 

Upon  arrival  in  the  thoracic  muscles  the  larvae  become  qui- 
escent, lying  parallel  with  the  muscle  cells.  Here  in  the  course 
of  2  or  3  days  they  become  considerably  foreshortened,  often  to 
approximately  half  their  original  length,  and  at  the  same 
time  grow  considerably  in  girth,  assuming  what  is  known  as 
the  "sausage"  stage.  Only  the  caudal  tip  of  the  body  fails  to 
thicken,  and  is  retained  as  an  attenuated  tail-like  structure. 
Meanwhile  a  large  excretory  bladder  develops  and  subsequently 
a  large  rectal  cavity,  and  the  outlines  of  the  esophagus  and 
intestine  become  defined.  On  the  fifth  day,  according  to  Abe 
(1937),  the  larva  undergoes  its  first  molt,  the  cuticle  develop- 
ing an  annular  break  near  the  anterior  end.  After  this  molt 
the  larva  reaches  its  maximum  shortness  and  thickness  and  then, 
as  the  alimentary  canal  becomes  well  developed,  begins  to 
lengthen.  As  it  approaches  its  maximum  length  it  becomes 
active  again  and,  according  to  Abe  (I.e.),  undergoes  a  second 
molt  about  the  time  it  is  ready  to  leave  the  thoracic  muscles 
(In  his  experiments  on  the  13th  day).  The  loosened  cuticle 
breaks  near  the  middle  of  the  body  and  is  shed.  The  larvae 
now  become  active  and  migrate  out  of  the  thorax.  The  ma- 
jority go  through  the  neck  and  head  and  move  down  into  the 
interior  of  the  labium,  but  a  few  get  lost  and  can  be  fouud  in 
the  abdomen,  legs,  palpi,  etc.  Infective  larvae  commonly  reach 
the  labium  about  2  weeks  after  infection  in  warm  weather,  but 
have  been  known  to  complete  their  development  in  9%  days. 
In  the  labium  they  are  stimulated  by  warmth,  and  when  the 
mosquito  is  biting,  escape  through  the  delicate  membrane  where 
the  labella  join  the  shaft  of  the  labium.  The  larvae  do  not, 
of  course,  interfere  with  skin-piercing  as  do  the  larvae  of 
Habroncma  in  the  labium  of  Stomoxys,  since  in  mosquitoes 
the  labium  itself  is  not  a  piercing  or  sucking  organ.  After 
leaving  the  proboscis  and  becoming  free  on  the  skin  the  larvae 
were  believed  by  Fiilleborn  (1908),  on  the  basis  of  experiments 
with  Dirofilaria  imniitis,  to  penetrate  into  pores  and  enter 
through  unbroken  skin,  but  Yokogawa  (1938)  carried  out  a 
series  of  experiments  which  indicate  that  they  can  only  enter 
broken  skin,  and  presumably  in  nature  use  the  wound  made 
by  the  mosquito. 

Nothing  is  known  about  the  development  of  the  larvae  after 
they  enter  a  human  host  until  they  reach  maturity  iu  the  lym- 
phatic system.  Dirofilaria  immitis  requires  about  9  months  to 
reach  maturity,  and  it  is  improbable  that  IViichrrcria  bancrofti 
takes  any  longer,  if  as  long. 

Other  Fll.iriae 

The  life  cycles  of  comparatively  few  species  of  filariae  are 
known,  but  among  those  that  are  known  there  is  comparatively 
little  variation.  As  already  noted,  some  microfilariae  are 
sheathed  and  some  are  not,  but  there  is  no  evidence  that  the 
presence  of  a  sheath  has  a  "muzzling"  effect  in  keeping  the 
microfilariae  from  passing  in  or  out  of  the  capillaries,  as  Man- 
son  had  thought.     This  was  shown  by  O'Connor   (1931)   in  the 


288 


Fig.    194.      DEVELOPMKXT    OF    FIl.AK  I  (H  DKA 


A — -Mouth  parts  of  Simutium  dnmno»um,  fixed  in  alcohol,  cleared  in 
warm  clove  oil,  showing  position  of  larvae  of  Oiu^hocerca  volvulus 
emerging  and  in  situ,  B-E — O.  rohttlus  (B — Early  thoracic  form,  sec- 
ond day;  C — Thoracic  form,  seventh  day;  D--.SliKhtly  later  thoracic 
form;  E — Proboscis  form,  ninth  day).  F — Mature  larva  of  Wurhererui 
hancrofti  escaping  from  proboscis  of  Citlex  iaiiucnu.  G — Larvae  of 
Dirofiiaria  repens  in  AnophfUs  (11  days).  H — Wyrhfirpria  hancrofti 
larvae  two  days  after  entering  Aed^a  variegatuji.  I-Mature  larvae  of 
W.  hancrofti  in  thoracic  muscle.s  and  proboscis  of  itio>^(iuito.  J — Em- 
bryonic development  of  Loa  Ion.  K — Detailed  drawing  r)f  Witrhf^rprin 
hancrofti    larva,      L — Microfilaria    in    deeper    layers    of    mnjunctiva    in 


rase  with  disturbance  of  vision,  keratiti.s,  and  iritis,  M — Second  larval 
stage  of  Onchocerca  in  the  thoracic  muscles  of  Simulum  metallicum. 
uppro.^imately  4H  hours  after  fe.'ding  upon  infested  patient.  N — Third 
larval  stage  or  so-called  "sausage  form"  of  Onchorerca  on  edge  of 
thoracic  niusdes  of  S.  or  hi  arrum  several  days  after  feeding  upon  in- 
fested case.  A-E.  after  Blacklock.  O.  B..  1926.  Ann.  Trop.  Med.  v. 
20  (2).  F.  after  Francis.  E.,  1919.  Hyg.  Lab.  Bull.  117.  G.  H,  &  J. 
after  Fuelleborn.  F.  Handb.  path.  Mikr.  Jena  v.  6.  I  &  K.  after 
Chandler.  A.  C,  1940  (Figs.  Ifiri  and  IfiO).  L-N.  after  Strong,  et  al.. 
19:^4.   Contrib.   Dept.  Trop.   Med..   Harvard.   VI. 


289 


case  of  Wuchereria  bancrofti  and  by  Harwood   (1932)   in  the 
ease  of  Litomosoides  carinii. 

The  microfilariae  of  Onchocerca,  which  are  unsheathed,  differ 
from  those  of  other  filariae  in  that  they  live  in  the  skin,  and 
do  not  enter  eitlier  the  lymphatic  or  blood  systems.  The  adult 
worms,  living  in  subcutaneous  tissues,  are  encapsulated  by  the 
host  in  hard  nodules,  through  which  the  larvae  are  able  to 
burrow  and  escape.  The  salivary  secretion  of  the  intermediate 
hosts  (Simulium)  seems  to  exert  a  definite  chemotactic  effect 
on  the  microfilariae,  since  they  may  be  many  times  more  nu- 
merous in  the  stomach  of  a  fed  fly  than  in  a  comparable  quan- 
tity of  tissue. 

The  intermediate  hosts  are  usually  Diptera.  Fleas  were 
stated  by  Brein!  (1921)  to  serve  as  intermediate  hosts  for 
Dirofilaria  immitis  and  Summers  (1940)  corroborated  this, 
showing  that  development  would  occur  in  several  species  of 
fleas,  and  in  a  shorter  time  than  in  mosquitoes.  Noe  (1908) 
followed  the  development  of  Dipetalonema  (jrassH  in  a  tick, 
Shipicephalus  sanguineus;  the  microfilariae  of  this  species  are 
said  to  be  too  large  to  enter  the  blood  circulation  and  are  found 
m  the  lymph,  which  the  ticks  suck  more  than  they  do  blood  at 
the  beginning  of  a  meal.  This  work  has  not  been  confirmed 
and  is  open  to  suspicion  in  view  of  the  fact  that  the  embryos 
of  related  species  {Dirofilaria  reconditum,  Dipetalonema  per- 
stans)  live  in  the  blood  and  develop  in  mosquitoes.  Savani 
(1933)  has  also  reported  filariae  in  dog  ticks  in  areas  where 
Dirofilaria  immitis  is  common.  The  intermediate  hosts  of 
Wuchereria  and  Foleyella  are  various  mosquitoes;  of  Dipeta- 
lonema perstans  and  Mansonella  ozzardi,  Culicoides;  of  Loa  loa. 
Chrysops;  of  Onchocerca  spp.,  Simnlium  or  Culicoides;  and  of 
Dirofilaria,  fleas  and  mosquitoes. 

There  is  some  variation  with  respect  to  the  site  of  develop- 
ment in  the  intermediate  hosts.  The  majority  of  the  species 
studied — Tfuchereria  bancrofti,  Microfilaria  malayi  (adult  per- 
haps unknown),  Dipetalonema,  Mansonella,  Dirofilaria  recon- 
ditum, and  Onchocerca  spp. — develop  in  the  thoracic  muscles 
of  their  dipteran  hosts,  but  Loa  loa  develops  principally  in 
the  muscles  or  fatty  connective  tissue  of  the  abdomen  of  Chry- 
sops (Connal  and  Connal,  1922),  and  Dirofilaria  immitis  devel- 
ops in  the  haemocoele  of  fleas  and  in  the  Malpighian  tubules  of 
mosquitoes.  These  sites  of  development  are  of  great  interest 
in  view  of  the  similar  sites  utilized  by  Draschia  and  Habronema 
in  museoid  files. 


Fig.  195. 

Development  of  Wtichererm  bancrofti,  1 — Larva  10  hours  after  in 
fection.  2-4 — Larva  2-3  days  after  infection.  6-6 — Larva  four  days 
and  tliree  hours  after  infection.  7-8 — Larva  5V2  days  after  infection. 
1'  Larva  5  M*  days  after  infection,  just  before  first  molt.  2'-3' — Larva 
7^  days  after  infection.  4' — Larva  9V2  days  after  infection  of 
posterior  end  of  esopliagus.  5'-6' — Larva  11  days  and  10  hours  after 
infertioa. 


290 


CAMALI.ANINA 

Tlio  iiii'inlicrs  of  Imlli  sii|»"rfiiiiiilics  iif  tliis  siiIkikIit.  I'mih.iI 
liinoiilc;!  ami  Orin'iiiu'iiloidoa,  so  far  as  known  utilize  coin'iioiis 
as  intorniodiato  hosts.  Tlu'io  can  ho  no  doutit,  from  a  oonsid 
oration  of  tlio  habitat  ami  life  cycU-,  that  tho  Caniallanoidoa, 
ihvi'llinK  as  adnlts  in  the  alimentary  canal  of  aquatii'  liosts,  arc 
the  more  primitive,  and  that  the  tissue  dwcllinR  Draciincnloidca, 
sometimes  occurring  in  land  animals,  are  a  later  evolutionary 
development.  The  relation  of  these  two  groups  is  conip;iratilc, 
in  a  broad  way,  with  the  relation  of  the  Si)irnroidea  and  the 
Kilarioidea.  In  the  case  of  the  Filarioidca  a  habitat  in  the 
tissues  is  accompanied  by  evolution  of  a  new  method  of  exit  and 
rtiitrance  of  embryos  via  the  skin,  whereas  in  the  Dracuuculoidea 
it  is  accompanied  by  a  new — but  difTerent — method  of  exit  via 
the  skin,  suitable  for  an  aquatic  animal,  but  with  retention  of 
the  primitive  oral  path  of  entry. 


C.\M.VT,I..\NUS  SWEETI 

The  life  cycle  of  this  worm  was  worked  out  by  Moorthy 
(1038).  The  adult  worms  live  in  the  intestine  of  a  freshwater 
fish  (Ophiciplialus  flachiin)  and  produce  free  larvae  which  es- 
cape with  the  feces  of  the  host.  The  embryos  have  a  tinely 
striated  cuticle,  a  single  dorsal  denticle  or  boring  cuticular 
tooth,  and  fairly  well  differentiated  internal  organs.  On  reach- 
ing water  the  larvae  are  swallowed  by  suitable  species  of 
Cjirlops  and  reach  the  body  cavity  2  or  .S  hours  after  infection. 
These  larvae  undergo  the  first  molt  '2i  to  36  hours  later,  and 
the  second  one  after  -■)  to  7  days,  in  hot  weather.  The  third- 
stage  larvae  are  provided  with  ridged  jaws  suggestive  of  those 
of  the  adult,  and  have  three  unequal  mucrones  at  the  tip  of 
the  tail.  No  mention  is  made  of  these  larvae  becoming  en- 
cysted in  Cyclops.  When  infected  Cyclops  are  eaten  by  small 
fish  the  larvae  are  activated  by  fish  bile,  escape  from  their 
copcpod  hosts  and  undergo  further  development,  including  pos- 
sibly the  third  molt,  in  the  intestines  of  these  fish.  The  infec- 
tion of  the  final  host  is  thought  to  result  from  feeding  on  the 
second  intermediate  host,  and  the  larvae  undergo  their  fourth 
and  final  molt  in  the  intestines  of  this  host,  acquiring  the  adult 
type  of  mouth.  Whether  the  intervention  of  a  second  inter- 
mediate host  is  optional  or  obligatory  was  not  determined,  but 
in  nature  it  would  probabl.v  be  the  usual  thing,  since  the  final 
liost  does  not  ordinarily  feed  on  Cyclops  directly. 


A-B — CamaUanuB  gtreeti  (A — Head,  fourth  stage;  B — Tail,  same). 
C — Procamailanus  fulvidraconin,  mature  embryo.  D — Uninfected  Cy- 
clops. K — Cyclops  infected  with  Dra4'uncutu«  medinfnsU.  F-G — Dra- 
cuneulus  medinensis  (F — Cephalic  region  undergoing  second  molt;  G — 
Tail,  same.  A-B,  after  Moorthy,  19:i8,  J.  Parasit.  v.  24  (4).  C.  after 
Li,  1935.  J.  Parasit..  v.  21  (2).  D.  F,,  after  Fuelleborn.  1913.  Filario- 
•en  des  Mensch.     F.  G.  after  Moorthy.   1938,  Am.  J.  Hyg.  v.  27    (2). 


.No  encysted  forms  of  ('.  siicti  were  fouiul  in  fish  hosts,  nor 
was  any  evidence  found  of  their  penetrating  the  walla  of  the 
intestine,  but  caniallaniil  larvae  of  another  type  were  found 
encysted  in  the  body  cavity,  loosely  attached  to  the  intestines. 
These  were  observed  to  exeyst  when  eaten  by  Opliiciphaliis 
(jachua,  but  failed  to  undeugo  further  develoimient  in  that  host. 

An  essentially  .similar  develoi)nu'nt  in  Cyclops  has  been  dem- 
on.strated  for  I'rocamallanus  fill  roil  raconis  by  Li  (l!t3.">),  except 
that  only  one  molt  was  observed.  It  seems  i)robal>le  that  the 
first  one  was  overlooked,  since  Li's  figure  of  a  (i-day  old  larva 
corresponds  with  Moorthy 's  second  stage  larva  of  Camallaniix, 
and  his  second  stage  larva  with  Moorthy 's  third  stage.  How- 
ever, Fereira  vl  al  (Ifi.Sfi)  state  that  P.  cearetisis  develops  only 
to  the  second  stage  in  Ditiptomiis,  the  third  and  fourth  stages 
being  |)a.sscd  in  the  intestines  of  the  fiy  of  a  fish  other  than 
the  definitive  host.  Although  they  speak  of  this  host  as  a 
"waiting  host"  (i.e.,  transport  host)  it  would  appear  to  be  a 
true  second  intermediate  host  if  their  observation  is  correct 
that  development  to  the  third  stage  does  not  occur  in  Cyclops, 

It  will  be  seen  that  the  canuillanid  life  cycle  is  e-ssentially 
the  same  as  that  of  Hpiroxys  or  of  Gnatlwstoma  except  for  the 
l)roducti"n  of  free  embryos  instead  of  eggs  by  the  parent 
worms. 


DrACUNCULUS    ilEDlNEXSIS 

The  adult  female  guinea  worm,  nraciinculiis  medinensis, 
when  preparing  for  parturition,  appears  in  the  subcutaneous 
tissues  of  her  host  and  jiroduces  a  small  ulcer  on  the  surface  of 
the  skin.  Upon  stimulation  by  chilling  of  the  skin,  which  hap- 
pens in  nature  when  the  skin  is  plunged  into  water,  she  con- 
tracts violently  in  such  a  manner  that  a  portion  of  the  larva- 
filled  uterus  is  prolai)sed  through  a  rupture  in  the  cuticle,  and 
the  prolapsed  portion  of  the  uterus,  bursting,  liberates  a  small 
cloud  of  larvae.  These  larvae  are  unusually  large  (about  OOO 
/;»  long),  have  a  striated  cuticle,  a  cuticular  boring  tooth  or 
denticle,  well-developed  esophagus  and  intestine  with  dilated 
lumen,  and  a  long  filiform  tail. 

These  larvae  swim  about  in  water  and  undergo  further  devel- 
opment only  after  being  swallowed  by  certain  species  of  cope- 
pods.  The  details  of  their  development  was  worked  out  by 
Moorthy  (1938).  They  reach  the  body  cavity  a  few  hours 
after  being  swallowed.  They  undergo  two  molts  in  the  body 
cavity,  the  first  one  on  the  .5th  to  7th  day  after  infection,  the 
second  on  the  8th  to  12th  day  in  hot  weather.  They  start  under- 
going the  second  molt  before  casting  off  the  exuviae  of  the 
first.  The  larvae  grow  very  little  in  size,  and  actually  de- 
crease in  length  due  to  the  loss  of  most  of  the  filamentous  tail. 
The  third  stage  larvae  increase  slightly  in  size  for  about  a 
week  after  the  second  molt,  but  after  that  undergo  no  further 
development;  they  are  infective  for  the  definitive  host  4  to  8 
days  after  the  exuviae  of  the  second  molt  are  shed.  They  have 
a  long  esophagus  of  the  adult  type,  and  four  mucrones  at  the 
tip  of  the  tail.  They  remain  active  in  the  body  cavity  of  the 
Cyclops  for  4  or  o  weeks,  but  subsequently  coil  up  and  become 
quiet,  but  are  not  encysted.  In  addition  to  the  usual  type  of 
larvae  Moorthy  also  found  a  small  proportion  (1:  900)  of 
"abnormal"  larvae  in  which  the  tail  is  malformed.  Moorthy 
suggested  timt  these  may  have  been  males,  but  it  is  more  likely 
that  they  should  be  regarded  as  abnormal  individuals. 

The  early  development  of  the  larvae  in  the  definitive  host  has 
not  been  followed.  Sexually  mature  females  12  to  24  mm  in 
length  were  found  by  Moorthy  and  Sweet  (1938)  in  deep  con- 
nective tissues  of  experimentally  infected  dogs  67  days  after 
infection,  and  Moorthy  believed  that  at  this  time  fertilization 
had  already  taken  place.  Migration  of  the  worms  to  the 
subcutaneous  tissue  and  the  formation  of  an  ulcer  for  the 
egress  of  larvae  occurs  about  a  year  after  Infection  in  man. 

An  essentially  similar  life  cycle  occurs  in  the  case  of  D. 
ophithnsis  of  garter  snakes  (Brackett,  1938).  Cyclops  infected 
with  this  species  may  be  eaten  by  tadpoles  and  possibly  other 
transijort  hosts;  in  tadpoles  the  larvae  were  found  to  remain 
free  and  viable  in  the  body  cavity  for  at  least  2  weeks,  but  no 
further  growth  or  development  was  observed. 

The  Philometridae,  which  have  been  found  in  a  great  variety 
of  parenteral  locations  in  aquatic  hosts,  have  a  life  cycle  es- 
sentially similar  to  that  of  Dracunculits.  Thomas  (1929)  found 
that  the  first-stage  larvae  of  Fhilometra  nodtilosa  are  devoured 
by  Cyclops  and  invade  its  body  cavity.     Attempts  at  infection 


291 


Fig.    197.      DEVEIAU'lIENT   OF   C.'i.MALI.ANlXA 


A-TI — Cnmtitlnnus  sivreti  (A — First  stage  larva;  B — Anterior  end  >in- 
dergoing  second  molt;  C — Posterior  end  undergoing  second  molt.  D — 
Head,  third  stage).  E-J — DracuiiaiUis  medineiixix  (E — First  stage, 
anterior  end;  F — Same,  posterior  end;  G — Anterior  end  moulting  larva; 
H — Posterior  end;  I — Posterior  end  of  normal  larva  undergoing  first 
molt;  J — Normal  third  stage  larva),  K-L — Procamnllnnus  iulvidriicrinis 
(K — Larva.  6  days  old;   L — Larva,    14  days  old).     M — Cross-section   o£ 


guinea  worm  showing  uterus  filled  with  enihryos.  -X  about  30  {after 
Leuckart).  N  -Diagram  of  guinea  worm  iti  the  skin  at  the  time  of 
blister  formation.  A-D,  after  Moorthy,  1938,  J.  Parasit.  v.  ?4  (4). 
E-J,  after  Moorthy.  1938,  Am.  J.  Hyg.,  v.  27  (2).  K-L,  after  Li.  1935. 
J.  Parasit.  V.  21  (2).  M,  N,  after  Chandler,  1940,  Introduction  to 
Parasit. 


■M2 


•<>r  nsli  from  Citclopx  a  wcok  aftrr  iiifrctiim  failod,  pii'sumalily 
hwaiisi'  of  iiia(lo<niatc  timi"  for  tlio  larvar  lo  ri'aili  llio  iiifi'ctivc 
staRC.  Fiiruyama  (  I!i:f4l  suci'ccilcii  in  cimipU'liiiK  llio  life 
cycU",  ill  till'  case  of  /'.  ftijimoloi.  Iiv  foi'diiiif  oxpi'riini'iitally 
infoctod  Cui'lops  to  thi"  liotiiiilivo  liost.  Voiins  iiialc  ami  finialc 
worms  won'  found  in  tlu"  liody  cavity,  from  wluMici'  tin'  finialrs 
siilisoiiut'iitly  mittrati'd  to  their  final  liahitat  in  tlio  tins.  In 
I'liilonu'tridao  tlio  motliod  of  ivscapo  of  the  larvae  is  not  as  sp<> 
eializod  as  in  the  ease  of  hrarunviiliis :  the  larvae  of  some  spe 
eies  escape  via  the  oviducts  of  the  fish,  while  in  the  case  of 
I',  fiijininloi  the  ripe  viviparous  females  leave  the  fins  of  their 
host,  rupture,  and  liberate  their  larvae  into  the  water.  It  is 
easy  to  .see  how  the  ffuine.-i  worm  life  cycle  could  h;ivc  evulvnl 
from  the  camallanoid  type  liy  the  substitution  of  escape  i)f 
eiuliryos  IhroUKh  the  skin  for  escape  via  the  anus,  which  would 
be  very  simple  ia  the  case  of  parasites  which  reproduced  in 
parenteral  habitats  in  acpiatic  hosts. 

TRICHUROIDEA 

The  membors  of  this  superfamil.v,  with  the  exccjition  of 
Trirhiiiilhi  and  CjixtDopxis  (see  below  1,  have  a  simjile  life  cycle 
eharactorizod  by  embryoiiation  of  eggn  outside  the  body  of  the 
host;  access  to  a  new  host  by  swallowing  of  crks  coutainiuK 
first  stage  larvae  provided  with  an  oral  spear;  au<l  direct  mi 
gration.  via  the  blood  stream  if  outside  the  alimentary  canal,  to 
the  site  of  developmi'nt.  without  jireliminary  development  el.se- 
where  in  the  body.  The  life  cycle  of  CapiUaria  col  it  m  hii  r ,  re- 
cently worked  out  in  detail  by  Wehr  (IPH!)),  will  serve  as  an 
example  of  the  t.vpical  Trichuroidea. 

C'APII.I..\RI.V  COHMB.VF, 

The  adults  living  in  the  small  intestine  are  more  or  less  im 
bedded  in  the  mucosa,  but  the  eggs  make  their  way  into  the 
lumen  and  escape  with  the  feces  in  an  unsegniented  state. 
I'nder  favorable  conditions  of  temperature,  moisture,  and  oxy- 
gen segmentation  occurs  slowly,  the  first  cleavage  occurring  in 
about  48  hours,  the  morula  stage  in  about  .'•!  days,  and  the  in- 
fective first-stage  larva  in  t>  to  8  days.  No  molting  was  ob- 
served to  occur  in  the  egg.  and  hatching  does  not  normally 
take  place  before  the  egg  is  swallowed  by  a  host.  The  entire 
development  from  newly  hatched  larvae  to  adult  worms  takes 
place  in  the  small  intestine  of  the  definitive  host. 

The  first-stage  larva,  like  all  other  trichuroid  larvae,  has  an 
oral  spear.  It  has  a  long  slender  esophagus  which  posteriorly 
lies  superficial  to  and  only  partly  imljcdded  in  the  stichosome, 
which  consist  of  two  rows  of  opposing  cells.  The  intestine  is 
much  shorter  than  the  esophagus  (ratio  1:3.."))  and  is  termi- 
nated by  a  short  rectum.     The  anus  is  subterminal. 

The  first  molt  occurs  between  7  and  14  days  after  infection. 
The  second-stage  larvae  are  slenderer,  and  appear  to  have  no 
oral  spear;  the  stichosome  consists  of  only  a  single  row  of  cells, 
and  the  intestine  is  relatively  longer.  The  second  molt  occurs 
about  14  days  after  infection.  The  third  stage  larvae  are  still 
slenderer,  with  relatively  longer  intestine,  and  the  genital  iirim- 
ordium  is  long.  The  third  molt  occurs  between  14  and  Til  days 
after  infection.  The  fourth-stage  larvae  are  very  slender,  and 
sexually  differentiated.  The  time  of  the  final  molt  was  not 
determined,  but  some  sexually  mature  adults  with  eggs  were 
found  by  the  liHh  day. 

Other  TRicnrRiDAE 

The  available  evidence  indicates  that  the  life  cycle  of  Tri- 
chiirtK  is  essentially  the  same  as  that  of  CupiUaria  ciilnmlxii , 
and  it  is  probalile  that  it  is  also  the  same  for  other  species 
of  CapiUaria  which  inhabit  the  intestines  of  their  hosts.  The 
aliility  of  CapiUaria  larvae  to  use  transport  hosts  was  shown 
by  Wehr's  (19.'!6  i  demonstration  that  earthworms  can  serve  as 
vectors  for  C.  annulata,  the  crop-worm  of  chickens.  Fiilleborn's 
(l!l23b)  figures  of  Trichuris  trichiura  larvae  are  strikingly 
similar  to  Wehr's  figures  of  the  first  stage  larva  of  CapiUaria. 
.Mthough  Neshi  (IBIS,  quoted  by  Yokogawa,  l!l:20)  reported  the 
finding  of  four  larvae  of  Trichiiris  vtilpix  in  the  lungs  of  a  dog 
■Jl  hours  after  experimental  infection,  such  migration  on  the 
l>art  of  Trichuris  has  not  been  observed  by  other  workers 
either  in  normal  or  abnormal  hosts  (see  Fiilleborn,  ]!l23a). 

.As  Vogel  (li)30)  pointed  out,  the  entire  group  of  Trichuroi- 
dea show  a  remarkable  tendency  to  localization  during  their 
larval  development  in  paiticular  organs  or  tissues — what  Vogcl 
called  "organotropism."  In  all  cases  except  Trifliiiirlla  this 
organotropism  continues  throughout  the  adult  life  of  the  worms. 
Different  species  of  Trichuridae  are  known  to  develop  and  live 
as  adults  in  the  esophagus,  stomach,  small  intestine,  cecum, 
colon,  respiratory  tree,  liver,  spleen,  urinary  bladder,  and 
epithelium.  The  available  evidence  indicates  that  the  newly 
hatched  larvae  of  those  species  which  do  not  grow  to  maturit.v 
in  the  intestine  itself  reach  their  destination  by  burrowing  into 


the  inlestiii.'il  wall,  entering  the  circulatory  system,  .'ind  escap- 
ing from  the  capillaries  in  the  organ  in  which  tlu'.v  are  to  de 
veloii  (iood  evidence  for  this  li;is  been  obtained  in  the  c'lsc  of 
CapiUaria  iKpalira  of  the  liver  of  rals.  Vogel  (lit.'iO)  showe<l 
that  if  young  larvae  of  C.  Inpat ira,  recovered  frinu  the  liver  a 
few  <l;iys  ;iftei'  infection,  were  planted  in  the  si)leen,  lungs,  or 
under  the  skin,  a  few  would  succeed  in  reaching  the  liver. 
Normall.v  this  worm  penetrates  the  cecum,  sometimes  as  early 
as  (i  hours  after  infection  (Lnttcrmoser,  l!!38b),  and  is  carried 
directly  to  the  liver  via  the  hejjatic  |)ortal  system  (Fiilleborn, 
l'.>;;4;  .Nishigori,  lil:;.")),  only  an  exceiitional  few  peru't rating 
into  the  abdominal  cavity,  or  being  carried  beycnid  the  liver 
to  the  lungs  :uid  systemic  cii'cnlation.  In  the  cise  of  Tri- 
(■liiisi>n\oi<l(  s  crassifaiula  of  the  nr-in:u'y  bt.-idder  of  i-ats,  ^'oko- 
gawa  (UfJl)  fed  embryonatcd  eggs  to  rats  and  1  to  4  days 
later  fouini  a  few  larvae  in  the  abdominal  and  pleural  cavities 
and  the  lungs;  these  he  thought  were  Trirlmsomoidrs  larvae 
from  his  fei'ding.  but  their  size  makes  it  evident  that  they 
were    not. 

.\n  unusual  situation  with  resjiect  to  transfer  of  infection  to 
new  hosts  exists  in  the  case  of  CapiUaria  hi'patica,  which  is  sug- 
gestive of  a  inissible  step  in  the  evolution  of  the  TrichineUa  life 
cycle.  The  eggs  of  this  worm  are  deposited  in  the  liver  tissues 
of  rats  or  mice,  and  reni;iiii  there  in  an  early  stage  of  devel- 
opment (one  to  four  cells),  viable  for  at  least  7  or  8  months 
(Luttermoser,  l!t.'i8a).  Only  exceptionally  do  any  of  the  eggs 
escape  from  the  liver  to  be  voided  with  the  feces,  and  eating  of 
an  infected  liver  by  a  susceptible  animal  cannot  result  in  infec- 
tion because  the  nonembryonated  eggs  are  not  infective. 
Momma  (1!I30)  suggested  tlies  as  a  factor  in  disseminating  the 
eggs  from  decaying  carcasses,  and  also  showed  that  eggs  in 
the  feces  of  cats  that  have  fed  on  infected  rats  .-ire  viable. 
Troisier  and  Di'schiens  (19311)  and  Shorb  (1931)  independently 
suggested  that  the  usual  method  of  transmission  in  n:ituie  is 
by  ingestioii  of  eggs  that  have  become  embryonatcd  after  being 
freed  from  the  liver  of  an  infected  animal,  either  by  decompo- 
sition or  by  being  eaten  Ity  another  animal,  usually  the  latter. 

Trichinell.\  spir.\i,is 

The  life  c.vcle  of  this  worm  is  unique  among  parasitic  nema- 
todes in  that  the  period  of  waiting  for  a  new  host  is  pas.sed  in 
the  pniental  host  instead  of  in  the  open  or  in  an  intermediate 
host.  The  life  cycle  of  CapiUaria  hepatica,  described  above,  is 
a  ste|i  in  this  direction,  since  in  this  case  there  are  two  periods 
of  waiting,  one  in  the  liver  tissue  of  the  parental  ho.st,  the 
other  (the  usual  one)  after  embryonation  in  the  o])eu.  In  the 
case  of  TrichineUa  this  double  period  is  reduced  to  one  by  the 
complete  elimination  of  the  usual  period  of  waiting  outside  the 
host,  resulting  from  (1)  precocious  development  to  a  burrow- 
ing larval  stage  in  the  uterus  of  the  mother,  and  (2)  consequent 
ability  to  infect  the  tissues  of  the  parental  host  and  to  sub- 
stitute development  in  this  for  the  usual  development  in  the 
open  or  in  an  alternate  host. 

The  life  cycle  of  this  worm  was  one  of  the  first  to  be  worked 
out  in  its  essential  features,  contributions  having  been  made  by 
Herbst,  Kiicheumeister,  Leuckart,  and  Virchow  from  184S  to 
ISliO.  The  first  entirely  cojrect  account  of  it  was  given  by 
Leuckart  (IS(iO).  The  adult  worms  live  in  the  small  intestine. 
The  females  produce  no  egg  shells,  and  the  ova,  unlike  those 
of  other  Trichuroidea,  develop  precociously  in  the  uterus,  being 
born  as  active  burrowing  larvae,  though  in  a  very  early  stage 
of  development,  suggestive  of  microfilariae.  There  is  an  oral 
spear  as  in  other  members  of  the  group,  but  the  alimentary 
canal  is  rudimentary.  This  very  immature  larva  enters  the 
circulation,  passing  capillaries  in  lioth  liver  and  lungs,  and  is 
distributed  over  the  entire  body.  Presumably  as  the  result  of 
a  special  organotropism  as  suggested  by  Vogel  (1930),  the 
attraction  in  this  particular  case  being  the  striated  voluntary 
muscles,  the  larvae  leave  the  caiiillaries  and  immediately  pene- 
trate through  the  sarcolemma  into  the  interior  of  muscle  cells, 
Iiossibly  by  means  of  extra-corporeal  digestion.  As  to  whether 
the  larvae  actually  penetrated  into  the  muscle  cells  has  long 
been  a  matter  of  dispute,  but  seems  finally  to  have  been  set- 
tled by  Jensen  and  Roth  (1938).  Immediately  after  penetra- 
tion, accomplished  b.v  a  boring  movement  of  tlie  spear-bearing 
head  end,  the  larva  is  seen  lying  lengthwise  .iust  under  the 
.sarcolemma,  or  between  the  sarcolemma  and  adjacent  muscle 
cells,  .leusen  and  Koth  think  it  likely  that  a  histolytic  enzyme 
is  also  involved  in  the  i)enetration  of  the  muscle  cells  and  in 
dissolving  the  fibrillae  inside. 

Once  inside  the  cells  the  larvae  come  to  rest  and  begin  their 
growth  and  differentiation,  the  muscle  substance  meanwhile 
undergoing  degenerative  changes.  By  the  17th  day,  according 
to  .Jensen  and  Roth,  the  larva  has  grown  from  100  to  400  or 
.jOO  m  in  length  and  has  its  esophagus  and  intestine  clearly  dif- 
ferentiated. According  to  Stiiubli,  however,  it  ma.v  have  in- 
creased its  length  10  times,  to  800  to  1,000  M,  in  from  10  to  14 
da.vs.     After  11  days  it  begins  to  roll  up  spirally  in  a  spindle- 


293 


Fig.    198.      DEVELOPMENT   OF  TRICHUROIDEA 

of  victim  uf  trichiniasis.  F-J—CripinniU,  cohtmbne  (F— Anteiior  end  of 
unhatched  first  stage  larva;  G— Late  first  stage  larva  from  intestine  of 
pigeon  7  days  after  infection;  H— Embryo  or  unhatched  first  stage 
larva;  I— Second  stage  larva;  J— Third  stage  larva_  in  _molt._  A-E,  after 
Chandler.    1940.    introduction   to   Parasitology. 


A-C — Stages  in  calcification  of  TrichineUa  (A — Ends  calcified;  B — 
Thin  layer  of  calcareous  material  over  whole  cyst;  worm  beginning  to 
degenerate.  C — Complete  calcification).  D — Larvae  of  TrichineUa  spv- 
rails  encysted  in  striped  muscle  fibers  in  pork.  Camera  lucida  draw- 
ing of  cysts  in  infected  sausage.  E — Larvae  of  trichina  worms  burrow-  „  „  ,^  ,  a,  ,  n  i,  r 
ing  in  huniar,  fiesh  before  encystment,  from  preparation  from  diaphragm  U.S.U.A.    tech     hsull.   b 


F-J.   after   Wehr,    1939, 


294 


Fig.  199.     TRICHURon)K.\   -VND  ])I  OCTOPHYMATOIDEA 


A-D — Cijatnnpxiii  ncipenneri  (A — Embrj'o;  B — Head,  male;  C — Adult 
female;  D — Conneclion  of  esojihageal  region  and  body  proper  of  fe- 
male.) E — CnntonpKitt  larvii  enc.vsted  in  appendage  of  Gnnniiantu  jjhttth 
cheir.  Fl —  TrichineUa  npimlui  (F.  Molt  at  fourth  hour;  G — Molt  after 
14  hours;  H — Third  molt  of  female  after  48  hours;  I — Molt  after  70 
hours).  J-K — Trichuris  friyliiiirn  (J — From  the  (.-eeum  of  a  guinea  pig: 
K — Larva  pressed  from  egg).    1,-R — Tiirliinella  spiralis    (  L — .Section  of 


intestine  showing  female  in  lunii-a  propria;  M — Young  larva  entering 
muscle;  N — Young  larvae;  ()-R — Stages  in  encystment  and  calcifica- 
tion). S-T — Eiislrongi/lides  (S — Head:  T — Tail).  A-D.  and  E,  after 
Janicki,  ('.,  and  Rasin.  F..  19:10.  Ztschr.  Wise.  Zool.  v.  136.  F-I, 
after  Kreis.  H.  A.,  1937,  Zentralbl.  f.  Bakt.  v.  138.  J-K,  after  Fuelle- 
born,  F..  1923,  Arch.  Schiffs--u.  Tropen.  v.  27.  L-R,  after  Staubli,  in 
Handb.  path.   Mikroorg.   v.   8.      Remainder  original. 


295 


shaped  enlargement  of  the  muscle  fiber,  and  after  4  to  6  weeks 
becomes  encapsulated.  If  not  ingested  by  a  host  suitable  for 
their  future  development,  the  larvae  ultimately  die  and  there 
is  fatty  degeneration  and  finally  calcification  of  the  cysts. 
Trichinae  are  said  to  remain  alive  and  infective  for  as  long  as 
11  years  in  the  muscles  of  swine,  and  to  have  lived  for  12  to  24 
years  in  man,  according  to  Baylis.  Prenatal  infection  with 
trichinae  has  been  demonstrated  in  guinea  pigs  by  Roth 
(1936);  Mauss  got  negative  results  in  rats,  rabbits  and 
hamsters.  In  spite  of  the  fact  that  the  larva  undergoes  so 
much  growth  and  differentiation  Staubli  was  unable  to  detect 
any  evidences  of  molts,  and  the  writer  has  seen  no  reports  of 
any  being  seen  by  later  observers.  By  analogy  with  other 
nematodes,  however,  it  seems  probable  that  the  infective  larvae 
have  undergone  at  least  two  molts.  Infection  has  not  been  ob- 
tained with  larvae  less  than  19  days  old  and  only  after  21  days 
can  one  obtain  a  high  percentage  of  infections.  This  seems  to 
indicate  that  the  larvae  undergo  a  change,  such  as  a  molt, 
prior  to  that  time. 

When  the  larva  has  undergone  its  full  development,  whether 
encapsulated  or  not,  it  is  infective  when  eaten  by  another  ani- 
mal. Development  in  the  intestine  is  extremely  rapid,  sexual 
maturity  being  reached  and  copulation  occurring  on  the  third 
dav,  and  embryo  production  beginning  on  the  fifth  day.  Ac- 
cording to  Kreis  (1937)  there  are  four  molts  in  this  brief 
period,  at  about  4,  12,  48  and  70  hours  after  ingestion.  How- 
ever, his  evidence  is  not  very  convincing.  According  to  recent 
investigations  one  molt  was  obtained  after  ingestion  and  the 
cuticle  of  the  resultant  nema  passed  uninterrupted  over  the 
vulva,  indicating  that  at  least  one  more  molt  would  be  neces- 
sary before  maturity. 

It  is  evident  from  this  account  that  Tiichinella  spiralis  is  not 
only  unique  among  nematodes  in  utilizing  the  parental  host  as 
a  sole  resting  place  while  awaiting  an  opportunity  to  gain  ac- 
cess to  another  host  by  cannibalism  (insofar  as  it  passes  from 
individual  to  individual  of  one  species)  but  it  is  also  unique 
among  the  Triehuroidea  in  having  different  "organotropisms" 
for  the  larval  development  and  for  the  adult  development,  the 
former  being  the  striated  voluntary  muscles,  particularly  the 
most  active  ones  (pectoral  and  tongue),  the  latter  the  mucous 
membrane  of  the  small  intestine. 

Cystoopsis  acipensem 

This  is  an  aberrant  worm  with  respect  to  both  its  morphology 
and  its  life  cycle.  The  females  with  their  large  spherical 
bodies  and  the  small  cylindrical  males  live  in  pairs  in  cyst-like 
cavities  just  under  the  skin  of  young  sturgeons.  According  to 
Janicki  and  Rasin  (1930),  a  well-developed  vulva  and  muscular 
vagina  are  present,  but  they  seem  to  be  used  only  for  the  en- 
trance of  sperms  and  not  for  the  exit  of  eggs.  The  spherical 
body  is  filled  with  numerous  coils  of  the  uterus  filled  with 
embryonated  eggs.  These,  according  to  the  authors  quoted, 
escape  only  by  a  bursting  of  the  thin  wall  of  the  cyst  and 
rupture  of  the  parasite. 

Experimentally  the  embryonated  eggs  are  eaten  by  certain 
species  of  amphipods,  and  the  larvae,  liberated  in  the  stomach, 
penetrate  into  the  body  cavity.  The  young  larvae  possess  a 
mouth  spear  like  other  Triehuroidea,  and  are  in  a  very  early 
stage  of  development.  At  the  end  of  about  2  weeks  they  have 
reached  their  full  size,  and  then  migrate  into  the  appendages 
or  into  muscle  layers.  Here  they  coil  up  after  the  manner  of 
Trichinella  larvae  and  soon  become  encapsulated.  The  capsule 
thickens  with  time,  and  by  the  end  of  3  months  cannot  be 
broken  under  a  coverglass.  No  experiments  have  been  per- 
formed to  prove  the  infectiousness  of  the  larvae  encysted  in 
Gammarus,  but  there  seems  to  be  no  reasonable  doubt  but  that 
•  young  sturgeons  are  infected  by  eating  amphipods,  and  that  the 
young  worms  migrate  through  the  tissues  of  the  host  to  their 
location  in  the  skin  as  do  some  species  of  Trichuridae. 


DIOCTOPHYMATINA 

The  life  cycles  of  members  of  this  group  are  very  imper- 
fectly known.  The  available  information  concerning  the  genus 
Enstrongylides  has  been  summarized  by  Cram  (1927).  Larvae 
described  by  Rudolphi  as  Filaria  cystica  from  under  the  peri- 
toneum and  in  the  abdominal  muscles  of  certain  Brazilian  fish 
were  regarded  by  Jagerskibld  as  belonging  to  this  genus. 
Ciurea  (1924)  found  similar  larvae  in  other  fish  from  the 
Danube,  and  he  also  regarded  them  as  belonging  to  Eustrongi/- 
tides.  Larvae  found  in  Brazilian  fishes  by  Schneider  and  by 
Leuckart  are  stated  by  Jiigerskiold  to  resemble  E.  ignotus  of 
water  birds. 

Chapin  (1926)  found  the  preadult  stage  of  this  species  in 
Fiindulus  diaphanus  at  Washington,  D.  C.  From  one  to  three 
specimens  were  found  in  each  fish,  and  adult  characters  could 


be  seen  beneath  the  last  cuticle,  corresponding  exactly  to  those 
of  adult  worms  found  by  him  in  Ardea  herodias  from  the  same 
locality. 

More  recently  Mueller  (1934)  reported  similar  larvae  from 
Fttnduhis,  in  cysts  attached  to  the  mesenteries.  They  were  100 
mm  long  by  0.685  mm  in  diameter,  blood  red  in  color,  and  the 
head  was  provided  with  12  papillae,  in  2  circles  of  6  each,  char- 
acteristic of  the  genus.  Von  Brand  (1938)  found  a  high  per- 
centage of  Finulidus  from  Chesapeake  Bay  parasitized  with 
this  same  larval  form;  individual  fish  harbored  from  1  to  8 
worms.  Von  Brand  states  that  the  encapsulated  nematodes  did 
not  harm  the  host,  but  that  after  the  host  died  they  left  their 
capsules  and  endeavored  to  escape  from  the  dead  host  by  bur- 
rowing through  the  tissues,  eventually  emerging  through  the 
gill  region  or  body  wall.  He  Avas  able  to  keep  the  worms  alive 
on  sterile  nutrient  media  for  as  long  as  2  months,  but  there 
was  no  growth  or  development. 

The  larvae  found  by  Ciurea  are  large,  28  to  70  mm  long  by 
264  to  539  /^  wide,  and  are  rose-red  or  brown-red  in  color.  On 
each  side  of  the  body  near  the  anterior  end  is  a  row  of  small 
lateral  papillae.  The  mouth  aperture  has  the  form  of  a  cleft 
and  has  three  small  pointed  papillae  on  each  side  of  it,  and 
three  larger  papillae  just  outside  of  these.  The  larvae  have  tails 
of  two  types,  one  enlarged  near  the  end  and  regarded  as  that  of 
the  male,  and  the  other  rounded  off  without  enlargement  and 
regarded  as  that  of  the  female.  Whether  the  fish  are  first  or 
second  intermediate  hosts  is  unknown.  The  thick-shelled  eggs 
are  undeveloped  when  they  leave  the  body  of  the  host. 

Even  less  is  known  about  the  life  cycle  of  Dioclophiiwn 
reiiale.  The  adults  are  usually  found  in  the  pelvis  of  the  kid- 
neys, partieularlv  the  right  one,  where  they  eventually  destroy 
the  entire  pareiichvma.  Worms,  often  immature,  are  frequently 
found  in  other  locations,  particularly  in  the  peritoneal  cavity. 
The  eggs,  in  an  unsegmented  condition,  normally  escape  from 
the  body' with  the  urine.  They  develop  slowly  in  water,  re- 
quiring from  1  to  7  months  for  embryonation,  according  to 
the  temperature,  and  then  remain  viable  for  at  least  2  years, 
although  they  do  not  hatch.  Beyond  this  point  nothing  is 
definitely  known  about  the  life  cycle,  but  the  frequency  of  in 
fection  in  fish-eating  animals  makes  its  highly  probable  that 
fish  serve  as  vectors  for  this  worm  as  well  as  for  Eustrongyhdes. 
Ciurea  (1921)  found  a  specimen  63  cm  long  in  the  peritoneal 
cavity  of  a  dog  fed,  between  3  and  4  months  previously,  on  14 
specimens  of  a  cvprinid  fish  ildiis  idiis)  from  the  Danube,  Init 
it  is  doubtful  whether  the  worm  was  actually  acquired  from 
this  feeding.  Ciurea  also  found  an  active  larva  in  the  muscles 
of  Idus  which  he  thought  might  be  that  of  Dioclophyma.  but 
his  figure  and  discription  are  more  suggestive  of  an  ascarid 
larva.  Swales  (1933)  reported  D.  reiialc  as  a  very  common  and 
important  parasite  of  mink  in  Canada,  and  stated  that  on  mink 
farms  the  infection  was  definitely  associated  with  the  feeding 
of  fish  to  these  animals. 

It  has  generallv  been  assumed  that  Dioctophi/ma.  after  enter- 
ing the  alimentaiv  canal  of  a  definitive  host,  is  carried  via  the 
blood  stream  to  the  kidneys  as  a  young  larva,  there  to  undergo 
its  growth  to  maturity.  Its  occurrence  in  the  peritoneal  cavity 
was  thought  to  be  accidental  and  rare,  and  due  to  rupture  of 
the  cvst-like  remnant  of  the  kidneys  after  the  complete  atrophy 
of  its  parenchvina.  As  a  matter  of  fact,  however,  the  worms 
are  very  frequently  found  in  the  abdominal  cavity  of  dogs,  in 
the  majority  of  cases  without  evidence  of  damage  to  the  kid- 
neys. Wislocki  (1919)  found  them  in  that  location  in  every  one 
of"  12  dogs  which  he  examined,  and  in  only  two  cases  could  a 
portal  of  entry  through  a  partially  destroyed  kidney  be  sur- 
mised. Brown,  Sheldon  and  Taylor  (1940)  found  13  of  20 
■  infected  dogs  in  North  Carolina  with  worms  in  the  body  cavity 
onlv  6  had  worms  in  the  right  kidney  as  well,  and  1  had  them 
only' in  the  right  kidney.  Lukasiak  (1930)  called  attention  to 
the"  fact  that  in  spite  of  numerous  searches,  especially  in  the 
kidneys,  larvae  have  never  been  found,  and  relatively  young 
forms"  have  been  found  not  in  the  kidneys  but  in  the  alidominal 
cavity,  by  preference  between  the  lobes  of  the  liver.  Stefanski 
and  Stra'nkowski  (1936)  found  a  case  in  which  a  worm  in  the 
abdominal  cavity  was  clearly  in  process  of  entering  the  right 
kidney;  its  anterior  end  was  lodged  in  the  tissue  of  the  right 
kidiie"y,  the  substance  of  which  had  not  been  destroyed.  From 
this  and  similar  cases  which  they  quote  from  the  literature, 
and  from  the  other  evidence  cited  above,  these  authors  conclude 
that  the  larvae  of  the  worm,  travelling  via  the  blood  stream, 
stop  in  the  liver,  grow,  and  finally  continue  their  development 
in  the  abdominal  cavitv,  probably  penetrating  the  kidney  only 
after  the  final  molt,  and  hollowing  out  a  canal  in  the  substance 
of  this  organ.  Since  the  larvae  are  probably  too  large  to  enter 
capillaries,  it  seems  to  us  more  probable  that  the  worms  reach 
the  body  cavity  by  directly  burrowing  into  it,  as  do  Gnath- 
ostoma  "larvae;"  we  know  of  no  evidence  that  the  liver  is  in- 
volved at  all. 


296 


Fig.  200. 
Diartofihftma    rfnule    feinnlc.    anterior   extrprnily   of   the   j)ar;isite    coiled 
in    the    pelvis   of   the   right    kidney.      .After    Stefanski    and    Strankowski, 
1936.  An.  de  rarasit.  Hninaine  et  Conip.  v.   14    (1). 

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1931. — Developmental  stages  of  some  nematodes  of 
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Foster,  A.  O.  and  Cross,  S.  X.  1934. — The  direct  development 
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1914. — Untersuchungen  ueber  den  Infektionsweg  Viei 
StrongyJoides  und  Aiil-ylostoma  und  die  Biologic  dieser 
Parasiten.  Beiliefte  5,  Arch.  Schiffs-  u.  Tropen  Hvg.  v. 
18:   26-80   (182-236),  figs.  1-14,  pis.  1-7. 

lS20a. — Perkutaue  lufektion  bei  Angiostomiim  nigro- 
venosum.    Ibid.  v.  24:  176. 

1920b. — Ueber  die  Anpassung  der  Nematoden  an  den 
Parasitismus  und  den  Infektionsweg  bei  Askaris  und  and- 
eren   Fadenwiirmeu  des  Menschen.  Ibid.  v.  24:    340-347. 
Fadenwiirmen  des  Menschen.     Ibid.  v.  24:  340-347. 

1921a. — Askarisinfeckion  durch  Verzehren  eingekap- 
selter  Larven  und  iiber  gelungene  intrauterine  Askarisin- 
fektion.     Ibid.  v.  25:  367-375. 

1921b. — Ueber  die  Wanderung  von  Askaris  und  and- 
eren  Nematoden-larven  in  Korper  und  intrauterine  As- 
karis infektion.     Ibid.  v.  25:  146-149. 

1923a. — Ueber  die  Entwicklung  von  Trichozejihalus  ini 
Wirte.    Ibid.  v.  27:  413-420. 

1923b. — Ueber  den  "  Mundstachel"  der  Trichotraeli- 
eliden-larven  und  Bemerkuiigen  iiber  die  juugsten  Stadien 
von  Tricliocephalus  Irichinrus.     Ibid.  v.  27:   421-425,  1  pi. 

1924. — Ueber  den  Infektionsweg  bei  Bepalicola  he- 
patica.    Ibid.  v.  28:  48-61. 

1925. — Ueber  die  Durchlassigkeit  der  Blutcapillaren 
fiir  Xematodenlarven.  Iliid.  v.  29,  Beiheft  3,  100  pp. 
4  pis. 

1926. — Ueber  das  Verhalten  der  Hakenwurmlarven 
bei  der  Infektion  per  os.     Ibid  v.  30:   638-653. 

1927. — Ueber  das  Verhalten  der  Larven  in  Korper  des 
Wirtes.    Ibid.,  Beihefte  2.  v.  31,  56  pp.,  figs.  1-5. 

1928. — Ueber  den  Infektionsweg  bei  Rhabdias  hufonis 
(Rhabdonema  nigrovcnosiim)  des  Froschi's  nebst  Versuchen 
ueber  die  Lymphzirkulation  des  letzteren.  Centralbl.  Bakt. 
[etc.],  Abt.  I,  Orig.,  v.  109:   444-462,  1   pi. 


1929a. — On  the  larval  migration  of  some  parasitic 
nematodes  in  the  body  of  the  host  and  its  biological  sig- 
nificance.     J.   Helm.,  V.    7    15-26. 

1929b. — Filariosen  des  Menschen.  In  Handb.  Path. 
Mikroog.,  6,  Lief.  28,  10431224,  3  pis. 

FuRUYAMA,  T.  1934. — On  the  morphology  and  life  history  of 
Fhilometra  fujimotui  Furuyama,  1932.  Keijo  J.  Med.,  v. 
5    (3):    165-177. 

GooDEY,  T.  1922. — Observations  on  unsheathed  larvae  of  nema- 
todes. Ann  Applied  Biol.,  v.  9.  33. 

1923. — Experiment  on  the  feeding  of  embrj'onated 
eggs  of  Ascaris  meqaiocephala  to  domesticated  animals. 
Ann.  Appl.  Biol.,  v. 'lO :   116-121. 

1924a. — The  anatomy  of  Oesophagoslomnm  deniatum 
(Rud.)  a  nematode  parasite  of  the  pig,  with  observations 
on  the  structure  and  biologv  of  tlie  free-living  larvae.  J. 
Helm.,  V.  2:    1-14. 

1924b. — The  anatomy  and  life  history  of  the  nema- 
tode Rhabdias  ftiscovenosa  (Railliet)  from  the  grass  snake 
Tropidonotus  natrix.  Ibid.,  v.  2  (2)  :  51-64. 

GooDEY,  T.  and  Cameron,  T.  W.  M.  1923. — Observations  on  the 
morphology  and  life  cycle  of  Ascaris  columnaris  Leidy, 
a  nematode  parasite  of  the  skunk.     J.  Helm.,  v.  1:  1-8. 

GR.iHAM,  G.  L.  1936. — Studies  on  Strongyloides.  1.  S.  ratti  in 
parasitic  series,  each  generation  in  the  rat  established 
mth  a  single  homogonic  larva.  Am.  J.  Hvg.,  v.  24  (1)  : 
71-87. 

1938. — Idem.  II.  Homogonic  and  lieterogonic  prog- 
eny of  the  single  honiogonicalh-  derived  S.  ratti  parasite. 
Ibid.,  V.   27    (2):    221-234. 

1939a. — Idem.  IV.  Seasonal  variation  in  the  ijro- 
duction  of  heterogonic  progeny  by  singly  established  S. 
ratti  from  a  homogonieallv  derived  line.  Ibid.,  v.  30 
(Sect.  D.),  15-27. 

1939b. — Idem.  \.  Constitutional  differences  between 
a  homogonic  and  a  heterogonic  line  of  S.  ratti.  J.  Para- 
sit., V.  25   (4)  :   365-375. 

Guberlbt,  J.  E.  1924. — Note  on  the  life  history  of  Ascaridia 
perspicilliim.  Tr.  Am.  Micr.  Soc,  v.  43:   152-156. 

Harwood,  p.  D.  1930. — A  new  species  of  Oxysomatiitm  (Nema- 
toda)  with  some  remarks  on  the  genera  Oxysomatium  and 
Apiectana  and  observations  on  the  life  historv.  J.  Para- 
sit., V.  17:  61-73. 

1932. — A  note  on  the  tissue-penetrating  abilities  of 
sheathed  microfilariae.  Tr.  Am.  Micr.  Soc,  v.  51  (2) : 
153-1.54. 

Heller.  A.  1903. — Ueber  Oxyuris  vermicularis.  Deutsch  .\rcli. 
Klin.   Med.,   Berlin,   v.   77,    (1-2)  :    21-28,   pis.   13. 

Herrick,  C.  a.  1928. — A  quantitative  study  of  infections  with 
Ancyclostoma  caninnm  in  dogs.  Am.  J.  Hyg.,  v.  8:  125- 
157. 

Hedrick,  L.  E.  1935. — The  life  history  and  morphology  of 
Spiroxys  contort ns  (Rudolphi)  ;  Nematoda:  Spiruridae. 
Tr.  Am.  Micr.  Soc,  v.  54   (4)  ;   307-335. 

H0B.MAIER,  M.  1930. — Life  history  of  Probostrongyins  (Syn- 
thetocaulus  rufescens.  Proc.  Soc.  Exper.  Biol.  &  Med.,  v. 
2S:   156-158. 

1934a. — Lungenwurmlarven  in  Mollusken.  Ztschr.  Par- 
asitenk.,  v.  6:   642-648. 

lP34b. — Elaphnstrongyhis  iidocodei  n.  sp.,  ,i  new  lung- 
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1935. — Intermediate  hosts  of  AelnrostrongyJus  (i)> 
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HOBMAIEB,  A.  and  Hobmaiek,  if.  1929. — Die  Entwicklung  d  'i- 
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Hu,  C.  H.  and  Hoeppli,  R.  J.  C.  1936. — Tlie  migration  route 
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Hsu,  H.  F.  and  Cho'O',  C.  Y. — On  the  intermediate  host  and 
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LUCKEH,  J.  T.  l934a.^Devclopiiunt  of  the  swine  nematode 
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193(i.- -Preparasitic  molts  in  Xippostroiigyliis  miiris, 
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193H. — Description  and  differentiation  of  infective 
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LfTTERMOSEK,  G.  W.  1938a. — Factors  influencing  the  develop- 
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193Sb. — An  e.\perinH'iital  study  of  Capillaria  hepatica 
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Mac.\rthuk,  W.  P.  1930. — Threadworms  and  pruritis  ani.  .T. 
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JIcCoY,  G.  R.  1929. — The  growth  of  hookworm  larvae  on  pure 
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McIntosii,  a.  and  CiimvooD,  B.  G.  1934. — A  new  nematode 
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Manson,  p.  1878. — Gn  the  development  of  Filaria  sanguinis 
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MAKKOW'sKr,  S.  1937. — Ueber  die  pjntwickluiigsgeschichte  und 
Biologic  des  Nematoden  Contracarrtim  adancum  (Rudolphi, 
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M.AUP.^.s,  E.  and  Seurat,  L.  G.  1913. — La  Mue  et  I'enkystement 
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JIecinzkow,  E.  1865. — Ueber  die  Entwickelung  von  Ascaris 
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MlYAGAW.*.,  Y.  1916. — Ueber  den  Wanderungsweg  der  Ankylos- 
toina  duodenale  innerhalb  des  Wirtes  bei  Oralinfektion 
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K.  Univ.,  Tokyo.,  v.  15:   411-452. 

MiYAGAWA,  Y.  and  Okada,  R.  1930. — Biological  significance  of 
the  lung  journey  of  Anchylostoma  larvae  in  the  normal 
host.  First  Report.  Jap.  J.  E.xper.  Med.,  v.  8:  2S5-308. 
1931.— Idem,  Second   Report.     Ibid.,  v.  9:    151-207. 

Momma,  K.  1930. — Notes  on  modes  of  rat  infestation  with 
Hepaticola  hepatica.  .4nn.  Trop.  Med.  &  Parasit.,  v  24 
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MoNNiG,  H.  0.  1930. — Studies  on  the  bionomics  of  the  free- 
living  stages  of  Trichostrongylu.'i  spp.  and  other  parasitic 
nematodes.  Union  So.  Africa  Dept.  Agric,  16th  Rpt.  Dir. 
Yet.  Service,  pp.  175-198. 

MOORTUY,  Y.  N.  1938. — Observations  on  the  de%'elopment  of 
Dracuiiculus  niedinciisis  larvae  in  Cvclops.  Am.  J.  Hvg  , 
V.  27   (2):   437-460. 

1938b. — Observations  on  the  life  history  of  Camallanus 
sueeti.    J.  Parasit.,  v.  24  (4) :  323-342. 

MOORTHY,  Y.  N.  and  Sweet,  W.  C.  1938.— Further  notes  on 
the  experimental  infection  of  dogs  with  draeontiasis.  Am 
J.  Hyg.,  V.  27   (2) :  301-310. 

MoRo.iN,  D.  C.  1928. — Parastrongyloides  winchesi  gen.  et  sp. 
nov.  A  remarkable  new  nematode  parasite  of  the  mole  and 
the  shrew.    J.  Helm.,  v.  6:  79  86,  4  figs. 

Mueller,  J.  F.  1934. — Additional  studies  on  parasites  of  Onei- 
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299 


Neshi,  G.  1918. — Ueber  die  Entwickluiig  des  TrichocephaUia 
inuerhalb  des  Wirtes.  (Japanese).  Tokyo.  Med.  Woclieu- 
schr.,  No.  2080. 

Nevbu-Lemaire,  M.  l!>3t).— Traite  d'lielmiiitliologie  medieal  et 
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NiSHiGORl,  M.  192.J.— On  the  life  history  of  Bepaticola  hepati- 
ca.    Second  Report,  J.  Formosa  Med.  Soc.,  t.  247:  3-4. 

1928. — The  factors  which  influence  the  external  devel- 
opment of  Strongijlnidcfs  stercoraJix  and  on  auto-infection 
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NoE,  G.  1908. — II  ciclo  evolutivo  della  Filaria  gmssi,  milii, 
1907.  Atti  R.  Accad.  Lincei,  Roma,  Rendic.  CI.  Sc.  Fis., 
Math.  &  Nat.,  an.  30.";,  5.  s.,  v.  17  (.')),  1.  semester:  282- 
293,  figs.  1-4. 

Nolan,  M.  0.  and  Rf.ardox,  L.  193!.. — Studies  on  oxyuriasis, 
XX.  The  distiiliution  of  the  ova  of  Enlerobiiis  rermicu- 
lari^  in  household  dust.     J.  Parasit.,  v.  2.5:  173  177. 

O'Connor,  F.  W.  1931.— Filarial  periodicity  with  observations 
on  the  mechanism  of  the  migration  of  the  microfilariae 
from  the  parent  worm  to  the  blood  stream.  Puerto  Rico  .1. 
Pub.  Health  &  Trop.  Med.,  v.  6:  2(33-272. 

Okada,  R.  1931. — Experimental  studies  on  the  oral  and  per 
cutaneous  infection  of  Anchylostoma  caiiiniim  (Four  Re- 
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Olt,  a.  1932. — Das  Aneurysma  vermlnosum  des  Pfcrdes  und 
seine  unbekaunten  Beziehungen  zur  Kolik.  Deutsch.  Tier- 
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Ortlepp,  R.  J.  1922. — On  the  hatching  and  niigrMfion  in  a 
mammalian  host  of  larvae  of  ascarids  normally  parasitic  in 
cold-blooded  vertebrates.  J.  Trop.  Med.  &  Hyg.,  v.  2.5: 
97-100. 

1923. — The  life  history  of  Syrigamiis  Irachea  (Mon- 
tagu) V.  Siebold,  the  gapeworm  of  chickens.  J.  Helm., 
v.  1   (3):   119-140. 

192;'). — Observations  on  the  life  history  of  Triofhni- 
tophorus  tenuicoUis,  a  nematode  parasite  of  the  horse. 
Ibid.,  V.  3:    1  14. 

1937. — Observations  on  the  morphology  ;itid  life  his- 
tory of  Gaigeria  pachi/ttcclis  Raill.  and  Henry,  ISIO:  a 
hookworm  parasite  of  sheep  and  goats.  Onderstepoort  J. 
Vet.     Sc.  &  Anim.  Indus.,  v.  8  (1)  :   183-212. 

Pavlov,  P.  1937. — Recherches  cxperimentalcs  sur  le  cycle  evolu 
tif  de  Si)"Hn'lii<'i"ilii'<  capillaris:.  Ann.  Parasit.,  v.  l."i:  ."lOO- 
503,  pl."l4. 

Pereira,  C.  v.,  Vianna  Dias,  M.  and  de  Azevebo,  P.  1936. — 
Biologia  do  nematoide  Pyocamallanvs  cearrnsis  n.  sp. 
(English  summary,  p.  225).  Arch.  Inst.  Biol.,  Sao  Paulo,  v. 
7:    209-22G. 

Philpot,  F.  1924. — Notes  on  the  eggs  and  early  development 
of  some  species  of  Oxyurides.    J.  Helm.,  v.  2:  239  252. 

Pkommas,  C.  and  Daengsvang,  S.  1933. — Preliminary  report 
of  a  study  on  the  life  cycle  of  Gnatliostoma  spiiiigenim. 
J.   Parasit.,  v.   19    (4):    287-292. 

1936. — Further  report  of  a  study  on  the  life  cycle 
of  Gnathostoma  spiiiioerum.  J.  Parasit.,  v.  22  (2)  :  180- 
186. 

1937. — Feeding  experiments  on  cats  with  GitaDiustoma 
spinigeriim  larvae  obtained  from  the  second  intermediate 
host.     Ibid.,  v.  23   (1):   115-116. 

Railliet,  A.  1899. — Evolution  sans  heterogonie  d'un  angios- 
tome  de  la  couleuvre  a  collier.  Compt.  Rend.  Acad.  Sc, 
Paris,  V.  129   (26)  :   12711273. 

Ransom,  B.  H.  1906.— The  life  history  of  the  twisted  wire 
worm  (Hacmonclius  contortu.i)  of  sheep  and  other  rumi 
nants.     Bur.  Anim.  Indus.,  U.  S.  Dept.  Agric,  Cir.  No.  93. 

1907. — Prdbstmayria  vivipara  (Probstmayr,  1865). 
Ransom,  1907,  a  nenmtode  of  horses  heretofore  unreported 
from  the  United  States.     Tr.  Am.  Micr.  Soc,  v.  27:   33-40. 

1911. — The  nematode  parasites  in  the  alimentary  tract 
of  cattle,  sheep  and  other  ruminants.     Bur.  Anim.  Indus 
U.  S.  Dept.  Agric,  Bull.  No.  127. 

Ransom,  B.  H.,  and  Ckaji,  E.  B.  1921. — The  course  of  migra- 
tion of  Ascari.'i  larvae.  Am.  J.  Trop.  Med.,  v.  1 :  129156 
2   pis. 

Ransom,  B.  H.  and  Foster,  W.  D.  1917. — Life  history  of  As- 
caris  lumbricoid rs  and  related  forms.  J.  Agric  "  Res  v 
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1920. — Observations  on  the  life  history  of  Aticari.i 
lumhricoides.     U.  S.  Dept.  Agric,  Bull.  No.  817,  47  pp. 

Ransom,  B.  H.  and  H.all,  M.  C.  1916.— The  life  history  of 
Gongylonema  scutatum.     J.  Parasit.,  v.  2:   80-86. 

Rbfuerzo,  p.  G.  and  Gariia,  E.   V.  1938. — The  crustacean  in- 
termediate   hosts    of     Giiatinislomiim     spinigenim     in     the 
Philippines    and    its    pre-    and     iuter-crustacean    develop 
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5   pis. 

RouBAUD,  E.  and  Descazeaux,  J.  1921. — Contributions  a  I'his- 
toire  de  la  mouclie  domestique  comme  agent  vecteur  des 
habronemoses  des  equides.  Cycle  evolutif  et  parasitisme  do 
I'Habronema  megastoma  (Rudolphi,  1819)  chez  la  mouche. 
Bull.  Soc  Path.  "Exot.,  v.  14:   471-506. 

1922. — Evolution  de  I'Habionema  miiscue  Carter  chez 
la  mouche  donu'stiijue  et  de  \'H.  microstominii  Schneider 
chez  le  stomoxe.     Note  preliminaire.     Ibid.,  v.  15:  572  574. 

1922. — Evolution  de  \'Hubroiidiia  mtiscae  Carter  che  ■, 
dans  leurs  rapports  avec  1  'evolution  des  Habrouemes 
d 'equides.     Ibid.,  v.   15:    978-1001. 

Roberts,  F.  H.  S.  1934. — The  large  roundworm  of  pigs,  Ascari.i 
Itimbricoideii  L.  1758.  Anim.  Health  Sta.,  Queensland 
Dept.  Agric  &  Stock,  Bull.  No.  1,  81  pp.,  11  figs.,  2  pis. 

1937. — Studies  on  the  biology  and  control  of  the 
large  roundworm  of  fowls,  Ascaridia  qaUi  (Schrank,  1788). 
Ibid.,  Bull.  No.  2,  106  pp.,  7  pis. 

Ross,  I.  C.  and  Kauzal,  G.  1932.--The  life  cycle  of  Stepliaim- 
rus  dentatus  Diesing,  1839;  the  kidney-worm  of  pigs; 
with  observations  on  its  economic  importance  in  Australia 
and  suggestions  for  its  control.  Austral.  Council  Sc.  & 
Indus.  Res.,  Bull.  No.  58,  80  pp.,  illus. 

Sandground,  J.  H.  1926. — Biological  studies  on  the  life  cycle 
in  the  genus  Strongiiloides,  Grassi,  1879.  Am.  J.  Hvg., 
V.  6  (3):  337-388. 

1939. — Cephalobus  j-arasUicus  n.  sp.  and  pseudostron- 
gvloidiasis  in  Macaca  irns  morda.r.  Parasit..  v.  31  (1)  :  132- 
137. 

Schwartz.  B.  1922. — Observations  on  the  life  cycle  of  AKcaris 
vitiilorum,  a  parasite  of  bovines  in  the  Philippine  Islands. 
Preliminary  Paper.  Philippine  J.  Sc,  v.  20  (6):  661669. 
1   pi. 

1925a — Two  new  larval  nematodes  belonging  to  the 
genus  T-orrocaecum  from  mammals  of  the  order  Insect i- 
vora    Proc  U.  S.  Natl.  Mus.,  v.  67,  Art.  17.  8  pp.,  1  pi. 

1925b — Preparasitic  stages  iu  the  life  history  of  the 
cattle  hookworm  (Bunostomiim  phlfbotomnm) .  ,1.  Agrir. 
Res.,  V.  29:   451-458. 

1931. — Nodular  worm  infestation  of  domestic  swine. 
Vet.  Med.,  v.  26:   411-415. 

Schwartz,  B.  and  Alioata,  J.  E.  1929. — The  development  of 
Metastrongylus  eloTigatus  and  M.  piidendotectiis  in  their 
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1936. — Life  history  of  Loiigistriata  miisctiU,  a  nema- 
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146. 

Schwartz,  B.  and  Price,  E.  W.  1929.— The  life  history  of  the 
swine  kidney-worm.  Science,  v.  70  (1825)  :  613-614. 

1931. — Infection  of  pigs  through  the  skin  with  tMe 
larvae  of  the  swine  kidney  worm,  Stephaniiriis  dcntatiiii. 
J.  Am.  Vet.  Med.  Assoc,  v.  79:  359-375. 

1932. — Infection  of  pigs  and  other  animals  with  kid- 
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325-347. 

Soott,  J.  A.  1928. — An  experimental  study  of  the  develop 
ment  of  Ancylostoma  catiiniim  in  normal  and  abiutrmal 
hosts.  Am.  J.  Hyg.,  v.  8   (2):   158-204. 

Seurat,  L.  G.  1920a. — Historic  naturelle  des  nematodes  de  le 
Berberie,  Algiers.   221    +   vi   pp.,   34   figs. 

1920b. — Developpement  embryonnaire  et  revolution 
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lidae).   Compt.   Rend.   Soc   Biol.,   Paris,  v.   83:    1472  1474. 

Shorb,  D.  a.  1931. — Experimental  infestation  of  white  rats 
with  Eepaticola  hepatica.  J.  Parasit.,  v.  17:  151-154. 

Spindler,  L.  a.  1933. — Development  of  the  nodular  worm  oeso- 
phagostomnm  lonqicaiidum  in  the  pig.  J.  .\gric.  Res.,  t. 
46:  531-542. 

St.wbli,  C.  1913.— Trichinose.  In  Haiidb.  Path.  Mikmorg., 
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300 


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Aim.   I'arasit.,  v.   1-t:    ,').'i  00,   1   jil. 

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Walker,  H.  D.  1886. — The  gapeworm  of  fowls  (Syngamus 
trachralis),  the  earthworm  (.Lumbriciis  lerrestris)  its  origi 
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300. 


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Ihymatoxy.i  rrligcra  (Rudolphi,  1819)  Schneider,  1860, 
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Toxaxcaris  Uonina  (Nematoda:  Ascaiidae).  Proc.  Helm. 
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1920. — On  the  oral  infection  by  the  hookworm.  Arch. 
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aoi 


CHAPTER  VII 

EPIDEMIOLOGY  AND  SANITARY  MEASURES  FOR  THE  CONTROL  OF 
NEMIC  PARASITES  OF  DOMESTICATED  ANIMALS 

T.  W.  M.  CAMERON,  Institute  of  Parasitology,  Macdonald  College,  Quebec,  Canada 


The  parasitic  existence  of  a  nematode  is  dependent  on  its 
finding  a  suitable  environment  in  which  it  can  mature  and  re- 
produce and  this  involves  four  sets  of  factors: 

(a)  SuccESSFUi,  Admission  to  the  Host. — The  host  must 
traverse  the  ground  where  the  free  stages  of  the  parasite  are 
found,  it  must  eat  suitable  foodstuffs  in  or  ou  which  tlie 
larval  stages  occur;  it  must  be  exposed  to  the  intermediate 
host,  and  so  on.  Even  slight  differences  in  habits;  e.g.,  such 
as  exist  between  a  sheep  and  an  ox  in  eating  grass,  may 
make  all  the  difference  in  the  parasite  gaining  admission. 
The  anatomy  of  the  host,  including  the  thickness  of  the  skin 
is  a  factor  to  be  considered  under  this  head. 

(b)  Suitable  Environ ment.\l  Conditions  in  the  Host. — 
Once  inside  the  host,  the  parasite  must  find  a  suitable  habitat 
— type  of  mucosa  in  the  intestine,  length  of  intestine,  pres- 
ence of  suitable  food,  and  so  on. 

(c)  Possession  of  a  Suit.able  Protective  Mechanism 
Against  the  Normal.  Metabolic  Processes  of  the  Host. — 
When  the  parasite  lies  in  the  alimentary  system,  it  must 
possess  some  means  of  preventing  itself  being  digested  or 
being  passed  out  by  peristalsis,  etc. 

(d)  Absence  op  a  Host  Reaction  that  Would  Interfere 
WITH  THE  Normal  Metabolism  of  the  Parasite. — This  fac- 
tor applies  most  obviously  to  parasites  that  leave  the  lumen 
of  the  alimentary  tract  at  some  period  of  their  life,  but  it  may 
apply  to  all.  If  there  is  any  host  reaction,  the  parasites  must 
be  able  to   resist  its  effects. 

Under  natural  conditions,  nematodes  are  more  or  less  spe- 
cific to  a  single  species  or  a  group  of  closely  related  species 
of  animals.  In  general,  it  may  be  taken  that  nematodes  of 
ruminants  are  not  transmissible  to  horses,  pigs,  poultry,  nor 
those  of  the  latter  to  each  other.  However,  many  parasites 
of  wild  ruminants  are  transmissible  to  domesticated  ruminants, 
of  wild  carnivores  to  dogs,  cats  and  foxes,  of  wild  birds  to 
domestic  ones,  and  so  on.  The  important  exceptions  to  this 
generalization  include  the  Trichina  and  some  members  of  the 
genus   Tricltostrongyhis. 

Very  few  parasitic  nematodes  can  complete  their  entire  life 
cycle  within  the  same  vertebrate  animal,  any  more  than  they 
can  live  a  free  independent  existence.  At  one  stage  or  an- 
other they  must  leave  the  host  to  undergo  some  form  of  devel- 
opment outside  of  it — either  free,  or  in  an  alternate  or  inter- 
mediate host.  In  effect,  this  means  that  a  single  young  nema- 
tode develops  into  a  single  adult  only;  there  is  no  multiplica- 
tion as  in  the  case  of  bacteria.  In  both  groups,  disease  de- 
pends upon  numbers,  but  whereas  the  entrance  of  a  single 
bacterium  into  the  body  may  cause  disease,  the  entrance  of  a 
single  larval  nematode  usually  does  not.  Parasitic  disease  de- 
jiends   on   actual   numbers   entering   the   body. 

The  stages  which  leave  the  body,  are  never  immediately 
infective.  Some  essential  development  must  take  place  before 
they  are  ready  to  re-enter  and  this  development  takes  a  definite 
period  of  time  and  requires  a  definite  set  of  conditions — heat, 
moisture,  oxygen,  presence  of  correct  intermediate  host  and 
so  on — before  they  are  able  to  infect.  Once  the  infective 
stage  is  reached,  they  are  often  able  to  live  for  a  long  period 
before  re-entry;  while  the  minimum  time  necessary  outside  of 
the  body  can  be  fairly  accurately  ascertained,  the  maximum 
time  is  much  more  difficult   to  determine. 

In  many  cases,  after  entrance  to  the  body,  complicated 
migrations  through  various  organs  are  an  essential  part  of 
the  life-cycle  and  the  greatest  damage  to  the  host  is  often 
caused  at  this  period.  We  know  of  no  means  of  preventing 
these  migrations  and  we  know  of  no  therapeutic  agents  which 
can  affect  the  nematodes  during  migration  .  Accordingly, 
prevention  of   ingress  is  of   the  greatest  importance. 

Scientific  control  consists  in  making  development  as  difificult 
as  possible  and  so  depends  essentially  on  a  knowledge  of  the 
life  history  and  bionomics  of  the  parasite  involved.  This 
necessitates  the  correct  identification  of  the  nematode  con- 
cerned. The  need  for  correct  identification  is  most  important 
as  not  only  are  no  two  parasites  quite  alike  in  their  biology, 
but  treatment  is  often  different. 

In  determining  control  methods  it  is  important  to  remem- 
ber that  there  are  economic  aspects  of  the  problem  to  be  con- 
sidered. The  cost  of  control  may  be  excessive  and  it  must  be 
balanced  against  the  loss  to  the  stockowner — and  loss  should 
include  not  only  actual,  but  potential  future  loss.  It  is  often 
accordingly    necessary    to    adopt    several    methods    of    control 


simultaneously  rather  than  to  employ  a  single  method.  Control 
may  be  nationwide  or  it  may  be  individual.  Individual  con- 
trol is  at  best  a  palliative,  and  campaigns  directed  over  a 
wide  area  and  infinitely  more  satisfactory.  This  not  only  in- 
volves cooperation  between  veterinarians,  agriculturists,  ad- 
ministrators and  parasitologists  but  it  involves  careful  co-ordi- 
nation as  well.  A  central  authority  and  enabling  legislation 
are  almost  essential,  but  the  legislation  to  be  successful  must 
come  as  the  result  of  a  demand  from  the  majority  of  the 
farmers  involved.  A  central  laboratory  with  a  good  informa- 
tion service  is  also  desirable,  with  adequately  staffed  branch 
or  associate  laboratories  throughout  the  country. 

Control  measures  aim  at  breaking  at  some  point  the  essen- 
tial life-cycle  of  the  parasite.  If  more  than  one  point  is  at- 
tacked, the  chances  of  successful  results  are  increased.  These 
measures  will  be  discussed  convenientl.v  in  several  groups,  al- 
though it  must  be  understood  that  such  a  hard  and  fast  divi- 
sion as  is  here  adopted  does  not  occur  in  nature  and  that 
methods  described  under  one  may  be  equally  applicable  under 
another.  The  parasite  may  be  attacked  at  one  or  other  of  the 
following   points   in   its   life   cycle:  — 

1.  While  in  the  ovum  or  as  a  young  developing  larva. 

2.  During  the  developed  infective  stage,  which  does  not 
grow  and  ' '  rests ' '  until  it  enters  the  host. 

3.  Before  entrance  of  this  larva  into  the  host. 

4.  Within  the  intermediate  host  or  vector,  within  which 
1  and  2  may  be  found  and  which  may  be  the  means  of 
entry  to  the  host. 

-■).    During   the   parasitic   stages   in   the   host. 

1.    Methods  of  Destroying  the  Eggs  of  Pre-Infective 
Larvae 

These  are  those  stages  passed  in  the  faeces  as  well  as  the 
subsequent  stages  which  develop  therein.  (In  a  small  minority 
of  cases  the  larvae  are  not  passed  in  the  faeces,  but  may 
leave  by  the  mouth  or  the  urinary  system  or  be  abstracted 
from  the  blood  b.v  blood-sucking  animals,  or  may  come  to  rest 
in  the  host's  muscles).  As  we  know  of  no  efficient  method  of 
destroying  the  eggs  in  the  host,  this  section  is  accordingly 
mainly  concerned  with  manure  and  its  treatment.  It  is  not  a 
new  subject,  having  been  advocated  for  years  in  connection 
with  human  hookworm  disease,  but  curiously  enough,  very  lit- 
tle indeed  has  been  done  about  it  in  connection  with  nema- 
todes of  animals  in  which  it  is  infinitely  more  important. 

There  are  two  ways  of  treating  manure.  The  first  is  to 
disregard  its  parasite  content  and  concentrate  on  its  dispersal 
in  such  a  manner  as  to  keep  it  out  of  harm's  way.  The  sec- 
ond is  to  treat  it  in  such  a  way  that  its  parasite  content  is 
destroyed.  Some  twenty  years  ago,  the  late  Dr.  Maurice 
C.  Hall  stated  that  this  subject  offered  a  field  for  a  large 
amount  of  investigation  but  this  investigation  has  not  been 
done. 

"Broadly  speaking,"  he  said,  "one  would  have  to  deter- 
mine how  long  the  larvae  and  eggs  of  the  various  species  of 
worms  involved  live  in  manure  piles,  in  spread  manure,  in 
closely  packed  manure;  the  effect  of  sunlight,  of  moisture,  of 
various  chemicals,  the  chemicals  in  turn  being  of  a  nature 
not  to  injure  the  fertilizing  value  of  the  manure.  There  are 
practically  no  data  on  this  and  little  could  be  surmised  with- 
out such  data. ' ' 

Since  that  was  written  a  considerable  amount  of  investiga- 
tion has  been  carried  out  on  this  subject  and  it  may  be  con- 
sidered under  the  following  headings: 

1.  Storage.  The  prompt  daily  collection  of  all  manure  in 
the  stables  is  an  essential  routine  in  farm  practice  and  if 
correctly  carried  out  is  a  valuable  preventive  measure.  If  this 
manure  were  stored  in  a  proper  container  for  a  suflScient  length 
of  time,  without  any  other  treatment  all  eggs  and  larvae  would 
be  destroyed.  Unfortunately,  the  time  factor  is  too  long  to  be 
practical  and  resource  to  additional  methods  is  necessary. 

'2.  Heating.  In  piles  of  horse  manure,  all  eggs  and  larvae 
of  the  strougyle  type  are  destroyed  in  4  days  by  the  natural 
heat  generated,  with  the  exception  of  those  in  the  outer  6 
inches.  As  a  temperature  as  high  as  107  degrees  F.  is  generated 
in  the  central  zone,  all  other  parasites  should  be  destroyed 
also,  although  we  are   without   definite   knowledge  of   this.  If 


302 


rill'  inaiiiirc  is  contiiU'd  witliiii  wmnli'ii  hoxi's  oitlii'r  :ili<ivi'  (ir 
lielow  Kroiiiul — all  except  the  o\iter  layer  of  It  iiielie.s  heroines 
hot  enough  to  destroy  the  panisites,  while  if  the  womleii 
lioxes  are  doiihle  walled  with  sawdust  lietweeii,  all  are  killed 
ill  a  week.  Kxperiiiieiits  with  artitieial  heat,  have  shown 
that  steam,  at  l."i  lbs.  pressure,  destroyed  in  itO  luiimtes  all 
e^Ks  and  larvae  in  a  special  niaiiiire  box. 

While  these  data  indieate  that  iiiainire  can  In'  I'lVcctively 
sterilized,  the  iiicthods  with  the  exception  of  the  first,  have 
the  disadvantage  of  leipiiriiiii  special  a|)paratus.  This  en 
tails  expense  and  limits  their  application  to  well  eciiiiiiped 
stables.  However,  a  compact  manure  pile,  which  has  the 
outer  (>  inches  turned  in  every  .'>  days  or  so,  will  iiiHloiiliteilly 
kill  a  very  high  percentage  of  the  eggs  and  larvae. 

3.  Drying.  This  is  a  method  which  is  only  occasionally 
possible  and  the  drying  of  large  (piantities  of  manure  is 
l>ractically  confined  to  countries  with  a  hot,  dry  climate  wlu're 
dried  dung  is  used  for  fuel,  or  where  its  value  is  secondary 
to  military  conditions  and  it  may  be  spread  out  in  the  hot  sun. 
Ill  the  latter  case,  however,  imincdiate  daily  <lrying  is  essen 
tial  as  only  the  eggs  and  jire  infective  stages  are  easily 
destroyed  by  this  method.  Drying  is  of  some  value  also 
in  destroying  larvae  on  bare  ground.  Iturning  of  manure  is 
the  logical  extension  of  drving  it,  but  this  is  seldciru  i>raiti 
cable. 

In  a  rather  dilTerent  way  this  method  has  been  used  to 
combat  the  lung  and  intestinal  nematodes  of  silver  foxes  in 
Canada.  There  the  animals  are  raised  on  floorboards  which 
are  easily  kept  dry  by  being  roofed.  This  inhibits  develop- 
ment of  the  eggs  and  larvae  of  the  worms  so  effectively 
that   it   is   now  almost   routine   practice. 

In  the  open,  short  grass  assists  drying  and  is  frciiuentl.v  of 
value  ill  reducing  the  infectivity  of  p.'istures,  as  of  course,  is 
drainage.  Very  wet  iiasturos,  however,  are  not  suitable  environ- 
ments for  the  development  of  most  nematodes  (except  Did ylo- 
raiiliix  of  horses,  sheeji  and  oxen).  Damp  pastures  are  more 
generally  favourable  for  parasitism  and  every  effort  should  be 
made  to  render  them  unsuitable  for  the  development  of  eggs 
into  larvae. 

4.  Chemical  Tre:atmext.  Comparatively  little  has  been 
done  to  find  chemical  methods  of  destroying  the  free-living 
stages  of  parasites.  It  is  a  problem  which  presents  many  diffi- 
culties, probably  the  greatest  of  which  is  the  faet  that  the  eggs 
and  larvae  are  always  in  close  contact  with  faeces,  soil  or  grass, 
and  many  chemicals  which  might  be  used,  are  iiartially  or  com- 
jiletely  counteracted  by  contact  with  organic  matter.  Never- 
theless, chemical  control  of  all  the  free-living  stages  does  ap- 
pear to  have  considerable  practical  possibilities. 

It  offers  the  opportunity  of  using  the  faecal  material  as 
manure  and  even  of  enriching  the  manurial  value  and  it  does 
not  necessitate  special  equipment. 

The  method  has  been  sporadically  used  with  a  certain  limited 
success  in  some  human  hookworm  areas,  the  chemicals  employed 
being  kainit,  lime  and  some  nitrogenous  fertilizers  such  as 
nitrate  of  soda,  sulphate  of  ammonia,  and  calcium  cyanamide. 

The  addition  of  a  chemical  to  faeces  containing  nematode 
eggs,  may  have  varied  effects  on  the  eggs  and  larvae  depend- 
ing not  only  on  the  nature  but  also  on  the  quantity  of  chemical. 

1.  It  may  increase  the  percentage  of  larvae  which  reach  the 
infective  stage  and  which  continue  to  survive.  Even  in  small 
cultures  of  fresh  horse  faeces  in  sterilized  containers,  fungi 
parasitic  on  nematodes  have  occasionally  become  established 
very  rapidly  and  in  a  short  time  have  destroyed  all  the  larvae. 
The  evidence  suggests  that  some  chemicals  may  destroy  or 
retard  the  growth  of  these  fungi  without  harming  the  larvae; 
flowers  of  sulphur  is  an  example.  Other  evidence  suggests 
that  some  chemicals,  which  are  lethal  to  eggs  or  larvae  when 
mixed  with  faeces  in  a  certain  i)roportion  may,  in  a  lesser 
proportion,  be  lethal  to  the  fungi  without  harming  the  larvae; 
it  follows  that  these  chemicals  may,  if  used  too  s])aringly, 
actually  increase  rather  than  decrease  the  number  of  larvae 
which  survive.  Fungi  are  more  likely  to  be  common  in  manure 
pits  and  similar  locations  than  in  cultures  and  may  be  of 
practical  importance  as  a  method  of  natural  biological  con- 
trol. It  is  probable  that  there  are  many  chemicals  of  quite 
different  types  which  possess  this  danger.  A  chemical  may  also 
decrease  putrefaction  which  may  be  lethal  to  larvae. 

2.  It  may  have  no  effect  at  all  on  the  eggs  or  larvae.  The 
majority  of  the  chemicals  which  can  be  added  to  faeces  without 
afTecting  the  eggs  or  larvae,  are  those  which  are  most  inert; 
exam])lcs  are  ferrous  sulphide,  ferric  oxide,  ground  limestone, 
rock  phosphate,  basic  slag,  derris  root,  white  hellebore,  and 
pyrethrum  powders. 

3.  It  may  allow  larvae  to  reach  the  infective  stage  but 
cause  many  to  exsheath.  Some  chemicals  cause  larvae  to  ex- 
sheath  without  necessarily  causing  their  immediate  death,  al- 
though  most   of   these  chemicals  are   lethal   in   higher   propor- 


tions. I,ap;ige  has  shown  that  the  factors  which  are  impor- 
tant in  causing  I'xshcathment  when  free  of  faeces,  include  age 
of  the  larvae  and  |ill  of  I  heir  environment,  and  that  chlorine 
and  sulphides  make  the  sheath  more  permeable.  Iji  the  pres- 
ence' of  faeces,  some  chloriib'S  and  sulphates,  sodium  and  potas- 
sium hydroxide  and  potassiuui  peruiang.-inate  occasionally 
cause  exsheathment.  Tln'se  cliemicals,  in  slightly  greater  pro- 
portions, gener.'illy  cause  the  death   of   larvae. 

4.  It  may  allow  many  l.nrvae  to  reach  the  infective  stage 
but  subse(iuently  cause  their  death.  Many  chemicals  mixed  with 
faeces  in  certain  proportions,  allow  a  considerable  number  of 
the  eggs  to  hatch  and  the  larvae  to  reach  the  infective  stage 
and  then  kill  them  comparatively  rapidly.  The  most  ontstand 
ing  exami>les  so  far  noted  with  this  property  are  (piicklime, 
(in  qu:uitities  too  small  to  I'.'iiise  death  through  tin'  heat  of  the 
clieiuical  reaction),  cupric,  ferric  and  ferrous  sulphates,  zinc, 
cupric  nitrate,  sodium  fluosilicate,  and  oxyquinoline  sulphate. 
Wlicn  ajiplied  to  fresh  faeces,  in  some  cases  only  a  third  of 
the  quantity  of  chemical  may  be  required  to  cause  delayed 
deiith  compared  with  the  (luantity  required  to  cause  death 
ln'fore  the  infective  stage  is  reached.  Numerous  other  chemi- 
cals (but  to  a  lesser  extent)  have  the  characteristic  of  causing 
dcl.-iyed  death  under  certain  conditions;  examples  arc  nicotine 
suliiliate,  trisodium  phosphate,  sulphate  and  chloride  of  man- 
gaiu'se.  so<liuin  and  magnesium  borates,  strong  cresol,  phenol, 
anil  calcium   liypt)chIoritc. 

."i.  It  may  allow  a  few  larvae  to  survive.  It  is  probable 
th.it  the  thickness  of  the  sheath  may  be  an  important  factor  in 
lircventing  the  action  of  some  chemicals  on  the  larvae.  If  this 
is  so.  it  would  account  for  the  fact  that,  in  spite  of  careful 
mixing,  a  few  larvae  survive  in  cultures  treated  with  sufficient 
(or  more  than  sufficient)  chemical  to  kill  most  of  them.  In 
many  cases  when  a  few  larvae  have  survived  they  have  been 
mainly  the  larger  sclerostome  larvae.  (In  some  cases  the  posi- 
tion of  the  eggs,  e.g.,  in  the  centre  of  a  lump  of  faeces,  may 
have  enabled  them  to  survive.) 

G.  It  may  rapidly  kill  all  the  eggs  or  free-feeding  larvae. 
When  a  chemical  is  highly  lethal  its  method  of  causing  death 
may  be  of  considerable  practical  importance.  Chemicals  which 
are  lethal  but  insoluble — they  are  not  common — and  which  kill 
by  contact  would  be  difficult  to  use  in  practice,  because  many 
larvae  would  escape  by  remaining  away  from  the  chemical, 
e.g.  inside  a  lump  of  faeces.  These  chemicals  would,  there- 
fore, be  especially  useless  in  dry  conditions.  Applied  dry, 
chemicals  which  are  deliquescent  have  more  prospect  of  being 
of  practical  value,  for  the  moisture  which  they  attract  may 
also  attract  the  larvae.  With  solutions  it  is  much  easier  to 
obtain  effective  contact  with  eggs  or  larvae  scattered  through- 
out the  manure,  especially  if  the  chemical  is  sufficiently  lethal 
to  be  effective  when  applied  as  a  very  weak  solution.  With 
very  lethal  chemicals  such  as  iodine  salts,  it  has  been  found 
that  very  considerably  less  chemical  is  necessary  to  produce 
sterilization  with  a  very  weak  rathei'  than  with  a  very  strong 
solution.  In  extreme  cases  a  chemical  applied  as  a  1:2  solu- 
tion may  require  from  20  to  even  50  times  the  amount  neces- 
sary when  applied  as  a  1:300  or  a  1:1,000  solution. 

Some  chemicals — including  some  which  are  very  effective 
(such  as  chloropicrin,  calcium  cyanide,  naphthalene,  Ortho-  and 
Para-dichlorbenzene) — can  be  used  as  gases.  Application  of 
this  class  of  sterilizing  agent  should  have  many  practical 
advantages,  provided  that  a  suitable  container  is  available 
and  that  the  faeces  are  not  packed  too  tightly  for  the  gases  to 
permeate  them,  but  results  suggest  it  is  possible  for  a  small 
percentage  of  eggs  or  larvae  to  avoid  gases,  again  probably 
when  they  are  in  the  centre  of  a  lump  of  faeces.  However, 
whether  this  class  of  chemical  is  applied  as  a  solid  or  fluid, 
it  is  probable  that  the  chemical  will  distribute  itself  effectively 
through  the  faeces.  Unfortunately,  some  of  the  most  effective 
gases  are  dangerous  or  at  best,  most  unpleasant,  to  man  him- 
self. 

Apart  from  the  efifectiveness  of  a  chemical  and  ease  with 
which  it  can  be  applied,  the  practicability  of  its  use  depends 
largely  on  its  cost.  When  sufficient  urine  is  available  it  has 
practically  all  the  possible  advantages.  The  next  most  prac- 
tical group  of  agents  is  the  artificial  fertilizers,  since  if  care  is 
taken  to  avoid  loss  of  nitrogen,  part  or  all  of  their  cost  may 
be  recovered  in  increased  manurial  value. 

Occasionally  it  may  be  possible  to  use  a  chemical  which  is 
not  only  lethal  to  nematode  larvae,  but  also  to  other  pests,  such 
as  fly  larvae;  if  this  can  be  done  the  advantages  are  obvious. 
Unfortunately,  it  by  no  means  follows  that  because  a  chemi- 
cal is  lethal  to  fly  larvae,  it  also  kills  nematode  larvae.  For 
example,  hellebore,  borax,  aniline  and  pyridine  have  all  been 
shown  to  be  effective  in  fly  control.  Hellebore,  however,  is 
not  lethal  to  sclerostome  larvae,  while  borax  has  to  be  used  in 
larger  quantities  than  for  fly  control  and  in  greater  quantities 
than  are  jiracticable  if  the  faeces  are  to  be  used  as  fertilizer 
(because  of  the  toxicity  of  an  excess  of  borax  to  plants).   Ani- 


303 


(in  weak  solution") 

(in  very  weak  solution) 

(in  weak  solution) 


Jine  and  pyridine,  on  the  other  hand,  are  both  vor3-  lethal  to 
the  free-living  stages  of  sclerostomea. 

The  cost  of  treating  faeces  can  also  be  reduced  if  a  lethal 
by-product  is  available  or  if  a  chemical  is  being  bought  in 
bulk  for  other  purposes.  In  these  eases  the  possibility  of  the 
presence  of  impurities  must  be  considered,  as  they  may  alter 
the  lethal  value  of  the  chemical  or  they  may  make  it  unsuit- 
able by  containing  a  plant  poison. 

A  large  number  of  chemicals  has  been  tested  at  the  Insti- 
tute of  Parasitology  for  their  effect,  under  controlled  labo- 
ratory conditions,  on  the  pre-infective  stages  of  horse  sclero- 
stomes.  The  more  ' '  practical ' '  of  these  are  given  in  the  fol- 
lowing table,  with  the  percentage  required  to  completely  steril- 
ize small  quantities  of  horse  manure: 

Percentage  Chemical  Brmarls 

0.04.'5  Chloropicrin 

0.19  Calcium  cyanide 

0.2.T  Paradiihlorbenzene 

0.33  Formalin 

Sodium  fluoride 
0.37  Phenol 

Naphthalene 

0.62  Cresol  (in  weak  solution) 

0.75  Urea  (in  strong  solution) 

1.0  Sodium  borate  (in  weak  solution') 
Zinc  chloride  (in  weak  solution) 
Ammonium  thiocyanate      (in  medium  solution) 

1.25  Calurea 

1.5  Potassium  cyanate 

1.9  ' '  Powdered' '  Cyanamide 

2.5  "Granular"   Cyanamide 

Sodium  chloride  (in  medium  solution) 

Sodium  hydroxide 

3.1  Carbon  disulphide 

Calnitro  (in  medium  solution") 

Ammonium  nitrate  (in  medium  solution) 

Kaiuit  (in  medium  solution) 

3.75  Sodium  nitrate  (in  medium  solution) 

4.4  Potassium  nitrate  (in  strong  solution) 

4.5  Nitro  chalk  (in  medium  solution) 
5.75              Calcium   hypochlorite  (in  strong  solution) 
6.0                Ammonimum  sulphate  (in  medium  solution) 
6.25             Carbonate  of  potash  (in  medium  solution) 
8.0                Carbon  tetrachloride 

14.0  Sulphate  of  potash  (in   strong  solution) 

20.0  2i)'/c   Superphosphate 

Phenothiazine 
23.0  Dog  urine 

Horse  urine 
37.0  Cow  urine 

40.0  16%  Superphosphate  (in  strong  solution) 

50.0  Quicklime 

65.0  Hydrated  lime 

Of  Xo  Value 

Flowers  of  sulphur 

Ground  limestone 

Raw  rock  phosphate 

Basic  slag 

Pyrethrum  powder 

Derris  powder 

White  hellebore  powder 
Among  the  numerous  other  chemicals  tested,  in  attempts  to 
find  reasons  for  the  lethal  factors,  compounds  of  iodine  were 
found  to  be  of  a  very  high  efficiency  indeed ;  thus  for  example, 
0.01%  of  methyl  iodide  (in  a  dilution  of  over  1:200)  was  com- 
pletely etfeetive.    Iodine  salts,  however,  are  expensive. 

On  farms  the  most  easily  obtained  (in  efficiently  drained 
stables)  is  urine;  in  addition  there  are  many  artificial  fertiliz- 
ers with  lethal  properties,  part  or  all  of  the  cost  of  which  may 
be  recovered  in  added  manurial  value. 

The  chemical  and  lethal  composition  of  urine  varies  consid- 
erably, not  only  according  to  the  species,  but  also  according 
to  the  food  and  health  of  the  animal  from  which  it  is  taken. 
In  a  few  cases  its  lethal  value  may  be  almost  nil,  but  generally 
speaking,  about  30  to  40  percent  of  the  weight  of  urine  to 
fresh  faeces  kills  the  free-living  stages  of  selerostomes.  Of  the 
artificial  fertilizers,  urea  is  the  most  potent,  requiring  about 
three-quarters  of  1  percent  by  weight  of  the  fresh  faeces  to 
sterilize  them  against  selerostomes.  Calurea  should  be  used  at 
the  rate  of  1%  percent,  while  about  2  percent  of  powdered 
cyanamid  is  needed  and  another  half  of  1  percent  if  used  in  the 
granular  form.  A  high  grade  kaiuit  is  one  of  the  next  most 
lethal  fertilizers  and  it  should  be  used  at  the  rate  of  5  lbs.  to 
100  lbs.  of  manure.  Closely  following  in  potency  are  many 
other  artificial  fertilizers  which  should  be  iised  at  the  rate  of 
about  6  percent  or  slightly  over,  compared  with  the  weight  of 
fresh  faeces. 


It  must  be  remembered  that  the  addition  of  some  alkali  fer- 
tilizers to  faeces  will  cause  the  loss  of  ammonia.  With  urea 
and  calurea,  much  ammonia  escapes  as  gas. 

The  quantities  mentioned  above  would  be  too  great  in  many 
cases  for  common  manurial  practice  if  the  whole  manure  heap 
had  to  be  treated,  but  since  the  heat  of  fermentation,  lack  of 
oxygen  and  other  factors,  prevent  the  development  of  larvae 
in  the  centre  of  a  well-built  heap,  is  should  only  be  necessary 
to  treat  the  top  and  sides,  provided  that  the  faeces  are  put 
there  as  soon  as  they  are  passed,  that  the  fertilizer  is  immedi- 
ately well  mixed  in,  and  that  the  pile  is  sufficiently  well- 
packed  and  protected  to  keep  the  fertilizer  in  contact  for 
some  time. 

The  use  of  a  well  constructed  manure  pit  is  highl3'  desirable 
and  ideally  should  be  divided  into  two  portions — one  to  con- 
tain manure  under  treatment  while  the  other  is  being  filled; 
the  first  portion  is  then  emptied  and  the  procedure  reversed. 
The  size  and  design  will  depend  on  local  circumstances.  Ma- 
nure stored  in  yards,  no  matter  how  stored,  should  be  inaccessi- 
ble to  stock. 

Selective  Dispos.\l.  As  there  is  normally  a  marked  speci- 
ficity shown  by  the  parasites  of  various  species  of  animals,  the 
manure,  especially  if  untreated,  should  be  used  on  ground 
which  is  inaccessible  to  the  species  of  animal  from  which  it 
came.  Thus,  horse  manure  should  not  be  used  for  top-dressing 
liastures  to  be  used  by  horses,  but  it  is  safe — or  reasonably  so 
— to  use  it  for  pastures  used  by  cattle  and  sheep.  It  may  also 
be  used  for  growing  crops — except  hay  crops  which  will  subse- 
quently be  fed  to  horses. 

Plowing  Under.  Wherever  possible,  manure  should  be 
plowed  under.  However,  this  procedure  cannot  be  guaranteed 
to  keep  eggs  and  larvae  below  ground.  Earthworms  bring  some 
to  the  surface  and  strongyle  larvae  are  capable  of  a  certain 
degree  of  upward  migration.  The  horse  selerostomes  have 
practically  no  migrating  ability  in  clay  soil  (provided  that 
there  are  no  cracks  in  the  soil),  but  in  sandy  clay  they  can 
migrate  4  inches  and  in  sandy  loam  '<  inches  upwards;  more- 
over, they  can  live  for  over  4  years  under  these  circumstances.. 
The  sheep  nematodes  Osterlagia  and  Xematodirus  can  regain 
the  surface  after  being  plowed  under  and  survive  for  S  to  10 
months;  Hacmonchus  survives  less  well.  Plowingin  may 
actuallj'  assist  development  by  breaking  up  the  soil  and  faeces. 

Fly  Destructiox.  Flies  are  important  in  connection  with 
manure  as  mechanical  carriers  of  worm  eggs  (e.g.  Ascari.s)  and 
as  actual  essential  intermediate  hosts  of  worms  (e.g.  Habro- 
iiciiia)  ;  the  part  they  play  as  mechanical  carriers  is  probably 
of  secondary  importance. 

From  the  second  point  of  view,  flies  must  be  prevented  from 
feeding  on  horse  manure;  this,  if  perfect,  would  completely 
eradicate  Eabrotieina  from  horses.  Cleanliness  in  stables  is 
essential,  even  small  quantities  of  manure  being  removed  daily. 
Spraying  manure  with  hellebore  (V-i  lb.  dissolved  for  24  hours 
in  10  gallons  of  water,  will  treat  10  cubic  feet)  or  powdered 
borax  (at  the  rate  of  1  lb.  to  16  cubic  feet)  are  recommended 
by  the  United  States  Department  of  Agriculture  for  the  pre- 
vention of  fly  breeding.  The  hellebore  has  no  injurious  effect ; 
the  borax  also  is  not  injurious  if  the  manure  is  not  used  in 
excess  of  l."i  short  tons  to  the  acre.  Creosote  oil  also  has  been 
recommended  as  a  deterrant ;  it  is  mainly  useful  under  war 
conditions  and  for  dead  horses. 

The  heat  generated  in  the  centre  of  a  well-constructed  ma- 
nure pile  or  throughout  the  manure  in  a  box  will  destroy  many 
maggots.  The  outer  layers  of  the  pile,  however,  will  not  be- 
come sufficiently  hot  and  will  require  treatment. 

Comparatively  few  eggs  or  larvae  leave  the  host  other  than 
in  the  faeces.  Those  that  do  include  the  pinworms,  trichina 
worms,  kidney  worms  and  microfilaria. 

Pinworms.  The  female  O.ryuris  equi,  the  only  known  pin- 
worm  of  importance  in  domestic  mammals,  leaves  the  host  to 
deposit  her  eggs  on  the  perianal  skin  or  stable  furnishings; 
sometimes  she  is  evacuated  in  the  faeces  or,  dying  in  the  rec- 
tum, her  eggs  are  so  passed,  but  this  is  exceptional  and  the 
few  cases  in  which  it  occurs  are  provided  for  by  the  usual 
procedures.  Most  eggs  are  actually  laid  on  the  skin  and  al- 
though very  little  is  yet  known  of  their  bionomics,  it  would 
seem  that  excess  of  water  is  quickly  fatal  to  them.  Accord- 
ingly, washing  of  stable,  stable  furniture,  grooming  kit  and 
perianal  skin,  would  reduce  the  possibilitj'  of  reinfection.  The 
removal  of  eggs  from  the  skin  by  washing  will  also  reduce  the 
local  irritation  and  render  reinfection  less  i)robable,  while  in 
heavy  infections,  warm  water  enemata  will  remove  gravid  fe- 
males mechanically  and  so  reduce  the  egg  output.  Infection  is 
by  swallowing  the  embryonated  eggs  either  directly  from  the 
skin  (where  the  irritation  causes  the  horse  to  bite)  or  as  a 
contamination  in  food.  General  cleanliness  and  the  use  of  hot 
water   (as  for  Ascarids)   will  undoubtedly  reduce  infections. 

Trichina.     While  a  few  larvae  pass  in  the  faeces  of  car- 


304 


nivores  mid  pigs,  tlirx  ild  not  :i|>|U'iii'  capaMc  nt'  Ihtoiiuiik  in 
t'cotivo.  Tliosf  wliii'h  will  lu'cnino  iiitVctivc  puss  into  tlio  imis 
I'K'S.  Control  lies  ontirclv  in  :ippi'(>pi'i.'itt<  fecdin);.  I'lKS  must 
not   lie  pcrmitti'd  to  cat  iincookiMl  inont  foods. 

KlPNKYWOKMS.  Till'  fggs  of  tlu'  snino  ki<lni'.v  worm  nri' 
passoil  ill  the  nriiio  and  cxposuro  to  drviiij;  and  8iiidi);lit  will 
dostroy  them.  This  can  often  l)C  done  liy  the  iirovision  of  a 
l>are  lot  around  the  hoK  h>t,  kept  free  from  grass  or  shade  and 
well  drained.  The  ckks  of  the  kidney  worm  of  carnivores  are 
also  passed  in  the  urine  hut  m)thinf;  is  yet  known  of  their 
I'ionomics  and  so  no  control  measures  can  he  adopted. 

Mu'iiO>'il,.\Ri.v.  Few  lilaria  worms  are  important  in  stock. 
.Ml  depend,  however,  on  their  removal  from  lilood  or  skin  l)y 
a  hlood  sucking  insect.  Control  accordinijly  deiieiids  on  insect 
control,  screening  of  houses  and  related  measures. 

2.     Methods   of   Destroying    Infective    Larvae 
(free  or  enclosed  in  egg  shells) 

(a>      Disinfection 

(i.)  Chemical — There  is  no  good  chemical  disinfectant  for 
larvae  enclosed  in  their  vgg  shells  (e.g.  Ascarids^  and  disin 
fectaitts  for  this  ])uritose  are  jiractically  useless;  in  f:ict  they 
may  assist  the  larvae  hy  destroying  fungi  and  bacteria  which 
are  themselves  harmful  to  the  ]iarasites.  The  use  of  chcmi 
cals  against  free  lai*\"ae  has  lieeu  discussi'd  ahovc  as  it  is  not 
po.ssihle  to  separate  the  actions  of  chemicals  on  the  preinfectivc 
l.-irvae  from  the  action  on  infective  larvae,  although  in  general 
the  latter  are  more  resistant. 

(ii)  Urat  is  lethal  for  all  forms  of  parasites  and,  in  the 
form  of  very  hot  water  or  live  steam,  is  one  of  the  most  efti 
sient  disinfectants  at  our  command.  It  is  the  only  one  of  any 
practical  value  against  -X.scarids  and  its  use  is  fundamental  in 
the  control  of  these  very  serious  parasites  in  awine  and  car 
nivores.  It  can  be  used  either  as  hot  water  (with  lye  or  soap 
to  loosen  the  dirt)  or  steam.  Its  use  is  recommended  in  all 
kinds  of  stables  as  it  kills  every  kind  of  larva.  While  its  value 
has  been  recognized  for  many  years,  it  is  only  reci'utly  that 
accurate  knowledge  has  been  obtained  on  the  amount  of  heat 
required  and  it  was  found  that  ascarid  eggs  could  be  killed  in 
1  second  at  158°  F.,  "J  seconds  at  140°  F.  and  ."  seconds  at 
140°  F. 

(iii),  Cleanliiics.i  both  of  animals  and  of  ijuarters,  is  of 
great  value  in  reducing  numbers  of  parasites.  Washing  of 
udders  of  sows  with  warm  water  and  soap  removed  man.v  infec- 
tive ascarid  eggs.  Washing  of  stables  (including  window-sills 
and  other  places  where  dust  lies)  mechanically  removes  selero 
sfome  larvae  which  have  very  great  powers  of  resisting  drying 
and  which  otherwise  would  be  blown  on  to  the  animals'  feed 
or  water. 

(b)     Pasture 

Little  work  has  yet  lieeu  done  on  the  control  of  parasites  on 
pasture  and  arable  land  although  the  sub.ject  is  of  great  impor 
tance  in  all  parts  of  the  world.  Pastures  cannot  l>e  treated 
daily  as  can  a  manure  liejt])  and  so  it  is  uminly  infective  larvae 
which  have  to  be  killed.  They  are  then  in  position  in  which 
destruction  is  difficult.  Chemical  treatment  has  many  dis- 
advantages— cost  being  one  of  the  most  obvious.  Nevertheless 
some  chemicals  have  been  tried;  copper  sulphate,  bleaching 
powder  and  lime  have  jiroved  unsatisfactory  in  practice.  The 
mo.st  promising  appear  to  be  those  which  could  be  applied  as  a 
gas  and  retained  on  the  ground  by  a  mulch  of  paper,  a  tarpau- 
lin trailed  behind  a  tractor  or  some  similar  method.  Such  gases 
as  chloropicrin  (a  tear  gas),  calcium  cyanide  and  others  men- 
tioned have  at  least  possibilities  in  that  direction.  .Mternately 
it  may  be  practical  to  use  a  delii|uescent  salt  alone  or  mi.xed 
with  a  very  lethal  chemical  so  that  the  larvae  may  be  attracted 
toward  the  moisture. 

These  are  suggestious  for  the  future;  meanwhile,  the  only 
effective  way  is  to  collect  the  droppings  daily  before  the  larvae 
can  migrate  to  soil  or  grass.  Obviously  this  method  has  very 
considerable  limitations,  but  it  has  been  done  on  stud  farms. 

.\s  infective  larvae  of  bursate  nematodes  do  not  feed  but  live 
entirely  on  foodstuffs  stored  up  in  their  bodies,  their  life  can 
be  shortened  by  causing  them  to  use  up  this  source  of  eiu'rgy 
more  quickly  than  usual.  Modeiate  warmth  and  light  are 
natural  stimulants  and,  as  continual  spreading  and  harrowing 
e.xposes  them  to  these  physical  ageuts,  it  is  of  assistance  in 
reducing  the  numbers  but  will  not  completelv  eradicite  them. 
It  is  especially  effective  in  dry,  warm  climates. 

The  burning  of  grass — often  a  valuable  agricnitur.il  practice 
- — theoretically  must  destroy  some  larval  worms  on  the  pasture 
aud  in  the  ground  beneath;  it  cannot  be  relied  uijon  to  destroy 
them  all  aud  it  may  also  give  the  larvae  access  to  the  more 
succulent  grass  beneath.  It  does,  however,  help  to  raise  the 
nutrition  plane  of  the  animals. 


.\  II  worm  lai'vac  icqniii'  ,-i  degree  of  moisture  for  develop- 
ment, allhongli  only  »  few  (e.g.  Did jiiirniiliiK)  .are  capable  of 
de\cIopment  in  w:iter  :ilone.  Drainjige,  an  essential  step  in  the 
control  of  these  luiigworms,  is  always  of  general  value  In  damp 
pastures,  it  impro\-es  the  (piality  of  the  gr'ass  ami  so  improves 
the  resistance  of  the  host,  but  it  is  donbtfnl  if  it  di'strovs  many 
larvae. 

Drying  of  larvae  has  very  variable  results.  Oidin.ary  drying 
is  quickly  leth.il  to  uuiny  of  the  lu'uiatode  larvae  of  slieej)  but 
only  slightly  so  to  other  larvae  and  forms  enclosed  in  egg  shells, 
like  .\scari<ls.  Ten  per  cent  of  sclerostouie  larvae  can  survive 
4  nuinths  air  drying  in  an  incubator  at  7.")°  to  HU°  F.  and  they 
have  been  f(Uind  alive  in  window  dust  in  stables  out  of  use  for 
several  ye.ars.  ()rdin;uy  drying  distroys  only  some  larvae  but 
it  may  destr<iy  sufficient  to  prevent  disease. 

Urought  has  not  nece.ss;irily  the  .same  effect  as  draining  of 
|i;istures.  In  dry  seasons  grass  is  short  and  scarce,  more  must 
be  eaten,  (especially  by  sheep)  it  is  eaten  "short"  and  a 
greater  area  of  the  pasture  is  grazed  daily.  Larvae  of  some 
worms  tend  to  live  near  the  roots  of  the  grass  and  .so  under 
these  conditions  m;iny  more  reach  the  host:  the  i)arasite  intake 
varies  directly  with  the  time  of  grazing.  The  resistance  of  the 
host,  through  poorrii'ss  of  the  feed,  is  lowered  and  so  serious 
disease  may  result. 

.Moreover,  embiyouated  but  uidiatched  eggs  of  sheep  gastro- 
intestinal nematodes  are  often  very  resistant  to  drought  aud  so 
these  tend  to  accumulate.  When  the  drought  breaks  they  hatch 
simultaneously,  and  if  the  moist  weather  continues  for  a  week  or 
so,  they  may  cause  an  explosive  outbreak  of  disease.  However, 
short  jieriods  of  drought  interrupted  by  short  showeis  have  an 
ojiposite  effect. 

Heavy  rain  is  inimical  to  the  development  of  sclerostome 
larvae  in  their  ])reinfective  st;iges ;  whether  this  is  due  to  the 
fact  that  subsecpient  drying  is  easier,  is  not  yet  known.  Heavy 
rainfall  in  hill  country  often  has  the  effect  of  mechanically 
washing  Larvae  and  faeces  off'  the  hillsides  and  so  reduces  the 
number  of  infective  larvae;  this  is  especially  true  in  troi)ical 
islands  and  uplands  where  rainfalls  are  often  very  heavy.  How- 
ever, it  may  concentrate  infections  in  the  valleys.  In  fiat  country 
the  larvae  are  washed  off  the  grass  but  quickly  crawl  back 
again.  (It  should  be  noted  that  an  excessive  growth  of  grass 
may  encouiage  sheep  to  feed  between  the  tall  grasses.  It  is  in 
this  ])osition  that  most  larvae  are  found  and  so  heavy  infections 
ma.v  result ) . 

Continued  exposure  to  extreme  cold  undoubtedly  has  a  serious 
effect  on  the  free  stages  of  parasites  but  in  many  cases  we 
cannot  rely  on  the  natural  cold  of  winter  to  act  as  an  important 
agent.  Destruction  dci)ends  at  least  to  some  extent  on  snowfall. 
Where  the  snow  is  adequate,  the  temperature  of  the  grouiul  be- 
neath is  almost  independent  of  the  air  temperature,  and  even 
when  the  air  temperature  falls  to  0°F.,  the  ground  temperature 
is  still  little  below  freezing.  The  type  of  winter  most  destruc- 
tive is  the  siioiflixx  winter  and  a  comparatively  mild  winter 
with  little  snow,  is  much  more  destructive  than  a  severe  one  with 
a  heavy  snowfall. 

Moreover,  in  countries  with  a  normally  cold  winte~,  animals 
of  all  kinds  are  stabled  during  cold  weather  and  the  parasites 
can  be  carried  over  as  adults  in  the  host  or  as  eggs  in  the  ma- 
nure in  the  barn. 

In  countries  with  a  mild  winter  climate,  frost  may  actually 
increase  the  life  span  of  the  parasites,  although  repeated  freez- 
ing and  thawing  is  much  more  lethal  than  continued  freezing. 
There  is  little  accurate  knowledge  yet  available  on  the  lower 
thermal  death  points  of  parasites.  It  is  known,  however,  that 
some  forms,  such  as  horse  .sclerostome  larvae,  can  survive  very 
low  temiieratures  (-3t)°F.)  for  long  periods;  others  such  as 
sheep  nodular  worms,  are  easily  killed  by  cold.  Each  species 
has  its  own  critical  temperature  or  range  of  temperature  and 
this  tends  to  control  its  distribution  independently  of  man. 
However,  man  may  often  jiermit  a  parasite  to  survive  in  an 
otherwise  unfavourable  environment — by  suitable  methods  of 
animal  husbandry.  Eastern  Canada  has  a  hot  summer  and  a 
cold  winter,  but  animals  are  housed  for  the  coldest  months  of 
the  yea  I'.  This  i)ermits  of  the  existence  of  such  parasites  as 
Orsopliai/fislfnninn  c'lliunbinintni  in  eastern  Canada,  although  it 
is  absent  from  British  Columbia  and  Great  Britain,  both  of 
which  are  less  extreme   in  temperature. 

Sunlight  is  harmful  to  most  nematodes  but  whether  because 
of  light  or  heat  or  both  is  not  definitely  known.  Its  value  in 
destloying  larvae  of  pig  kidney  worms  is  well  recognized. 

Dung  feeding  insects  such  as  beetles,  are  known  to  destroy 
many  worm  I'ggs  but  in  some  cases,  the  eggs  appear  to  pass 
through  them  and  they  may  act  as  distributors  rather  than 
destroyers.  Such  insects  may  act  as  true  vectors  of  some 
worms. 

Mixed  glazing  on  pasture  is  usually  of  great  value,  as  horses 
will  eat  and  digest  the  larvae  of  worms  which  mature  in  cattle 
and  so  on.  In  this  way,  the  number  of  infective  larvae  swal- 


S05 


lowed  by  eat-h  kind  of  host  is  greatly  reduced.  This  simple 
procedure  often  causes  (|uite  startling  results  and  may,  by  it- 
self, be  sufficient  to  prevent  actual  disease.  Thus,  on  heavily 
infected  horse  pastures,  sheep  may  remove  100,000  eggs  per 
head  daily. 

Hay  often  has  the  effect  of  mechanically  removing  a  large 
number  of  infective  larvae  from  a  pasture. 

Actual  removal  of  the  turf  and  re-so«ing  to  permanent  pas- 
ture may  be  and  has  been  used  in  extreme  cases.  But  this  can 
only  be  recommended  when  heavily  infested  but  very  valuable 
land  is  concerned  or  where  the  tu:f  may  be  sold  for  urban 
purposes. 

3.  Avoidance  of  Infection  of  the  Host  and  Prevention 
of  Ingress  of  the  Parasite 

(a)  General  Hygiene — This  is  of  the  utmost  importance. 
Many  horses  are  confined  to  stables  throughout  the  year  and 
when  they  are  kept  clean  and  permanent  litter  avoided,  the 
worm  infections  are  at  a  decidedly  low  level.  Ordinary  methods 
of  cleanliness  alone  can  be  of  great  value.  This  indeed  is 
one  of  the  basic  principles  underlying  the  very  successful  Mc- 
Lean County  Sanitation  System  for  controlling  Ascarids  in 
pigs;  in  its  essentials,  this  system  simply  requires  cleanliness 
of  sow  and  breeding  places  and  avoidance  of  exposure  of  the 
young  animals  to  infection. 

(b)  Disinfection — Small  quantities  of  faeces,  overlooked  in 
general  cleaning  of  stables  are  important  sources  of  infection. 
These  may  be  sterilized  by  very  hot  water  or  steam.  The  gen- 
eral bactericidal  disinfectants  are  not  very  good  for  this  jiur- 
pose,  the  least  ineffective  being  3  percent  lye  and  .l  percent 
lysol.  These  are  of  value  both  for  horse  and  sheep  strongyles, 
but  require  an  hour's  contact  to  destroy  them.  They  are  prac- 
tically useless  against  A.scarids  and  related  worms,  however. 
Lye  in  its  usually  applied  strength  (about  1  percent)  is  quite 
useless  iis  a  disinfectant  for  any  kind  of  worm,  although  it  is 
useful  in  freeing  parasite  eggs  from  dirt  and  making  them 
more  readily  available  to  the  destructive  action  of  other  agents. 

(c)  Permanent  Pastures — There  is  no  doubt  that  permanent 
pastures  form  the  greatest  single  danger  to  stock  and  that 
Maurice  Hall's  dictum  "Permanent  pastures  perpetuate  para- 
sites'' is  still  of  the  utmost  importance.  The  pastures  con- 
centrate eggs  and  larvae,  and  improved  pasture  culture,  by  in- 
creasing the  stock-carrying  capacity,  still  further  increases 
the  danger.  At  present  there  is  no  effective  method  of  pre- 
venting infection  on  them. 

It  was  once  believed  that  temporary  pastures,  plowed  in  and 
re-sown  would  overcome  this  difficulty,  but  recent  work  has 
shown  that  heavy  infections  of  sheep  may  result  from  such  a 
practice.  The  eggs  and  larvae  plowed  in  are  protected  from 
sun,  heavy  rain  and  drought  and  many  emerge  with  the  new 
grass. 

So  far  attempts  at  altering  the  pasture  flora  to  produce  an 
environment  less  suitable  for  development,  or  a  type  of  grass 
less  suitable  for  migration  of  the  worms  and  so  less  likely  to 
cause  an  infection,  have  been  comparatively  ineffective  but  are 
still  being  tested.  Taylor  finds  that  larvae  climb  higher  on 
clover  than  on  grass  and  that  such  fertilizers  as  basic  slag, 
by  encouraging  clover  growth,  increase  parasitism.  On  tlie 
other  hand,  sainfoin  carries  only  5.50  larvae  per  pound,  under 
conditions  where  grass  carries  1,1)00,  probably  because  of  the 
relatively  slight  contact  with  the  ground  which  the  large  sain- 
foin  plant   makes. 

Manuring  a  pasture  by  nitrates  encourages  rapid  growth  of 
grass  and  may  lead  to  a  reduction  in  larvae  per  pound  of  grass 
and  so  produce  a  smaller  intake.  However,  a  dense  growth  of 
grass  provides  favourable  cover  for  parasites  and  infection  is 
proportional  to  density  of  cover;  sparse  growth  permits  natural 
agencies   to   reach   them. 

(d)  notations.  Rotation  of  permanent  pasture  when  this  is 
possible,  is  of  value  but  it  postulates  a  large  amount  of  pasture 
land  and  much  fencing  as  the  animals  have  to  be  moved  on 
before  the  eggs  they  have  passed  give  rise  to  infective  larvae 
(5  to  7  days)  and  kept  away  from  the  "used"  land  until  all 
larvae  are  dead;  this  period  varies  with  the  parasite  con- 
cerned, the  soil  and  the  climate  and  no  general  rules  are  yet 
possible.  The  cleanest  land  should  always  be  reserved  for  grow- 
ing stock  which  is  more  susceptible  to  worm  disease  than  older 
stock. 

However,  a  certain  amount  of  rotation  of  stock  may  be  prac- 
ticed. Not  only  may  horses  follow  ruminants,  but  cattle  may, 
to  some  extent,  follow  sheep  and  old  animals  follow  young 
ones.  Under  these  circumstances,  a  shorter  fallow  period  is 
possible  as  subsequent  animals  eat  many  of  the  larval  parasites 
of  their  predecessors. 

It  is  often  practicable  to  graze  lambs  on  clean  pasture  and 
follow  them  by   old  sheep  which  have  some  degree   of   resist- 


ance to  gastro  intestinal  nematodes.  In  choosing  a  rotation 
such  as  this  (or  such  as  cattle  following  sheep)  care  must  be 
taken  to  know  which  parasites  are  concerned  as  only  some  may 
thus  be  treated.  The  simultaneous  grazing  of  several  kinds  of 
animals  (such  as  horses  and  sheep)  is  only  an  extension  and 
improvement  of  this  method. 

(e)  Bare  Lots — The  use  of  bare  lots  for  young  stock  has 
much  to  recommend  it.  There  is  no  grass  for  them  to  eat  and 
conditions  for  development  of  worms  are  highly  unfavourable, 
iloreover,  as  the  animals  must  be  watered  from  troughs  the 
danger  of  infection  is  further  decreased. 

This  method  has  enabled  lambs  to  be  raised  in  districts  where 
worm  infections  are  so  high  as  to  kill  a  large  percentage  of  ani- 
mals raised  on  pasture. 

Partial  bare  lots  in  pig  pastures,  in  lands  where  the  kidney 
worm  is  prevalent,  are  of  assistance  in  controlling  this  parasite 
also.  Faeces  also  are  concentrated,  making  their  removal  or 
treatment  easier. 

(f )  Fencing — Fencing  is  of  value  in  dividing  pastures  for  ro- 
tation, or  to  ensure  uniform  grazing  and  to  avoid  overgrazing 
of  certain  parts.  Temporary  fencing  (as  in  folding)  so  ar- 
ranged to  allow  lambs  (but  not  ewes)  to  reach  new  pastures 
in  a  progressive  system  of  feeding,  is  also  of  value,  but  entails 
a  certain  amoui\t  of  labour,  as  the  fences  must  be  moved  weekly. 
In  this  case  the  lambs,  if  they  are  not  weaned,  have  the  run 
of  the  pasture  ahead  as  well  as  the  one  in  which  the  ewes  are 
kept,  or,  if  they  are  weaned,  the  one  ahead  only.  The  very 
greatest  care  must  be  taken  to  prevent  the  lambs  gaining  ac- 
cess to  old  ground  already  grazed  by  the  ewes  and  from  which 
they  have  been  moved  on.  If  this  is  not  done  a  heavy  infec- 
tion is  extremely  probable. 

(g)  Limitation  of  Numbers — Limitation  of  numbers  is  really 
an  attempt  to  return  to  nature  from  artificial  conditions  of 
modern  farming.  It  is  the  rational  method  with  permanent 
pastures  where  over-stocking  has  such  disastrous  results.  A 
reduction  of  .50  percent  in  numbers  on  a  pasture  means  a  much 
greater  reduction  than  that  in  parasites.  It  also  spreads  out 
the  rate  of  intake  of  parasites  and  allows  resistance  to  de- 
velop. Moreover,  overstocking  decreases  the  food  yield  of  the 
pasture  and  encourages  closer  grazing  and  a  higher  worm  in- 
take. The  poorness  of  the  food  supply  decreases  body  resist- 
ance and  so  encourages  parasitic  disease. 

(h)  Night  Housing — Night  housing  is  often  valuable  as  most 
strongyle  larvae  are  able  to  climb  on  to  grass  but  do  so  only 
when  it  is  damp,  retreating  towards  the  soil  as  it  dries.  Heavy 
dews  are  very  suitable  for  this  upward  migration  and  the  simple 
procedure  of  keeping  stock — especially  young  stock — off  the  pas- 
ture until  the  dew  has  evaporated,  has  frequently  made  all  the 
difference  between  health  and  disease.  Husk  in  cattle  is  often 
caused  by  early  grazing  and  night  housing  is  particularly  use- 
ful with  that  disease. 

(i)  Saised  Troughs — Feed  racks,  raised  troughs  and  clean 
water — especially  in  connection  with  bare  lots  and  permanent 
pastures  which  are  heavily  stocked — is  valuable  in  reducing 
intake  of  parasites.  It  is  of  value  also  in  stables  where 
the  floors  are  often  heavily  contaminated  with  infective  larvae 
and   it   is   especially   valuable   for   young   stock. 

(j)  Silage  and  Folding — The  use  of  silage  helps  to  reduce 
numbers  of  larvae  taken  in  by  the  host,  and  the  temjierature 
generated  in  its  preparation  may  destroy  some  larvae  and  shor- 
ten the  life  of  others;  in  general,  silage  does  not  carry  the 
heavy  infections  that  grass  does. 

Folding  on  green  crops,  with  the  aid  of  hurdles,  is  also  of 
value,  provided  the  same  ground  is  not  used  too  often  for 
this  purpose.  The  animals  must  be  moved  every  6  days  or  so 
and  the  young  must  have  first  choice — even  going  one  fold  ahead 
of  the  adults — and  must  not  under  any  circumstances  be  per- 
mitted to  enter  old,  used  folds. 

Eotational  grazing  (e.g.,  nitrogenous  stimulation  of  grass 
which  is  grazed  on  successive  fields)  may  cause  a  heavy  infec- 
tion but  generally  increases  resistance  to  disease. 

The  penning  of  stock  on  arable  ground  is  more  dangerous 
than  the  free  ranging  of  stock  on  permanent  pastures  as  they 
tramp  faeces  into  the  ground  and  so  improve  the  chances  of 
the  parasites  developing;  under  these  conditions  sandy  soil 
is  probably  more   dangerous   than   clay. 

Food  cabinets,  as  recently  developed,  afford  a  method  for 
the  quick  growing  of  green  crops  under  circumstances  which 
preclude  any  infection  at  all.  The  animals,  if  housed  on  con- 
crete and  kept  clean,  need  never  acquire  aii.v  intestinal  para- 
sites at  all  with  this  system.  The  food  cabinets  permit  of 
the  growing  of  "grass"  in  a  week  from  seed  without  the  aid 
of  soil.  This  is  done  by  using  perforated  trays  of  certain 
grains  (notably  barley,  wheat  and  maize)  in  a  constant  tem- 
perature cabinet  and  exposing  them  to  the  action  of  moisture 
and  artificial  fertilizer  daily.    By  a  suitable  rotation  a  constant 


306 


output  of  (Tinss  is  tliiis  olitjiiiu'd.   fnc   fmni   iliscasc  oi'|;!>>>>"<"'< 
mid   iiidopoiidont   of   rliiiiatr. 

(k^i  Cookinii — Larvai"  cani'.-d  liv  food  aiiiinalH  arc  dcsl roved 
liy  lii'atinK  and  so  all  meat  and  tisli  foods  fed  to  pitjs  or  car- 
iiivori's  should  bo  cooked  unless  free  from  siispicion ;  this  is 
liiKlilv  important  in  the  control  of  the  trichina. 

U)  Flourboarils — The  use  of  floorlKUirds,  wire  or  concrete 
Hoors  for  i>iKs,  carnivores  and  poultry,  provided  they  are  kept 
clean,  niit  only  iiermits  of  ellicient  I'nj;  destruction  lu  elitnina 
tion,  liut  prevents  infection,  or  .it  least  reduces  it  very  con 
sideralily. 

(ni^  Qiuiraiitiiii — New  stock  should  not  be  introduced  to  a 
worm  controlled  farm,  until  it  has  tieen  carefully  cxainincd 
for  parasites.  A  single  boar,  for  example,  may  introduce 
ascarids  to  a  worm  free  pigBeiy.  Kiioiin  c.irriers  of  any 
kind  of  parasites  already  present  should  be  treated,  iso- 
lated or  at  least  excluded  from  common  crazing.  Wild  aiii 
mals  which  harbour  parasites  communicable  to  domestic  nni 
mals    should    be    denied    access    or    be    destroyed. 

Vectors 

Many  roundworms  of  domesticated  animals,  require  essen- 
tial intermediate  hosts.  These  may  be  arthropods,  earth- 
worms, snails,  or  vertebrates  such  as  fish,  amidiibia,  and 
even  other  mammals.  A  knowledf;''  of  the  life  history  of 
both  carrier  and  parasite  is  essential  before  control  can  be 
nndertaken.  This  may  involve  not  only  destruction  of  the 
vector  but  avoidance  of  infection  of  the  vector,  in  many 
oases   a    procedure   of   almost    equal    importance. 

Destruction  of  infective  larvae  in  vertebrates  may  be  un- 
dertaken by  meat  inspection  and  physical  or  chemical  de- 
struction of  condemned  material.  Cooking  of  all  garbage 
fed  to  pigs  is  an  invaluable  means  of  controlling  Trichina 
in  pigs  and  so  in  man.  In  the  case  of  pork  for  human  con- 
sumption, thorough  cooking  until  the  flesh  turns  white,  is  a 
perfect  safeguard;  pork  is  often  eaten  undercooked.  Where  it 
is  eaten  raw.  it  should  be  subjected  to  chemical  treatment, 
chilling  or  heating  (as  laid  down  in  the  regulations  of  the 
I'nited   States    Bureau   of   Aiiiinal    Industry). 

Earthworms  carry  a  considerable  number  of  parasites  to  do- 
mestic animals  and  their  control  is  extremely  difficult.  Chemi- 
cals and  sand  have  been  used  but  more  successful  results  are 
obtained    by   avoidance   of.  infection. 

Insect  destruction  is  almost  as  difficult.  Most  of  the  im- 
portant carriers  are  dung  feeders  and  are  not  easily  attacked. 
Many  of  the  usual  contact  or  stomach  ]ioisoiis  are  available  but 
their  use  has  been  extremely  limited.  A  more  rational  means 
of  control  is  an  attack  on  the  breeding  places  and  this  is 
feasible   for   house    flies,   mosquitoes   and    ectoparasites. 

Avoidance  of  infection  of  the  vectors  is  almost  as  im- 
portant as  their  destruction.  This  can  be  effected  not  only 
by  proper  manure  disposal  and  treatment,  but  by  means  de- 
signed to  keep  animals  and  vectors  apart.  Thus,  for  ex- 
ample, the  lungworms  of  swine  are  carried  by  manure-fre- 
quenting earthworms;  if  swine  faeces  are  disposed  of  in 
situation  where  the  swiue  themselves  cannot  reach  the  para- 
sites can  be  controlled.  Swine  confined  entirely  to  proper 
concrete    pens,    should    never   have    lungworms. 

In  cases  where  the  larvae  are  actually  removed  from  the 
bodv  by  biting  flies,  protection  from  these  will  not  only 
prevent  vectors  becoming  infected  hut  will  prevent  the  hosts 
being  infected  in  turn.  In  addition,  of  course,  measures  for 
the  control  of  these  insects  (mo.squitoes.  midges,  black  flies 
and   stable  flies)    should   be   undertaken. 

As  the  spirurid  nematodes  are  carried  l;irgely  by  dung-fre- 
quenting insects,  manure  treatment  and  disposal  will  help  to 
reduce  infections. 


Destruction  Within  the  Host 

Antiparasitic  drugs  are  used  for  two  purposes — to  treat 
clinical  cases  or  to  provide  a  clean  herd.  The  first  requires  the 
removal  of  only  sufficient  parasites  to  relieve  the  symptoms; 
the  second  postulates  a  much  more  efficient  drug,  one  which 
would  destroy  all  parasites  being  the  ideal.  There  are  few  such 
drugs  availalde  as  yet  and  such  as  are,  may  be  used  with  suc- 
cess against  a  comparatively  small  number  of  species;  fortu- 
nately, however  these  include  some  of  the  important  forms. 
Where  these  drugs  are  available,  for  either  internal  or  external 
parasites,  their  use  as  a  means  of  control  is  highly  important. 
All  members  of  the  herd  should  be  treated  regularly  until  all 
parasites  have  disappeared  and  no  residual  infection  left  to  act 
as  a  starting  point  for  re-infection. 

This  mass  treatment,  where  it  has  been  employed  correctly 
and  under  strict  supervision,  has  given  excellent  results.     It  is 


ncccssaiy  to  emphasii'.c  the  necessity  for  strict  supervision.  .Ml 
drugs  used  to  destroy  parasites  ari'  animal  poi.sons,  at  least  to 
sonic  exii'iit.  and  their  indisi  rimiii.'ili'  use  by  l;iyinen  is  apt  not 
only  to  nullity  their  results  but  to  be  actii.-illy  dangerous  to 
the  animals.  Their  use  ;iccordingly  requires  the  aid  of  the 
practicing  vi'terinarian.  No  other  jierson  knows  the  h.'ibits  and 
location  of  the  parasite,  the  physiology  of  the  host,  the  correct 
drug  to  use,  the  technique  of  its  administration  and  its  contra- 
indications. If  this  jirinciple  is  accepted,  it  follows  that  co- 
(qierative  district  schemes,  involving  panels  of  jiractitioners, 
.•ire  essential.  It  is  useless,  as  a  control  measure,  to  er;idicate 
any  |iarticular  parasite  on  one  farm  if  the  next  remains  lic;ivily 
infested.  The  first  sti'ps  to  be  taken  must  be  those  of  an  cdii 
cational  nature  to  be  followed  by  some  cii.'ibling  order  frinii  a 
higher  .•luthoiity  ;  this  order,  however,  should  come  only  as  the 
result  of  a  demand  from  the  district  itself.  Thereafter,  by  a 
suitably  designed  veterinary  jianel  treating  animals  in  groujis 
in  sub  districts,  the  entire  population  in  the  district  can  lie 
treated  ipiickly,  cheaply  and  efficiently. 

Reservoir  Hosts 

NVild  aitiin.'ils  belonging  to  the  s;iiiu'  major  groiijis  as  domcsti 
cated  ones,  often  harbour  jiarasites  transnii.ssible  to  them  and 
there  are  innumerable  cases  on  record  of  such  animals  or  even 
animals  more  distantly  related,  acting  as  reservoirs  of  infec- 
tion as  well  as  transmitters  of  new  species  to  domestic  :.ni- 
mals.  It  is  of  ini])(irtaiice  to  know  what  parasites  occur  in  the 
wild  fauna  of  a  cdinitry  or  district  and  to  take  such  stejis 
as  may  be  possilile  to   keep  those   parasites  ivithin   control. 

At  present  only  one  or  both  of  two  jilaiis  of  action  are  avail- 
able; cither  to  destroy  all  the  wild  carriers  or  to  prevent  their 
intermingling  with   domestic  ones  by  suitable  segregation. 

Indigenous  wild  mammals  and  birds  not  only  possess  jiara- 
sites  transniissilile  to  man  and  to  domesticated  stock  but  may 
become  infected  from  the  introduced  stock  and  act  as  uncon- 
trolled reservoirs  of  the  new  iiarasites.  An  adequate  knowledge 
of  the  parasitic  fauna  of  the  indigenous  wild  animals  is  an  es- 
sential steji  in  controlling  parasites  of  domestic  stock.  It  is 
surprising  how  little  has  been  done.  The  Institute  of  Parasi- 
tology in  Canada  is  conducting  such  a  parasitological  survey  to 
ascertain  the  distribution  and  intensity  of  infections  in  all 
forms  of  animal  life  in  the  Dominion.  A  large  amount  of 
voluntary  assistance  in  collecting  has  been  readily  given  by 
all  classes  of  persons — official,  commercial  and  private — and 
although  many  years  must  pass  before  the  survey  is  even  aji- 
proximately  complete,  it  has  already  yielded  invaluable  re- 
sults. This  survey  has  also  been  extended  to  the  West  Indies 
and  it  is  to  be  liojied  that  other  countries  will  take  similar 
steps  and  enable  a  world  map  to  be  prepared  showing  the  dis 
tribution  and  importance  of  all  parasites  in  all  kinds  of  animal 
life. 

Avoidance  of  Parasitic  Disease 

Effective  control  of  any  species  of  parasites  will  eliminate 
the  disease  caused  liy  it,  but  even  when  this  cannot  be  done, 
steps  should  be  taken  to  reduce  or  avoid  the  disease.  With  a 
very  few  obvious  exceptions,  disease  depends  on  numbers  of 
parasites  present  but  we  are  unable  to  state  the  exact  point  at 
which  clinical  disease  begins,  even  if  we  admit  the  theoretical 
concept  that  even  a  single  jiarasite  causes  some  disease.  There 
is  too  little  real  knowledge  aliout  the  action  of  parasites  and 
too  many  factors  involved,  including  nourishment,  resistance 
and  presence  of  other  parasites. 

In  general,  however,  it  may  be  stated  that  any  attemiit  to 
reduce  the  number  of  parasites  ingested,  to  increase  the  re- 
sistance of  the  host  or  to  raise  the  standard  of  fitness  of  an 
animal  offsets  the  effects  of  the  parasite  to  some  extent  and 
helps  to  reduce  parasitic  disease  even  if  it  does  not  eliminate 
parasitism. 

(a)  Prireutivc  Licks — The  theory  underlying  the  use  of  pre- 
ventive licks  is  that  a  small  daily  dose  of  some  drug  taken  in  a 
mineral  lick,  will  either  kill  the  larvae  taken  in  the  food  or 
else  render  their  environment  so  abnormal  that  they  will  not 
develop;  it  is  not  suggested  in  this  way  to  administer  drugs 
against  adult  parasites.  There  is  no  conclusive  proof  yet  that 
preventive  licks  are  .satisfactory.  Good  results  have  been 
claimed  with  tobacco  and  bluestone,  but  the  subject  must  still 
be  considered  as  in  the  exiicrimental  stage. 

There  is  no  doubt  that  the  efficiency  of  some  of  the  older 
worm  medicines  was  due  to  their  "tonic"  action  on  the  liody 
and  that  this  was  particularly  the  ca.se  with  such  elements  as 
iron,  copper,  cobalt,  arsenic,  phosphorus  and  calcium.  These 
appear  to  be  used  by  the  body  to  repair  or  counteract  damage 
done  by  the  parasites,  as  well  as  in  some  cases  to  destroy  the 
parasites  themselves.  A  supply  of  such  materials  in  mineral 
licks   is   often   of   great   importance   in   jireventing   the   develop- 


307 


ment  of  disease  symptoms.  It  not  infrequently  happens  that 
animals  fed  on  a  "  natural ' '  diet  may  be  receiving  insufficient 
phosphates  or  calcium  or  other  elements,  and  the  use  of  licks 
containing  these  substances  immediately  increases  the  general 
condition  of  the  animal  and  so  assists  in  control  of  parasitic 
diseases. 

(b)  Diet — It  is  extremely  difficult  to  separate  many  para- 
sitic diseases  from  those  caused  by  deficiencies  in  diet.  There 
is  evidence  to  suggest  that  in  many  cases  the  two  are  so  closely 
interwoven  as  to  be  inseparable  and  that  their  effects  are  mu- 
tually cumulative.  There  is  no  doubt  that  in  very  many  cases, 
a  sufficient,  well  balanced  diet,  balanced  in  all  its  accessory 
factors  as  well  as  its  main  constituents,  will  prevent  parasitic 
disease  and  will  often  actually  reduce  the  numbers  of  para- 
sites harboured.  Pasture  treatment,  such  as  "top-dressing," 
is  often  a  valuable  way  of  doing  this.  This  adequate  diet  is 
jiarticularly  important  for  immature  animals  and  every  effort 
should  be  made  to  secure  this.  This  is,  of  course,  true  for  all 
preventive  measures  to  be  taken  but  is  especially  important,  ia 
connection  with  diet. 

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parasitic  worms.  Proc.  7th  World's  Poultry  Cong.  & 
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s.,  V.  13(18):  399-506. 

1935. — The  veterinarv  aspect  of  parasitologv.  Ibid., 
V.  15(5):   103-114. 

1938a. — Grazing  hygiene  with  respect  to  parasitic  dis 
eases.     Proc  13th  Internatl.  Vet.  Cong.,  v.  1 :  672-682. 

1938b. — Observations  on  the  bionomics  of  strongyloid 
larvae  in  pastures.  I.  The  duration  of  infection  in  pasture 
herbage     Vet.  Rec.  v.  .50(40):   1265-1272. 

1939. — The  role  of  pastures  in  the  development  of  the 
strongyloid  diseases  of  grazing  animals.  Ibid.,  v.  51(1S): 
495-504. 


308 


CHAPTER  VIII 
EPIDEMIOLOGY  AND  SANITARY  MEASURES  FOR  THE  CONTROL  OF  NEMIC  PARASITES  OF  MAN 

WILLIAM  W.  CORT,  Department  of  H.lminthology,  School 
of  Hygiene  and  Public  Health,  the  Johns  Hopkins  Univer- 
sity, Baltimore,  Md. 

ELOISE  B.  CRAM,  Division  of  Zoology.  National  Institute  of 
Health,  U.  S.  Public  Health  Service,  Washington,  D.  C. 

DONALD  L.  AUGUSTINE,  Department  of  Comparative 
Pathology  and  Tropical  Medicine,  School  of  Medicine  and 
Public  Health,  Harvard  University,  Boston,  Mass. 


General  Discussion 
W.  W .  C. 

.Xt'tor  the  disfdvi'ry  of  :i  liuiiuiii  piujisito  the  next  st("]>  in  flic 
si'<|»oiUH'  loading  to  ofFective  control  must  he  the  detcrniiiuitioii 
of  its  life  cvclc  and  method  of  luinian  infection.  Such  iiifor 
mation  suggests  the  liroad  lines  along  which  control  measures 
can  be  developed,  but  needs  to  be  sii|i|ilcmented  by  eiiidemi 
olugic  studies  to  gain  information  on  tlic  vjirious  factors  in- 
volved in  dissemination  in  population  groups.  These  factoi's 
differ  greatly  for  the  different  nemic  jiarasites  of  man,  which 
vary  in  their  host   relations  and  life  cycles. 

In  those  species  in  which  eggs  or  larval  stages  have  a  free 
life,  vis.,  the  hookworms,  asearis,  trichuris,  enterobius,  etc., 
knowledge  is  essential  on  the  effect  of  general  environmental 
factors,  such  as  temperature,  moisture,  and  physical  and  chemi 
cal  conditions  of  the  soil;  for  only  when  the  environment  out- 
side the  host  is  favorable  can  these  free  stages  persist  and  in- 
fect nuiu.  The  relations  of  these  factors  depend  on  the  anu)unt 
of  development  <mtside  the  host  necessary  before  the  infective 
stage  is  reached  and  vary  greatly  between  snch  species  as  en- 
terobius and  the  hookworms.  In  those  si)ecies  with  interme- 
diate hosts  the  relations  outside  the  definitive  host  are  still 
more  complicated,  since  they  involve  all  the  factors  related  to 
the  infection  of  the  intermediate  host  and  the  transmission  by 
it  of  the  parasite.  Thus  all  the  relations  of  Trichi/irlla  spiralis 
to  the  rat  and  pig  become  of  vital  significance  in  its  tranmis- 
sion ;  with  the  guinea  worm,  Dractinculus  medinensis,  the  Cy- 
clops is  brought  into  the  picture:  and  in  the  filariae  the  rela- 
tions of  mosquitoes  and  certain  other  blood  sucking  flies  must 
be  considered. 

Equally  significant  in  epidemiologic  studies  of  nemic  para- 
sites is  the  consideration  of  human  habits  in  relation  to  trans- 
mission. For  those  species  in  which  the  eggs  pass  out  with  the 
feces,  habits  of  excreta  disposal  are  of  great  significance. 
Kqnally  important  also  are  all  the  human  habits  that  make 
jiossible  the  entrance  of  the  free  stages  into  the  human  body. 
With  those  nematodes  which  have  intermediate  hosts  the  human 
habits  that  are  related  to  spread  are  entirely  different  and  vary 
greatly  with  the  species.  In  the  filariae,  habits  that  bring  about 
exposuie  to  the  bites  of  the  insect  vector  are  important  both 
in  relation  to  the  infection  of  the  insect  and  in  the  transmission 
of  the  parasite  l)ack  to  man.  In  certain  cases  the  human  rela 
tions  may  be  very  peculiar.  As  for  example  with  TricliiiitlUi 
.spiralis  where  the  methods  of  feeding  pigs  and  habits  in  rela- 
tion to  pork  eating  have  to  be  considered;  or  with  the  guinea 
wonn  where  transmission  depends  on  the  drinking  of  water 
containing  cyclops,  in  which  infected  individuals  have  waded 
or  washed   their  feet. 

.\nother  phase  that  cannot  be  neglected  is  the  host  parasite 
relations.  For  example,  the  development  of  a  specific  immunity 
or  the  presence  of  an  age  resistance  may  be  important  in  de- 
termining the  distribution  of  the  parasite  in  the  population  ; 
or  undernourished  individuals  may  be  more  snsceiitible  than 
are  those  on  a  good  diet.  We  know  least  about  these  factors 
and  in  the  present  state  of  our  knowledge  their  relation  to 
epidemiology  is  difficult  to  evaluate. 

It  is  evident  that  the  more  extensive  is  the  understanding  of 
the  epidemiology  of  a  parasite,  the  more  effective  the  control 
program  can  be  made;  thus,  weak  links  in  the  cycle  of  trans- 
mission can  be  more  effectively  discovered  and  mistakes  avoided. 
Most  effective  in  control  are  ,'ittempts  to  ch.ange  human  habits 
that  make  possible  transmission.  In  fecal  borne  infections  the 
improvement  of  sanitation  to  prevent  soil  pollution  is  most 
important.  Where  transmission  is  by  insect  vectors,  control 
measures  are  chiefly  concerned  with  the  jirotection  of  tlie  peo 
[lie  from  their  bites  and  with  their  eradication  from  areas  near 
liuman  habitations.  Where  treatment  is  eflFective  and  easily  ap- 
plied to  large  groups,  mass  treatment  may  be  an  efficient  con- 
trol measure  in  breaking  the  cycle  at  the  stage  passed  in  the 
human   body. 


In  the  following  discussion  only  the  most  important  and  best 
kiu)wn  of  the  nemic  iiarasites  of  man  will  be  considered,  viz., 
the  hookworms,  .liiciirlosloma  iliioilinalr  and  Ncrator  amrri- 
callus:  the  large  round  worm,  Asearis  liimbricoitlis ;  the  whi|) 
worm,  Trichuris  trichiiira:  the  pin  worm,  Eiitrrohiiis  rcrnii- 
ciilaris;  the  flesh  worm,  'I'ricliiiii lla  siiiralis;  the  guinea  worm, 
DraciDiciilus  iiiiiliiiciisis ;  and  the  most  impoitant  of  the  filariae, 
ll'iiclicrcria  baiicrofti.  Onchocerca  volvulus,  and  Microfilaria 
nialaiii.  For  most  other  human  nematodes  there  is  little  in- 
formation on  epidemiology  or  control  methods,  and  they  are 
for  the  most  part  of  minor  significance  as  human  parasites. 
.\lso,  the  knowledge  iiresented  on  the  more  important  forms 
gives  a  backgiound  for  understanding  similar  relations  for  the 
other  sjiecies. 

The  Hookworms 
W.  W.  C. 

In  ancient  Egyptian,  .\rabian,  and  Greek  writings  are  founl 
descriptions  that  may  possibly  have  referred  to  hookworm  dis- 
ease. .-Vlso,  accounts  in  medical  treatises  of  the  17th  and  ISth 
centuries  from  Brazil,  Guadeloupe,  and  Jamaica  almost  cer- 
tainly referred  to  this  disease.  Modern  knowledge  dates  from 
the  description  of  Ancylostoma  diiodrnalr  by  Dubini  (1S43). 
In  1S7S  Grassi  and  the  brothers  Parona  demonstrated  that 
hookworm  infection  could  be  diagnosed  by  fecal  examinations. 
Leichtenstern  in  1887  demonstrated  experimentally  that  infec- 
tion could  be  brought  about  by  the  ingestion  of  larvae.  Looss 
(1898)  first  discovered  infection  by  skin  penetration  with  mi- 
gration through  the  lungs  and  over  a  period  of  years  carried 
out  extensive  investigations  on  hookworm  biology  which  cul- 
minated  in   his  Iftll  monograph. 

By  tlic  beginning  of  the  lIlUli  century  the  scene  had  shifted 
to  the  Western  Hemisphere,  where  Lntz  in  Brazil,  .\shford  in 
Puerto  Rico,  and  .Stiles  in  the  Ignited  States  had  demonstrated 
the  importance  of  hookworm  disease.  Of  especial  significance 
was  the  discovery  by  Stiles  (1902)  of  the  second  species  of 
human  hookworms,  \rcator  americaniis.  Very  important  also 
was  the  work  of  the  Puerto  Rico  .\nemia  Commission  from 
1904  to  1908  (Ashford  and  Gutierrez,  1911)  which  carried  out 
the  first  extensive  investigation  and  control  program  in  a  trojii 
cal  country.  Later  (1909  to  1914)  came  the  campaign  of  the 
Rockefeller  Sanitary  Commission  in  the  southern  United  States, 
which  was  followed  in  1914  by  the  establishment  of  the  In- 
ternational Health  Board  of  the  Rockefeller  Foundation,  which 
in  the  next  few  years  extended  hookworm  control  campaigns 
widely   into   other   parts  of   the   world. 

The  true  human  liookworms,  Aiici/lostoma  ihiodcnalr  and  Xic 
ator  americaniis,  are  widely  distributed  between  the  3t5th  paral 
U'l  north  latitude  and  the  30th  parallel  south.  Within  this  belt 
there  are  extensive  regions  where  the  combination  of  favorable 
temperatures  and  rainfall  make  possible  the  development  of 
widespread  heavy  infections  and  clinical  disease  in  populations 
living  close  to  the  soil  under  iiriniitive  conditituis  of  sanitation. 
Such  populations  are  still  found  in  very  limited  areas  in  the 
sonthein  t'nited  States  and  more  extensively  in  the  West  In 
dies.  Central  America,  northern  South  .\merica.  Tropical  -Af- 
rica, and  in  certain  parts  of  southern  Asia  and  the  East  In- 
dies.* While  A.  (liioilenale  and  N.  americaniis  are  present  to- 
gether in  a  considerable  part  of  the  hookworm  belt  they  show 
important  differences  in  geographical  distribution  and  appear 
to  have  origiimted  in  different  parts  of  the  world  (Darling, 
1920). 

A.  diiodcnale  and  N.  americaniis  differ  greatly  in  the  mor- 
phology of  the  adults.  The  former  is  larger,  appears  to  be  more 
injurious  to  its  host  and  is  harder  to  eliminate  with  anthelmin- 
tics (Darling,  Barber,  and  Hacker,  1920).  The  female  of  A. 
duodcnalc   produces   about   22,000   eggs   every   24   hours   while 


*For   a  detailed   discussion   of   the  geographical    distribution   of   hook- 
worm disease  see  Chandler,  1929.  pp.  18-54. 


309 


that  of  N.  americanus  only  about  8,000  to  10,000  (Super,  1927) 
Also  the  infective  larrae  of  the  first  species  are  slightly  larger, 
of  different  structure,  and  more  resistant  to  environmental  con- 
ditions than  those  of  the  second  (Svensson,  1925).  In  experi- 
mentally infected  human  volunteers,  the  adults  of  A.  duodenale 
lived  almost  7  years  and  those  of  X.  americanus  over  5  years 
(Kendrick,  1934).  In  these  infections,  however,  the  egg  counts 
in  the  individuals  infected  with  the  first  species  fell  to  a  very 
low  level  in  less  than  2  years,  and  in  those  harboring  the  sec- 
ond species  they  were  greatly  reduced  in  about  a  year.  In  spite 
of  all  these  differences,  both  species  are  very  similar  in  their 
host  relations  and  life  cycles;  and  the  symptomatology,  epi- 
demiology, treatment,  and  control  of  the  diseases  they  produce 
are  alike  in  all  essential  particulars. 

Although  in  a  few  cases  the  human  hookworms  have  been  re- 
ported incidentally  in  other  hosts,  and  A.  americanus  appears 
to  be  a  normal  parasite  of  anthropoid  apes,  there  is  at  present 
no  good  evidence  that  such  animals  serve  as  true  reservoir  hosts. 

Besides  the  true  human  hookworms  there  are  several  others 
that  have  some  relation  to  man.  The  dog  and  cat  hookworms, 
.4.  caninum,  A.  braziliense,  and  Uucinaria  sienocephaia  have 
been  extensively  used  in  studying  host-parasite  relation  prob- 
lems. The  larvae  of  the  last  two  have  been  shown  to  produce 
linear  skin  lesions  in  man,  and  A.  braziliense  is  the  causative 
agent  of  creeping  eruption  which  is  especially  prevalent  in 
certain  parts  of  the  southern  United  States  (Fiilleborn,  1928; 
Kirliy  Smith,  Dove,  and  White,  1929).  N.  suiUus,  described 
by  Ackert  and  Payne  (1923)  and  by  some  workers  considered 
as  a  synonym  of  A.  americanus,  has  received  consideration  in 
relation  to'the  possibility  that  its  host,  the  domestic  pig,  may 
serve  as  a  reservoir  host  for  humau  hookworm  disease. 

FACTORS  AFFECTING  THE  FREE  STAGES  OF  THE 
HOOKWORM  LIFE  CYCLE 

Development  of  hookworm  larvae  can  be  completed  at  tem- 
peratures ranging  from  about  12°  to  37°  C,  with  the  optimum 
from  about  2.5°  to  30°  C.  (Stiles,  1921;  McCoy,  1930).  Below 
22°  C.  the  development  is  greatly  slowed  up;  and  at  tempera- 
tures approaching  37°  C,  although  development  is  very  rapid,  a 
considerable  proportion  of  the  larvae  either  fail  to  develop  or 
soon  die.  The  eggs  and  larvae  are  quickly  killed  by  tempera- 
tures above  40°  C.  and  have  little  resistance  to  temperatures 
close  to  freezing  (Looss,  1911;  Svensson,  192.")).  The  injurious 
effect  of  low  temperatures  on  hookworm  eggs  and  larvae  is  the 
determining  factor  in  limiting  the  distribution  of  hookworm 
disease  almost   entirely  to  tropical  and  subtropical   regions. 

All  the  free  stages  of  the  hookworm  life  cycle  are  quickly 
killed  by  desiccation.  Therefore,  in  regions  of  low  rainfall  in- 
fection is  absent  or  kept  at  a  low  level  (Chandler,  1926-1928; 
Sawyer,  1923;  Docherty,  1926).  On  the  other  hand,  while  the 
eggs  and  infective  larvae  will  live  for  a  considerable  period 
under  water,  they  will  not  develop  eitlier  under  water  or  in  cul- 
tures that  are  saturated  with  moisture.  Therefore,  in  areas 
where  the  soil  is  flooded  for  a  part  of  the  year  hookworm  in- 
fection may  be  kept  at  a  low  level  (Chandler,  1926;  Barnes  and 
O'Brien,  1924).  Hookworm  larvae  require  the  presence  of 
oxygen  for  development  (McCoy,  1930)  and  it  is  probably  its 
absence  that  prevents  their  development  in  a  saturated  medium. 
Also,  they  require  a  loose  porous  culture  medium  and  do  not 
develop  well  in  clay  soils  (Stoll,  1923b).  Soil  relations  are 
very  important  in  the  southern  United  States  where  infection 
is  almost  entirely  absent  in  areas  with  clay  soil  and  is  par- 
ticularly intense  in  those  with  a  loose  sandy  soil  (Augustine 
and  Smillie,  1926;   Rickard  and  Kerr,  1926). 

The  developing  larvae  can  apparently  feed  normally  only  on 
living  bacteria,  which  must  be  present  in  considerable  numbers 
for  development  (McCoy,  1929).  It  seems  probable  that  the 
growth  of  enough  bacteria  for  the  needs  of  the  larvae  depends 
chiefly  on  the  mixture  of  feces  with  the  soil  and  if  the  eggs 
become  separated  from  the  fecal  material  in  which  they  are 
passed  development  will  be  checked. 

Epidemiologic  studies  of  recent  years  have  given  illustrations 
of  the  types  of  field  conditions  that  are  suitable  or  unsuitable 
for  the  development  of  the  hookworm  larvae  in  the  soil.  Loose 
porous  humus,  sandy,  or  loam  soils  that  are  well  shaded  give 
the  best  development.  Places  of  intense  soil  infestations  under 
such  conditions  have  been  reported  in  fields  of  sugar  cane  in 
Trinidad  (Cort  and  Payne,  1922).  in  coffee  groves  in  the  hills 
of  Puerto  Rico  (Cort,  Riley,  and  Payne,  1923),  and  in  fields 
of  cultivated  mulberry  trees  in  the  Yangtse  Delta  region  of 
China  (Cort,  Grant,  and  Stoll,  1P26).  In  clay  soil  not  covered 
b.v  a  layer  of  humus  or  a  growth  of  grass  almost  no  larvae 
will  develop  even  where  the  rainfall  is  considerable  (Cort  and 
Payne,  1922).  Even  on  soils  of  loose  texture  in  regions  of 
abundant  rainfall,  development  of  soil  infestation  will  be  great- 
ly inhibited  if  there  is  no  shade,  since  exposure  of  the  soil  sur- 
face to  the  sun's  rays  produces  alternate  periods  of  wetting  and 


drying  which  quickly  destroy  a  large  proportion  of  the  larvae 
(Augustine,  1923c).  Unshaded  areas  covered  with  a  thick 
growth  of  grass  have  in  some  cases  been  reported  as  very  favor 
able  for  development  (Korke,  1925).  In  hookworm  infected 
population  groups,  therefore,  significant  sources  of  infection 
may  be  limited,  even  where  there  is  extensive  soil  pollution,  to 
the  Comparatively  few  places  where  the  eggs  are  deposited  on 
a  loose  soil  that  is  well  shaded. 

When  the  larvae  develop  in  the  soil  they  migrate  toward  the 
surface  and  are  found  frequently  singly  or  in  clumps  extending 
from  the  particles  (Augustine,  1922b;  1923b).  In  only  a  few 
cases  have  they  ever  been  reported  at  depths  below  the  super- 
ficial surface  layers  (Baermann,  1917b).  When  covered  with  a 
loose  soil  they  can  migrate  vertically  from  considerable  depths 
(12  to  36  inches),  while  in  a  water  soaked  or  stiff  clay  soil 
almost  no  upward  migration  occurs  (Payne,  1922  and  1923). 
Lateral  migration  is  very  restricted  and  they  will  not  spread  out 
from  the  place  of  development  unless  carried  by  water  or  ani- 
mals (Augustine,  1922a;  Chandler,  1925).  After  the  second 
molt  they  no  longer  feed  and  will  continue  to  live  only  as  long 
as  their  reserve  of  food  material  lasts.  Therefore,  the  more 
active  they  are  the  shorter  will  be  their  life.  Under  artificial 
conditions  in  water,  however,  infective  hookworm  larvae  have 
been  kept  alive  for  as  long  as  18  months  (Ackert,  1924).  In 
the  soil  in  the  tropics  their  life  may  be  limited  to  only  6  to  9 
weeks,  with  the  great  majority  dying  in  3  or  4  weeks  (Augus- 
tine, 1922c  and  lS23c).  Under  conditions  less  favorable  for 
activity  they  may  persist  in  the  soil  for  periods  up  to  4  to  6 
months  (Hirst,  1924;  Baermann,  1917b).  There  is  also  evi- 
dence that  the  larvae  of  A.  duodenale  live  somewhat  longer 
than  those  of  X.  americanus  (Svensson,  1925). 

A  consideration  of  the  activities  of  the  infective  hookworm 
larvae  in  the  soil  lead  to  certain  practical  considerations  iii 
relation  to  the  epidemiology  and  control  of  hookworm  disease. 
The  larvae  tend  to  remain  in  "nests''  where  the  stools  are 
deposited ;  so  only  limited  places  are  sources  of  infection. 
Further,  the  burying  of  feces  except  under  a  very  stiff  clay 
soil  is  dangerous  because  the  larvae  will  soon  reach  the  surface. 
There  is  no  evidence,  however,  that  they  will  migrate  out  of 
latrines  (Payne,  1922).  Finally,  where  soil  pollution  is 
stopped,  sources  of  infection  will  be  naturally  sterilized  in  a 
comparatively  short  time  b.v  the  death  of  the  larvae. 

HOST  RELATIONS  TO  HOOKWORil  INFECTION 

The  penetration  of  the  infective  hookworm  larvae  through 
the  skin  produces  lesions  which  are  commonly  known  as  ground 
itch.  Secondary  bacterial  infection  frequently  increases  the 
severity  of  this  condition.  Also,  the  type  of  reaction  suggests 
in  many  cases  an  allergic  condition  associated  with  the  pres- 
ence of  immunity.  Thus  Sarles  (1929)  noted  a  much  more 
severe  skin  reaction  to  hookworm  larvae  in  old  resistant  dogs 
than  in  susceptible  puppies. 

Lung  symptoms  produced  by  the  migrations  of  the  larvae 
have  frequently  been  noted.  They  are  only  occasionally  at  all 
severe  except  in  extremely  heavy  infections,  suggesting  that  the 
larvae  usually  enter  a  few  at  a  time. 

In  the  intestine,  the  hookworms  bite  deeply  into  the  mucosa 
and  appear  to  suck  blood  constantly  throughout  their  adult 
life  (Wells,  1931;  Nishi,  1933).  It  seems  evident  that  they 
feed  chiefly  on  elements  derived  from  the  blood  (Hsii,  1938). 
They  move"  from  place  to  place  and,  therefore,  when  numerous 
injure  the  intestinal  wall  over  considerable  areas.  Blood  con- 
tinues to  flow  from  the  lesions  even  after  they  have  moved 
away.  Disturbances  of  the  digestive  system  which  are  com- 
monly present  in  moderate  as  well  as  heavy  infections  have 
been  "explained  chiefly  in  relation  to  the  injury  of  the  intes- 
tinal mucosa  produced  by  the  worms. 

Anemia  is  the  most  prominent  symi)tom  of  hookworm  disease. 
Indeed,  most  of  the  long  train  of  symptoms  found  in  chronic 
hookworm  patients  can  be  related  to  the  presence  of  long 
standing  anemia.  The  etiology  of  hookworm  anemia  has  been 
the  subject  of  considerable  controversy.  A  review  of  the  liter- 
ature indicates  that  there  is  no  convincing  evidence  that  it  is 
caused  by  toxic  products  of  the  worms.  Recent  investigations 
have  emphasized  the  importance  of  blood  loss  in  the  production 
of  the  anemia.  In  experimentally  infected  dogs  the  blood  pic- 
ture follows  exactly  that  produced  by  artificially  induced  hem- 
orrhage (Foster  and  Landsberg,  1934;  Landsberg  and  Cross, 
1935;  Landsberg,  1937).  Apparently,  blood  loss  produced  by 
the  worms  is  only  one  factor  in  the  production  of  the  anemia 
in  hookworm  infected  populations.  Disturbances  produced  by 
dietary  deficiencies,  particularly  lack  of  iron,  have  been  em- 
phasized as  important  additional  factors  (Rhoads,  Castle,  Payne, 
and  Lawson,  1934  a  &  b;  Cruz,  1934).  More  recent  work, 
however,  stresses  general  dietary  deficiency  rather  than  lack  of 
iron  alone  (Otto  and  Landsberg,  1940;  Payne  and  Payne, 
1940).    Anemia   produced   by   other   diseases   especially   malaria 


310 


may  hIso  W  a  oonipliiatinK  faotnr.  It  .sivms  rvidriil  alsi>  that 
the  clironic  lilood  loss  imnjiu'cd  liy  the  wmins  aiiKlit  in  ccitaiii 
t'asos  be  ouo  of  tin-  t'ai'tors  that  would  (iiially  lead  to  the  dovol 
opiuont  of  oiif  of  the  • '  idiopalhio "  aiiomiaH.  In  addition,  it 
si'onis  oi'itaiii  that  aiicmlas  of  a  variety  of  ctioloKii'S  are  fre 
(luently  referred  to  hool<\vorm  infeetion  ia  eases  where  the  few 
worms  present  have  litth>  if  any  part  in  the  prodnetion  of  the 
anemie  eondition   lAndrews,   liMlU. 

Reeently  it  lias  lieen  shown  that  a  speeifio  imninnity  is  ae 
((Uired  hy  dogs  in  response  to  repeated  infections  with  .1.  <-<nii 
iiiim  in  wliieh  antil>odies  are  formeil  ehielly  in  response  to  [\[<- 
secretions  and  excretions  of  the  worms  (Kerr,  ISlHti;  Otto  and 
Kerr,  ISlH't;  Otto.  1!I40).  It  seems  practically  certain  that  a 
similar  immunity  develo|>s  in  man  in  response  to  hookworm 
infection.  In  fact,  several  workers  have  recently  expressed  the 
view  that  host  immunity  must  play  an  important  role  in  the 
regulation  of  human  hookworm  infection  ( KiiUeborn,  Dios,  and 
Zuccarini,  1!I2S:  FiiUcliorn.  \'.^-2'.^;  fort,  1!132;  Pessoa  and  Pas 
eale,  1937  a  &  h;  Cort  and  Otto,  \'.)iO) .  Such  a  postulation 
makes  it  easy  to  explain  the  relatively  moderate  infections  and 
slight  evidence  of  hookworm  disease  found  in  many  individuals 
and  groups  of  jieople  who  appear  to  live  under  conditions  giving 
constant  opportunity  for  the  invasion  of  the  larvae.  Severe 
cases,  especially  in  children,  might  perhaps  be  explained  in 
part  by  exposure  to  infections  so  extrenu'  that  the  develoimu'iit 
of  the  immunity  is  prevented.  Also,  it  seems  probable  that 
uadernourishment  or  other  debilitating  factors  prevent  the  de 
velopment  of  the  immune  reactions.  In  experimental  infections 
in  young  dogs  either  undernourishment  or  too  rapid  infection 
which  weakens  the  host  from  extreme  blood  loss  will  prevent 
the  immune  response  (Otto  and  Kerr,  1!)39);  and  the  immu 
nity  already  developed  in  highly  resistant  older  animals  is 
easily  broken  down  by  placing  them  on  a  deficient  diet  {  Foster 
and  Cort.  I!i3l2;  l!l3.'i).  If  the  same  relations  hold  in  human 
infection,  individuals  or  groups  that  are  badly  debilitated  liy 
undernourishment  or  other  factors  may  be  expected  to  acipiire 
heavy  norm  burdens  arui  will  also  be  less  able  to  compensate 
by  the  regeneration  of  new  blood  for  the  losses  caused  by  the 
norms.  It  seems  probable  also  that  malaria  and  other  diseases 
are  more  important  than  is  at  present  realized  in  weakening 
the  defense  mechanism  against  hookworm  infection.  In  fact, 
the  hypothesis  has  reeently  been  suggested  that  widespread 
chronic  hookworm  disease  of  the  type  found  specially  in  tropical 
countries  seldom  results  from  uncomplicated  hookworm  infec- 
tion, but  is  produced  by  hookworm  infection  plus  undernourish- 
nu'nt  or  other  debilitating  factors  that  weaken  the  host  defense 
(Cort  and  Otto,  l<t4ii:   Cort,  1940). 

HUMAN  HABITS  I.\   RELATION   TO   HOOKWORM 
DISSEMINATION 

Insanitary  methods  of  excreta  disposal  and  activities  bring 
ing  about  contact  with  infested  soil  are  the  most  important 
human  habits  in  hookworm  dissemination.  Careless  depositing 
of  stools  on  the  ground  (soil  pollution)  is  a  widespread  habit 
among  most  of  the  i)opuiation  of  the  world  especially  in  tropical 
and  subtropical  regions.  Recently,  epidemiologic  evidence  has 
emphasized  soil  pollution  in  the  general  vicinit.v  of  dwellings 
as  important  in  hookworm  infection.  Adults  and  older  chil 
dren  arc  apt  to  go  for  defecation  to  protected  places  not  far 
from  their  houses  and  often  the  most  important  contact  with 
infested  soil  appears  to  come  about  during  the  act  of  defeca- 
tion (Cort,  192.5;  Cort,  Stoll,  Sweet,  Riley,  and  Schapiro,  1929; 
Chandler,  1928).  Young  children  usually  defecate  in  the  door- 
yards  close  to  the  houses  or  even  under  or  in  the  houses  them- 
selves, where  the  soil  conditions  are  usually  not  suitable  for  the 
development    of   hookworm    larvae. 

It  is  usuall.v  difficult  to  determine  the  extent  to  which  field 
work  brings  the  laborer  into  contact  with  sources  of  infection. 
People  living  near  cultivated  areas  such  as  vegetable  gardens, 
banana  groves,  sugar  cane  fields,  or  coffee  groves,  may  by  their 
defecation  habits  produce  concentrated  places  of  soil  infestation 
that  will  infect  field  laV)orers.  Usually,  however,  stools  passed 
by  laborers  at  work  are  widely  scattered  and  would  be  only 
occasionally  sources  of  infeetion,  as  compared  with  the  con- 
stant exposure  in  the  defecation  areas  near  the  houses. 

Some  occupational  relations  especiall.v  important  in  hook- 
worm dissemination  have  been  noted.  Coffee  picking  in  the 
hills  of  Puerto  Rico  has  been  shown  to  be  responsible  for  ex- 
tremely heavy  infection  (Ashford  and  Gutierrez,  1911;  Cort, 
Riley,  and  Payne,  1923).  Here  groups  of  people  work  in  the 
groves  for  long  hours  and  spread  their  stools  widely  when  they 
pick  the  coffee  at  weekly  intervals  for  (!  or  7  weeks.  Toward  the 
end  of  the  picking  season  the  soil  of  these  groves  becomes  so 
impregnated  with  infective  larvae  that  extensive  infection  of 
the  workers  occurs.  In  places  in  the  Orient  where  human  excre 
ment  is  used  as  fertilizer,  the  practices  in  connection  with  the 
cultivation  of  particular  crops  determine  the  extent  of  hook- 


\Miini  dissemination.  In  regions  in  China  where  sericulture  is 
important  hookworm  infection  m:iy  be  widespread  because  the 
mi'thods  of  f<'rtili/,ing  the  mulberry  trees  nnike  po.ssible  the 
developnu'nt  of  intense  soil  infestation  ((^ort,  (irant,  and  Stoll, 
I!i2(>):  fr<nn  such  places  the  iieople  who  pick  the  mulberry 
le.ives  to  feed  the  silkworms  ln'come  intensely  infected.  Other 
"i-cnpational  relationships  that  |iroduce  sources  of  infection 
might  be  cited,  but  as  we  consider  the  cviileni'c  it  beconu's  nu)re 
.Hid  niori'  evident  th;it,  except  when'  lunnan  excrenu'nt  is  used  as 
feililizcr,  soil  iiollntion  in  tin'  vicinity  of  the  <lwellings  is  by 
I'ai    the  must   irnporlant   f;ictcir  in  hookworm  di.sseminatiori. 

iiisrijii-.rTioN  or  hookwor.m  infection  within 

I'OITI.ATIONS 

The  use  of  the  Stoll  dilution  egg  counting  method  in  the 
extensive  epidemiologic  stinlies  of  hookworm  disease  of  the 
last  two  decades  has  given  a  large  anjount  of  information  from 
different  parts  of  the  world  on  the  distribution  of  hookworm 
infection  in  population  groups.  Estimates  of  worm  burdens  by 
this  niethod  have  made  it  possible  to  compare  (|uantitatively 
the  infection  according  to  age,  sex,  occupation,  race,  and  other 
categories,  as  well  ;is  to  comp.-ne  the  ilistribution  in  populations 
living  under  ilifti'rent  conditions.  Thus  d;it;i  can  be  obtained 
for  a  .scientific  planning  of  control  progr.-inis  ami  the  results 
of  the  campaigns  in  reducing  the  intensity  of  infection  can  be 
measured.  Attention  has,  therefore,  been  turned  from  the  per 
centages  of  positive  cases  ;ind  has  been  focused  on  the  number 
of  worms  harbored   (worm  burden). 

There  has  been  an  increasing  emiihasis  on  the  importance  of 
a  proper  evaluation  of  the  lightly  infected  cases,  especially 
those  that  might  be  considered  as  carriers  or  subclinical,  as 
compared  with  the  heavier  cases.  A  high  incidence  of  hook 
woiin  infection  nuiy  occur  in  groups  where  the  number  of 
worms  present  is  so  small  that  they  have  little  if  any  injurious 
c'ffect.  Such  situations  may  be  found,  as  in  certain  parts  of 
North  China  (Cort,  (irant,  and  Stoll,  192li)  and  Egypt  (Scott, 
1937)  where  human  habits  are  favorable  for  hookworm  disseni 
ination  but  climatic  conditions  are  unfavorable.  Similar  wide 
spread,  practically  sub-clinical  infections  are  also  jiresent 
where  sanitation  and  treatment  have  reduced  the  intensity  of 
infection  to  a  low  level,  but  where  widely  scattered  light 
sources  of  infection  still  exist.  It  is  not  possible  to  indicate 
definitely  the  actual  number  of  worms  necessary  to  produce 
clinical  symptoms  since  this  would  vary  in  relation  to  a  variety 
of  factors;  also  it  is  not  easy  to  accurately  evaluate  the  injury 
to  a  population  produced  by  widespread  light  infections.  It  caii 
be  .said,  however,  that  light  infections  are  of  but  little  conse- 
quence as  compared  with  heavy;  and  that  hookworm  disease 
becomes  a  real  i)ublic  health  problem  only  in  groups  with 
fairly   heavy   worm   burdens. 

The  individual  family  except  when  isolated  is  not  nearly  so 
much  the  unit  of  hookworm  infection  as  is  the  case  with 
ascaris.  This  appears  to  be  due  to  the  fact  that  sources  of 
infection  are  fairly  widesjiread  and  because  defecation  places 
near  dwellings  are  commonly  shared  by  more  than  one  family. 
Frequently  almost  all  the  individuals  in  even  large  populations 
are   infected. 

The  relative  intensity  of  infection  in  the  sexes  and  in  differ- 
ent age  groups  varies  greatly  in  different  iiopulations.  Usually, 
however,  infection  is  almost  completely  absent  in  children  under 
3  years  of  age,  gradually  increases  up  to  10  years  and  reaches 
the  adult  level  somewhere  in  the  early  teens  or  even  later 
(Smillie,  1922;  Payne,  Cort,  and  Rile.v",  1923).  It  may  vary 
considerably  in  the  different  age  groups  of  middle  life  and 
most  often  has  a  tendency  to  decline  in  older  people.  Females 
usually  have  a  distinctly  lower  level  of  infection  intensity  than 
males  (Carr,  1926;  Hill,  1927a;  Cort,  Stoll,  Sweet,  Riley,  and 
Schapiro,  192S).  It  has  been  suggested  that  this  type  of  age 
and  sex  distribution  is  most  t.vpical  of  situations  where  in- 
fection comes  from  soil  infestation  in  the  general  vicinity  of 
the  houses.  It  can  be  suggested  that  in  most  situations  the 
children  only  have  considerable  exposure  to  infection  when  they 
begin  to  visit  adult  defecation  places.  Greater  activity  of  boys 
than  of  girls  brings  greater  contact  with  infection;  and  adult 
males  usually  have  more  contact  with  sources  of  infection 
away  from  home  than  do  females.  Unusually  heavy  infection 
in  very  young  children  has  been  noted  in  certain  groups  in 
Panama  (Cort,  Stoll,  Sweet,  Riley,  and  Schapiro,  1929),  in  the 
Argentine  (Fiilleborn,  Dios,  and  Zuccarini,  192S),  in  Puerto 
Rico  (Hill,  1927a),  and  in  southeastern  (ieorgia  (Andrews, 
1940).  This  seems  to  occur  only  where  soil  conditions  in  the 
dooryards  are  favorable  for  the  development  of  hookworm 
larvae.  Heavier  infections  in  women  than  in  men  have  been 
found  in  a  few  places  like  the  areas  of  coffee  cultivation  in 
Puerto  Rico  (Cort,  Riley,  and  Payne,  1923)  and  in  certain 
groups  engaged  in  sericulture  in  China  (Cort,  Grant,  and  Stoll, 
192())    where  the  women  are  eng;iged  to  a  greater  extent   than 


311 


the  men  in  oeeupatioiis  that  bring  thcni  into  contact  with  nn- 
usually  intense  sources  of  infectiou.  In  parts  of  the  southern 
United  States  the  level  of  infection  rises  rapidly  from  6  to  l.i 
vears  and  then  declines  rapidly  until  after  20  years  the  «-orni 
burden  is  almost  negligible  (Smillie  and  Augustine,  1<J2... 
Chart  4)  Such  a  situation  cau  probably  be  attributed  to  the 
wearing  of  shoes  and  the  greater  use  of  sanitary  facilities  by 

the  adults.  ,      ,  .   j.     ■■  i 

Evidence  on  racial  differences  m  hookworm  mteetion  and 
disease  is  rather  conflicting.  It  does,  however,  seem  clear  that 
negroes  in  the  southern  United  States  have  much  lighter  mtec- 
tious  than  whites  (Knowlton,  Um-.  Smillie  and  Augustine, 
19-1.)  •  Keller,  Leathers,  and  Densen,  1940).  It  seems  possible 
that  this  difference  is  due  to  a  true  racial  immunity  m  the 
negro  race,  although  further  investigations  are  needed  b 'tore 
differences  in  environment  and  nutrition  can  be  completely 
ruled  out.  There  is  also  evidence  that  suggests  that  groups 
with  negro  and  negro-indian  blood  are  more  resistant  to  the  iii- 
iurious  effects  of  the  worms  than  those  of  the  white  race 
(Gordon  192.-> ;  Cort,  Stoll,  Sweet,  Riley,  and  Schapiro,  1919). 
However',  it  is  difficult  to  rule  out  other  factors  and  here  also 
the   whole  question   needs  much  further  investigation. 

CONTROL  OF  HOOKWORM  DISEASE 

Four  different  methods  of  preventing  the  spread  of  hook- 
worm infection  have  been  generally  recognized,  viz.,  (1)  disin- 
fection of  feces  or  infested  soil,  (2)  the  encouraging  of  wear- 
ing shoes,  (3)  anthelmintic  treatment,  and  (4)  improvement 
in  sanitation.  Extensive  experimentation  has  shown  that  hook- 
worm eggs  in  feces  and  the  larvae  in  the  soil  can  be  killed 
bv  the  application  of  salt,  lime,  or  other  chemicals.  Such 
methods  are  useful  in  limited  areas  such  as  mines  (Fisc-lier, 
19'>8)  or  in  sterilizing  human  excrement  which  is  to  be  used  as 
fCTtili'zer  (Cort,  Grant,  and  Stoll,  19l2(i).  The  wearing  of  shoes 
has  been  shown  to  be  a  potent  factor  in  keeping  hookworm  in- 
fection at  a  low  level  (Smillie,  1922;  Davis,  192.'.;  Chandler, 
1929  pp.  208-211,  380-3S2).  However,  attempts  to  increase  the 
wearing  of  shoes  in  hookworm  infected  populations  by  propa- 
ganda or  legal  requirements  do  not  seem  to  have  been  very 
effective  Hookworm  control  campaigns,  therefore,  have  been 
organized  chieflv  around  treatment  and  sanitation.  The  use  of 
anthelmintics  improves  the  health  of  the  people  and  reduces 
soil  infestation.  The  sanitary  phase  of  the  program  is  a  fight 
against  soil  pollution  and  involves  education  and  the  introduc- 
tion of  latrines.  Much  work  has  been  done  in  developing  sani- 
tary conveniences  suitable  for  people  of  different  types.  The 
pit" latrine  (privy)  has  been  most  widely  used  in  the  Western 
Hemisphere:  and  the  recently  developed  bored-hole  latrine 
(Teager,  1931  and  1934)  seems  to  be  best  adapted  for  the 
jieoples  of  certain  countries  of  Asia  and  Africa. 

In  the  early  hookworm  campaigns  in  Puerto  Eico  and  the 
southern  United  States  the  so-called  "dispensary  method 
was  used  This  consisted  of  the  examination  and  treatment 
of  large  groups  of  people  who  flocked  to  the  numerous  dis- 
pensaries that  were  set  up.  Significant  results  were  attained 
in  the  treatment  of  severe  cases  and  in  preliminary  education, 
but  only  a  beginning  was  made  in  the  reduction  of  infection 
and  in  the  improvement   of   sanitation. 

\s  a  reaction  against  the  inadequacy  of  the  "dispensary 
meUiod  "  the  "intensive  method"  was  developed  by  certain 
members  of  the  field  staff  of  the  International  Health  Board  ot 
the  Rockefeller  Foundation.  Its  ob.ieetive  was  the  complete 
eradication  of  hookworm  infection  by  a  systematic  program  of 
sanitation  and  treatment  to  "cure"  of  all  infected  individuals 
(Howard  1919).  First,  every  effort  was  made  to  get  latrines 
installed  in  every  house  in  a  given  area.  Then,  after  systeinatic 
stool  examinations,  the  positives  were  given  treatment.  Ihey 
were  later  reexamined,  and  those  still  infected  were  given  a 
second  treatment.  Reexamination  and  retreatment  were  sup- 
posed to  be  continued  until  the  stool  samples  of  all  the  people 
of  the  area  were  negative  for  hookworm  eggs.  Sometimes  as 
many  as  9  or  10  treatments  were  required  for  "cure."  Efforts 
to  improve  the  sanitation  were  continued  during  and  after  the 
treatments.  Although  hookworm  infection  was  never  completely 
eradicated  from  any  area  by  this  method,  striking  results  were 
obtained  in  a  number  of  places.  Least  defensible  of  the  pro- 
cedures of  the  intensive  method  was  "treatment  to  cure"  in 
which  much  effort  and  money  were  wrstcd  in  treating  very 
light  infections  and  in  trying  to  remove  tlie  last  few  worms  by 
retrcatments.  On  the  other  hand,  the  emphasis  on  intensive 
sanitation  especially  before  treatment  and  on  a  careful  follow- 
ing up  of  the  sanitation  after  treatment,  was  an  important 
contribution    to   hookworm    control    procedures. 

The  "mass  treatment"  method  came  as  a  reaction  against 
the  complete  ineffectiveness  of  the  intensive  method  to  cope 
with  the  situation  in  a  large  country  such  as  Brazil.  As  advo- 
cated by  Darling   (1922)   mass  treatment   required  first  the  de 


termination  of  the  index  of  infection  (approximate  womi  inir- 
deu)  by  the  examination  by  worm  counts  of  a  representative 
sample  of  the  population.  Later,  the  development  of  the  Stoll 
dilution  egg  counting  method  (Stoll,  1923a)  made  it  possible 
with  much  less  effort  to  obtain  a  better  estimate  of  infection 
intensity.  Then,  wherever  incidence  was  high,  a  whole  group 
was  simultaneously  given  anthelmintic  treatment  of  known 
efficacy  without  a  previous  diagnostic  examination  and  without 
reexamination.  Thus  large  groups  of  people  could  be  rapidly 
treated.  An  adequate  sanitary  program  was  sometimes  com- 
liined  with  mass  treatment.  In  many  jilaces,  however,  the  great 
emphasis  on  treatment  and  the  rapidity  with  which  the  cam- 
paign moved  brought  about  a  neglect  of  sanitation.  Whenever 
this  was  true  reinfection  occurred  at  a  rather  rapid  rate  as 
suggested  bv  the  investigations  of  a  number  of  workers  (Baer- 
niaiin,  1917b;  Sweet,  192.3;  Docherty,  1926;  Hill,  192.J,  1926, 
1927b).  Mass  treatments,  therefore,  were  particularly  effective 
if  repeated  at  intervals  of  2  or  3  years  (Rice,  1927;  Lambert, 
1928).  Perhaps  of  greatest  importance  was  the  emphasis  on 
the  quantitative  viewpoint ;  the  object  of  the  campaign  was  to 
reduce  the  worm  burden  of  the  population  and  not  to  cure 
cases.  Also  important  was  the  idea  that  a  preliminary  survey 
was  needed  to  estimate  the  ' '  index  of  infection  ' '  before  control 
wink   was  started. 

A  campaign  against  hookworm  disease  at  the  present  time- 
can  be  planned  on  the  basis  of  the  wealth  of  experience  of  the 
last  2.')  years.  Such  a  campaign  under  ideal  conditions  might 
include  five  steps  which  have  actually  been  utilized  in  cam- 
paigns; and  to  these  a  sixth  might  be  added.  (1)  a  presurvey 
to  evaluate  the  problem  quantitatively;  (2)  presanitation  to- 
reduce  soil  pollution  as  much  as  possilile  before  treatment;  (3) 
mass  treatment  to  reduce  the  worm  burden  of  the  group  to  a 
.subclinical  level  in  as  short  a  time  as  possible;  (4)  follow-up 
sanitation  to  keep  soil  pollution  at  a  low  level;  and  (5)  a  post- 
survey  to  measure  quantitatively  the  results  of  the  campaign. 
Finally  (6),  every  effort  possible  should  be  made  to  improve 
the  general  health  by  the  correction  of  dietary  deficiences  and 
the  elimination  of  other  diseases. 

The  central  feature  of  the  presurvey  should  be  an  examina- 
tion by  the  dilution  egg-counting  method  of  a  representative 
sample  of  the  population  to  obtain  information  on  the  quanti- 
tative distribution  of  hookworm  infection  in  the  population 
and  on  the  extent  of  true  hookworm  disease.  Investigations  of 
the  amount  of  sanitation  present  and  of  soil  pollution  habits 
wiU  aid  in  planning  the  program  for  sanitar.v  improvement 
which  in  most  situations  is  by  far  the  most  important  part  of 
the  campaign.  In  regions  where  hookworm  infection  is  found 
to  be  chiefly  at  or  near  the  subclinical  level,  even  if  its  inci- 
dence is  high,  control  work  may  well  be  limited  entirely  to 
sanitation.  When  the  preliminary  survey  shows  heavy  infec- 
tion and  \videspread  disease  every  effort  should  be  made  to  re- 
duce soil  pollution  to  the  greatest  possible  extent  before  treat- 
ment is  started  by  the  introduction  of  latrines  and  education 
in  their  use.  This  is  done  in  order  to  reduce  the  amount  of 
reinfection  after  treatment. 

A  course  of  treatments  should  be  chosen  which  has  been 
shown  by  quantitative  study  on  a  group  of  considerable  size  to 
reduce  the  worm  burden  by  at  least  90  percent.  If  the  inci- 
dence of  infection  shown  by  the  preliminary  survey  is  over  90 
percent,  treatment  without  diagnostic  examination  according 
to  the  mass  treatment  method  may  seem  desirable.  Such  a  pro- 
cedure, however,  should  not  be  applied  to  the  youngest  age 
group  where  infection  is  almost  always  least  and  danger  f  rom  ■ 
treatment  greatest.  Mass  treatment  should  be  given  by  popu- 
lation units  so  that  all  the  people  living  in  the  same  environ- 
ment would  be  freed  of  their  worms  as  nearly  at  the  same  time 
as  possible.  Individual  examinations  after  treatment  and  re- 
treatments  cannot  be  justified  where  the  object  is  to  reduce  the 
worm  burden  as  much  as  possible  with  a  given  amount  of  treat- 
ment. In  tropical  regions  treatments  toward  the  end  of  the 
dry  season,  when  the  soil  has  been  unsuitable  for  a  considerable 
period  for  the  development  of  the  larvae,  will  have  more  last- 
ing value  than  those  given  during  the  rainy  season,  when  rein- 
fection is  very  extensive  (Chandler,  1929,  pp.  40.5-408;  Me  Vail, 
1922)  ;  and  in  colder  regions  treatments  at  the  end  of  the  win- 
ter will  be  most  eft'ective. 

Even  in  the  best  organized  campaigns  a  varying  percentage 
of  the  worm  burden  will  he  left  after  treatment.  Whether  in- 
fection will  soon  return  to  a  high  level  again  depends  on  the 
extent  to  which  the  people  are  prevented  from  returning  to 
their  former  habits  of  soil  pollution.  Real  success  in  hook- 
worm control,  therefore,  will  be  achieved  only  where  efforts  to 
improve  sanitation  have  been  permanently  organized  and  effec- 
tively continued  over  long  periods  of  time  as  part  of  the  per- 
manent public  health  program. 

The  final  step  in  an  ideal  program  for  hookworm  control 
would  be  a   resurvey  carried  out   about   2  or  3  years  after  the 


312 


■cdiiililetion  of  the  tieatiiioiits  by  the  same  methods  used  in  tlu' 
preliminary  survey.  Such  an  investigation  will  make  it  [los 
silile  to  elieek  the  sanitation  and  to  determine  whether  the 
level  of  infection  has  retnri\ed  to  a  jioiat  where  further  treat- 
ment is  needed. 

Most  important  iii  .-ittaikint;  the  hookworm  problem  is  the 
acceptance  of  the  quantitative  point  of  view  and  the  nsiiij;  of 
(juantitative  methods  to  determine  the  "hookworm  index''  in 
the  preliminary  survey  and  the  resiirvey.  Much  effort  and 
money  have  been  wasted  in  trying  by  active  treatment  cam 
liaigns  to  reduce  hookworm  infection  in  poi)ulations  whi're  it 
ivas  already  close  to  the  subclinical  level.  Most  fundamental 
perhaps  of  all  is  the  changed  objective  of  the  modern  hook 
worm  campaign,  which  is  to  reduce  hookworm  infection  to  a 
subclinical  level  by  treatment  and  to  keep  it  tlu're  by  per 
mauent   improvement  in   sanitation. 

Finally,  certain  new  viewpoints  need  to  be  developed  on  ac- 
count of  the  recent  ticw  information  on  the  significance  of  ac 
quired  immunity  in  hookworm  infection  and  its  relation  to  un- 
dernourishment and  other  debilitating  factors.  If  the  immune 
respons'-  in  man  to  his  hookworms  proves  to  be  of  the  same 
grade  as  tliat  of  the  dog  to  .1.  en )i i ii ii iii ,  measures  to  remove 
factors  that  interfere  with  the  normal  host  responses  are  just 
as  important  in  hookworm  control  as  those  directed  against 
the  spread  of  infection.  In  fact,  it  seems  altogether  likely  that 
if  it  were  possible  to  eliniin:ite  dietary  deficiencies  from  a 
population  suffering  from  hookworm  disease  by  furni.shing  an 
adequate  food  suppl.v,  the  restoration  of  the  normal  host  resis 
tancc  would  in  itself  strikingly  reduce  hookworm  infection  and 
disease  (Otto  and  I,andsl)erg,  n)40 ;  Cort  and  Otto,  1940). 
Emphasis  in  hookworm  control,  therefore,  should  be  placed  not 
on  isolated  spectacular  treatment  campaigns,  but  on  the  at- 
tempt to  reduce  hookworm  infection  by  all  the  methods  that 
will  improve  the  sanitation  and  raise  the  general  economic  and 
health  level  of  the   infected  populations. 

Ascaris  lumbricoides 

W.  W.  C. 

References  to  human  ascaris  are  found  in  the  ancient  medi- 
cal literature  of  the  Chinese,  Egyptians,  and  Greeks.  Edward 
Tyson  in  1683  and  Francesco  Redi  in  l()8-t  studied  the  anatomy 
of  this  parasite,  distinguished  the  sexes,  and  expressed  the  view- 
that  it  reproduced  by  eggs  and  not  by  spontaneous  generation. 
From  that  time  on,  ^l.s'ror/.<  liimbricnirles  became  a  favorite  ob- 
ject for  study,  and  investigations  on  its  anatomy  laid  the  foun- 
dation of  our  present  knowledge  of  nematode  structure.  Al- 
though much  information  on  the  prevalence,  pathology,  and 
geographical  distribution  of  ascaris  in  man  has  been  long  avail- 
able, it  is  only  recently  that  much  attention  has  been  paid  to 
the  epidemiology  of  ascariasis  in  relation  to  control. 

PATHOLOGY  AND  SYMPTOMATOLOGY 
In  laboratory  animals  and  in  pigs  the  migrations  of  ascaris 
larvae  are  known  to  produce  lesions  in  the  intestinal  wall, 
liver,  Ivmph  nodes,  and  especially  in  the  lungs  (Ransom  and 
Foster,"  1920 ;  Yokogawa,  102,S  ;  Martin,  1926;  Roberts,  1S34). 
The  lesions  in  the  lungs  consist  of  petechial  hemorrhages  and 
inflammatory  processes.  In  heavy  infections  the  lungs  may  be 
very  extensively  involved,  being  edematous,  hemorrhagic,  and 
even  completely  consolidated.  The  picture  is  that  of  a  multiple 
lobar  pneumonia,  which  frequently  causes  the  death  of  experi- 
mental animals.  A  disease  of  young  pigs  known  as  "thumps" 
has  been  identified  as  ascaris  pneumonia  (Ransom,  1920).  In 
man  severe  pulmonary  symptoms  may  l)e  produced  by  hea^'y 
infections  (Koino,  1922)  and  in  some  tropical  regions  lung  sym- 
toms,  especially  in  children,  have  been  attributed  to  ascaris  in- 
fection. In  most  infected  populations,  however,  it  is  extremely 
difficult  to  assign  a  definite  symptomatology  to  the  lung  mi- 
grations of  ascaris   (Keller,  Hillstrom,  and  Gass,  1932). 

It  is  not  easy  to  define  clearly  the  symptoms  produced  by 
the  worms  in  the  intestine.  Perhaps  the  most  common  com- 
plaint is  an  intermittent  intestinal  colic.  Normal  digestion 
may  be  disturbed  and  there  may  be  loss  of  appetite  and  in- 
somnia. Nervous  sym))toms  are  particularly  common  among 
heavily  infected  young  children.  Individuals  having  a  special 
sensitivity  may  develop  a  generalized  toxemia  or  specific  ner- 
vous symptoms.  In  young  children  very  heavy  infections  may 
cause  severe  illness  or  even  death.  Large  numbers  of  ascarids 
may  produce  intestinal  blockage.  Also,  the  migrations  of  adult 
worms  sometimes  produce  penetration  of  the  intestinal  wall 
and  severe  injury  to  the  appendix,  liver,  lungs,  or  other  or- 
gans. However,  only  a  small  proportion  of  infected  individuals 
show  symptoms  that  can  be  definitely  attributed  to  ascariasis. 

DI.'!TRIBI'T10X   .^XD   EPIDEMIOLOGY 
Doling  tlie   last    1."   years   our   knowledge   of   the   factors   in- 
fluencing the  dissemination  of  ascaris  has  been  very  greatly  in- 


creased by  a  number  of  siiecific  epidemiologic  studies  in  differ 
ent  i)arts  of  the  world.  The  distribution  of  the  worm  burden 
has  been  studied  by  the  StoU  dilution  egg  counting  method, 
and  attempts  have  been  made  to  get  at  the  sources  of  infec- 
tion liy  the  observation  of  soil  pollution  habits  and  by  the  iso 
lation  of  eggs  from  the  soil  (Spindler,  1929a;  Majilestone  and 
Mukerji,  193(i).  Data  from  these  investigations  and  infornm 
tion  on  the  factors  influencing  tlie«development  and  viability 
of  ascaris  eggs  outside  the  body  of  the  host  have  given  a  fairly 
good  body  of  ei)idcmiological  knowledge  on  wliich  to  base  con- 
trol measures.  In  addition,  recent  studies  indicate  that  host 
relations  may  be  of  importance  in  determining  the  distribution 
of  ascaris  in  populations. 

DISTRIBUTION 

.1.  Iiimbricoidffi  in  man  has  a  world  wide  distribution  and 
appears  to  rival  Eiitcrohiiis  rcniiinilnri.':  for  the  distinction  of 
being  the  commonest  of  all  human  parasites.  It  has  been  found 
within  the  Arctic  Circle  and  in  regions  where  almost  desert 
conditions  i)revail.  It  is  most  abundant  in  tropical  countries 
with  a  heavy  rainfall  and  is  especially  widespread  in  the  Orient, 
although  extensive  endemic  centers  are  also  present  in  Europe 
and  in  the  United  States  (Otto  and  Cort,  1934a;  Denecke,  1937; 
Girges,  1S34). 

Recently  the  information  on  the  distribution  of  ascaris  within 
population  groups  has  been  greatly  increased.  The  family  is 
almost  always  the  unit  of  infection  (Cort,  Stoll,  Sweet,  Rih'v, 
and  Schapiro,  1929;  Cort,  Otto,  and  Spindler,  1939;  Otto,  Cort, 
and  Keller,  1931).  This  is  true  in  urban  as  well  as  rural  areas 
(Headlee,  1936;  Winfield  and  Chin,  1938).  Only  in  Egypt 
(Scott,  1939)  and  In  certain  special  institutional  situations 
(Caldwell,  Caldwell,  and  Davis,  1930)  was  a  larger  group  in- 
dicated as  the  unit.  In  numerous  situations  negative  or  lightly 
infected  families  are  found  living  close  to  those  that  are  heav- 
il.v  infected.  With  few  exceptions  (Scott,  1939)  about  •")n  per- 
cent of  the  total  worm  burden  of  any  population  group  is  con- 
centrated in  about  .5  percent  of  the  infected  individuals.  These 
heavy  cases  are  largel.v  found  in  a  small  number  of  families, 
the  so  called  "ascaris  families."  Usually  the  peak  of  the  in- 
fection curve  comes  early  in  life,  sometimes  even  in  the  o  to  9 
age  group,  and  the  worm  burden  in  adults  is  only  a  fraction 
of  that  in  children.  Also,  women  of  child-bearing  age  are  fre- 
quently more  heavily  infected  than  men  of  the  same  age  groups. 
However,  heavy  infections  are  sometimes  found  in  adults,  es- 
pecially in  certain  places  in  the  Orient   (Cort  and  Stoll,  1931). 

Ascaris  is  in  general  a  parasite  of  people  on  a  low  economic 
and  social  level.  "Ascaris  families"  are  usuall.v  among  the 
poorest  and  most  degraded  of  the  population.  Not  infrequently, 
however,  infections  in  children,  sometimes  rather  heavy,  are 
found  in  families  of  a  higher  type  living  under  favorable  en- 
vironmental conditions.  In  the  Orient,  also,  ascaris  is  often 
widespread  in  people  of  the  better  classes  (Mills,  1927).  It  is 
not  primarily  a  parasite  of  rural  districts  since  in  many  jjarts 
of  the  world  it  is  present  and  sometimes  very  common  in  cities 
of  various  sizes.  The  reasons  for  most  of  the  pecularities  in 
the  distribution  of  ascaris  which  have  just  been  summarized 
become  clear  when  the  knowledge  available  on  the  various  fac- 
tors that  influence  dissemination  is  considered.  These  factors 
may  be  grouped  under  (1)  host  relations,  (2)  general  environ- 
mental factors,  and  (3)  human  habits. 

HOST  RELATIONS 
In  this  connection  one  of  the  important  problems  is  the  re- 
lation of  the  ascaris  of  pig  to  human  infection.  Extensive 
investigations  have  shown  no  differences  between  the  ascarids 
of  these  two  hosts  in  morphology  or  in  physiological  and  bio- 
chemical relations  (Schwartz,  1920;  Bakker,  1921;  Barker, 
1923).  Almost  all  attempts  to  infect  pigs  with  eggs  from  hu- 
man sources  have  been  unsuccessful  fPayne,  .\ckert,  and  Hart- 
man,  192.");  Martin,  1926).  Also,  the  attempts  to  infect  man 
with  the  pig  ascaris  have  given  negative  results  (Koino,  1922; 
Payne,  Ackert,  and  Hartman,  292.'i;  Buckley,  1931).  Several 
workers  have  expressed  the  view  that  the  human  and  pig  as 
carids  are  physiological  or  host  varieties  which  have  each  lost 
their  infectivity  for  the  other  host.  As  Lane  (1934)  has  sug 
gested,  however,  the  evidence  from  these  experimental  infections 
is  not  very  conclusive  because  of  the  lack  of  adequate  controls 
and  because  of  the  difficulty  reported  by  a  number  of  workers 
of  infecting  pigs  with  the  pig  ascaris  (see  also  Roberts,  1934). 
Also,  de  Boer  (193."ia  &  b)  reported  that  he  succeeded  in  infect- 
ing suckling  pigs  with  eggs  from  both  pig  and  human  sources 
and  Hiraishi  (1928)  and  others  in  .Japan  have  infected  pigs 
deficient  in  vitamin  .\  with  human  ascaris.  It  is  difficult,  how- 
ever, to  escape  the  conclusion  that  under  field  conditions  in- 
fection of  man  with  pig  ascaris  is  at  least  very  infrequent.  In 
fact,  no  evidence  has  been  found  in  the  reports  of  epidemiologi- 
cal studies  of  undoubted  human  infection  from  pig  sources.  At- 
tention has  also  been  called  to  areas  in  which  differences  in  the 


313 


incidence  of  the  pig  and  human  asearis  are  very  great  under 
conditions  that  would  seem  to  favor  cross  infection  (Payne, 
Aekert,  and  Hartman,  1925;  Caldwell  and  Caldwell,  192(3;  Mar- 
tin, 1926;  Roberts,  1934).  Therefore,  until  some  evidence  can 
be  'presented  of  human  infection  with  asearis  from  the  pig,  it 
hardly  seems  reasonable  to  consider  the  domestic  pig  as  a 
reservoir  host  of  any  significance  in  the  dissemination  of  asearis 
in  human  populations. 

There  is  some  evidence  that  a  specific  immunity  is  acquired 
to  infection  with  A.  himbricoiiles.  Some  of  the  studies  showing 
this  have  been  made  on  abnormal  hosts  and,  therefore,  involve 
only  the  stages  of  the  cycle  through  the  lung  migration  (Kerr, 
1938).  Other  workers  have  reported  experiments  that  sug- 
gested the  development  of  immunity  in  pigs  (Morgan,  1931; 
de  Boer,  193(ib;  Roberts,  1934).  In  pigs  abo  infection  is  very 
much  greater  in  young  than  in  old  animals  (Ransom  and  Fos- 
ter, 1920;  Roberts,  1934).  Such  differences  might  be  explained 
as  the  result  of  an  immunity  produced  by  repeated  infection. 
There  is  some  suggestion  also  that  in  older  animals  poor  nutri- 
tion may  increase  susceptibility  (Morgan,  1931;  Hiraishi, 
1928).  Possibly  in  man  a  part  at  least  of  the  reduction  of  in- 
fection in  adults  as  compared  with  children  may  be  due  to  the 
development  of  an  acquired  immunity,  although  difference  in 
habits  cannot  be  excluded.  Also,  it  seems  not  unlikely  that 
undernourishment  or  other  debilitating  factors  may  influence 
susceptibilitv  to  this  parasite. 

There  is  some  suggestion  that  A.  Iiimbricoidcs  is  not  well 
adapted  to  its  host.  This  has  been  suggested  by  several  work- 
ers because  of  the  difficulty  of  producing  experimental  infec- 
tions in  pigs  (Ransom  and  Foster,  1920;  Martin,  1926;  Hirai- . 
shi,  192S;  Roberts,  1934).  A  similar  relationship  in  man  may 
explain  the  rarity  of  heavy  infections.  Another  significant 
host  relation  is  the  rapid  turnover  of  the  infection  and  the  con- 
stant loss  of  worms  in  infected  populations  (Otto,  1930).  In- 
dividuals frequently  pass  worms;  heavy  worm  burdens  are  only 
kept  up  by  constant  reinfection;  and  groups  removed  from  ex- 
posure to  "reinfection  soon  lose  their  worms  (Keller,  1931).  It  is 
not  clear  whether  this  instability  of  infection  is  due  to  lack 
of  attachment  of  the  worms  or  to  immunity  reactions  of  the 
host.  Finally,  it  seems  probable  that  host  reactions  have  a 
part  in  keeping  asearis  infections  in  human  populations  at  a 
low  level  except  under  extreme  conditions  of  exposure  to  infec- 
tion, and  in  establishing  the  peculiar  age  distribution  of  this 
parasite. 

GENERAL  ENVIRONMENTAL  F.\CTORS 

The  eggs  of  A.  lumbricoidrs  live  for  long  periods  of  time 
and  are  remarkably  resistant  to  most  external  conditions.  They 
have  been  kept  alive  for  4  to  't  years  (Davaine,  18.")8  and  1863; 
Martin,  1920)  and  under  natural  conditions  will  live  for  1  to 
2  years  and  survive  the  winter  (Brown.  1928;  Roberts,  1934). 
Under  field  conditions,  where  they  would  be  exposed  to  a  larger 
variety  of  factors,  it  seems  probable  that  they  remain  viable 
for  somewhat  shorter  periods,  although  it  is  evident  that  in- 
fested soil  renuiins  dangerous  for  a  very  much  longer  time 
than   is   the  case   with  hookworm. 

Asearis  eggs  have  been  shown  to  have  a  remarkable  resistance 
to  a  wide  variety  of  chemical  agents  (Yoshida,  1920;  Ransom 
and  Foster,  1920).  It  seems  evident,  therefore,  that  in  nature 
they  would  rarely  if  ever  meet  chemical  conditions  in  the  soil 
that  would  be  unfavoralile.  The  eggs  require  a  constant  supply 
of  oxygen  for  their  development,  they  can,  however,  live  for 
several  weeks  under  anaerobic  conditions  and  can  develop  in 
cultures  where  oxygen  tension  in  the  surrounding  water  is  only 
a  fraction  of  saturation  (Brown,  1928a).  It  seems  evident, 
therefore,  that  under  natural  conditions  they  can  readily  find 
oxygen  enough  for  development  except  in  polluted  water  or 
saturated    media    where    bacterial    growth    would    use    up    the 

supply. 

Asearis  eggs  in  all  stages  of  development  can  withstand  freez- 
ing temperatures  for  surprisingly  long  periods  of  time  (Cram, 
1924;  Nolf,  1932)  and  will  develop  slowly  at  temperatures  as 
low  a's  12°  C.  The  optimum  temperature  for  development  seems 
to  be  about  30°  to  33°  C.  and  development  is  almost  completely 
inhibited  at  temperatures  of  about  37°  C.  Higher  temperatures 
are  very  iniurious  to  the  eggs  and  at  temperatures  above  W°  C. 
they  are  killed  in  a  short  time  (Ogata,  192."i;  Nolf,  1932). 
Desiccation  is  also  an  important  factor  in  killing  asearis  eggs, 
although  they  will  remain  viable  for  several  days  when  dried  on 
glass  slides  and  kept  at  a  relative  humidity  of  about  ."JO  percent 
(Otto,  1929;  Roberts,  1934).  On  the  dry  surface  of  soil  they 
survive  much  longer  (Caldwell  and  Caldwell,  1928;  Brown. 
1928b).  Their  resistance  to  desiccation  is  also  greatly  increased 
by  low  temperatures  (Martin,  1920).  They  will  develop  nor- 
mally when  air  dried  on  glass  slides  and  kept  in  an  incubator 
with"  a  relative  humidity  above  80  percent  (Otto,  1929).  A 
number  of  authors  have  reported  that  direct  sunlight  is  lethal 
to  asearis  eggs,  although  in  many  of  the  experiments  the  effect 


of  high  temperature  vias  not  excluded.  There  is,  however,  defi- 
nite evidence  that  sunlight  per  sc  docs  in.iure  the  eggs  since 
Nolf  (1932)  demonstrated  that  they  were  quickly  killed  by  ultra 
violet  light.  Under  conditions  in  the  field,  a  combination  of 
high  temperatures  with  desiccation  is  probably  most  important 
in  killing  the  eggs  as  is  shown  by  the  rapidity  with  which  they 
die  when  exposed  to  direct  sunlight  on  certain  types  of  soils 
(Brown,  1927b;   Otto,  1929). 

The  resistance  of  the  eggs  of  the  human  asearis  to  external 
environmental  conditions  accounts  for  its  wide  geographical  dis- 
tribution. Studies  in  the  United  States  (Otto,  Cort,  and  Keller, 
1931)  have  shown  that  they  can  develop  and  persist  on  the  hard- 
packed  clay  soil  of  unshaded  dooryards  where  the  eggs  of  tri- 
churis  and  hookworm  are  soon  killed.  Certainly,  A.  lumbri- 
coides  is  less  restricted  in  its  spread  by  clinuitic  and  soil  con- 
ditions than  any  other  human  parasite  with  free  stages.  Of 
course,  tropical  and  semitropical  countries  with  a  high  rainfall 
oft'er  the  most  favorable  conditions  for  its  spread;  but  where 
human  habits  are  particularly  favorable  a  high  incidence  with 
heavy  infections  may  occur  in  regions,  such  as  in  certain  places 
in  North  China,  where  there  is  low  lainfall  and  a  long  cold 
winter  (Cort  and  Stoll,  1931;  Winfield,  1937a). 

HUMAN  HABITS  AND  SOURCES  OF  INFECTION 
Studies  of  the  last  few  years  in  such  widely  separated  regions 
as  tropical  America,  the  southern  United  States,  North  China, 
and  the  Philippine  Islands,  have  shown  that  the  chief  sources 
of  asearis  infection  are  from  eggs  deposited  Ijy  young  children 
in  the  yards,  under  the  houses,  and  even  within  the  houses  them- 
selves (Brown,  1927a;  Cort,  Stoll,  Sweet,  Riley,  and  Schapiro, 
1929;  Cort  and  Stoll,  1931;  Cort,  Otto,  and  Spindler,  1930; 
Nair,  1935;  Otto  and  Cort,  1934a;  Tubangui,  Basaca,  and  Pas- 
co, 1934;  Winfield,  1937  a  &  b).  This  household  pollution  by 
young  children  results  in  the  accumulation  of  large  numbers  of 
viable  eggs  in  the  dooryards  which  are  frequently  carried  into 
the  houses.  Under  these  conditions  eggs  can  easily  contaminate 
food  and  water  and  also  infect  directly  by  hand-to  mouth  trans- 
fer the  youngest  children  who  play  in  the  dirt  and  are  most 
careless  in  their  habits.  More  general  areas  of  concentrated 
soil  infestation  are  frequently  found  such  as  those  near  unsani- 
tated  schools  or  in  the  yards  of  institutions  (Caldwell,  Cald- 
well, and  Davis,  1930).  In  Egypt  the  sources  of  infection  ap- 
pear to  be  chiefl.v  from  eggs  on  the  floors  of  the  houses  (Scott, 
1939).  The  point  has  been  repeatedly  stressed  that  heavy  in- 
fection of  a  family  can  only  be  brought  about  by  the  grossest 
type  of  soil  pollution  close  to  the  house  combined  with  very 
careless  habits,  especially  in  the  children.  Families  without 
infection  have  frequently  been  found  living  next  door  to  heav- 
ily infected  "asearis  families."  Also,  in  certain  regions,  as 
for  example  western  Tennessee,  where  there  is  little  or  no 
sanitation  in  some  of  the  rural  areas,  asearis  infection  may  be 
at  a  low  level  or  absent  where  the  stools  are  deposited  at  some 
distance  from  the  dooryards  (Otto,  Cort,  and  Keller,  1931). 
Sucli  relations,  and  the  rarity  of  heavy  infections,  can  only  be 
explained  by  postulating  that  in  man,  as  has  been  shown  in 
the  pig,  infection  is  difficult.  The  ingestion  of  large  numbers 
of  eggs  is  evidently  necessary  to  produce  even  moderate  infec- 
tions of  adult  worms.  When  the  constant  loss  of  worms  is  also 
considered,  it  is  easy  to  understand  why  constant  exposure  to 
intense   infection   is  necessary  to   produce  heavy   infections. 

The  contamination  of  drinking  water  has  been  frequently 
suggested  as  a  method  of  infection  with  asearis.  In  most  of 
the  epidemiological  studies  that  have  been  made  in  the  United 
States,  Tropical  America,  and  the  Orient  the  possibility  of  in- 
fection from  this  source  has  been  practically  ruled  out.  In  cer- 
tain parts  of  India,  however,  evidence  was  found  that  the 
contamination  of  shallow  pools  of  water  was  a  factor  in  infec- 
tion (Chandler,  1928).  Recently  the  suggestion  has  been  made 
(Lane,  1934)  that  the  breathing  in  of  dust  containing  viable 
asearis  eggs  might  be  a  source  of  infection  of  considerable  sig- 
nificance. While  infection  in  this  way  seems  possible,  it  could 
hardly  be  a  method  of  major  importance  except  under  very 
unusual   circumstances. 

It  has  been  commonly  considered  that  vegetables  fertilized 
with  human  feces  are  an  important  source  of  asearis  infection 
(Mills,  1927;  Yoshida,  1925;  Walker,  1927;  Khalil,  1931;  Rob- 
ertson, 1936).  This  would  explain,  as  suggested  b.v  Mills 
(1927),  the  distribution  of  asearis  among  all  ages  and  classes 
of  the  population  in  Korea.  Several  workers  in  the  Orient  have 
found  viable  eggs  of  asearis  clinging  to  vegetables  that  are 
used  for  food  uncooked  (see  summary  by  Winfield  and  Yao, 
1937).  Also,  where  human  excrement  is  used  as  fertilizer,  the 
storage,  transportation,  and  distribution  of  night  soil  on  the 
fields  would  serve  to  scatter  the  eggs  of  asearis  widely  in  the 
general  environment  of  the  villages.  However,  definite  evidence 
has  been  presented  in  studies  in  China  that  pollution  by  chil- 
dren in  the  yards  and  streets  of  the  villages  is  a  very  common 
and  perhaps  the  most  important  method  of  asearis  dissemina- 


314 


tioii  iCiirt  aiui  Stiill.  ]'X\\  ;  W  iritiold.  l<):f.'ili ;  Wiiiticld  and  e'liiii, 
l!i;iS).  Also,  ill  North  C'liina,  Wiiiliold  and  Yao  (I'.CiT)  eould 
tiiid  no  evidence  of  asearis  eggs  on  vegetables  after  they  were 
prei>ared  for  food,  and  expressed  the  opinion  that  infection 
from  this  source  was  of  little  if  any  significance  in  this  part 
of  China.  It  seems  clear,  however,  that  the  use  of  human  ex 
crenieiit  as  fertilizer  does  spread  asearis  probably  in  a  number 
of  different  ways,  since  in  China,  Korea,  and  Japan  infection 
witli  this  parasite  appears  to  be  more  common,  especially  in  the 
atlults,  than  anywhere  else  in  the  world. 

CONTROL  OF  ASCAEIASIS 

Treatment  of  infected  populations  and  improvement  in  house- 
hold sanitation  are  the  obvious  suggestions  for  the  control  of 
ascariasis.  On  account  of  the  enormous  numbers  of  eggs  pro- 
duced and  their  great  resistance  to  chemicals,  sterilization  of 
sources  of   infection   \vould  seem   to  have  a   very   limited  value. 

In  spite  of  the  availability  of  effective  nntlieliuintics  (Brown, 
]!'34),  there  is  clear  evidence  that  mass  treatment  of  infected 
pojuilations  is  not  an  effective  control  measure  against  asearis 
because  of  rapid  reinfection  (Cort,  Schapiro,  and  Stoll,  1929; 
Otto,  1930;  Otto  and  Cort,  1934b).  Perhaps  if  the  treatments 
could  be  made  almost  100  percent  effective  in  removing  the 
worms,  and  if  they  were  administered  at  the  end  of  a  dr}' 
season  or  winter  when  the  numbers  of  viable  eggs  in  the  soil 
would  be  reduced  (Cort,  Schapiro,  Riley,  and  Stoll,  1929),  they 
might  have  some  real  value  as  a  control  measure.  At  any  rate, 
treatment  in  ascarisinfected  populations  is  imi)ortant  for  re- 
lieving heavily  infected  individuals,  especially  young  children, 
of   dangerous   worm   burdens. 

There  are  also  certain  difficulties  to  be  met  in  the  attempt  to 
control  asearis  by  improved  sanitation  (Cort,  1931,  p.  137). 
It  was  found  in  Panama  (Cort,  Stoll,  Sweet,  Riley,  and  Scha- 
piro, 1929)  that  in  certain  areas  sanitary  improvements  that 
had  definitely  reduced  the  level  of  hookworm  infection  did  not 
appear  to  limit  the  spread  of  asearis.  Also,  more  than  half  of 
the  families  with  heavy  asearis  infection  that  were  studied  in 
the  mountains  of  Tennessee  had  privies  which  in  almost  all 
cases  were  in  use  (Otto,  Cort,  and  Keller,  1931).  Examples  have 
also  been  reported  from  cities  of  families  with  flush  toilets 
connected  with  the  sewage  system  in  which  the  children  had 
considerable  asearis  infection  (Otto  and  Cort,  1934a;  Headlee, 
193(5).  Under  all  these  conditions  the  infection  is  kept  up  be- 
cause the  young  children  fail  to  use  the  sanitary  facilities  and 
deposit  their  stools  in  the  yards  close  to  the  houses. 

In  attempts  to  improve  sanitation  in  rural  districts  certain 
practical  points  of  special  importance  in  the  control  of  asearis 
seem  to  have  been  entirely  overlooked  in  a  number  of  places. 
First,  the  latrines  should  lie  placed  near  enough  to  the  houses 
so  that  they  can  be  reached  by  the  young  children,  and  in  the 
second  place  they  should  have  special  seats  for  the  children. 
Usually  seats  are  designed  only  for  adults  and  are  difficult  or 
even  dangerous  for  children  to  use.  In  addition,  real  progress 
in  asearis  control  will  have  to  depend  on  the  instruction  of  the 
children  and  their  parents  in  the  homes  and  in  the  schools  in 
the  dangers  of  soil  pollution  and  in  the  minimum  requirements 
of  a  proper  household  sanitation.  In  most  places  widespread 
asearis  infection  is  associated  with  general  low  standards  of 
living,  and  any  raising  of  standards  will  have  a  tendency  to 
reduce    infection. 

Trichuris  trichiura 
W.  W.  C. 

The  whipworm,  Tricliiiri.i  tricliiiira,  was  first  described  by 
Roederer  in  1761,  although  it  was  apparently  observed  much 
earlier.  Davaine  (18.")S  and  18(53)  studied  the  development  of 
the  eggs.  Leuckart  (1866)  demonstrated  experimentally  the 
direct  development  of  the  trichuris  of  the  sheep  and  pig,  and 
Grassi  (1887)  produced  experimental  infection  with  T.  tricliiiira 
in  man.  About  the  liegiuning  of  the  20th  century  the  patho 
genie  role  of  trichuris  was  greatly  emphasized  and  it  was  con- 
sidered to  be  an  important  factor  in  infection  with  such  dis- 
eases as  typhoid  fever,  cholera,  appendicitis,  and  dysentery 
(Guiart,  1911).  More  recently,  however,  these  views  have  been 
discounted  by  most  workers.  The  extensive  surveys  of  the  last 
three  decades  by  fecal  examination  have  greatly  extended  the 
knowledge  of  the  distribution  of  trichuris.  Also,  considerable 
information  on  the  factors  influencing  its  dissemination  has 
been  obtained,  chiefly  in  connection  with  field  studies  on  as- 
earis  and   hookworm. 

The  adults  of  T.  trichiura  are  most  frequently  found  in  the 
caecum,  vermiform  appendix,  and  colon  with  their  long  at- 
tenuated anterior  ends  sewed  into  the  superficial  mucosa.  The 
great  majority  of  infections  with  the  human  trichuris  involve 
only  a  few  worms,  but  in  occasional  cases  hundreds  may  be 
present.  The  length  of  life  of  the  adult  worms  is  not  definitely 
known,  although   it   appears   to  be  much   greater   than    that   of 


ascaiis.  .Mso,  there  is  no  evidence  of  the  constant  loss  of  worms 
and  rapid  turnover  of  infections  found  in  that  species.  There 
is  some  evidence  that  an  acquired  immunity  is  developed  in 
trichuris  infections   (Suzuki,  1934;   Miller,  1941). 

PATIIOGKNECITV 
The  adult  worms  produce  some  injury  to  the  int<'stinal  mu- 
cosa and  when  present  in  large  numbers  may  cause  considerable 
inflammation.  Therefore,  in  the  heaviest  cases  they  may  pro 
duee  rather  severe  intestinal  disturbances.  There  is  no  real 
evidence  that  they  serve  as  a  "lancet  of  infection"  for  other 
diseases  as  suggested  by  many  earlier  workers  (Guiart,  1911) 
and  their  relation  to  the  production  of  anemia  is  rather  doubt- 
ful (Otto,  1935;  Swartzwelder,  1939).  In  most  cases  their 
presence  would  pass  unnoticed  except  for  the  finding  of  the 
characteristic  eggs  in  fecal  examinations. 

DISTRIBUTION    AND    EPIDEMIOLOGY 

Trichuris  trichiura  is  widely  distributed  in  the  world  and 
is  frequently  found,  especially  in  tropical  and  subtropical  re- 
gions, associated  with  both  asearis  and  hookworm.  Its  range 
is  not  as  extensive  as  that  of  asearis,  especially  in  the  temperate 
zones  and  it  is  absent  in  the  colder  regions.  In  the  majority 
of  places  where  both  these  parasites  are  found  together  the  in- 
cidence of  trichuris  is  lower.  In  the  mountain  regions  of  the 
southeastern  United  States,  where  the  incidence  of  asearis  is 
several  times  that  of  trichuris,  families  are  common  that  harbor 
only  asearis,  but  almost  always  where  trichuris  is  f(Hind  as- 
earis will  also  be  present  (Otto,  Cort,  and  Keller,  1931).  There 
are,  however,  many  situations  where  examinations  have  shown 
the  incidence  of  trichuris  to  be  equal  to  or  even  higher  than  that 
of  asearis.  Such  situations  are  usually  in  tropical  or  subtropical 
countries,  but  there  are  a  number  of  places  in  Europe,  especial- 
ly in  the  U.  S.  S.  R.,  where  the  incidence  of  trichuris  is  sur- 
prisingly high. 

Examinations  of  the  last  few  years  by  the  dilution  egg-count- 
ing method  have  given  us  considerable  information  on  the  dis- 
tribution of  trichuris  within  population  groups,  especially  in  the 
United  States  (Cort,  Stoll,  Sweet,  Riley,  and  Schapiro,  1929; 
Otto,  Cort,  and  Keller,  1931;  Cort  and  Otto,  1937).  Its  dis- 
tribution resembles  that  of  asearis  in  having  the  family  as  the 
unit  of  dissemination,  and  in  the  concentration  of  a  large  pro- 
portion of  the  worm  burden  in  a  small  percentage  of  heavy 
cases,  usually  grouped  in  families.  Also,  the  distribution  of 
trichuris  according  to  age  and  sex  is  much  like  that  of  asearis 
except  that  the  peak  of  infection  comes  almost  always  at  a 
somewhat  later  age.  Usually  adult  females  are  more  heavily 
infected  than  males  of  the  same  age  groups. 

The  human  habits  involved  in  the  spread  of  trichuris  and 
asearis  appear  to  be  exactly  the  same.  Differences  in  egg 
production,  susceptibility  of  hosts  to  infection,  stability  and 
persistence  of  infection  in  the  hosts,  or  in  immunity  relations 
cannot  be  evaluated  in  the  present  state  of  our  knowledge  in 
relation  to  differences  in  the  methods  of  dissemination  or  dis- 
tribution of  these  two  parasites.  Therefore,  in  attempting  to 
explain  such  differences  we  must  concern  ourselves  chiefly  with 
the  differences  that  have  Iteen  found  in  the  resistance  of 
their  eggs  to  external  environmental  factors.  The  eggs  of  tri- 
churis are  much  less  resistant  to  low  temperatures  than  are 
those  of  asearis,  and  are  somewhat  less  resistant  to  high  tem- 
peratures (Nolf,  1932).  They  are  also  less  resistant  to  desic- 
cation, require  slightly  more  moisture  for  development,  and  de- 
velop more  slowly  when  the  moisture  is  reduced  (Caldwell  and 
Caldwell,  1928;  Spindler,  1929  a  &  b;  Nolf,  1932;  Onorato, 
1932).  They  are  very  long  lived  and  like  those  of  asearis  are 
very  resistant  to  chemicals,  and  they  are  considerably  more 
resistant  than  the  eggs  of  asearis  to  ultra  violet  light  (Nolf, 
1932). 

The  differences  just  discussed  in  the  resistance  to  external 
environmental  conditions  of  the  eggs  of  asearis  and  trichuris 
appear  to  exjjlain  .satisfactorily  at  least  some  of  the  differences 
in  their  distribution.  Certainly  the  absence  of  trichuris  in  cold 
regions  and  its  scarcity  wherever  there  is  a  long  cold  winter 
can  be  explained  on  the  basis  of  the  lack  of  resistance  of  its 
eggs  to  low  temperatures.  It  seems  unlikely  that  the  eggs  of 
trichuris  on  the  soil  could  live  through  even  a  short  period  of 
freezing   temperatures. 

Following  suggestions  that  trichuris  is  limited  more  in  its 
distribution  by  dry  conditions  than  asearis  (Sweet,  1924; 
Chandler,  1928),  this  relation  was  first  carefully  studied  by 
Spindler  (1929b)  in  the  United  States.  It  was  found  that  in 
the  mountains  of  southwestern  Virginia  trichuris  occurred  in 
a  much  lower  incidence  than  asearis  except  in  a  few  limited 
localities,  where  dense  shade  in  the  yards  produced  moist  con- 
ditions where  the  eggs  were  deposited.  This  finding  led  to  the 
suggestion  supported  by  a  careful  review  of  the  literature  that 
the  incidence  of  trichuris  tends  to  be  as  great  or  greater  than 
asearis  onlv  where  there  is  a  considerable  amount  of  moisture 


Sl.j 


Ill  tlic  soil  due  to  Iieavy  rainfall  or  protection  by  dense  vege- 
tation. Later  epidemiologic  investigations  elsewhere  in  the 
United  States  supported  this  view  by  showing  that  in  other 
areas  where  the  incidence  of  ascaiis  was  much  higher  than 
trichuris,  infections  with  the  latter  were  largely  limited  to 
households  where  dense  vegetation  or  poor  drainage  produced 
moist  areas  around  the  dwellings  where  the  eggs  were  deposited 
(Otto,  Cort,  and  Keller,  1931;  Otto,  1932);  Cort  and  Otto, 
1937). 

Certain  field  studies  in  the  United  States  (Cort  and  Otto, 
1937;  Otto,  1932;  Caldwell,  Caldwell,  and  Davis,  1930)  were 
made  of  situations  where  the  incidence  of  trichuris  was  higher 
than  ascaris.  In  these  places  the  soil  where  the  eggs  were  de- 
posited was  moist  and  appeared  very  favorable  for  develop- 
ment. The  soil  pollution  in  the  yards  and  close  to  the  houses, 
however,  seemed  to  be  considcrabl.v  less  than  that  found  asso- 
ciated witli  heavy  ascaris  infections.  It  was  suggested,  there- 
fore, that  given  favorable  conditions  for  the  development  of 
the  eggs  the  advantage  in  dissemination  would  be  in  favor 
of  trichuris  on  account  of  its  longer  life  and  greater  stability 
in  the  host.  Undoubtedly,  other  differences  in  the  life  cycle, 
host  relations,  and  general  environmental  relations  of  these 
two  parasites  also  produce  differences  in  their  distribution. 

Finally,  since  the  human  habits  responsible  for  the  spread  of 
trichuris  and  ascaris  appear  to  be  the  same,  control  measures 
would   be  the  same  for   both. 

Trichinella  spiralis 
E.  B.  C. 

The  old  Mosaic  law  against  eating  pork  is  perhaps  traceable 
to  suspicions  regarding  the  casual  relationship  between  pork 
and  the  disease  later  called  trichinosis.  From  very  earlj'  days 
epidemics  were  recorded  with  symptoms  strikingly  similar  to 
those  of  trichinosis;  Glazier  (1881)  refers  to  such  a  disease 
among  the  Carthaginians  sent  (B.  C.  427)  to  subjugate  Sicily; 
descriptions  of  outbreaks  from  the  l.^ith  century  on,  in  Ger- 
many, France,  the  British  Isles,  and  America  correspond  so 
closely  with  those  of  trichinosis  that  there  is  now  no  doubt 
as  to  the  etiology.  However,  it  was  not  until  the  19th  century 
that  evidence  was  produced  as  to  the  cause  of  the  disease. 

The  principal  hosts  of  TrichineUa  spiralis  are  swine,  rat  and 
man.  In  addition,  however,  the  following  other  animals  either 
have  lipen  fmiiid  naturally  infected  or  have  been  experimentally 


infected.  Naturally  infected:  mice,  rabbits,  beaver  (coypu),. 
domestic  eat,  palm  civet,  dog,  wolf,  coyote,  fox,  pole  cat,  martin, 
ferret,  European  and  American  badgers,  raccoon,  polar  bear, 
common  bear  {Ursiis  sp.),  and  mongoose.  Experimentally  in- 
fected: guinea  pig,  monkeys,  sheep,  cattle,  horse,  young  chick- 
ens, pigeons,  magpies,  and  rooks.  In  young  chickens  the  larvae 
in  the  muscles  soon  die  (Augustine,  1933;  Matoff,  1938).  Lar- 
vae developed  to  the  infective  stage  in  very  young  [ligeon.s 
(Matoff,  1936;  1938)  and  in  adult  pigeons  affected  by  avita- 
niinosis  (Pavlov,  1940).  In  the  latter  case  infectivity  was 
demonstrated  32  days  after  the  feeding  of  trichinous  meat  to 
tlie  pigeons  (personal  communication).  Coldblooded  animals 
are  apparently  immune  (Pavlov,  1937). 

DIAGNOSIS 

During  life,  diagnosis  of  trichinosis  may  l>e  made  from  the 
clinical  history,  the  differential  blood  picture,  and  immunologi- 
cal tests.  Other  tests,  sometimes  used  but  less  reliable,  are 
the  following.  Stool  examination:  the  evidence  indicates  it  is 
of  little  or  no  value.  Biopsy:  a  bit  of  muscle  excised  usually 
from  the  deltoid,  biceps  or  gastrocnemius  is  examined  as  a 
fresh  press  preparation  and  by  digestion,  as  the  trichinae  are 
thus  more  easily  detected  than  in  sections.  This  method  has 
the  limitation  of  being  not  deiiendable  until  the  end  of  the  third 
week  after  infection  and  in  addition  a  negative  biopsy  does 
not  exclude  trichinosis.  Examinatinn  of  blood  and  cerebrospinal 
fluid  for  larvae:  For  a  period  of  about  3  weeks,  beginning 
about  1  week  after  infection,  the  larvae  may  be  present  but 
are  not  always  easy  to  find. 

Immunological  reactions,  consisting  of  intradermal  and  pre- 
cipitin tests,  are  more  reliable  when  properly  used  and  inter- 
]>reted.  Bachman  (1928)  initiated  both  tests;  they  have  been 
somewhat  modified  by  Augustine  and  Theiler  (1932)  and  other 
workers.  Bozicevich  (1939)  developed  an  improved  antigen, 
sujierior  in  having  larvae  with  a  miniinum  of  debris  and  in 
being  extracted  with  neutral  O.S.'i  percent  solution  of  sodium 
chloride,  without  preservatives;  the  result  is  much  greater  speci- 
ficity and  impioved  maintenance  of  potency.  With  the  im- 
proved antigen  a  positive  skin  test  in  ralibits  may  be  obtained 
8  or  9  days  after  infection;  however,  in  man  positive  reactions 
are  seldom  obtained  until  after  the  second  week  of  infection. 
Both  skin  and  precipitin  tests  should  be  used  for  diagnosis, 
even   though   the  skin   test   is   negative.     Positive   precipitin    re- 


Tablb  9.   Findings  of  trichinae  in  local  stirveys  in  the  United     States 


Author  Date 

Whelpley  1891 

Thornbury 1897 

Williams 1901 

Queen 1931 

1937* 

Riley  and  Scheifley  ..  1934 

Hinman 1936 

McNaught  and  Anderson 1936 

Magath 1937 

Sawitz 1937 

Pote 1937 

Scheitiey 1938 

Walker  and  Breckenridge    .  1938 

Evans 1938 

Hood  and  Olson  1939 

Sawitz   - -  1939 

Butt  and  Lapeyre  ..  1939 

Gould 1939 

Gould  - 1939 

Harrell  and  Johnston 1939 

Oosting    1940 

Catron 1940 

Totals    

•Reported  by  Scheifley,  1938. 


Place 


St.  Louis,  Mo. 

Buffalo,  N.  Y. 

Buffalo,  N.  Y. 

Philadelphia,  Pa. 

Baltimore,  Md. 

1  >enver,  Colo. 

Rochester,  N.  Y. 

Boston,  Mass. 

Denver,  Colo. 

Minneapolis,  Minn. 

New  Orleans,  La. 

San  Francisco,  Cal. 

Rochester,  Minn. 

New  Orleans,  La. 

St.  Louis,  Mo. 

Minneapolis  &  St.  Paul,  Minn. 

Birmingham  &  Tuscaloosa,  Ala. 

Cleveland,  Ohio 

Chicago,  111. 

New  Orleans,  La. 
Los  Angeles,  Cal. 
Eloise,  Mich. 
Eloise,  Mich. 
Durham,  N.  C. 


Dayton,  Ohio 
Ann  Arbor,  Mich. 


Number  of 

Number 

Percent 

examinations 

positive 

positive 

20 

1 

5.0 

21 

3 

14.3 

362 

21 

.^.8 

7 

0 

0.0 

126 

5 

4.0 

10 

1 

10.0 

344 

59 

17.2 

58 

16 

27.6 

431 

70 

16.2 

117 

20 

17.1 

200 

7 

3..T 

200 

48 

24.0 

220 

17 

7.7 

200 

10 

.").0 

1,060 

163 

15.4 

118 

15 

12.7 

100 

33 

33.0 

100 

36 

36.0 

208 

12 

5.8 

220 

25 

11.4 

200 

14 

7.0 

170 

31 

18.2 

90 

11 

12.2 

410 

82 

20.(1 

44 

0 

0.0 

6 

0 

0.0 

55 

3 

.').4 

134 

27 

20.1 

300 


.-,.-.31 


44 


774 


14.7 


13.9 


Method 


Microscopic 

Microscopic 

Microscopic 

Microscopic 

Microscopic 

Microscopic 

Digestion 

Digestion 

Digestion 

Microscopic 

Digestion 

Digestion 

Microscopic 

Micros.  &  digestion 

Sections 

Microscopic 

Micros.  &  digestion 

Micros.  &  digestion 

Digestion 

Digestion  &  micros. 

Micros.  &  digestion 

Digestion 

Digestion 

Micros.  &  digestion 

Digestion 

Microscopic 

Micros.  &  digestion 

%     Digestion ;      % 

Micros.  &  digest. 
Digestion   and   270 

microscopic 


316 


mictions  appear  usually  at  the  end  of  tlie  thiid  week.  Liuiita 
tions  of  the  use  of  these  reactions  for  diagnosis  of  the  disease 
should  l)e  kept  iu  mind;  after  an  attack  of  trichinosis,  a  posi- 
tive skin  test  may  he  obtained  for  as  long  as  7  years  and  a 
I)()sitive  precipitin  reaction  for  as  long  as  2  years.  In  addition, 
persons  with  subclinical  trichina  infections  may  also  give  posi- 
tive skin  and  precipitin  reactions. 

For  postmortem  diagnosis,  the  compressor  method  and  the 
digestion-Bacrmann  method  are  used.  The  former  consists  of 
direct  microscopic  exauiination  of  a  press  preparation  of  mus- 
cle. The  l;itter  method  consists  of  the  digestion  of  muscle  in 
jirtificial  gastric  .iuice,  the  digested  nmterial  being  put  through 
the  Baermann  apparatus  and  examined  microscopically  for  lar- 
vae. Either  of  the  two  methods  has  special  value  and  certain 
limitations  for  certain  types  of  infection,  the  two  methods 
being  supplementary  (Hall  and  Collins,  1!I37).  Both  methods 
have  therefore  been  used  in  recent  surveys  and  on  a  quantita- 
tive basis  of  trichinae  per  gram  of  diaphragm  muscle  examined. 
The  two  methods  have  been  described  in  detail  by  Nolan  and 
Bozicevich. 

Investigation  (Sawitz,  1937;  Schapiro  et  al,  1938)  has  shown 
a  correlation  between  the  skin  test  for  diagnosis  of  trichinosis 
in  living  persons  and  postmortem  findings. 

SYMPTOMATOLOGY 

Trichinosis  is  characterized  by  lack  of  regularity  in  its  course 
(Ransom,  191:1;  Hall,  1937;  Kaufman,  1940).  A  history  of 
eating  raw  or  undercooked  pork  containing  trichina  may  or  may 
not  be  followed  by  a  gastrointestinal  disturbance,  including  ab- 
dominal pains,  nausea,  vomiting,  diarrhea  or  constipation  or  one 
succeeding  the  other,  and  intestinal  henu>rrhages.  Eosinophilia 
of  10  to  45  percent  and  at  times  OS  to  7S  percent  may  be 
present ;  on  the  other  hand  it  may  not  be  present  at  all.  There 
may  be  edema  (usually  periorbital),  high  fever,  myositis  and 
l>neumonia.  The  heart  may  be  involved.  There  may  be  ner- 
vous derangement,  including  encephalitis,  meningitis  and  de- 
lirium. The  variegated  clinical  picture  results  from  differences 
in  intensity  of  infection,  organs  invaded  and  resistance  of  the 
patient.  A  clinical  but  nonfatal  case  may  show  at  biopsy  as 
few  as  8  larvae  per  gram  of  gastrocnemius  (Ferenbaugh  et  al). 
Hall  (1937)  tentatively  designated  as  "heavy  to  critical"  cases 
showing  101  to  1,000  larvae  per  gram.  Conclusions  concern- 
ing man  can  not  be  drawn  from  quantitative  data  from  labora- 
tory animals,  as  in  man  (Xevinny,  cited  by  Roth,  1939)  inflani- 
matorj-  and  other  injurious  processes  are  more  pronounced  and 
extensive,  than  in  those  animals.  Schwartz  (1938)  found  that 
experimentally  infected  hogs  showed  no  symptoms  when  there 
were  less  than  800  to  900  larvae  per  gram  of  diajihragm  muscle 
tissue. 

EPIDEMIOLOGY 

In  California  outbreaks  of  trichinosis  have  resulted  from  the 
eating  of  jerked  bear  meat  (Walker,  1932;  Geigcr  and  Hob- 
maier,  1939)  and  in  Europe  from  the  meat  of  the  polar  bear 
and  the  dog  (cited  by  Kaufman,  1940)  and  the  Coypu  (Rubli, 
1936;.  These  cases  are  rare,  however;  swine  are  the  principal 
source  of  infection  to  man  and  it  is  probable  that  most  cases 
of  infection  of  other  animals  could  be  traced  back  ultimately 
to  swine. 

The  incidence  of  trichinae  in  swine  varies  according  to  the 
locality  and  manner  of  feeding,  the  principal  source  of  the 
infection  being  uncooked  pork  scraps  fed  to  swine  in  garbage 
or  swill ;  the  eating  by  swine  of  infected  rats  or  of  carcasses  of 
infected  pigs  are  very  minor  sources.  Hall  (1937a),  Schwartz 
(1938)  and  Wright  (1939)  have  analyzed  the  data  from  dif- 
ferent parts  of  the  United  States;  trichinae  were  found  in  only 
about  0.5  percent  of  swine  fed  on  cooked  garbage  and  southern 
swine  which  range  the  fields  and  woods  and  get  little  garbage; 
in  1  to  1.5  percent  of  swine  iu  the  Central  West,  where  feeding 
of  grain  predominates  over  garbage  feeding;  in  4  to  (5  percent 
of  swine  fed  on  uncooked  garbage;  and  in  10  to  20  percent  of 
swine  fed  on  slaughter  house  offal,  this  last  group  now  being 
small. 

As  regards  the  incidence  in  man,  data  have  been  inadequate; 
due  to  the  variability  of  symptoms,  cases  are  frequently  un- 
recognized. To  reports  of  outbreaks  of  acute  trichinosis,  which 
have  often  involved  large  numbers  of  persons,  and  those  of 
sporadic  cases  must  be  added  necropsy  findings  which  detect 
subclinical  infections  as  well  as  previously  undiagnosed  clinical 
cases.  In  the  94  year  period,  1842-1936,  according  to  Sawitz 
(1938),  there  were  between  5,000  and  6,000  clinical  cases  of 
trichinosis  diagnosed  and  recorded  in  the  United  States.  Stiles 
(1901)  found  that  in  Germany  between  1860  and  1898  there 
were  reported  14,820  cases  of  trichinosis  with  831  deaths,  a 
mortalitj'  of  5.6  percent.  Hall  (1938a)  points  out  that  iu  the 
1880 's  competent  authorities  maintained  that  the  incidence  of 


tricliinae  was  mucli  greater  in  the  United  States  than  in 
Europe  and  that  these  oi)iuions,  long  neglected,  were  borne  out 
by  later  findings  which  indicate  that  the  United  States  has  the 
greatest  trichinosis  problem  of  any  country  in  the  world.  The 
incidence  here  is  about  5  times  greater  than  in  middle  Europe 
(Magath,  1937),  or  even  higher  (Hall,  1938a).  Comiiarative 
data  are  Lacking  from  many  parts  of  the  world.  A  very  low 
iiu-idence  has  been  found  iu  England  (Van  Someren,  1!I37). 
Eleven  clinical  cases  arc  known  from  the  Hawaiian  Islands 
(Alicata,  1938);  trichinae  have  been  found  in  the  rat,  mon- 
goose and  wild  .-md  domestic  pigs  there.  Apparently  only 
one  hunmn  case  has  been  reported  from  Chiim  although  the  dog, 
cat  and  swine  have  been  found  infected  there   (Ch'n,  1937). 

Early  examinations  of  necropsy  material  were  confined  to 
direct  microscopic  examination  of  muscle  by  the  compressor 
method  and  for  the  most  part  did  not  represent  real  surveys. 
In  more  recent  years  a  digestion  method  has  also  been  used; 
there  is  evidence  that  either  technique  alone  fails  to  detect  one- 
third  of  the  infections,  so  that  a  correction  figure  of  33%  per- 
cent should  be  applied  if  only  one  method  is  used.  Local  sur- 
veys have  been  nmde  in  various  parts  of  the  United  States 
(Table  9)  and  a  nationwide  surveys  of  unselected  cases  from 
various  population  groups  (Table  10)  is  in  progress.  To  date 
the  findings  from  necropsy  examinations  of  over  9,000  persons 
show  that  15  percent  were  infected  with  trichinae,  and  the  ac- 
tual incidence  figure  would  be  higher  if  corrections  could  be 
made  to  eliminate  all  variables.  As  regards  severity  of  infec- 
tion, the  majority  of  488  positive  cases  (Wright,  1939)  showed 
less  than  11  larvae  per  gram  of  diaphragm  but  2.5  iierceiit  of 
the  cases  had  between  101  and  1,000  larvae  per  gram. 

An  analysis  of  the  findings  according  to  sex,  age,  lace,  oc- 
cupation and  social-economic  status  of  2,000  individuals 
(Wright,  1939)  failed  to  show  any  special  correlation  in  most 
of  the  groups  represented.  However,  a  geographical  correlation 
is  indicated,  especially  as  regards  reported  cases  of  cliiiical 
trichinosis;  the  heaviest  incidence  is  found  along  the  North 
Atlantic  coast  and  along  the  Pacific  coast,  correlated  with  gar- 
bage feeding.  In  New  York,  Massachusetts  and  California  from 
501  to  over  1,000  clinical  cases  per  state  were  reported  up  to 
1938  (Hall,  1938)  ;  these  are  areas  where  there  is  extensive 
feeding  of  uncooked  garbage  to  swine. 

CONTROL 

With  regard  to  trichinosis,  the  significance  of  chemotherapy 
is  decidedly  different  than  in  the  case  of  most  other  helminth 
infections, "as  in  oxyuriasis  (p.  324).  In  trichinosis  it  is  en- 
tirely therapeutic,  administered  only  for  the  patient's  sake;  in 
oxyuriasis  it  is  both  proi)hylactic  and  therapeutic,  preventing 
reinfection  of  the  patient  and  infection  of  others. 

Since  human  trichinosis  results  from  the  operation  of  two 
factors  (Hall,  1938),  its  prevention  lies  in  control  of  those 
faetors— namely,  (1)  food  habits  of  the  individual,  including 
infection  from  accidents  and  failures  of  cookery,  and  (2)  the 
frequency  of  occurrence  of  live  trichinae  in  swine  supplying 
the  pork.  It  is  evident  from  necropsy  findings  as  well  as  from 
numerous  sporadic  cases  and  occasional  outbreaks  of  trichino 
sis,  that  a  very  large  number  of  persons  have  eaten  unprocessed, 
uncooked  or  undercooked  infected  pork.  The  great  majority  of 
swine  are  free  from  trichinae;  pork  from  a  small  minority  of 
swine  serves  as  the  principal  source  of  both  human  and  porcine 
trichinosis.  This  source  may  be  combatted  (Hall,  1936;  1937a; 
1938a;  Schwartz,  1938;  Wright,  193S)  by  (1)  meat  inspection; 
(2)  avoidance  of  the  use  of  raw  or  inadequately  cooked  pork  or 
pork  products;  (3)  the  swine  sanitation  system;  (4)  cooking 
of  garbage;   and   (5)   rat  destruction. 

In  Germany  microscopical  inspection  of  pork  for  trichinae 
was  instituted  iu  1875.  Exclusion  of  American  pork  from  Ger- 
many caused  a  loss  of  millions  of  dollars  to  farmers  and  ex- 
porters in  the  United  States  and  led  to  diplomatic  complica- 
tions. Stiles'  (1901)  study  of  the  German  system  indicated 
that  inspection  can  not  detect  all  infected  meat,  that  there  was 
a  false  sense  of  security  from  inspected  meat  and  that  the 
system  was  very  elaborate  and  expensive.  In  the  United  States 
tiiere  has  never  been  federal  meat  inspection  for  trichinae  in 
pork  intended  for  domestic  consumption.  The  principal  mea- 
sures relied  upon  have  been  education  as  to  cooking  pork  thor- 
oughly, and  the  preparation  under  meat  inspection  of  pork 
products  customarily  eaten  raw.  Freedom  from  infective 
trichinae  is  assured  "by  cooking  at  137°  F.  (that  this  tempera- 
ture requirement,  originally  set  by  Ransom  and  Schwartz 
(1919),  is  adequate  has  been  verified  by  Otto  and  Abrams, 
(1939),  by  refrigeration  at  5°  F.  for  not  less  than  20  days 
(Ransom,  1916),  or  by  special  processing  of  the  pork  (Ransom, 
Schwartz  and  Raffensperger,  1920).  That  the  intradermal  test 
be  applied  to  all  hogs  killed  in  all  slaughter  houses,  for  the 
detection  of  trichina  infections,  has  been  advocated  (Nelson, 
1939)   but  the  evidence   (Spindler  and  Cross,  1939;  Lichterman 


317 


and  Klcemai),  1939)  indicates  that  the  test  does  not  detect  all 
trichina  infected  swine. 

The  evidence  shows  that  the  control  measures  of  the  past 
have  been  palliative  and  casual  and  have  not  controlled  trichi- 
nosis; a  basic  program  should  aim  at  elimination  of  tlie  prin- 
cipal source  of  infection  of  swine — namely,  pork  scraps  in  gar- 
bage or  slaughter  house  waste.  The  swine  sanitation  system 
is  of  great  value  where  used;  pigs  are  raised  on  pasture,  are 
not  fed  swill  or  garbage,  and  have  little  or  no  opportunity  to 
eat  rats  or  other  pigs.  As  alread.v  noted,  the  incidence  of  por- 
cine infection  is  correlated  with  the  method  of  feeding  pigs. 
Localities,  as  England  (Van  Somereii,  1937),  which  require 
cooking  of  any  garbage  fed  to  pigs  have  a  low  incidence.  A 
survey  made  by  Wright  (1940)  shows  that  in  the  United  States 
over  50  percent  of  reporting  cities  having  a  population  of 
10,000  or  over  dispose  of  municipal  garbage  in  whole  or  in 
part  by  feeding  it  to  swine.  Very  few  cities  cook  it ;  it  is 
evident  therefore  that  municipalities  are  contributing  substan- 
tially to  the  spread  of  trichinosis.  The  problem  of  control 
clearly  lies  in  that  field. 

Table  10. — Findings  of  trichinae  in  Xational  Institute  of 

Health  nationwide  survey* 

Direct  microscopic  and  digest ion-Baermann  methods 

Number  of    Number  of 
diaphragms  diaphragms  Percent 
Series examined       positive      positive 

Base  (10  hospitals  in  Washington, 

D.  C,  2   Marine  and  4  Naval 

hospitals    in    eastern    seaboard 

cities)    ___ _ 3,000  488  16.3 

Random    (diaphragms  selected  at 

random  from  hospitals  selected 

at  random  throughout  U.S.  A.)         436  80  1S.3 

Negative   (from  States  in   which 

clinical    trichinosis    has    never 

been  reported)  140  26  18.6 

Traumatic       (persons       suffering 

traumatic  death  and  not  hos- 
pitalized)   - _.._   212  3S  17.9 

Jewish  (orthodox  and  unorthodox 

Jews)    _... 134  1  0.7 

Totals 3,922  633  16.1 


*As  reported  by  Hall  and  Collins,  1937;  Nolan  and  Bozice- 
vich.  193S;  Wright,  1939;  Kerr,  1940;  and  Kerr,  Jacobs  and 
Cuvillier  (in  press). 

The  F'tlariae 
D.  L.  A. 

The  superfamily  Filarioidea  contains  a  large  number  of  spe- 
cies of  which  Wnchereria  bancrofti  (Colibold,  1877)  Seurat, 
1921  and  Onchocerca  rolrnlns  (Leuckart,  1893)  Railliet  and 
Henry,  1910,  are  important  pathogens  for  man.  Less  important 
species  that  infect  man  include  Loa  hia  (Cobbold,  1864)  Cas- 
tellani  and  Chalmers.  1913;  Dipelaloiiema  perstans  (Manson, 
1891)  Yorke  and  Maple.stone.  1926;  and  ilansnneUa  oszardi 
(Manson,  1897)  Faust,  1929.  Several  other  species  have  been 
reported  from  man  which  are  known  only  in  the  immature 
stages.  Of  these  only  Microflnria  malai/i  (Brug,  1927)  appears 
to  be  of  clinical  importance.  The  following  discussion  will  be 
limited  to  the  first  two  species  named  and  Microfilaria   malai/i. 

1.  BANCROFTIAN  FILARIASIS 

The  enormous  enlargements  of  parts  of  the  body,  particularly 
of  the  legs  and  external  genitals,  so  frequently  accompanying 
Bancroftian  filariasis  were  noted  and  much  studied  long  before 
the  etiological  agent,  Wnchereria  bancrofti,  was  discovered. 
According  to  Menon  (193.1),  the  first,  and  a  very  good  descrip- 
tion of  these  conditions  was  written  about  600  B.  C.  by  Susliruta 
in  India.  The  disease  was  probably  also  well  known  in  Persia, 
Arabia,  Egypt,  and  parts  of  Africa  at  that  time.  Hillary 
(1766)  gives  a  very  good  account  of  its  occurrence  in  Barliados, 
describing  the  recurring  attacks  of  fever,  the  lymphangitis,  the 
lymphadenitis,  and  the  slowly  increasing  swellings  of  the  af- 
fected part  up  to  the  stage  at  which  typical  elephantoid  appear- 
ances become  definite  and  iironiinent.  Hillary  was  certain 
that  the  disease  had  been  brought  to  the  West  Indies  from 
Africa  by  Negro  slaves  and,  at  his  time,  was  observed  to  be 
"too  frequent  among  them  and  among  the  white  people  also." 
Neumann  (O'Connor  and  Beatty,  1938)  estimated  that  6  per- 
cent of  the  population  of  St.  Croix,  Virgin  Islands,  had  elephan- 
tia.sis  in  1881. 


Obsei-vations  demonstrating  the  etiology  of  elephantiasis  were 
initiated  in  1863  by  the  French  surgeon  Demarquay,  who  found 
microfilariae  in  chylous  urine  of  a  person  who  had  lived  in 
Cuba,  were  continued  by  the  investigations  of  Lewis  (1879)  in 
India  and  by  others,  and  culminated  in  the  research  of  Patrick 
Manson  in  China  between  1876  and  1900.  Early  in  his  inves- 
tigations Manson  discovered  filarial  periodicity  and  experimen- 
tally demonstrated  that  a  mosquito.  Cule.r  fatigans,  was  an  es- 
sential intermediate  host  and  the  agent  for  dissemination  of 
the  parasite.  More  recent  investigations  have  been  largely  epi- 
demiological and  pathological.  Noteworthv  among  these  arc  the 
studies  of  Bahr  (1912),  Low  (1913),  O'Connor  (1923;  1931), 
Anderson  (1924),  Fiilleborn  (1929),  Iyengar  (1938),  and  Payn- 
ton  and  Hodgkin  (1938). 

The  adult  worms  are  parasites  only  of  the  lymphatic  system 
of  man.  They  maj'  occur  at  any  level  of  the  system,  but  are 
found  most  frequently  in  the  limbs,  scrotum  and  inguinal  re- 
gions. The  two  sexes  are  frequently  coiled  together  in  the 
periglandular  tissues,  the  lymphatic  vessels  of  the  capsule  and 
in  the  cortical  sinuses.  In  heavy  infections  they  may  also  oc- 
cur in  the  medulla. 

The  microfilariae  (for  life  history  see  p.  288)  occur  in  the 
lymph,  the  blood  stream,  and,  under  certain  conditions  (chy- 
luria),  may  be  found  in  the  urine.  Tliese  larvae  characteris- 
tically exhibit  a  marked  nocturnal  periodicity.  They  are  found 
in  greatest  numbers  between  10  o'clock  in  the  evening  and  2 
o'clock  in  the  morning,  but  during  the  day  they  may  be  en- 
tirely absent  from  the  blood.  In  the  Philippine  Islands  and 
largely  throughout  Polynesia,  however,  the  microfilariae  show- 
no  periodicity;  while  in  Australia  and  New  Guinea,  periodicity 
is  the  rule,  but  both  types  do  occur.  As  far  as  is  known  botli 
types  represent  one  and  the  same  species.  In  order  to  continue 
their  life  cycle  microfilariae  must  be  taken  up  by  an  appropriate 
mosquito. 

GEOGRAPHICAL  DISTRIBUTION 

IVnchcreria  bancrofti  is  practically  world-wide  in  distribu- 
tion, but  is  largely  limited  to  tropical  and  subtropical  coun- 
tries. Its  spread  necessarily  depends  on  the  extent  of  the  mi- 
grations of  individuals  showing  microfilariae  in  the  blood,  and 
on  the  presence  or  absence  of  appropriate  mosquitoes  in  new 
areas  to  serve  as  intermediate  hosts.  The  parasite  is  eharac- 
teristicall.y  found  in  island  populations  or  along  more  or  less 
broad  low-lying  coastal  areas  of  larger  islands  and  continents. 
In  Asia  it  is  established  along  coastal  areas  from  Arabia  to  the 
Shantung  Province  in  Eastern  China,  and  cases  have  been  re- 
ported as  far  north  as  Manchuria.  It  is  prevalent  in  the  islands 
of  the  East  China  Sea,  southern  Japan,  southern  Chosen  and 
throughout  Oceania.  In  Australia  its  distribution  is  mainly 
along  the  Queensland  coasts. 

Bancroftian  filariasis  is  common  across  tropical  Africa, 
Madagascar,  Mauritius  and  neighboring  islands  and  along  the 
Mediterranean  shores.  It  has  been  reported  to  be  indigenous  in 
Spain,  Hungary  and  Turkey.  It  is  of  very  common  occurrence 
throughout  the  West  Indies,  the  Guianas.  and  Venezuela,  and  is 
less  frequent  in  northern  Colombia  and  eastern  Brazil  (Bahia). 
It  appears  not  to  have  become  established  along  the  Pacific 
coast.  A  small  endemic  focus  was  reported  in  191.5  and  again 
in  1919  in  North  America  near  Charleston,  South  Carolina 
(Francis,  1919).  Sporadic  cases  of  infection  have  been  noted 
from  time  to  time  in  various  parts  of  the  United  States,  but 
these,  invariably,  were  of  foreign  origin  or  from  the  Charles- 
ton area.  Thus,  it  is  evident  that  Bancroftian  filariasis  has 
a  world-wide  geographic  distribution.  Its  distribution  within 
any  given  country  is,  however,  characteristically  and  markedly 
spotted  and  discontinuous  due  to  the  local  physical  factors  and 
the  differences  in  social  standards  and  .sanitation. 

PATHOLOGY 

It  is  generall.v  held  that  living  microfilariae  are  not  patho- 
genic. It  has  been  observed  that  microfilariae  readily  pass 
through  lymph  nodes  without  phagocytic  filtration  (Drinker, 
Augustine  and  Leigh,  193.5).  'They  are  exceedingly  active  in 
the  blood  stream.  They  are  not  only  passively  carried  about 
with  the  blood  stream  but  actively  move  against  the  lilood 
stream  in  the  arterioles,  making  slow  progress  by  bracing  them- 
selves through  the  crests  of  the  alternate  undulations  of  their 
bodies  against  the  walls  of  the  vessel.  They  frequently-  occlude 
the  capillaries  and  then  make  their  way  through  the  stagnated 
column  of  blood  cells  to  reenter  the  active  circulation.  They 
apparently  never  make  permanent  plugs  or  form  emboli  (Au- 
gustine, Field  and  Drinker,  1936;   .\ugustine,  1937). 

The  serious  disorders  are  brought  about  by  dead  micro- 
filariae and  the  living  and  dead  adult  worms.  These  disorders 
in  every  case  can  be  traced  to  interference  with  the  lymphatic 
system.  Living  worms,  however,  apparently  cause  little  damage 
other  than  varying  degrees  of  blockage  of  the  afferent  approach 
of   the   vessels   in   which   the3-   lie.     However,   when   the   adult 


318 


worms  dio  tlu'y  Iiecoino  forciK"  bodies.  Inflamiiiation  follows 
their  death  and  degeiieiation.  s"'i"K  rise  to  lymphangitis, 
lYnii)liadenitis,  intlammatovy  varicose  j^roin  glands,  abscess  and 
fever.  The  obstructed  and  dilated  lymphatics  sometimes  rup- 
ture, with  escape  of  chyle  into  the  bladder,  and  less  frequently 
into  the  intestine  and  the  abdominal  cavity,  and  thus  (j'^'c  ''se 
to  chyluria,  chylous  diarrhea  and  cliylous  ascites.  Without 
ru|)ture  of  the  vessel,  superficial  or  deeji  lymph  varices  may 
develop,  such  as  varicose  (flands  of  the  );roin  or  axilla,  h.ydrocelo 
and  lymph  scrotum. 

All  active  changes  are  associated  with  the  defeneration  and 
absorption  of  dead  parasites.  The  end  result  is  always  fibro 
sis  with  complete  occlusion  of  the  parasitized  vessel.  Elephan- 
tiasis, one  of  the  commonest  lesions,  is  the  result  of  long  and 
widespread  lymphatic  obstruction. 

Pyogenic  Ijactcria,  streptococci  and  stajihylococci  have  been 
isolated  fairly  frequently  from  the  region  of  the  lymphedema. 
Their  responsibility  in  the  disease  syndrome,  however,  is  not 
clear.  Drinker,  Field  and  Homans  (1934)  and  Drinker  (1936) 
have  shown  experimentally  that  loss  of  lymph  circulation  pre- 
disposes to  streptococcic  infection,  that  these  liacteria  cause 
attacks  of  severe  chill  and  high  fever,  and  usually  can  be  iso- 
lated from  the  tissue  fluids  only  in  the  early  stages  of  the 
seizures. 

The  diagnosis  of  infections  with  W.  bancrofti  is  made  by 
finding  the  characteristic  microfilariae  in  the  blood.  Many 
cases,  however,  having  clinical  symiitoms  show  no  microfilariae 
in  the  blood  nor  in  the  contents  of  the  dilated  vessels.  In  such 
instances  the  infection  is  usually  of  long  standing  and  either 
the  adult  worms  have  died  or  the  lymphatics  draining  the  af- 
fected area  have  become  obstructed  by  the  worms  and  their 
products  to  such  an  extent  that  the  microfilariae  cannot  pass 
along  the  vessels  to  enter  the  circulating  blood. 

EPIDEMIOLOGY 

Bancroftian  filariasis  characteristically  occurs  in  low  lying 
coastal  areas  and  along  the  shores  of  lakes  and  rivers.  In- 
digenous infections  are  seldom  to  be  found  in  the  foothills  or 
beyond  coastal  ranges.  The  incidence  of  infection  and  clini- 
cal manifestations  in  endemic  regions  vary  greatly  in  adjoin- 
ing areas.  The  incidence  of  infection  is  always  in  direct  rela- 
tion to  the  prevalence  of  the  mosquito  concerned;  and,  in  turn, 
the  prevalence  of  these  mosquitoes  in  an  area  is  in  direct  rela- 
tion to  the  favorableness  of  that  area  for  moscpiito  breeding. 
The  parasite  is  naturally  limited  to  the  range  of  its  insect 
vectors,  and  local  physical  factors,  such  as  temperature,  hu- 
midity, porosity  of  the  soil,  prevailing  winds,  and  character 
of  the  vegetation  which  may  influence  the  development  and 
presence  of  the  vector,  will  also  indirectly  influence  the  inci- 
dence and  intensity  of  filariasis  in  the  human  population. 

O'Connor  (1923)  found  a  very  low  incidence  of  filariasis 
and  but  a  very  few  mosquitoes  on  some  atolls  of  the  Ellice 
group  having  narrow,  broken  land  strips  and  lacking  depth  of 
bush  favorable  to  Aerlr.t  rarirgaUi.i.  On  other  atolls  with  larger 
land  areas,  the  central  lagoon  reduced  to  a  swamp,  and  cov- 
ered with  d?nse,  dark  bush,  Aedrx  raruiiatiis  was  obs?rved  in 
swarms  throughout  the  day,  and  over  70  percent  of  the  in- 
habitants over  16  years  of  age  showed  some  sign  of  filarial  in- 
fection. Again,  a  favorable  high  temperature  with  a  suitable 
amount  of  moisture  is  absolutely  necessary  for  the  development 
of  the  parasite  in  the  mosquito  and  for  its  transfer  from  the 
mosquito  to  the  human  skin.  The  low  incidence  of  infection 
or  absence  of  infection  in  many  places,  particularly  in  the  in- 
terior of  China  where  proved  mosquito  carriers  are  present,  is 
attributed  to  cold  or  to  dryness  and  high  temperature  (Feng, 
1931).  Thus,  local  conditions  may  have  a  marked  influence  on 
the  distribution  of  the  infection  within  an   endemic  area. 

While  the  mosquito  is  the  sole  vector  of  W iichrreria  bancrofti, 
as  in  malaria,  the  transmission  is  accomplished  with  much  less 
certainty  and  promptness  in  the  case  of  filariasis.  There  is  no 
.multiplication  of  filaria  larvae  in  the  intermediate  host.  There 
develops  but  one  infective  larva  from  each  microfilaria  sucked 
in  by  the  mosquito,  whereas  the  malaria  parasite  multiplies 
enormously  and  the  chance  of  the  infection  being  returned  to 
man  is  by  thousands  of  times  more  likely.  The  actual  number 
of  microfilariae  sucked  up  by  the  mosquito  is  also  relatively 
small  in  comparison  with  the  number  of  malarial  organisms  in 
the  blood  which  may  be  taken  up  in  a  similar  manner.  A  high 
mortality  occurs  among  the  microfilariae  which  actually  reach 
the  .stomach  of  the  mosquito. 

O'Connor  and  Beatty  (193S)  estimated  that  about  3.5  per- 
cent of  the  microfilariae  ingested  by  mosquitoes  die  within  20 
hours  after  an  infective  meal  in  the  stomach  blood  clot,  that  a 
very  heavy  mortality  of  larvae  may  occur  after  their  arrival 
in  the  thorax,  and  that  many  infected  mosquitoes  may  die  dur- 
ing the  first  f^ew  days  after  such  feeding.  Of  ,").nOO  wild  Culex 
fatiganx  collected  over  a  period  of  12  consecutive  months  in  St. 


Croix,  V.  I.,  fr(un  within  and  near  dwellings  occupied  by  per 
sons  with  filariasis,  only  2.3  percent  were  found  to  contain 
fully  "infective"  larvae.  These  authors  believe  that  the  ])er- 
centage  of  C.  fatiflaii.s  which  actually  transmit  the  infection  to 
man  is  much  smaller,  due  to  death  of  mosquitoes  from  various 
causes  such  as  strong  winds,  torrential  rains,  spiders,  bats,  liz- 
ards and  chickens.  Chickens  wandering  into  the  laboratory 
were  observed  to  search  and  eagerly  devour  mosquitoes  resting 
in  the  darker  corners  of  the  room.  It  was  also  observed  that 
r.  fali(/a)i.s  readily  feeds  upon  domestic  fowl.  It  is  probable 
that  many  parasites  are  deposited  on  the  skin  or  feathers  of 
birds  and  thus  liecome  lost. 

Bancroftian  filariasis  char.'icteristically  occurs  in  small,  dense 
ly  populated  and  poorly  .sanitated  villages.  It  is  particularly 
common  in  the  overcrowded  dwellings  of  poor  people,  and  the 
incidence  and  morbidit.y  in  a  given  family  ma.v  be  striking. 
Infection  is  usually  commoner  in  males  than  in  females,  which 
difference  in  China  is  attributed  to  the  custom  among  women 
of  wearing  more  clothes  while  sleeping  at  night,  and  thus  ex- 
posing less  body  surface  to  the  attack  of  mosquitoes  (Lee, 
1926).  The  severity  of  the  disease  characteristically  increases 
with  advancing  age,  thus  indicating  absence  of  any  develop- 
ment of  immunit.Y  in  filarial  infection.  All  races  of  mankind 
appear  to  be  equall.v  susceptible.  Differences  noted,  particu- 
larly absence  of  infection  or  lighter  infection  among  North 
Americans  and  Europeans  residing  in  the  area  are  due  to  their 
better  sanitary  conditions,  better  protection  against  mosquitoes, 
and  homes  removed  from  the  over  crowded  dwellings  of  the 
native  population.     Better  housing  is  always  essential  in  control. 

In  view  of  the  fact  that  the  parasite  is  transmitted  solely 
through  the  bites  of  mosquitoes,  its  prevention  is  primarily 
one  of  mosquito  control,  and  measures  taken  against  these 
insects  in  the  control  of  malaria  and  yellow  fever  are  eciually 
effective  against  infections  with  TTuchereria  bancrofti.  Culex 
fatifiann  is  a  domestic  mosquito  which  breeds  near  dwellings 
in  cisterns,  rain  liarrels,  discarded  tin  cans,  sullage  drains, 
ditches,  etc.  Tight  screens  and  gauze  coverings  will  prevent 
mosquito  breeding  in  cisterns,  vats  and  rain  barrels.  Discarded 
pots,  tins  and  other  utensils  should  be  buried  or  destroyed,  and 
drains  arid  ponds  kept  clear  of  vegetation  in  order  to  effect 
proper  mosquito  control.  All  breeding  places  should  receive 
weekly  treatment  with  larvicides.  In  the  Oceanic  Islands, 
where  Ai^des  variegatus  is  the  most  important  vector,  attention 
must  be  centered  on  discarded  cocoanut  husks  and  shells,  natu- 
ral and  artificial  cavities  in  trees,  tin  cans,  and  other  possible 
containers  of  clean  water.  O'Connor  (1923)  observed  that  the 
Pacific  rat  makes  breeding  places  for  A.  variegatus  in  trees  by 
gnawing  and  cutting  young  cocoa-pods.  The  pods  then  die, 
become  dry,  and  form  hanging  breeding  places  for  the  mos- 
quito. 

With  modifications  to  meet  local  conditions,  the  methods  ad- 
vocated by  O'Connor  and  Beatty  (193S)  to  reduce  Bancroftian 
filariasis  in  Christiansted,  St.  Croix,  might  be  effectively  ap- 
plied elsewhere.     They  include  the  following  recommendations: 

-4.     The  general  measures  adopted  should  be  as  follows: 

1.  The  incidence  of  persons  with  microfilariae  should  be  de- 
termined at  the  same  time  for  the  whole  population. 

2.  The  percentage  of  infective  mosquitoes  should  be  deter- 
mined in  tlie  same  houses  and  outhouses,  etc.  The  mosquito  "in- 
fective" incidence  may  be  more  valuable  than  the  mierofilarial 
incidence,  partly  because  while  some  natives  do  not  readily  sub- 
mit to  having  blood  taken  from  them,  yet  when  the  reasons 
are  explained  to  them  they  rarely  ob.iect  to  their  mosquitoes 
lieing  collected.  Furthermore,  a  person  with  microfilariae  hav- 
ing been  infected  in  another  locality  may  be  in  a  place  where 
there  are  few  or  no  mosquitoes  and  so  will  not  be  a  serious 
menace.  On  the  other  hand,  the  repe.'.ted  finding  of  infected 
mosquitoes  is  proof  positive  that  one  or  more  persons  with 
microfilariae  is  near  l)y. 

3.  These  studies  might  well  be  repeated  aliout  every  3  years. 

B.  In  houses  of  high  human  and  mosquito  infectivity  inci- 
dence, the  following  local  measures  should  be  carried  out: 

1.  The  nature  of  filariasis,  its  transmission  and  prevention 
should  be  completely  and  simply  explained  to  the  occupants  of 
the  house  where  control  measures  are  in.stituted. 

2.  Suitable  containers  for  potable  and  other  water  supplies 
should  be  adequately  .screened  with  wire  netting.  Where  con- 
tainers are  not  suitable  they  should  be  replaced. 

3.  The  use  of  the  mosquito  net  should  be  demonstrated.  (If 
the  occupants  cannot  afford  them  these  should  be  provided  from 
public  funds.) 

4.  The  proper  maintenance  and  us?  of  all  screening  should  be 
supervised  at  intervals  by  the  existing  sanitary  officers. 

5.  When  possible  occupants  should  be  encouraged  to  keep 
fowls  in  their  yards  near  the  house. 

6.  The  number  of  mosc|uitoes  in  the  houses  and  the  percentage 
of  these  which  are   infective  should  be  recorded  from   time  to 


319 


time  in  order  to  evaluate  the  results  of  preventive  measures. 

7.  Efforts  to  have  adult  mosquitoes  killed  daily  by  the  in- 
habitants wliile  highly  desirable  will  usually  be  found  imprac- 
ticable. This  measure  would  be  too  expensive  for  government 
maintenance,  but  where  full  cooperation  is  assured  it  should  be 
adopted  to  supplement  the  foregoing. 

The  control  of  filariasis  in  the  Orient  is  complicated  by  the 
presence  of  another  filariid,  quite  recently  discovered,  which  has 
long  been  confused  with  IViichercria  bancrofti.  This  species. 
Microfilaria  inalayi,  was  discovered  in  1927  by  Leichtenstein  in 
the  Dutch  East  Indies.  Leichtenstein  had  failed,  after  numer- 
ous attempts,  to  infect  Ciilex  fatigans  and  other  eulicine  mos- 
quitoes with  microfilariae  of  the  area,  and  noting  the  absence 
of  acute  forms  of  the  disease,  although  elepliantiasis  of  the  leg 
was  common,  it  occurred  to  him  that  he  might  be  dealing  with 
a  new  species  of  filaria.  Brug  (1927)  examined  Leichtenstein 's 
material,  found  morphological  characters  distinct  from  Ban- 
croftian  microfilariae,  and  proposed  the  name  Filaria  malayi 
for  the  parasite.  Brug's  observations  have  since  been  confirmed 
by  various  workers,  and  the  species  now  appears  established  on 
morphological  characters  of  the  microfilariae  and  extensive  epi- 
demiologic studies,  although  the  adult  worms  are  yet  to  be 
discovered. 

Thus  far.  Microfilaria  malayi  appears  to  be  strictly  oriental 
in  geographic  distribution.  It  is  known  to  occur  in  the  Fed- 
erated Malay  States,  Sumatra,  Java,  Ceylon,  parts  of  India, 
Indo-China  and  in  north-eastern  Chekiang  Province  of  China. 
It  is  often  the  dominant  species  of  a  given  region  and  occurs 
typically  in  rural  districts  along  river  or  forest  settlements. 
Elephantiasis  of  the  feet  and  legs  is  typically  associated  with 
J/,  malayi  infection.  The  genitals  and  upper  extremities  are 
rarely  involved  as  in  Bancroftian  filariasis.  The  microfilariae 
show  nocturnal  periodicity,  but  do  not  disappear  entirely  from 
the  peripheral  blood  during  daytime.  Mosquitoes  of  the  genus 
Manxotiia,  subgenus  Maiisonioidcs,  are  the  principal  vectors, 
particularly  M.  (Monsonioides)  annulifera.  These  are  noc- 
turnal feeders  and  are  most  active  during  the  evening  from 
7  p.m.  to  S  p.m. 

Recently,  extensive  studies  have  been  made  on  the  control  of 
filariasis  in  India,  particularly  in  Travancore,  where  Microfilaria 
malayi  is  chiefly  concerned  (Sweet  and  Pillai,  1937;  Iyengar, 
1938).  It  was  demonstrated  by  these  investigators  that  the 
presence  of  a  floating  plant,  Pistia  stratioitcs,  is  essential  for 
tlie  breeding  of  Maiismiia.  The  female  mosquito  does  not  or- 
dinarily lay  eggs  except  on  the  leaves  of  Pi.'<tia,  and  the  larvae, 
being  structurally  adapted  to  obtain  their  supply  of  oxygen 
from  the  air  cavities  in  the  root,  are  not  capable  of  living  apart 
from  this  particular  plant. 

In  experimental  areas  the  clearance  of  ponds  and  tanks  of 
Pixtia  markedly  reduced  the  incidence  of  Maiifioiiia  mosquitoes 
and  checked  further  spread  of  the  infection.  Pistia  plants  can 
be  cheaply  and  effectively  removed  by  hand.  Here  we  have  an 
excellent  example  of  the  suppression  of  a  mosquito-borne  disease 
by  a  strictly  limited  S])ecies  control  of  the  carrier. 

2.  ONCHOCERCIASIS 

Onchocerciasis  in  man  is  caused  by  Onchocerca  volviihi.<< 
(Leuckart,  1893),  the  adult  forms  of  which  are  characteris- 
tically found  in  prominent,  subcutaneous,  fibromatous  tumors. 
The  microfilariae  aiipcar  in  large  numbers  in  the  skin,  especial- 
ly in  the  skin  in  the  vicinity  of  the  tumor,  the  eyes,  the  con- 
.iuMctivao  and  the  cornea,  and  in  the  central  portion  of  the 
tumor  with  the  adult  worms.  They  do  not  appear  in  the  cir- 
cnlation  but  may  rarely  occur  in  the  deeper  tissues  and  viscera 
(Rodhain,  1937).  When  seen  in  fresh  sections  of  the  epidermis 
or  conjunctiva  they  are  actively  motile  and  possess  no  sheath. 
Two  types  are  clearly  distinguished.  It  has  been  suggested 
that  the  smaller  forms  with  a  more  compact  arrangement  of 
the  nuclei  may  represent  male,  and  the  longer  ones  female 
microfilariae. 

It  is  believed  that  the  tumor  results  from  the  irritation  pro- 
duced by  the  presence  of  the  adult  worms  and  the  products 
of  their  metabolism.  Unencapsulnted  adult  worms  have,  how- 
ever, been  noted  (Sharp,  1927;  van  den  Berghe,  193li).  The 
microfilariae  have  been  considered  to  be  a  cause  of  an  erysipela 
tons  condition  of  the  face  and  head  and  of  disturbances  in 
vision,  iritis,  punctate  keratitis  and  total  lilindness.  The  part 
tliat  these  microfilariae  play  in  the  production  of  these  condi- 
tions is  not  clear. 

Onchocerciasis  is  very  common  along  the  west  coast  of  Africa 
from  Sierre  Leone  to  the  Congo  liasin  and  extending  eastward 
through  the  Congo  into  I'ganda,  Anglo-Egyptian  Sudan  and 
Kenya.  It  also  occurs  endemically  in  southern  Mexico  and 
Guatemala  upon  the  Pacific  or  southern  slopes  of  the  volcanic 
ranges  at  altitudes  between  2,000  and  4,500  feet  (Caldernn, 
1920).  The  parasite  in  Central  America  was  discovered  by 
Robles  in   191.5   and   named    Onchocerca   cacculieiif:  by   Brumpt 


in  1919,  who  considered  the  American  form  distinct  since,  in  the 
great  majority  of  cases,  the  tumor  was  located  upon  the  scalp  or 
in  the  region  of  the  face,  whereas  the  tumor  in  African  cases 
was  generally  found  on  the  body.  Further,  the  disease  in  America 
was  observed  only  in  areas  mainly  inhabited  by  native  Indians 
and  into  which  regions  the  negro,  apparently,  had  never  been 
introduced.  Later  studies  by  Strong  and  associates  (1934) 
have  shown  that  the  Central  American  form  cannot  be  sep- 
arated from  the  African  form  on  either  morphological  charac- 
ters or  on  biological  criteria.  The  two  forms  are  now  gen- 
erally regarded  as  belonging  to  the  same  species,  0.  volvulus. 

Blackloek  (1926)  demonstrated  that  the  black-fly  Simulium 
(lamnosum  is  particularly  concerned  in  the  transmission  of 
onchocerciasis  throughout  tropical  Africa.  S.  ncavci,  however, 
is  said  to  be  the  chief,  if  not  the  only  carrier  of  the  parasite 
in  the  Lubilash-Sankuru  region  in  the  Province  of  Lusambo 
(Kasai).  S.  metaUicum,  S.  caUidum  and  S.  ochraceum  are  the 
vectors  in  endemic  regions  of  Mexico  and  Guatemala  (Strong 
et  al,  1934).  The  development  of  the  parasite  in  these  flies 
and  its  transmission  to  man  are  essentially  the  same  as  the 
development  and  transmission  of  W uchercria  bancrofti  in  and 
liy  mosquitoes. 

The  control  of  onchocerciasis  in  Africa  is  exceedingly  diffi- 
cult due  to  its  widespread  distribution  and  the  general  topog- 
raplo'  of  the  country,  dense  vegetation  or  forests  and  running 
streams,  ideal  environments  for  the  breeding  of  Simulium. 
Vegetation  is  usually  cleared  only  in  the  vicinity  of  the  vil- 
lages and  plantations.  This  limited  clearance  of  vegetation  is 
probably  of  little  value  in  control  since  these  flies  are  capable 
of  fl.ying  great  distances.  The  people  are  attacked  by  the  flies 
most  frequently  while  defecating  at  the  edges  of  streams  (a 
common  and  usual  practice),  while  collecting  water  for  drinking 
jiurposes  or  while  engaged  in  agricultural  pursuits,  rice,  cotton 
or  coffee  cultivation  which  bring  them  into  the  immediate 
environment   of  the   fly. 

Measures  of  individual  protection  against  the  bites  of  these 
flies,  such  as  wearing  of  fly-proof  clothing  and  masks,  proper 
screening  of  houses  and  bed  nets,  the  use  of  smudges  and  re- 
pellents, are  to  be  recommended,  but  are  usually  not  practical 
and  are  rarely  applied  by  native  populations.  It  is  obvious 
that  effective  control  of  onchocerciasis  rests  in  the  eradication 
of  Simulium  flies  but,  as  yet,  there  is  no  practical  method 
known  to  destroy  their  eggs,  larvae  or  pupae  which  abound 
under  stones  in  the  swiftly-flowing  streams  of  the  endemic 
areas. 

In  Central  America  attempts  Imve  been  made  to  control  the 
human  carriers  which  infect  the  flies.  Surgical  removal  of  the 
tumors  containing  adult  worms  has  been  a  public  health  proce- 
dure of  importance,  and  where  a  systematic  attempt  has  been 
made  to  eradicate  the  disease  in  sharply  circumscribed  areas, 
the  late  of  infection  has  been  greatly  reduced.  It  is  recom- 
mended (Strong  et  al,  1934)  that,  under  local  conditions  as  in 
Guatemala,  periodic  microscopic  examinations  should  be  made 
in  each  individual  after  operation  to  detect  the  number  of 
microfilariae  which  may  persist  and,  if  large  numbers  of  micro- 
filariae are  present,  the  patient  should  be  regarded  as  a  dan- 
gerous carrier  and  be  isolated,  or  removed  to  a  region  where 
Simiiliitm   does   not    occur,   until   the   parasites   disappear. 

Dracunculus  medinensis 
W.  W.  C. 

Although  the  guinea  worm,  Dracunculus  nicdini  iisis,  has 
been  known  since  ancient  times  nothing  was  understood  of  its 
life  cycle  until  Fedtschenko  (1871)  implicated  Cyclops  in  its 
transmission.  Since  that  time  various  species  of  cyclops  have 
been  infected  experimentally  and  recently  Moorthy  (1938)  has 
given  an  adequate  account  of  the  developmental  stages  in  this 
liost.  Leiper  (1907)  re])orted  the  experimental  infection  of  a 
monkey  and  the  finding  of  two  immature  males,  and  recently 
experiments  with  dogs  (Issajev,  1934a;  Moorthy  and  Sweet, 
1936  &  1938)  have  made  possible  the  adequate  description  of 
the  male  (Moorthy,  1937)  and  added  nmch  to  our  knowledge 
of  all  the  stages  in  the  definitive  host.  The  researches  of 
Fairley  and  Listen  (1924a),  Fairley  (1924),  and  others  have 
served  to  give  a  picture  of  the  pathology  and  symptomatology 
of  dracontiasis  and  numerous  and  widely  scattered  publications 
have  given  the  present  conception  of  its  geographical  distri- 
bution, epidemiology,  and  control.  In  spite  of  numerous  sug- 
gestions no  treatment  of  real  value  is  yet  known.  Although  the 
extent  of  the  studies  on  this  parasite  is  impressive,  much  more 
needs  to  be  done  to  bring  our  knowledge  even  up  to  the  level 
of  that  of  the  other  important  human  helminths. 

Natural  infections  with  worms  identified  as  D.  medinensis 
have  been  reported  from  a  number  of  mammals  including  dog, 
horse,  cattle,  jackal,  wolf,  leopard,  monkey,  deer,  baboon,  rac- 
coon, mink,  and  fox  (Leiper,  1910;   Turkhud.  1920;  Chitwood, 


320 


in3;<).  While  some  of  those  records  niiiv  he  due  to  eoiit'usion 
of  elosoly  rehited  species,  there  is  no  reason  to  donlit  th;it  in 
some  ciises  the  worms  actually  were  1).  mcdininsis.  There  is  no 
evidence,  however,  that  any  of  these  animals  are  si{;riilicant 
reservoir  hosts  in  the  endemic  areas.  Infection  in  aniumls,  liow 
ever,  might  serve  to  spread  this  jiarasite  into  new  areas  as 
suggested  by  its  presence  in  animals  in  Chimi  (Ilsii  and  Watt, 
VXV.>.)  and  in  the  United  States  (Chitwood,  1!)33)  where  en- 
demic cases  in  man  have  never  been  reported. 
INJURY   TO   HOST 

There  appears  to  be  no  evidence  that  the  guinea  worm  appro 
ciably  injures  its  host  during  tlu-  developmental  period  in  the 
deep  connective  tissues.  Just  before  the  female  worms  reach 
the  skin  they  secrete  toxins  which  produce  general  symptoms 
such  as  urticaria,  nausea,  vomiting,  diarrhoea,  severe  dys]Hiea, 
and  syncope.  These  symptoms  disapjjoar  after  the  worms  have 
established  an  opening  through  the  skin.  Later  injury  to  the 
host  is  produced  by  secondary  infection  and  by  tissue  reactions 
to  the  worms  liefore  and  after  their  deatli.  Severe  inflammation 
is  produced  if  the  worms  are  broken  in  the  tissues  and  the 
embryos  freed.  The  iiresence  of  the  guinea  worms  may  also 
produce   permanent   joint    injuries    (Pradhan,   liiHO). 

Tn  endemic  areas  dracontiasis  is  often  a  medical  and  public 
health  jiroblem  of  great  importance.  Large  numbers  of  people 
are  iru'apacitated  for  3  to  <i  months  of  the  year;  severe  sulier- 
ing  and  occasionally  death  are  produced;  and  the  economic  life 
of  the  community  is  often  severely  disturbed.  For  example, 
Moorthy  (1932a)  stated  that  iu  certain  villages  in  the  endemic 
areas  of  Mysore  a  large  jjercentage  of  tlie  people  were  more 
or  less  completely  incapacitated  for  ."i  to  li  months  of  the  year 
and  that  outside  labor  had  to  be  imported.  The  statements  of 
other  authors  indicate  that  this  samp  situation  holds  in  the 
enormous  number  of  villages  in  various  parts  of  India  where 
this  parasite  is  endemic.  Also  over  large  areas  of  Tropical 
Africa  the  guinea  worm  is  a  real  scourge. 

GEOGRAPHICAL  DISTRIBUTION* 

Dracontiasis  is  widely  distributed  in  a  number  of  parts  of 
Tropical  Africa  and  is  endemic  over  large  areas  of  India.  It 
is  also  found  in  Arabia,  Iran,  Afganistan,  and  Russian  Tur- 
kestan. It  is  supposed  to  have  been  introduced  into  the  West- 
ern Honiisphere  with  slaves  from  the  Gulf  of  Guinea.  It  was 
formerly  thought  to  have  become  endemic  in  Curacao,  Demerara, 
and  Surinam  but  seems  now  to  have  disajipeared;  it  is  only  in 
a  limited  region  in  the  state  of  Bahia,  Brazil,  that  it  is  still 
endemic.  There  is  other  evidence  that  the  guinea  worm  is  not 
easily  spread  to  new  regions.  Although  it  has  been  constantly 
introduced  into  the  Dutch  East  Indies  it  apparently  has  never 
been  establislied  (Brug,  1930)  and  no  evidence  was  found  of 
endemic  centers  along  the  north  coast  of  Africa  and  in  southern 
Europe. 

In  Africa  are  located  the  most  widespread  and  perhaps  the 
worst  endemic  areas  of  guinea  worm  infection  in  the  world. 
In  general  it  can  be  said  that  almost  all  the  important  endemic 
centers  in  Africa  are  north  of  the  equator  and  south  of  the 
Tropic  of  Cancer.  In  West  Africa  they  are  in  general  scat 
tered  from  Mauritania  to  Gabun,  especially  in  Mauritania. 
Senegal,  Upper  Volta,  Ivory  Coast,  Gold  Coast  and  Northern 
Territories,  Togo,  Dahomey,  Nigeiia,  and  Cameroon.  East  of 
this  region  endemic  areas  are  known  especially  East  of  Lake 
Chad,  over  much  of  the  southern  part  of  the  Anglo-Egyptian 
Sudan  and  in  Uganda. 

In  Arabia  the  guinea  worm  is  present  along  the  shore  of 
the  Bed  Sea  and  in  some  places  in  the  interior;  it  is  endemic 
in  certain  jiarts  of  Russian  Turkestan,  Afganistan,  and  in  Iran 
it  appears  to  be  almost  entirel.v  limited  to  certain  towns  and 
villages  in  the  province  of  Laristan,  wiiicli  is  located  in  the 
.south   on   the   Persian   Gulf    (Lindberg,    1930). 

Next  to  Africa  the  real  home  of  the  guinea-worm  is  India. 
Imjiortant  endemic  centers  in  this  country  are  limited  to  the 
western  half  of  the  peninsula,  little  infection  being  found  east 
of  Delhi  and  the  Central  Provinces.  In  Rajputana  and  Central 
India  the  infection  exists  almost  everywhere  except  in  a  few 
desert  regions;  in  the  Central  Provinces  it  is  prevalent  in  all 
the  districts  except  a  few  on  the  eastern  side;  in  the  Bombay 
Presidency  it  is  widely  distributed  except  in  the  sea  coast 
area  south  of  Bombay;  in  the  iladras  Presidency  it  is  preva 
lent  except  for  a  few  districts  on  the  western  coast;  in  Hydera- 
bad 9  out  of  16  districts  liave  the  infection;  in  Mysore  it  is 
practically  limited  to  one  district  in  the  north  ;  it  is  also  pres- 
ent but  with  lower  incidence  in  the  valle.v  of  the  Indus  and 
the  Northwest  Frontier  Provinces;  elsewhere  in  western  and 
central   India   there  are  a   few  limited  centers. 


*Infortnation  gathered  by  questionn.iires  and  suniiiied  up  in  a  recent 
work  by  E,  B.  lIcKinley  (]9;^5)  suppleniented  the  numerous  luiblica- 
tions  found  in  the  lite  ature  on  the  distril)Ution  of  dracontiasis  in  vari- 
ous parts  of  the  wfirld.  A  personal  communication  from  Dr.  V.  N. 
Moortb\'    gave  ^the   latest    information    on    India. 


'I'hcn'  are  certain  general  iioints  of  iiitori'st  in  regard  to  the 
geogra|ihical  distribution  of  dracontitisis.  It  extends  from  the 
tropics  in  -Xfrica  and  southern  liuiia  well  up  into  the  tem- 
perate zone  in  Russian  Turkestan,  Afgaiii.stan.  .and  the  innth- 
western  frontier  i)roviiK'es  of  India.  Even  where  it  is  wide- 
spread .as  in  tropical  .\frica  north  of  the  e(iuator  and  in  west- 
ern and  ccntr;il  India,  its  distribution  is  very  discontinnous,  and 
importtmt  endemic  centers  are  often  separated  by  wide  areas 
where  it  is  not  present.  In  limited  regions  too  its  distribution 
is  very  si)otted.  In  Mysore,  for  examide,  the  infection  is  al- 
most entirely  limited  to  the  Chitaldrug  district,  and  in  this 
district  itself  there  w-as  only  a  small  iiroiiortion  of  infected 
villages  which  are  widely  scattered  (Moorthy,  193:ia).  The 
same  spotted  distribution  has  been  noted  by  other  authors  in 
the  other  endemic  areas  of  India.  The  same  type  of  distribution 
has  been  noted  by  vari(uis  workers  in  different  parts  of  Africa, 
where  guinea  worm  villages  may  be  close  to  others  where  the 
parasite  is  absent.  It  has  also  been  noted  that  in  an  infected 
village  itself  only  part  of  the  families  suffer.  Even  more  sur- 
prising is  the  point  emphasized  by  Moorthy  (1932a)  and  Trewn 
(1937)  that  in  infected  families,  where  there  appear  to  be  no 
differences  in  habits,  some  Individuals  will  remain  entirely  free 
from  infection.  All  these  peculiarities  of  distribution  suggest 
that  the  factors  involved  in  the  dissemination  of  the  guinea 
worm  are  very  complicated. 

EPIDEMIOLOGY 

In  general  it  may  be  said  that  the  guinea  worm  can  only 
spread  where  infected  individuals  wade  or  bathe  in  drinking 
water  in  which  Cyclops  are  present.  While  most  of  the  endemic 
areas  are  in  hot  countries  there  is  no  evidence  that  tempera- 
ture per  se  is  a  determining  factor.  This  parasite  is  chiefly 
prevalent  in  regions  where  there  is  a  low  annual  rainfall.  This 
seems  to  be  related  to  the  fact  that  in  such  regions  the  people, 
during  at  least  part  of  the  year,  are  forced  to  depend  for  their 
drinking  water  on  open  pools,  wells,  or  cisterns  in  which  the 
population  of  Cyclops  becomes  concentrated.  In  a  personal 
communication  Dr.  V.  N.  Moorthy  recently  made  the  follow- 
ing statement  in  regard  to  the  distribution  of  dracontiasis  in 
India:  "The  most  significant  fact  to  note  in  this  distribution 
is  that  the  intensity  of  infection  appears  to  vary  directly  with 
the  scarcity  of  water  supply  during  the  season  of  infection. 
In  provinces  like  Bengal  and  Assam  where  there  is  a  plentiful 
supply  of  water  all  through  the  year  dracontiasis  hardly  exists 
at  all."  Roubaud  (1913)  and  others  have  also  pointed  out 
that  in  the  forested  regions  of  west  equatorial  Africa  where 
the  rainfall  is  abundant,  as  the  lower  Ivory  Coast  and  the 
Congo   Basin,  guinea   worm   has  not   been   observed. 

A  number  of  authors  have  noted  a  seasonal  relation  in  guinea 
worm  infection.  Since  the  development  of  the  worms  takes 
about  a  year,  the  yearly  period  when  the  people  are  suffering 
from  the  disease  coincides  with  the  conditions  most  favorable 
for  its  transmission.  In  India  the  outbreaks  are  almost  en- 
tirely limited  to  the  first  half  of  the  year  with  most  of  the 
infection  coming  in  March,  April,  and  May.  This  is  the  driest 
season  just  before  the  Monsoon.  In  Dahomey,  Roubaud  (1913) 
found  the  disease  most  frequent  also  in  the  driest  months  of 
the  year  which  are  from  December  to  February.  The  same 
author  noted,  however,  that  in  the  endemic  areas  of  the  Lake 
Chad  region  it  occurs  almost  entirely  in  the  rainy  season, 
which  is  in  the  middle  of  winter.  He  explains  this  by  the  use 
during  this  period  of  water  from  little  cisterns  and  pools 
which  are  temporarily  filled.  Davis  (1931)  lujted  that  epi- 
demics of  dracontiasis  occurred  in  southern  Sudan  during  the 
rains  from  April  to  June.  In  Iran,  Lindberg  (193(3)  found 
the  season  of  infection  to  be  from  March  to  August  with  the 
maximum  in  June,  which  are  the  hottest  months  of  the  year 
just  after  the  rainy  season.  It  is  evident,  therefore,  that  the 
seasonal  incidence  of  dracontiasis  varies  greatly  in  different 
endemic  areas  and  is  related  to  the  water  supply  of  the  people 
and  not  to  general  climatic  conditions. 

Little  significant  information  is  available  on  the  relation  of 
the  distribution  of  the  various  species  of  cyclops  to  the  epi- 
demiology of  dracontiasis.  These  copepods  are  widely  dis- 
tributed over  the  world  and  immerous  species  occur  wherever 
they  are  found.  In  general,  therefore,  it  seems  possible  that  in 
most  regions  ivhere  the  guinea  worm  would  be  introduced  and 
where  the  human  habits  are  favorable  for  its  spread,  suitable 
intermediate  hosts  would  be  present.  Only  certain  species  of 
cyclops  can  serve  as  intermediate  hosts.  Chatton  (1918)  tried 
to  infect  four  different  species  of  Cyclops  in  Tunis  with  larvae 
from  introduced  cases.  One  of  these,  Cyclops  macrnrus,  was  en- 
tirely refactory  to  infection.  In  three  others,  C.  viridis,  C. 
prasiniis,  and  an  undetermined  species,  the  larvae  were  ingested 
and  penetrated  into  the  body  cavity  but  failed  to  develop  al- 
though they  remained  alive  for  from  40  to  .10  days.  In  India, 
Lindberg    (193:"i)    fouiul    that   C.    multicolor   dies   quickly   after 


321 


ingesting  guinea  noira  larvae  and  noted  no  development  after 
7  days. 

We  know  little  also  of  the  relation  of  the  reactions  of  the 
definitive  host  to  this  dissemination  of  this  parasite.  If  any 
immunity  is  produced  bj'  the  presence  of  worms  it  must  be 
quickly  lost  after  the  completion  of  development  because  re- 
peated infection  of  the  same  individual  year  after  year  is  a 
common  phenomenon.  Moorthy  (lS32a)  recorded  that  out  of 
a  total  of  1,363  patients  suffering  from  draeontiasis  83  per- 
cent gave  histories  of  having  suffered  in  previous  years.  He 
also  noted  that  certain  individuals  seem  to  be  entirely  lacking 
in  susceptibility  to  infection  and  escape  the  disease  year  after 
year,  although  they  live  in  the  same  houses  and  drink  the  same 
water  as  those  who  become  infected.  He  suggested  from  in 
vitro  studies  that  in  such  individuals  there  might  be  physiologi- 
cal factors,  such  as  hypo-  or  hyperchlorhydria,  which  would 
prevent  the  freeing  of  the  infective  larvae  from  the  cyclops  in 
the  stomach  or  which  would  kill  them  before  they  could  pene- 
trate into  the  tissues. 

As  suggested  above,  the  character  of  the  water  supply  is 
of  the  greatest  importance  in  the  dissemination  of  draeontiasis. 
Infected  individuals  must  have  access  to  drinking  water  that 
contains  suitable  species  of  Cyclops.  Absence  of  this  parasite 
in  people  who  obtain  their  water  supply  from  rivers  or 
smaller  streams  can  probably  be  attributed  to  the  absence  or 
scarcity  of  the  proper  species  of  Cyclops  (Lindberg,  ISS.j). 
Small  open  collections  of  water  such  as  step  wells,  cisterns, 
or  small  pools  in  which  the  people  frequently  wade  or  bathe 
are  chiefly  implicated.  For  example,  in  the  Gold  Coast 
surface  collections  of  rain  water  and  shallow  open  wells 
are  considered  to  be  the  sources  of  infection  (Leiper,  1907)  ; 
in  the  upper  Volta,  village  ponds  and  hollows  made  by  the 
natives  in  obtaining  mud  for  building  their  huts  (LeDentu, 
1024)  ;  in  the  Lake  Chad  basin,  temporary  cisterns  or  pools 
(Roubaud,  1913)  ;  in  southern  Sudan,  shallow  wells  or  drink- 
ing pools  (Davis,  1931);  in  Iran,  cisterns  of  rain  water 
(birkehs)  or  washing  basins  in  the  mosques  (Lindberg,  1936)  ; 
a,nd  in  India,  the  step  wells  and  village  pools  (Turkhud,  1919; 
Pradhan,  1930;  Moorthy,  1932a:  Lindberg,  1936).  Such  bodies 
of  water  only  become  of  considerable  danger  in  spreading  the 
infection  when  the  water  is  low  and  the  Cyclops  are  present  in 
large  numbers  and  concentrated  near  the  surface  (Turkhud, 
1912;  Pradhan,  1930;  Lindberg,  193.i).  This  explains  the  sea- 
sonal cycle  of  infection  in  India  because  the  season  of  great- 
est infection  (March  to  May)  is  near  the  end  of  the  dry  sea- 
son when  the  water  is  lowest.  It  also  explains  the  greater 
prevalence  of  guinea  worms  in  those  villages  with  the  poorest 
water  supply.  The  epidemiological  data  makes  clear  the  diffi- 
culty that  the  guinea  worm  has  in  finding  conditions  in  human 
populations  suitable  for  its  spread  and  goes  far  to  explain 
the  discontinuity  of  the  endemic  centers,  the  failure  of  the 
disease  to  spread  readily  into  new  territory,  and  its  spotted 
distribution  over  the  endemic  areas.  All  these  facts  on  epidem- 
iology suggest  obvious  methods  for  control  and  indicate  that 
any  serious  attempt  to  apply  control  measures  should  bring 
rapid  and  permanent  results. 

CONTROL 

It  is  obvious  that  prophylaxis  and  control  of  draeontiasis  in 
the  endemic  areas  can  either  deal  with  habits  of  the  individual 
or  with  community  relations  to  the  water  supply.  Boiling,  filter- 
ing, or  even  straining  the  drinking  water  through  a  cloth  would 
be  effective  in  individual  protection.  The  rapid  extraction  of 
the  gravid  worms  from  infected  individuals  and  their  exclu- 
sion from  the  water  supply  would  help  in  preventing  the  in- 
fection of  the  C3-clops.  However,  all  the  workers  who  have 
considered  the  problem  are  in  agreement  that  permanent  con- 
trol in  an  infected  community  can  be  achieved  only  by  chang- 
ing the  water  supply  to  eliminate  sources  of  infection.  Thus 
Leiper  (1907)  pointed  out  that  on  the  Gold  Coast  the  fencing 
of  the  pools,  the  building  of  parapets  or  covering  the  open 
wells,  and  the  digging  of  draw  wells  would  permanently  elimi- 
nate the  disease.  Turkhud  (1919)  argued  that  the  changing 
of  all  step  wells  in  the  infected  villages  in  India  to  draw 
wells  would  save  many  times  the  cost  of  the  pumps  by  eliminat- 
ing the  economic  losses  from  the  disease.  Moorthy  (1932b) 
found  that  where  this  was  done  in  the  Chitaldrug  "district  of 
Mysore  great  reduction  and  in  some  cases  entire  elimination 
of  the  disease  resulted. 

Where  for  some  reason  it  is  not  possible  to  change  the  coii- 
struction  of  the  wells  or  pools  the  employment  of  methods  to 
kill  the  Cyclops  have  been  suggested.  Such  measures  have  to 
be  used  repeatedly  since  they  serve  only  to  eliminate  the  Cy- 
clops temporarily.  A  number  of  authors  have  experimented  on 
the  use  of  chemicals  to  kill  cyclops.  Davis  (1931)  recom- 
mended lime,  either  unslaeked  or  slacked,  in  proportions  of  1 
to    1,000.    In   fact   in   the   previous   year   Pradhan    (1930)    had 


already  reported  an  extensive  lield  experiment  in  which  the 
use  of  lime  (about  1  drachm  per  gallon  of  water)  in  27  in- 
fected step  wells  had  reduced  the  incidence  of  guinea  worm  in 
the  people  using  them  21  to  -l-j  percent.  Moorthy  (1932b)  re- 
ported that  when  perchloron  (3  lbs.  per  100,000  gallons)  in 
combination  with  copper  sulphate  (1  lb.  per  200,000  gallons) 
was  used  in  wells  they  could  be  rendered  completely  free  of  cy- 
clops for  about  a  month.  He  advocated  the  use  of  this  method 
during  the  infection  period  (March  to  June)  as  a  good  method 
of  reducing  the  number  of  cases  in  areas  where  permanent  con- 
trol methods  could  not  be  undertaken. 

Several  authors  have  suggested  the  "biological  control"  of 
guinea  worm  infection  by  the  introduction  into  the  wells  or 
ponds  of  fish  that  feed  on  cyclops,  but  Moorthy  and  Sweet 
(193fic)  appear  to  have  been  the  first  to  report  on  the  success- 
ful use  of  this  method.  They  found  a  number  of  cases  in 
which  people  using  wells  containing  certain  species  of  small  fish, 
particularly  of  the  genus  Barbus,  were  entirely  free  from  guinea 
worm  infection.  This  led  to  the  development  of  methods  for 
raising  and  introducing  fish  into  the  step  wells.  Use  of  this 
control  method  in  3.")  infected  villages  in  1934  and  193-5  caused 
complete  elimination  of  draeontiasis  in  six  and  a  marked  reduc- 
tion in  four.  Their  results  led  to  the  conclusion  that  the  use 
of  fish  was  not  only  cheaper  but  much  more  effective  than  chemi- 
cal methods. 

Finally  it  seems  clear  from  all  the  evidence  in  the  literature 
that  prospects  for  the  control  of  draeontiasis  are  excellent  in 
any  endemic  area  where  a  systematic  effort  can  be  made.  It 
is  very  encouraging  that  Moorthy  and  Sweet  (1936b)  were  able 
to  report  that  from  1S29  to  1936,  by  the  introduction  of  draw 
wells,  the  use  of  chemicals,  and  the  introduction  of  fish,  dra- 
eontiasis was  entirely  eliminated  from  all  but  25  of  112  in- 
fected villages  in  the  Chitaldrug  district  of  Mysore,  India. 

Enterobius  vermicularis 
E.  B.  C. 

The  human  pinworm  or  seatworm,  Enterobius  rermiciilaris 
(Linn.,  17."iS)  Leach,  in  Baird,  18.13,  was  one  of  the  first  of 
the  intestinal  helminths  to  be  described  from  man,  a  fact  easily 
understood  since  it  comes  to  the  exterior  and  there  produces 
local  sj-mptoms  which  would  lead  to  its  discovery.  According 
to  Schmidt,  it  was  discussed  by  Hippocrates,  Aristotle,  Galen 
and  others  under  the  name  Ascaris,  before  Linnaeus  gave  it  its 
specific  name. 

E.  vermicularis  is  apparently  restricted  to  man.  In  view  of 
Cameron's  (1929)  study  indicating  that  in  primates  one  species 
of  Enterobius  is  restricted  to  hosts  of  one  genus,  reports  of  E. 
vermiculari.<i  from  primates  other  than  man  must  be  regarded 
with  suspicion  unless  supported  by  unimpeachable  evidence. 
This  parasite  occurs  in  the  intestine  but  is  not  limited  in  loca- 
tion as  are  many  other  intestinal  nematodes.  It  occurs,  in  va- 
rious stages  of  development,  from  the  lower  ileum  through  the 
rectum  and  gravid  females  migrate  through  the  anus  to  the 
perianal  region  to  lay  eggs. 

SYMPTOMATOLOGY  AND  PATHOLOGY 

Symptoms  are  extremely  variable  in  nature  and  degree  being 
apparentlj'  absent  in  some  cases  and  severe  in  others.  There  is 
mechanical  stimulation  and  irritation  of  the  gastrointestinal 
tract,  occasionally  with  nausea  and  vomiting,  and  of  the  ex- 
ternal surfaces  during  migration,  producing  pruritus  ani  and 
vulvae,  in  some  cases  apparently  allergic  in  nature  (Brady  and 
Wright,  1939).  By  transporting  organisms  during  migrations, 
the  parasites  may  induce  vaginitis  and  even  peritonitis  and  may 
cause  the  formation  of  cysts  in  the  female  genital  tubes  or  in 
the  peritoneal  cavity,  with  resulting  irritation  (summarized  by 
Africa,  1938).  Probably  there  is  slight  eosinophilia.  The  role 
in  appendicitis  is  debatable  (Bachman,  193.5;  Driiner,  1921; 
Penso,  1939;  and  others)  but  worms  apparently  may  give  rise 
to  the  .syndrome  of  appendicitis  without  characteristic  histo- 
logical changes  (Botsford,  Hudson  and  Chamberlain,  1939). 
Restlessness  and  others  secondary  effects  in  behaviorism,  in- 
cluding scholastic  difficulties,  feeling  of  shame  and  poor  social 
attitude,  may  be  pronounced. 

DIAGNOSIS 

The  most  reliable  method  of  diagnosis  is  by  the  microscopic 
detection  of  eggs  in  scrapings  made  from  the  perianal  region. 
This  technique  has  been  standardized  by  the  use  of  a  cellophane- 
tipped  swab  (Hall,  1937;  Folan,  193"9),  known  as  the  NIH 
(National  Institute  of  Health)  swab  (Fig.  201)  ;  the  cellophane 
is  detachable  for  mounting  and  examination  under  the  micro- 
scope. Swabs  should  be  made  during  the  night  or  first  thing 
in  the  morning,  preferable  on  at  least  7  days  if  first  results 
are  negative. 


322 


ruiber  st^pnf 


*—  Tmst  tube 


-  Rubber  band 


v_y 


Kig.  201. 
N-I-H  swab   (National  Institute  of  Health)    for  the  detection  of  Ente- 
robius  infections. 


T.Mii.K  11. — IiifiiUiicc  of  Jiiitcrbiiis   vcrmiculan.'i 
By  use  of  various  kinds  of  swabs  and  scrapers 


Date 

published  Country 


Population 
group     Race 


Age 


No. 
e,\am. 


No. 
posi- 
tive 


posi- 
tive 


1886- 

Germany 

Children 

W 

Under  IB  3,.")06 

2,068 

59 

1925 

Militia 

W 

Adult            -too 

76 

19 

1926- 

U.S.S.R. 

Various 

\v 

All              7,074 

4,255 

GO 

1931 

1933- 

Sweden 

.\svluni 

w 

?                       60 

42 

70 

1936 

('liildrcii 

w 

Under  1.1      340 

123 

36 

1905- 

Finland 

Various 

w 

All              2,7.13 

81 

3 

1911 

Children 

w 

Under  16      300 

95 

32 

1935- 

U.S.A. 

Ment.  hosp 

.w 

15-60             282 

62 

22 

1937 

Boys  inst. 

w 

12-20             213 

3 

1.4 

Boys  inst. 

N 

J2-20             187 

3 

l.(> 

Summary 

1886- 
1937 

5  countries  Various   Mostly  All           15,115     6,808     45 
groups      white 

By  use  of  NIH  swab — Institutionalized  persons 

Date 
pub- 
lished 

No.      %         Swabs 
No.    posi-  posi-         per 
Locality    Race    Age     Sex    exam,  tive    tive        person 

U 

nited  Stata 

1937 

D.  C. 

N 

14-20     F 

23 

0 

0 

1 

W 

14-20     F 

4 

0 

0 

1 

1939- 

40 

Louisiana 

W 

6-14    MF 

365 

302 

83 

7 

N 

6-14     M 

63 

53 

84 

7 

N 

6-14     F 

63 

10 

16 

1 

1939 

Alabama 

W 

All       M 

384 

317 

S3 

(2  or 

W 

All       F 

2.53 

98 

39 

more) 

1941 

Georgia 

w 

Adults  F 

100 

31 

31 

av.  2.9 

w 

Adults  F 

65 

52 

80 

6 

1941 

D.  C. 

w 

6-8       M 

17 

14 

82 

4 

1941 

Puerto  Rico 

■» 

5-19     M 

52 

6 

12 

4 

* 

6-19     F 

50 

15 

30 

4 

1940 

Canada 
Toronto         W 

2  14    MF 

140 

98 

70 

av.  3.7 

Smnmary 

1937- 
1941 

6  localities  WN 
N.  America 

All       MF 

1,579 

996 

63 

1  to  7 

Fig.  202. 
Egg  of  Enterohiiis  vermirularis. 

EPIDEMIOLOGY 

Critical  investigations,  based  on  examination  of  perianal 
scrapings,  have  been  made  in  European  countries,  in  the  United 
States,  including  Puerto  Rico,  in  Canada,  and  in  the  Philippines. 
The  results  of  these  investigations  are  summarized  in  table  11. 
These  results  show  that  examinations  of  22,376  persons  revealed 
pinworm  infections  in  9,703  persons,  or  43   percent. 

Additional  studies,  differing  in  method  or  scope  and  not 
shown  in  table  11,  include  .stool  examination  of  495  children  of 
preschool  age  in  Brazil  (Moniz  de  Aragao,  193S)  ;  E.  venni- 
ctdaris  was  found  in  49  percent,  an  extremely  high  figure  con- 
sidering the  method  of  diagnosis.  In  Spain,  Darriba  and  de 
Cardenas  (1935),  from  examination  of  feces,  anal  scrapings, 
finger  nails  and  nasal  mucus,  found  11  of  46  children,  or  34 
percent,  infected  with  pinworms;  in  Greece,  Pandazis  (1937) 
reported  pinworms  in  28  percent  of  infants  and  6  percent  of 
adults,  apparently  from  fecal  examination  supplemented  by 
finger  nail  examination. 

FACTORS  INFLUENCING  PREVALENCE 

R.\cE.  As  noted  previously,  the  Negro  race  has  shown  a 
lower  incidence  than  the  white  race.  Although  Sawitz,  D'An- 
toni,  Rhude  and  Lob  concluded  from  a  small  group  of  boys  of 
the  same  ages  in  institutions  of  similar  environments  that  the 
incidence  was  almost  identical  in  the  two  races,  the  eonsideralily 
lower  incidence  found  in  Negroes  than  in  white  persons  in  the 
general  population  of  Washington,  D.  C,  is  contrary  to  what 
would  be  expected  if  environmental  conditions  are  the  deter- 
mining factor.  The  significance  of  the  racial  factor  deserves 
further  study;  that  many  persons  classed  as  Negroes  in  the 
United  States  are  mulattoes  should  be  kept  in  mind,  in  this 
connection.  Of  Interest  are  racial  differences  in  the  relative 
frequency  of  pinworms  in  2,317  appendices  removed  surgically; 
the  incidence  was  2.88  percent  for  the  white  population,  10.04 
percent  for  Indians  of  the  United  States,  and  23.91  percent 
for  Eskimos  and  Aleutians. 

Age  appears  significant  only  to  the  extent  that  in  the  general 


By  use  of  NIH  swab — Nouinstitutionalized  persons 


Date 

No. 

% 

Swabs 

pub- 

No. 

posi-  posi- 

per 

lished 

Locality    Race 
United  States 

Age 

Hex 

exam. 

tive    t 

ive 

person 

1937- 

11  D.  C.             W 

All 

MF 

2,895 

1,202 

42 

(Usually 

N 

All 

MF 

1,099 

142 

13 

2  to  4) 

1939 

Sample         W 

12-19 

M 

166 

21 

13 

1 

from  va-      N 

12-19 

M 

137 

0 

4 

1 

rious  parts  W 

12-19 

M 

198 

40 

20 

av.4 

of  U.S.A.     N 

12-19 

M 

105 

9 

9 

av.4 

1940 

Phila.           W  ? 

To  12 

? 

144 

36 

25 

1  to  3 

1941 

Florida         W 

Philippines 

6-12 

MF 

438 

71 

16 

1 

1939 

Manila          W 

Mostly 

500 

376 

75 

1 

6-10 

MF 

Summary 


1937-41  U.S.A.  and  WN 
Philippines 


All       MF    5,682    1,903     33       1  to  4 


'Mixed  group  of  white,  mulatto  and  Negro  persons. 

population  the  incidence  is  highest  in  children  of  school  age, 
next  highest  in  those  of  preschool  age,  and  lowest  in  adults 
(Cram  and  Reardon,  1939;  Chanco  and  Soriano,  1939).  There 
is  evidence  that  the  school  is  the  determining  factor  in  these 
differences;  the  incidence  in  children  of  so-called  "preschool" 
age  who  attended  nursery  schools  has  been  found  as  high  as 
that  in  older  children   (Table  12). 

Sex.  The  incidence  in  males  has  usually  been  found  slightly 
higher  and  in  an  Alabama  institution  was  much  higher,  but  in 
the  Philippines  was  slightly  lower,  than  in  females.  Consider- 
ing both  sex  and  age,  Sawitz  et  al  found  the  peak  of  infection 
at  9  years;  after  that  there  was  a  drop  in  incidence  in  females, 
probably  correlated  with  stricter  sanitary  habits,  whereas  in 
males  the  incidence  remained  relatively  constant  up  to  15  years 
of  age. 

The  factor  of  crowding  is  important  in  the  spread  of  pin- 
worms.    The  familial  nature  of  the  infection  has  been  empha- 


323 


si/.ed  (Schmidt,  IIIU;  Loiitze,  lilST);  Wright  and  Cram,  11)37; 
Hall  and  Cram,  193!)).  From  a  study  of  about  300  piinvorm- 
infected  families  in  Washington,  D.  C,  it  was  apparent  that 
multiple  eases  are  the  rule  rather  than  the  exeeption  and  that 
frequently  all  the  children  of  the  family,  and  one  or  both  par- 
ents, may  be  infected.  Bozicevich  and  Brady  (1938)  found  a 
correlation  between  the  size  of  the  family  and  the  incidence 
of  Enterobiiis,  easily  explained  in  that  the  larger  the  number  of 
persons  in  a  family,  the  more  chance  there  is  for  introduction 
of  the  infection  into  the  household  and,  once  introduced,  the 
easier  its  spread,  the  infection  increasing  in  a  geometrical,  not 
an  arithmetrical  rate.  Under  institutional  conditions  Sawitz 
et  al  found  the  incidence  of  infection  much  lower  among  chil- 
dren  occupying  rooms  with  one  or  two  beds  than  where  larger 
groups  were  quartered  in  dormitories.  Families  with  pinworm 
infections  are  found  most  numerous  in  older,  comparatively 
congested  residential  sections  but  are  by  no  means  confined  to 
those  sections  (Cram  and  Reardon,  1939);  the  social-economic 
status  is  not   limited  to  any  one  level. 

T.\BLE  12. — liwicJeticc  of  Enterobiiis  vermicidaris  according  to 
age  and  race  of  children  in  camps  and  iiiirxirii  sclioolt:. 


Reported  by 


Waxhington.  D.  C. 
Race  Age 


Xum-    %     Swabs 
ber    posi-     per 
.Sex  exam,  five   person 


Bozicevich  White'  6-18  M       230     31         1 

Bozicevich  &  Bradv  White'  618  M        504     57      2  4 

Cram  White  (Jewish)' 6-12  MF     147     25         4 

Negro"  6-12  MF       63     21         4 

Ciam  &  Nolan  White"  2-  5  MF       91    -55  av.  9 

Cram  White"'  2-  5  MF      62     52         4 

Negro' 2-  5  MF 68 ^19 4  _ 

'Camps.     "Private  nursery  school.     'Public  nursery  schools. 


CONTROI. 

Control  of  pinworm  infection  is  extremely  difficult.  The 
number  of  eggs  deposited  may  be  enormous,  one  worm  being 
capable  of  producing  from  5,000  to  17,000  eggs  (Reardon, 
1938),  and  the  time  of  development  of  eggs  on  the  skin  of  the 
perianal  region  is  short,  as  little  as  6  hours.  The  infected 
individual  may  contaminate  the  hands  while  scratching  or  when 
using  the  toilet  and  subsequently  carry  the  eggs  to  the  month 
or  may  contaminate  other  objects.  Eggs  which  fall  off  of  the 
person  develop  more  slowly,  depending  on  temperature  and 
humidity;  they  can  pass  through  cloth  and  there  is  considerable 
evidence  that  airborne  infection  is  a  possiliility  (Lentze,  1932; 
Oleinikov,  1929;  Nolan  and  Reardon,  1939;  Sondak,  1935). 
In  households  and  schools  with  infected  members  pinworm  eggs 
have  been  found  in  dust  from  a  large  variety  of  locations  and 
objects  at  various  levels.  The  eggs  may  float  on  the  surface 
of  water  and  a  certain  proportion  would  therefore  remain  on 
the  sides  of  wash  bowls,  bath  tubs,  laundry  tubs  and  similar 
containers  when  they  are  emptied. 

The  eggs  are  very  resistant  to  i)h3-sical  and  chemical  agents. 
Temperature  and  humidity  influence  the  length  of  their  sur 
vival.  Lentze  (1935)  found  that  a  temperature  of  55°  C.  and 
above  killed  the  eggs  in  a  few  seconds;  at  the  optimum  tempera- 
ture (36°  to  37°  C.)  on  a  damp  base,  as  on  the  human  skin, 
especially  under  the  nails,  eggs  survived  for  about  10  days. 
Jones  and  Jacobs  found  that  temperatures  above  28°  C,  with 
humidities  below  50  percent,  detinitely  aft'ect  the  eggs  within 
24  hours;  less  than  10  percent  of  eggs  survived  after  2  to  3 
hours  and  none  survived  after  16  hours  at  a  temperature  of  3))° 
to  37°  C.  and  relative  humidity  of  38  to  41  percent.  On  the 
other  hand,  at  lower  temperatures,  20°  to  24%°  C,  and  higher 
humidity,  62  to  91  percent,  30  percent  of  eggs  survived  6  days; 
on  water  at  3°  to  5°  C.  a  maximum  of  93  percent  survived  18 
days.  According  to  Sondak  (1935),  eggs  were  still  viable  after 
drying  at  room  temperatures  averaging  10°  to  12°  C.  for  3 
weeks  but  not  viable  after  35  days.  Exposure  of  eggs  to  mea- 
sured quantities  of  monochromatic  ultraviolet  radiation  (Hol- 
laender,  Jones  and  Jacobs,  1941 ;  Jones,  Hollaender  and  Jacobs, 
1941)  showed  an  increased  sensitivity  of  the  eggs  at  wave- 
lengths below  2400A.  As  regards  the  effect  of  chemicals,  Son 
dak  (1935)  found  that  eggs  were  not  killed  by  formalin  in 
strengths  of  1,  2,  5,  and  10  percent;  by  corrosive  sublimate 
1:1,000;  by  saturated  solution  of  corrosive  sublimate  and  cop- 
per (eupric  sulphate)  ;  by  5  percent  antif  ormin ;  by  1  and  2 
percent  solutions  of  carbolic  acid  or  by  1,  2,  and  5  percent 
lysol  solutions,  but  they  were  killed  by  5  percent  carbolic  acid 
and  by  10  percent  lysol. 

Because  of  the  large  numbers  of  eggs  scattered  by  an  infected 
individual  and  because  of  the  resistance  of  the  eggs,  hygienic 
measures  alone  can  not  be  relied  upon  to  control  the  spread  of 


pinworm  infection.  This  was  pointed  out  by  Wright  and  Cram 
(1937)  and  was  given  a  practical  demonstration  by  D'Antoni 
and  Sawitz  (1940)  who  put  in  force  a  vigorous  cleanliness  pro- 
gram for  (i  weeks  in  one  of  the  institutions  studied  by  them; 
at  the  end  of  that  period  swab  examination  showed  an  increase 
from  38  percent  to  51  percent  in  incidence  of  pinworms.  The 
greatust  promise  for  control  lies  in  medicinal  treatment  admin- 
istered over  a  period  which  is  sufficiently  long  to  cover  the 
period  of  survival  of  eggs  in  the  surroundings,  tlms  preventing 
reinfection  of  the  individual. 

Bibliography 

THE  HOOKWORMS 

ACKERT,  J.  E.  1924. — Notes  on  the  long.nity  and  infectivity  of 
hookworm  larvae.     Am.  J.  Hyg.,  v.  4(3)  :222-225. 

AcKERT,  J.  E.  and  Payne,  F.  K.  1923. — Investigations  on  the 
control  of  hookworm  disease.  XII.  Studies  on  the  occur- 
rence, distribution  and  morphology  of  Necafor  sitHlus  in- 
cluding descriptions  of  other  species  of  Xceator.  Am.  J. 
Hyg.,  V.  2(l):l-25,  pis.   1-2. 

Andrews,  J.  1940. — Hookworm  disease  and  plans  for  its  con- 
trol in  Georgia.  The  (Tcorgia  Malaria  Bull.,  Hookworm 
Suppl.,  V.  3(2):64-77. 

AsHFORD,  1!.  K.  and  Gutierrez  loARAvroEZ,  P.  1911. — Un- 
cinariasis (hookworm  disease)  in  Porto  Rico;  a  medicinal 
and  economic  problem.  U.  S.  61st  Cong.,  3d  Sess.,  Senate 
Doc.  808,  335  pp.,  pis.  and  figs. 

AuiiUSTlNE,    D.    L.      1922a. — Investigations    on    the    control    of 

hookworm  disease.     VIII.     Experiments  on   the  migration 

of  hookworm  larvae  in  soils.     Am.  J.  Hyg.,  v.  2(2)  :  162-171. 

1922b. — Idem.      IX.   On    the   position   of   the   infective 

hookworm  larvae  in  the  soil.     Ibid.,  v.  2(2)  :172-176. 

1922c. — Idem.  X.  Experiments  on  the  length  of  life 
of  infective  hookwurm  larvae  in  soils.  Ibid.,  v.  2(2):]i7- 
187. 

1923a. — Idem.  XIX.  ObservatioTis  on  the  completion 
of  the  second  ecydvsis  of  Xeeafor  uincricanKS.  Ibid.,  v. 
3(3):280-2f.5,  figs.  i-9. 

1923b. — Idem.  XXII.  Further  obseivations  on  the 
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in  the  soils.     Ibid.,  v.  3(4):   416-419. 

1923c. — Idem.  XXIII.  Experiments  on  the  factors 
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Augustine,  D.  L.  and  W.  G.  Smillie.  1926. — The  relation  of 
types  of  soils  of  Alabama  to  the  distriliution  of  hookworm 
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Babrmanx,  G.  1917a. — Eine  einfache  Methode  zur  Auffindung 
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Geneesk.  Lab.  Waltevrededen,  Fecst  bund  i,  Batavia,  pp. 
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1917b.— Ueber  .\nkylostoiniasis,  deien  .\usbreitung3- 
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Barnes,  M.  E.  and  O'Brien,  H.  R.  1924.— Final  report  on 
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14(3):733-744;  v.  14(3)  :745-7.i9 ;  v.  14(3)  :761-773 ;  v. 
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1926. — Idem.  Part  V.  Tea  estates  of  Assam  and  Ben- 
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1928. — Idem.  Part  XII.  General  summary  and  con- 
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324 


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325 


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328 


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Harlev,  G.  W.  1932. — A  theory  regarding  the  role  of  insect 
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Stkono,  R.  p.,  Saniwround,  J.  H.,  Bequaert,  J.  C.  and  Ochoa, 
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Strong,  R.  P.,  Hi.ssette,  ,J.,  SANixiRouND,  J.  H.  and  Bequaert, 
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Sweet,  W.  C.  and  Pillai,  V.  M.  1937. — Clearance  of  Pistia 
stratiotrs  as  a  control  measure  for  F.  malayi  infection. 
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Van  den  Berghe,  L.  1936. — Note  preliminaire  sur  la  localisa- 
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TRICHINULLA  SPIRALIS 

.\LICATA,  J.  E.  193H. — A  Study  of  Trichinella  spiralis  in  the 
Hawaiian  Islands.  Pub.  Health  Rpts.,  U.  S.  Pub.  Health 
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Augustine,  D.  L.     1933.— Experimental  trichinosis  in   chicks. 

Science,  n.s.,  v.  78(2035)  :608-609. 
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tests  as  aids  in  diagnosing  trichinosis.     Parasit.,  v.  24(1)  : 

60-86,  fig.  1,  pi.  8,  figs.  1-2. 

Baohman,  G.  W.  1928. — A  precipitin  test  in  experimental 
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1928. — An  intradermal  reaction  in  experimental  trichi- 
niasis.    Ibid.,  V.  2(6)  ; 513-523,  fig.  1,  pi.  1. 

1935. — Helminths  as  agents  of  disease.  Reprinted  from 
"Agents  of  disease  and  host  resistance,"  Chap.  57,  1324- 
1409,  figs.   160-207. 

Baylis,  H.  a.  1929. — A  manual  of  Helminthology,  medical  and 
veterinary.     303  pp.,  200  figs.     London. 

BozicEYiCH,  J.  1939. — Studies  on  trichinosis.  XII.  The  prep- 
aration and  use  of  an  improved  trichina  antigen.  Pub. 
Health  Rpts.,  U.  S.  Pub.  Health  Service,  v.  53(48)  :2130- 
2138,  fig.  1. 

Ch'in,    Yao-Ting.      1937. — Trichinella    infection    in    a    cat    in 

Mukden.     Chinese  Med.  J.,  v.  51:500-501. 
Chitwood,  B.  G.     1930.— [Notes  on  the  esophagus  of  the  Tri- 

chinelloidea.]      J.  Parasit.,  v.  16(3)  :165-166. 
Ferenbaugh,  T.  L.,  Seoal,  L.  and  Schulze,  H.  A.     1938. — A 

trichinosis    epidemic    of    sixty  four    eases.      J.    Am.    Med. 

Assoc,  V.  110:1434-1436,  2  figs. 
Gbigbr,   J.   C.   and   Hobmaier,   M.      1939. — Trichinelliasis   and 

carnivorous  mammals  (Bears).     Calif.  &  Western  Med.,  v. 

51(4):249-250. 

Glazier,  W.  C.  W.  1881.— Report  on  trichinae  and  trichinosis. 
Prepared  under  the  direction  of  the  Supervising  Surgeon- 
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Hall,  M.  C.  1937a.— Studies  on  Trichinosis.  III.  The  com- 
plex clinical  picture  of  trichinosis  and  the  diagnosis  of  the 
disease.  Pub.  Health  Rpts.,  U.  S.  Pub.  Health  Service,  v. 
52(18)  :539-551. 

1937b.— Idem,  IV.  The  role  of  the  garbage-fed  hog 
in  the  production  of  human  trichinosis.  Ibid.,  v.  52(27): 
S37-886,  1  fig. 

1938a. — Idem,  VII.  The  past  and  present  status  of 
trichinosis  in  the  United  States,  and  the  indicated  control 
measures.     Ibid.,  v.  53(33)  :1472-1486. 

1938b. — Idem,  VI.  Epidemiological  aspects  of  trichi- 
nosis in  the  United  States  as  indicated  by  an  examination 
of  1,000  diaphragms  for  trichinae.  Ibid.,  v.  53(26)  :1086- 
1150,  1  fig. 

Hall,  M.  C.  and  Collins,  B.  J.     1937. — Studies  on  trichinosis. 

I.    The  incidence  of  trichinosis  as  indicated  by  post-mortem 

examinations  of  300  diaphragms.    Pub.  Health  Rpts.,  U.  S. 

Pub.  Health  Service,  v.  52(16)  :468-490. 
Kaufman,  R.  E.     1940. — Trichiniasis:   Clinical  considerations. 

Ann.  Int.  Med.,  v.  13(8)  :1433-1460. 
Kerr,  K.  B.     1940.— Public  Health  Aspects  of  the  trichinosis 

problem  in  the  South.    South.  Med.  J.,  v.  33(5)  :511-516. 


329 


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trichinae  as  indicated  by  post-mortem  examination  of  3,000 
diaphragms  from  Washington,  D.  C,  and  ')  eastern  sea- 
board cities.  Pub.  Health  Epts.,  U.  S.  Pub.  Health  Serv- 
ice, v..j6(16)  : 836-8.3."). 

LiCHTERMAN,  A.  and  Kleeman,  I.  1939. — Detection  of  Trichi- 
neUa  infestation  in  hogs  by  the  intradermal  test.  Am.  J. 
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McCoy,  0.  R.  1932. — Experimental  trieliiniasis  infections  in 
monkeys.     Proe.  Soc.  Exper.  Biol.  &  Med.,  v.  30:8.5-86. 

Magath,  T.  B.  1937. — Encysted  trichinae.  Their  incidence  in 
a  private  practice  and  the  bearing  of  this  on  the  inter- 
pretation of  diagnostic  tests.  J.  Am.  Med.  Assoc,  v.  108 
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Matoff,  K.  1936. — Bei  Taulien  auf  entcralcm  Wege  erzengtc 
Muskeltrichinellose.  Rpt.  Tierarztl.  Rundschau,  v.  -12:401- 
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1938. — Zur  Frage  der  Muskeltrichinellose  beim  Ge- 
flugel.  Ztschr.  Infektionskrank.  Haustiere,  v.  5-1(1/2)  : 
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Mauss,  E.  A.  1940. — Transmission  of  immunity  to  TrichincVa 
spiralis  from  infected  animals  to  their  offspring.  Am.  J. 
Hyg.,  V.  32,  Sect.  D   (2):75-79. 

Nelson,  T.  C.  1939. — A  practical  plan  for  the  control  of 
trichinosis.     J.  Parasit.,  v.  25(6)    (suppl.)  :33-34. 

Nolan,  M.  O.  and  Bozicevich,  J.  1938. — Studies  on  trichinosis. 
V.  The  incidence  of  trichinosis  as  indicated  by  post  mortem 
examinations  of  1,000  diaphragms.  Pub.  Health  Rpts.,  V. 
S.  Pub.  Health  Service,  v.  53(17)  :652-673. 

Otto,  G.  F.  and  Abrams,  E.     1939. — Quantitative  studies  on 

the  effect  of  heat  on  trichina   (Tricltinella  spiralis)   larvae. 

Am.  J.  Hyg.,  v.  29,  Sect.  D  (3)  :115-120. 
Pavlov,  P.    1937a. — Eecherches  experimentales  sur  la  trichinose 

des  volailles.     Ann.  Parasit.,  v.  15:   434-439. 

1937b. — Recherches    experimentales    sur    la    trichinose 

des  volailles  et  des  vertebres  a  sang  froid.     Ibid:   440-447. 
1940. — Le  role  de  I'avitaminose  dans  1 'infestation  du 

pigeon  par  le  Taenia  echinococciis  (les  pigeons  ages  sont-ils 

susceptibles   de   servir   d'   hote   an  parasite?).     Bull.   Soc. 

Path.  Exot.,  v.  33(,2):93-96. 
Ransom,  B.  H.     1915. — Trichinosis.     Rpt.  18th  Ann.  Meeting 

IJ.  S.  Live  Stock  Sanit.  Assoc,  pp.  1-19. 

1916. — Effects  of  refrigeration  upon  larvae  of  Trichi- 

nclla  spiralis.    J.  Agric  Res.,  v.  5:819-854. 
Ransom,  B.  H.  and  Schwartz,  B.     1919. — Effects  of  heat  on 

trichinae.     J.  Agric  Res.,  v.  17:201-221. 
Ransom,  B.  H.,  Schwartz,  B.  and  Rafpensperger,  H.  B.   1920. 

— Effects    of    pork-curing    processes    on    trichinae.      U.    S. 

Dept.  Agric  Bull.  880,  37  pp. 

Roth,  H.  1935. — Ein  Beitrag  zur  Frage  der  prenatalen  Trichi- 
neninfection.  Acta  Path.  Microbiol.  Scand.,  v.  12(1-2): 
203-215. 

1936. — Ueber  das  Vorkommen  pranatalen  Trichinenii- 
bertragung  bei  kiinstlich  infizierten  Meerschwein.schen. 
,  Zentralb).  Bakt.   [etc.],  Abt.  1,  Orig.,  v.  136:279-284. 

1938a. — On  the  localization  of  adult  trichinae  in  the 
intestine.     J.  Parasit.,  v.  24(3)  :225-231. 

1938b. — Experimental  studies  on  the  course  of  trichina 
infection  in  guinea  pigs.  I.  The  minimum  dose  of  trichina 
larvae  required  to  i)roduee  infestation  of  the  muscles;  with 
an  account  of  the  jiotential  productiveness  of  the  female 
trichina.     Am.  J.  Hyg.,  v.  28(1)  :85-103. 

1939. — Idem.  II.  Natural  susceptibility  of  the  guinea 
pig  to  experimental  trichina  infection.  Ibid.,  v.  29,  Sect. 
D.  (3):89-104. 

Rubli,  H.  1936. — Trichinose  beim  sumpfbiber,  Myocastor  coij- 
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Sawitz,  W.  1937. — Are  post-mortem  statistics  on  trichinosis 
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1938. — Prevalence  of  trichinosis  in  the  United  States. 
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365-383,  figs.  1-6. 

Schapiro,  M.  M.,  Crosby,  B.  L.  and  Sickler,  M.  M.  1938. — 
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Schwartz,  B.  1938. — Trichinosis  in  swine  and  its  relation- 
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Sobel,  I.  P.  1936. — Sporadic  trichinosis  in  children.  Am.  .T. 
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1940. — Idem.  XIV.  A  survey  of  municipal  garbage 
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ENTEROBR'S  vermicularis 

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Cram,  E.  B.  1940. — Studies  on  oxyuriasis.  XXIV.  Compara 
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Cram,  E.  B.  and  Folan,  J.  P.  1939.— Intestinal  helminths 
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Cram,  E.  B.,  and  Nolan,  M.  O.     1939. — Studies  on  oxyuriasis. 

XIX.  Examinations  of  children  in  a  private  nursery  school 
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330 


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V.  2(1):12  43. 


331 


CHAPTER   IX 

ANTHELMINTIC  MEDICATION  FOR  NEMIC 
DISEASE  OF  DOMESTIC  ANIMALS  AND  MAN 

WILLARD  H.  WRIGHT,  Washington,  D.  C. 

and 

PAUL  D.  HARWOOD,  Ashland,  Ohio 


History 

The  use  of  remedies  for  the  removal  of  worms  dates  far 
back  into  aiiticiuity.  As  primitive  man  became  aware  of  his 
intestinal  parasites  by  observing  the  passage  of  such  a  large 
nematode  as  Ascaris  or  the  proglottids  of  large  cestodes  such 
as  Taenia  saginata  or  Taenia  solium,  he  no  doubt  sought  from 
his  limited  armamentarium  weapons  for  the  removal  of  these 
undesirable  boarders.  Since  most  of  his  medicines  were  de- 
rived from  the  plants  found  in  his  circumscribed  environment, 
he  turned  to  them  for  his  worm  treatments.  He  chose  so  well 
that  derivatives  of  some  of  these  plants  in  one  form  or  another 
are  still  in  use  as  anthelmintics.  Thus  male  fern,  a  frequently 
employed  taeniafuge,  was  known  to  the  early  Greek  physicians, 
if  not  before  them;  Jerusalem  Oak,  Chcnopoditim  anthdininti- 
cuin,  was  used  as  a  worm  remedy  by  the  North  American  In 
dians;  and  a  decoction  of  the  leaves  of  Mallotus  pliilippinrnsis. 
from  which  the  taeniafuge  kamala  is  obtained,  was  employed 
by  the  early  Ethiopians. 

Developments  in  anthelmintic  medication  have  been  divided 
aptly  into  three  epochs:  The  first,  comprising  centuries  of  un- 
critical empiricism;  the  second,  comprising  several  decades  of 
critical  empiricism;  and  the  third  and  last,  comprising  a  rela- 
tively few  years  of  critical  experimentation. 

The  first  epoch  marked  the  period  of  primitive  groping  and 
the  centuries  of  acceptance  of  its  empirical  findings  without 
any  marked  advance  being  registered  in  the  field. 

The  second  epoch  followed  the  discovery  of  the  Old  World 
hookworm,  Ancitlostoma  duodenale,  by  Dubiui  in  1843,  and  the 
gradual  uufoldment  of  knowledge  regarding  the  importance  of 
the  parasite  and  the  recognition  of  ancylostomiasis  as  a  disease 
entity.  Gricsingcr's  association  of  the  hookworm  with  Egyp- 
tian chlorosis,  Wucherer's  work  which  showed  its  relation  to 
tropical  anemia  in  Brazil  and  Perroncito's  discovery  of  hook- 
worm as  the  cause  of  the  St.  Gothard  tunnel  disease  stimulated 
interest  in  the  hookworm  problem.  These  discoveries,  followed 
by  Sonsino's  classical  observations,  demonstrated  the  need  for 
specific  therapeusis  and  prepared  the  way  for  the  development 
of  a  number  of  anthelmintics  which,  if  not  thoroughly  efficient, 
provided  useful  treatments;  these  held  their  place  for  a  period 
of  four  decades  and  until  the  epoch  of  critical  testing  provided 
more  specific  and  more  effective  drugs.  The  year  1881  marked 
Perroncito's  proposal  of  male  fern  as  a  hookworm  treatni/nt. 
the  introduction  by  Bozzolo  of  thymol,  and  Baumler's  unfavor- 
able report  on  oil  of  chenopodium  for  this  purpose.  Male  fern 
had  only  limited  use  as  a  hookworm  treatment  but  thymol 
proved  to  have  considerable  efficacy  and  enjoyed  a  long  vogue. 
In  fact,  the  latter  drug  was  used  more  extensively  than  any 
other  until  Schiiffner  and  Verwoort  reintroduced  oil  of  cheno- 
podium in  1913  and  showed  that  Baumler's  conclusions,  which 
were  apparently  based  on  the  treatment  of  only  one  ease,  were 
erroneous.  In  the  meantime,  Bentley  in  1904  reported  his 
findings  with  betanaphthol  and  advocated  its  use  In  hookworm 
disease. 

In  1905  Herman  introduced  a  mixture  of  chloroform,  eucalyp- 
tus and  castor  oil  as  a  treatment  for  ancylostomiasis  in  miners 
at  Mons,  Belgium.  The  mixture  was  later  modified  by  Phillips 
and  others  and  was  subsequently  employed  extensively  in  the 
treatment  of  hookworm  disease  in  many  parts  of  the  world. 
Schultz  later  found  chloroform  to  be  the  active  ingredient  of 
Herman's  Mixture  and  reported  the  drug  to  be  effective  against 
hookworms  in  the  dog. 

In  the  meantime  progress  was  being  made  also  in  the  field  of 
anthelmintics  for  veterinary  use.  As  early  as  1894  Perroncito 
and  Bosso  discovered  the  efficacy  of  carbon  disulphide  for  the 
removal  of  bots,  Gasternphihis  spp.,  from  the  horse.  In  fact, 
the  first  critical  testing  of  anthelmintics  was  actually  carried 
out  by  Grassi  and  Calandruccio  in  1884  and  188.5  and  by  Per- 
roncito in  1885  and  1886  in  establishing  the  value  of  male  fern 
for  the  destruction  of  liver  flukes  in  sheep  by  post-mortem 
examination  of  treated  animals.  However,  this  method  of  test- 
ing  found   no   further   advocates   for   a    quarter   of   a   century. 

A  work  of  far  reaching  economic  importance  was  the  dis- 
covery by  Hutcheon  in  South  Africa  in  1891  of  the  efficacy  of 
copper  sulphate  solution   for  the  removal  of  the  common  sheep 


stonuich  worm.  Hai  iiioiicJius  niniui-lus.  The  wireworm  remedy 
of  copper  sulphate  and  sodium  arseuite  worked  out  by  Theiler 
in  1912  and  Veglia  in  1920  has  also  been  used  extensively  in 
South  Africa  and  was  an  important  contribution  to  anthel- 
mintic therapy.  In  the  United  States,  Lewis  and  Guberlet 
added  a  tobacco  infusion  to  the  copper  sulphate  solution ;  Lam- 
son  introduced  nicotine  sulphate  solution;  and  Curtice  com- 
bined copper  sulphate  and  nicotine  sulphate  into  the  "Cu-Nic" 
solutiou  with  an  increase  in  efficacy  against  the  common  stom- 
ach worm  and  some  other  gastrointestinal  parasites  of  rumi- 
nants. In  general,  however,  it  may  be  said  that  the  four  dec- 
ades of  critical  empiricism  produced  less  progress  in  the  de- 
velopment of  veterinary  anthelmintics  than  in  anthelmintics 
for  human  use.  It  was  not  until  1915  that  substantial  progres."; 
was  achieved  in  the  former  field. 

The  year  1915  marked  the  practical  beginning  of  the  epoch 
of  the  critical  testing  of  anthelmintics.  Hall  laid  down  the 
basic  principles  of  this  method  and  together  with  his  associates, 
including  Foster,  .\very,  Snead,  Wolf,  Wilson,  Wigdor  and 
Shillinger,  checked  critically  the  efficacy  of  empirical  anthel- 
mintics and  developed  new  compounds  of  far  reaching  and 
fundamental  importance  in  both  human  and  veterinary  medi 
cine. 

The  method  which  Hall  adopted  was  to  administer  known 
doses  of  drugs  to  test  animals  of  various  species,  collect  all 
worms  passed  in  the  feces  for  a  given  period  of  time,  identify 
and  count  these  worms,  sacrifice  the  test  animals  and  make 
thorough  post-morten  examinations  with  the  recovery,  the  iden- 
tification and  the  counting  of  all  worms  remaining.  This 
method  gave  specific  information  concerning  the  number  of 
worms  present,  the  number  removed  and  the  number  left  after 
treatment  and  provided  an  accurate  index  concerning  the  effi- 
cac.v  of  the  drug  tested.  The  method  was  relatively  ponderous 
and  time  consuming  compared  to  the  favored  process  of  drop 
ping  ascarids  or  some  other  easily  collected  invertebrate  into 
solutions  of  drugs  and  calculating  the  anthelmintic  efficacy  of 
the  drug  by  observing  the  ultimate  fate  of  the  animal  in  the 
solution.  However,  critical  testing  developed  precise  informa- 
tion whereas  in  vitro  tests  were  often  entirel.v  valueless. 

The  method  of  critical  testing  was  of  particular  value  in 
veterinary  medicine.  It  enabled  an  accurate  assay  of  drugs 
whose  value  was  often  more  traditional  than  real,  and  its  use 
confirmed  in  many  cases  the  efficacy-  of  empirically  selected 
anthelmintics  and  enabled  dependable  information  to  be  ob- 
tained concerning  their  therapeutic  dose  rate,  their  margin  of 
safety,  the  contraindications  for  their  use  and  the  type  and 
mode  of  purgation  most  suitable  to  promote  the  efficacy  of  the 
drug  and  to  protect  the  patient. 

Many  of  the  tests,  especiall.v  those  on  dogs,  provided  results 
which  were  applicable  with  but  slight  modification  to  human 
medicine.  The  outstanding  discovery  in  this  connection  was 
that  by  Hall  in  1921  of  the  value  of  carbou  tetrachloride  for 
the  removal  of  hookworms  from  the  dog.  Hal!  immediately 
suggested  the  use  of  the  drug  in  the  treatment  of  hnmai]  hoo!< 
worm  disease,  a  suggestion  which  was  forthwith  adopted  by 
a  number  of  investigators  particularly  Laml)ert  and  other 
physicians  on  the  staff  of  the  International  Health  Board.  It 
was  soon  found  that  the  efficacy  of  carbon  tetrachloride  ex- 
ceeded that  of  all  other  drugs  in  this  condition  and  it  was 
adopted  practicall.y  as  a  standard  treatment  and  used  in  mil- 
lions of  cases  in  various  parts  of  the  world.  Another  discovery 
less  spectacular  but  actually  of  greater  importance  was  that 
of  Hall  and  Shillinger  in  1925  of  the  value  of  tetrachlorethy- 
lene  for  the  removal  of  hookworms.  Because  of  its  greater 
safety  and  the  fact  that  it  produces  little  or  no  hepatic  or 
renal  damage,  tetrachloreth.vlene  is  replacing  carbou  tetra- 
chloride in  human  ancylostomiasis  and  for  many  parasitic  in- 
fections of  domesticated  animals. 

Using  the  method  of  critical  testing,  Hall  and  his  coworkers 
established  or  confirmed  the  value  of  many  anthelmintics  in- 
cluding copper  sulphate  for  Ilaenwiiclnis  contortus,  oil  of 
chenopodium  for  ascarids  in  dogs  and  swine  and  for  strongyles, 
cyclicostomes,  and  pinworms  in  horses;  carbon  disulphide  for 
bots  and  ascarids  in  equines;  carbon  tetrachloride  for  stomach 
worms     and     other     worms     in     sheep     and     for     a-scarids     and 


332 


Stroiifrvli's  ill  liorsrs:   tctr:irlili)ii'tlivK'iio  for  iM'rtaiii  slircp  p.-ira- 
sites;   and  other  troatnicnts. 

The  method  devised  li.v  Hall  has  since  been  widely  adopted 
and  employed  by  nnini'rous  iiivestiRatois  in  establishing  the 
value  of  many  other  anthelmiTitics. 

Except  in  the  rase  of  eondenmed  eriniinals  who  will  volun- 
tarily submit  to  tist,  till'  nu'thod  of  eritieal  testing  cannot  be 
used  in  man.  t)ther  metliods  have  necessarily  been  adopted  for 
evaluating  the  ei^cacy  of  anthelmintics  for  nematode  infections 
in  this  host.  One  of  these,  the  use  of  a  so-called  standard 
treatment,  was  based  on  the  administration  of  the  test  drug, 
the  screening  of  the  stools  an<l  the  recovery  of  worms,  followed 
witliin  a  suitable  period  by  the  administration  of  the  standard 
treatment,  the  relative  efTicacy  of  which  was  known.  Worms 
passed  following  this  treatment  were  collected  and  counted  and 
a  comparison  between  .the  results  obtained  with  botli  treatments 
enabled  the  investigator  to  arrive  at  sonu'  evaluation  of  the 
efficac.v  of  the  test  drug.  While  the  method  necessarily  had  its 
limitations,  its  use  led  to  findings  of  value  particularly  when 
applied  to  relatively  large  numbers  of  persons  to  obviate  the 
margin  of  error  in  individual  differences.  Under  these  con- 
ditions, the  standard  treatment  method  was  used  effectively  by 
Caius  and  Mliaskar  in  their  extensive  investigations  in  connec- 
tion with  the  hookwtirm  in.jury  in  the  Madr'as  Presidency  and 
similarly  by  Darling,  Rarlicr,  Hackett,  Smillie  and  other  physi 
cians  on  the  staff  of  the  International  Health  Board  in  their 
far-flung  search  for  the  most  effective  treatment  for  hookworm 
disease. 

Following  the  discovery  by  Stoll  in  1!)2.3  and  Stoll  and 
Hausheer  in  lS)2(i  of  a  method  of  counting  nematode  ova  in 
feces  with  some  degree  of  accuracy,  the  Stoll  count  has  been 
used  extensively  in  evaluating  anthelmintic  treatments  in  man. 
With  due  regard  for  the  limitations  imposed  upon  it  by  the 
varying  factors  involved,  the  method  has  been  of  marked  value 
in  gauging  the  efflciency  of  certain  anthelmintics  particularly 
those  designed  for  the  treatment  of  Asearin  and  hookworm  in 
fections  in  man.  Because  of  its  greater  reliability  and  its  ease 
of  application,  this  method  has  replaced  largely  the  use  of  the 
standaid  treatment  method.  Hall  and  .\ugustiiie  in  1920  sup- 
plemented the  Stoll  count  with  a  count  of  worms  passed  fol 
lowing  treatment  in  evaluating  certain  anthelmintic  treatments 
for  man. 

At  times  it  is  protit.-ible  to  employ  several  different  methods 
of  research.  Lamson  and  his  associates  used  in  vitro  testing, 
critical  testing  and  the  Stoll  egg-counting  method  in  their  ex- 
tensive investigations  into  the  anthelmintic  value  of  the  alkyl 
h.vdroxy  benzenes  and  related  compounds.  In  this  case,  com- 
parable in  vitro  tests  on  Jscaris  linnbriroides  with  large  num 
bcrs  of  compounds  gave  leads  which  could  be  developed  further 
by  the  employment  of  other  methods. 

Mode  of  Action 

Little  information  is  available  concerning  the  manner  in 
which  anthelmintics  act  on  worms.  An  extensive  use  of  in  i'i(ro 
tests  in  this  field  of  investigation  may  yield  some  data  but, 
since  it  is  difficult,  if  not  impossible,  to  simulate  in  vitro  the 
environmental  conditions  of  the  parasite  in  its  natural  host,  re- 
sults obtained  in  this  manner  must  be  used  with  great  caution. 
The  physiology  of  nematodes  in  itself  is  an  almost  totallj'  un- 
explored field.  In  the  absence  of  precise  knowledge  concerning 
the  life  processes  of  a  parasite,  it  is  not  likely  that  we  shall 
know  in  what  manner  toxins  act  on  the  organism.  The  meager 
information  which  is  available  throws  little  light  on  the  prob- 
lem in   hand. 

According  to  their  mode  of  action,  anthelmintics  may  be 
divided  roughly  into  the  following  groups: 

1.  Narcotizing   or   paralyzing   agents. 

2.  Compounds  exhibiting  a  destructive  action   on   protein. 

•S.    Compounds  containing  enzymes  capable  of  digesting  nem- 
atode tissues. 
4.    Anthelmintics  of  unknow^n  action. 

The  first  group  contains  such  well  known  anthelmintics  as 
santonin  and  the  chlorinated  hydrocarbons.  Worms  eliminated 
following  the  administration  of  these  anthelmintics  may  ex 
hibit  more  or  less  movement.  This  characteristic  is  so  marked 
with  santonin  that  earlier  authors  were  led  to  describe  this 
drug  as  a  vermifuge,  a  term  which  originally  designated  an 
anthelmintic  that  irritated  the  parasites  and  drove  them  into 
the  colon  where  they  might  be  removed  with  a  brisk  purge. 
(Trendelenburg,  191.T.)  However,  as  Lo  Monaco  demonstrated 
in  ISilfi  and  as  Chopra  and  Chandler  (1928)  have  pointed  out, 
santonin  is  highly  toxic  to  ascarids  in  vitro  if  the  test  solutions 
are  properly  prepared.  If  santonin  is  partially  dissolved  in 
suitable  quantities  of  normal  liexane,  a  chemical  which  in  it- 
self is  innocuous,  the  drug  causes  in  vitro  successive  stages  of 


sliiiiiil.-ition  and  profound  paralysis.  Therefore,  it  is  now  con- 
sidered that  .santonin  |iarlially  paralyzes  the  jiarasites,  which 
in  that  condition  are  unable  to  maintain  their  position  in  the 
alimentary  canal.  The  prompt  elimination  of  the  parasites  by 
the  action  of  a  pnrgalivi-  may  increase  the  efficacy  of  santonin 
as  shown  by  Morris  and  Martin    (li):U)   and  by  others. 

The  chlorinated  hydrocarbons  contain  several  well  known 
compounds  which  exert  an  anesthetic  action  on  worms.  In  vitro 
the  parasites  gradually  lose  their  motility  and,  if  exposure  to 
the  drug  is  continued  after  iinmotility  sets  in,  the  parasite  may 
be  killed.  However,  if  removed  from  the  solution  promptly, 
it  may  recover.  The  authors  have  observed  hookworms  and 
a.scarids  moving  feebly  when  removed  from  dogs  with  drugs 
belonging  to  this  series. 

On  the  other  hand,  oil  of  chenopodium  belonging  in  the 
first  group  apparently  has  a  paralyzing  action  on  the  mus- 
culature, an  effect  which  almost  always  results  in  the  death  of 
the  nematode. 

The  largi'  group  of  hydroxy  benzenes  are  examples  of  those 
aiithelinintics  in  the  second  group.  If  solutions  of  egg  albumin 
are  treated  with  these  compounds,  the  iiroteins  are  promptly 
precipitated.  With  the  more  water  soluble  coniponnds  of  this 
series,  such  as  phenol,  the  preeijiitation  is  relatively  com- 
plete; with  comjiounds  such  as  thymol  and  hexylresorcinol,  the 
precipitation  is  partial;  while  the  extremely"  insoluble  com- 
pounds precipitate  only  small  quantities  of  the  protein.  In 
vitro,  he.xylresorcinol  exerts  a  searing  effect  on  the  cuticle  of 
A.'icaris  liimbricoidef!.  resulting  in  the  destruction  of  tissue;  if 
the  exposure  is  closely  controlled,  blisters  may  be  formed.  In 
solutions  of  hydro-xy  benzenes  which  are  not  quickly  fatal, 
Ascaris  exhibits  a  marked  stimulation  of  activity  greater  than 
that  observed  in  solutions  of  santonin  or  of  the  halogenated 
hydrocarbons.  Since  Lamson  and  Ward  (1932)  have  described 
a  blistered  condition  of  the  cuticle  of  ascarids  removed  from 
patients  treated  with  hexylresorcinol,  tin.  mode  of  action  in 
VIVO  may  be  identical  with  the  action  observed  in  vitro. 

In  connection  with  the  third  group,  Robbins  (1930)  has 
shown  that  the  anthelmintic  activity  of  leche  de  higueron,  the 
sap  of  the  Central  and  South  American  fig  tree,  Ficiis  laiiri- 
folia,  is  correlated  with  the  presence  of  a  proteolytic  enzyme, 
which  he  has  named  "ficiii."  Asenjo  (1940)  has  shown  re- 
cently that  the  destructive  effect  of  fresh  pineapple  .juice  on 
Ascnris  liimbriroi/lrx  in  vitro  is  probably  associated  with  the 
action  of  the  proteolytic  enzyme,  bromelin.  However,  there  is 
no  evidence  as  yet  that  the  above-mentioned  .jiiice  has  any  an- 
thelmintic value. 

The  fourth  group  probably  includes  the  ma.jority  of  anthel- 
mintics. Any  comments  regarding  the  mode  of  action  of  these 
drugs  would  be  speculative  for  the  most  part.  For  instance, 
we  do  not  know  how  trivalent  antimony  compounds  act  on 
somatic  nematode  parasites,  although  in  the  case  of  "Fouadiu" 
the  action  of  the  drug  is  cumulative  on  iJirofilaria  immitis  and 
the  adult  worms  succumb  very  gradually.  Some  observations 
of  the  senior  author  seemed  to  indicate  that  sterilization  of  the 
adult  female  worms  is  due  to  fatty  degeneration  and  necrosis 
of  the  reproductive  cells  of  the  ovary  and  perhaps  the  drug 
acts  similarly  on  the  somatoplasm. 

Little  is  known  concerning  the  nature  of  the  anthelmintic 
activity  of  various  dyes.  Gentian  violet  stains  the  tissue  of 
such  nematodes  as  Strong/iloidcs  and  Enterobinx.  against  which 
it  is  effective.  In  Enterobiii.i  passed  following  treatment,  the 
cuticle  is  usually  slightly  stained,  the  digestive  tract  more  so, 
and  the  reproductive  organs,  particularly  in  the  female,  are 
intensely  stained.  The  dye  no  doubt  has  a  cumulative  action 
since  some  stained  gravid  female  pinworms  will  migrate  in 
the  early  stages  of  treatment.  Furthermore,  the  prolonged 
course  of  treatment  necessary  to  eradicate  infections  with  both 
of  these  nematodes  supports  the  view  that  the  anthelmintic  is 
not  one  of  the  contact  type. 

Similarly,  worms  eliminated  following  the  administration 
of  phenothiazine  are  stained  reddish,  but  there  is  little  reason 
for  thinking  that  the  action  of  this  drug  is  in  anyway  cumula- 
tive, as  prolonged  treatment  seems  to  be  relatively  less  effective 
than  a  single  large  dose.  Many  worms  eliminated  following 
treatment  with  this  drug  are  alive  and  move  feebly,  a  circum- 
stance which  suggests  that  phenothiazine  should  be  classed 
with   the  narcotics  and  para].yzants. 

The  manner  in  which  anthelmintics  reach  the  tissues  of  the 
parasite  is  as  little  known  as  is  the  action  of  drugs  on  these 
tissues.  One  assumption  has  been  that  nematode  parasites  with 
their  well  developed  digestive  tract  ingest  the  anthelmintic  in 
solution  with  the  food  and  absorption  therefore  takes  place 
from  the  oesophagus  or  through  the  cells  lining  the  wall  of 
the  intestine.  However,  evidence  for  such  a  hypothesis  is  not 
convincing.  For  instance.  Well's  (1931)  striking  demonstra- 
tion of  the  blood  sucking  proclivities  of  the  dog  hookworm  has 
shown  that  the  parasite  may  take  up  as  much  as  0.S4  cc.  of  the 


333 


host's  blood  in  24  hours.  The  blood  passes  rapidly  through  the 
digestive  tract  and  apparently  is  not  subjected  to  any  material 
amount  of  digestion.  Consequently,  the  worm  probably  uses 
as  food  diffusible  substances  in  the  plasma.  In  spite  of  the 
marked  diffusibility  of  carbon  tetrachloride,  the  drug  has 
little  or  no  action  on  hookworms  when  injected  intravenously. 
Wright  and  Underwood  (1934)  cite  work  with  Bozicevieh  in 
which  repeated  intravenous  injections  of  carbon  tetrachloride 
failed  to  have  any  effect  on  the  microfilariae  or  adults  of 
Dirofilaria  immiiis.  While  it  is  probable  that  this  parasite 
takes  only  a  limited  amount  of  nourishment  orally  because  of 
the  atrophied  digestive  tract,  yet  it  is  bathed  continuously  in 
the  blood  plasma.  Even  under  these  conditions  of  intimate 
contact,  the  anthelmintic  had  no  effect. 

The  studies  of  Mueller  (1929)  indicated  that  carbon  tetra- 
chloride penetrated  the  cuticle  of  Ascaris  and  was  not  taken  in 
through  the  digestive  tract.  Mueller  believed  that  fat  soluble 
compounds  such  as  chloroform  and  carbon  tetrachloride  exert 
an  anthelmintic  effect  by  reason  of  their  action  on  the  fat 
content  of  the  muscle  cells. 

Brown  (1937)  has  reported  the  results  of  some  ingenious 
experiments  designed  to  ascertain  the  manner  in  which  certain 
anthelmintics  reach  the  tissues  of  Ascaris  lumbricoidcs.  While 
the  results  were  in  part  inconclusive  because  of  the  difficulty 
of  handling  worms  without  injuring  them  traumatically,  the 
evidence  seemed  to  indicate  that  oil  of  chenopodium  and  car- 
bon tetrachloride  in  solution  are  absorbed  through  the  body 
wall.  Brown  was  able  to  show  that  Ascaris  will  ingest  solutions 
of  carbon  tetrachloride  in  mineral  oil  but  will  refuse  to  ingest 
dilute  solutions  of  chenopodium.  Brown  did  not  believe  that 
the  drugs  tested  acted  directly  on  the  nervous  system  of  the 
parasite  even  when  injected  in  the  region  of  the  nerve   ring. 

The  experiments  of  Strong  (1918),  Lambert  (1923),  Hall 
and  Sliillinger  (192."))  and  Fernan-Nihiez  (1927)  may  be  cited 
as  bearing  on  this  problem.  Strong  injected  oil  of  chenopo- 
dium intramuscularly  for  the  removal  of  whipworms  without 
success.  Lambert  was  equally  unsuccessful  with  intramuscular 
injections  in  two  eases  in  man  but  obtained  better  results  in  a 
third  case.  However,  when  used  intravenously,  the  drug  had 
a  marked  vennicidal  action  again.st  Trichiiris,  little  action  on 
Ascaris  and  none  on  hookworms.  Hall  and  Shillinger  obtained 
very  indift'erent  results  on  dogs  but  Fernan  Nunez  reported 
marked  success  against  Trichiiris  in  man  with  intramuscular 
and  intravenous  injections.  The  manner  in  which  whipworms 
derive  their  nourishment  is  still  a  deliatable  point  although 
Garin  (1913)  was  able  to  demonstrate  lilood  in  th^>  intestinal 
contents  and  Schwartz  (1921)  reported  a  hemolysin  from  Tri- 
chiiris viilpis.  The  evidence  from  the  above-mentioned  experi- 
ments would  seem  to  indicate,  however,  that  the  drug  was 
possibly  absorbed  through  the  digestive  tract  in  view  of  the 
little  likelihood  that  under  these  conditions  it  would  have  been 
in  adjacent  tissues  in  sufficient  concentrations  to  have  been 
absorbed  through  the  cuticle.  Recently  Trum  (1938)  found 
that  oil  of  chenopodium  injected  intravenously  was  very  toxic 
for  horses,  but  had  very  little  effect  on  the  blood  sucking 
strongyles  present  in  these  animals. 

Correlation   Between   Chemical   Structure   and 
Anthelmintic  Efficacy 

Compounds  comprising  the  group  of  cft'ective  anthelmintics 
and  those  for  which  some  anthelmintic  efficacy  has  been  re- 
ported are  associated  with  such  widely  divergent  chemical 
groups  that  no  general  correlations  can  be  drawn  between  aii- 
thelmic  efficacy  and  chemical  composition.  As  a  rule,  anthel 
mintics  are  very  specific  in  their  action,  exhibiting  their  opti- 
mum efficacy  against  one  species  of  parasite  or  at  best  against 
closely  allied  species  of  parasites.  Drugs  specific  for  the  re- 
moval of  nematodes  are  seldom  effective  for  the  removal  of 
cestodes.  The  one  glaring  exception  to  this  rule  is  carbon  tet- 
rachloride which  is  a  fairly  effective  treatment  for  Taenia  and 
Diphyllobnthriiim  lafiim  infections  of  man  although  of  little  or 
no  value  against  other  cestodes.  On  the  contrary,  there  is  no 
taeniafuge  which  is  effective  for  the  removal  of  nematode 
parasites. 

The  specificity  of  anthelmintics  is  conditioned  not  only  by 
the  anatomy  and  physiology  of  the  parasite  but  also  in  part  by 
the  anatomy  and  physiology  of  the  host.  In  this  connection, 
drugs  effective  for  the  removal  of  strongylid  parasites  from 
carnivores  fail  to  a  great  extent  when  employed  against  simi- 
lar parasites  of  ruminants.  Such  drugs  are  frequently  held 
in  the  rumen  with  a  resultant  dissipation  of  their  action  long 
before  they  reach  the  object  of  their  attack  farther  down  in 
the  complicated  digestive  tract.  On  the  other  hand,  the 
anthelmintic  value  of  copper  sulphate  solution  against  Hacmon- 
chus  contorUis  in  ruminants  is  associated  with  the  peculiar 
stimulus  which   the   drug  exerts   in   bringing  about  the  closure 


of  the  oesophageal  groove  thus  permitting  the  solution   to  be 
diverted  directly  into  the  abomasum. 

The  optimum  action  of  two  effective  drugs  is  often  lost  or 
markedly  reduced  when  such  drugs  are  combined  in  a  single 
dose.  Frequent  efforts  have  been  made  to  develop  a  single 
method  of  treatment  which  would  be  effective  against  both  in- 
testinal nematodes  and  cestodes.  These  efforts  have  nearly 
always  resulted  in  failure.  In  such  cases,  drugs -which  are 
effective  against  nematodes  and  cestodes,  respectively,  lose 
much  of  their  efficacy  when  combined.  Fnder  these  varied  cir- 
cumstances, attempts  to  correlate  anthelmintic  efficacy  and 
chemical  structure  must  be  made  on  the  basis  of  a  selection  of 
closely  related  compounds  on  a  single  species  of  parasite. 

Hall  and  Wigdor  (192(i)  were  apparently  the  first  to  carry 
out  studies  of  this  sort.  Their  work  was  carried  on  in  19lV 
and  1918  but  was  interrupted  by  military  service.  Their  lim- 
ited study  was  made  with  terpenes  and  certain  other  aromatic 
hydrocarbons.  Unfortunately,  the  study  provided  little  infor- 
mation of  value  partly  because  of  the  divergent  structure  of 
the  compounds  tested  and  partly  because  of  tlie  feeble  anthel- 
mintic activity  of  many  of  them. 

Cains  and  Mhaskar's  extensive  investigation  into  the  value 
of  hookworm  remedies  was  a  thorough  piece  of  work.  How- 
ever, here  again  too  many  compounds  (70  in  all)  of  too  di- 
vergent a  character  were  employed.  In  the  summary  and 
conclusions  of  their  work,  Cains  and  Mhaskar  (1923)  stated 
that  the  effective  hookworm  treatments  studied  by  them  dif- 
fered so  much  in  molecular  composition  and  structure  that  no 
general  correlations  could  be  said  to  exist  between  anthelmintic 
properties  and  chemical  composition.  They  concluded  that 
anthelmintic  action  on  hookworms  is  specific. 

Wright  and  Sehaffer  (1932)  selected  a  series  of  chlorinated 
alkyl  hydrocarbons,  a  feiv  of  which  had  been  .studied  by  Hall 
and  his  associates.  The  previousl.v  unstudied  compounds  were 
tested  critically  for  their  anthelmintic  efficacy  against  hook- 
worms and  general  correlations  were  drawn  l>etween  anthel- 
mintic efficacy,  chemical  structure  and  physical  properties. 

In  the  homologous  series,  there  was  a  rise  in  anthelmintic 
efficacy  against  Anciilostoma  caniiniiii  with  an  increase  in  the 
length  of  the  hydrocarbon  chain  from  the  low  member  of  each 
group  to  the  next  higher  member.  In  each  case,  there  was  an 
accomjianying  decrease  in  solubility  from  above  the  optimum 
solubility  range  to  a  solubility  within  that  range.  In  one 
homologous  series  (normal  monochlor  compounds)  a  iieak  of 
anthelmintic  efficacy  was  teached.  It  was  pointed  out  that  in 
a  similar  way  other  homologous  series  would  no  doubt  each 
have  a  peak  of  anthelmintic  efficacy,  for  the  reason  that  a 
point  will  be  reached  Avhere  the  solubility  of  a  higher  member 
will  be  so  slight  as  to  result  in  little  or  no  anthelmintic  effi- 
cacy. It  was  concluded  that  although  the  addition  of — CH2 — 
groups  to  the  hydrocarlion  chain  results  in  a  progressive  change 
in  solubility  from  one  member  to  the  next  in  homologous  series, 
a  progressive  change  in  anthelmintic  efficacy  does  not  neces- 
sarily follow. 

An  increase  in  anthelmintic  efficacy  against  A.  canininn  did 
not  always  result  with  an  increase  in  the  number  of  chlorine 
atoms  in  the  molecule  or  with  an  increase  in  the  relative  per- 
centage weight  of  chlorine  in  the  molecule.  In  those  cases 
where  a  high  degree  of  anthelmintic  efficacy  was  associated 
with  increase  in  the  chlorine  content,  the  resulting  compounds 
without  exception  possessed  a  solubility  within  the  optimum 
range.  Further,  the  siireading  of  the  chlorine  atoms  in  the 
hydrocarbon  molecule  did  not  invariabl.v  result  in  an  increase 
or  decrease  in  anthelmintic  efficacy. 

Differences  in  position  of  the  chlorine  atom  in  the  molecule 
resulted  in  changes  in  anthelmintic  efficacy  and  the  accompany- 
ing change  in  water  solubilitj'  was  an  important  factor  in 
determining  anthelmintic  efficac.v.  Even  among  comjiounds 
with  the  same  number  of  carbon,  hydrogen  and  chlorine  atoms, 
changes  in  the  position  of  the  chlorine  atom  resulted  in  com- 
pounds showing  marked  differences  in  anthelmintic  efficacy  for 
hookworms.  In  addition,  differences  in  iinthelmintic  efficacy 
were  exhiljited  when  the  methyl  radical  was  introduced  in  dif- 
ferent  positions   in   the   clilorinated   liydrocarlicju   molecule. 

Wright  and  Sehaffer  concluded  that  antlu'lmintic  efficacy  of 
chlorinated  alkyl  hydrocarlions  against  A.  ciiniinnii  is  intimately 
linked  with  water  solubility  which  varies  with  the  chemical 
structure  of  the  molecule  and  that  the  anthelmintic  efficacy  is 
not  solely  dependent  on  the  halogen  concentration  or  on  the 
position  of  the  chlorine  atom  or  atoms  in  the  molecule.  With  a 
single  exception  those  compounds  having  water  solubilities  be- 
tween 1:1250  and  1:.5300  showed  a  high  degree  of  anthelmintic 
efficacy  for  hookworms  in  the  dog  regardless  of  the  halogen 
concentration  or  the  position  of  the  diloiine  atom  or  atoms  in 
the  molecule.  Water  solubility  is,  therefore,  the  factor  most 
definitely  correlated  with  the  anthelmintic  efficacy  of  chlori- 
nated alkyl  hydrocarbons  for  hookworms. 


334 


It  is  intcrfStiiig  to  note  that  tho  al>ovo  iiu'iitioiu'd  coni'lusidiis 
did  not  apply  in  tlie  case  of  aiitlu'lniintie  efficacy  of  the  com- 
pounds asainst  To.vocara  caiii.s  and  Tuxuscari.s  Iroiiina. 

In  critical  tests  on  doRS  with  nionolironi  hydrocarbons, 
Wright,  Schaffer,  Bozicevicli  and  Underwood  (li)37)  fovuid  that 
an  increase  in  the  hydrocarbon  chain  was  associated  Avith  a 
]irogressive  decrease  in  water  solubility  from  one  member  to 
the  next  without  a  progressive  change  in  anthelmintic  cfti 
cacy  against  JnciiluKtoiiia  canhiKin.  The  jieak  of  anthelmintic 
efficacy  against  hookworms  was  reached  with  n  butyl  bromide, 
the  efticacy  thereafter  declining.  This  compound  was  the  only 
member  of  the  series  possessing  a  water  solubility  lying  within 
the  optimum  solubility  range  of  chlorinated  hydrocarbons.  It 
appeared  probable  that  an  optimum  solnbilit.v  range  similar 
to  that  for  chlorinated  hydrocarbons  exists  among  lironiinated 
hydrocarbons  so  far  as  anthelmintic  efficacy  against  hookworms 
is  concerned.  These  authors  concluded  that  water  solubility 
api'earcd  to  be  the  factor  most  definitely  correlated  with  an- 
thelmintic efficacy  of  bromiuated  hydrocarbons  for  hookworms, 
as  it  is  with  chlorinated  hydrocarbons.  Wright  and  Schaffer 
(lil.31)  came  to  similar  conclusions  in  connections  with  mono- 
iodated  compounds. 

l.amson  and  his  associates  (1934,  1935)  studied  extensively 
the  anthelmintic  value  of  a  large  number  of  phenolic  coni- 
jionnds,  most  of  the  comparalde  tests  having  been  carried  out 
on  AKcaris  Uimhricoidfs  in  I'itro.  These  compounds  included 
(1)  alkyl  resorcinols,  (2)  alkyl  phenols,  (3)  alkyl  eresols,  (4) 
polyalkyl  phenols,  and  (5)  phenols  with  other  than  normal 
alkyl  side  chains.  The  authors  concuded  that  the  ascaricidal  ac- 
tivity of  phenolic  compounds  is  related  to  the  local  irritating 
action  although  all  phenols  exhibiting  such  action  are  not 
necessarily  active  ascaricides.  To  be  effective  as  an  asearicide, 
it  was  found  that  a  phenol  should  lie  a  liquid  or  a  substance 
which  will  lifjuify  or  emulsify  in  the  intestinal  tract.  Such 
substances  were  found  to  have  a  melting  ])oint  of  not  over  7.5° 
C.  The  solubility  range  of  ascaricidal  phenols  was  found  to 
lie  between  1:1,000  to  1:35,000,  although  the  most  effective 
anthelmintic  of  this  type  in  the  large  number  of  compounds 
studied  was  hexylresorcinol  with  a  water  solubility  of  1:2,000. 

It  was  found  that  the  ascaricidal  properties  of  phenols  and 
resorcinols  are  increased  by  the  introduction  of  alkyl  radicals. 
Such  properties  become  more  marked  with  the  lengthening  of 
the  alkyl  chain  and  reach  a  maximum  which  differs  in  differ- 
ent series,  thereafter  declining  rapidly.  The  ascaricidal  value 
of  dihydroxybenzenes  was  not  strikingly  different  from  that 
of  mouohydroxybenzenes.  No  significant  differences  were 
found  between  ortho  and  para  alkyl  phenols.  The  introduction 
of  single  normal  chains  into  the  nucleus  was  more  effective 
than  the  introduction  of  multiple  chains  with  the  same  total 
number  of  carbon  atoms.  Normal  chains  in  general  were  more 
effective  than  branched  chains,  although  exceptions  were  noted, 
such  as  the  increased  efficacy  of  thymol  over  that  of  n-propyl 
meta  cresol.  Some  of  the  differences  in  activity  were  thought 
to  be  accounted  for  by  the  higher  melting  point  of  the  branched 
chain  compounds  over  that  of  normal  compounds.  Cyclic  side 
chains  behaved  similarly  to  forked  chains. 

From  the  evidence  at  hand  it  may  be  concluded  that  little 
or  no  correlation  can  be  drawn  between  the  anthelmintic  effi- 
cacy and  the  chemical  constitution  of  compounds  differing 
widely  in  their  chemical  structure.  When  closely  allied  com 
pounds  have  been  tested  against  a  single  species  of  parasite, 
the  results  have  indicated  generally  that  there  is  a  rise  and  fall 
in  anthelmintic  activity  within  the  homologous  series,  the  ac- 
tivity reaching  a  peak  and  then  declining.  In  the  case  of 
liquids,  the  anthelmintic  efficacy  is  definitely  linked  with  the 
water  solubility  and  in  the  case  of  solid  compounds  with  the 
water  solubility  and  the  melting  point.  In  general,  in  homolo- 
gous series  compounds  with  normal  chains  are  usually  more 
effective  than  those  with  branched  chains.  Finally,  the  evi 
denee,  meager  as  it  is,  emphasizes  almost  dramatically  the 
extreme  specificity  of  anthelmintics. 

Chemical  Classification 

The  following  classification  showing  the  various  chemical 
groups  to  which  anthelmintics  belong  is  taken  mainly  from  the 
excellent  summary  of  Lamson  and  Ward  (1932).  The  listing 
includes  for  the  most  part  the  compounds  more  commonly  em- 
ployed against  nematode  parasites  and  contains  mainly  those 
drugs  which  have  been  shown  by  adequate  test  to  possess 
marked  anthelmintic  properties.  For  information  concerning 
the  chemical  grouping  of  other  drugs,  including  those  employed 
in  cestode  and  trematode  infections,  the  reader  is  referred  to 
the  more  detailed  classification  of  Lamson  and  Ward. 

1.    Inorganic  substances 
Bismuth  subcarbonate 
Copper  sulphate 


.\ntimony  i)otassiuni  tartrate 
Colloidal  iodine 
Sodium  arsenite 
(^;irbon  disulphide 
Hydrogen   peroxide 

2.  Hiilofii  nuUil  Itydrocarbons 
a.    Alipathic 

(1)  Saturated 
Chloroform 
Rromoform 
Carbon  tetrachloridi' 
n  Butyl  chloride 
n-Butylidene  chloride 
n-Butyl  bromide 

(2)  Unsaturated 
Tetrachlorcthylene 

3.  PItcnols 

a.  Monoliydric  phenols 

uHexylm  cresol 
Thymol 
Carvacrol 
Betanaphthol 

b.  Diliydric  phenols 

n  Hexylresorcinol 
n-Heiitylresorcinol 

4.  Oiiionic  acids  and  their  salts  or  esters 
Aluminum  subacetate 

5.  Orijnnic  dioxides 
Disuccinyl  perovide 

(i.    Organic  antimomi  coiiiponnds 

Sodium  antimony  III  jiyrocatechin  disulphonate  of  sodium 

' '  Filsol ' ' 

"Stibsol" 

7.  Terpcnes 

a.  Bridged  ring 
(1)    Peroxides 

Ascaridol 

b.  Sesquiterpenes 
Santonin 

8.  Alkaloids 
Nicotine 
Pyrethrine 

9.  Enzymes 
Fie  in 
Bromelin 

10.  Plant  products 
Leche  de  higueron 
Digenea  simplex 
Oleum  chenopodii 
Oleum  eucalypti 
Oleum  terebinthinae 
Quassia 

Tobacco 

11.  Dyes  and  similar  conij)ounds 

a.  Thiaziu 
Phenothiazine 

b.  Triamino  triphenyl   methane 
Gentian  violet 

c.  Phthalein 
Mercurochrome 

General   Principles   of   Anthelmintic   Medication 

Elscwliere  in  this  discussion  we  have  emphasized  the  specific- 
ity of  anthelmintics,  a  thing  which  is  of  prime  importance 
from  a  medical  standpoint.  It  is  not  only  a  waste  of  time  and 
effort  to  employ  a  nonspecific  treatment  against  a  given  para- 
sitic infection  but  it  is  a  hazard  to  the  safety  and  well  being 
of  the  host.  Specific  treatments  cannot  be  chosen  unless  an 
accurate  diagnosis  is  made.  Hence  any  anthelmintic  medica- 
tion should  be  predicated  on  such  a  diagnosis.  Even  today  when 
the  average  physician  or  veterinarian  is  far  better  qualified 
than  formerly  in  the  field  of  parasitolog.y,  we  find  practitioners 
administering  anthelmintic  treatment  on  the  basis  of  a  clinical 
diagnosis  without  proper  laboratory  checks.  No  parasitic  in- 
fection is  characterized  by  pathognomonic  symptoms  and  the 
shifting  sand  of  the  clinical  picture  is  not  a  sufficiently  firm 
foundation  upon  which  to  base  treatment  with  drugs  which  at 
best  have  only  a  small  margin  of  safety. 

In  the  past,  mass  treatment  of  large  population  groups  has 
been  a  popular  method  of  attack  against  a  given  parasite. 
The  benefits  anticipated  from  such  a  procedure  have  not  been 
generall.v  realized  for  all  too  frequently  the  important  sub.iect 
of  prophylaxis  has  not  been  given  sufficient  attention.  Under 
such  circumstances,  the  population  groups  involved  have  con- 
tinued to  indulge  in  the  habits  responsible  for  their  parasitic 


335 


infection  and  after  a  suitable  period   of   time  are  again   ready 
for  further  treatment. 

With  improved  techniques  for  determining  the  presence  of 
most  parasites  and  for  evaluating  the  relative  degree  of  in- 
fection with  many  of  them,  mass  treatment  is  no  longer  justi- 
fied in  the  field  of  medicine.  Even  in  veterinary  medicine  it 
can  be  condoned  only  in  the  case  of  large  flocks  or  herds  in 
which  individual   diagnosis  would  be  economically  unsound. 

The  question  is  frequently  raised  as  to  whether  an  infection 
with  a  given  number  of  worms  is  of  clinical  importance  and 
thus  warrants  treatment.  No  categorical  answer  can  be  given 
to  such  a  question.  An  infection  with  a  certain  number  of 
worms  might  be  injurious  to  the  health  of  one  individual  with- 
out aft'ecting  in  any  appreciable  degree  the  well  l)eing  of  an 
other  individual.  No  one  has  been  able  to  define  the  line  of 
demarcation  between  a  clinical  and  a  sub-clinical  infection. 
In  mass  treatment  such  finesse  of  judgment  is  not  required  or 
at  least  is  not  exercised  but  in  medical  practice  it  is  best  that 
due  cognizance  be  taken  of  the  relative  degree  of  parasitism. 
If  the  patient  has  only  a  few  worms,  such  as  hookworms,  he 
liad  better  go  without  treatment  rather  than  be  subjected  to 
the  potential  hazards  of  anthelmintic  medication.  However, 
with  such  a  circumscribed  environmental  parasite  as  Enterobiiis 
rr.rmicularia,  it  is  necessary  from  a  control  standpoint  to  treat 
siniultaneou.sly  all  infected  individuals  in  the  household  re- 
gardless of  the  degree  of  infection  or  the  presence  or  absence 
of  clinical  symptoms.  Otherwise,  untreated  individuals  provide 
direct  avenues   of   reinfection   for   treated   individuals. 

Methods  of  Application.  Anthelmintics  are  administered 
in  a  great  many  different  ways,  depending  on  the  kind  of 
parasite,  its  location  within  the  host  and  the  species  of  host 
animal.  In  man,  palatability  is  a  matter  of  some  importance 
and  it  is  desirable  to  administer  the  drug  in  a  manner  least 
distasteful  to  the  patient.  While  the  esthesia  of  taste  is  not 
usually  considered  in  the  case  of  lower  animals,  palatable  doses 
of  drugs  are  more  apt  to  be  retained  by  dogs  and  cats  in 
which  the  vomiting  reflex  is  acutely  sensitive.  Many  of  the 
anthelmintics  now  on  the  market  are  dispensed  in  soft  gelatin 
capsules.  Hard  gelatin  capsules  are  still  employed  by  some 
practitioners  who  prefer  to  fill  the  capsules  at  the  time  they 
are    used. 

For  certain  parasites  located  far  down  in  the  digestive  tract, 
the  use  of  enteric-coated  tablets  is  an  advantage.  However, 
most  of  the  enteric  coatings  employed  become  harder  with  age 
and  are  less  apt  to  dissolve  in  the  digestive  tract.  A  new  type 
of  water-soluble  coating  has  recently  been  devised  to  obviate 
the  disadvantages  of  the  usual  enteric  coating.  The  new  coat- 
ing permits  timed  disintegration  of  the  tablet  witliin  c^'rtain 
definite  periods  after  administration  and  radiographic  evidence 
in  support  of  this  has  been  furnished  by  Worton,  Kempf,  Bur- 
rin  and  Bibbins    (1038). 

For  ruminants,  certain  anthelmintics  such  as  solutions  of 
copper  sulphate  and  nicotine  sulphate  are  given  as  a  drench. 
In  fact,  Ortlepp  and  Miinnig  (1936)  have  shown  that  the  ad- 
ministration of  a  dose  of  copper  sulphate  solution  immediatel.y 
))rior  to  the  use  of  other  drugs  has  the  effect  of  closing  the 
oesophageal  groove  and  permitting  the  drug  to  reach  the  abom- 
asum  directly.  This  is  of  marked  advantage  in  connection  with 
some  treatments  against  ruminant  parasites.  On  the  other 
hand,  some  anthelmintics,  such  as  the  sodium  arsenite-bhiestoiie 
mixture  for  the  common  sheep  stomach  worm,  are  given  in 
j)owdered  form. 

The  duodenal  tube  method  of  administration  is  an  advantage 
in  some  instances  and  is  particnl.'irly  valuable  in  stubborn 
cases  of  strongyloidosis  in  man  in  which  ordinary  methods  of 
administration    fail. 

Somatic  helminths,  when  they  can  be  reached  at  all,  are 
usually  attacked  through  the  intramuscular  or  intravenous 
route.  Lungworms  in  domestic  animals  are  susceptible  to  some 
extent  to  anthelmintics  introduced  intratrachcally  and  good 
results  have  been  reported  in  this  connection  by  certain  workers 
in  the  Soviet  Union.  The  inhalation  method  was  used  by 
Wehr,  Harwood  and  Schaffer  (193S)  in  the  attack  against 
Symgamus  trachea  in  chickens  with  barium  antimonyl  tartrate 
dust. 

Parasites  in  the  lower  bowel  are  subject  to  attack  per  rec- 
timi.  The  employment  of  enemas  is  a  common  practice  against 
Entcrohins  vrrmiciihirix  in  man.  The  method  has  been  used  by 
Miinnig  in  South  Africa  and  by  others  in  removing  nodular 
worms  from  sheep,  while  intracecal  injections  have  been  advo- 
cated and  employed  with  some  success  for  the  expulsion  of 
whipworms  from  the  dog.  In  a  like  manner,  HcteraMs  galUnae 
can  be  reached  with  anthelmintics  injected  by  way  of  the 
cloaca. 

The  individual  anthelmintic  treatment  of  farm  animals  has 
never  appealed  to  the  livestock  owner  and  there  has  always 
been  keen  demand  for  an  anthelmintic   which  could  be  given 


with  the  feed.  Other  than  the  tobacco  dust  or  nicotine  treat- 
ment for  Ascaridia  in  poultry,  anthelmintics  administered  in 
tlie  feed  are  generally  ineffective.  The  method  has  the  disad- 
vantage that  some  animals  ingest  too  much  and  others  too  little 
of  the  drug.  More  recent  tests  with  phenothiazine  seem  to  in- 
dicate that  for  some  parasites  this  drug  may  be  of  value  when 
given  with  the  feed.  If  results  are  substantiated  in  further 
trials,  the  method   will   no  doubt  find  widespread  use. 

While  most  anthelmintic  therapy  is  based  on  the  use  of  single 
dose  treatments,  it  is  sometimes  of  advantage  to  employ  divided 
doses.  The  dose  of  chenopodium  for  man  is  occasionally  divided 
into  two  or  three  parts  administered  at  one  half  to  one  hour 
intervals.  When  given  in  this  way,  the  efficacy  of  tlie  drug 
against  hookworms  is  believed  by  some  workers  to  be  slightly 
enhanced.  If  toxic  symptoms  are  manifested  by  individuals 
having  an  idiosyncrasy  for  the  drug,  dosage  can  be  discontin 
ued.  However,  the  purgative  is  usually  withheld  until  the  last 
portion  of  the  dose  has  been  administered  and  under  these 
conditions  increased  absorption  of  the  anthelmintic  is  apt  to 
occur. 

Repeated  treatment  over  a  period  of  time  is  required  for  the 
eradication  of  such  parasitic  nematodes  as  Strongyloides  ster- 
coralis  and  Enterobiiis  vcnnioilaris.  Likewise  some  degree  of 
efficacy  can  be  secured  against  whipworms  by  repeated  dosing 
with  a  drug  such  as  santonin  which  exerts  little  or  no  action 
against  these  parasites  when  given  in  a  single  dose. 

The  above  citations  will  be  sufficient  to  indicate  to  the  reader 
that  anthelmintic  warfare  against  parasites,  whether  in  man  or 
the  lower  animals,  requires  the  employment  of  varied  methods 
of  attack  based  on  the  nature  of  the  lio,st  terrain  and  the  ac- 
cessibility of  the  parasite  to  the  range  of  the  weapon  or 
weapons  available.  Some  parasites  can  be  overcome  by  a 
single  anthelmintic  onslaught  but  others  are  expelled  from 
their  position  only  after  repeated  attacks.  The  method  of  ap- 
plying treatment  is  therefore  an  important  factor  in  anthel- 
mintic medication. 

Prelimin.\ky  Fasting.  It  is  custoniary  usually  to  fast  the 
jiatient  before  the  oral  administration  of  most  anthelmintics 
with  a  view  of  emptying  the  stomach  and  reducing  the  bulk  of 
the  intestinal  contents.  In  the  treatment  of  Axcaris  and  hook- 
worm infections  in  man,  the  patient  is  usually  given  a  light 
supper  the  night  before  and  the  anthelmintic  administered  in 
the  morning,  no  food  being  permitted  until  adequate  purgation 
has  ensued.  Dogs  and  cats  are  usually  fasted  overnight.  Various 
periods  of  fasting  are  prescribed  for  larger  domestic  animals. 
Swine  should  be  fasted  for  24,  and  preferably,  36  hours.  For 
equines  it  is  advisable  to  withhold  feed  for  18  hours  prior  to 
anthelmintic  medication  for  parasites  in  the  stomach  and  small 
intestine  and  36  hours  for  parasites  in  the  large  intestine. 
Conditions  are  somewhat  different  in  the  case  of  ruminants. 
Even  prolonged  fasting  will  not  entirely  reduce  the  bulk  of 
the  contents  of  the  rumen.  Formerly,  it  was  customary  to  fast 
animals  for  12  to  IS  hours  but  more  recently  Clunies,  Ross  and 
Gordon  (1934,  1935)  have  shown  that  there  is  no  increase  in 
the  efficacy  of  a  number  of  drugs  used  for  the  removal  of  the 
common  sheep  stomach  worm  in  animals  fasted  for  24  hours  as 
compared  to  the  efficacy  of  the  same  drugs  in  nnsfarved  sheep. 
Consideration  op  the  Patient.  Since  tlie  safety  of  the  pa- 
tient is  of  paramount  importance,  it  is  the  duty  of  the  prac- 
titioner to  satisfy  himself  that  no  contraindications  for  anthel- 
mintic treatment  are  present.  This  calls  for  an  adequate  physi- 
cal examination  to  rule  out  general  contraindications  and  a  suit- 
able inquiry  to  ascertain  the  possible  presence  of  specific  con- 
traindications for  the  drug  of  choice.  General  contraindications 
include  febrile  conditions,  extreme  youth  or  old  age,  chronic 
debilitating  diseases,  pregnancy,  gastro-intestinal  disturbances, 
chronic  constipation  and  alcoholism.  The  presence  of  one  or 
more  of  these  conditions  does  not  necessarily  mean  that  treat- 
ment should  be  withheld  but  it  does  mean  that  due  regard 
should  be  taken  with  respect  to  the  type  of  drug  and  the  dosage 
employed.  The  practitioner  must  decide  whether  the  injury 
from  parasitism  is  sufficient  to  warrant  the  risks  attendant  on 
treatment  and  must  weigh  the  advisability  of  substituting  a 
less  specific  but  safer  drug  for  a  more  specific  but  more  dan- 
gerous drug.  In  patients  who  are  poor  risks  for  adciiuate  doses 
of  specific  drugs,  it  is  advisable  to  reduce  the  dose  and  remove 
a  few  worms  at  a  time  rather  than  hazard  injury  to  the  patient. 
In  persons  with  severe  hookworm  disease,  it  is  questionable 
whether  anthelmintic  treatment  should  be  resorted  to  until  the 
anemia   has   been   corrected   by   .suitable   doses   of   iron. 

In  particular,  doses  of  anthlemintics  for  children  should  be 
computed  very  carefully  and  apparent  age  rather  than  chrono- 
logical age  should  form  the  basis  of  computation.  Since  the 
evacuation  habits  of  children  are  not  always  regular,  the  ad- 
ministration of  a  high  soapsuds  enema  on  the  morning  of 
treatment  often  helps  to  prevent  reactions  to  such  anthelmin- 
tics  as   the   chlorinated   hydrocarbons. 


336 


The  pr;u-liti(iiu'r 's  iibligatiiiii  t(i  tlic  |i;itieTit  has  not  been 
fiiltilli'd  until  a  suitablo  cliofk  is  made  on  the  results  of  the 
tioatiui'iif.  In  the  case  of  most  parasites,  it  is  advisable  to 
wait  two  weelis  before  a  reexamination  since  some  anthelmin- 
tics definitely  inhibit  egg  production  in  some  parasites.  With 
such  a  specialized  [larasite  as  Enlfrobiiis  vcrniicularis  a  longer 
period  of  time  is  needed  to  determine  freedom  from  infection 
following  treatment.  In  evaluating  the  efficacy  of  any  treat- 
ment due  cognizance  slionld  be  taken  of  the  possibilities  of  mi 
grating  larvae  developing  to  maturity  and  also  of  possible 
exposure  to  reinfection  following  treatment. 

Choice  of  tub  Anthelminxic.  An  ideal  anthelmintic  would 
be  one  which  could  be  given  with  complete  safety  to  the  pa- 
tient; would  be  nontoxic  in  all  cases;  would  be  effective  in  re 
moving  all  of  the  i^articnlar  kind  or  kinds  of  worms  against 
which  it  was  directed;  could  be  easily  administered  even  in 
large  scale  treatments;  and  would  be  sufficiently  cheap  that 
cost  would  be  no  obstacle  to  its  use. 

In  spite  of  the  exuberant  enthusiasm  of  some  investigators, 
the  ideal  anthelmintic  has  yet  to  be  discovered.  Drugs  which 
on  first  test  seem  to  fulfill  such  specifications  are  usually  found 
wanting  in  some  rcsjject  when  submitted  to  adequate  field  trials 
on  large  numbers  of  individuals. 

Keeping  in  mind  the  general  specificity  of  anthelmintics,  it  is 
best  to  select  the  most  effective  drug  available  provided  no 
general  or  specific  contraindications  exist  for  the  use  of  that 
specific  drug.  If  contraindications  are  present,  they  usually 
modify  either  the  selection  of  the  anthelmintic  or  the  dose  em- 
ployed. The  presence  of  more  than  one  nematode  parasite  or 
concomitant  infections  with  cestode  or  trematode  parasites  fre- 
quently changes  the  picture.  In  the  latter  case  the  administra- 
tion of  a  single  drug  will  seldom  be  effective  in  eradicating  such 
diverse  helminths.  Even  in  multiple  nematode  infections  treat- 
ment with  a  single  anthelmintic  may  not  be  effective.  In  the 
case  of  certain  parasites,  a  combination  of  two  drugs  may  be 
of  value  such  as  the  chenopodium-tetrachlorethylene  mixture  in 
concomitant  ascarid  and  hookworm  infectious  in  man.  In  other 
cases,  different  kinds  of  parasites  have  to  be  attacked  by  means 
of  separate  treatments. 

One  method  of  attack  has  been  suggested  as  being  of  value 
for  the  removal  of  all  intestinal  helminths  in  certain  animals. 
DeRivas  (1926,  1S>27.  1936)  advocated  the  use  of  trans-duodenal 
lavage  with  hot  water  or  hot  saline  for  parasites  in  the  small 
intestine  and  colonic  lavage  with  l:.'iOOO  copper  sulphate  solu- 
tion for  parasites  in  the  large  bowel.  He  carried  out  experi- 
ments on  dogs  and  man  and  reported  that  the  use  of  two  liters 
of  hot  saline  at  temperatures  of  4.5°  to  47°  C.  resulted  in  the 
elimination  of  worms  with  little  discomfort  to  the  patient.  Hall 
and  Shillinger  (1926)  used  the  method  on  dogs  with  water 
having  an  initial  temperature  of  49°  to  .52°  C.  in  the  container 
and  cooled  to  47°  to  48°  C.  at  the  time  of  administration.  The 
use  of  2  to  4  gallons  of  fluid  resulted  in  an  efficacy  of  97.7 
percent  against  ascarids,  77  percent  against  hookworms  and 
51.6  percent  against  tapeworms.  However,  the  treatment  re- 
sulted in  the  death  of  half  the  experimental  dogs  and  was  re- 
sponsible for  hemorrhage,  enteritis  and  intestinal  edema  in 
those  surviving.  The  safety  of  this  method  of  treatment  does 
not  seem  to  be  well  established  and  perhaps  for  this  reason 
the  technique  has  never  become  popular. 

Somewhat  the  same  method  of  treatment  was  used  by  Whit- 
ne3-  (1939)  for  removing  various  species  of  intestinal  parasites 
from  dogs.  He  employed  a  1.5  percent  solution  of  hydrogen 
peroxide  in  warm  water  and  injected  this  solution  per  rectum 
under  pressure  until  the  act  of  vomiting  indicated  that  the 
material  had  passed  through  the  entire  gastro  intestinal  tract. 
The  treatment  was  said  to  be  highly  effective  against  all  of 
the  helminth  parasites  commonly  found  in  the  gastrointestinal 
tract  of  the  dog.  Reactions  were  encountered  in  some  of  Whit- 
ney's cases.  Serious  after  effects  in  the  form  of  gastro  enteritis 
and  paralysis  have  since  been  reported  by  some  veterinarians 
following  the  use  of  the  treatment.  Apparently,  the  treatment 
does  not  have  an  adequate  margin   of  safety. 

PURQ.^TION.  The  administration  of  a  purgative  in  connection 
with  anthelmintic  medication  is  of  the  utmost  importance  in 
the  case  of  most  drugs.  Usually  the  purgative  acts  to  promote 
the  efficiency  of  the  anthelmintic  by  distributing  it  throughout 
the  intestinal  tract  and  by  aiding  in  the  prompt  expulsion  of 
the  parasites.  In  most  cases,  purgation  is  of  marked  value  in 
safeguarding  the  patient  by  reducing  the  absorption  of  the 
anthelmintic.  Some  purgatives  also  give  local  protection  against 
the   irritating  action   of   certain   drugs. 

The  choice  of  the  purgative  is  conditioned  by  the  method 
of  treatment  and  the  drug  or  drugs  employed.  The  use  of  the 
chlorinated  hydrocarbon  group  of  anthelmintics  requires  the 
administration  of  saline  purgatives,  since  fats  and  oils  tend  to 
increase  the  ab.sorption  of  such  compounds,  a  thing  which  re- 
sults in   more  marked  reactions   to  the  treatment.    In   the  ease 


of  oil  of  chenopodium,  castor  oil  is  the  purgative  of  choice 
even  though  saline  jiurgatives  have  been  used  with  this  drug. 
Castor  oil  not  only  i)romotes  promjit  expulsion  of  the  drug 
and  reduces  absorption  but  it  also  exerts  a  local  emollient  ac- 
tion and  protects  the  intestinal  mucosa  against  the  irritating 
properties   of   chenopodium. 

Purgatives  are  usually  administered  concomitantly  with  the 
anthelmintics  but  practice  in  this  regard  varies  with  the  host, 
the  parasite  and  the  drug  employed.  In  treating  large  numbers 
of  hookworm  patients  at  one  time,  it  is  customary  to  give 
carbon  tetrachloride  or  tetrachlorethylene  in  a  solution  of 
magnesium  or  sodium  sulphate.  However,  in  this  case  the  drug 
may  be  given  in  gelatin  capsules  and  immediately  preceded  or 
followed  by  the  purgative.  In  the  treatment  of  Ascaris  infec- 
tions in  man  w'ith  hexylresorcinol,  it  is  the  usu.al  practice  to  ad- 
minister the  purgative  24  hours  after  the  drug.  Calomel  has 
always  been  the  time  honored  purgative  for  use  with  santonin 
but  it  is  probable  that  better  results  would  follow  the  employ- 
ment of  a  saline  purgative. 

Adequate  protection  presupposes  the  administration  of  full 
doses  of  the  purgative.  Perhaps  more  injury  has  followed  the 
use  of  inadequate  doses  of  purgatives  in  connection  with  anthel 
mintics  than  has  come  from  over  dosing  with  the  anthelmintics 
themselves.  By  this  we  mean  that  over  doses  of  anthelmintics 
will  frequently  be  tolerated  if  accompanied  by  adequate  doses 
of  purgatives  whereas  many  fatalities  have  resulted  from  stand 
ard  doses  of  certain  anthelmintics  used  without  adequate  pur- 
gation. Therefore,  in  using  nearly  all  anthelmentics,  attention 
should  be  given  to  gauging  accurately  both  the  dose  of  the 
anthelmintic   and   the   dose   of   the   purgative. 

In  event  that  adequate  purgation  does  not  ensue  within  a 
reasonable  time,  prompt  measures  must  be  taken  to  protect  the 
patient.  High  enemas  should  be  resorted  to  and,  if  necessary, 
an  additional  dose  of  the  purgative  should  be  given  by  duo 
denal  tube.  Warm  applications  to  the  lower  extremities  and 
to  the  abdomen  will  hasten  evacuation.  The  point  of  most  im- 
portance in  such  circumstances  is  the  rapid  institution  of  cor- 
rective measures.  Every  effort  should  be  made  to  stimulate 
bowel  movements  and  promote  prompt  expulsion  of  the  anthel- 
mintic. If  the  patient  is  permitted  to  go  unaided,  increased 
absorption  of  the  anthelmintic  will  ensue  and  the  life  of  the 
individual  may   be  endangered. 

No  doubt  much  of  the  distress  following  the  administration 
of  many  anthelmintics  is  caused  by  the  purgative  and  not  by 
the  anthelmintic.  Malloy  (1926)  showed  that  the  nausea,  dizzi- 
ness, headache  and  abdominal  pain  following  the  administration 
of  carbon  tetrachloride  in  magnesium  sulphate  solution  was 
due  in  most  cases  to  the  purgative  and  not  to  the  anthelmin- 
tic. Wright,  Bozicevich  and  Gordon  (1937)  found  that  reac- 
tions to  the  tetrachlorethylene  treatment  in  children  were 
markedly  reduced  when  magnesium  citrate  solution,  a  more 
pleasant  and  palatable  purgative,  was  used  instead  of  mag- 
nesium sulphate.  In  most  cases,  the  symptoms  described  above 
are  not  alarming  and  usually  pass  off  rapidly  after  the  bowels 
move. 


Anthelmintic   Medication   for   Nematode   Parasites 
of  Man 

TREATMENT   TOR   ASCARIS    LUMBRICOIDES    INFTtCTION 

HEXYLRESORriNOL.  This  is  the  drug  of  choice  since  it  is 
highly  effective  and  is  safer  than  other  drugs  formerly  em- 
ployed for  this  purpose. 

Proper  fasting  is  important  since  hexylresorcinol  combines 
with  protein  and  is  rendered  inert  insofar  as  its  anthelmintic 
action  is  concerned.  The  patient  should  be  given  a  light  sup- 
per on  the  evening  before  treatment  and  the  drug  should  be 
administered  on  an  empty  stomach  the  following  morning. 
Hexylresorcinol  is  used  in  the  form  of  Caprokol  pills,  each  of 
which  contains  0.2  gram  of  the  drug.  The  dosage  for  adults 
consists  of  5  pills  or  a  total  of  1.0  gram.  The  dosage  for 
children  is,  as  follows:  Under  six  years,  2  pills;  six  to  eight 
years,  3  pills;  eight  to  twelve  years,  4  pills;  over  twelve  years, 
.5    pills. 

The  pills  should  be  swallowed  with  a  little  water;  special 
care  should  be  taken  that  they  are  not  chewed  since  the  drug 
is  a  local  irritant  and  produces  annoying  burns.  Children  in 
particular  should  be  observed  closely  to  make  sure  that  the 
pills  are  properly  swallowed.  Food  should  be  withheld  for  4 
hours  following  administration  of  the  drug.  A  saline  purga- 
tive should  be  given  24  hours  after  treatment  to  sweep  out 
the  dead   worms. 

As  a  usual  thing  there  is  little  or  no  discomfort  from  the 
drug  although  some  patients  may  complain  of  nausea  and 
slight  abdominal  pain.  Occasionally  a  slight  burning  sensation 
in  the  epigastrium  is  noted  but  this  soon  passes  off. 


337 


There  are  no  well  established  contraindications  for  hexylre- 
soreinol  therapy.  However,  it  is  advisable  for  the  patient  to 
abstain  from  alcohol  immediately  before  and  after  treatment. 
As  a  precautionary  measure,  it  is  probably  well  to  avoid  treat- 
ing persons  suffering  from  gastric  or  duodenal  ulcer  and  any 
form    of    gastroenteritis. 

Oil  of  Chenopodium.  This  drug  has  had  widespread  appli- 
cation in  the  treatment  of  aseariasis  and  hookworm  disease 
but  its  margin  of  safety  is  small  and  it  has  prol>ably  been  re- 
sponsible for  more  fatalities  than  any  other  single  anthelmin- 
tic.   However,  its  efficacy  against  ascarids  is  very  high. 

The  active  principle  of  chenopodium  is  ascaridol  which  varies 
in  content  with  different  oils.  Effort  has  been  made  to  stand- 
ardize the  ascaridol  content  at  70  percent  in  order  to  have 
available  a  uniform  product  but  various  oils  on  the  market 
may  vary  in  the  content  of  the  active  principle. 

In  using  chenopodium,  the  ijatient  should  be  given  a  light 
evening  meal.  If  constipated,  a  saline  purge  is  indicated  fol- 
lowed by  a  high  soapsuds  enema  the  next  morning.  These  pre- 
cautions are  important  in  the  ease  of  constipated  individuals 
since  chenopodium  itself  tends  to  produce  constipation. 

The  drug  is  given  on  an  empty  stomach  and  no  food  should 
lie  allowed  until  the  bowels  move.  The  adult  dose  should  not 
exceed  1.5  ce.  The  dose  for  children  is  based  on  0.0.3  ce.  for 
each  year  of  apparent  (not  chronological)  age.  The  drug  may 
be  given  in  gelatin  capsules  and  immediately  preceded  or  fol- 
lowed by  adequate  dose  of  a  saline  purgative.  Some  authorities 
recommend  dividing  the  dose  into  two  jiarts  and  administering 
the  doses  2  hours  apart,  in  which  case  the  purgative  is  given  im- 
mediately after  the  last  dose.  If  the  patient  shows  any  signs 
of  reaction,  the  second  half  of  the  dose  should  be  omitted  and 
the  purgative  given  immediately.  The  advisability  of  the  split 
dose  method  is  problematical  since  increased  absorption  and 
toxicity  may  result  when  the  purgative  is  thus  delayed. 

The  preferred  method  of  administering  chenopodium  is  to 
mix  it  with  castor  oil  and  give  as  a  single  dose.  One  to  2  ce. 
of  castor  oil  should  be  given  for  each  year  of  apparent  age 
in  children.  The  larger  dose  provides  more  adequate  protection. 
The  oil  not  only  produces  adequate  purgation  but  protects  the 
intestinal  mucosa  against  the  irritating  action  of  the  drug. 

When  chenopodium  is  measured  by  the  drop  method,  there  is 
a  wide  variation  in  dosage.  Measurement  should  be  made  by 
a  standard  1  cc.  pipette  graduated  into  tenths  in  order  to 
avoid   errors   in    dosage. 

Toxic  symptoms  manifested  in  chenopodium  poisoning  are 
nausea,  vomiting,  dizziness,  a  tingling  sensation  of  the  ex- 
tremities, muscular  incoordination,  stupor,  profound  collapse, 
cyanosis  and  respiratory  failure  followed  by  death.  Severe 
and  even  permanent  deafness  may  result.  If  purgation  does 
not  ensue  within  a  reasonable  time,  strenuous  efforts  should  be 
made  to  evacuate  the  bowels  as  promptly  as  possible.  Any  delay 
in  instituting  rigorous  measures  maj'  seriously  endanger  the  life 
of  the  patient. 

Contraindications  for  chenopodium  therapy  include  gastro- 
enteritis, chronic  constipation,  alcoholism,  pregnancy,  deljilitat- 
ing  diseases,  and  moderate  to  severe  cardiovascular-renal  dis- 
ease. Very  young  children  or  aged  individuals  are  poor  risks 
for  treatment. 

S.'INTONIN'.  Santonin  is  a  time  honored  remedy  for  the  re- 
moval of  large  intestinal  roundworms,  although  its  efficacy  in 
single  doses  does  not  approach  that  of  either  hexylresorcinul 
or  oil  of  chenopodium.  However,  it  is  non-irritating  and  easily 
administered  and  can  be  used  to  advantage  when  there  are  defi- 
nite reasons  for  avoiding  the  two  other  drugs. 

The  patient  should  be  given  a  light  evening  meal  and  the 
dose  of  santonin  administered  with  an  equal  amount  of  calomel 
at  10.00  p.m.  The  next  morning  before  breakfast,  a  saline 
purgative  should  be  given.  The  dose  of  santonin  for  adults  is 
3  to  5  grains  (0.2  to  0.3  gram).  For  children,  the  dose  rate  is 
based  on  1/6  grain  (0.01  gram)  for  each  year  of  apparent  age. 
Santonin  is  more  effective  when  given  in  repeated  treatments 
over  a  period  of  time.  A  satisfactory  routine  is  to  give  1  to  2 
grains  (0.06  to  0.12  gram)  for  adults"  and  %  to  %  grain  (0.015 
to  0.03  gram)  for  children  daily  over  a  period  of  7  days.  The 
drug  is  given  with  an  equal  amount  of  calomel  and  no  other 
purgative  employed.  With  continued  treatment,  the  patient 
should  be  observed  carefully  for  any  evidence  of  toxicity. 

Santonin  is  responsible  in  some  cases  for  disturbances  in 
perception  and  there  may  result  yellow,  green,  and  occasion- 
ally, blue  vision.  Symptoms  of  toxicity  are  evidenced  by  nau- 
sea, vomiting,  dizziness,  diarrhea,  hematuria  and  convulsions. 
The  drug  is  contraindicated  in  nervous  disorders  such  as  epi- 
lepsy. Fats  and  oils  should  be  avoided  as  they  increase  ab- 
sorption. The  factor  of  safety  for  santonin  is  considerably 
greater  than  that  for  chenopodium  but  the  drug  is  not  without 
its  hazards.  Some  authorities  recommend  that  a  single  dose  of 
3   grains  for  adults  be   not   exceeded. 


TREATMENT    FOR    THE    KE.MOVAL    OF    HOOKWORMS,    ANCYLOSTOM.^ 
DUODENALE  AND   NEGATOR  AMERICANTJS 

TBTRACHLORf;THYLENE.  Because  of  its  greater  safety,  this 
drug  is  largely  replacing  carbon  tetrachloride  and  other  treat- 
ments for  hookworm  disease. 

The  patient  should  be  given  a  light  evening  meal  and  should 
receive  the  drug  on  an  empty  stomach  the  following  morning. 
No  food  should  be  allowed  until  aftei-  the  bowels  move.  The 
dose  for  adults  is  3.0  ec.  and  for  children  0.1  to  0.2  ec.  for 
each  year  of  apparent  (not  chronological)  age.  Better  results 
are  obtained  with  a  dose  of  4.0  cc.  for  adults  but  the  larger 
dose  is  apt  to  be  followed  by  more  severe  reactions.  The  drug 
may  be  administered  in  gelatin  capsules  followed  immediately 
by  an  adequate  dose  of  magnesium  or  sodium  sulphate.  In 
mass  treatment,  tetrachlorethylene  is  given  with  the  purgative. 
In  such  cases,  the  mixture  should  be  stirred  while  the  patient 
is  drinking  it  so  that  the  tetrachlorethylene  will  be  distributed 
evenly  throughout  and  not  sink  to  the  bottom  of  the  container. 
The  purgative  should  lie  dissolved  in  a  liberal  amount  of  water. 
One  of  the  preferred  methods  is  to  use  30  ec.  of  a  saturated 
solution  of  the  saline  purgative  plus  60  cc.  of  water  for  an 
adult  patient.  As  previously  noted,  a  solution  of  magnesium 
citrate  meets  with  less  objection  on  the  part  of  children  and 
apparently  causes  less  disagreeable  reactions.  In  constipated 
individuals,  it  is  best  to  give  a  saline  purgative  the  night  be- 
fore treatment  followed  the  next  morning  by  a  high  soapsuds 
enema. 

In  the  hands  of  various  investigators,  tetrachlorethylene  has 
sliown  a  degree  of  efticacy  varying  between  75  and  95  percent. 
T^ike  carbon  tetrachloride,  it  is  more  effective  against  Necator 
than    against    Ancylci.il oma. 

Following  treatment,  patients  frequently  complain  of  dizzi- 
ness, headache,  nausea,  vomiting  and  abdominal  pain.  Experi- 
ence indicates  that  these  reactions  are  less  severe  if  the  pa- 
tient remains  quietly  in  bed  and  for  safety's  sake  it  is  best 
to  insist  on  his  doing  so.  Reactions  usually  disappear  rapidly 
following  action  of  the  jiurgative.  If  the  bowels  do  not  move 
within  the  expected  period  of  time  or  if  minatory  symptoms 
develop,  prompt  measures  should  be  taken  to  hasten  evacuation. 

Tetrachlorethylene  is  contraindicated  in  cases  of  gastro- 
enteritis, chronic  constipation  and  concomitant  infections  with 
A.tcaris  himbricoidrs.  Fats  and  oils  should  lie  withheld  from 
the  diet  for  48  hours  prior  to  the  administration  of  the  drug 
since  they  increase  absorption  and  add  to  the  toxicity.  Pa- 
tients  receiving   arsenical   treatments  are   poor   risks. 

Hexyresorcinol :  This  drug,  administered  as  for  Ascaris,  is 
about  50  to  60  percent  effective  for  the  removal  of  hookworms. 
Because  of  its  relatively  wide  margin  of  safety,  it  can  be 
used  to  advantage  in  cases  in  which  the  physician  might  hesi- 
tate to  employ  tetrachlorethylene. 

TREATENT  FOR  CONCOMITANT  ASCARIS   AN"D  HOOKWORM 
INFECTIONS 

Tb;trachlorethvi,ene  and  Oil  of  Chenopodium.  A  mixture 
of  these  two  drugs  can  be  used  in  cases  in  which  both  kinds  of 
parasites  are  present.  By  itself,  tetrachlorethylene  should  not 
lie  given  when  Axcaris  is  present  because  the  drug  tends  to 
stimulate  clumping  of  the  worms  with  possible  intestinal  ob- 
struction. 

The  dosage  of  the  mixture  for  adults  is  1.0  cc.  of  oil  of 
chenopodium  plus  2.0  cc.  of  tetrachlorethylene.  For  children, 
the  dose  rate  is  based  on  0.05  ec.  of  chenopodium  and  0.1  cc. 
of  tetrachlorethylene  for  each  year  of  apparent  (not  chrono- 
logical) age.  The  mixture  is  given  in  one  dose  and  followed 
immediately  by  a  saline  purgative  as  outlined  for  tetrachlor- 
ethylene. The  contraindications  and  precautions  are  those  noted 
in  connection  with  the  use  of  chenopodium  for  Ancaris. 

Hexylresorcinol.  Because  of  its  greater  safety,  this  drug 
is  to  be  preferred  over  the  above-mentioned  mixture  for  the 
treatment  of  combined  hookworm  and  A.trarix  infections.  The 
method  of  administration  is  the  same  as  tli:it  for  the  latter 
]iarasite. 

treatment    for    trichuris    trichiura    infection 

While  various  anthelmintics  in  single  doses  will  remove  a 
small  percentage  of  these  worms,  treatment  is  generally  un- 
satisfactory. Repeated  doses  of  santonin,  as  outlined  under 
therapy  for  Aficaris  himbricoidcf!,  represent  the  most  practical 
treatment  at  the  present  time.  Even  this  regimen  of  treatment 
may  have  to  be  repeated  on  several  different  occasions  to  ap- 
proach  any  considerable   degree   of   efficacy. 

Hexylresorcinol  and  tetrachlorethylene  each  will  remove  small 
numbers  of  worms,  as  will  oil  of  chenopodium.  Leche  de 
higueron,  the  sap  of  the  Central  and  South  American  fig  tree, 
Ficv.i  Jaiirifolia,  is  a  fairly  effective  treatment  when  given  in 
doses   of   30   to   60   ce.     However,   this   material    is   not   usually 


338 


availnliU'  oiitsuk'  of  tlic  iiativi'  lialiitat  of  the  tiou  siiu-o  thv 
sap  undoigoi's  rapid  fcriiu'iitatioii  ami  becomes  very  uiipalata 
ble  at  ordinary  temperatures.  Kffort  is  being  made  to  preserve 
the  material  in  a  way  whieli  will  jiermit  of  its  transportation 
and  storage.  Fiein,  the  proteolytic  enzyme  isolated  from  the 
sap  by  Robbins.  cannot  be  used  safely  in  man  because  of  its 
marked  jiroperty  of  digesting  the  mucosa  of  the  gastro-intesti- 
nal  tract   in   the  presence  of  abrasions. 

TKK.VTIIK.NT  FOR   STRONG YLOIBES   STERCORjUjlS   INFECTION' 

Kwa  Tjaon  Sioe  (1928)  and  de  Langen  (1928)  introduced 
gentian  violet  for  the  treatment  of  infectious  with  this  para- 
site and  the  treatment  was  further  developed  by  Faust  (l!t30). 
For  adults,  Faust  recommends  a  dose  of  1  grain  (04  mgm.) 
three  times  a  day  before  meals  over  a  period  of  10%  days  or  a 
total  dose  of  CO  grains.  For  children,  the  drug  ma.v  be  given 
at  the  rate  of  1/0  grain  (10  mgm.)  per  day  for  each  year 
of  apparent  age  or  approximately  V2  grain  (32  mgm.)  for  each 
3  years  of  apparent  age,  given  over  a  similar  period  of  time. 
Gentian  violet  is  procurable  in  %  grain  and  3/20  grain  enteric- 
coated  or  water  soluble  coated  tablets. 

Some  Sirongyloidcs  cases  are  refractory  to  oral  therapy  with 
gentian  violet  and  for  such  cases  Faust  recommends  the  duo 
deual  intubation  of  2."i  cc.  of  a  1  percent  solution  of  the  dye. 
The  patient  should  remain  quietly  in  bed  after  this  treatment 
as  nausea  and  vomiting  are  apt  to  ensue. 

About  one-third  of  the  patients  treated  with  gentian  violet 
experience  reactions  consisting  of  one  or  more  of  the  follow- 
ing symptoms:  Nausea,  vomiting,  diarrhea,  headache,  dizziness 
and  abdominal  pain.  These  reactions  are  usually  not  of  a  seri- 
ous character  and  can  be  controlled  by  reducing  the  dosage 
for  a  short  time  or  discontinuing  treatment  for  a  day  or  two. 

Contraindications  for  gentian  violet  are  not  clearly  defined 
but  as  a  precautionary  measure  the  drug  should  not  be  given 
to  patients  suffering  from  gastroenteritis,  moderate  to  severe 
cardiac,  hepatic  or  renal  disease  and  concomitant  infections 
with  Asearis  liimbricoidcs.  Pregnant  women  are  apt  to  be 
markedly  nauseated  by  the  treatment.  The  consumption  of 
alcohol  should  be  prohibited   during  the  period  of  treatment. 

TREATMENT    TOR    ENTEROBIUS     VERMICULARIS     INFECTION 

The  ease  with  which  many  individuals  become  constantly  re- 
infected with  pinworms  makes  eradication  of  the  parasite  an 
extremely  difficult  matter.  The  failure  in  many  cases  to  achieve 
control  by  the  rigid  application  of  hygienic  measures  calls 
for  supplementing  such  measures  in  most  cases  with  suitable 
therapeutic    procedures. 

It  is  probable  that  man3'  of  the  failures  to  control  pinworm 
infection  are  attendant  on  the  fact  that  treatment  is  usually 
administered  only  to  those  persons  in  the  household  who  show 
clinical  symptoms.  Frequently,  other  members  of  the  family 
may  be  infected  without  being  aware  of  the  fact.  Under  such 
circumstances,  these  persons  serve  as  reservoirs  of  infection 
which  is  again  acquired  by  the  treated  individuals.  Wright  and 
Cram  (1937)  have  emphasized  tlu>  importance  of  carr.ying  out 
adequate  diagnostic  tests  on  all  members  of  a  household  and 
treating  all  infected  individuals  simultaneously  with  the  view 
of  eliminating  at  one  time  all  sources  of  infection  within  tin- 
home. 

The  literature  probably  contains  a  greater  array  of  drugs 
recommended  for  the  removal  of  pinworms  than  for  any  other 
parasite.  Single  dose  treatments  are  not  well  adapted  for 
combating  this  parasite.  Tetrachlorethylene,  probably  the  best 
of  these,  is  less  than  .50  percent  effective.  In  general,  better 
results  follow  the  employment  of  repeated  doses  of  drugs  over 
a  period  of  time  sufficient  to  allow  for  desiccation  of  ova  in 
the  patient's  surroundings  and  thus  reduce  opportunities  for 
reinfection. 

Santonin  in  repeated  doses  as  for  Asearis  has  been  used  fre- 
quently, although  its  efficacy  is  somewhat  less  than  50  percent. 
Enemas,  medicated  or  non-medicated,  are  of  value  particularly 
in  young  children  but  they  must  be  carried  over  a  period  of 
time  sufficient  to  care  for  the  possibilities  of  reinfection. 

Brown  (1932)  obtained  good  results  in  a  small  series  of  pa- 
tients with  hexylresorcinol  enemas  administered  at  varying 
intervals  and  supplemented  by  oral  therapy  with  Caprokol 
pills.  Wright,  Brady  and  Bozicevicli  (1!I39)  treated  27  patients 
without  oral  therapy  and  found  18  negative  on  post-treatment 
swabs,  although  some  of  the  negative  patients  failed  to  fur- 
nish an  adequate  number  of  such  swabs.  A  preliminary  soap- 
suds enema  was  given  at  bedtime  followed  immediately  after 
its  expulsion  by  an  enema  consisting  of  a  1:2000  solution  of 
hexylresorcinol  in  water.  The  above-mentioned  workers  found 
that  satisfactory  results  in  most  cases  required  the  administra- 
tion of  at  least  10  such  enemas  over  a  period  of  3  weeks.  No 
doubt    more    consistent    results    would    follow   more    prolonged 


treatment,  it  is  possible  that  Caprokol  orally  once  or  twice- 
during  the  jjcriod  of  treatment  would  add  to  the  efficacy  of 
the  regimen,  although  the  preparation  in  single  doses  is  not 
effective    in    eradicating    the    worms. 

It  would  appear  that  the  drug  coming  closest  to  fulfilling 
the  requirements  for  a  satisfactory  treatment  for  oxyuriasis  is 
gentian  violet  as  reported  by  Wright,  Brady  and  Bozicevich 
(1938)  and  Wright  and  Brady  (l!i40).  These  investigators 
completed  experimental  treatment  on  224  individuals,  of  whom 
84  percent  were  negative  for  pinworm  ova  on  7  consecutive 
daily  anal  swab  examinations  taken  at  various  intervals  after 
the  end  of  the  treatment. 

The  dosage  for  gentian  violet  is  the  same  as  that  used  for 
the  treatment  of  strongyloidosis.  However,  the  regimen  of 
treatment  is  somewhat  different,  the  patient  being  given  the 
drug  over  a  period  of  8  days,  foUow-ed  by  a  rest  period  of  one 
week  and  then  another  course  of  treatment  for  8  days.  The 
contraindications  and  precautions  are  the  same  as  those  out 
lined  under  therapy   for  strongyloidosis. 

Recently  Manson  Bahr  (1940)  reported  good  results  in  the 
treatment  of  pinwoi-m  infection  with  phenothiazine.  Of  6  chil- 
dren and  3  adults,  clinical  cures  were  said  to  have  been  ob- 
tained in  all  cases,  although  3  individuals  required  a  second 
course  of  treatment.  The  following  dosage  was  recommended: 
For  children  under  8  years  of  age,  2  grams  daily'for  7  days; 
for  children  under  4  years  of  age,  one  half  of  the  above-men- 
tioned dose;  and  for  adults,  8  grams  daily  for  at  least  5  days. 
In  the  cases  in  question,  results  of  treatment  were  not  checked 
by  swab  technique  or  other  methods  to  determine  disappear- 
ance of  infection.  Nothing  is  said  in  Manson-Bahr 's  paper  con- 
cerning the  dangers  of  blood  dyscrasias  from  the  use  of  pheno- 
thiazine, although  DeEds,  Stockton  and  Thomas  (1939)  re- 
ported the  occurrence  of  secondary  anemia  in  3  of  49  patients 
given  phenothiazine  as  a  urinary  antiseptic.  The  maximum  to- 
tal dose  recommended  by  Manson-Bahr  is  greatly  in  excess  of 
that  specified  by  DeEds,  Stockton  and  Thomas  as  being  with 
in  the  limits  of  safety.  It  would  seem  that  this  treatment 
should  he  used  with  considerable  caution. 

TREATMENT  FOR  WUCHERERIA   BANCROFTI   INFECTION 

There  is  no  specific  medication  for  this  condition.  Various 
drugs  have  been  reported  as  being  of  value  for  the  destruc- 
tion of  the  microfilariae  or  preventing  their  appearance  in  the 
peripheral  circulation.  However,  evidence  for  the  efficiency  of 
such  drugs  is  meager  as  in  many  cases  the  larvae  reappear  later. 
There  is  no  known  drug  effective  for  the  destruction  of  the 
adult    worms. 

Chopra  and  Sundar  Rao  (1939)  have  reported  on  tests  ex- 
tending over  10  years  with  patients  treated  with  a  large  num- 
ber of  different  drugs  at  the  Calcutta  School  of  Tropical  Medi- 
cine. None  of  the  compounds  employed  was  of  value  in  effect 
ing  the  destruction  of  adult  or  larval  worms.  Soamin,  an  ar- 
senical preparation,  reduced  the  number  of  febrile  and  in- 
flammatory attacks.  Fouadin  had  a  temporary  sterilizing  ef 
feet  on  the  parasite  but  microfilariae  reappeared  in  the  blood 
after  several  days.  However,  the  drug  was  said  to  be  very 
useful  in  controlling  inflammation  and  fever  over  comparatively 
long  periods  of  time.  In  a  few  cases,  chyluria  disappeared  even 
after  a  single  dose.  Prontosil  and  its  derivatives  were  found 
of   value   in    the   treatment   of   secondary   infection. 

Roentgen  ray  therapy  has  been  advocated  as  being  of  value 
in  filariasis  but  Golden  and  O'Connor  (1934)  were  unable 
to   obtain   consistently   promising   results. 

In  filarial  lymphangitis  and  elephantiasis,  surgical  interven- 
tion by  means  of  the  Auchincloss  technique  or  one  of  its  modifi- 
cations will  bring  some  temporary  relief.  Knott  (1938)  has 
advocated  prolonged  tight  bandaging.  The  use  of  the  method 
on  105  unselected  patients  in  his  series  indicated  apparently 
that  it  is  of  value  for  the  gradual  removal  of  the  lymphoedema 
and  in  the  prevention  of  the  recurrent  attacks  of  lymphangitis. 

Anti-streptococcal  vaccines  have  been  reported  to  be  effec- 
tive in  some  cases  but  O'Connor  (1932)  pointed  out  that  the 
relief  is  only  temporary  and  that  any  serum  or  vaccine  produces 
similar  relief,  indicating  probably  that  temporary  cure  is  due 
to  protein  shock  rather  than  to  specific  anti-bacterial  action. 

Anthelmintic    Medication    for    Nematode    Parasites    of 
Dogs,  Cats  and  Related  Carnivores 

TREATMENT    FOB   ASCAKID    INFECTIONS 

Tetrachlorethylene.  This  drug  in  a  dose  of  0.2  cc.  per 
kilogram  (2.2  pounds)  of  body  weight  is  effective  for  the  re- 
moval of  dog  ascarids.  In  using  chlorinated  hydrocarbons  in 
the  presence  of  heavy  ascarid  infections,  particularly  in  pup- 
pies and  young  dogs,  it  is  advisable  to  follow  the  anthelmintic 
in  3  or  4  hours  by  an  adequate  dose  of  castor  oil,  or  to  give 


339 


a  saline  purgative  immediately  following  the  treatment.  The 
purpose  of  this  is  to  prevent  clumping  of  the  ascarids,  which 
are  inordinately  stimulated  by  these  compounds,  and  a  possible 
intestinal  obstruction  which  sometimes  causes  enteritis,  necro- 
sis and  death.  Tetrachlorethylene  may  be  given  to  cats  at 
the  same  dose  rate  and  in  the  same  manner  as  for  dogs.  The 
drug  in  doses  of  1  cc.  has  been  reported  to  be  of  value  for  the 
removal  of  ascarids  from  foxes.  In  these  animals,  it  is  said 
to  cause  a  slight  enteritis  which  is  not  of  serious  consequence. 

Oil.  of  Chenopodium.  Xumerous  experiments  have  shown 
that  this  drug  is  very  effective  for  the  removal  of  ascarids 
from  dogs.  The  rate  of  dosage  is  0.1  ec.  per  kilogram  of  body 
weight  or  1.0  cc.  for  a  10  kilogram  (22pound)  dog.  For  prac- 
tical purposes,  this  can  be  regarded  as  equivali'iit  to  th.'  lol 
lowing  doses:  For  dogs  weighing  10  pounds  or  1  ss  (except  toy 
dogs),  5  minims;  for  dogs  weighing  10  to  20  pounds,  10 
minims;  for  dogs  weighing  20  to  30  pounds,  1.1  minims;  and 
for  dogs  weighing  over  30  pounds,  20  minims.  Toy  dogs  re- 
quire small  doses  and  considerable  precaution  should  be  ex- 
ercised in  treating  such  animals ;  a  dose  of  2  or  3  minims  is 
advisable.  The  dog  should  be  fasted  from  the  afternoon  of  the 
day  previous  to  treatment  and  should  be  dosed  the  following 
morning.  The  chenopodium  should  be  accompanied  by  at  least 
an  ounce  (30  cc.)  of  castor  oil.  It  is  not  advisable  to  give  the 
chenopodium  in  the  castor  oil.  as  chenopodium  is  salivating  and 
the  combination  produces  a  disagreeable  slobbering  effect.  For 
choice,  the  chenopodium  should  be  given  in  gelatin  capsules  and 
the  castor  oil  administered  immediately  before  or  after  the 
capsules.  The  animal  should  not  be  fed  until  3  hours  after 
treatment.  If  dogs  show  serious  toxic  effects,  large  additional 
doses  of  castor  oil  should  be  given  and  enemas  used  to  insure 
prompt  purgation.  The  contraindications  for  chenopodium  have 
been  discussed  in  connection  with  the  treatment  of  ascariasis 
in    man. 

Chenopodium  is  very  effective  for  the  removal  of  ascarids 
from  cats  but  the  drug  is  more  toxic  for  these  animals  than 
it  is  for  dogs.  The  dose  for  the  cat  should  not  exceed  O.O.")  ec. 
l)er  kilogram  (2.2  pounds)  of  body  weight,  immediately  pre- 
ceded or  followed   by   an   adequate  dose   of   castor   oil. 

For  fox  pups,  Young  (1930)  recommended  1-minim  doses  of 
oil  of  chenopodium  in  castor  oil  and  found  this  safe  for  pups 
3  weeks  old  and  effective  for  pups  up  to  8  weeks  of  age.  He 
preferred  not  to  treat   them   until   tlun-   were  4   weeks  old. 

Santonin.  When  there  are  contraindications  for  other  treat- 
ments, santonin  in  repeated  doses  may  be  used  to  remove  as- 
carids from  dogs.  Experiments  show  that  single  doses  of 
santonin,  even  very  large  doses,  such  as  '2  grain  for  each 
pound  of  body  weight,  are  less  effective  than  a  single  thera- 
peutic dose  of  chenopodium,  but  that  smaller  doses  of  santonin 
daily  for  several  days  gives  very  good  results.  Small  dogs  may 
be  given  Vn  grain  of  santonin  and  an  equal  amount  of  calomel, 
and  large  dogs  double  this  dose,  daily  for  a  week.  Tliis  should 
be  given  early  in  the  morning  and  the  animal  not  fed  for  2  or 
3  hours.  As  previously  stated,  a  saline  purge  following  single 
doses  of  santonin  seoms  to  increase  materially  the  efficacy  of 
the   drug. 

N-BuTYL  Chloride.  The  administration  of  tetrachlorethylene 
to  dogs  is  frequently  followed  by  a  temporary  narcosis  which 
often  embarrasses  the  veterinarian  and  alarms  the  client.  Har- 
wood,  Jerstad,  Underwood  and  Schaffer  (1940)  are  of  the 
opinion  that  n-butyl  chloride  does  not  produce  such  reactions. 
For  the  removal  of  ascarids,  these  investigators  recommend  the 
following  dosages:  For  dogs  weighing  2.3  to  4..''i  kilos  (•")  to  10 
pounds),  2  cc;  4.."i  to  9  kilos  (10  to  20  pounds),  3  cc;  9  to  18 
kilos  (20  to  40  pounds),  4  cc;  and  18  or  more  kilos  (40  or 
more  pounds),  5  cc. 

Hextlresorcinol.  Lamson,  Brown  and  Ward  (1930)  have 
reported  that  hexylresorcinold  is  very  effective  for  the  removal 
of  dog  ascarids.  The  drug  is  given  in  doses  of  0.5  to  1  gram. 
With  hexylresorcinol,  it  is  necessary  to  withhold  food  for  12 
to  18  hours  before  treatment.  Animals  should  not  be  per- 
mitted to  crush  or  chew  capsules  or  pills  of  hexylresorcinol 
since,  as  previously  stated,  the  drug  is  irritant  to  the  mucosa 
of  the  mouth. 


TRE.\TMENT     FOR     HOOKWORM     INFECTION 

Tetrachlorethylene.  At  the  present  time,  this  is  the  drug 
of  choice  having  largely  replaced  carbon  tetrachloride  because 
of  the  toxicity  of  the  latter.  The  therapeutic  dose  rate  of 
tetrachlorethylene  for  dogs  and  cats  is  0.2  cc  per  kilogram 
(2.2  pounds)  of  body  weight,  or  2  cc.  for  a  10-kilogram  or  22- 
pound  animal.  It  is  usually  not  necessary  to  give  a  purgative 
in  connection  with  tetrachlorethylene,  but  a  purgative  is  ad- 
vantageous as  it  helps  to  sweep  out  worms  killed  by  the  treat- 
ment  and  to   eliminate  the   drug  rapidly   from  the  intestinal 


tract.  It  is  advisable  in  coneomitant  heavy  ascarid  infections, 
particularly  in  puppies,  to  follow  tetrachlorethylene  with  a 
suitable  dose  of  purgative.  However,  castor  oil  or  other  oils,  or 
fats,  should  not  be  given  immediately  preceding  or  following 
tetrachlorethylene  as  they  aid  in  tlie  al)sorption  of  the  drug. 
Tetrachlorethylene  has  the  disadvantage  of  causing  in  some 
cases  a  transient  vertigo  or  dizziness,  which  may  be  :ilarming  to 
the  owner  of  the  aninuil,  hut  which  in  fact  is  not  serious  and 
which  soon  passes  off.  For  this  reason,  as  mentioned  under  the 
section  on  the  treatment  of  ascarid  infection,  n  butyl  chloride 
may  be  used  in  place  of  tetrachlorethylene.  The  dosages  sug- 
gested for  the  removal  of  hookworms  are  the  same  as  those 
suggested  for  the   removal   of   ascarids   from  dogs. 

Tetrachlorethylene  can  be  used  to  advantage  in  the  removal 
of  U ncinaria  slenocrphala  from  foxes.  The  dosage  is  the  same 
as  that  for  dogs.  However,  foxes  do  not  tolerate  anthelmintic 
treatment  as  well  as  do  dogs,  and  particular  care  should  be 
taken  to  judge  accuratel.v  the  dosage  of  the  drug  and  to  ap- 
praise closely  the  possible  presence  of  contraindications  for 
treatment.  Care  should  be  taken  to  see  that  capsules  are  not 
broken  in  the  mouth,  as  inhalation  of  tetrachlorethylene  may 
lead  to   serious  complications,  particularly  in   fox  pups. 

He.xylresorcinol.  This  drug  can  be  used  to  advantage 
when  contraindications  for  other  treatments  are  present.  How- 
ever, its  efficacy  falls  below  that  of  tetrachlorethylene  and 
many  other  halogenated  hydrocarbons.  The  dosage  is  the  same 
as  that  given  under  treatments  for  the  removal  of  ascarids. 

TREATMENT  FOR  TRICHURIS   VULPIS   INFECTION 

Numerous  experiments  on  dogs  indicate  that  a  large  number 
of  anthelmintics  are  potent  in  the  removal  of  whipworms  but 
that  a  single  dose  of  such  drugs  will  rarely  remove  many 
whipworms.  The  failure  of  single  dose  treatments  is  no  doubt 
due  in  part  to  the  fact  that  the  anthelmintic  fails  to  enter  the 
cecum  or  enters  it  only  in  insufficient  amounts.  It  is,  therefore, 
necessary  to  give  a  drug  from  day  to  day,  until  it  does  come 
in  contact  with  the  worms  in  effective  doses,  or  to  give  large 
doses  of  relative^-  non -toxic  drugs  to  ensure  the  entry  of  the 
drug  into  the  cecum. 

Santonin.  For  the  [uirposes  of  repeated  treatments,  san- 
tonin is  a  very  satisfactory  drug  since  it  does  not  cause  gastro- 
intestinal irritation  even  when  given  over  a  period  of  time. 
The  drug  may  be  given  to  dogs  in  a  dose  of  '4  to  1  grain 
each  of  santonin  and  calomel,  according  to  the  size  of  the 
animal,  daily  for  7  days.  The  treatment  may  then  be  dis- 
continued and  repeated  after  an  interval  of  a  week. 

Leche  de  Higueron.  This  drug  has  been  described  under 
treatment  for  whipworms  in  man.  While  adequate  tests  have 
not  been  carried  out  to  estalilish  its  eflficac.v  for  the  removal 
of  T.  viilpix,  it  seems  jirobable  that  it  would  be  effective  for 
that  purpose.  However,  until  the  material  becomes  more  gen- 
erally available,  its  use  will  l)e  restricted  to  the  geographical 
areas  in   which  the  tree  is  indigenous. 

N  Butyl  Chioride.  Harwood,  Jerstad,  Underwood  and 
Schaft'er  (1640)  showed  n  butyl  chloride  to  be  over  .')0  percent 
effective  for  the  removal  of  whipworms.  While  this  degree  of 
efficacy  is  certainly  not  satisfactory,  these  workers  pointed  out 
that  the  drug  is  superior  nevertheless  to  anj-  other  single  dose 
treatment  known  at  present.  As  it  is  highl.v  eft'ective  for  the 
removal  of  ascarids  and  hookworms,  it  seems  worthy  of  trial 
in  whipworm  infections.  For  whipworms,  the  above-mentioned 
investigators  recommend  a  dose  of  3  to  o  cc.  for  dogs  weigh- 
ing ."1  pounds  or  less;  0  to  8  cc.  for  .j  to  10-pound  dogs;  10  to 
12  cc.  for  10  to  20-pound  dogs;  lo  cc  for  20  to  40-pound  dogs; 
and  2.J  cc.  for  dogs  weighing  over  40  pounds.  If  the  dog  is 
infected  with  ascarids,  a  saline  purgative  should  be  given  im- 
mediately following  the  anthelmintic* 

Other  Methods.  Hall  and  Shillinger  (1926)  found  that 
mercurochrome  gave  fairly  satisfactory  results  for  the  removal 
of  whipworms  from  dogs  when  the  drug  was  given  in  doses  of 
2  to  5  tablets  each  containing  l.'i  grains  (96  mgm.)  daily  for 
')  to  11  days.  The  drug  removed  273  of  311  whipworms  from 
9  dogs,  or  88  percent,  and  removed  all  whipworms  from  4  of 
6  infected  animals.  The  safet.v  of  this  treatment  has  not  been 
established.  Although  it  has  never  come  into  general  use,  it 
would  seem  worthy  of  trial. 

The  use  of  drugs  injected  into  the  cecum  by  means  of  a 
catheter  passed  per  rectum  has  been  advocated  for  the  removal 
of  whipworms.  However,  it  is  extremely  difficult  to  pass  a 
fiexable  rubber  tube  in  such  a  way  that  the  operator  has  any 
assurance  that  the  orifice  of  the  catheter  is  opjiosite  the  ori- 
fice of  the  cecum  and  that  the  drug  actually  enters  that  organ. 
In   critical   tests,   Underwood,   Wright   and    Bozicevich    (1931), 


*Chitwood  (personal  communication)  has  obtained  100  percent  effi- 
cacy for  whipworms  when  n.  butyl  chloride  was  administered  in  Ice 
hard  gelatin  capsules  at  the  rate  of  Ice  per  kilo  body  weight  and  with 
no  purgative.     Purgatives  appear  to  lower  the  efficacy  of  this  drug. 


340 


using  ti'tiju-liUiiotliyU'iic,  oil  of  ilu'iiniuiiliuiii  or  ctliyluk'iu' 
cliloriilf,  olitaiiK'd  an  efHiiuy  of  100  iioici'iit  in  one  dog,  H.l 
pi'iTont.  in  a  second  dog  but.  complete  fnihire  in  11  other 
animals. 

Surgical  intervention  witli  tlic  removal  of  tlic  cecum  is  prac- 
ticed by  some  veterinarians  who  report  veiy  good  results  in 
cases  in  wliich  it  is  impossible  to  remove  the  worms  by  anthel- 
mintic treatment.  Symptoms  of  abdominal  distress  with  alter- 
nating constipation  and  diarrhea  associated  with  whipworm 
infection  are  said  to  l)e  relieved  permanently  following  re- 
moval of  the  cecum.  While  this  method  will  not  obviate  rein- 
fection, subsequent  infections  in  the  colon  are  usually  of  very 
light  di'grec  and  not  associated  with  clinical  sym])toms. 

•niK.\T.Mr.NT  KOR   iWPILL.iRIA    .\EROPHn-.\   .\ND    CHKNOSOM.V 
VULPIS    IXrECTIONS 

Intratracheal  injection  of  various  medicinal  substances  has 
been  advocated  in  the  treatment  of  these  very  serious  parasites 
of  foxes  on  fur  farms  but  it  is  doubtful  whether  any  great 
benefit  has  resulted.  On  the  other  hand,  the  develoinnent  within 
recent  years  of  the  tracheal  swab-syringe  and  the  tracheal 
brush  for  the  mechanical  removal  of  Inngworms  from  the 
trachea  of  the  fox  has  provided  a  fairly  satisfactory  metliod 
for  the  removal  of  worms  which  are  actually  in  the  trachea,  the 
instruments  owing  to  mechanical  difficulties  being  of  little 
value  for  the  removal  of  worms  from  the  bronchi  or  bronchioles. 
Hanson  (l!t33),  who  was  largely  instrumental  in  developing 
this  method  of  treatment  to  its  present  satisfactory  state,  has 
l)ublishcd  results  of  critical  tests  with  the  instruments  and  de- 
tailed information  concerning  their  use.  This  method  of  treat- 
ment is  more  effective  in  the  case  of  C.  aerophila  than  with 
Crciiosoma  vulpLi,  since  the  latter  parasite  is  more  frequently 
located  in  the  bronchi  and  bronchioles,  where  it  cannot  be 
reached  by  the  tracheal  brush  or  swab. 

Recently  Russian  investigators  have  reported  that  a  solu- 
tion consisting  of  iodine,  1  gram;  potassium  iodide,  2  grams; 
and  water,  1,;")00  cc.  is  effective  for  the  destruction  of  these 
parasites  when  injected  intratraeheally.  The  animal  is  placed 
on  its  back  with  the  head  elevated  at  an  angle  of  30  degrees. 
One-half  the  dose  is  injected  while  the  animal  is  rolled  slightly 
to  one  side;  then  the  animal  is  rolled  slightly  to  the  other 
side  and  the  remainder  of  the  dose  injected.  The  treatment 
is  repeated  after  8  da.vs.  Maximum  doses  are  3  cc.  of  the  solu- 
tion. It  is  reported  that  maximum  doses  remove  80  percent  of 
the  lungworms. 

TRE.\TMENT    FOR    SPIROCEBCA    LUPI    INFECTION 

There  is  no  anthelmintic  treatment  of  value  in  this  condi- 
tion. Treatment  is  symptomatic  with  the  view  of  relieving  the 
cough  and  nausea  and  maintaining  the  condition  of  the  animal. 
Oil  of  chenopodium  has  been  suggested  but  it  is  unlikely  that 
worms  in  the  tumors  would  be  affected.  On  theoretical  grounds, 
chlorinated  hydrocarbons,  such  as  carbon  tetrachloride,  should 
be  more  penetrating  and  more  effective  than  chenopodium. 
Suehanek  (1932)  reported  a  case  of  spirocercosis  in  a  dog 
which  was  diagnosed  by  means  of  X  ray  and  the  esophagoscope. 
The  dog  was  placed  under  chloral  hydrate  narcosis,  the  blade 
of  a  scalpel  was  fixed  in  a  pair  of  forceps  which  were  passed 
through  a  tube  and,  with  the  aid  of  the  esophagoscope,  the 
tumor   was    removed. 

TREATMENT    FOR    PHYSALOPTEKA    SPP. 

Ehlers  (lSi31)  reported  on  the  anthelmintic  treatment  for  in- 
fections with  Physalopicra  sp.  in  badgers  {Taxidra  laxits) 
and  it  is  probable  that  the  treatments  found  effective  can  be 
used  also  on  other  animals.  Tetrachlorethylene  in  doses  of 
0.5  to  1  cc.  (8  to  1(3  minims)  failed  to  remove  the  worms  but 
a  dose  of  5  cc.  killed  all  physalopterids  although  it  proved  fatal 
to  one  animal.  Ehlers  stated  that  the  drug  deserves  further 
trial  in  doses  of  1.3  to  2  cc.  (20  to  32  minims).  Carbon  disul- 
phide  was  found  to  be  very  effective  in  doses  of  0.8  to  1  cc. 
(12  to  Ki  minims),  administered  after  a  period  of  fasting  for 
18  to  24  hours,  and  followed  in  ti  hours  by  a  table  spoonful 
(1.5  cc.)  of  castor  oil  mixed  with  honey,  a  mixture  which  bad- 
gers will  eat  readily  out  of  a  spoon.  While  the  administration 
of  a  purgative  is  desirable,  no  ill  effects  w^ere  observed  in 
those  animals  to  which  a  purgative  was  not  given. 

TREATMENT  FOR  DIROPILARIA  IMMITIS  INFECTION 

Fouadin  (sodium  antimony  III  pyrocatechin  disulphonate  of 
sodium )  has  been  used  more  extensively  than  any  other  drug 
for  this  condition.  As  .shown  by  Wright  and  Underwood  (1934). 
a  suitable  course  of  treatment  results  usually  in  the  permanent 
disappearance  of  microfilariae  from  the  peripheral  circulation, 
in  the  sterilization  of  female  worms,  and  in  the  eventual  de 
stniction   of  some  or  all  of  the  adult   worms   in   the  heart  and 


Body  tfeiglit  of  dog 


pulmonary  aitery.  The  action  of  Foiuidin  oTi  adult  worms  is- 
cumulative  and  is  exerted  over  a  relatively  long  period  of 
time.  The  destruction  of  any  considerable  number  of  adult 
worms  at  any  one  time  ina.v  result  in  embolic  pneumonia  or  in 
an  acute  toxemia  with  consequent  danger  to  the  life  of  the 
l)atient.  Cons<'(|uently,  heavily  infected  animals  should  be 
treated  with  caution  and  in  such  animals  treatment  should  not 
lie  administered  rajiidly,  or  in  large  doses,  or  at  too  frequent 
intervals.  The  adTuinistration  of  moderate  doses  of  the  drug 
over  a  period  of  time  results  in  a  central  necrosis  of  the  liver 
and  in  an  acute  toxic  nephrosis.  The  liver  damage  may  lead 
to  guanidine  retention  with  a  lowering  of  the  blood  calcium 
level.  Symptoms  of  calcium  tetany  should  be  combated  through 
the  use  of  calcium  gluconate.  Considerable  judgment  must  be 
exercised  in  the  administration  of  this  treatment  and  due 
weight  should  be  given  to  the  presence  of  chronic  or  acute 
disease  conditions  which  might  influence  the  tolerance  of  the 
animal  for  the  drug.  Wright  and  Underwood  recommended  the 
following  dose  rates  for  intramuscular  and  intravenous  injec- 
tions for  dogs  in  good  physical  condition  and  not  suffering 
from  cardiac,  hejiatic  or  renal  disease:  these  dose  rates  have 
been  generally  followed  by  most  veterinarians. 

IiilraitiKucuIar  inject ioins 

Daily  dose  Daily  dose  Daily  dose 
for  first  6  for  second  after    sec- 
days  6  days  and  6  days- 
cc.  cc.                  cc. 
Under  10  kgms.  (22  lbs.)                  0..1  1.0                  1.0 
10  to  ir,  kgms.   (22  to  33  lbs.)        1.0  1..5                  1.5 
l.T  to  20  kgms.   (33  to  44  lbs.)        1.0  1..5                  2.0 
20  to  25  kgms.   (44  to  55  lbs.)        1.5  2.0                  2.0 
Over  25  kgms.    (55  lbs.)           .        2.0  2.5                  2.5 

Intravenous  injections 

Days  of  treatment 

Body  weight  of  dog  1st  3rd  5th  7th  8th  9th  10th  12th 
['nder    10    kgms.    (22 

lbs.)   - 0.5     0.5     0.5     1.0     1.0     1.5     1.5     1.5 

10  to  15  kgms.   (22  to 

33  lbs.) -      1.0      1.0     1.0     1.5     1.5     2.0     2.0     2.0 

15  to  20  kgms.   (33  to 

44  lbs.)     -.- 1.5     1.5     1.5     2.0     2.0     2.5     2.5     2.5 

20  to  25  kgms.  (44  to 

55  lbs.)       2.0     2.0     2.0     2.5     2.5     3.5     3.5     3.5 

Over     25     kgms.     (55 

lbs.)      2.5     2.5     2.5     3.5     :\5     5.0     5.0     5.0 

Intramuscular  injections  are  without  apjjreciable  unfavora- 
ble local  reaction  and  are  particularly  applicable  for  use  in 
small  dogs  in  which  the  subcutaneous  veins  are  so  small  as  ta- 
make  intravenous  injections  difficult.  However,  intravenous  ad- 
ministration permits  the  use  of  a  smaller  total  dose  in  most 
cases,  and  the  results  desired  are  obtained  in  a  shorter  period 
of  time. 

In  connection  with  other  treatments,  Hayes  (1933)  recom- 
mended the  use  of  an  antimony  preparation  called  "Filsol," 
the  chemical  composition  of  which  has  never  been  made  public. 
This  preparation  appears  to  be  more  toxic  than  Fouadin  and 
should  be  used  with  even  greater  caution. 

Brown  and  Austin  (1939)  have  published  case  reports  on  the 
use  of  "Stibsol."  said  to  be  antimonial-3-catechol-thiosalicylic- 
acid-sodium,  and  to  contain  30  percent  of  antimony.  The  solu- 
tion contains  approximately  8.5  mg.  of  trivalent  antimony  per 
cubic  centimeter.  These  investigators  recommend  for  this 
compound  the  same  dose  rates  as  recommended  by  Wright  and 
Underwood  for  the  intravenous  injection  of  Fouadin.  Evalua- 
tion of  the  efficacy  of  this  compound  must  await  either  the 
publication  of  more  extensive  and  more  critical  tests  or  the 
results  of  field  trials  in   relatively   large  numbers  of  cases. 

Simonelli  (1936)  and  Lucas  (1937)  have  reported  success- 
ful results  in  the  treatment  of  canine  filariasis  following  the 
use  of  emetine  hydrochloride  at  dose  rates  varying  from  10  to 
60  mgm.  per  day,  but  more  critical  evidence  is  needed  before 
this  treatment  can  be  evaluated.  The  drug  had  been  previously 
used  by  MacCallum  (1921)  for  this  purpose. 

Anthelmintic   Medication   for   Nematode   Parasites 
of  Swine 

TREATMENT  FOR   ASCARIS   SUUM    INFECTION 

On.  OF  Chenopodium.  This  is  probably  the  most  effective 
treatment  available  at  the  present  time.  The  drug  is  given  at 
a  dose  rate  of  V2  to  1  fluid  dram  (2  to  4  cc.)  for  a  100-pound 
(45.5-kilogram)    animal,   immediately   preceded   or   followed   by 


341 


at  least  2  fluid  ounces  (GO  ee.)  of  castor  oil,  or  the  drug  nun- 
be  administered  with  the  oil.  Doses  for  animals  of  various 
sizes  should  be  computed  on  a  weight  basis,  though  it  is  likely 
that  a  dose  of  2  fluid  drams  is  adequate  for  animals  weighing 
300  to  400  pounds  (136.4  to  1S1.8  kilograms).  The  drug  mav 
be  given  with  a  dose  syringe  or  by  stomach  tube.  The  animals 
should  be  fasted  for  18  to  24  hours  prior  to  treatment  and 
should  not  be  fed  or  watered  for  3  hours  after  treatment. 
Oil  of  chenopodium  should  not  be  given  to  animals  suffering 
from  gastroenteritis,  constipation  or  febrile  conditions,  or  to 
very  young  animals  or  sows  in  advanced  pregnancy.  If  a  herd 
is  to  be  treated  without  regard  to  possible  contraindications  in 
individuals,  the  lower  dose  rate  of  chenopodium  should  be  used. 

Santonin.  Santoniu  has  been  widely  recommended  as  a 
treatment  for  the  removal  of  ascarids  from  swine.  At  various 
times,  it  has  been  tested  critically  by  Mote,  Vadja,  Shillinger, 
and  others,  all  of  whom  have  found  that  santonin  in  the  doses 
commonly  recommended  and  given  in  the  manner  usually  rec 
ommended  exhibits  a  relatively  low  efficacy  for  the  removal  of 
these  worms.  Under  these  conditions,  the  efficacy  of  santonin 
does  not  compare  favorably  with  that  of  oil  of  chenopodium. 
More  recently,  Morris  and  Martin  (1931)  as  well  as  Shcherbo- 
vich  (1935)  have  found  that  santonin  administered  in  relative- 
ly large  doses  and  followed  by  an  adequate  dose  of  an  active 
purgative,  such  as  magnesium  sulphate  or  castor  oil,  will  re- 
move a  large  percentage  of  the  ascarids  from  swine.  Morris 
and  Martin  administered  santonin  at  dose  rates  varying  be- 
tween 1/6  to  %  grain  (10.7  to  43  mgm.)  per  pound  (4.j  cgm.) 
of  body  weight,  followed  in  12  hours  by  1  dram  (4  grams) 
of  magnesium  sulphate  per  pound  of  body  weight.  It  would 
seem  that  adequate  purgation  is  necessary  and  relatively  large 
doses  required  if  satisfaetorj'  results  are  to  follow  the  use  of 
this   drug 

PHiiNOTHi.^ziNE.  Swanson,  Harwood  and  Connelly  (1940) 
have  recently  reported  on  the  use  of  this  drug  for  swine  and 
it  appears  to  have  considerable  efficacy  for  the  removal  of  as- 
carids. However,  better  results  were  obtained  in  the  removal  of 
mature  ascarids  than  in  the  removal  of  immature  forms.  In 
view  of  the  marked  efficacy  of  the  drug  for  the  removal  of 
nodular  worms  from  swine,  it  could  probably  be  used  to  ad 
vantage  in  animals  in  which  both  kinds  of  worms  are  present. 
The  above  mentioned  investigators  have  suggested  dose  rates 
of  phenothiazine  for  experimental  use  in  swine  and  these  may 
be  found  under  the  treatment  for  Oesophagostomum  spp. 

TREATMENT  FOR   THE  REMOVAL   Or   HOOKWORMS 

Satisfactory  medication  has  not  been  established.  On  theo 
retical  grounds,  some  of  the  chlorinated  hydrocarbons  would 
seem  to  be  promising.  However,  Eaffensperger,  as  reported  by 
Wright  and  Raffensperger  (1930),  did  not  find  carbon  tetra- 
chloride in  a  dose  of  25  cc.  in  75  cc.  of  castor  oil  for  pigs 
weighing  125  pounds  effective  for  the  removal  of  Gtobocephahis 
urosubulatus.  Tetrachlorethylene  or  n-butyl  chloride  might  be 
more  promising  since  carbon  tetrachloride  is  not  well  tolerated 
by  swine  and  is  more  soluble. 

TREATMENT  FOR  THE  REMOV.\L  OF  SWINE  STOMACH  WORMS 

Bozicevich  and  Wright  (1935)  found  that  carbon  disulphide, 
administered  in  capsules  or  by  stomach  tube,  at  a  dose  rate  of 
0.1  cc.  per  kilogram  (2.2  pounds)  of  body  weight,  or  4.5  cc. 
for  a  100  pound  pig,  was  approximately  90  percent  effective 
for  the  destruction  of  Hyostrongylus  rubidus  and  even  more 
effective  for  the  removal  of  Ascarops  strongylina.  Food  must 
be  withheld  for  36  to  44  hours  prior  to  treatment,  as  the 
presence  of  food  in  the  stomach  interferes  with  the  action  of 
the  carbon  disulphide  and  acts  to  reduce  the  efficacy  of  the 
treatment.  Lower  doses  of  carbon  disulphide  were  less  effec- 
tive. Pigs  killed  2  hours  after  treatment  showed  a  slight  to 
moderate  gastritis  but,  as  in  the  administration  of  carbon  di- 
sulphide to  horses,  this  gastritis  does  not  constitute  a  marked 
objection  to  the  use  of  the  treatment  as  it  probably  clears  up 
rather  quickly.  It  appears  that  this  treatment  should  be  effec 
five  also  for  the  removal  of  Physocephalus  sexalatus  and  other 
nematodes  occurring  free  in  the  stomach  of  awine. 

TREATMENT    FOR     THE    REMOVAL     OF     NODDLAR    WORMS, 
OESOPHAGOSTOMUM    SPP. 

Of  a  number  of  drugs  tested  for  the  removal  of  these  worms, 
none  showed  a  high  efficacy  until  Harwood,  Jcrstad  and  Swan- 
son  (1938)  and  Swanson,  Harwood  and  Connelly  (1P40)  dem- 
onstrated the  marked  efficiency  of  phenothiazine  for  this  pur- 
pose. In  experiments  reported  bj'  the  latter  investigators,  con- 
ditioned phenothiazine  removed  4,753,  or  92.1  percent,  of  5,162 
nodular  worms  from  22  pigs.  In  other  tests,  recrystallized 
phenothiazine   showed   approximately  the   same   degree   of   effi 


cacy.  Swanson,  Harwood  and  Connelly  recommended  the  fol- 
lowing dose  rates  for  phenothiazine  for  experimental  use  in 
swine : 

tr eight  of  pig  Size  of  dose 

Up  to  11.4  kgm.  (25  lbs.)  5  gm.   (1.2  drams) 

11.4  to  22.8  kgm.  (25  to  50  lbs.)  8  gm.   (2.0  drams) 
22.8  to  45.5  kgm.  (50  to  100  lbs.)              12  gm.   (3.0  drams) 

45.5  to  91.(1  kgm.   (100  to  200  lbs.)  20  gm.    (5.0   drams) 
Over  91  kgm.   (200  lbs.)  30  gm.   (7.5  drams) 

Phenothiazine  may  be  administered  to  swine  in  hard  gelatin 
capsules  if  the  operator  is  sufficiently  skilled  to  avoid  lodging 
the  capsules  in  the  pharyngeal  pouch,  or  it  may  be  adminis- 
tered mixed  with  any  ground  feed  to  which  the  pigs  are  ac- 
customed. Pigs  varying  greatly  in  size  should  not  be  treated 
at  one  time  in  the  latter  manner,  and  the  chemical  should  not 
be  offered  to  the  animals  except  when  they  are  sufficiently 
hungry  to  consume  the  medicated  food  at  once.  The  efficacy 
of  the  drug  when  administered  with  the  feed  needs  further 
investigation  but  this  promises  to  be  a  very  valuable  method 
of   treatment. 

TREATMENT   FOR    STEPHANURUS    0ENTATUS    INFECTION 

No  effective  treatment  is  known  for  the  destruction  of  swine 
kidney  worms.  Turpentine  has  been  recommended  on  the 
ground  of  the  great  diffusibility  of  the  drug  but  it  has  not 
been  established  that  the  drug  could  reach  the  adult  worms  in 
the  perirenal  fat.  Kauzal  (1932)  interpreted  his  experimental 
results  with  carbon  tetrachloride  as  indicating  that  the  treat- 
ment was  of  some  benefit,  as  no  worms  were  found  in  the  liver 
of  one  of  the  treated  animals,  while  worms  in  the  liver  of  a 
second  animal  were  encapsulated.  It  is  possible  that  this  drug 
might  check  the  migration  of  worms  or  destroy  migrating 
worms  in  the  liver,  although  it  is  probable  that  the  drug  would 
have  no  effect  on  adult  worms  in  the  perirenal  tissue. 

TREATMENT    FOR    LUNGWORM    INFECTIONS 

Freeborn  (1916)  recommended  the  injection  into  the  nostrils 
of  swine  of  5  cc.  of  chloroform  repeated  at  intervals  of  3  to  5 
days  until  the  infection  is  controlled.  However,  there  is  no 
critical  evidence  that  this  treatment  is  effective  in  the  de- 
struction of  the  worms. 

Skrjabin  and  Schul'ts  (1936)  reported  that  one  part  of 
chlorine  in  30,000  parts  of  air  had  little  effect  on  the  host 
after  one  hour  and  claimed  that  this  exposure  destroyed  73.3 
percent  of  the  lungworms  present.  The  same  authors  also 
recommended  intratracheal  injections  of  the  iodine  solution 
described  under  the  treatment  of  lungworms  of  carnivores. 
The  doses  employed  for  swine  are  0.25  cc.  per  kilogram  of  body 
weight  for  small  pigs  and  0.5  cc.  per  kilogram  of  body  weight 
for  average  sized  pigs. 

The  treatment  which  appears  to  be  safest  and  best  is  good 
nursing  in  connection  with  an  abundance  of  good  feed  and 
adequate  shelter.  In  the  absence  of  specific  therapy,  emphasis 
should  be  placed  on  prevention  and  animals  should  be  isolated 
and  removed  from  areas  where  the  intermediate  hosts  are 
prevalent. 

TREATMENT    FOR    TRICHURIS    SUIS    INFECTION 

Medication  for  whipworm  infection  in  swine  is  entirely  un- 
certain and  no  effective  treatment  is  known  at  present.  Single 
doses  of  various  anthelmintics  will  remove  a  few  whipworms 
at  times  but  consistent  results  are  not  obtained  with  any  of 
them.  In  the  absence  of  more  information  concerning  the 
pathogenicity  of  this  parasite,  chemotherapy  dors  not  s?em  to 
be  a   matter  of  any  considerable  importance. 

Anthelmintic   Medication  for  Nematode  Parasites 
of  Equines 

TRE.iTMENT     FOR     PARASCARIS     EQUORDM     INFECTION 

Carbon  Disulphide.  This  drug  is  probably  the  most  effec 
five  treatment  available.  It  should  be  administered  in  a  dose 
of  6  fluid  drams  (24  cc.)  for  a  1,000  pound  animal,  after  a 
fast  of  18  hours,  or  at  a  dose  rate  of  1.5  fluid  drams  (6  cc.) 
for  each  250  pounds  of  body  weight.  No  purgative  is  needed 
but  a  saline  purgative  may  be  advisable  in  the  case  of  heavy 
infections;  oils  should  be  avoided  as  they  increase  absorption 
and  add  to  the  toxity  of  the  drug.  Carbon  disulphide  should  be 
administered  by  stomach  tube;  if  capsules  containing  the  drug 
are  broken  in  the  mouth,  asphyxiation  and  death  may  result. 
Capsules  containing  carbon  disulphide  adsorbed  on  various 
kinds  of  powdered  material  are  available;  these  capsules  un- 
doubtedly are  safer  to  administer  but  fail  to  provide  the  same 
high  efficacy  as  exerted  by  the  liquid  drug.  Carbon  disulphide 
produces  a  well  marked  inflammatory  reaction  in  the  stomach 
and  upper  duodenum.  This  inflammation  usually  clears  up  in 
a  short  time  however.    Carbon  disulphide  is  contraindicated  in 


342 


till'  iiroseiioe  of  Ku^^tro  entoiitis;  it  is  luit  indicated  in  the 
treatment  of  pregnant  mares. 

C.VRBON  Tetr^\chix)Kide.  This  is  also  an  oft'cetive  treatment 
for  tlie  removal  of  asearids  from  horses.  It  is  given  in  the 
same  manner  as  for  the  removal  of  strongyles,  but  in  heavy 
asearid  infections  it  is  advisable  to  follow  the  drug  by  a 
saline  iiurgative  in  order  to  sweep  out  dead  worms  and  jire 
vent  their  oluniiiing  in  the  small  intestine.  This  is  particularly 
indicated   in   the  case  of  foals. 

PllENOTHiAZlNH.  E.xperiments  indicate  that  this  drug  will 
remove  some  asearids  but  more  data  are  needed  before  it  can 
be  established   as   a   satisfactory   treatment. 

TREATMENT  FOK  THE  RE.MOVAI,  OF  L/VRGE  AND  S.MAI, I.  .STRONGYLES. 
STRONOYLUS   SPP.,   TRU'HONEMA   SPP.   AND  RELATED  GENERA 

Oil  OF  Chenopodium.  Chenopodium  is  very  effeetive  for  the 
removal  both  of  large  and  small  strongyles.  Aninuils  slumld 
be  fasted  for  3ti  hours  and  oil  of  chenopodium  administered  in 
a  dose  of  4  to  5  fluid  drams  (16  to  20  cc.)  for  a  1,000  pound 
animal,  or  at  a  dose  rate  of  1  fluid  dram  (4  cc.)  for  each  2.'i0 
pounds  of  body  weight,  immediately  preceded  or  followed  by 
1  quart  of  raw  linseed  oil.  Cases  of  excessive  jmrgation  have 
been  reported  in  some  instances  following  the  use  of  raw  lin- 
seed oil.  It  is  possible  that  this  undesirable  action  is  due  to 
impurities  in  the  product ;  consequently  a  good  grade  of  oil 
should  be  used.  Veterinarians'  of  the  V.  S.  Army  have  pro- 
posed a  substitute  puigative  of  castor  oil  and  mineral  oil, 
claiming  that  this  mixture  provides  snitalde  purgation  fol- 
lowing treatment  with  chenopodium  and  is  without  undesirable 
effects.  The  following  are  the  doses  of  the  mixture  recommend- 
ed: For  weanlings,  castor  oil  4  to  6  ounces  and  mineral  oil 
1  pint;  for  yearlings  and  2year-olds,  castor  oil  6  to  8  ounces 
and  mineral  oil  1  pint ;  for  3-year-olds  and  older,  castor  oil  8 
to  10  ounces  and  mineral  oil  1%  pints.  Oil  of  chenopodium  is 
contraindieated  in  the  presence  of  constipation,  gastroenteritis 
and  febrile  conditions,  and  in  pregnant  mares. 

Carbon  Tetrachloride.  This  drug  is  effective  for  the  re- 
moval of  large  strongyles  but  only  about  50  percent  effective 
against  small  strongyles.  It  should  be  given  in  capsule  or  by 
stomach  tube  in  a  dose  of  6  to  12  fluid  drams  (2.'')  to  50  cc. ) 
for  a  1,000-pound  animal  after  fasting  for  24  to  36  hours.  The 
drug  need  not  be  accompanied  by  a  purgative  but  if  one  is 
used,  sodium  sulphate  is  to  be  preferred.  If  linseed  oil  is  used, 
it  should  be  given  4  to  5  hours  after  carbon  tetrachloride.  The 
administration  of  carbon  tetrachloride  to  equines  is  followed  by 
a  fall  in  the  blood  calcium  level  and  by  a  marked  increase  of 
bilirubin  in  the  blood.  In  carbon  tetrachloride  intoxication,  it 
is  advisable  to  use  calcium  gluconate.  The  drug  is  contrain- 
dieated in  animals  suffering  from  hepatic  disease  or  from  cal- 
cium deficiencies,  such  as  rickets  or  osteomalacia. 

N-Butylidene  Chloride.  In  a  dose  of  0.2  cc.  per  kilogram 
of  body  weight,  this  compound  is  very  effective  for  the  removal 
both  of  large  and  small  strongyles.  It  is  probable  that  the 
dose  could  be  reduced  to  0.15  cc.  per  kilogram  without  ma- 
terially aifecting  the  efficacy  of  the  treatment;  this  dose  is 
equivalent  approximately  to  70  cc.  for  a  1,000-pound  animal. 
As  n-butylidene  chloride  is  constipating,  it  is  advisable  to  fol- 
low the  drug  in  5  hours  by  raw  linseed  oil  in  a  dose  of  1  quart 
for  a  1,000  pound  animal. 

N-BUTYL  Chloride.  Because  of  the  relatively  higher  cost 
of  n-butylidene  chloride,  Harwood,  Underwood  and  Schaffer 
(1938)  tried  n-butyl  chloride  for  the  removal  of  strongyles. 
In  a  dose  of  approximately  0.2  cc.  per  kilogram  of  body  weight, 
the  compound  proved  very  effeetive  for  the  removal  of  small 
strongyles  and  reasonably  effective  for  the  removal  of  large 
strongyles.  In  the  tests  in  question,  the  drug  was  given  in  10 
times  its  volume  of  raw  linseed  oil.  In  tests  by  the  above- 
mentioned  workers,  two  horses  succumbed  to  treatment  with 
doses  ten  times  the  therapeutic  dose.  It  would  appear  that 
the  compound  is  not  as  safe  as  is  n-butylidene  chloride  and  that 
further  tests  are  needed  to  clarify  this  point. 

Phenothiazine.  This  is  a  very  effective  drug  for  the  re- 
moval of  strongyles  from  horses.  Several  authors  have  reported 
excellent  results  following  the  use  of  doses  varying  from  30  to 
100  grams  for  adult  animals.  However,  the  only  critical  ex- 
periments reported  thus  far  were  by  Harwood,  Habermann, 
Roberts  and  Hunt  (1940)  and  Habermann,  Harwood  and  Hunt 
(1941).  In  the  tests  described  in  the  latter  paper,  it  was 
found  that  this  drug  in  doses  varying  from  50  to  100  grams 
per  equine  removed  practically  all  of  362,797  cylicostomes  and 
96  percent  of  137  Strongyliis  spp.  These  authors  concluded 
that  the  dose  per  adult  equine  should  be  held  at  50  grams 
pending  additional  critical  experimentation  with  smaller  dos- 
ages. In  some  instances,  a  dose  of  50  grams  failed  to  remove 
a  few  of  the  Strongyliis  spp.  present  In  the  treated  animals 
and,  since  these  are  the  most  pathogenic  of  the  nematodes 
present  in  equines,  it  does  not  seem  advisable  to  employ  dos- 


ages of  ;i(i  giams  per  horse  such  as  recommended  by  Taylor 
and  Sanderson  (1!I4I))  on  the  basis  of  tests  checked  by  the  egg 
count  method  alone. 

Single  doses  of  ])henothiazine  as  high  as  500  grams  have 
been  given  to  horses  without  producing  alarming  symptoms, 
but  these  dosages  may  cause  pronounced  cloudy  swelling  of 
the  liver,  the  formation  of  methaemoglobin,  and  anemia  (La- 
page,  1040;  Habermann,  Harwood  and  Hunt,  1941).  Single 
doses  of  1,00(1  grams  have  produced  fatalities  in  horses.  Since 
the  toxic  manifestations  appear  to  be  associated  with  the  de- 
struction of  the  erythrocytes,  it  is  advisable  to  administer  the 
drug  cautiously  to  horses  suffering  from  anemia.  The  Bureau 
of  Animal  Industry  has  issued  a  press  release  terming  poor, 
weak  animals  and  those  suffering  from  infectious  anemia  as 
bad  risks  for  treatment  and  it  would  appear  that  the  drug 
.  should  be  employed  with  considerable  caution  in  such  cases. 

Hatcher  (1941)  reported  the  death  of  5  of  12  horses,  each 
of  which  was  given  a  dose  of  approximately  120  grams  of 
phenothiazine  as  an  anthelmintic.  Under  experimental  condi- 
tions, doses  of  this  size  have  caused  no  symptoms  other  than 
discoloration  of  the  mucous  membranes,  transient  loss  of  ap- 
petite and  a  temporary  anemia.  Grahame,  Morgan  and  Sloane 
(1940)  administered  100  grams  to  each  of  35  horses  without 
accident,  and  others  have  reported  similar  results.  Possibly 
under  certain  conditions  horses  may  prove  more  sensitive  to 
phenothiazine  than  present  experimental  evidence  suggests.  As 
a  measure  of  precaution,  wholesale  treatment  should  be  avoided. 
The  Bureau  of  Animal  Industry  recommends  that  when  large 
numbers  of  animals  are  to  be  treated  with  this  drug,  one  or 
two,  the  least  valuable  of  the  lot,  be  treated  first  to  determine 
tolerance  for  the  drug.  Such  animals  should  be  kept  under 
observation  for  a  week  before  others  are  treated.  If  no  bad 
results  are  observed,  the  remaining  animals  should  be  treated  a 
few  at  a  time  and  the  observations  repeated.  This  procedure 
should  be  followed  until  the  entire  group  has  been  treated. 

Phenothiazine  may  be  administered  to  horses  in  gelatine  cap- 
sules or  in  a  suitable  suspension.  In  order  to  make  a  suspen- 
sion of  phenothiazine  suitable  for  administration  to  animals, 
it  is  necessary  to  use  some  chemical  as  a  dispersing  agent. 
Numerous  dispersing  agents  are  known  and  many  of  these  have 
been  employed ;  however,  few  of  these  suspensions  have  been 
given  critical  test.  It  is  known  that  certain  agents  will  greatly 
reduce  the  efficacy  of  phenothiazine  when  such  chemicals  are 
employed  as  suspending  agents.  Therefore,  it  is  not  advisable 
to  employ  such  mixtures  unless  they  have  been  tested  critically. 
A  formula  which  has  been  found  satisfactory  consists  of 
phenothiazine  50  grams  (1.67  ounces),  molasses  20  cc.  (0.67 
fluid  ounces),  and  water  to  make  90  cc.  (3  fluid  ounces).  The 
molasses  is  thoroughly  mixed  with  the  phenothiazine,  then  a 
small  portion  of  water  is  added  and  thoroughly  stirred  in. 
The  process  of  alternately  adding  water  in  small  quantities 
and  of  stirring  is  repeated  until  a  smooth  suspension  of  the 
required  volume  results.  Also,  phenothiazine  may  be  mixed 
with  almost  any  ground  feed.  Since  certain  animals  do  not 
take  readily  feed  medicated  with  phenothiazine,  the  following 
regimen  may  be  employed : 

For  one  week  prior  to  the  administration  of  the  drug  the 
horse  should  receive  no  salt.  During  this  time  it  should  re- 
ceive daily  one  pint  of  a  mixture  containing  equal  parts  of 
oats  and  bran  to  which  50  grams  (about  2  fluid  ounces)  of 
molasses  have  been  added.  For  administration  of  the  drug, 
.50  grams  (1.67  ounces)  of  phenothiazine  is  incorporated  in 
about  150  grams  (about  5  fluid  ounces)  of  molasses,  and  this 
mixture  is  mingled  thoroughly  with  2  quarts  of  an  oats  bran 
mixture.  Two  ounces  of  salt  are  added  to  this  formula.  While 
fasting  is  unnecessary,  the  medicated  mixture  should  not  be 
placed  before  the  horse  until  the  animal  is  hungry.  If  the 
horse  hesitates  to  eat  the  medicated  mixture,  it  may  often  be 
encouraged  to  do  so  by  sprinkling  a  small  quantity  of  untreated 
oats  or  corn  over  the  surface  of  the  mixture.  Even  if  the  drug 
is  administered  in  the  feed,  it  is  better  to  treat  horses  indi- 
vidually rather  than  to  attempt  mass  treatment. 

treatment  for  lungworm  intection 

Skrjabin  and  Schul'ts  (1936)  and  Kulikov  and  Tamarin 
(1937)  have  advocated  the  use  of  iodine  in  a  solution  of  po- 
tassium iodide  for  the  removal  of  lungworms  from  horses.  The 
material  is  injected  intratraeheally  while  the  horse  is  on  its 
back,  slightly  inclined  to  one  side  for  the  first  half  of  the 
injection,  and  to  the  other  side  for  the  remainder.  The  dose 
is  250  to  300  cc.  of  a  0.1  percent  solution  of  iodine  in  a  0.2 
percent  solution  of  potassium  iodide. 

trb^tment  for  oxyuris  equi  infection 

Oil  of  turpentine  is  an  effective  treatment  for  the  removal 
of  pinworms   from  the  horse.     Animals  should  be  fasted  for 


343 


36  hours  and  the  drug  administered  in  a  dose  of  I!  fluid  ounces 
(60  cc.)  for  a  1,000-pound  animal,  immediately  preceded  or 
followed  hj  1  quart  of  raw  linseed  oil.  The  drug  should  not 
be  given  to  animals  already  suffering  from   renal   disorders. 

Oil  of  chenopodium,  as  administered  for  large  and  small 
strongj'les,  is  effective  also  for  the  removal  of  pinworms. 

TREATMENT    FOR    THE    REMOVAL    OF    STOMACH    "WORMS 

Carbon  disulphide  in  a  dose  of  6  fluid  drams  (24  cc.)  for  a 
1,000-pound  animal,  preceded  by  gastric  lavage  with  S  to  10 
liters  of  a  2  percent  solution  of  sodium  bicarbonate,  is  very 
effective  for  the  destruction  of  Eabroncma  muscae  and  H. 
microstoma,  as  determined  by  Wright,  Bozicevich  and  Under- 
wood (lt)31).  Without  preliminary  lavage,  the  drug  gave  less 
favorable  results  in  the  tests  of  these  investigators.  Appar- 
ently the  alkaline  solution  serves  to  remove  excess  mucus  from 
the  stomach  wall  and  permits  the  drug  to  reach  the  parasites 
more  effectively.  Furthermore,  the  solution  seems  to  give 
some  protection  against  the  irritating  action  of  the  carbon 
disulphide.  In  the  above-mentioned  experiments,  Draschia 
megastoma  in  stomach  tumors  was  not  affected  by  the  treat- 
ment. It  is  advisable,  though  not  necessary,  to  siphon  oft  the 
sodium  bicarbonate  solution  .">  to  10  minutes  after  its  admin 
istration.  The  contraindications  for  the  treatment  are  the 
same  as  those  listed  under  the  discussion  of  this  drug  for  the 
removal  of  asearids. 

While  not  determined  by  critical  tests,  it  would  appear  that 
carbon  disulphide  would  be  a  fairly  satisfactory  treatment  for 
the  destruction  of  Irk-)iost>oiigi/his  axci  in  the  stomach  of  the 
horse. 


Anthelmintic   Medication   for   Nematode   Parasites 
of  Ruminants 

TREATMENT   FOR    STRONGVLOIDES    PAPILLOSUS    INFECTION 

There  is  no  established  treatment  for  strongyloidosis.  The 
parasite  appears  to  be  resistant  to  most  of  the  anthelmintics 
commonly  employed  in  sheep  and  even  prolonged  dosage  with 
some  of  these  drugs  fails  to  eradicate  it.  Gentian  violet,  the 
only  known  drug  which  has  shown  any  specificity  against 
worms  of  this  genus,  has  not  been  tried  in  ruminants. 
TREATMENT    FOR    INFECTION    WITH    TRICHURIS    SPP. 

Like  whipworms  in  other  animals,  those  forms  occurring  in 
ruminants  are  difficult  to  remove.  Occasional  whipworms  will 
be  removed  by  many  of  the  anthelmintics  used  for  the  removal 
of  other  worms  from  sheep  but  there  is  no  specific  treatment 
available  at  the  present  writing.  The  enema  treatment  de- 
scribed under  therapy  for  oesophagostomiasis  is  said  to  be 
fairly  effective  against  T.  oris.  However,  in  view  of  the  lack 
of  evidence  concerning  the  pathogenicity  of  the  parasite,  there 
would  be  little  need  for  the  use  of  the  treatment  in  uncom- 
plicated  infections. 

TREAT.MENT    FOR    INFECTIONS    WITH    OESOPHAGOSTOMUM    SPP. 

Phenothiazixe.  The  introduction  of  phenothiazine  by  Har- 
wood,  Habermann  and  Jerstad  (1939),  provided  the  first  an 
thelmintic  which  is  useful  for  the  removal  of  0.  columbiauiim 
when  administered  orally  in  a  single  dose.  These  investigators 
found  that  the  conditioned  drug  administered  as  20  percent  of 
a  meal  of  concentrates  after  a  period  of  fasting  at  a  dose  rate 
of  0.5  gram  per  pound  of  body  weight  removed  90  percent  of 
the  nodular  worms,  almost  SO  percent  of  the  Haemonchus,  76.7 
percent  of  the  hookworms,  and  apparently  100  percent  of  the 
Ostertagia.  Subsecjuent  investigations  in  the  U.  S.  Bureau  of 
Animal  Industry  (Habermann  and  Harwood,  1939;  Haber- 
mann, Harwood,  and  Hunt,  1940)  demonstrated  that  either 
rccrystallized  phenothiazine  or  the  ci'ude  non-conditioned  drug 
was  even  more  effective  than  the  product  which  had  been  con- 
ditioned for  use  as  an  insecticide  and  which  was  employed  in 
the  earlier  tests.  A  dose  of  25  grams  has  been  recommended 
for  adult  sheep.  These  results  have  been  confirmed  by  a  num- 
ber of  other  workers,  including  Swales  (1939),  Roberts  (1939.) 
and  Gordon    (1939). 

Swales  administered  phenothiazine  in  an  enema  without  ob- 
taining any  efticacy  for  the  removal  of  Chabcrtia  ovina  or  0. 
culumbiaiiiim.  This  finding  would  .seem  to  confirm  the  view 
of  Harwood  and  his  associates  that  the  drug  probably  under 
goes  some  chemical  change  in  the  digestive  tract  of  the  host 
which  acts  to  promote  its  efficacy.  Failing  to  find  that  sheep 
regularly  consumed  mixtures  of  the  anthelmintic  with  the  feed. 
Swales  reduced  the  bulk  of  the  commercial  product  by  prepar- 
ing compressed  tablets  according  to  the  following  formula : 

Commercial  phenothiazine    (pulverized)  SO  parts 

Starch    ( pulverized  1  S  parts 


Effervescent  salt  (sodium  bicarbonate,  ."0  parts, 

dehydrated  tartaric  acid,  45  parts)  9  parts 

Dried  ox  gall 2  parts 

Phenolplithalein _  _ __.        1  part 

The  individual  dosage  of  sheep  at  the  rate  of  0.3  gram  of 
phenothiazine  for  each  pound  of  bod^'  weight  in  Swales'  ex- 
periments was  very  effective  for  the  removal  of  H.  contort ux, 
Bunostomuiii  trigonoccphaUim,  0.  colKiiibiarium,  Chabertia 
uviiia,  Ncmatodirus  sp.,  Cooperia  sp.  and  Ostertagia  sp.  The 
treatment  was  approximately  50  percent  effective  for  the  re- 
moval of  Tricliontroiigi/Uix  spp.  but  was  apparently  ineffective 
against  Strungijloidcs  and  Capillaria  longipes. 

Roberts  (1S>39)  tested  Thio.x,  a  commercial  preparation  con- 
taining 93  percent  phenothiazine,  on  a  large  number  of  ani- 
mals and  found  that  satisfactory  results  were  secured  against 
0.  cohimbianum  with  a  dose  rate  of  0.15  gram  per  pound  of 
body  weight  given  immediately  after  previous  stimulation  of 
the  oesophageal  reflex  with  2  cc.  of  a  10  percent  copper  sul- 
phate solution  and  following  a  24-hour  fast.  Without  fasting 
or  the  use  of  the  copper  sulphate,  a  dose  of  0.4  gram  per 
pound  was  effective.  Good  results  were  obtained  also  against 
H.  contortus  but  the  treatment  failed  to  remove  Trichuris  par- 
vispiciilum  and  T.  globulosa.  In  certain  of  Roberts'  tests  some 
of  the  sheep  failed  to  respond  to  treatment  even  with  the  higher 
dose  rate  of  the  drug. 

Gordon  (1939)  confirmed  also  results  against  II.  c(iiitortii.i 
and  nodular  worms.  He  found  also  that  phenothiazine  in  a 
dose  of  0.6  gram  per  kilogram  (2.2  pounds)  of  body  weight 
reduced  the  egg  counts  of  Triclio.stroiigi/liis  spp.  by  90  peicent 
or  more.  Small  daily  doses  of  the  drug  ( 1  gram  daily  for  -5  ■ 
days)  were  effective  against  the  common  stomach  worm  and  the 
nodular  worm. 

Insoluble  Copper  Salts.  A  treatment  which  was  developed 
by  Monnig  (1935)  in  South  Africa  is  of  considerable  value 
against  0.  cohimbianum  but  does  not  approach  the  efficacy  of 
jiheiiothiazine.  This  treatment  consists  in  the  administration 
of  certain  insoluble  salts  of  copper  in  the  proportions  and 
doses  given  below : 

Dosage  in  grams  for  sheep 

of  various  ages 

Over  6 
3  to  6        and  under         Over 
Drug  Parts        months      18  months    IS  mo)ilh.i 

Copper  arsenate    __ 2  0.2  0.36  0.5 

Calcium  hydroxide    3  0.3  0.54  0.75 

Copper  tartrate         5  0.5  0.9  1.25 


Total  dose  in  grams  1.0  1.8  2.5 

In  an  effort  to  deliver  the  mixture  into  the  abomasum,  the 
sheep  are  given  2.5  cc.  each  of  a  10  percent  solution  of  copper 
sulphate  and  this  is  followed  immediately  by  the  appropriate 
dose  of  the  mixture.  Sheep  should  be  watered  immediately  be- 
fore treatment  but  should  be  fasted  for  48  hours  prior  to  dos- 
ing and  24  hours  after  dosing.  Water  should  be  withheld  for 
1  to  2  hours  after  treatment.  Recommendations  call  for  ro- 
peating  the  treatment  on  the  following  day.  The  treatment 
is  said  to  have  a  fair  degree  of  efficacy  against  E.  contortus 
and  Moniezia  crpansa. 

Enema  Treatment.  This  treatment,  originally  recommended 
by  Brumpt  35  years  ago,  has  more  recently  been  developed 
further  by  South  African  and  Australian  workers.  The  tieat- 
ment  consists  of  a  solution  of  2  grains  (125  mgm.)  of  sodium 
arsenite  per  liter  of  water.  The  solution  is  administered  by 
enema   in  the  following  doses: 

Lambs  up  to  4  months  of  age  1      pint 

Lambs  4  to  6  months „. 1.5  pints 

Six  months  old  to  2-tooth  sheep 1      quart 

Aged  sheep  _ _ _ .     1.5-2  qts. 

Sheep  should  be  fasted  for  24  hours  before  treatment.  The 
solution  may  be  allowed  to  flow  by  gravity,  may  be  given  by 
syringe,  or  may  be  injected  by  a  specially  devised  apparatus. 
The  forced  in,iection  of  the  solution  involves  some  risk  and 
deaths  have  followed  its  use.  This  method  of  treatment  is  time 
consuming  and  ill  adapted  to  large  scale  application. 

Swauson,  Porter  and  Connelly  (1940)  found  that  uncondi- 
tioned phenothiazine  removed  99. S  percent  of  0.  radiatum  from 
calves  when  the  drug  was  administered  in  doses  varying  from 
50  to  80  grams  (0.44  to  1.1  gram  per  kilogram  of  body  weight). 
While  it  is  not  possible  to  make  definite  therapeutic  recom- 
mendations on  the  basis  of  these  preliminary  experiments,  it 
would  appear  that  phenothiazine  is  of  considerable  promise  for 
the  removal  of  nodular  worms  from  cattle. 

treatment    for    CHABEHiTIA    OVINA    INFECTION 

As  previously  stated.  Swales  found  phenothiazine  100  percent 
effective  for  the  removal  of  these  worms  from  a  limited  num 
ber    of    animals.      Habermann    and    Harwood    (1939)    reported 


344 


lator  tliat  iioii  coiuiitiHiii'd  plionotliiaziiio  in  doses  of  ['.'  Id  12 
grains  lemoved  2<i.7  i)eri-oiit  of  12(5  Clutbcrda  from  li  slieep;  in 
dosos  of  In  to  2(1  grams,  47.9  lu'reont  of  4S  worms  from  .'i 
slioep;  and  in  doses  of  22  to  2G  grams,  i)3.8  percent  of  32 
worms  from  3  slieep.  The  enema  treatment  described  under  O. 
foliiiiihidiiKm  is  .said  to  be  satisfactory  also. 

TRE.^TMKNT    FOR    (l.\IGERI.\    PACHYSCELIS    INFECTION 

Ortlepp  (193.1)  found  tetrachloretliyleiie  effective  for  the 
removal  of  these  worms  when  given  in  a  dose  of  10  cc.  in  10 
to  20  cc.  of  liquid  paraffin  and  immediately  preceded  by  a  dose 
of  2..")  cc.  of  a  10  percent  solution  of  copper  sulphate  to  stimu- 
late closure  of  the  oesophageal  groove.  Smaller  doses  should 
be  used  for  lambs  and  young  sheep.  Fasting  is  not  necessary. 
Treatment  should  be  repeated  twice  at  intervals  of  10  to  14 
days.  Some  reactions  may  be  encountered  with  this  relatively 
large  dose  of  tetrachlorethylene. 

To  reduce  the  number  of  reactions,  Ortlepp  and  Monuig 
(193(i)  investigated  a  number  of  preparations  containing  tetra- 
chlorethylene. The  results  of  a  limited  number  of  experimen- 
tal trials  suggested  that  an  emulsion  consisting  of  25  cc.  of  an 
aqueous  solution  of  7.7  grams  of  soft  soap,  37.5  cc.  of  tetra- 
chlorethylene and  37. .J  cc.  of  liquid  paraffin  might  be  satisfac- 
tory-. Later  croton  oil  was  added  in  a  dose  of  1  cc.  to  each 
40  cc.  of  the  emulsion  which  contained  10  cc.  of  tetrachlor- 
ethylene, this  amount  of  the  emulsion  being  the  dose  for  an 
adult   animal. 

Subsequently,  certain  disadvantages  were  encountered  in  the 
use  of  this  emulsion  and  Mbunig  and  Ortlepp  (1939)  conducted 
further  experiments  in  order  to  devise  a  more  satisfactory 
vehicle  for  the  tetrachlorethylene.  The  formula  finally  worked 
out  was  made  up,  as  follows:  To  -"iOO  cc.  of  tapwater  heated  to 
70°  C.  are  added  6  grains  NaOH  and  then  40  grams  of  casein 
is  rapidly  stirred  in.  The  solution  is  then  heated  to  S.l"  C.  and 
40  grams  of  ground  resin  is  stirred  in  rapidly.  A  highly  sa- 
ponifiable  resin  should  be  emplo.ved  and  this  should  be  ground 
to  a  fine  powder.  The  solution  should  be  kept  at  S."i'  C  and 
stirred  for  about  Id  to  20  minutes  until  complete  combination 
of  the  alkali  with  the  other  ingredients  has  occurred.  It  is 
then  made  up  to  SOO  cc.  with  cool  water.  The  tetrachlorethy- 
lene is  added  in  successive  small  quantities  while  mixing  pro- 
ceeds in  the  proportion  of  7.3  cc.  of  tetrachlorethylene  to  2.j  cc. 
of  the  emulsifier.  The  emulsion  is  issued  in  concentrated  form 
and  is  diluted  with  an  equal  quantity  of  water  before  use. 
The  dose  for  an  adult  sheep  is  20  cc.  of  the  diluted  emulsion 
(i.e.  7.5  cc.  of  tetrachlorethylene)  for  adult  animals;  15  cc. 
for  lambs  6  to  12  months  old,  and  10  cc.  for  lambs  3  to  0 
months  old.  The  remedy  is  given  after  a  preliminary  dose  of 
2.5  cc.  of  10  percent  copper  sulphate  solution.  This  treatment 
is  said  to  be  effective  against  Hacmonchus  coiitortiis,  Tiiclio- 
utronffybis  spp.,  A'ematodirus  spp.,  Gaigeria  pachijscrlix  and 
Bunostomum  irigonocephalinn. 

While  no  tests  are  on  record,  it  would  seem  that  phenothia- 
zine   would  be  effective  against   Gaigeria. 

TREATMENT  FOR  BUNOSTOMUM   TRIOONOCEFHAI-UM    INFECTION 

The  phenothiazine  treatment,  as  described  under  nodular 
worms,  is  the  most  effective  available  at  the  present  time. 
Tetrachlorethylene,  as  used  against  Gaigeria,  is  also  quite  ef- 
fective but  is  probably  more  hazardous.  The  "Cu-Nic"  solu 
tion,  described  under  treatment  for  the  common  stomach  worm, 
will  usually  remove  a  high  percentage  of  hookworms. 

Little  is  known  concerning  removal  of  B.  phU'botomum  from 
cattle  but  it  is  probable  that  the  "Cu-Nic"  solution  would 
be  of  value.  For  dosage,  the  reader  is  referred  to  treatment  for 
H.  contortus.  Swauson,  Porter  and  Connelly  (1940)  reported 
that  phenothiazine  in  dosages  of  50  to  SO  grams  removed  1,160 
of  1,729  B.  phlebotomum  from  6  calves.  In  these  limited  tests, 
the  unconditioned  drug  at  a  dose  rate  of  0.44  to  0.55  gram 
per  kilogram  of  body  weight  in  calves  weighing  over  91  kilo- 
grams (200  pounds)  was  less  effective  against  this  species  than 
when  given  to  lighter  calves  at  a  dose  rate  of  0.66  to  1.1 
grams  per  kilogram  of  body  weight.  The  drug  is  promising 
but  more  information  is  needed  concerning  its  exact  efficacy 
;ind   its  safety  for  cattle. 

TRBLYTMBNT    FOR    HAEMONCHUS    CX)N"l'ORTUS    INFECTION 

Copper  Sulphate.  The  treatment  which  has  been  used  most 
extensively  is  the  copper  sulphate  solution  devised  by  Hutcheon 
(1891)  in  South  Africa.  In  the  United  States  a  1  percent 
solution  has  been  employed  most  commonly  and  this  is  admin- 
istered in  a  dose  of  50  cc.  for  sheep  up  to  a  year  old  and  100 
ce.  for  mature  sheep.  The  dose  for  calves  is  100  cc,  for 
yearlings  up  to  200  cc,  and  for  mature  cattle  up  to  1  liter. 
Where  sheep  cannot  be  adequately  protected  against  severe  in 
fection  by  light  stocking,  pasture  rotation  and  other  measures, 


tre;itiiieiil  slioiilcl  lie  repeated  in  tcm])erate  climates  under  con- 
ditions of  moderate  stocking  at  intervals  of  3  weeks.  In  warm 
climates  with  heavy  stocking  of  pastures,  it  is  necessary  to  re- 
peat treatment  every  2  weeks.  It  is  usually  necessary  to  con- 
tinue treatment  throughout  the  wanner  months  of  the  year 
and  in  warmer  climates  it  may  be  of  value  to  continue  dosing 
during  the  winter.  Tlie  repeated  administration  of  copper 
sulphate  is  apparently  not  detrimental  to  sheep  and  in  fact 
there  is  some  evidence  to  indicate  that  animals  so  treated  make 
better  gains  that  non-treated  animals.  Wright  and  Bozicevich 
(1931)  found  that  the  1  percent  solution  of  copper  sulphate 
may  be  administered  in  the  usual  doses  as  often  as  once  a  week 
without  harm  to  sheep.  When  so  administered,  there  is  a 
marked  increase  in  the  copper  content  of  the  liver  after  a 
period  of  time  with  no  appreciable  pathological  changes.  In 
view  of  the  relationship  of  copper  salts  and  liver  to  anemia, 
the  increased  amount  of  copper  in  the  livers  of  sheep  treated 
frequently  with  copper  sulphate  solution  may  be  beneficial 
rather  than  detrimental   to  the  health  of  the  animals. 

The  1  percent  solution  may  be  made  up  on  the  basis  of  1 
gram  of  copper  sulphate  to  99  cc  of  water,  or  by  dissolving 
Vi  pound  of  copper  sulphate  in  1  pint  of  boiling  water  and 
adding  cold  water  to  make  3  gallons  of  the  solution.  This  lat- 
ter will  make  a  quantity  sufficient  to  dose  100  sheep,  allowing 
10  percent  for  waste.  Only  clear  blue  crystals  should  be  used 
in  preparing  the  solution.  Porcelain,  enamelware  or  wooden 
vessels  should  be  employed,  as  copper  sulphate  solution  will 
corrode  metal. 

Various  writers  have  advocated  the  use  of  a  1.5  percent 
solution  or  stronger  solutions  of  copper  sulphate.  As  shown 
by  Cluiiies  Ross  (1934)  and  Monnig  and  Quin  (1935)  solutions 
of  this  salt  stimulate  the  closure  of  the  oesophageal  groove  in 
sheep  with  a  resultant  delivery  of  the  solution  directly  into  the 
abomasum  in  a  considerable  proportion  of  the  cases.  No  doubt 
this  quality  of  copper  sulphate  is  responsible  to  a  considerable 
extent  for  its  efficacy  against  H.  contortus.  Gordon  (1939)  has 
shown  recently  that  the  usually  prescribed  dose  in  Australia, 
i.e.,  1  fluid  ounce  of  a  4  percent  solution  of  copper  sulphate, 
is  not  an  efficient  treatment  against  H.  contortti.<i  in  adiilt  sheep. 
His  investigations  indicated  that  a  dose  of  2  iliiid  ounces  of 
a  solution  of  this  strength  was  very  effective  in  adult  sheep. 
Gordon  (1939)  determined  also  that  the  copper  sulphate  treat- 
ment is  relatively  ineffective  against  immature  Haemonchiis 
and  stated  that  apparent  failures  of  treatment  in  severe  out- 
breaks of  haemonchosis  in  the  field  could  be  explained  on  this 
basis.  As  a  result  of  the  findings,  Gordon  suggested  that  in 
flocks  heavily  infected  with  the  parasite,  treatment  with  copper 
sulphate  should  be  applied  every  10  to  14  days. 

Copper  Sulphate  and  Nicotine  Sui,phate.  As  previously 
stated,  the  copper  sulphate  and  tobacco  solution  of  Lewis  and 
Guberlet  and  the  nicotine  sulphate  solution  of  Lamson  have 
been  replaced  largely  by  the  "Cu-Nic"  solution  developed  by 
Curtice.  This  latter  solution  is  made  up  by  adding  1  ounce 
of  40  percent  nicotine  sulphate  to  each  gallon  of  a  1  percent 
solution  of  copper  sulphate.  The  dose  of  the  combined  solu- 
tion is  3.5  ounces  (100  cc.)  for  adult  animals  and  1.5  ounces 
(50  cc.)  for  weanling  lambs.  Experience  has  shown  that  this 
solution  is  occasionally  toxic  for  weak  animals  or  for  very 
young  lambs.  Furthermore,  the  operator  should  be  certain  that 
the  precipitate,  which  forms  in  this  mixture,  is  not  allowed 
to  settle  in  the  container  from  which  the  sheep  are  being  dosed. 
If  there  is  any  reason  to  believe  that  animals  will  not  tolerate 
the  treatment,  the  dose  should  be  reduced  or  trial  treatment 
should  be  made  on  a  few  animals  to  establish  tolerance.  For 
cattle,  the  "Cu-Nic"  solution  may  be  used  in  the  same  doses 
as  for  the  1  percent  solution  of  copper  sulphate.  For  sheep, 
the  solution  is  effective  against  immature  as  well  as  mature 
Haemonchiis  and  in  addition  is  a  fairly  satisfactory  treatment 
for  the  removal  of  hookworms,  small  trichostrougyles  and 
Monicsia  expansa.  In  uncomplicated  stomach  worm  infections, 
it  is  probably  of  no  great  advantage  over  copper  sulphate  solu- 
tion because  of  its  greater  toxicity. 

Carbon  Tetrachloride.  While  the  use  of  this  drug  in  un- 
complicated stomach  worm  infections  has  been  largely  dis- 
continued in  the  United  States,  it  is  still  popular  in  Australia, 
especially  in  concomitant  liver  fluke  infections.  In  the  United 
States,  it  is  usually  given  in  gelatin  capsules  in  a  dose  of  5 
cc.  for  adult  sheep  and  2.5  cc.  for  weanling  lambs.  In  Aus- 
tralia, the  doses  employed  are  2  cc.  for  adult  sheep,  aud  1  cc. 
for  lambs  under  6  months  of  age,  the  drug  being  mixed  with 
4  parts  of  liquid  paraffin.  Not  infrequently  losses  follow  the 
use  of  carbon  tetrachloride  in  sheep  and  for  this  reason  it 
should  be  used  with  caution.  Where  the  drug  is  used,  precau- 
tion should  be  taken  to  place  the  sheep  on  a  diet  rich  in  avail- 
able calcium  for  2  to  3  weeks  prior  to  treatment.  Changes  in 
feed  other  than  to  provide  calcium  should  not  be  made  for 
several    weeks    prior    to    treatment ;    animals    appear    to    suffer 


345 


fewer  reactions  when  maiutaiiied  for  several  weeks  ou  pasture 
prior  to  and  subsequent  to  treatment  with  carbon  tetrachloride. 

Tetrachlokethylene.  This  treatment,  tirst  tested  by  Hall 
and  Shilliuger  (unpublished  data),  has  been  employed  exten- 
sively. In  the  United  States,  the  drug  is  admini.stered  iu  gela- 
tin capsules  in  a  dose  of  5  cc.  for  adult  sheep  and  2.5  c.e.  for 
lambs.  In  Australia,  it  is  combined  with  equal  parts  of  liquid 
paraffin.  While  several  investigators  have  reported  it  to  be 
very  effective  against  the  common  stomach  worm,  there  is 
some  divergence  of  opinion  on  this  point  with  the  probability 
that  its  efficacy  does  not  approach  that  of  carbon  tetrachloride. 
However,  tetrachlorethyleue  is  a  much  safer  treatment.  In 
repeated  treatments  over  a  period  of  time,  it  is  of  some  value 
in  mixed  infections  involving  stomach  worms,  hookworms  and 
small  trichostrougyles. 

Copper  Sulphate  and  Sodium  Arsenite.  This  mixture  in 
powder  form  has  long  been  employed  in  South  Africa,  where 
it  is  known  as  the  "Government  Wireworm  Remedy."  It  is 
composed  of  4  parts  of  copper  sulphate,  partly  dehydrated, 
and  1  part  of  sodium  arsenite.  Special  measuring  spoons  are 
employed  to  insure  correct  dosage,  which  is  as  follows:  For 
lambs  2  to  4  months  old,  0.2  gram  of  the  mixture;  4  to  6 
months  old,  0.25  gram;  6  months  to  2-tooth  animals,  0.375 
gram;  2-tooth  sheep,  0.5  gram;  4-tooth  sheep  and  over,  0.625 
gram.  The  remedy  is  said  to  be  contraiudicated  in  the  pres- 
ence of  heavy  Trichostrongylus  infections;  smaller  doses  should 
be  used  when  the  sheep  are  in  poor  condition  or  when  they 
are  grazing  on  young  grass  in  the  spring.  All  animals  should 
be  kept  from  water  for  at  least  7  hours  before  and  after  treat- 
ment; otherwise  rapid  absorption  of  the  drug  may  occur  and 
lead  to  arsenical  poisoning. 

Phenothiazine.  Evidence  presented  under  the  discussion 
of  the  treatment  against  nodular  worms  indicates  that  this  drug 
represents  an  effective  treatment  against  H.  contortus.  While 
its  use  on  more  animals  may  disclose  some  limitations  or  con 
traindications,  it  appears  to  be  of  great  value,  particularly 
because  of  its  eiBcaey  in  concomitant  infections  with  many  of 
the  other  gastrointestinal  parasites  which  are  commonly  found 
in  sheep.  If  onlj-  the  common  stomach  worm  is  present,  doses 
as  small  as  10  grams  per  adult  sheep  may  be  employed;  how- 
ever, if  other  species  are  present,  it  is  probably  advisable  to 
use  a  dose  of  25  grams. 

treatment   for   infeptions   with    small    trichostronoyles, 

trichostrongyles   spp.,  ostertaoia   spp.,   cooperia  spp.,  and 

nematodirus  spp. 

On  the  basis  of  present  evidence,  phenothiazine  is  the  treat- 
ment of  choice  for  the  removal  of  worms  of  these  genera  from 
sheep.  From  tests  carried  out  to  date  it  would  appear  that  in 
sheep  phenothiazine  is  probably  less  effective  against  Cooperia 
spp.  and  Nematodirus  spp.  than  against  these  other  genera. 
However,  the  general  utilitarian  value  of  the  drug  against 
most  nematode  parasites  of  the  gastrointestinal  tract  of  sheep 
ranks  it  above  all  others  at  present.  English  investigators 
(Taylor  and  Sanderson,  1940;  Lapage,  1940)  have  reported 
that  sheep  treated  with  doses  of  phenothiazine  varying  from 
5  to  30  grams  gained  more  rapidly  than  untreated  controls; 
Ostertagia  spp.  were  the  principal  nematodes  encountered  in 
the  test  animals. 

The  "Cu  Nic"  solution  will  freciuently  remove  satisfactory 
percentages  of  these  various  worms.  In  Australia,  Gordon  and 
Clunies  Ross  (1936)  found  that  sheep  exposed  to  continual 
heavy  infection  with  Trichostrongylus  spp.  were  adequately  pro 
tected  by  routine  treatment  at  intervals  of  3  weeks  with  a  2 
percent  solution  of  copper  sulphate  and  commercial  nicotine 
sulphate.  Similar  protection  was  obtained  by  the  use  of  15 
ec.  of  a  2  percent  solution  of  copper  sulphate  followed  imme- 
diately by  2.5  cc.  of  tetrachlorethyleue  repeated  at  the  same 
intervals.  The  recommended  dose  of  the  2  percent  copper 
sulphate  and  nicotine  sulphate  solution  is  as  follows: 

Adult  sheep  2        ounces   (60  cc.) 

Sheep  12  to  18  months       1.5     ounces   (45  cc.) 

Lambs  8  to  12  month  1.0     ounce     (30  cc.) 

Lambs  4  to  8  months  0.75   ounce     (22  cc.) 

Lambs  under  4  months  0.5     ounce     (15  cc.) 

Treatment  for  the  removal  of  worms  of  the  above-mentioned 
genera  from  cattle  is  not  well  established.  In  limited  experi 
ments,  Swanson,  Porter  and  Connelly  (1940)  found  that  un- 
conditioned phenothiazine  administered  to  calves  in  doses  of 
50  to  80  grams  (0.44  to  1.1  grams  per  kilogram  of  body  weight) 
removed  all  T.  axci  present.  The  treatment  was  approximately 
84  percent  effective  against  0.  ostertagi  but  only  slightly  effec- 
tive against  Cooperia  spp. 

TREATMENT  FOR  LUNOWORM  INFECTION 

Protostrongylnx  and  Mnellerivs  infections  are  not  susceptible 
to    treatment    but    numerous    drugs    have    been    recommended 


against  Dictyocauliis  filaria,  chiefly  for  administration  by  in- 
sufflation or  by  intratracheal  injection.  Evidence  for  the  use 
of  these  preparations  is  not  convincing.  Orloff  (1935)  recom- 
mended injections  into  the  trachea  on  2  successive  days  of  10 
cc.  of  a  mixture  of  1  cc.  of  a  10  percent  tincture  of  iodine,  50 
cc.  of  glycerin  and  150  cc.  of  distilled  water.  The  sheep  are 
placed  on  the  back  and  after  injection  are  held  in  a  sitting 
position  for  half  a  minute.  McGrath  (1931)  found  Lugol's 
solution  of  no  value  and  responsible  for  the  causation  of 
pneumonic  lesions.  McGrath  believed  that  the  intratracheal 
injection  of  the  mixture  recommended  by  the  New  South 
Wales  Department  of  Agriculture  provided  good  results.  This 
mixture  consisted  of  chloroform  0.5  cc,  oleum  terebinthinae  1 
cc,  and  olive  oil  2  cc.  However,  Kauzal  (1932)  was  not  suc- 
cessful in  removing  all  worms  with  this  mixture.  Vein  and 
Zottner  (1937)  used  a  dose  of  10  cc.  of  an  aqueous  solution  of 
1  mgm.  of  pyrethrin  per  dose ;  this  was  repeated  three  times. 
These  treatments  are  for  sheep  but  could  probably  be  used 
for  calves  also. 

Until   more   substantial   evidence   is   obtained   for   the   value 
of  medicinal  treatment,  the  most  logical  procedure  is  to  give 
infected   animals   good  nursing   treatment,   remove  them   from 
infected  pastures  and  provide  feed   which  will  satisfy  all  nu 
tritional  requirements. 

Anthelmintic  Medication   for  Nematodes  of  Poultry 

TREATMENT  FOR   STRONGVLOIDES   INFECTION 

Gentian  violet  exerts  a  specific  action  against  Strongyloidcs 
avium  and,  in  birds  in  which  treatment  is  indicated,  this  would 
be  the  drug  of  choice.  Wright  and  A^an  Volkenberg  (1937) 
found  that  a  dose  of  1  grain  (64  mgm.)  three  times  a  day  for 
10  days  for  birds  weighing  3  to  4  pounds  removed  all  of  these 
worms  from  the  small  intestine  and  the  ceca.  However,  this 
course  of  treatment  resulted  in  inflammation  of  the  digestive 
tract.     Single  doses  up  to  10  grains  were  not  effective. 

TRflATSIENT  FOR  CAPILLARIA  COLUMBAE  AND  C.  RETUSA  INrBCTIONS 

There  is  no  established  treatment  for  the  removal  of  capil- 

larids  from  the  lumen  of  the  digestive  tract.  Carbon  tetra- 
chloride has  been  reported  to  be  of  value  in  chickens  when 
given  in  a  dose  of  1  cc  and  repeated  in  1  week.  However, 
the  evidence  for  this  is  contradictory  as  other  investigators 
have  not  obtained  promising  results  with  this  drug  either  in 
chickens  or  pigeons.  Thymol  has  been  recommended  for  pigeons 
in  a  dose  of  5  cgm.,  repeated  on  alternate  days  until  3  doses 
have  been  given.  The  last  dose  is  followed  by  castor  oil.  Per- 
haps halogenated  hydrocarbons  other  than  carbon  tetrachloride 
might  be  of  benefit,  although  to  be  of  value  any  treatment 
would  probably  have  to  be  repeated  several  times.  In  any  ease, 
worms  in  the  ceca  would  be  particularly  difficult  to  remove. 

TREATMENT  FOR  ORNITHOSTRONGYLUS  QUADRIRADIATUS  INFECTION 

Thymol  has  been  reported  to  be  of  value  though  such  reports 
have  not  been  confirmed.  Tetrachlorethyleue  in  doses  of  0.5 
to  1  cc.  will  sometimes  remove  some  of  the  worms,  although  it 
does  not  constitute  a  dependably  eft"ective  treatment.  In  fact, 
Cuvillier  (1937)  stated  that  the  lack  of  any  anthelmintic  of 
demonstrated  efficacy  against  the  parasite  indicated  the  impor- 
tance of  applying  preventive  measures. 

TREATMENT  FOR  AMIDOSTOMIIM   ANSBXIS   INFECTION 

Schmid  (1930)  treated  geese  with  carbon  tetrachloride  in 
doses  of  1  to  1.5  cc.  in  8  cc  of  flour  paste  injected  into  the 
crop  and  reported  excellent  results,  the  birds  improving  in 
condition  and  the  losses  in  the  flock  being  checked.  Schu- 
mann (1930)  had  good  results  following  doses  of  1  ec  of  car- 
bon tetrachloride  administered  in  gelatin  capsules.  Jerstad 
(1936)  removed  all  of  11  Amidostomum  from  a  goose  ivith  a 
single  dose  of  2  ec.  of  carbon  tetrachloride. 

TREATMENT  FOR  SYNGAMUS  TR.\CHEA  INFECTION 

Mechanical  removal  of  the  worms  may  be  accomplished  by 
means  of  a  fine  wire,  a  barbed  feather  or  other  similar  devices 
commonly  used  by  poultrymen.  However,  the  method  is  te- 
dious and  time  consuming  and  not  adapted  for  flock  treatment. 
Several  workers  have  recommended  the  intratracheal  injection 
of  several  drops  of  a  5  percent  solution  of  Aniodol  (trioxy- 
methylene). 

Wehr,  Harwood  and  Sehaffer  (1938)  obtained  an  indicated 
efficacy  of  98  percent  for  the  removal  of  these  worms  by  in- 
sufflation with  barium  antimonyl  tartrate.  The  birds  are 
placed  in  a  tightly  closed  container  and  the  finely  powdered 
drug  is  dispersed  throughout  the  air  several  times  by  means 
of  a  blower. 


346 


■I'liKATJlKNT    FOll    llKTKRAKl.S    (iAl.1.1  N  AK    INKKCTION 

Siiisle  doses  of  a  lunubor  of  dviiRs  luliiiiMisteiod  iirallv  will 
ri'iuove  some  lieterakiiis  but  few  of  tlu'se  drupts  exliiliit  a  ilc 
peudable  efficacy.  It  is  probable  that  in  most  eases  tlie  drus 
does  not  actually  penetrate  into  the  ceca  to  any  great  extent. 
Tlu'  flock  treatment  for  Ascaridia  with  tobacco  dust  mixed 
with  mash  will  remove  some  worms  over  a  period  of  tinu^  liut 
results  are  variable. 

Recently  McCuUoch  and  Nicholson  (1940)  reported  that 
phenothiazine  in  doses  varying  from  O.O.")  to  1  gram  per  bird 
removed  :;,0.">li  Ilcterakis  from  1:2  chickens  and  failed  to  re- 
move 8S0,  but  of  the  worms  not  removed  all  except  121  had 
been  killed  by  the  action  of  the  drug  by  the  time  the  birds 
came  to  necropsy.  Also  in  repeated  doses  varying  from  O.O.'i 
to  0.5  grams  per  dose,  phenothiazine  removed  4,C(>3  worms  from 
l.")  chickens.  All  of  the  277  Hctcrakis  not  removed  by  the  time 
the  birds  came  to  necropsy  had  been  killed  by  the  action  of 
the  drug. 

Rectal  injections  by  means  of  a  hard  rubber  enema  syringe 
of  a  mixture  of  0.1  cc.  of  oil  of  ehenopodium  in  5  ec.  of  cot- 
tonseed oil  for  a  1..5  pound  (080  gram)  bird  were  found  by 
Hall  and  Shillinger  (1923)  to  remove  90  percent  of  the  heter- 
akids  from  chickens.  Probably  double  this  dose  would  be  ef- 
fective for  birds  weighing  3  pounds  (1.36  kgm.)  or  more. 
This  mixture  may  be  made  up  at  the  rate  of  1  teaspoonful 
(4  ce.)  of  oil  of  ehenopodium  in  li  fluid  ouncQS  (180  cc.)  of 
cottonseed  oil,  and  given  at  the  rate  of  Vs  fluid  ounce  (10  cc.) 
for  birds  weighing  3  pounds  or  more,  using  a  proportionately 
small  dose  for  smaller  birds.  The  two  ingredients  should  be 
thoroughly  mixed  before  administration.  The  tip  of  the  syringe 
should  be  passed  along  the  floor  of  the  cloaca  and  the  mix- 
ture injected  slowly. 

TRE.\TMF.N'T   FOR   ASCARIDIA   OOLUMBAE   INFECTION 

Carbon  tetrachloride  in  repeated  doses  of  0.5  to  2  ce.  ad- 
ministered in  liquid  paraffin  on  several  consecutive  days  has 
been  found  entirely  effective  in  removing  these  worms  from 
pigeons.  Tetrachlorethylene  in  a  dose  of  0.6  cc,  preceded  and 
followed  by  sodium  sulphate,  is  said  to  constitute  an  effective 
treatment. 

TRE,\TMENT  FOR  ASCAKIDIA  GALLI  INFECTION 
Various  treatments  are  available  in  single  doses  for  the  re 
moval  of  these  worms.  Tetrachlorethylene  in  a  dose  of  1  cc. 
for  average  sized  birds  is  very  effective.  For  young  chickens, 
the  dose  should  be  reduced  in  accordance  with  the  weight  of 
the  bird.  Carbon  tetrachloride  is  not  as  effective  as  tetra- 
chlorethylene but  n-butylidene  chloride  in  doses  of  2  cc.  for 
adult  birds  removed  all  ascarids  from  test  birds.  These  drugs 
may  be  administered  in  gelatin  capsules  but  care  should  be 
taken  that  the  drugs  do  not  enter  the  lungs. 

Nicotine  sulphate  combined  with  Lloyd's  alkaloidal  reagent, 
a  selected  diatomaceous  fuller's  earth,  is  a  very  effective 
single  dose  treatment.  Recommendations  call  for  the  adminis- 
tration to  each  bird  of  a  No.  2  capsule  containing  35  cgm. 
(5.45  grains)  of  a  mixture  of  6.6  cc.  of  40  percent  nicotine 
sulphate  solution  and  16  grams  (4  drams)  of  Lloyd's  reagent. 
Certain  flock  treatments  are  effective  for  the  removal  of 
Ascaridia  and  obviate  the  individual  treatment  of  birds.  The 
one  recommended  first  by  the  California  experiment  station 
calls  for  the  addition  to  the  mash  of  2  percent  by  weight  of 
tobacco  dust  containing  at  least  1.5  percent  of  nicotine;  this 
mixture  is  fed  for  a  period  of  3  to  4  weeks  and  repeated  at 
3-week  intervals.  For  a  single  flock  treatment,  the  California 
station  recommended  the  use  of  1  teaspoonful  of  oil  of  eheno- 
podium, thoroughly  mixed  with  moist  mash,  for  each  lot  of  12 
chickens. 

TREATMENT    FOR    OXYSPIRURA    MANSONI    INFECTION 

A  treatment  which  has  been  found  of  value  consists  in  the 
administration  of  1  or  2  drops  of  a  5  percent  solution  of  creo- 
lin  under  the  nictitating  membrane  of  the  eye  which  is  first 
anaesthetized  with  cocaine  or  a  5  percent  solution  of  butyn. 
The  creolin  should  be  washed  out  promptly  with  water.  The 
worms  killed  by  the  treatment  are  usually  carried  down  the 
lacrimal  duet.  The  use  of  a  10  percent  solution  of  argyrol 
as  a  supplementary  treatment  is  of  value  in  relieving  the  irri- 
tation and  in  helping  to  control  concomitant  bacterial  infection. 

TREATMENT  FOR  DISPHARYNX  SPIR.VLIS  INFECTION 
Whitney  (1925)  tried  carbon  tetrachloride  and  turpentine  in 
pigeons  and  believed  the  latter  to  be  more  effective.  He  gave 
a  No.  0  gelatin  capsule  filled  with  dry  magnesium  sulphate  12 
to  24  hours  prior  to  treatment;  one  No.  0  capsule  of  turpen- 
tine was  then  given  night  and  morning  for  4  days,  the  last 
dose  being  followed  by  2  cc.  of  castor  oil.  Pigeons  treated  by 
this  method   showed  marked  clinical   improvement. 


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Wright,  W.  H.  and  Underwood,  P.  C.  1934. — Fouadin  in  the 
treatment  of  infestations  with  the  dog  heartworm,  Diro- 
filaria  immitis.    Vet.   Med.,  v.   29(6)  :234-246. 

Wright,  W.  H.  and  Van  Volkenbert,  H.  L.  1937. — Critical 
tests  with  various  dyes  as  anthelmintics  for  chickens.  Rev. 
Med.  Trop.  y  Parasit.,  v.  3(2)  :125-132. 

Young,  D.  B.  1930. — Diagnosis  of  worm  pa-asites  in  the  fox. 
Am.   Fur  Breeder,  v.  3(3)  :31. 


349 


CHAPTER  X 
FEEDING  HABITS  OF  NEMATODE  PARASITES  OF  VERTEBRATES 

J.  E.  ACKERT  and  J.  H.  WHITLOCK,  Kansas  State  College.  Manhattan,  Kansas 


'J'lit'  obscured  habitats  of  the  parasitic  nematodes  preclude 
ready  observations  upon  their  feeding  haljits.  Indications  of 
their  nutritive  needs  have  been  gained  from  chemical  analyses 
of  the  worm  bodies.  Weinland  (litOl)  found  that  glycogen 
made  up  one  fourth  to  one-third  of  the  dry  substance  of  the 
ascarid  body.  Flury  (1912)  was  led  to  believe  that  ascarids 
had  essentially  the  same  chemical  constitution  as  other  animals. 
He  found  only  such  minor  differences  as  a  lack  of  uric  acid, 
creatinine  and  the  substitution  of  a  high  molecular  alcohol 
(ascarjl  alcohol)  for  glycerol  in  combination  with  fatty  acids. 
From  these  studies  it  seemed  probable  that  the  nutritive  needs 
of  parasitic  nematodes  are  fundamentally  the  same  as  those  of 
other  animals,  although  Aekert  (1930)  has  shown  that  there  is 
no  evidence  to  indicate  that  Atirarklia  galli  needs  Vitamin  .\, 
Vitamin  B   (complex),  or  Vitamin  D. 

As  most  of  the  research  on  the  feeding  habits  of  nematodes 
has  been  upon  adult  forms,  they  will  be  discussed  first;  then 
tl  larval  forms  will  be  compared  with  the  adults,  and  the  sec- 
tion will  close  with  a  brief  review  of  digestion  in  the  parasitic 
nematodes.  Although  there  are  many  diverse  groups  of  nema- 
todes, few  methods  of  parasitic  feeding  have  been  evolved. 
The  similarity  of  these  feeding  habits  in  nematode  groups 
which  are  widely  separated  morphologically  would  make  a  dis- 
cussion of  nutrition  from  a  primarily  taxonomic  standpoint 
repetitious;  hence  the  subject  will  be  discussed  from  an  eco- 
logical and  physiological  standpoint  rather  than  from  that  of  a 
morphological  classification. 

Ecologically,  iiarasitie  nematodes  may  be  grouped  as  to 
whether  they  are  associated  with  the  physiological  interior  or 
exterior  of  the  host  body.  The  physiological  exterior  of  the 
body,  as  here  considered,  is  marked  by  any  epithelial  mem- 
brane lining  a  cavity  which  communicates  with  the  exterior  of 
the  host  body. 

Most  of  the  parasitic  helminths  are  associated  with  the  physi- 
ological exterior  of  the  bodj',  particularly  the  mucosae.  This 
group  will  be  subdivided  upon  the  l>asis  of  being  attached  to 
the  mucosae  most  of  the  time  or  usually  unattached.  Attached 
nematodes  maj-  hold  their  positions  by  the  buccal  capsule  grasp- 
ing the  mucosa  {Ancylostoma,  A'ecator,  Strongylus)  or  by  pene 
tration  of  the  mucosa  (Fhysaloptcra,  Trichuris).  Nematodes 
unattached  to  the  mucosa  may  be  closely  associated  with  it 
(Haemonchus,  Mctastrongylns)  or  not  closely  associated  with 
it  {A.icaris,  Ascaridia,  Hrtcrakis,  Oxyuris).  Nematodes  in- 
habiting the  physiological  interior  of  their  hosts  are  best  ex 
emplified  by  Dirofilaria,  Spirocerca  and  Strongyloides. 

Nematodes  in  the  Physiological  Exterior  of  the  Body 

NEMATODES   ATTACHED   TO   Ml'COSA    BY  BUCCAL 
CAPSULE 

The  best  examples  of  this  group  are  the  hookworms  Aiii-i/hi 
stoma  and  Necator  which  apparently  remain  attached  to  the 
intestinal  mucosa  much  of  the  time.  The  sucker-like  oral  open 
ing  and  the  adjacent  teeth  or  cutting  plates  afford  effective 
means  of  attachment  and  bloodletting.  Since  the  earliest 
recorded  observations,  blood  has  been  considered  as  a  prob 
able  food  of  hookworms.  Grassi,  according  to  Leichtenstern 
(1886),  saw  hookworms  eject  blood  both  from  the  mouth  and 
the  anus.  Leichtenstern  thought,  as  did  Grassi,  that  much 
more  blood  is  withdrawn  by  the  parasite  than  is  necessary  for 
its  food.  As  the  fecally  deposited  red  cells  seemed  to  be  prac 
tically  unchanged,  Leichtenstern  inferred  that  the  plasma  must 
be  the  main  source  of  nourishment.  In  1888  Ernst  noted  the 
emission  of  blood  from  the  mouth  cap.sule  and  Whipple  (1909) 
observed  the  oral  and  anal  emission  of  blood  in  both  Xecator 
and  Ancylostoma.  Whipple  believed  that  there  was  a  rapid 
ingestion  of  blood  by  the  parasite.  Aekert  and  Payne  (1923) 
who  took  Necator  suillus  repeatedly  from  the  intestines  of 
freshly  killed  swine  frequently  noted  female  specimens  v\-ith 
bodies  colored  red  from  ingested  blood.  On  the  other  hand 
some  workers,  notably  Looss  (190.5)  and  Ashford  and  Igara 
videz  (1911),  maintained  that  blood  is  not  the  normal  food  of 
hookworms.  They  observed  worms  lacking  blood  even  when 
they  were  attached  to  the  intestine.  They  found  tissue  ele 
ments  and  shreds  of  mucosa  in  both  the  esophagus  and  intestine 
and  concluded  that  the  parasites  fed  primarily  on  the  mucous 
membranes;  the  blood  in  the  tract  was  thought  to  be  due  to 
accidental  hemorrhage  from  hookworm  bites.  Support  for  the 
view  that  portions  of  the  mucosae  serve  as  food  for  such  worms 
was  given  by  Hoeppli  (1930),  who  found  that  Ancylostoma 
duodenale  is  more  than  a  blood  sucker.  The  piece  of  mucous 
membrane  taken  in  )iy  the  mouth  capsule  is  rasped  by  the  teeth. 


Blood  from  surface  vessels  pours  into  the  buccal  capsule  where 
.secretions  from  the  esophageal  glands  partially  digest  the 
blood  and  loosened  portions  of  the  mucosae.  "After  this  di- 
gestion has  taken  place,  the  liquefied  masses  are  swallowed  by 
the  worm."  Evidence  that  disintegration  had  taken  place  wa.s 
furnished  by  staining  the  tissue  at  the  bottom  of  the  mouth 
capsule  and  in  the  lumen  of  the  esophagus. 

Wells  (1931)  in  a  series  of  ingenious  experiments  was  able 
to  observe  living  Ancylostoma  canitium  in  the  act  of  feeding. 
He  was  able  to  observe  the  attachment  of  the  hookworms  to 
the  mucosa,  study  the  details  of  the  blood-sucking  process,  the 
passage  of  the  blood  through  the  intestine  of  the  worm,  and 
its  ejection  through  the  anal  orifice.  From  the  volumes  of 
blood  withdrawn  by  the  parasite  and  the  rapid  rate  at  which  it 
passed  through  the  intestine.  Wells  was  of  the  opinion  that  the 
food  of  the  hookworm  consists  of  simple  dift'usable  substances 
in  the  host  blood. 

In  studies  upon  the  food  of  the  dog  hookworm,  Ancylostoma 
caniiiiim,  Hsii  (1938)  made  serial  sections  of  hookworms  taken 
from  living  hosts  and  found  red  blood  cells  in  all  worms;  ho 
also  found  fragments  of  host  tissue  and  white  blood  cells  all 
of  which  were  in  stages  of  disintegration.  As  further  evidence 
of  blood  as  food  for  the  hookworms,  Hsii  reported  the  find  g  of 
pigment  granules  in  the  cytoplasm  of  the  worms'  intestinal 
cells,  which  gave  positive  iron  reaction.  These  granules,  which 
were  found  in  large  quantities  throughout  the  whole  intestine, 
the  author  interpreted  as  owing  their  origin  to  the  breaking 
down  of  red  blood  corpuscles.  Hsii  did  not  find  intestinal  con 
tents  of  the  host,  worm  eggs,  or  bacteria  in  the  hookworms' 
intestines.  He  concluded  that  the  food  of  A.  caninum  consisted 
of  blood  and  mucosa  cells. 

Other  nematodes  that  attach  by  means  of  buccal  capsules  in- 
clude such  forms  as  Strongyhis,  Chabertia  and  Camallanus,  all 
of  which  are  known  to  draw  intestinal  epithelium  into  their 
mouths.  From  the  disintegrated  condition  of  the  tissue  so 
drawn  in,  it  is  probable  that  epithelial  tissue  and  blood  form 
a  portion  of  their  food.  Whitlock  (unpublished),  who  has 
worked  extensively  with  living  equine  strongyles,  has  noted  in 
the  worm  intestines  material  resembling  partially  digested 
blood.  Wetzel  (1931b),  studying  Chabertia  ovina  (Fab.)  in 
sheep  colons,  found  that  the  nematodes  feeds  on  the  propria 
mucosae  which  it  draws  into  its  buccal  capsule.  The  tissue 
fragments  which  are  loosened  by  the  gnawing  of  the  nematode 
are  partially  digested,  according  to  Wetzel,  by  secretions  from 
the  dorsal  esophageal  gland. 

Support  of  the  view  that  C.  ovina  attacks  the  mucous  mom 
brane  is  afforded  by  the  work  of  Kauzal    (1936)    who  found 
numerous  small  hemorrhages  on  the  mucous  membrane  of  the 
large  intestine  of  sheep  which  he  attributed  to  C.  ovina.    He 
examined  250  of  these  specimens  quantitatively  for  iron  which 
he  assumed  to  be  derived  from  haemoglobin.    The  presence  of 
the    haemoglobin   and    the    reddish    tint    of    the    intestinal    con 
tents  of  the  immature  C.  ovina  led  Kauzal  to  infer  that  thi.s 
nema   ingests   considerable   quantities   of   blood.      That   the   at 
tachment  to  the  intestinal  mucosae  by  the  buccal  capsule  is  a 
widespread    feeding    phenomenon    among    the    Strongyloidea    is 
further  shown  by  Magath  (1919)  for  Camaltanus  amcricanus  in 
the   turtle  intestine  and   by  Hoeppli  and  Hsii    (1931)    t'oi-   h'ul- 
icephalus  sp.   in  the   enteric  caual  of  snakes. 

NEMATODES  ATTACHED  MUCH  OF  THE  TIM  10   I'.V 
PENETRATION  OF  THE  MUCOSA 

Typical  examples  of  this  group  are  Trichuris  and  Physalop- 
tera.  The  food  of  Trichuris  apparently  is  secured  while  the 
anterior  extremity  is  imbedded  in  the  mucous  membrane  of 
the  large  intestine.  Christofferson  (1914)  who  reviewed  the 
literature  on  Trichuris  (Trichoccphalns)  up  to  1914,  observed 
a  peculiar  cell  transformation  about  the  imbedded  anterior  por 
tion  of  these  nematodes.  Hoeppli  (1927)  found  such  changes 
in  human  and  baboon  intestines  in  which  the  Trichuris  made 
tunnels  in  the  mucosa  parallel  with  the  surface  of  the  intestinal 
lining.  Surrounding  the  anterior  ends  of  the  trichurids  in 
these  tunnels,  the  epithelial  cells,  according  to  Hoeppli,  were 
transformed  into  syncytial-like  structures  with  eosinophilic 
homogeneous  protoplasm  and  pycnotie  nuclei  as  a  result  of  the 
action  of  a  liquifying  secretion  from  the  worm.  Hoeppli 's 
studies  (1927,  1933)  led  him  to  believe  that  the  liquified  syn- 
cytial material  was  taken  by  the  trichurids  as  food. 

That  Tricliuris  may  take  blood  was  indicated  by  the  studies 
of  Guiart  (1908)  who  found  blood-engorged  trichurids.  Garin, 
cited  by  Otto  (1935),  likewise  found  Trichuris  filled  with  blood 
and  reported  that  blood  was  found   in   the  stools  of  50  out  of 


3.50 


.'>4  tricliuris  iiit'i'c-tod  patients.  In  support  of  tlie  view  that 
these  nematodes  may  feed  on  lilood  were  the  tindinjjs  of  Li 
(1933e)  and  Chitwood  and  C'hitwood  (My^l)  that  the  adult  Tri- 
chtiria  bears  a  stylet  capable  of  insertion  suflieient  for  drawing 
blood.  Chitwood  and  Chitwood  (ISU?")  showed  that  the  anterior 
muscular  [lart  of  the  trieluiroid  esophaKUs  possesses  uiuselcs 
capable  of  the  dilation  necessary  for  .sucking.  Moreover,  they 
found  by  serial  sections  a  large  number  of  red  coipuscles  in  Ihc 
esophageal  lumen  of  Trichi(ri.i.  While  Smiruov  (1936),  after 
a  comprehensive  study  of  the  literature  and  of  serial  sections 
of  worms,  concluded  that  there  was  no  convincing  evidence 
that  trichurids  feed  on  blood,  the  fact  remains  that  Whipple 
(IIHH))  and  Garin  (1913)  reported  the  occurrence  of  hemolytic 
enzymes  in  Trichiiris.  From  the  various  studies  made  it  ap- 
pears that  trichurids  secure  their  food  from  the  intestinal 
mucosa  and  that  it  may  consist  of  liquified  mnco.sal  tissue  and 
Idood  elements. 

Studies  on  the  food  of  Tricliim  Uti  xpiralix  were  made  by 
Heller  (1933)  who  introduced  encysted  trichina  larvae  enclosed 
in  collodion  sacs  into  the  snuiU  intestines  of  cats  and  rats. 
While  the  meat  around  the  larvae  was  digested  in  0  to  8  hours, 
they  made  no  growth  in  1  to  3  days.  Trichiiiella  larvae  en- 
closed in  fine  silk  bags  and  thus  kept  away  from  the  intestinal 
mucosa  likewise  did  not  develop.  That  these  nearly  adult 
trichinae  do  not  feed  on  intestinal  contents  seems  likely  also 
from  other  tests  by  Heller  who  fed  India  ink  along  with  meat 
containing  encysted  larvae,  but  failed  to  find  any  ink  in  the 
worms'  intestines.  Sections  of  intestinal  tissue  made  after 
the  encysted  trichinae  were  fed  showed  that  the  freed  larvae 
penetrated  the  intestinal  mucosa,  where  the  maturing  trichinae 
doubtless  secure  their  food. 

Following  the  work  of  Heller,  McCoy  (1934)  injected  sterile 
TrichineUa  larvae  from  digested  rat  muscle  into  the  amniotic 
sac  of  chick  embryos  li  to  1.5  days  old.  Definite  growth  of  the 
maturing  larvae  occurred  in  only  about  1  or  2  percent  of  the 
trichinae.  A  single  female  developed  to  sexual  maturity.  Bet 
ter  success  was  attained  in  a  second  series  of  experiments  in 
which  the  sterile  larvae  were  injected  into  the  amniotic  sacs  of 
rat  embryos  on  approximately  the  14th  day  of  gestation.  In 
2  to  ,■)  days,  practically  all  worms  were  developing  at  nearly 
the  normal  rate  and  on  the  fifth  day,  numerous  female  trichinae 
were  found  with  embryos  developing  in  their  uteri.  These  re 
suits  give  further  evidence  that  TrichineUa  normally  feeds  upon 
host  body  fluids  secured  from  the  mucous  membrane.  Moreovei', 
van  Someren  (1939)  reported  a  functional  buccal  stylet  in  T. 
spiralis  and  indicated  that  it  is  used  to  lacerate  the  host  tissue 
and  release  tissue  fluids.  From  the  examination  of  living 
specimens  immediately  after  recovery,  van  Someren  believed 
that  the  food,  which  is  in  a  fluid  state  when  ingested,  consists 
of  tissue  fluids,  cell  contents,  or  perhaps  predigested  tissue  acted 
on  by  a  tissue  lysate  from  the  anterior  esophageal  glands. 

Among  other  nematodes  attached  much  of  the  time  to  the 
enteric  mucosa  is  Plnisaloptcra.  Studies  by  Hocppli  and  Feng 
(1931)  showed  that  the  mucosa  about  the  anterior  ends  of  these 
attached  worms  was  liquified  or  partially  digested,  presumably 
from  esophageal  secretions  from  the  nematodes.  Studies  of 
sectioned  mucosa  showed  definite  excavation  of  tissue  immedi- 
ately around  the  anterior  ends  of  the  worms,  presumably  from 
the  taking  of  the  liquified  tissue  as  food. 

UNATTACHED   NEMATODES   CLOSELY   ASSOCIATED 
WITH  THE  MUCOSA 

Many  nematodi's  belonging  to  this  grou]),  while  Iniving  jioorly 
developed  buccal  capsules,  are  able  to  puncture  the  mucous 
membrane  and  draw  blood.  For  example,  Stadehnann  (1891) 
found  blood  corpuscles  in  the  nearly  nuiture  Ostertagia  oster- 
tagi  (Strongylu.i  convolutiis)  in  nodules  of  the  abomasum,  and 
Dikmans  and  Andrews  (1933)  found  such  stages  of  Ostertagia 
circwmcincta  in  the  mucosa  and  partly  free  in  the  abomasal 
lumen  of  sheep.  Unfortunately,  however,  much  of  the  evi- 
dence is  circumstantial.  Thus  Ransom  (1911),  writing  of 
Haemonchus  contortiis  and  Ostertagia  ostertagi,  stated  that 
they  evidentl.v  suck  blood  for  the  heavily  infected  liosts  arc 
anaemic.  Other  writers  simply  state  that  they  suck  blood. 
Veglia's  (191(5)  observations  on  living  worms  demonstrated 
that  the  oral  lancet  made  definite  cutting  movements.  Fallis 
(1938)  placed  Nematodirus  among  the  blood  suckers  on  the 
basis  of  a  spectroscopical  analysis  of  the  body  fluid  which 
showed  the  absorption  bands  for  oxyhaemoglobin.  In  the  same 
year,  Davey  (1938),  who  studied  the  food  of  nematodes  of  the 
alimentary  tract  of  sheep,  questioned  the  spectroscopic  demon 
stration  of  haemoglobin  in  nematodes  as  evidence  of  their  being 
blood  suckers.  He  found  that  haemoglobin  was  present  in  tissues 
other  than  the  alimentary  canal  of  Nematotlinis  spathigrr  and 
that  its  absorption  bands  had  different  positions  from  those  in 
the  blood  of  their  hosts.  These  facts,  together  with  his  finding 
of  haemoglobin  in  species  of  Trichostrongylidae  long  after 
any  haemoglobin  from  the  host  would  have  decomposed,  proved 


Ihat  these  nematodes  could  synthesize  haemoglobin.  Davey 's 
(1938)  culture  tests  with  serum,  blood  digests,  and  defibrinated 
blood  as  food  for  Ostertagia,  Cooperia,  Nematodirus  and  Tri- 
vliostrongi/lus  were  unsuccessful,  as  were  also  those  on  abo- 
masum fluid  for  Ostertagia  circumciiicta.  These  negative  re- 
sults led  him  to  the  conclusion  that  these  nematodes  with  rudi- 
mentary buccal  capsules  pjobably  feed  on  tissue  elements  at  oi 
ill  the  mucosa. 

Other  evidence  of  intinuite  association  of  trichostrongyles 
with  the  mucosa  of  the  alimentary  tract  is  available  from  rab- 
bit neumtodes.  Alicata  (1932)  experimentally  infected  rabbits 
with  Olxliscoides  ciinieiili  by  feeding  infective  larvae.  Ex 
amination  about  2  months  later  showed  nematodes  free  on  the 
mucous  membrane  of  the  stomach  or  under  the  membrane  and 
into  the  snbmncosa.  That  such  trichostrongyles  feed  from  the 
enteric  wall  was  the  opinioTi  of  Wetzel  and  Enigk  (1937)  who, 
on  infecting  raljbits  with  (irapliidiiim  strigosum,  found  tlie 
stonuich  mucosa  bloody.  Enigk  (1938)  examined  the  intestinal 
contents  of  several  sexually  mature  G.  strigosum  and  found  a 
colorless  viscous  mass  containing  nuclear  remnants  apparently 
from  white  blood  cells,  granules  and  bacteria.  Other  tests  such 
as  feeding  the  rabbits  pulverized  chaicoal.  trypan  blue  and  car 
mine  resulted  in  these  substances  being  ingested  by  the  nenm 
todes.  Also,  injecting  the  hosts  intravenously  with  trypan  blue 
for  several  days  resulted  in  the  worms  taking  up  several  blue 
colored  particles  presumably  desquamated  mucosa  cells.  Enigk 
concluded  that  G.  strigosiim's  food  consists  of  gastric  mucosa, 
gastric  juice  and  stonnxch  contents. 

Other  unattached  nematodes  closely  associated  with  the  mn 
cosa  include  lungworms  which  inhabit  the  bronchi  and  bron 
chioles.  Hung  (1920)  studying  swine  lungs  infected  with  adult 
Metastrongylus  elongatus  frequently  found  eosinophiles  and  red 
blood  corpuscles  in  the  worms'  intestines.  The  findings  of  Por- 
ter (1930),  who  made  similar  studies,  indicated  that  the  mate- 
rial in  the  worms '  intestines  consisted  of  elements  identical 
with  those  found  in  the  exudate  surrounding  the  nematodes. 
In  cross  sections  of  the  worms.  Porter  recognized  large  uum 
bers  of  eosinophilic  and  neutrophilic  polymorphonuclear  leuco- 
cytes, lymphocytes  and  desquamated  epithelial  cells.  Erythro- 
cytes w^ere  seen  in  some  instances.  These  and  some  of  the  leuco- 
cytes and  epithelial  cells  appeared  to  have  been  digested  in  part 
by  the  worms. 

From  the  findings  of  the  investigators  cited,  the  food  of 
many  of  the  unattached  sti'ongyles  appears  to  consist  mainly 
of  substances  derived  from  the  mucosa,  namely,  leucocytes, 
erythrocytes,  lymphocytes,  plasma,  exudates  and  desquamated 
mucosa  cells,  but  also  of  some  extra-mucosal  material  such  as 
stomach  contents. 

UNATTACHED   NEMATODES   NOT  CLOSELY   ASSOCI- 
ATED WITH  THE  MUCOSA 

Chief  among  the  parasitic  nematodes  not  closely  associated 
with  the  intestinal  mucosa  are  members  of  the  Oxyuroidea  and 
Asearidoidea.  Among  the  early  observations  of  the  food  of 
such  nematodes  were  those  of  Leuckart  (1876)  who  found  that 
the  intestine  of  Enterutiius  vermicidaris  usually  contained  yel- 
low fluid  which  on  microscopical  examination  proved  to  br 
identical  with  the  liquid  host  feces.  Similar  observations  wi'rr 
made  by  Leuckart  on  Oxyuris  equi  whose  intestinal  contents 
contained  small  particles  of  vegetable  material  identical  with 
the  contents  of  the  horse  intestine. 

Early  in  the  present  century,  Weinberg  (1907)  examined  the 
intestines  of  many  Ascaris  specimens  but  could  not  find  red 
blood  corpuscles  in  them  and  expressed  the  opinion  that  the 
horse   Parascaris   feeds   on    the   contents   of   tlie   host    intestine. 

To  ascertain  whether  Ascaris  feeds  upon  intestinal  contents, 
Vogel,  cited  by  Hoeppli  (1927),  fed  powdered  animal  charcoal 
to  a  human  patient  infected  with  Ascaris.  The  results  of  the 
first  test  were  negative,  but  in  a  second  test  carried  out  simi- 
larly, numerous  charcoal  particles  w-ere  found  in  the  intestine 
of  the  worm.  On  the  other  hand,  a  number  of  early  workers 
held  to  the  view  that  the  ascarids  are  blood  suckers.  This  view 
was  derived,  in  part,  from  microscopical  and  chemical  examina- 
tions which  showed  evidence  of  blood  in  the  intestines  of 
Ascaris  and  related  forms.  For  example,  Mueller  (1929),  on 
studying  specimens  of  Anisakis  simplex  from  the  sperm  whale 
stated  that  the  intestine,  in  all  cases,  contained  blood  in  con- 
siderable quantities  with  occasional  fragments  of  muscle  and 
other  tis.sues.  From  the  quantities  of  blood  corpuscles  pres- 
ent, Mueller  was  of  the  opinion  that  the  nematode  had  a  blood- 
sucking habit.  Mueller  was  unable  to  determine  the  nature  of 
the  intestinal  contents  of  any  other  genus  of  the  Anisakinae 
that  he  studied. 

If  such  ascarid  forms  are  blood  suckers  some  specimens 
should  be  found  in  contact  with  the  mucosa.  Hoeppli  (1927) 
reported  on  the  examination  of  350  cadavers  in  which  large 
numbers  of  ascarids  were  found.  No  evidence  was  available 
to  show  that  anv  of  these  nematodes  were  attached  to  the  mu- 


351 


cosa.  Hoeppli  further  stated  that  in  Fiilleborn  's  Laboratory  no 
cases  had  been  found  with  the  asearid,  Toxocara  canis,  attached 
to  the  dog  intestine.  Other  workers  on  examining  large  num- 
bers of  horse  intestines  at  slaughter  houses  always  found 
Parascaris  equornm  free  in  the  lumen  of  the  gut. 

Standard  textbooks  carry  the  statement  that  Ascaris  Iximhri- 
coides  feeds  on  intestinal  contents  but  gnaws  at  the  mucosa. 
This  statement  doubtless  is  due  to  the  occasional  finding  of 
reddish  spots  in  the  intestinal  epithelium  in  cases  of  asearid 
infection.  While  such  spots  occur  occasionally,  those  who  have 
examined  hundreds  of  mammalian  and  avian  intestines  which 
contained  numerous  ascarids  can  testify  that  in  the  great  ma- 
jority of  eases,  no  evidences  of  the  adult  ascarids  attaching 
the  mucosa  are  available. 

As  to  certain  Asearidoidea  being  attached  to  the  intestinal 
wall  presumably  for  feeding,  Guiart,  cited  by  Hoeppli  (1927), 
found  in  the  stomach  of  a  dolphin  the  clear  imprint  of  the 
worms'  lips  in  pit-like  depressions  of  the  mucous  membrane. 
Similar  observations  were  made  by  Hoeppli  (1927)  on  a  Con- 
tracaeciim  sp.  from  a  seal  from  northern  waters.  It  is  quite 
possible  that  instead  of  being  attached,  the  dying  worms 
pressed  their  anterior  ends  deeply  into  the  mucous  membrane 
of  the  dead  host. 

As  to  the  food  of  ascarids,  Archer  and  Peterson  (1930),  by 
giving  patients  infected  with  Ascaris  liiinbricoides  a  barium- 
cereal-meal,  found  that  the  enteric  canals  of  the  parasites 
showed  string  like  shadows,  indicating  that  the  nematodes  in 
the  host  intestine  had  swallowed  the  barium.  These  observa- 
tions indicated  that  Ascaris  lumbricoides  feeds  on  the  intes- 
tinal contents  of  man. 

Following  this  work,  Li  (1933a)  fed  to  six  dogs,  positive  for 
ascarids,  liquid  Chinese  ink  or  powdered  charcoal  twice  a  day 
for  several  days.  While  most  of  the  tests  were  negative,  due 
presumably  to  a  vermicidal  action  of  the  charcoal,  one  dog 
gave  unquestioned  positive  evidence.  The  one  female  worm 
from  the  dog 's  intestine  definitely  showed  charcoal  and  beef 
particles  in  its  enteric  tract.  In  a  subsequent  series  of  tests, 
Li  (1933b)  fed  a  mixture  of  powdered  charcoal,  clotted  blood, 
striated  beef  muscle  and  starch  granules  to  experimental  ani- 
mals harboring  ascarids  as  follows:  Dog,  Toxocara  canis;  cat, 
Toxascaris  leonina ;  and  chicken,  Ascaridia  (/alii.  The  re- 
sults from  the  dogs  gave  no  positive  evidence ;  that  from  the 
cat  showed  that  the  worm  intestine  contained  diarcoal,  blood 
cells,  and  beef  particles.  These  findings  were  confirmed  by 
examination  of  paraffin  sections  of  the  worms.  The  results 
from  four  chickens  showed  charcoal  and  beef  particles  in  the 
intestines  of  all  worms  including  both  male  and  female  sjjeci- 
mens.  From  similar  experiments,  in  which  starch  granules 
were  substituted  for  powdered  charcoal,  all  worms  recovered 
showed  starch  granules  and  some  beef  particles. 

To  ascertain  the  nature  of  food  of  the  chicken  cecal  worm 
SeteraMs  gallinac,  Li  (1933b)  fed  infected  chickens  powdered 
charcoal  and  beef  as  l)efore.  On  examination,  most  of  the 
worms  showed  charcoal  in  the  entire  intestine.  In  further 
studies,  Li  opened  tlic  intestines  of  Ancaris  lumbricoides  from 
man  and  mounted  tlie  intestinal  contents  on  slides  for  micro- 
scopic examination.  Wliile  most  of  these  contents  could  not  be 
identified,  Li  found  in  one  specimen  two  Ascaris  eggs  and  a 
piece  of  striated  muscle.  The  results  of  Li 's  experiments 
(1933a,  1933b)  indicate  that  the  intestinal  contents  of  the  host 
constitute  part  of  the  food  of  Ascaris  lumbricoides,  Toxocara 
cauis,  Toxascaris  leonina,  of  mammals;  and  Ascaridia  galli  and 
Jleteralcis  gallinac  of  fowls. 

The  findings  of  Li  and  of  other  workers  cited,  while  showing 
tliat  certain  ascaroids  take  intestinal  contents,  do  not  pre- 
clude the  possibility  that  these  nematodes  may  also  feed  upon 
the  intestinal  epithelium.  In  a  study  of  the  food  of  the  fowl 
nematode,  Ascaridia  galli  (Schneider),  Ackert  and  Whitloek 
(1935)  deprived  chickens  infected  with  Ascaridia  galli  of  food 
by  mouth;  the  experimental  chickens  were  nourished  by  intra- 
muscular injections  of  glucose.  The  results  of  the  first  series 
of  experiments  on  141  chickens  with  worms  of  various  ages  indi- 
dated  that  little  growth  occurred  in  the  worms  after  the  host 
chickens  were  taken  off  the  regular  feed.  In  the  second  series 
in  which  96  additional  chickens  were  used,  Ackert,  Whitloek 
and  Freeman  (1940)  used  worm  infections  of  one  week's  dura- 
tion in  the  tests.  Experimental  and  control  chicks  under  com- 
parison were  of  the  same  age  and  the  developing  worms  were 
from  the  same  egg  cultures.  The  results  of  this  series  of  tests 
were  very  uniform,  namely,  that  in  the  chickens  given  only 
water  per  os  and  intramuscular  injections  of  glucose,  the  young 
Ascaridia  galli  ceased  growing  whereas  tlie  worms  in  the  regu- 
larly fed  control  chickens  made  normal  growth.  These  results 
indicate  that  the  large  nematode  of  chickens  wliose  mouth  parts 
are  very  similar  to  those  of  mammalian  ascarids,  did  not  secure 
nutriment  from  the  intestinal  epithelium  of  the  host.  These 
nematodes  may  have  fed  to  some  extent  on  duodenal  mucus 
from  the  goblet  cells  but  Ackert,  Edgar  and  Friek  (1939) 
have  shown  recently  tliat  such  mucus  ninv  contain  an  inhibitory 


growth  factor  for  young  Ascaridia  tliat  have  been  grown  in  the 
culture  media  developed  by  Ackert,  Todd  and  Tanner  (1938). 
This  last  group  of  workers  prepared  a  salt-dextrose  solution  in 
which  young  Ascaridia  galli  will  grow.  On  the  introduction  of 
mucus  from  growing  chickens  into  the  nutrient  solution,  the 
cultured  Ascaridia  ceased  growing,  whereas  the  control  worms 
in  the  nutrient  solution  continued  to  increase  in  length.  In 
the  glucose-injected  chickens,  the  duodenal  mucus,  while  con- 
taining an  inhibitory  growth  factor,  may  have  afforded  the 
Ascaridia  galli  food  sufficient  for  maintaining  life,  but  not  for 
growth. 

The  literature  cites  cases  in  which  lilood  has  been  found  in 
the  digestive  tracts  of  ascaroids.  For  example,  Mueller  (1929) 
found  blood  in  the  intestine  of  Anisahis  simplex  and  Guiart, 
cited  by  Lievre  (1934),  saw  some  Ascaris  whose  digestive  tracts 
were  full  of  blood.  On  the  other  liand,  Lievre  cited  Brumpt 
as  having  performed  numerous  autopsies  to  see  if  Ascaris 
caused  ecchj-motic  spots  on  the  mucosa.  But  Brumpt  was  un- 
able to  find  such  spots,  and  the  intestinal  contents  of  the  worms 
showed  only  chyme,  never  blood. 

Indirect  evidence  of  blood  as  a  nutrient  of  ascarids  is  avail- 
able from  the  finding  of  haemoglobin  in  the  worms'  bodies  by 
such  tests  as  the  Benzidine  blood  test  and  spectroscopic  analy- 
sis. That  the  former  is  an  unreliable  test  for  blood  has  been 
shown  recently  by  Davey  (1938).  Using  spectroscopic  analy- 
sis, Lievre  (1934)  found  traces  of  haemoglobin  in  the  intestine 
of  the  dog  asearid,  Toxocara  canis.  Even  though  the  spectro- 
scopic examination  of  blood  was  positive  in  7.')  percent  of  the 
cases,  the  quantity  of  haemoglobin  noticed  was  so  small  that 
Lievre  was  led  to  think  that  the  haemoglobin  had  come  from 
the  flesh  colored  food  of  the  animal.  Lievre,  on  macerating  the 
intestines  of  Ascaris  lumbricoides,  Parascaris  equorum  and 
Ascaris  suum  was  unable  to  find  any  haemoglobin  present  in 
these  worms  by  spectroscopic  analysis.  He  concluded  that  there 
is  no  haemophagia  in  Ascaris  and  only  in  exceptional  circum- 
stances would  there  be  ingestion  of  blood.  Davey  (1938)  dem- 
onstrated haemoglobin  in  the  dermo-muscular  tube  of  Toxocara 
canis  and  in  tissues  other  than  the  alimentary  canal  of  Ascaris. 
He  found,  further,  that  the  absorption  bands  of  the  haemoglo- 
bin in  the  tissues  had  different  positions  from  those  in  the 
blood  of  their  hosts,  indicating  that  these  nematodes  were  able 
to  synthesize  haemoglobin.  Thus  the  presence  of  haemoglobin 
in  the  tissues  of  nematodes  is  not  necessarily  evidence  tliat  tliey 
feed  on  blood. 

Further  indicative  evidence  that  ascarids  may  take  blood  is 
available  from  the  work  of  Schwartz  (1921)  who  found  that 
the  body  fluid  of  Ascaris  lumbricoides  inhibited  coagulation  of 
rabbit  blood  to  a  moderate  extent.  Extracts  of  Parascaris 
equorum  and  of  Toxocara  sp.  had  a  slight  effect  on  the  coagula- 
tion of  sheep's  blood.  Whether  or  not  this  property  of  the 
asearid  body  is  utilized  by  the  living  nematodes  is  unknown. 
It  is  conceivable  that  asearid  nematodes  living  with  hookworms 
which  are  known  to  draw  l)lood  in  excess  would  swallow  blood 
from  time  to  time.  But  as  other  writers  have  indicated,  this 
would  be  exceptional  rather  than  normal. 

In  the  light  of  our  present  knowledge,  it  appears  that  tlie 
oxyuroids  and  ascaridoids  feed  normally  on  the  intestinal  con- 
tents of  the  host  including  also  any  mucus,  desquamated  muco- 
sa cells,  and  blood  elements  that  may  be  free  in  the  lumen  of 
the  intestine. 

Nematodes  in  the   Physiological  Interior  of  the  Body 

The  nematodes  that  live  in  the  physiological  interior  of  the 
liody  are  exemplified  by  Dirofilaria,  Spirocerca  and  intra-mueo- 
sal  Strongyloides.  In  a  recent  study,  Hsii  (1938a)  was  led  to 
believe  that  Dirofilaria  immitis  feeds  exclusively  on  red  and 
white  blood  cells.  In  the  ease  of  Diplotrinena  triciispis,  Hsii 
(1938b),  after  studying  the  intestinal  contents  of  this  parasite 
of  the  crow,  concluded  that  the  worms '  food  consisted  of  the 
inflammatory  exudate  in  the  thoracic  cavity.  While  there  was 
evidence  of  blood  being  ingested,  Hsii  believed  that  it  is  not 
taken  normally.  As  the  adult  Tt'uchereria  bancrofti  normally 
lives  in  lymph  vessels  and  nodes,  it  doubtless  normally  feeds 
upon  lymphocytes  and  other  constitutents  of  lymph.  When 
such  encapsulation  as  shown  by  Faust  (1939)  occurs,  the  en- 
capsulated worm  dies,  apparently   from  lack   of  food. 

In  a  further  study  of  the  food  of  nematodes,  Hsii  (1938a) 
concluded  that  Spirocerca  lupi  feeds  on  inflammatory  cells  that 
Iiass  through  the  nodule  walls. 

Observations  on  the  food  of  another  nematode  of  this  group, 
Strongyloides  stercoralis,  were  recorded  by  Askanazy  (1900) 
who  concluded  that  the  mother  worms  in  the  intestinal  mucosa 
fed  on  chyle;  he  found  no  indication  that  they  take  blood. 
Faust  (193.5),  studying  Strongyloides  in  the  mucosa  of  the 
jejunum,  found  evidence  of  lytic  action  by  the  female  worms, 
particularly  around  the  head  of  the  worm  where  disintegration 
of  the  tissue  was  observed.  Considering  the  facts  that  the  adult 
females  spend  much  of  their  time  in  the  intestinal  mucosa  and 


352 


tliMl  Ilu'v  liiivi-  luit  ln'i'ii  (ilisiMvcd  to  take  liUiod,  it  is  iinilialilc 
that  they  feed  on  t-liylo  and  tlio  partially  disintegrated  tissues 
ill  their  tunnels. 

The  Food  of  Larval  Parasitic  Nematodes 

The  nutrition  of  the  larval  parasitic  nematodes  is  funda- 
mentally like  that  of  adult  parasitie  or  free  liviiiK  iieiuatodcs 
subject  to  the  modifications  imposed  by  the  environment  and 
the  structure  of  the  larvae  in  question.  For  example,  the  re- 
searches of  McCoy  (1<)2!)),  Lepage  (10.S3,  in37)  and  Glaser  and 
StoU  (lil.'iiS)  on  "the  free-living  stages  of  Strongylina  have  re- 
vealed no  essential  differences  between  the  mode  of  nutrition 
of  these  immature  forms  and  that  of  the  free-living  stages  of 
Rhabdiasidae  (see  Chu,  l!)3(i)  and  Strongyloididae  (see  Faust. 
lO.Si;').  Tlie  feeding  mechanisms  (buccal  capsule  and  rhabdi- 
toid  esophagus)  and  sources  of  food  (bacteria  or  fluid  organic 
matter")  are  essentially  the  same.  The  method  of  feeding  of 
RhabdHix  as  described  by  Chitwood  and  Chitwood  (1038,  p.  7<i 
of  this  series)  is  probably  typical  of  this  group. 

Of  the  larvae  of  heteroxenous,  parasitic  nematodes  in  their 
intermediate  host,  no  complete  study  of  the  feeding  habits  is 
available.  But  their  locations  in  the  intermediate  hosts  are 
fundamentally  similar  to  those  of  various  adult  forms  in  pri- 
mary hosts.  Since  many  of  such  larvae  increase  in  size  without 
the  presence  of  reserve  food  stuff,  they  must  secure  their  niiur- 
ishment  from  their  lu>st.  From  the  foregoing  it  would  be  logi- 
cal to  conclude  that  larval  nematodes  in  secondary  hosts  feed  as 
do  adult  nematodes  in  analagous  positions  in  primary  hosts. 
Inactive  encysted  forms  are  at  such  low  levels  of  metabolic 
activit.v  in  both  types  of  host  that  simple  diffusion  is  probably 
more  than  adequate  to  maintain  the  parasite. 

The  nutrition  of  immature  nematodes  in  a  primary  host  is, 
as  far  as  known,  like  that  of  adult  nematodes  in  similar  posi 
tions  except  for  (a)  larval  nematodes  carrying  reserve  food- 
stuff and  (b)  larva!  nematodes  which  may  be  nourished  by  dif- 
fusion. For  the  rest  it  is  possible  to  find  a  larval  nematode 
feeding  habit  identical  with  each  ma.ior  type  of  adult  nematode 
method  of  feeding. 

Wetzel  (1930)  has  shown  fourth  stage  Oxyiiris  equi  to  feed 
like  adult  Strovgyliis  sp.  Ortlepp  (lfl37)  found  the  same  true 
of  larval  Gaipcria  pachysceHs.  According  to  Ackert  (1931), 
Ascaridia  ffalli  larvae  penetrate  the  mucosa  of  the  small  intes 
tine  and  feed  much  as  do  Physaloplcra  sp.  or  StronqyJoidrs  sn. 

In  a  study  of  Cooperia  curticei,  Andrews  (1939)  noted  the 
third  stage  larvae  feeding  in  the  lumen  of  the  gut.  The  fourth 
stage  larvae  of  this  parasite  had  their  anterior  ends  in  the 
crypts  of  Liebcrkiihn  and  grew  while  in  this  position  indicating 
the  same  type  of  nutrition  as  that  observed  in  the  adult 
Triehostrongylidae. 

Immature  Probstmayria  rivipara  are  found  free  in  the  gut 
tube  like  ascarids  indicating  a  similar  mode  of  nutrition.  Ac- 
cording to  Ransom  (1911)  immature  Oesophapostonm  colnm- 
biaviim  feed  on  the  cheesy  material  in  the  nodule  making  their 
mode  of  nutrition  essentially  similar  to  such  forii's  as  Cnatlm- 
stoma.  Ascarid  larvae  in  the  blood  stream  ingest  and  digest 
blood  cells,  according  to  Sminiov  (193r>),  hence  resemliling  adult 
Dirofilaria.  Wetzel  (1931a)  has  reported  a  case  of  what  he 
considers  to  be  extra-intestinal  digestion  by  the  fourth  stage 
larva  of  Dermatoxys  veJtgera  which  attaches  to  the  intestinal 
mucosa  by  means  of  four  cephalic  hooks,  a  unique  attachment 
mechanism  in  nematodes. 

The  recent  development  of  culturing  techniques  for  parasitie 
nematodes  promises  more  information  regarding  their  food. 
However,  to  date  only  one  parasitie  nematode  has  been  cul- 
tured throughout  its  life  cycle.  This  is  Neopleciana  glaseri 
which  is  parasitic  in  the  .Japanese  beetle,  PopiUia  japonic'a 
(Glaser,  1932).  Attempts  to  grow  Haemonchus  contortiis  of 
sheep  by  Lapage  (1933)  and  Glaser  and  Stoll  (1938),  and 
Ascaridia  galli  of  chickens  by  Ackert,  Todd  and  Tanner  (1938) 
have  been  only  partially  successful.  Hence,  these  are  included 
with  the  discussion  of  the  nutrition  of  the  larval  forms.  No 
direct  observations  of  the  food  of  these  parasitic  nematodes 
have  been  made,  but  the  fact  that  the  nematodes  have  grown 
and  developed  in  an  artificial  environment  indicates  that  at 
least  part  of  the  environment  is  a  source  of  food.  Table  1 
lists  these  attempts  at  culturing  parasitic  nematodes. 

From  these  considerations  it  appears  that  the  food  of  lar- 
val parasitic  nematodes  may  include  bacteria,  enteric  contents, 
vascular  fluids  and  elements,  and  mucosal  cells  and  ti.ssnes. 

Digestion  in  Parasitic  Nematodes 

Most  of  the  parasitic  nematodes  are  placed  in  intimate 
contact  with  the  host 's  physiological  fluids  which  carry  nu- 
trient materials  to  its  cells.  Since  these  nutrients  are  in  their 
simplest  diffusable  form  it  might  be  assumed  that  much  of  the 
nourishment  of  parasitic  nematodes  is  derived  from  this  source 
and  that  no  true  digestion  is  required.    However,  a  number  of 


Author 

Nematode 

Glaser 

N  roplcctana 

(1932) 

glaseri 

McCoy   and 

Neopleciana 

Glaser 

glaseri 

(1936) 

McCoy   and 

Neopleciana 

Girth 

glaseri 

(1938) 

Glaser  and 

Baemonchns 

Stoll 

conlorivs 

(1938) 

Ackert, 

Ascaridia 

Todd   and 

galli 

Tanner 

(1938) 

Tahi,k  1. — Siiiiiiiiary  of  ulliiiipis  Ui  ciilliirc  iiarasilic  nematodes. 

Successful 
Degree  of  Culture  Normal 

Growth  Media  host 

Complete  Dextrose    -    veal   .lapaneso 
infusion    agar  beetle 
with  yeast 
Complete   Fomented     po    Japanese 
tato    medium        hi    \: 

Complete  Veal  infusion  &  Japanese 
preservatives        beetle 

L    a    s    t  Agar,   liver    ex-  Sheep 
part    of   tract,    sheep 
fourth  blood    and    kid- 
larval   ney  defibrinated 
stage  blood 

Me  asur    Incubating  Chicken 
able.       hens'    eggs, 
growth       starch,  dextrose, 
commercial  agar 


workers  have  demonstrated  the  existence  of  a  true  digestion  in 
phylogenetically  widely  sejiarated  parasitic  nematodes;  hence, 
it  is  probable  that  they  all  carry  on  some  form  of  digestion. 
According  to  the  location  of  the  digestive  processes,  various 
workers  have  distinguished  between  an  intestinal  and  extra- 
intestinal digestion.  Much  of  the  evidence  of  extra-intestinal 
digestion  rests  upon  the  occurrence  of  necrotic  or  cytolyzed  ma- 
terial around  the  anterior  attached  end  or  within  the  buccal 
capsule  of  parasitic  worms.  That  such  .-i  i  (i"fl>iiiM  of  the  host 
tissue  is  so  often  interpreted  as  extra-intestinal  digestion  is 
somewhat  questionable  since  the  effect  of  parasite  excretions, 
simple  trauma,  mechanical  pressure,  and  heterophilogenous 
proteolytic  enzymes  upon  the  host  tissue  would  produce  many 
of  the  conditions  described  as  extra-intestinal  digestion.  This 
form  of  digestion  may  be  possible  in  some  nematodes,  how- 
ever, since  Hoeppli  (1927)  has  discovered  an  epitheliolytic  ma- 
terial present  in  the  anterior  end  but  not  in  the  posterior  por- 
tion of  Stroiigyhis. 

The  intestinal  digestion  in  nematod"s  has  been  th?  sub.ject 
of  work  by  a  considerable  number  of  investigators.  Most  of 
the  studies  have  been  confined  to  the  demonstrations  of  en- 
zymes within  extracts  of  the  parasites.  Because  of  the  early 
workers'  limited  knowledge  of  enzyme  action,  much  of  their 
results  need  confirmation  before  they  can  be  accepted.  Flury 
(1912),  for  example,  made  no  attempt  to  crifically  evaluate 
the  research  of  other  workers.  He  simply  listed  the  worker's 
name  and  the  enzymes  which  he  reported.  In  little  of  this 
early  work  was  the  action  of  bacterial  enzymes  adequately 
controlled.  The  demonstration  of  a  peptolytic  enzyme  in  the 
gut  of  Toxocara  caiiis  by  Abderhalden  and  Heise  (1909)  is 
questionable  for  this  reason.  Nor  was  any  particular  attempt 
made  in  the  early  work  to  differentiate  between  intracellular 
and  extracellular  enzymes.  Most  of  it  was  done  with  extracts 
of  the  parasite  being  studied,  and  peroxidases  and  proteases 
were  reported  as  though  the  question  of  their  respective  origins 
was  of  little  importance. 

Recent  researches  have  been  more  accurate.  Enigk  (1938) 
showed  that  Graphidium  strigosnm  produces  an  amylase  and  a 
protease  which  are  active  in  the  gut  tube  of  the  parasite.  He 
was  unable  to  demonstrate  a  lipase.  Chitwood  (1938)  demon- 
strated in  an  extract  of  the  esophagus  of  Asearis  lumiricoides, 
a  proteolytic  enzyme  which  was  inactive  at  its  isoelectric  point 
(ph  8.0)  and  most  active  in  a  weak  acid  solution.  The  fact 
that  such  workers  as  Wetzel  (1928)  and  Hoeppli  and  his  co- 
workers have  demonstrated  digested  epithelial  cells  within  the 
alimentary  tracts  of  certain  parasitic  nematodes,  gives  evidence 
of  the  existence  of  ,jroteoIytie  enzymes  in  parasitie  nematodes. 
Enigk 's  (1938)  finding  of  a  varying  reaction  in  the  gut  tube 
of  Graphidium  strigosiim  (pH  7.0  at  the  ends  and  4.4-4.8  in 
the  middle),  and  Van  Someren's  (1939)  report  of  an  acid  re- 
action in  the  intestine  and  rectum  of  Trichinella  spiralis  are 
additional  confirmation  of  the  presence  of  enzymes  because  al- 
teration of  the  reaction  of  the  digestive  tract  of  animals  is 
universally  coordinated  w^ith  the  optimum  pH  for  the  enzymes 
present. 

Anticoagulants  in  blood  sucking  nematodes  have  been  dem- 
onstrated by  a  number  of  workers.  While  such  products  are 
not  primarily  digestive,  they  doubtless  prevent  blocking  of 
the  parasite's  alimentary  tract  with  clotted  blood;  hence,  they 
are  an  aid  to  digestion.  Such  products  have  been  reported  by 
Schwartz  (1921)  and  Hoeppli  and  Feng  (1933). 

Careful  consideration  of  the  relative  values  of  the  researches 
demonstrating  the  presence  of  enzymes  leads  to  the  conclusion 
that  at  least  one  and  probably  more  proteolytic   enzymes  are 


353 


present  in  the  intestine  of  many  parasitic  nematodes  as  well 
as  at  least  one  amylytie  enzyme.  Demonstrations  of  lipases 
have  been  impossible  or  questionable.  Although  little  research 
has  been  done  on  digestion  in  parasitic  nematodes,  the  demon- 
stration of  these  enzymes  lends  weight  to  the  hypothesis  that 
digestion  in  parasitic  nematodes  is  essentially  like  that  of  other 
animals  possessing  a  digestive  tract. 

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355 


CHAPTER  XI 
CHEMICAL  COMPOSITION  AND  METABOLISM  OF  NEMATODE  PARASITES  OF  VERTEBRATES, 

AND  THE  CHEMISTRY  OF  THEIR  ENVIRONMENT 

THEODOR  VON  BRAND,  Department  of  Biology,  Catholic  University  of  America  and 
THEODORE  LOUIS  JAHN,  Department  of  Zoology,  State  University  of  Iowa 


The  metabolic  procLSses  of  nematode  parasites  comprise  a 
subject  which  has  l)een  under  investigation  for  many  years. 
Progress  in  the  field,  however,  has  been  particularly  rapid  dur- 
ing the  last  decade,  and  it  is  the  purpose  of  the  present  au- 
thors to  present  a  summary  of  the  known  facts  of  metabolism 
together  with  the  related  subjects  of  the  chemistry  of  the  worms 
and  of  their  environment.  Recent  reviews  which  deal  with 
some  of  the  subject  matter  here  presented  are  those  of  Slater 
(1928),  McCoy  (1935),  Lapage  (1S3S)  and  v.  Brand  (1934, 
1938). 

Peculiarities  of  Environment  Which  May  Influence 
Metabolism 

The  wide  differences  in  the  habitats  of  the  various  nematode 
parasites  of  vertebrates  are  undoubtedly  correlated  with  wide 
differences  in  metabolic  processes.  The  organisms  which  live  in 
the  digestive  tract,  blood  stream,  lungs,  kidneys,  subcutaneous 
tissue,  etc.,  are  subject  to  quite  a  variety  of  environmental 
conditions.  In  those  cases  where  open  contact  with  the  blood 
stream  or  lymph  is  maintained  the  parasites  are,  of  course, 
subjected  to  an  environment  very  similar  to  that  of  the  cells  of 
the  host  body.  Whenever  a  nematode  is  surrounded  by  a  cyst 
wall  which  reduces  the  availability  of  oxygen,  or  is  located  in 
a  region  deprived  of  free  blood  circulation,  metabolic  jirocesses 
are  probably  different  from  the  processes  in  those  species  which 
live  in  the  blood  stream.  Species  that  live  in  the  digestive  tract 
have  an  environment  which  is  peculiar  in  many  respects.  The 
chemistry  of  blood  is  adequately  described  elsewhere,  and  the 
chemical  environment  within  cysts  and  in  chemically  isolated 
tissues  is  practically  unknown  (except  for  cestode  cysts,  Schop- 
fer,  1932).  Therefore,  the  present  discussion  of  environment 
is  limited  to  the  chemistry  of  the  digestive  tract. 

From  the  viewpoint  of  nematology  the  chemistry  of  the  in- 
testinal contents  is  interesting  for  several  reasons.  A  thor- 
ough knowledge  of  the  chemistry  of  the  environment  may  allow 
a  better  understanding  of  the  physiology  of  the  intestinal 
parasites,  it  may  aid  in  the  formulation  of  culture  media  suit- 
able for  growth  in  vitru  (cf.  Glaser  and  Stoll,  1938),  and  it  may 
shed  light  on  the  problems  of  host  specificity  and  on  the  possi- 
bility that  experimental  modifications  of  intestinal  contents 
may  be  of  use  in  controlling  the  activities  of  the  nematodes. 
The  effect  on  nematodes  of  many  of  the  substances  found  in 
the  intestine  has  not  been  studied.  In  the  hope  that  the  pres- 
ent discussion  might  serve  as  a  partial  outline  of  substances  to 
be  investigated,  the  authors  have  included  a  general  discussion 
of  the  chemical  compounds  present. 

THE   SEQUENCE   OF   CHEMICAL   EVENTS   IN   THE 
DIGESTIVE  TRACT 

In  any  discussion  of  the  chemical  composition  of  the  contents 
of  the  digestive  tract  it  is  necessary  to  keep  in  mind  the  se- 
quence of  events  which  occurs  as  the  ingesta  pass  through  the 
alimentary  canal.  The  chemical  composition  of  the  contents 
of  the  gut  varies  with  diet,  with  species,  and  with  the  state  of 
health.  However,  in  any  healthy  animal  on  a  constant  diet 
there  is  a  definite  sequence  to  the  chemical  changes  which  occur. 

In  man,  the  stomach  leccives  the  mixture  of  food  and  saliva. 
To  this  is  added  mucus,  pepsin,  and  hydrochloric  acid.  The 
material  present  in  the  duodenum  is  derived  from  four  sources: 
chyme  from  the  stomach,  bile, .  pancreatic  juice,  and  succus 
entericus.  The  stomach  contents  when  emptied  into  the  duo- 
denum consist,  among  other  things,  of  proteoses  and  peptones, 
starch,  sugars,  fat  droplets,  some  fatty  acids  and  glycerol, 
hydrochloric  acid,  plant  fragments  containing  cellulose  and 
undigested  plant  tissue,  and  water. 

The  bile  contains  mucin,  the  pigments  biliverdin  and  bili- 
rubin, the  bile  salts  Na-taurocholate  and  Na  glycocholate,  cho- 
lesterol, lecithin,  fats,  soaps,  inorganic  salts  and  water.  The 
relative  amounts  of  taurocholate  and  glycocholate  vary  with 
the  species;  the  dog,  for  example,  is  entirely  lacking  in  glyco- 
cholate. The  pancreatic  secretion  contains  NasCOa  and  the 
enzymes  trypsin,  lipase,  and  amylopsin.  The  succus  entericus 
contributes  the  enzymes  erepsin,  lipase,  maltase,  invertase,  lac- 
tase, and  rennin,  and  a  large  amount  of  mucus  and  desqua- 
mated epithelial  cells.  Due  to  partial  sterilization  of  food,  or 
to  the  action  of  hydrochloric  acid  and  bile  salts,  living  bac- 
teria are  present  only  in  small  numbers  in  the  duodenum  and  in 


normal  men  may  sometimes  be  absent  (Kellogg,  1933).  As 
tliese  materials  pass  through  the  duodenum  and  jejunum  diges- 
tion is  completed,  and  tlie  products  of  digestion  and  most  of 
the  bile  salts  are  absorbed.  The  bacteria  increase  in  numbers, 
utilize  some  of  the  products  of  digestion  and  decompose  others. 
As  the  material  passes  through  the  large  intestine  water  is  ab- 
sorbed, and  calcium,  magnesium,  iron,  and  phosphates  are 
secreted  by  the  intestinal  wall. 

The  feces  of  an  animal  on  a  carnivorous  diet  are  composed 
mostly  of  the  intestinal  secretions  and  bacteria.  If  vegetables 
make  up  a  considerable  part  of  the  diet,  the  bulk  of  the  feces 
is  increased,  and  plant  fragments  appear  in  the  feces,  some- 
times with  the  contained  plant  protoplasm  only  jiartially  di- 
gested. The  large  bulk  of  undigested  cellulose  stimulates 
peristalsis,  and  consequently  causes  a  more  rapid  passage  of 
ingesta  through  the  intestine,  which  results  in  the  absorption 
of  less  water  liy  the  colon  and  a  more  liquid  feces. 

The  materials  which  are  present  in  tlie  digestive  tract  and 
which  may  affect  the  metabolism  of  nemas  are  for  convenience 
discussed  under  the  following  headings:  (1)  Composition  of 
the  intestinal  gases,  (2)  Hydrogen  ion  concentration,  (3)  Dis- 
solved materials  (exclusive  of  gases),  (4)  Antienzymes.  Nema- 
todes, esi^eeially  those  which  live  in  tissues,  are  known  to  secrete 
digestive  enzymes,  but  these  are  more  properly  discussed  under 
the  subject  of  nutrition  of  the  worms. 

COMPOSITION  OF  THE  INTESTINAL  GASES 

The  composition  of  the  gases  in  or  in  contact  with  the  in- 
gesta varies  greatly  in  different  parts  of  the  digestive  tract. 
The  gas  tension  of  the  stomach  contents  varies  at  different 
periods  following  a  meal  and  depends  on  the  amount  of  air 
ingested  with  food.  The  action  of  HCl  causes  a  release  of 
bound  COj,  most  of  which  is  probably  absorbed  either  in  the 
stomach  or  upper  intestine.  The  oxygen  ingested  with  the  food 
apparently  undergoes  a  rapid  decrease  so  that  it  is  almost  ab- 
sent from  the  intestine  below  the  duodenum.  The  analyses  of 
von  Brand  and  Weise  (1932)  show  that  very  little  oxygen  is 
introduced  into  the  intestine  by  the  bile.  These  investigators 
also  studied  the  oxygen  content  of  fluid  intestinal  matter  and 
of  intestinal  gases.  They  found  that  the  oxygen  content  of  the 
fluid  of  both  the  large  and  small  intestines  of  almost  all  ani- 
mals examined  was  practically  nil.  The  only  exception  was 
one  pig  which  contained  quite  appreciable  amounts  of  oxygen. 
This  might  have  been  caused  by  the  swallowing  of  large 
amounts  of  air,  perhaps  at  the  time  of  slaughtering.  The 
values  for  all  animals  except  the  pig  correspond  to  about  -5 
percent  saturation.  The  data  of  several  investigators  on  the 
oxygen  content  of  intestinal  fluids  and  gases  are  summarized 
in  Tables  13  and  14.  The  data  in  Table  14  demonstrate  the  ab- 
sence of  oxygen  in  the  gaseous  content  of  the  intestine  of  all 
animals  except  the  pig.  Long  and  Fenger  (1917)  found  that 
oxygen  was  present  in  appreciable  quantities  in  the  in- 
testinal gases  of  the  pig,  and  this  was  confirmed  by  v.  Brand 
and  Weise.  It  has  been  assumed  by  Slater  (1925)  that  the 
intestinal  walls  give  off  oxygen  to  the  intestinal  contents  during 
digestion.  This  has  not  been  proved  experimentally,  and  Long 
and  Fenger  (1917)  found  that  the  oxygen  content  was  lowest 
during  active  digestion.  It  seems  probable  (as  indicated  by 
the  data  of  Mclver,  Redfield,  and  Benedict,  1926)  that  oxygen 
may  diffuse  inward  from  the  intestinal  wall,  but  it  is  also  very 
likely  that  the  bacteria  present  near  the  wall  would  consume 
this  immediately  so  that  very  little  oxygen  from  this  source 
would  ever  reach  the  central  portion  of  the  lumen.  The  avail- 
able evidence  indicates  that  the  environment  of  intestinal  hel- 
minths is  not  devoid  of  oxygen  but  contains  oxygen  in  only 
small  quantities.  Worms  which  live  close  to  the  intestinal  wall 
may  have  access  to  larger  amounts.  In  the  case  of  the  hook- 
worm it  is  apparent  from  the  observations  of  Wells  (1931)  that 
the  blood  sucking  activities  represent  largely  a  respiratory 
function. 

Analyses  of  intestinal  gases  other  than  O:  are  not  numerous. 
The  intestinal  gases  of  man  vary  with  diet.  Ruge  (1861)  gives 
the  following  data  for  percentage  composition: 

Diet  CO.             H=  CH.           N= 

Vegetables  21-34  1.5-4.0  44-55  10.19 

Meat  813  0.7-3.0  26-37  45-64 

Milk --  916          43-54  0.9  36-38 


356 


Tlio  (lata  of  Fries  (liHUi)  slmw  tliat  tlif  gasos  of  man  iiu  a 
mixed  diet  are  similar  to  tliose  given  above  for  a  meat  diet. 
Further  analyses  are  given  hj  Baseli  (190S).  The  absorption 
of  intestinal  gases  is  diseiissid  liy  Melver,  Redfield,  and  Bene 
diet  (192(i),  and  the  subjeet  of  human  gastro  intestinal  gases 
is  reviewed  bv  Ziegler  and  Ilirseh  U!l2r))  and  Lloyd-Jones  aiiil 
Liljedahl   (l!t"34). 

The  intestinal  gases  of  the  dog  were  analyzed  by  Planer 
(ISlilO.  His  analyses  demonstrated  large  amounts  of  CO2  and 
N;,  and  a  smaller  amount  of  Hi;  througluiut  the  digestive  traet, 
a  small  amount  of  0»  in  the  snuill  intestine,  and  a  small  amount 
of  HaS  in  the  large  intestine  when  the  dog  was  on  bread  or 
meat  diets.  On  a  vegetable  diet  11=  largely  replaced  the  N-, 
while  O2  and  "US  were  absent.  In  these  analyses  methane  is 
conspicuously  absent. 

The  intestinal  gases  of  various  herl)ivores  have  been  ana- 
lyzed by  Tappeiner  (18S3),  and  the  literature  is  summarized 
by  Scheunert  and  Sehieblich  (1!127).  The  data  of  Tappeiner 
(1883)  on  the  percentage  composition  of  the  gases  in  cattle, 
sheep,  and  goats  (all  of  which  were  quite  similar)  are  as 
follows : 


Table  13. — Oxygen  Content  of  Fluid  Intestinal  Maxxi 


COa 
Os   - 

CH. 

Ha 


Rumen 

65 

.5 

30 
0.6-4.7 

1-40 


Small  Intestine 
62-92 

0 

.04-6.6 

0-37 

1 


Caecum 

and  Colon 

about  30 

0 

38.r)3 

2-6 

23-34 


Data  for  the  horse  (Tappeiner,  1883)  are: 

Small  Caecum 

Stomach  Intestine  and  Colon  Eectum 

COi. 75  15-43  55-85  29 

Os    0  0.57-76  0.14  0 

CHi 0  0  11-33  57 

H2 14  20-24  1.7-2.2  0.8 

Na   10  37-60  .9-10.0  13 

I>ata  for  the  rabbit  (Tappeiner,  1883)  are: 

Caecum 

Stomach  Small  Intestine  and  Colon 

CO2 32  75  6 

O2 0  0  0.6 

CH. 0  2  21.0 

Hj 0  18  0.6 

N2    ._             68  6  72 

Long  and  Fenger  (1917)  found  a  large  amount  of  N2  (74 — 
92'/i )  somewhat  less  CO2  (o — 28%),  and  about  5  percent  Os, 
but   no  methane  or  H2  present   in  the  small   intestine  of   hogs. 

The  production  ot  methane  is  probably  caused  mostly  by  bac- 
terial decomposition  of  cellulose,  althougli  the  data  of  Ruge 
indicate  that  it  can  also  be  produced  b.v  bacterial  action  when 
the  animal  is  on  a  meat  diet.  The  analyses  of  Tappeiner  and 
others  also  indicate  the  presence  of  H2S  in  some  cases.  H-S 
and  Xa  must  be  formed  by  the  action  of  bacteria  on  protein. 
Ammonia  is  also  formed  by  bacterial  decomposition  of  protein, 
Ijut  it  is  usually  bound  by  the  acids  of  the  intestine.  Most  of 
the  CO2  is  probably  of  bacterial  origin,  although  in  the  duo 
denum  it  may  also  be  formed  by  the  NaX'Oa  of  the  pancreatic 
juice  and  the  acid  of  the  chyme.  The  NH.,  and  the  CO2  of  the 
succus  entericus  are  discussed  by  Herrin  (1937).  Most  of  the 
intestinal  gases  are  eliminated  from  the  body  by  the  lungs. 
Tacke  (1H84)  found  that  10  to  20  times  as  much  of  the  in- 
testinal gases  of  rabbits  escape  by  means  cjf  the  blood  and 
lungs  as  by  way  of  the  anus. 

The  effect  of  the  gases  other  than  o-xygcn  on  intestinal  nema- 
todes is  entirely  unknown.  Methane,  H^,  and  N2  are  probably 
without  either  beneficial  or  harmful  effects.  The  utilization  of 
o.xygen  will  be  discussed  in  the  part  dealing  with  metabolism  of 
adult  nematodes.  The  effect  of  CO2  is  unknown.  Since  it  is 
incapable  of  further  oxidation  and  since  there  is  no  evidence 
of  chemosynthesis  in  the  nematodes,  the  only  apparent  effect 
it  could  have  would  be  the  ad,justment  of  intracellular  pH. 
Since  intestinal  nematodes  live  in  a  medium  usually  saturated 
with  CO2  it  is  conceivable  that  they  may  depend  on  this  sub- 
stance as  an  intracellular  buffer.  Therefore,  it  may  become 
important  to  maintain  a  high  CO2  content  in  in  vitro  cultures 
(Cf.  possible  role  in  growth  of  intestinal  protozoa,  Jahn,  1934, 
1936).  It  should  be  noted  that  Weinland  (1901)  found  that 
Ancarif:  survived  longer  in  vitro  when  the  medium  was  satu- 
rated with  ('Oj. 


Part  of 
.\nimal       intestine 


Oxygen  in    Number 
volume  per-    of 
cent  mean    deter- 
and  (      )     mina- 
extremes     tions 


Horse     Sm.  intestine    0.024 

(0.016  0.031) 
Dog. ...  Sm.  intestine    0.028 
Cattle    Sm.  intestine    0.013 

(0.00  0.02.-,) 
Sheep     Sm.  intestine    0.012 

(0.00  0.025) 
Pig  ....  Sm.  intestine    0.083 

(0.00-0.35,s) 
Cattle     Lg.  intestine    0.010 

(0.00  0.023) 
Pig    -.    Lg.  intestine    0,00 


Investigator 


2  Toryu   (1934) 

1  V.  Brand  &  Weise  (1932) 

2  V.  Brand  &  Weise  (1932) 

4  V,  Brand  &  Weise  (1932) 

(i  V.  Brand  &  Weise  (1932) 

3  V.  Brand  &  Weise  (1932) 
1  V.  Brand  &  Weise  (1932) 


Table  14. — Oxygen  Cont 

Oxygen  in 

volume  per 

cent  mean 

Part  of  and  (     ) 

Animal      intestine         extremes 

Horse. .-Sm. intestine    0.67 

(0.57-0.76) 
Cattle..-Sm.  intestine    0.00 
Cattle  -Sm. intestine    * 

Goat- Sm.  intestine    * 

Sheep-...Sm.  intestine    * 
Pig -Sm.  intestine    5.5 

(1.2  14.2) 
Pig Sm.  intestine    4.2 

(0.4-8.2) 
Dog Sm.  intestine    0.2 

(0.0-0.7) 
Horse.- Lg.  intestine    0.07 

(0.000.14) 
Cattle....Lg.  intestine    0.00 
Goat Lg.  intestine    0.03 

(0.00-0.07) 
Sheep-— Lg.  intestine    0.00 
Rabbit -Lg.  intestine    0.62 
Dog      -Lg.  intestine    0.00 

*Not  enough  gas  for  analysis. 


ent  of  Intestinal  Gases 


iS' umber 

of 
deter- 
mina- 
tions Investigator 


3  Tappeiner   (1883) 

1  Tappeiner   (1883) 

*  V.  Brand  &  Weise  (1932) 
»  Tappeiner  (1883) 

*  V.  Brand  &  Weise  (1932; 
9  Long  &  Fenger  (1917) 

6  V.  Brand  &  Weise  (1932) 

8  Planer  (1860) 

4  Tappeiner    (1883) 

1  Tappeiner   (1883) 

3  Tappeiner   (1883) 

1  Tappeiner   (1883) 

1  Tappeiner    (1883) 

6  Planer  (1860) 


HYDROGEN  ION  CONCENTRATION 

The  pH  of  the  stomach  and  intestine  has  been  measured  for 
a  large  number  of  animals,  and  some  of  the  representative  data 
ai'e  listed  in  Tables  ]."j  and  16.  Contents  of  the  stomach  of  car- 
nivores, omnivores,  and  herbivores  with  a  simple  stomach,  and 
of  the  abomasum  of  ruminants  are  distinctly  acid  in  character 
due  to  the  secretion  of  hydrochloric  acid.  The  rumen  and  oma- 
sum vary  from  neutral  to  distinctly  alkaline.  The  pH  of  the 
duodenum  is  extrenu^ly  variable  but  is  usually  acid  because  of 
the  introduction  of  HCI  from  the  stomach.  The  pH  of  the  re 
mainder  of  the  small  intestine  is  less  acid  than  the  duodenum, 
and  there  is  usually  a  progressive  rise  toward  neutrality  or  to 
a  slight  alkalinity;  the  pH  seldom  reaches  a  value  higher  than 
8.0  or  8.2.  The  colon  and  caecum  of  most  animals  are  neutral, 
slightl.y  acid,  or  slightly  alkaline.  Some  of  the  recent  litera- 
ture is  reviewed  by   Lenkeit   (1933). 

The  pH  of  the  intestine  may  be  lowered  b.v  the  administra- 
tion of  large  quantities  of  lactose,  especially  if  the  diet  is 
low  in  protein.  Robinson  and  Duncan  (1931)  found  that  the 
pH  of  the  rat  intestine  could  be  lowered  about  one  pH  unit  by 
the  administration  of  25  percent  lactose  with  a  low  protein 
diet  (other  literature  is  cited  by  these  authors).  In  man  it  is 
known  that  the  acidity  of  the  intestine  may  be  considerably 
decreased  if  large  amounts  of  lactose  accompanied  by  Lacto- 
bacilltis  aeidophiltis  are  ingested  (literature  cited  by  Kopeloff, 
1926,  and  Frost  and  Hankinson,  1931).  Comparable  results 
have  been  obtained  with  the  domestic  fowl  (Ashcraft,  1933). 
The  direct  addition  of  mineral  salts  such  as  NaCl,  MgSO<,  CaCU, 
Ca(0H)2,  CaSO.,  NaHCO:,,  and  NH.Cl  to  the  diet  may  have  no 
effect  on  pH  in  experimental  animals  (McClendon  et  al,  1919; 
Heller,  Owens,  and  Portwood,  1935 ;  Mussehl,  Blish,  and  Ack- 
erson,  1933).  However,  positive  results  with  mineral  salts  have 
been  obtained  by  Robinson  (1922),  Shohl  and  Bing  (1928)  and 
others.  A  deficiency  of  vitamin  D  is  also  known  to  cause  tlie 
intestinal  contents  to  become  alkaline  due  to  lack  of  Ca  ab- 
sorption  (Zucker  and  Matzner,  1923;  Jephcott  and  Bacharach, 


357 


Table  15. — The  pH  of  Stomach  Contents 


Animal 


pH 


Author 


Man      minimum  pH 

1.0  to  2..5 
Eat  _. 3.2-4.6 


Eat  

_1.8-5.6  (av.  3.6) 

Bat  

.,3.3-3.9 

Horse       - - 

1.13-6.8   (507c 

between  1.1 

and  3.3) 

Rabbit    

..1.8 

Cat 

_3.34 

Dog  . — 

_1.5-2.0 

Dog -  

..2.0-6.0 

Dog 

_1.37-5.7 

(av.  3.47) 

Chick,  gizzard  - 

..3.39 

Cliiclf.  gizzard 

.2.9-3.2 

Chicken 

proventriculus 

.5.9 

Chicken 

proventriculus 

.4.8-5.7 

Cattle 

abomasum 

..2.0-4.1 

Cattle 

abomasum 

.3.8 

Sheep 

abomasum 

..3.15-0.25 

(av.  4.0) 

Cattle  rumen  „ 

..8.89  (8.61-9.68) 

Cattle  rumen --. 

..7.5-8.0 

Sheep  rumen. ... 

..7.0-7.6 

McClendon  and  Medes  (1925) 
Kahn  and  Stokes  (1926) 
Sun,  Blumenthal,  Slifer,  Ber- 
ber and  Wang   (1932) 
Eastman  and  Miller  (1935) 
Kofoid,  McNeil  and  Cailleau 

(1932) 
Schwarz,  Steinmetzer,  and 
Caithaml  (1926) 

McLaughlin  (1931) 
McLaughlin   (1931) 
Maun  and  Bollman  (1930) 
Schwarz  and  Danziger  (1924) 
Nagl  (1928) 

McLaughlin   (1931) 
Ashcraft  (1933) 

McLaughlin  (1931) 

Ashcraft  (1933) 

Schwarz  and  Kaplan  (1926) 

Mangold  (1925) 

Davey   (1938) 

Schwarz  and  Gabriel  (1926) 
Kreipe  (1927) 
Ferber  (1928) 


1926;  Redman,  Willimott,  and  Wokcs,  1927).  The  pH  may  be 
appreciably  lowered  by  addition  of  cod  liver  oil  to  a  rachito- 
genic  diet.  The  effect  of  varying  the  proportions  of  protein, 
fat,  and  carbohydrate  has  been  reported  to  cause  no  marked 
change  in  the  pH  of  the  intestine  of  rats  (Redman,  Willimott 
and  Wokes,  1927),  dogs  (Grayzel  and  Miller,  1928;  Graham  and 
Emery,  1928),  or  man  (Hume,  Denis,  Silverman,  and  Irwin, 
1924).  However,  the  data  of  Robinson  and  Duncan  (1931) 
show  consistently  higher  pH  values  for  rats  fed  on  grain  and 
alfalfa  than  for  rats  on  a  high  protein  diet  (Table  16).  East 
man  and  Miller  (1935)  studied  the  effect  of  a  number  of  diets 
on  gastrointestinal  pH  in  rats. 

It  has  been  suspected  for  some  time  that  the  pH  of  the  cen- 
tral portion  of  the  lumen  is  not  the  same  as  that  close  to  the 
intestinal  wall.    Evidence  for  this  is  found  in  the  feces  in  that 


the  surface  of  stools  is  more  alkaline,  apparently  because  of 
secretion  of  alkaline  salts  by  the  intestinal  wall.  Kofoid,  Mc- 
Neil, and  Cailleau  (1932)  reported  ditterences  in  the  pH  of 
contents  and  wall  throughout  the  digestive  tract  of  the  rat.  (Ta- 
ble 16).  Robinson  (1935)  studied  the  effect  of  placing  various 
salt  solutions  in  the  small  intestine  of  dogs  on  the  pH  of  the 
solution  and  decided  that  each  portion  of  the  digestive  tract 
tended  to  produce  a  characteristic  pH  value  in  the  solution,  re- 
gardless of  the  initial  pH.  He  concluded  that  the  pH  of  the 
region  close  to  the  wall  increases  regularly  from  pH  6.5  to  7.5 
or  8.0  throughout  the  length  of  the  small  intestine  and  pointed 
out  that  the  pH  close  to  the  wall  is  probably  largely  indepen- 
dent of  changes  produced  in  the  lumen  by  the  action  of  bac- 
teria. Ball  (1939),  by  means  of  a  capillary  glass  electrode,  has 
measured  the  pH  of  the  wall  (data  given  in  Table  16). 

The  possibility  that  pH  may  be  a  limiting  factor  in  the  dis- 
tribution of  sheep  nematodes  was  investigated  by  Davej'  (1938). 
He  found  that  Ostertagia  circumcincta  was  able  to  live  between 
pH  3.2  and  pH  9.0.  This  range  allows  it  to  live  in  the  aboma- 
sum of  sheep  (pH  3.2-5.25)  but  apparently  may  be  one  rea- 
son why  it  does  not  infest  the  stomach  of  the  dog  (pH  2  or 
less)  or  horse  (pH  1.1-6.8)  or  the  abomasum  of  cattle  (pH 
2.0  to  4.1).  Two  duodenal  species  from  sheep,  Trichostrongylus 
cohibriformis  and  T.  vitrii-s.  were  alilc  to  stand  a  continuous 
acidity  as  low  as  pH  3.6,  but  five  other  species  {Nematodirus 
fiUcoUis,  N.  spathiger,  Cooperia  oncophora,  Cooperia  curticei, 
Strongyloides  papillosus)  from  the  middle  and  lower  small  in- 
testine were  killed  at  acidities  of  pH  3.9  to  4.6.  Since  the  duo- 
denum is  more  acid  than  the  ileum,  the  low  resistance  to  acidity 
may  be  an  important  factor  in  preventing  the  five  species  from 
the  middle  and  lower  intestine  from  infesting  the  duodenum. 
It  has  been  suggested  by  Lapage  (1935a,  1938)  that  pH  has  an 
influence  on  the  second  ecdysis  of  triehostrongylid  larvae  (out- 
side of  the  host)  and  that  this  may  be  of  importance  in  allow- 
ing development  of  the  parasite.  The  third  ecdysis  (in  the 
intestine)  might  be  similarly  affected. 

It  seems  possible  that  the  presence  of  nemas  in  the  digestive 
tract  might  cause  a  change  in  gastrointestinal  pH,  either 
directly  (perhaps  because  of  lesions  in  the  epithelium)  or  in- 
directly through  the  systemic  reactions  of  the  host.  In  cases 
of  ancylostomiasis  and  intestinal  schistosomiasis  Eldin  and 
Hassan  (1933)  found  evidence  of  gastric  disturbance  which 
disappeared  after  removal  of  the  worms.  Fernandez  (1934), 
however,  found  no  correlation  between  gastric  acidity  and  hel- 
minth parasites. 

DISSOLVED   SUBSTANCES    (EXCLUSIVE  OF  GASES) 

The  dissolved  materials  of  the  digestive  tract  consist  of  the 
ingesta  and  various  secretions  listed  above,  the  products  of 
digestion,  and  the  products  of  bacterial  decomposition.  Many 
of  these,  especially  the  carbohydrates,  may  serve  as  food  for 
nematodes;  many  others  may  be  toxic  and  may  be  effective  in 


Table  16. — The  pH  of  the  digest ive  tract  contents. 


Animal  and  Diet  Duodenum    Jejunum 


Ileum 


Caecum 


Colon 


Investigator 


Man  

Man  _ 

Man  

Dog   . — 

Dog   

Dog  - — 
Dog  — 
Cat  


2.27-7.8 
4.7  -6.5 


4.5 
2.0 
6.2 
5.9 


-5.1 
-7.6 
-6.5 


Rat 

Eat — grain  &  alfalfa 

Rat — high  protein 

Eat — high  base 

Rat 


Eat — lumen  of  gut . 
Rat — wall  of  gut... 

Rat — wall  of  gut 

Rabbit  

Cattle 

Cattle 

Horse  


6.5 

6.5 

6.75^ 

6.4> 

6.4^ 

5  gi 

(4.2  -6.9) 

6.93 
6.34 
7.35 
6.68 


7.0 

7.0-7.6 
6.0-7.0 
6.0-6.27 


to 

7.7' 
6.8' 
6.8' 
6.6' 
(5.0-7.3) 


8.42 


6.1-7.3 
5.9-6.5 

6.0-8.0 
6.0-7.0 
6.36 

6.8 
7.2 
8.2' 
7.3' 
7.25' 
6.9' 

(5.6-7.7) 
7.13 
7.34 
6.89 
8.0 
8.2 


Hogs,  calves,  lambs .. 

Fowl 

Fowl — meat  scrap 

Fowl h  20%  lactose 


6.72  ....  7.09 

Indefinitely  variable  6.48  to  7.76. 
More  often  acid  than  alk. 
6.3  _.  6.22 

5.96  ._  7.1 

6.51  .._  7.16 


6.0-6.5 
6.57 


6.5-7.2 
7.0 
7.3 
7.0 
6.4 

(5.1-7.4) 
7.13 
7.34 
7.06 
6.26 
8.2 

8712 


7.4 

6.84 
7.6  ■ 
5.25 
6.4  ■ 
7.2 
7.2 
7.2 
6.6 
(5.4  ■ 
7.33 
6.95 
6.91 


7.4-8.4 


8.4 
6.6 

7.5) 


Long  and  Fenger  (1917) 

Karr  and  Abbott  (1935) 

McClendon  (1920) 

Mann  and  Bollman   (1930) 

Graham  and  Emerv   (1927-28) 

Grayzel  and  Miller  (1928) 

Heupke  (1931) 

McLaughlin  (1931) 

Sun,  Blumenthal,  Slifer,  Herber,  and  Wang  ( 1932 ) 

Robinson  and  Duncan  (1931) 

Robinson  and  Duncan  (1931) 

Robinson  and  Duncan  (1931) 

Eastman  and  Miller  (1935) 

Kofoid,  McNeil,  and  Cailleau   (1932) 

Kofoid,  McNeil,  and  Cailleau   (1932) 

Ball  (1939) 

McLaughlin   (1931) 

Danniger,  Pfragner,  and  Sehultes  (1928) 

Heupke  (1931) 

Danniger,  Pfragner,  and  Sehultes  (1928) 

Long  and  Fenger  (1917) 


1.9= 

McLaughlin  (1931) 

7.0 

7.2 

Ashcraft  (1933) 

5.1 

6.3 

Ashcraft  (1933) 

'Intestine  divided  into  three  approx.  equal  portions  so  that  the  measurements  given  may  not  correspond  exactly  to  those 
of  the  duodenum,  jejunum,  and  ileum. 

"Possibly  a  misprint  in  the  original  paper. 


358 


causing  the  localization  of  iKMuatodos  in  ccitain  portions  of  the 
(ligestivo  tract. 

The  possibility  that  bile  salts  may  affect  the  growth  of  in- 
testinal parasites  has  been  recognized  for  some  time.  Accord- 
ing to  Moorthy  (l!t3."))  fresh  bile  from  certain  si)ecies  of  Barbiis 
and  from  sheep  and  man  is  capable  of  killing  Ci/clops  and  of 
activating  the  enclosed  larvae  of  linu-iinciihis  mrilini  iisix  to  es- 
cape. De  Waele  (liHU)  claimed  that  the  eestode,  Taenia  kyda- 
tigena  {Cysticcrcun  pixiformis),  is  able  to  infest  dogs  because 
of  the  absence  of  Na-glycocholate  in  dog  bile  and  that  since 
Na  glycocholate  is  toxic  to  the  organism  it  can  not  develo]i  in 
animals  which  secrete  this  substance. 

Davoy  (1938)  has  investigated  the  effect  of  bile  salts  ou 
sheep  nematodes.  He  found  that  the  species  which  infest  the 
duodenum  (Trichostrongylii.s  colubriformis  and  T.  vilriiius)  of 
sheep  were  much  more  resistant  to  Na-tauroeholate  and  Na-gly- 
cocholate than  other  species  {Ncmatodirim  fillicoUis,  A',  spathi- 
ger,  Coopcria  oncaphora,  Coupcria  curticci,  and  Ostcrtngia  cir- 
cumcxncta)  from  the  lower  small  intestine  and  abomasum. 
Cooperia  curticci,  which  lives  closer  to  the  opening  of  the  bile 
duct  than  the  other  species  except  Tricliostrongj/lus  colubrifor- 
mis and  T.  vitrinus,  has  a  resistance  second  only  to  Tricho- 
Ktrongylus.  Since  the  bile  salts  are  introduced  by  the  bile  duct 
and  are  largely  reabsorbed  in  the  snuill  intestine,  the  concen- 
tration of  bile  salts  decreases  along  the  intestine.  The  high 
concentration  in  the  upper  small  intestine  probably  prevents 
species  other  than  Tricliostrongylus  from  living  in  that  region. 
In  these  experiments  glj'cocholate  seemed  to  be  somewhat  more 
toxic  to  Trichostrongylus  than  tauroeholate.  Davey  mentioned 
the  possibility  that  difi'erential  susceptibility  to  the  two  bile 
salts  might  be  a  factor  in  the  determination  of  host  specificity. 

The  products  of  bacterial  decomposition  are  of  several  types: 

1.  Products  of  carbohydrate  decomposition  from: 

a.  Hydrolysis  of  cellulose  to  glucose  in  the  rumen  and 
large  intestine  of  herbivores. 

b.  Fermentation  of  simple  sugars  to  lower  fatty  acids  in 
the  small  and  large  intestine  of  all  vertebrates  and  in 
the  rumen  of  ruminants. 

2.  Products  of  protein  decomposition  from: 

a.  Hydrolysis  of  proteins  to  amino  acids  in  the  upper 
small  intestine. 

b.  Fermentation  of  amino  acids  to  aporrhegmas  and  to 
lower  products  in  the  lower  small  intestine  and  large 
intestine  of  animals  with  simple  stomachs  and  in  the 
rumeu  of  ruminants.  Some  of  the  products  of  fermen- 
tation are  indol,  skatol,  paraeresol,  phenol,  volatile  fatty 
acids,  H=S,  histamine,  and  tyramine.  The  relative 
amounts  of  these  products  depend  on  the  type  of  pro- 
tein and  on  the  species  of  bacteria  present. 

At  present  there  is  little  evidence  that  these  substances  are 
useful  or  harmful  to  intestinal  nemas.  Glucose  is  probably 
absorbed  by  nemas,  and  on  this  assumi)tion  changes  in  the  diet 
or  in  the  bacterial  flora  which  would  affect  the  distribution  of 
glucose  should  affect  the  parasites.  From  the  studies  of  Grove, 
Olmstead,  and  Koenig  (1929)  on  the  low'er  fatty  acids  in  feces 
it  seems  as  if  the  quantity  and  perhaps  the  distribution  of  these 
materials  along  the  digestive  tract  is  greatly  affected  by  diet. 
It  is  also  probable  that  the  products  of  protein  putrefaction 
may  exert  beneficial  or  harmful  effects  on  the  parasites.  If 
so,  then  experiments  in  which  the  amount  of  protein  putrefac- 
tion is  controlled  are  in  order.  Such  control  is  possible  by  the 
administration  of  large  amounts  of  lactose  and  bacteria  which 
ferment  glucose  to  acid  (review,  Arnold,  1933).  This  treatment 
results  in  the  replacement  of  the  protein  putrefying  organisms 
of  the  coli-aerogenes  group  by  those  which  ferment  carbohy- 
drate. The  change  in  type  of  fermentation  products  is  prob- 
ably due  to  both  the  protein  sparing  action  of  carbohydrate  and 
the  change  in  flora  produced  by  increased  acidity  of  the  intes- 
tine. Putrefaction  could  also  be  decreased  by  increasing  the 
rate  of  passage  of  ingesta.  It  is  possible  to  increase  protein 
putrefaction  at  least  in  the  large  intestine  by  feeding  such  large 
quantities  of  protein  that  some  of  it  escapes  complete  digestion 
and  absorption  in  the  small  intestine.  The  putrefying  organ- 
isms also  increase  under  conditions  of  achlorhydria  which  re- 
sult in  an  alkalinization  of  the  intestine,  and  if  the  achlorhydria 
is  severe  they  may  even  become  implanted  in  the  stomach.  It 
seems  probable  that  experimental  modification  of  the  intestinal 
contents  through  modification  of  the  intestinal  flora  may  bring 
about  changes  in  the  distribution  of  nemas  along  the  intestine, 
and  perhaps  such  experiments  may  result  in  methods  of  con- 
trolling or  eliminating  certain  species.  Any  changes  which 
may  prevent  eedysis  of  larval  nematodes  might  be  extremely 
useful   (Lapage,  193S). 

It  is  known  that  HiS  is  highly  toxic  to  vertebrates  and  that 
it  easily  passes  through  most  animal  membranes.  The  studies 
of  Enigk  (1936)  on  the  lethal  effects  of  H.S  on  the  eggs  of 
Ascaris  himbricoides  and  the  studies  of  Lapage   (193.5)   on  the 


infective  larvae  of  Triclionlroiigylus  suggest  that  the  outer  cov- 
ering of  eggs  and  larvae  may  be  permeable  to  H2S  and  other 
sulfur  compounds.  Lapage  (193.5b)  obtained  considerable  evi- 
dence that  the  permeability  of  the  sheaths  of  larvae  is  changed 
by  sulfur  compounds.  In  these  experiments  the  effect  of  pH 
was  not  carefully  controlled,  but  the  effect  of  1  percent  Na2S 
on  the  eedysis  of  infective  larvae  was  more  pronounced  than 
that  of  1  or  2  per  cent  NaOH.  The  sheaths  became  greatly 
distended  due  to  intake  of  water.  If  this  effect  is  really  due 
to  the  sulfur  compounds,  this  type  of  effect  may  give  a  chemi- 
cal basis  for  the  statements  of  Mudie  (1934)  and  Johnston 
(1934)  that  the  eating  of  garlic  will  cause  the  disappearance 
of  threadworms  from  the  human  digestive  tract.  Lapage 
(193.S)  suggested  that  compounds  which  yield  H:S  when  sub- 
.iectod  to  the  action  of  intestinal  bacteria  might  eventually  be 
used  as  anthelmintics. 

Some  of  the  products  of  protein  putrefaction,  especially  H2S, 
rapidly  combine  with  molecular  oxygen  and  when  in  solution 
produce  very  low  oxidation-reduction  potentials.  Bergeim 
(1924)  devised  a  chemical  method  of  obtaining  an  index  of  the 
reducing  power  of  intestinal  contents,  and  he  found  that  the 
amount  of  reduction  varied  with  diet.  Preliminary  electrical 
measurements  of  the  oxidation-reduction  potential  of  the  rat 
digestive  tract  (Jahn,  1933)  have  shown  that  the  Eh  value  may 
be  as  low  as  — 200  mv.  in  the  caecum  and  somewhat  higher  in 
the  lower  small  intestine.  These  measurements  are  well  within 
the  "anaerobic"  range  and  support  the  conclusions  mentioned 
above  that  oxygen  is  verj'  scarce  in  the  small  intestine  and  ab- 
sent in  the  caecum. 

The  osmotic  pressure  of  the  digestive  tract  is  usually  some- 
what higher  than  that  of  the  serum  and  tissues.  Schopfer 
(1932)  gives  the  following  freezing  point  depressions  for  va- 
rious animals:  sheep,  0.70-0.83°  C;  cow,  0.80°  C. ;  horse,  0.74- 
0.77°  C;  hog,  0.9-1.0°  C;  and  the  elasmobranch  Scylliorhini/s, 
2.4°  C.  With  the  exception  of  the  elasmobranch  the  serum  of 
the  above  animals  has  a  molecular  depression  of  about  0.55  to 
0.65°  G.  Davey  (1936b)  gave  a  value  of  0.55-0.63°  C.  for  the 
abomasal  contents  of  sheep.  The  osmotic  pressure  of  the  in- 
testinal contents  probably  varies  considerably  with  salt  intake, 
but  absorption  and  excretion  are  apparently  rapid  enough  to 
prevent  the  osmotic  pressure  from  ever  becoming  more  than 
twice  that  of  the  blood.  As  will  be  discussed  below  (General 
Chemical  Composition)  the  osmotic  pressure  of  the  medium 
determines  that  of  the  worms.  However,  the  effect  of  this 
change  in  osmotic  pressure  on  worm  metabolism  is  unknown. 
Davey  (1938)  has  shown  that  Ostertagia  circumcincta  is  capable 
of  living  in  NaCl  which  varied  from  .4  percent  to  1.3  percent 
(0.9  percent  is  equivalent  to  a  freezing  point  depression  of 
0.6°  C).  In  balanced  salt  solutions  the  range  would  probably 
be  greater. 

ANTIENZYMES 

Since  the  nematodes  of  the  vertebrate  digestive  tract  live  in 
a  medium  high  in  the  concentration  of  proteolytic  enzymes,  the 
question  of  how  they  are  able  to  resist  digestion  has  often  been 
mentioned  in  the  literature.  The  mechanism  seems  to  be  at 
least  dual:  (1)  the  cuticle  is  relatively  indigestible,  and  (2) 
the  worms  contain  or  secrete  antienzymes,  i.e.,  substances  which 
inactivate  the  digestive  enzymes.  Evidence  for  this  latter 
mechanism  was  first  described  by  Weinland  (1903)  who  de- 
scribed a  substance  with  antitryptie  powers  in  aqueous  extracts 
of  Ascaris.  Dastre  and  Stassano  (1904)  believed  that  the  ac- 
tion was  antikinasic,  but  the  experiments  of  Hamill  (1906) 
confirmed  the  original  conclusions  of  Weinland  (1903).  Hamill 
(1906)  ascribed  the  following  properties  to  the  antienzyme: 
highly  soluble  in  water  and  weak  alcohol;  insoluble  in  85  per- 
cent alcohol ;  thermostable  in  neutral  or  acid  solutions ;  ther- 
molabile  in  weakly  or  strongly  alkaline  solutions ;  readily  dif- 
fusible through  membranes  which  retain  colloids.  Harned  and 
Nash  (1932)  described  an  improved  method  for  preparing  high 
concentrations  of  antitrypsin  by  fractional  precipitation  with 
alcohol.  They  claimed  that  by  varying  the  concentration  of 
alcohol  a  preparation  of  antitrypsin  could  be  obtained  almost 
free  of  Ascaris  protease.  These  investigators  were  able  to 
demonstrate  that  their  antitrypsin  preparation  also  contained 
a  weak  antipepsin.  A  powerful  trypsin  inhibiting  fraction  was 
also  recently  isolated  by  Collier  (1941)  from  Ascaris.  An  anti- 
trypsin with  chemical  properties  similar  to  those  of  Ascaris 
antitrypsin  has  been  prepared  from  egg  white  by  Balls  and 
Swens'on  (1934). 

Sang  (1938)  investigated  the  mechanism  of  the  action  of 
Ascaris  antienzyme  and  confirmed  the  conclusion  that  the  sub- 
stance exerted  both  an  antitryptie  and  an  antipeptic  activity. 
However,  he  could  not  confirm  the  result  of  Harned  and  Nash 
(1932)  that  the  ratio  of  protease  to  antienzyme  could  be  varied. 
Sang  concluded  that  Ascaris  protease  and  Ascaris  antitrypsin 
and  antipepsin  are  all  one  and  the  same  substance,  and  he  pro- 


359 


posed  that  this  substance  be  called  "asearase."  His  investiga- 
tions showed  that  asearase  was  readily  diffusible  and  that  it 
either  is  or  is  associated  with  a  substance  of  the  order  of  a 
primary  albumose.  It  was  precipitated  by  ammonium  sulphate 
and  70  per  cent  alcohol,  and  was  not  destroyed  by  trypsin. 
Asearase  did  not  inhibit  the  action  of  papain.  Von  Bonsdorff 
(1939)  was  unable  to  confirm  the  existence  of  antitrypsin  or 
antipepsin  in  Ascaris  extracts,  but  he  did  find  that  the  extracts 
inhibited  proteolysis  of  casein  bv  depepsinized  gastric  juiee  at 
pH  7.4. 

Stewart  and  Shearer  (1933)  studied  the  digestion  of  pro- 
tein by  infected  and  noninfected  sheep  and  concluded  that  the 
nematodes  of  the  stomach  inhibited  the  normal  digestive  proc- 
esses. They  then  obtained  an  extract  from  the  worms  which 
was  capable  of  producing  a  40  to  7')  per  cent  inhibition  of  the 
peptic  digestion  of  casein.  For  this  sulistance  and  for  similar 
antienzymes  of  nematodes  they  siiggested  the  term  ' '  nezyme. ' ' 
Andrews  (1938)  could  not  repeat  the  results  of  Stewart  and 
Shearer  on  the  lowered  digestive  action  of  infected  sheep.  He 
found  that  the  digestibility  coefficients  were  the  same  in  infected 
and  noninfected  animals.  Infected  sheep  did  not  gain  weight 
as  rapidly  as  controls,  but  Andrews  concluded  that  this  was 
probably  caused  by  intestinal  irritation. 

The  existence  of  antienzymes  has  also  been  reported  for 
cestodes.  However,  de  Waele  (1933),  on  the  basis  of  experi- 
ments on  Taenia  sagiiiata,  has  questioned  the  existence  of  anti- 
enzymes and  has  assumed  that  protection  of  the  worms  from 
enzyme  action  is  due  entirely  to  the  resistance  of  the  cuticle. 
One  basis  for  this  assumption  is  found  in  the  fact  that  pieces 
of  worms  but  not  whole  worms  may  be  digested  by  trypsin. 
This  conclusion  is  sub.iect  to  criticism  in  that  when  worm  frag- 
ments are  placed  in  an  enzyme  solution  considerable  dilution 
of  any  antienzyme  may  occur  by  diffusion  and  the  antienzyme 
may  thereby  be  rendered  ineffective.  In  view  of  the  chemical 
isolation  of  the  antienzyme  mentioned  above  (Hamill,  1906; 
Nash  and  Harned.  1932;  Collier,  1941)  de  Waele's  conclusion 
certainly  can  not  Ije  extended  to  the  nematodes. 

General  Chemical  Composition 

DRY  WEIGHT 
There  have  been  only  a  few  determinations  of  the  dry  weight 
of  parasitic  nematodes,  and  the  values  recorded  are  fairly  high. 
The  average  figures  reported  for  Ascaris  lumbricoidcs  are  20.7 
percent  (Weinland,  1901)  and  15  percent  (Flury,  1912),  for 
Parascaris,  21  percent  (Schimmelpfennig,  1903)  and  14.8  per- 
cent (Flury,  1912),  and  for  a  larval  EiistrongtiUdes,  25  percent 
(V.  Brand",  1938).  Flury  (1912)  measured  the  dry  weight  of 
various  parts  of  the  body  and  obtained  the  following  results: 

Dry  weight  in  percent  of  fresh  weight 
Ascaris  fnmbricoidrs     Parascaris  equorum 

Body  wall  ..- 23.5-25.0  25.0 

Alimentary   tract 27.5  24.9 

Body  fluid  - 4.0-  6.7  5.0 

Reproductive  organs  ...         25.0-33.3  24.0-27.4 


It  can  be  calculated  from  Flury 's  figures  that  these  values 
represent  the  following  fractions  of  the  total  dry  weight:  body 
wall  65  percent,  alimentary  tract  3  percent,  body  fluid  10  per- 
cent, and  reproductive  organs  20  per  cent. 

CARBOHYDRATE.S 

Storage  of  carbohydrates  in  the  form  of  polysaccharides 
seems  to  be  quite  common  among  the  parasitic  nematodes.  .W- 
though  chemical  analyses  have  been  made  only  for  Ascaris,  it 
seems  likely  that  in  this  respect  other  species  are  very  similar. 
Weinland  (1901)  and  Flury  (1912)  found  an  optical  rotation 
of  +183°  to  +193°  for  the  polysaccharide  of  Ascaris.  Since 
these  workers  and  Campbell  (1936)  identified  the  sugar  result- 
ing from  hydrolysis  as  glucose,  and  since  the  solubility  of  the 
polysaccharide  and  its  color  reaction  with  iodine  are  typical 
of  glycogen,  it  seems  probable  that  the  substance  is  true  glyco- 
gen. Campbell  (1936),  however,  observed  antigenic  properties  of 
a  polysaccharide  fraction  isolated  from  Ascaris.  It  does  not  seem 
likely  that  pure  glycogen  would  be  capable  of  inducing  the  for- 
mation of  specific  anti-bodies.  One  should  therefore  expect  that 
another  polysaccharide  is  associated,  perhaps  in  very  small 
amounts  only,  with  the  glycogen.  However,  in  so  far  as  meta- 
bolic processes  are  concerned,  it  is  justifiable  to  speak  of 
glycogen  alone. 

The  occurrence  of  large  amounts  of  glj'cogen  in  ascarids  was 
established  in  a  qualitative  or  semi-quantitative  wav  by  Claude 
Bernard  (1859)  and  Foster  (1865),  but  Weinland  "(1901)  was 
the  first  to  undertake  a  large  series  of  quantitative  determina 
tions.  The  more  recent  data  on  the  glycogen  content  are  sum 
marized  in  the  following  table: 


Glyco- 
gen  in 

7o    of 
fresh 
sub- 

Species 

Sex 

stance 

Country 

Investigator 

.-{.scans  lumbricoidcs  ... 

? 

5.4 

Germany 

Weinland,  1901 

A.scaris  lumbricoidcs  ... 

? 

6.6 

Germanv 

Schulte,  1917 

Ascaris  lumbricoidcs  ... 

5 

7.2 

Denmark 

V.  Brand,  1934 

Ascaris  lumbricoidcs  .. 

9 

8.7 

Russia 

Smorodincev 
and 

S 

6.1 

Russia 

Bebesin,  1936 

Ascaris  lumbricoidcs  ... 

9 

5.3 

USA 

V.  Brand,  1937 

Ascaris  lumbricoicUs  ... 

$ 

5.8 

USA 

V.  Brand,  1937 

Dog  Ascaris 

? 

4.5 

Germany 
Germany 

Weinland    1901 

Parascaris  cqtiornm  .... 

t 

2.1 

Schimmelpfen- 

nig, 1903 

Parascaris  equorum  .... 

9 

3.8 

Japan 

Toryu,   1933 

Parascaris  equorum    ... 

S 

2.9 

Japan 

Toryu,  1933 

Ancylostoma  caninum 

mixed 

1.6 

USA 

V.  Brand  and 
Otto,  1938 

Slrottpi/lus  vulgaris  .... 

» 

3.5 

.Japan 

Toryu,  1933 

Filaria   equina   .. 

? 

2.2 

6.9 

Japan 
USA 

Torvu,   1933 

Larval    Eustrongylides 

V.  Brand,  1938 

Apparently  the  glycogen  content  of  parasitic  nematodes  is 
always  high.  The  lowest  value  amongst  the  intestinal  nema- 
todes was  found  in  Ancylostoma.  This  may  be  related  to  the 
fact  that  the  hookworms  have  access  to  larger  amounts  of 
oxygen  than  the  other  intestinal  helminths.  It  is  curious  that 
A.scaris  lumbricoidcs  analyzed  in  Denmark  and  Russia  yielded 
higher  average  glycogen  values  than  those  in  USA  and  Ger 
many.  It  is  unknown  whether  this  is  caused  by  a  different 
diet  of  the  host  and  therefore  of  the  parasite  in  various  couu 
tries,  or  merely  to  different  handling  of  the  pigs  before  slaugh- 
tering. 

Sexual  differences  in  glycogen  content  of  parasitic  nematodes 
do  not  seem  to  be  pronounced.  Smorodincev  and  Bebesin  (1936) 
and  Toryu  (1933)  found  more  glycogen  in  females  than  in 
males  of  Ascaris  and  Parascaris.  Von  Brand  (1937),  on  the 
other  hand,  found  slightlj'  more  polysaccharide  in  male  as 
carids. 

So  far,  only  adult  nematodes  of  warm-blooded  hosts  have 
been  analyzed,  and  contrary  to  what  is  known  about  many 
free-living  invertebrates,  no  evidence  of  seasonal  variation  in 
the  amount  of  stored  glycogen  has  been  found.  The  obvious 
explanation  of  this  difl'erence  lies  in  the  uniform  conditions 
under  which  the  parasitic  organisms  live  throughout  the  year. 
From  this  viewpoint,  it  should  prove  interesting  to  survey  para- 
sites from  poikilothermic  and  heterothermic  hosts,  in  which  such 
variations  are  more  likely  to  occur. 

The  glycogen  distribution  in  various  organs  and  tissues  has 
been  investigated  both  by  quantitative  chemical  methods  and 
by  differential  staining.  Toryu's  (1933)  analyses  of  various 
organs  of  Parascaris  equorum  are  summarized  in  the  following 
table: 


Organ 


Glycogen  in  percent  of 

fresh  substance     total  glycogen 


Body   wall    (cuticle    +    sub- 
cuticle  +  muscles)   

Intestine 

Ovary 

Uterus  - - 

Male  reproductive  system 


9 

s 

9 

s 

5.8 

4.9 

66 

96 

0.6 

0.6 

2 

0 

fi.5 

23 

1.6 

9 

0.5 


The   body   wall   is   obviously   the   most   important   storage   place 
for  glycogen  in  worms  of  both  sexes. 

Differential  glycogen  staining  has  been  used  chiefly  by  v. 
Kemnitz  (1912)  and  ilartini  (1916)  working  with  Ascaris 
and  O.Tyuris,  respectively.  These  workers  extended  the  earlier 
investigations  of  Brault  and  Loeper  (1904)  and  Busch  (1905). 
It  seems  that  in  both  cases  the  most  intensive  glycogen  reac- 
tions are  found  in  the  plasmatic  bulbs  of  the  muscle  cells  of 
the  body  wall  and  in  the  hypodermis,  cspeciall.v  in  the  region 
of  the  lateral  chords,  but  it  was  also  found  in  other  organs, 
for  example,  the  intestine  (compare  also  Hirsch  and  Bret- 
schneider,  1937)  and  the  reproductive  organs.  Glycogen,  how- 
ever, was  never  found  in  the  cuticle,  the  phagocytic  organs  and 
the  nervous  system.  Additional  data  om  the  glycogen  mor- 
phology of  other  parasitic  nematodes  (Parascaris,  Scleroslo- 
mum,  Helerakis  and  Ancylostoma)  are  found  in  the  papers  of 
Busch  (1905),  V.  Kemnitz  (]912\  Faure  Fremiet  (1913),  Tor- 
yu  (1933)  and  Giovaunola   (1935).    In  these  cases,  the  general 


360 


(lattoiii  of  glvcoKi'ii  storagi'  Sffiiis  to  Ix'  similar  to  that  of 
Ascaris.  In  acuordaiu'e  with  the  (luantitativc  cliemical  obsoiva 
tions  muoh  U'ss  glvcogon  was  fuuiul  l)y  morpliological  inothods 
ill  hookworms  than  in  ascarids.  In  the  former,  liowevcr,  the 
rays  of  the  bursa  are  an  important  storage  place,  and  prob- 
ably represent  an  energy  reserve  for  the  male  during  the  periods 
of  copulation  when  it  is  detached  from  the  intestinal  wall 
(Giovannola,  193.')). 

Not  much  is  known  about  the  occurrence  of  carbohydrates  of 
lower  molecular  weight  in  parasitic  nematodes.  Weinland 
(1901)  found  1.6  percent,  and  Schulte  (I'UT)  found  0.9  percent 
glucose  in  Ascaris  himbricoidt!!.  It  is,  however,  questionable 
whether  these  figures  are  not  too  high,  due  to  a  partial  break- 
down of  glycogen  during  the  analyses.  According  to  Foster 
(lSG;i)  and  v.  Brand  (1934)  only  very  small  amounts  of  re- 
ducing sugar  occur  in  Ascaris.  Faure-Fremiet  (1913)  found 
0.15  percent  glucose  in  the  body  fluid  of  Parascaris. 

ETHER  EXTRACTABLE  MATERIAL 

The  parasitic  nematodes  seem  to  contain  only  small  amounts 
of  material  extractable  with  ether  or  petrol  ether.  The  mean 
values  for  Ascari.i  Iinnhricoidcs  vary  from  1.2  to  1.6  percent 
(Weinland,  1901:  Flury,  1913;  Schulte,  1917;  v.  Brand,  1934; 
Smorodincev  and  Bebesin,  1936),  and  the  value  for  a  larval 
EustrongyJides  is  1.1  percent   (v.  Brand,  1S38). 

The  chemical  compounds  comprising  the  ether  extract  seem 
to  be  quite  similar  in  Ascaris  and  Parascaris  (Flury,  1912; 
Faure-Fremiet,  1913;  Schulz  and  Becker,  1933).  According  to 
Flury  (1912)  100  gm  of  ether  extractable  material  from  As- 
caris contains  the  following : 

Volatile  fatty  acids  _ 31.07  gm 

Saturated  fatty  acids  _. 30.89  gm 

Unsaturated  fatty  acids  34.14  gm 

Unsaponifiable  matter  24.72  gm 

Glycerol    „ 2.40  gm 

Lecithin 6.61  gm 

The  volatile  fatty  acids  were  represented  chiefly  by  valeric 
and  butyric  acids,  with  small  amounts  of  formic,  propionic  and 
acrylic  acid.  In  Parascaris  the  whole  series  of  volatile  fatty 
acids  has  been  reported  (Schimmelpfennig,  1903).  The  saturat- 
ed fatty  acids  of  higher  molecular  weight  were  recognized  as 
stearic  acid  with  a  small  admixture  of  palmitic  acid.  Oleic 
acid  was  the  chief  representative  of  the  unsaturated  fatty  acids. 
Flury 's  value  for  glycerol  is  probably  too  low.  Schulz  and 
Becker  (1933),  using  newer  methods,  found  glycerol  values 
ranging  up  to  8.8  percent.  It  is,  therefore,  unnecessary  to  as- 
sume as  seemed  necessary  to  Flury  (1912)  that  there  is  a  com- 
bination of  part  of  the  fatty  acids  with  the  unsaponifiable 
matter.  It  is  probable  that  all  the  fatty  acids  are  present  in 
form  of  glyceryl  esters.  The  unsaponifiable  material  is  of 
special  interest  because  it  contains  a  compound  which  so  far 
has  been  found  in  no  other  animal.  This  substance  was  found 
independently  by  Flury  (1912)  and  Faure-Fremiet  (1913), 
and  it  is  known  as  ascaryl  alcohol.  It  was  recently  reinvesti- 
gated by  Schulz  and  Becker  (1933),  who  assigned  it  the  for- 
mula C33Hr»404.  They  state  that  its  configuration  is  not  yet 
sufficiently  known,  but  that  it  may  be  an  ethereal  combination 
of  glycerol  with  some  higher  alcohol.  According  to  Faure- 
Fremiet  (1913)  ascaryl  alcohol  occurs  in  the  female  repro 
ductive  cells  only.  Under  these  circumstances  one  wonders 
why  neither  Flury  (1912)  nor  Schulz  and  Becker  (1933)  men- 
tion any  other  unsaponifiable  substance,  which  should  be  ex- 
pected in  other  parts  of  the  body.  Faure-Fremiet  (1913) 
found  small  amounts  of  cholesterol  in  the  body  fluid,  the  eggs, 
and  the  testes  of  Ascaris,  but  Bondouy  (1910)  found  no 
cholesterol  in  Strongylus  equinus.  The  ether  extract  of  the  lat- 
ter species  seems  to  be  characterized  by  the  presence  of  soaps. 

Little  is  known  about  the  distribution  of  the  ether  extract- 
able  material  in  different  organs.  Flury  (1912)  found  it  to 
comprise  1.00  percent  of  the  body  wall  of  Ascaris  and.  4.0  to 
6.2."i  percent  of  the  reproductive  organs.  The  latter  figure 
agrees  with  that  given  by  Faure-Fremiet  (1913)  for  the  testes. 
If  allowances  are  made  for  the  relative  weights  of  body  wall 
and  reproductive  systems,  it  seems  probalile  that  roughly  the 
same  amount  of  ether  extractable  material  is  stored  in  both 
these  places.  This  is  in  marked  contrast  to  the  distribution  of 
glycogen. 

Microscopical  examinations  (v.  Kemnitz,  1912;  Faure-Fre- 
miet, 1913;  Mueller,  1928/29;  Hirsch  and  Bretschneider,  1937) 
have  shown  that  fat  droplets  are  deposited  in  the  plasma  bulbs 
of  the  muscles  of  Ascaris,  in  which  the  nuclei  are  usually 
surrounded  by  an  accumulation  of  fat,  in  the  four  chords,  and 


especially  in  the  subcuticuhi.  Stainable  fat  was  also  found  in 
ganglion  cells,  the  intestinal  cells,  and  the  reproductive  or- 
gans. According  to  Mueller  (1928/29)  considerably  more  fat 
can  be  demonstrated  with  osniic  acid  in  Parascaris  than  in 
Ascaris,  although  the  pattern  of  fat  deposition  is  the  same  in 
both    species. 

NITROGEN  CONTAINING  SUBSTANCES 

Flury  (1912)  found  8.1  percent  proteins  in  Ascaris.  This 
is  somewhat  less  than  should  be  expected  from  Weinland 's 
(1901)  N  figure  of  1.80  percent.  Flury  (1912)  ascertained 
the  presence  of  albumin,  globulin,  albumoses  and  peptones, 
purinebascs,  amines  and  ammonia,  and  he  identified  a  series 
of  amino  acids  as  degradation  products  of  the  worm  i)rotein. 
Recently  Yoshimura  (1930)  performed  a  quantitative  analysis 
of  the  amino  acids  resulting  from  the  hydrolysis  of  ascarids 
with  sulfuric  and  hydrochloric  acid.  His  results  are  summarized 
in  the  following  table: 


Amino  acids  in  percent  of  dry  substance  upon  hydrolysis  with 


hydrochloric 
acid 


sulfuric 
acid 


Leucine   ._.  3.70 

Alanine   -- 1.4." 

Valine   0.79 

Proline  3.41 

Isoleucine   1.45 

Serine    - 0.72 

Glutaminie  acid  3.93 

Aspartic  acid  0.36 

Glycocoll   0.29 

Phenylalanine  0.02 


Leucine  15..54 

Histidine    0.45 

Arginine    1.28 

Lysine  ! 2.58 

Tyrosine  2.09 


The  N  containing  substances  constituting  the  cuticle  have 
already  been  discussed  in  another  chapter  (see  page  32),  and 
that  characteristic  of  the  eggs  (chitin)  is  mentioned  on 
page  177. 

Faure-Fremiet  (1913)  described  under  the  name  of  ascaridine 
an  intracellular  protein  of  the  spermatozoa  of  Ascaris.  It  con- 
tains 17.5  percent  N,  but  no  phosphorus  or  sulfur.  The  chemi- 
cal constitution  of  this  interesting  compound  is  not  yet  sufli- 
ciently  known.  It  is  insoluble  in  cold  distilled  water,"  but  dis- 
solves rapidly  in  water  of  50  to  51  °C.  This  critical  temperature 
varies  greatly  if  the  substance  is  dissolved  in  various  salt 
solutions  (Faure-Fremiet  and  Filliol,  1937).  According  to 
Champetier  and  Faure-Feimiet 's  (1937)  roentgenographie  stud- 
ies ascaridine  seems  to  be  a  semi-crystalline  substance,  but  it 
can  be  changed  experimentally  into   an   amorphous  state. 

In  recent  years  an  increasing  amount  of  attention  has  been 
given  to  the  occurrence  of  respiratory  pigments  in  parasitic 
nematodes.  Haemoglobin  seems  to  be  widely  distributed.  It 
has  been  found  in  Dioclophyma,  Ascaris,  Para.<icaris,  To.tocara, 
Nematodirns,  species  of  Trichosirougyiits,  Camallaniis,  Spiro- 
cerca,  a  larval  Eustrongylides  and  larvae  of  Trichinella  (Aduc- 
co,  1889;  Flury,  1912;  Faure-Fremiet,  1913;  Keilin,  1925; 
Kriiger,  1936;  v.  Brand,  1937;  Davey,  1938;  Stannard,  McCoy 
and  Latchford,  1638;  Wharton,  1938,  1941;  Hsii,  1938:  Janicki, 
1939).  The  best  known  case  is  that  of  Ascaris  where  it  is 
found  both  in  the  body  fluid  and  the  body  wall.  The  absorption 
bands  of  the  haemoglobins  occurring  at  these  two  places  are 
slightly  different,  and  this  indicates  the  presence  of  two  kinds 
of  haemoglobin  (Keilin,  1925).  In  all  the  above  cases,  where 
haemoglobin  has  been  found  beyond  the  intestinal  wall,  one 
can  safely  assume  that  it  has  been  synthetized  by  the  worm. 
Parts  of  the  host  haemoglobin  molecule  may,  of  course,  be 
used  in  this  process,  but  no  definite  data  on  this  possibility  have 
been  ob'oained.  Obviously,  haemoglobin  found  in  the  intestinal 
tract  of  a  worm  will  not  fall  in  the  same  category,  though  in 
some  instances  it  may  play  a  physiologically  similar  role  (hook- 
worm,  for   example). 

Tlye  only  other  respiratory  pigments  found  so  far  are  cyto- 
chrome, which  is  known  to  occur  in  Ascaris,  Parascaris  and 
Caviallanus  where  the  highest  concentration  is  found  in  the  eggs 
and  sperm  (Keilin,  1925;  Wharton,  1941)  and  flavine  found 
In- .Goureviteh    (1937)    in  Parascaris. 


361 


INORGANIC  SUBSTANCES 

Ascaris  lumbricoUIes  according  to  Flury  (1912)  contains  0.76 
percent  inorganic  substances,  and  a  larval  Etistrongi/lides  ac- 
cording to  V.  Brand   (1938)   contains  1.1  percent. 

A  quantitative  analysis  of  the  inorganic  substances  of  As- 
caris by  Flury   (1912)   gave  the  following  results: 

Na   - - —  1.104%    of    the    dry    weight 

K - 0.607 

Ca -- 0.404 

Mg  0.058 

Al  -- -- 0.131 

Fe —  0.019 

CI 1-272 

PO4    -- 1-315 

SO.  .  - -  0.114 

SiO=  0.029 

Neither  copper  nor  manganese  was  found,  and  it  can  be  said 
that  on  the  whole  the  composition  of  the  ash  of  Ascaris  seems 
to  be  quite  similar  to  that   of  free  living  organisms. 

The  osmotic  pressure  of  the  tissues  of  several  Ascaris  species 
and  that  of  the  body  fluid  of  Parascaris  (Vialli,  1923,  Schopfer, 
1926,  1932)  is  similar,  but  not  identical  to  that  found  in  the 
host  intestine.  The  osmotic  pressure  of  the  worms  always  seems 
to  be  a  little  lower,  so  that  they  live  in  a  slightly  hypertonic 
environment.  It  is  noteworthy  that  chlorides  seem  to  play  only 
a  minor  role  in  producing  the  normal  osmotic  pressure  of  the 
body  fluid  of  Parascaris  (Marcet,  I86.1,  Schopfer,  1932).  The 
total  osmotic  pressure  corresponds  to  a  freezing  point  depres- 
sion (A)  of  — 0.62°C.  wliercas  the  osmotic  pressure  due  to  the 
chlorides  is  equivalent  to  a  A  value  of  — 0.12°C.  The  osmotic 
pressure  varies  directly  with  that  of  the  environment.'  The 
osmotic  pressure  of  Frolcptiis  obtusus  living  in  the  marine 
elasmobranch  ScuUiorhiiiiis  is  considerably  higher  than  that 
of  the  other  parasites  mentioned  and  is  slightly  higher  than 
that  of  Sci/lliorhiitiis  blood  (A  =  —2.40°,  Schopfer,  1932). 

iPanikkar  and  Sproston  (1941)  give  data  for  Angusticneeum  sp.  from 
the  intestine  of  the  tortoise.  It  is  of  interest  that  according  to  Stoll 
(1940)  the  first  parasitic  ecdysis  of  Hiiemnnclius  contortus  is  favored 
by  hypotonic  solutions. 

Metabolism  of  Adult  Nematodes 

METABOLISM  UNDER  ANAEROBIC  CONDITIONS 
Most  of  the  experiments  on  nematodes  under  anaerobic  con- 
ditions have  been  performed  with  Ascaris  Uimbricoides.  Bunge 
(1889)  found  that  this  species  can  be  kept  for  several  days 
in  the  absence  of  oxygen  and  that  it  produces  during  this  time 
carbon  dioxide  and  a  volatile  acid.  Considerable  progress  was 
made  by  Weinland  (1901)  who  performed  quantitative  deter- 
minations of  the  amounts  of  various  substances  consumed  and 
produced  and  who  recognized  that  carbohydrates  were  pre- 
dominantly used.  In  starvation  experiments  of  several  days' 
duration  he  found  that  100  gm  of  worms  consumed  0.7  gm 
glycogen  and  0.1  gm  glucose  in  24  hours.  He  found  among  the 
end  products  0.4  gm  carbon  dioxide  and  0.3  gm  of  a  volatile 
fatty  acid  which  he  identified  as  valeric  acid.  Later  Weinland 
(1904)  found  that  caproic  acid  was  also  present  in  the  ether 
soluble  excreta  of  Ascaris.  A  quantitative  study  of  fat  and 
nitrogen  in  similar  starvation  experiments  led  Weinland  (1901) 
to  the  conviction  that  both  carbon  dioxide  and  fatty  acids  were 
derived  from  the  breakdown  of  glycogen,  and  he  compared  this 
process  to  the  fermentations  produced  by  microorganisms.  This 
view  concerning  the  anaerobic  processes  of  Ascaris  is  still  valid, 
although  subsequent  investigations  necessitated  certain  changes 
in  Weinland 's  conclusions.  In  the  first  place  it  was  found  that 
in  addition  to  valeric  and  caproic  acids,  some  formic,  butyric 
(Flury,  1912)  and  lactic  acid  (v.  Brand,  1934a)  were  also 
present  in  the  excreta.  At  present  it  is  certain  that  valeric 
acid  is  the  chief  end  product,  but  there  is  some  uncertainty  as 
to  the  type  of  valeric  acid  excreted.  It  seems  probable  that  it 
is  normal  valeric  acid  (Waechter,  1934),  although  Flury  (1912) 
believed  that  he  had  identified  isovaleric  acid.  Kriiger  (193(5) 
suggested  the  presence  of  methyl-cthyl-acetie  acid,  but  Oesterlin 
(1937)  pointed  out  that  this  identification  was  insulflciently 
supported  by  Kriiger 's  data. 

The  second  necessary  modification  of  Weinland 's  conclusions 
concerns  the  intensity  of  the  fermentation  process.  It  was 
found  that  with  increasing  length  of  starvation  a  deereising 
daily  amount  of  glycogen  was  used  and  that  less  carbon  dia"ide 
was  produced  (Weinland,  1901;  Schulte,  1917;  v.  Brand,  19'i4a, 
1937;  Kriiger,  1936).  In  experiments  conducted  for  only  24 
hours'  with  fresh  worms  about  1.4  gm  of  glycogen  was  used. 
This  is  twice  as  much  as  Weinland   (1901)   found  for  the  av"n- 


age  daily  glycogen  consumption  (11.7  gm )  in  experiments  whicli 
lasted  as  long  as  (i  days.  It  is,  however,  curious  and  not  yet 
sufficiently  understood,  tliat  despite  the  different  lengths  of 
their  experimental  periods,  most  of  the  above  mentioned  in- 
vestigators found  that  between  0.2  and  0.3  gm  of  valeric  acid 
was  produced  per  day.  Kriiger  (1936),  however,  found  that 
about  0..5  gm  fatty  acid  was  excreted  during  the  first  24  hours. 

The  last  complete  biochemical  balance  under  anaerobic  condi- 
tions was  given  by  v.  Brand  (1934a)  for  females  of  Ascaris 
hinihricoidcs.  He  found  that  100  gm  of  worms  consumed,  dur- 
ing 24  hours  at  37°C.,  1.39  gm  glj'cogen  and  produced  0.71  gm 
carbon  dioxide,  0.22  gm  valeric  acid,  and  0.02  gm  of  lactic 
acid.  No  complete  data  are  available  for  males.  It  has  been 
found,  however,  that  the  glycogen  consumption  is  identical  in 
both  sexes  during  the  first  24  hours  and  that  the  more  active 
males  later  consume  more  glvcogen  than  the  females  (v.  Brand, 
1937a). 

Parascaris  equorum  seems  to  have  a  (piite  similar  carbohy- 
drate metabolism.  Fischer  (1924)  ascertained  the  production 
of  small  amounts  of  lactic  acid.  Toryu  (1936a)  found  a  small 
amount  of  lactic  and  propionic  acid  and  a  large  amount  of 
valeric  acid,  but  no  formic,  acetic,  butyric,  caproic,  malic,  citric 
or  succinic  acids.  His  glycogen/acid  balance  for  the  first  24 
hours  of  anaerobiosis  for  100  gm  of  worms  was  as  follows: 
Consumed:  1.39  gm  glycogen.  Produced:  0.6."i  gm  valeric  acid 
and  0.02  gm  lactic  acid.  In  addition  carbon  dioxide  was  pro- 
duced and  the  amount  of  carbon  dioxide  differed  markedly  for 
females  and  males  (Toryu,  19361)).  It  is  not  clear  what  ani- 
mals were  used  for  the  glycogen/acid  experiments,  and  there- 
fore it  is  impossible  to  introduce  leliable  carlioii  dioxide  values 
into    the    above    balance. 

The  above  data  indicate  that  the  end  jiroducts  of  the  anaero- 
bic carbohydrate  metabolism  are  chiefly  lower  fatty  acids  and 
therefore  noticeably  different  from  that  of  a  vertebrate  muscle. 
This  concept  has  been  criticized  chiefly  by  Fischer  (1924)  and 
Slater  (192-")).  The  former  investigator  concedes  that  living 
Parascaris  excrete  only  a  small  amount  of  lactic  acid,  and  a 
larger  amount  of  an  unidentified  acid.  He  found,  however,  that 
in  minced  material  the  i)roduction  of  lactic  and  the  liberation 
of  phosphoric  acid  was  sufficient  to  account  for  the  whole 
acidity  oliscrved  in  aerobically  conducted  experiments.  There- 
fore, he  concluded  that  there  was  no  great  difference  between 
the  glycogen  breakdown  in  Parascaris  and  in  vertebrates.  In 
the  opinion  of  the  present  writers,  however,  his  observation  in- 
dicates merely  that  through  changes  in  the  experimental  condi- 
tions the  course  of  the  chemical  reactions  can  be  changed — a 
phenomenon  well  known  in  e.xpcriments  with  yeast  and  other 
lower  plants.  It  should  lie  remembered  that  Weinland  (1902) 
found  the  same  end  products  with  extracts  of  Ascaris  under 
anaerobic  conditions  as  he  had  found  in  experiments  with 
whole   worms. 

Slater  (1925)  demonstrated  that  bacteria  capable  of  trans- 
forming sugar  into  volatile  fatty  acids  could  be  isolated  from 
a  saline  solution  in  which  ascarids  had  been  immersed.  He 
failed,  however,  to  show  that  the^'  were  present  in  sufficient 
numbers  to  account  for  all  the  organic  acids  produced  in  ex- 
periments with  worms,  and,  furthermore,  he  did  not  demon- 
strate any  substance  which  could  have  served  as  a  substrate  for 
such   bacterial   fermentation. 

Several  lines  of  evidence  have  been  brought  forward  which 
seem  to  indicate  a  direct  connection  between  nematodes  and  the 
production  of  lower  fattj'  acids.  The  following  two  may  be 
mentioned.  The  volatile  acids  are  found  not  only  in  saline  in 
which  worms  have  been  kept,  but  also  in  distillates  of  minced 
worms  (Weinland,  1901)  and  in  the  ether  extract  of  whole 
worms  (Flury,  1912;  Schimmelpfeunig,  1903).  Valeric  acid 
has,  furthermore,  been  found  under  both  aerobic  and  anaerobic 
conditions,  although  one  should  expect  that  such  a  difference  in 
the  e.xternal  conditions  should  have  a  deep  influence  on  the 
development  of  a  bacterial  flora  in  the  surroundings.  For  fur- 
ther information  on  this  controversy  compare  the  discussion  of 
Slater  (1928)  with  those  of  Weinland  (1901)  and  v.  Brand 
(1934b). 

Several  methods  have  been  discussed  in  which  valeric  acid 
may  originate  from  carbohydrate.  Weinland  (1901)  favored 
the"  following  equation:  4G,Hi20,,  =  9C0=  +  SC^HioOi  +  9H=. 
It  must,  however,  be  emphasized,  that  the  postulated  hydrogen 
could  not  be  found.  Weinland  (1901)  had  to  assume  that  it 
was  used  at  once  in  other  reactions.  He  also  discussed  an  equa- 
tion   proposed    by    Koenigs: 

13CoH,20„  =   12C=H,oO.  +   18C0=  +   18H:0. 

Weinland  rejected  this  equation  because  it  did  not  predict 
nearly  as  much  carbon  dioxide  as  he  found  to  be  present. 
However,  the  excess  might  have  originated  either  from  bicar- 
bonate or  from  protein  decomposition.  Jost  (1928)  has  given 
the  following  chain  of  reactions  which  leads  to  Koenigs'  equa- 


362 


tion.  These  equatioiLs  are  piuely  tliooretical,  but  the  sorios  is 
interesting  in  that  it  sliowa  a  possible  link  between  the  prodne 
tion  of  lactic  and  valeric  acids. 


Glucose 


=     2     CjHoO;, 

Lactic  acid 


CH3.CIIOH.COOH  I 
CH3.CHOH.COOH  f 
2  Lactic  acid 


Dismutation 

and 
dehydration 


Pyruvic  acid 
(  CHn.CO.COOH 
(  CHs.CHj.COOH 

Propionic  acid 


+  H:0 


CH..CH».COOH 


t'Hn.CO.COOH  +  CHuCHo.COOH  =  CHa.COH.COOH 
CH,a'HOH.CH=.CH2.COOH  +  CO: 

-,  Hydroxy-valeric  aeid 


CH3.CH0H.CHs.CH..C00H 


=    CH3.CH2.CH2.CH2.COOH    4- 
Normal   valeric   acid 


1  CoH„0„  =  1  CH..CH..CH0.CH2.COOH  +  HjO  +  CO2  +  O 
12  C«H,=Oe   =12    CHr,.CHo.CH!.CH:.COOH    +    12    H:0    + 


1  C„H„Oo  +  6  0= 


12  CO.  +  6  O2 
6  CO2  +  6  H=0 


13  CoH,.0„  =  12  CH::.CH...CH=.CH2.COOH  +  18  CO2  +  18  H2O. 

In  effect,  then,  12  molecules  of  sugar  would  be  transformed 
into  12  molecules  of  valeric  aeid,  carbon  dioxide  and  water, 
and  the  oxygen  liberated  during  this  process  would  be  sufficient 
to  oxidize  completely  a  thirteenth  molecule  of  sugar. 

Toryu  (1936a)  proposed  the  equation:  4C„Hi:08  =  400.  + 
4C.'iHio02  +  H2O.  This  equation  needs  no  further  considera- 
tion, since  the  O  and  H  atoms  on  the  two  sides  do  not  balance. 
Correctly  written  it  would  read:  4CoHi-0,;  =  400:  +  4CgHio02 
+  4H;0  +  20=.  This  obviously  corresponds  closely  to  an  inter- 
mediate step  of  Koenigs'  equation  as  formulated  by  Jost. 

The  amount  of  heat  produced  during  the  metabolism  of 
Ascaris  lumbricoicles  was  first  determined  directly  by  Krum- 
macher  (1919).  His  experiments,  however,  were  performed  at 
a  time  at  which  o.xygen  was  regarded  as  an  inert  gas  for  these 
worms.  Krummacher's  experiments  were  neither  clearly  aerobic 
nor  anaerobic,  and  the  data  obtained  are  therefore  difRcult  to 
interpret.  Meier  (1931),  on  Krummacher's  suggestion,  per- 
formed similar  experiments  under  anaerobic  conditions.  He 
found  a  heat  production  of  0.300  gm  cal  per  gm  of  worm  per 
hour.  On  the  basis  of  Weinland  's  chemical  data  and  his  own 
heat  determinations  he  calculated  that  the  fermentation  process 
yields  22  percent  of  the  energy  obtainable  by  total  oxidation 
of  the  carbohydrate.  This  is  considerabl.v  more  than  usually 
found  in  bacterial  fermentations.  Undoubtedly,  however,  Meier 's 
figure  of  22  percent  is  far  too  high.  His  experimental  periods 
lasted  only  from  4  to  12  hours,  and  he  used  presumably  fresh 
worms.  Therefore,  the  carbohydrate  consumption  must  have 
been  much  higher  than  Weinland 's  figure.  Furthermore,  Schulte 
(1917)  has  demonstrated  by  direct  comparisons  of  the  heat  of 
combu.stion  with  the  glycogen  content  of  fresh  and  starving 
ascarids  that  the  carbohydrate  metabolism  accounts  for  only 
80  percent  of  the  total  loss  of  calories  from  the  body.  Meier, 
however,  assumed  that  the  total  heat  production  was  due  to 
carbohydrate  fermentation.  At  present  the  data  necessary  for 
an  e.xact  balance  sheet  of  the  energies  involved  seems  to  be 
unavailable.  A  fair  guess  .would  place  the  energy  yield  of  the 
fermentation  between  6  and  12  percent.  This  is  still  more  than 
that  usually  found  in  bacterial  fermentations.  Lactic  acid  fer- 
mentation, for  example,  yields  only  about  2.6  percent,  and  al- 
coholic fermentation  yields  4  percent. 

Changes  under  anaerobic  conditions  in  the  material  extract- 
able  with  ether  have  been  studied  less  thoroughly  than  the 
changes  in  glycogen  content.  Weinland  (1901)  found  that 
there  was  no  change  in  the  fat  content  of  ascarids  during  star- 
vation, and  V.  Brand  (1934a)  reached  the  same  conclusion. 
Schulte  (1917),  on  the  other  hand,  observed  a  fat  increase  of 
0.08  gm  per  100  gm  animals  per  day.  He  considered  this  fat 
to  be  a  product  of  carbohydrate  fermentation.  It  seems  cer- 
tain, at  least,  that  no  fat  is  consumed  under  anaerobic  condi- 
tions. This  is  not  astonishing,  because  it  seems  hardly  possible 
that  an  anaerobic  process  could  yield  energy  from  an  oxygen 
poor  substance  like  fat    (Weinland,  1901). 

The  nitrogen  metabolism  of  Ascaris  is  not  very  great.  For 
100  gm  of  worms  the  amount  of  nitrogen  excreted  in  24  hours 
was  found  by  Weinland  (1904b)  to  be  15  to  20  mgm  and  by 
V.  Brand  f  1934a)  to  be  29  mgm.  One  third  of  the  excreted  N 
is  ammonia,  and  the  greater  part  of  the  remainder  can  be 
precipitated  by  phosjjhotungstic  acid  (Weinland,  1904b).  Flury 
(1912)  found  that  the  worms  excreted  not  only  ammonia  but 
small    amounts    of    amine    bases,    substances    which    gave    the 


biuret  reaction,  hydrogen  sulfide  (also  Kniger,  1936),  and 
mercai)tan.  According  to  v.  Brand  (1934a)  about  one  fourth  of 
the  total  excreted  N  is  contained  in  discharged  eggs.  Chitwood 
(1938)  found  urea  in  a  concentration  of  about  0.02  percent  in 
the  tiuid  from  the  excretory  pore  of  freshly  collected  worms. 
.\ftcr  24  hours  of  starvation  the  tests  for  urea  were  negative, 
and  Chitwood  doubts  that  the  urea  was  formed  by  the  worm. 
It   may   have   been   obtained    from    the   host. 

METABOLISM  UNDER  AEROBIC  CONDITIONS 

Weinland  (1901)  believed  that  Ascaris  did  not  consume  oxy- 
gen. However,  he  did  observe  that  more  carbon  dioxide  was 
evolved  under  aerobic  than  under  anaerobic  conditions.  He 
explained  this  on  the  assumption  that  the  extra  carbon  dioxide 
was  due  eitlier  to  the  metabolism  of  ;ierobically  developing  eggs 
or  to  that  of  an  aerobic  bacterial  flora.  His  view  was  generally 
accepted  until  Adam  (1932)  proved  that  Ascaris  was  able  to 
consume  oxygen.  The  observations  of  Adam  were  soon  con- 
firmed and  extended  to  other  forms.  The  following  table  sum- 
marizes some  of  these  data  on  oxygen  consumption. 


O2  consumption  in 
gm  per  100  gm 
worms   in   24  hrs. 


Species 

Sex 

at 

body  temp. 

Investigator 

Ascaris  lumhricoides  __ 

-  S 

0.38 

Adam,  1932 

Ascaris  lumhricoides  __ 

-  9 

0.21 

Adam,  1932 

Ascaris  lumbricoides  . 

.  2 

0.21 

V.  Brand,  1934 

Ascaris  lumbricoides  „ 

-  9 

0.13 

f  Harwood   and 

Ascaris  luvibricoides  - 

-S 

0.21 

\  Brown,    1934 

Ascaris  lumbricoides  .. 

? 

0..1n* 

Kruger,    1936 

Ascaris  lumbricoides  .. 

? 

0.27* 

Kruger,   1936 

Parascaris    equoruin  .. 

-9 

0.08 

Toryu,    1936 

Parascaris    equorum.. 

-S 

0.35 

Toryu,    1936 

Setaria   equiviim    

? 

0.89 

Toryu,    1936 

Ancyloslomn  caninum 

Lj 

more  than  ten  times 

Harwood  and 

as 

much 

as   female 

Brown,    1934 

Ascaris 

The  oxygen  consumption  of  both  Setaria  and  Ancylostoma  is 
considerably  higher  than  that  of  Ascaris  or  Parascaris.  The 
former  undoubtedly  have  easier  access  to  oxygen  and  may 
therefore  be  better  adapted  to  aerobic  metabolism. 

The  amount  of  oxygen  consumed  by  Ascaris  is  influenced  by 
several  factors.  One  factor  is  size,  and  small  animals  consume 
relatively  more  than  large  ones.  However,  it  is  doubtful  if  the 
difference  in  oxygen  consumption  of  males  and  females  can  be 
explained  merely  on  the  basis  of  size.  Kruger  (1936)  gave  a 
formula  which  allows  one  to  calculate  approximately  the  in- 
crease of  oxygen  consumption  with  increasing  weight.  The 
formula  is  applicable  only  to  worms  which  weigh  over  1.4  gm. 
In  smaller  worms  the  increase  is  more  rapid.  Kruger  stated 
nothing  about  the  sex  of  his  worms,  but  the  deviation  of  his 
data  from  the  formula  begins  near  the  average  weight  of  males. 
In  a  recent  paper  Kruger  (1940)  shows  that  the  0=  consump- 
tion of  ascarids  of  various  sizes  is  fairly  constant  if  referred 
to  surface  rather  than  weight. 

The  oxygen  consumption  of  starving  ascarids  kept  for  long 
periods  of  time  at  the  oxygen  tension  of  air  show  a  general 
tendency  to  increase  (v.  Brand,  1934a;  Kriiger,  1937).  This 
might  be  an  indication  of  adaptation  to  the  abnormally  high 
oxygen    tension. 

The  oxygen  consumption  of  Ascaris  varies  directly  with  the 
oxygen  tension,  regardless  of  whether  whole  worms,  parts  of 
worms  or  even  minced  material  is  used  (Harnisch,  1933; 
Kriiger,  1936).  This  is  a  striking  contrast  to  what  is  known 
from  massively  built  free-living  organisms,  like  aetiuians.  In 
these  a  similar  dependence  is  observed  in  whole  animals,  but 
it  disappears  if  minced  material  is  used.  The  diffusion  rate 
of  oxygen  is  the  limiting  factor,  and  if  the  path  through  which 
oxygen  has  to  diffuse  is  shortened  by  using  minced  animals,  the 
oxygen  consumption  remains  virtually  unchanged  over  a  wide 
range  of  tensions.  This  explanation  can  not  hold  for  Ascaris. 
Harnisch,  however,  has  found  that  the  oxygen  consumption  of 
planarians  and  Chironomus  larvae,  which  is  normally  indepen- 
dent of  oxygen  tension,  may  become  dependent  if  the  animals 
are  subjected  to  anaerobic  conditions  prior  to  the  experiments. 
In  his  opinion  two  kinds  of  aerobic  processes  must  be  dis- 
tinguished: (1)  a  primary  aerobic  process  which  is  considered 
to  be  independent  of  the  oxygen  tension,  and  (2)  a  secondary 
process  which  is  considered  to  be  dependent.    In  Ascaris  only 

'ICriiger  (1936)  gives  data  of  various  sized  worms.  Those  for  worms 
of  about  the  average  size  of  males  and  females  have  been  introduced  in 
the  table,  the  higher  figure  being  for  worms  of  1.5  gm.  the  lower  for 
worms    of    4. .5    gm. 


363 


the  secondary  aerobic  process  is  present.  Harnisch  (1937)  of- 
fered support  of  this  view  in  the  observation  that  washed 
minced  Ascaris  material  has  only  a  negligible  oxygen  consump- 
tion. The  same  material,  suspended  in  Ascaris  body  fluid,  has 
a  very  high  oxygen  consumption  and  surpasses  even  that  of 
non-minced  material.  According  to  Harnisch  this  indicates  the 
presence  of  a  powerful  oxidizing  mechanism  outside  of  the  cells 
which  may  govern  the  entire  aerobic  processes  of  Ascaris. 
This,  he  claims,  is  in  accordance  with  his  explanation  of  ex- 
periments with  artificially  induced  secondary  aerobic  processes 
in  Chlronomiis.  The  cellular  agents  which  govern  the  primary 
aerobic  processes  in  Chironomns,  however,  could  not  be  re- 
moved from  the  cells  by  washing   (Harnisch,  1936). 

The  data  of  Kempner  (1937)  show  that  in  a  variety  of  bio- 
logical materials  the  effect  of  oxygen  tension  on  oxygen  con- 
sumption varies  with  pH,  CO2  tension,  salt  content,  and  tem- 
perature. It  is  apparent  that  certain  tissues  heretofore  con- 
sidered to  have  a  respiratory  mechanism  unaffected  by  oxygen 
tension  reallj'  show  an  independence  only  in  alkaline  COa-free 
media  in  a  certain  temperature  range.  These  observations  of 
Kempner  indicate  that  the  whole  question  of  oxygen  tension 
versus  oxygen  consumption  should  be  reexamined,  and  that  the 
respiration  of  no  material  can  be  said  to  be  completely  de- 
pendent or  independent  of  O2  tension  unless  the  effects  of  the 
above  factors  have  been  investigated.  It  is  possible  that  these 
factors  may  have  some  effect  on  the  nematode  data  discussed 
above.  A  discussion  of  the  theoretical  relationship  between 
oxygen  tension  and  oxvgen  consumption  is  given  by  Marsh 
(1935). 

It  seems  that  all  the  different  organs  of  Ascaris  are  able 
to  consume  oxygen.  This  has  been  shown  for  the  body  wall, 
intestine,  ovaries,  uterus  and  even  the  body  fluid  (Harnisch, 
1935,  1937;  Kriiger,  1936).  The  largest  absolute  amount  is 
consumed  by  the  body  wall,  although  the  intestine  shows  the 
highest  rate  of  oxygen  consumption. 

It  is  now  generally  believed  that  ascarids  evolve  larger 
amounts  of  carbon  dioxide  under  aerobic  than  under  anaerobic 
conditions  (Weinland,  1901;  v.  Brand,  in34a;  Kriiger,  1936), 
and  Harnisch  (1937)  has  abandoned  his  previous  contention  to 
the  contrary.  The  respiratory  quotient  in  air  is  consistently 
very  high.  In  fresh  worms  it  may  be  about  4  or  even  higher, 
and  in  worms  kept  for  several  days  in  saline  it  is  between  1.27 
and  1.88  (Kruger,  1937).  This  indicates  that  the  oxidation  of 
metabolites  is  not  complete  and  that  even  in  the  presence  of 
oxygen  the  metabolism  consists  in  part  of  anaerobic  fermenta- 
tions. 

The  excretion  of  organic  acids  under  aerobic  conditions,  fiist 
seen  by  Weinland  (1901),  is  definite  proof  of  the  presence  of 
fermentations.  The  acids  have  been  identified  as  small  amounts 
of  lactic  acid  (v.  Brand,  1934a),  formic,  acetic,  and  probably 
butyric  acid,  a  large  amount  of  valeric  acid  and  some  unidenti- 
fied higher  acids  (Oesterlin,  1937).  Since  these  products  are 
similar  to  those  formed  under  anaerobic  conditions  (see  above), 
it  seems  likely  that  the  fermentations  going  on  under  aerobic 
and  anaerobic  conditions  are  identical.  The  amounts  of  acids 
excreted  at  the  oxygen  tension  of  air  are  definitely  lower  than 
under  strictly  anaerobic  conditions  (v.  Brand,  1934a;  Kruger, 
1936,  1937),  but  at  low  oxygen  tensions  even  more  acids  are 
excreted   (Kruger.  1936). 

It  is  customary  in  the  nematode  literature  to  refer  to  the 
oxidations  which  involve  oxygen  consumption  and  which  lead 
to  the  production  of  carbon  dioxide  and  water  as  oxidative 
metabolism  and  to  refer  to  the  molecular  rearrangements  and 
oxido-reductions  which  lead  to  the  production  of  carbonic, 
lactic,  valeric,  and  other  acids  and  in  which  oxygen  is  not  con- 
sumed as  fermentative  metabolism.  Von  Brand  (1934a)  and 
Kruger  (1937),  by  basing  calculations  on  the  ratio  of  anaero- 
bically  evolved  carbon  dioxide  to  anaerobically  excreted  acids 
or  similar  data  at  low  oxygen  tensions,  calculated  the  amounts 
of  aerobically  evolved  carbon  dioxide  which  originated  in  fer- 
mentative and  in  oxidative  metabolism.  This  latter  figure  was 
used,  in  connection  with  the  oxygen  consumption,  to  calculate 
the  true  respiratory  quotient  which  was  found  to  be  about  0.9 
or  1.0.  In  some  cases  very  low  quotients  were  found,  and  these 
data  are  difficult  to  explain  at  the  present  time.  The  opinion 
of  Harnisch  (1933)  that  the  aerobic  processes  do  not  lead  to 
the  production  of  CO2  and  that  the  respiratory  quotient  is 
zero  has  been  generally  abandoned. 

Kruger  (1936)  found  that  the  uncorrected  respiratory  quo- 
tient of  ascarids  kept  in  air  instead  of  saline  fell  rapidly  to 
about  1.0  and  remained  at  this  level  for  some  time.  This  would 
indicate  (Kriiger,  1937)  either  that  the  fermentations  cease 
altogether,  or  that  the  fermentations  present  do  not  lead  to 
carbon  dioxide  production    (e.g.,  lactic  acid  formation). 

The  question  of  what  substances  are  oxidized  has  received 
some  attention  by  v.  Brand  (1934a).  He  found  that  under 
aerobic    conditions    somewhat    less    glycogen    is    consumed    than 


under  anaerobic  ones.  On  an  assumption  similar  to  that  made 
above  for  the  carbon  dioxide,  he  calculated  the  amounts  of  the 
consumed  glycogen  which  had  apparently  been  decomposed  by 
fermentative  and  by  oxidative  metabolism.  He  arrived  at  the 
following  balances: 

Uncorrected   balance   for   100   gm   worms   starving  at   37°   C. 
under   aerobic   conditions: 

Decomposed:    1.18  gm  glycogen.    Consumed:   0.21  gm  oxy- 
gen.   End  products:   0.84  gm  carbon  dioxide  +  0.10  gm 
valeric   acid    +    0.01    gm   lactic   acid. 
Oxidative  part  of  the  metabolism: 

Decomposed:   0.37  gm  glycogen.    Consumed:   0.21  gm  oxy- 
gen.   End  products:    0.34  gm  carbon  dioxide  +    ?. 
Fermentative   part   of   the   metabolism: 

Decomposed:  0.86  gm  glycogen.  End  products:  0.48  gm 
carbon  dioxide  +  0.16  gm  valeric  acid  +  0.01  gm  lactic 
acid. 
The  amount  of  glycogen  which  disappeared  was  so  great  that 
complete  oxidation  to  carbon  dioxide  and  water  could  not  be 
assumed  for  all  of  that  which  was  calculated  to  undergo  oxida- 
tive metabolism.  Probably  only  a  partial  oxidation  takes  place 
(formation  of  aldehydes?). 

Harnisch  (1935)  thought  that  possibly  isovaleric  acid  would 
be  oxidized  to  aceto  acetic  acid  or  ^Q  hydroxy-butyric  acid  which 
in  turn  would  lie  decomposed  to  acetone  and  carbon  dioxide. 
However,  chemical  determinations  on  the  excreta  do  not  favor 
this  view.  This  statement  applies  also  to  v.  Brand's  (1934a,  b) 
original  theory  that  fats  may  be  changed  into  carbohydrate. 

It  seems  as  if  Ascaris,  in  contrast  to  many  free  living  ani- 
mals, does  not  contract  a  noticeable  oxygen  debt  during  a  pe- 
riod of  anaerobiosis  (Adam,  1932;  Harnisch,  1933).  It  was 
found  (v.  Brand,  1937b),  however,  that  ascarids  sub.iected  to 
20  hours  anaerobiosis  and  then  brought  for  2  to  6  hours  into 
aerobic  conditions,  resynthesized  1/20  to  1/10  of  th"  glycogen 
consumed  during  the  anaerobic  period.  This  resynthesis  is  clear- 
ly an  aerobic  process,  and  it  is  apparently  much  l"ss  pronou"""d 
in  Ascaris  than  in  similarly  treated  vertebrate  muscles.  This 
may  be  due  to  the  fact  that  in  vertebrate  muscle  the  end  nrnd- 
ucts  accumulate,  whereas  in  Ascaris  they  are  excreted,  and  only 
those  present  in  the  liody  at  the  beginning  of  the  aerobic  period 
are  available  for  resynthesis.  It  is  unknown  whether  lactic  acid 
or  the  lower   fatty  acids  are  resynthesized   to   glycogen. 

There  is  still  some  controversy  concerning  the  .significance  of 
the  aerobic  processes  of  Ascaris.  Harnisch  (1933)  assumed  that 
the  aerobic  processes  would  yield  no  energy,  and  he  still  thinks 
(Harnisch,  1935)  that  thev  play  no  role  in  the  normal  energy 
supply  of  the  organism.  This  view  is  similar  to  that  of  Kriiger 
(1937)  who  states  that  they  are  probably  not  linked  to  any 
specific  organ  function  and  that  any  derived  energy  is  prob- 
ably wa.sted.  The  present  writers  are  of  the  opinion  that  at 
Hiis  time  no  definite  statements  regarding  the  possible  utiliza- 
tion of  this  energy  can  be  made. 

The  fact  that  the  rate  of  the  fermentative  processes  is  re- 
duced at  the  oxygen  pres.sure  of  air,  seems  to  indicate  rather 
clearly  that  fermentations  and  oxidations  are  not  entirely  inde- 
pendent as  Harnisch  (1933)  originally  assumed.  Whether  Krii- 
ger's  (1937)  view  is  correct  that  the  oxidations  follow  essen- 
tially the  same  course  as  in  truly  aerobic  organisms,  or  whether 
Harnisch  (1937)  is  right  in  assuming  that  they  correspond  only 
to  the  secondary  aerobic  processes  occurring  in  free  living  ani- 
mals only  under  sjiecial  conditions,  must  be  decided  by  future 
investigations. 

The  aerobic  metabolism  of  Parascaris  eqvoriim  has  been 
studied  by  Toryn  (1934  to  1936b).  He  found  an  almost  identi 
cal  glycogen  consumption  under  aerobic  and  anaerobic  condi- 
tions, but  since  the  worms  excreted  slightly  less  organic  acids 
under  aerobic  conditions,  he  concluded  that  a  small  amount  of 
glycogen  was  oxidized.  Apparently  the  aerobic  metabolism 
of  Parascaris  follows  the  same  pattern  as  that  of  Ascaris. 

The  question  of  whether  or  not  parasitic  nematodes  use  fat  nn 
der  aerobic  conditions  is  difficult  to  answer  satisfactorily  at  the 
present  time.  In  v.  Brand  (1934a)  aerobic  experiments  no  fat 
was  used.  In  view,  however,  that  his  experiments  lasted  only  24 
hours  and  that  in  general  carbohydrate  is  consumed  before  the 
fat  reserves  are  attacked,  these  experiments  can  not  be  accepted 
as  conclusive  evidence  that  no  fat  may  be  used  during  longer 
periods  of  starvation.  JIneller  (1928/29)  observed  that  in  ex- 
planted  pieces  of  Ascaris  a  loss  of  morphologically  demonstrable 
fat  occurred  after  several  days,  and  Hirsch  and  Bretschneider 
(1937)  have  shown  that  in  starving  ascarids  much  of  the  stain 
able  fat  disappeared  from  the  intestinal  cells  after  6  days. 
These  observations  are  suggestive  that  fat  may  be  used,  but 
they  should  be  confirmed  by  quantitative  chemical  methods.^ 
Bondony  (1910)  detected  a  lipase  in  Strongijlus  eqitintis,  and 
the  possible  significance  of  its  presence  warrants  further  study. 

iln  a  recent  paper  v.  Brand   (1914)   showed  that  Ascnrin  uses  no  fat 
for  production  of  energy  during  an  aerobic  starvation  period  of  5  day». 


364 


Tlic  aoi'obio  :iiul  aiiat'roliii'  iiitiogt'ii  iiu'talMilism  of  Axcari.i 
has  been  compaiod  by  v.  Brand  (l!i34a).  The  amounts  of  nitro- 
gen excreted  both  in  sohible  exereta  and  in  eggs  were  very 
nearly  identical  in  both  cases.  He  assumed  that  at  least  a 
large  part  of  the  X  metabolism  was  involved  in  the  transforma- 
tion of  the  protoplasm  of  the  body  into  that  of  eggs.  He  also 
considered  it  likely  that  at  least  a  large  i)art  of  the  nitrogen 
metabolism  was  always  anaerobic.  This  view  is  supported  by 
the  fact  that  free-living  animals,  like  tlie  leeches,  show,  in 
contrast  to  Ascarix,  a  marked  dift'erence  in  the  amount  of  nitro- 
gen e.\creted  under  aerobic  and  under  anaeroliic  conditions. 

DEDUCTIONS   CONCERXIXG   TIIK    MKTABOLISM 

IX  riro 

Deductions  concerning  the  nature  of  the  metaliolism  of  in- 
ternal parasites  can  be  drawn  only  from  the  chemical  composi- 
tion of  their  surroundings  and  their  metabolism  in  vitro.  Of 
special  interest  is  the  question  of  whetlier  the  nematodes  para- 
sitizing the  intestine  lead  an  anaerobic  or  an  aerobic  life.  On 
the  basis  of  the  investigations  of  Bunge  (LSSJ))  and  Weinland 
(1901)  the  first  possibility  was  accepted  for  many  years  as  an 
undisputed  fact.  More  recently  certain  investigators  (Slater, 
192.');  Mueller,  1928/29;  Adam,  1932;  Davey,  1938a  and  b) 
have  held  the  opposite  view,  i.e.,  that  tlie  worms  can  get  enough 
oxygen  in  the  intestine  to  allow  an  oxidative  metabolism.  Re- 
cently V.  Brand  (193S)  has  reviewed  the  question,  and  he  be- 
lieves that  a  general  answer  can  not  be  given.  Api)arently  the 
size  or  relative  surface  and  the  presence  of  respiratory  pigments 
will  have  a  great  influence  on  whether  a  worm  can  or  can  not 
obtain  sufficient  oxygen  at  the  low  tensions  prevailing  in  the 
intestine.  Large  parasites,  like  Ascaris  or  Parascaris,  must  be 
regarded  as  predominantly  anaerobic  organisms.  As  mentioned 
above,  the.v  show  a  marked  fermentative  metabolism  even  in 
air.  Since  their  oxygen  consumption  is  dependent  on  the  oxygen 
pressure,  one  can  be  reasonably  sure  that  fermentative  metabo- 
lism will  be  relatively  much  greater  in  the  intestine.  Further 
signs  of  their  adaptation  to  an  anaerobic  life  are  that  the.v 
are  remarkably  resistant  to  the  lack  of  oxygen  in  vitro  and 
that  they  are  able  to  excrete  the  end  products  of  anaerobic 
metabolism.  It  seems,  however,  quite  possible  that  the  small 
amounts  of  oxygen  available  in  the  intestine  are  not  entirely 
without  significance.  This  may  be  indicated  by  the  observations 
that  the  worms  contain  some  haemoglobin,  that  stimulated 
Ascaris  die  much  more  rapidly  in  absence  than  in  presence  of 
oxygen,  and  finally  that  they  are  able  to  perform  under  suitable 
conditions  such  a  clearly  aerobic  process  as  the  resynthesis  of 
gl.veogen. 

Small  nematodes,  on  the  other  hand,  offer  better  opportuni- 
ties for  the  diffusion  of  oxygen  because  of  their  relatively 
larger  surface.  This  may  explain  why  the  sheep  nematodes  do 
not  show  (Davey,  1937,  1938a  and  b)  the  same  resistance 
against  lack  of  oxygen  as  Ascaris.  The  conclusion  of  Davey 
that  these  worms  lead  an  aerobic  life  under  natural  conditions 
is,  therefore,  probably  only  in  apparent  contradiction  with  the 
statement  made  above  in   regard  to  large  helminths. 

An  entirel.y  different  way  of  getting  oxygen  may  be  realized 
in  worms  sucking  larger  amounts  of  blood  from  their  hosts. 
According  to  Wells  (1931)  the  blood  sucking  activities  of  hook- 
worms seem  to  serve  largely  as  a  respiratory  function.  His  data 
allow  the  calculation  that  under  optimal  conditions  100  gm  of 
worms  could  obtain  20  gm  of  oxygen  from  this  source  in  24 
hours.  This  would  be  about  ten  times  as  much  as  Harwood  and 
Brown   (1934)   found  to  be  the  actual  oxygen  consumption. 

No  data  are  known  about  the  metabolism  of  adult  parasitic 
nematodes  which  normally  live  outside  the  intestine.  It  is  there- 
fore unnecessary  to  enter  into  a  similar  discussion  concerning 
their  metabolism.  On  the  whole  one  may  assume  that  they  will 
have  frequently,  though  probably  not  in  every  case,  better  op- 
portunities to  get  larger  amounts  of  oxygen  than  the  intestinal 
helminths. 

SYNTHESIS  OF  RESERVE  SUBSTANCES 

There  are  only  a  few  investigations  which  concern  the  ques- 
tion of  the  synthesis  of  reserve  substances  in  parasitic  nema- 
todes. Hoffman  (1934)  and  Kriiger  (1936)  have  shown  that 
the  heat  production  and  the  o.xygen  uptake  of  ascarids  under 
both  anaerobic  and  aerobic  conditions  are  increased  if  sugar  is 
present  in  the  surrounding  medium.  Hirsch  and  Bretschneider 
(1937)  fed  ascarids  iron  saccharate  and  concluded  from  their 
histological  investigation  that  it  was  absorbed  as  colloid  and 
broken  down  only  in  a  certain  part  of  the  intestinal  cells  into 
iron   and   sugar. 

Quantitative  determinations  of  the  glycogen  content  of  car- 
bohydrate-fed ascarids  have  been  performed  by  Weinland  and 
Ritter  (1902).  They  found  no  increase  in  the  glycogen  con- 
tent of  animals  kept  in  solutions  containing  various  carbohy- 


drates, altliough  glucose  caused  a  lowering  of  the  rate  of  utili- 
zation of  body  glycogen.  More  positive  results  were  achieved 
by  injecting  the  sugar  solutions  into  the  animals.  In  these  ex- 
periments new  glycogen  was  foJined  after  injection  of  glucose 
and  probably  levulose.  The  consumption  of  body  glycogen  was 
decreased  by  injections  of  maltose  and  perhaps  galactose,  but 
not  by  injections  of  hictose. 

Von  Brand  and  Otto  (1938)  compared  the  glycogen  content 
of  hookworms  from  dogs  which  had  been  starved  for  48  to  72 
hours  before  death  with  those  from  dogs  which  had  been  given 
so  much  sugar  during  a  similar 'period  that  the  liver  glycogen 
rose  from  0.06  percent  to  .").04  percent.  No  difference  what- 
ever in  glycogen  content  of  the  worms  was  found.  This  may  be 
related  to  the  fact  that  hookworms  obtain  their  food  from  the 
tissues  rather  than  from  tho  lumen  of  the  intestine  and  there- 
fore can  gain  their  maximal  food  requirements  even  from  a 
starving    host. 

So  far  no  experiments  have  been  performed  on  the  deposition 
of  fat  in  parasitic  nematodes  except  the  above  mentioned  doubt- 
ful results  of  Schulte  (1917)  concerning  the  fat  increase  in 
ascarids  under  anaerobic  conditions.  The  whole  question  of 
synthesis  should  prove  interesting  for  future  investigations. 

Metabolism  of  Eggs  and  Larvae 

The  eggs  of  many  parasitic  nematodes  show,  like  the  adults, 
a  surprising  degree  of  resistance  to  lack  of  oxygen.  The  eggs 
of  such  forms  as  Anci/lostoma,  Parascaris,  Trichoccphalus  or 
yematodiriis  can  be  kept  for  days  or  even  weeks  in  the  absence 
of  oxygen,  but  they  do  not  complete  their  development  (Looss, 
1911;"Bataillon,  19*10;  Zawadowski,  1916;  Faure-Fremiet,  1913; 
Zawadowski  and  Orlow,  1927 ;  Zviaginzev,  1934 ;  Dinnik  and 
Dinnik,  1937).  In  Parascaris  oxygen  is  unnecessary  only  during 
the  early  stages,  i.e.,  maturation,  fertilization  and  perhaps  the 
first  cleavage  stages;  for  further  development  oxygen  is  indis- 
pensable (Faure-Fremiet,  1913;  Szweikowska,  1929;  Dyrdow- 
ska,  1931).  The  need  of  oxygen  for  completion  of  development 
seems  to  be  a  general  requirement,  although  the  stage  of  de- 
velopment at  which  oxygen  becomes  necessary  seems  to  vary 
somewhat  with  different  species.  Zawadowsky  and  Schalimow 
(1S29),  Schalimow  (1931),  and  Wendt  (1936)  conclude  that 
the  necessity  for  oxygen  begins  in  Enterobius  vermicularis 
with  the  tadpole  stage,  and  in  Oxi/iiris  eqni  with  the  gastrula 
stage.  Relatively  low  oxygen  pressures,  however,  are  sufficient 
to  insure  normal  development  in  Ascaris  and  Ancylostoma 
(Brown,   1928;    McCoy,   1930). 

The  amount  of  oxygen  consumed  by  one  Ascaris  egg  in  de- 
veloping from  the  one-cell  stage  to  the  motile  embryo  is  about 
0.002.5  cmm  with  only  slight  variations  whether  the  develop- 
ment is  completed  in  "21  days  at  23°C  or  in  11  days  at  30°C 
(Brown,  1928).  Huff  (1936)  obtained  a  value  of  0.0041  cmm 
for  Ascaris,  and  Nolf  (1932)  obtained  a  value  of  0.0027  for  the 
eggs  of  Trichuris.  It  is  surprising  that  an  Ancylostoma  egg  re- 
quires for  its  development  from  the  morula  stage  to  the  fully 
developed  larva  almost  exactly  the  same  amount  of  oxygen 
(0.0028  cmm  at  23°  C.  according  to  McCoy,  1930)  as  an  As- 
caris egg,  although  development  of  Ancylostoma  is  completed 
in  about  24  hours.  Since  these  eggs  are  about  the  same  size, 
it  seems  as  if  the  difference  in  the  rate  of  oxygen  consumption 
mentioned  above  for  the  adults  of  these  species  is  also  present 
in  the  embryonic  stages. 

Huff  (1936)  observed  that  the  o.xygen  consumption  of  As- 
caris eggs  increased  more  than  five  times  after  removal  of  the 
albuminous  coating  by  antiformin.  Friedheim  (1933)  found 
that  the  oxygen  consumption  of  Ascaris  eggs  is  considerably 
increased  if  they  are  immersed  in  a  dilute  solution  of  hallo- 
chrome  (a  pigment  which  is  a  reversible  oxidation-reduction 
system  isolated  from  the  polychaete  worm  Halla  parthenopea 
and  which  has  an  aceelcrative  eft'eet  on  respiration).  The  mech- 
anism of  the  increase  in  respiration  by  either  of  these  two 
methods  is  not  known.  Friedheim  (1933)  apparently  used  mixed 
stages  of  fertilized  eggs,  and  there  seems  to  be  no  reason  for 
assuming  that  hallochrome  could  penetrate  the  egg  shell.  There- 
fore, one  might  expect  the  acceleration  obtained  to  be  due  to 
an  increase  in  the  effective  oxygen  tension  or  to  an  increase 
of  respiration  in  only  those  eggs  on  which  an  impermeable  shell 
had  not  yet  been  formed.  The  experiments  of  Huff  might  also 
be  explained  as  being  caused  by  an  increase  in  effective  oxygen 
tension  because  of  slow  diffusion  of  oxygen  through  the  albumi- 
nous coat,  but  no  data  concerning  these  possibilities  are  avail- 
able. Since  the  R.  Q.  is  always  less  than  1.0  (see  below)  the 
possible  effect  of  oxygen  tension  could  not  be  merely  to  change 
the  ratio  of  oxidative  and  fermentative  metabolism.  The  ac- 
celerations produced  by  Friedheim  (1933)  and  Huff  (1936) 
must,  for  the  present,  be  accredited  to  changes  in  the  rate  of 
oxidative  metabolism,  and  the  reasons  for  the  changes  re- 
main obscure. 


36S 


The  oxygen  consumption  of  Ascaris  or  Farascaris  eggs  has 
also  been  reduced  experimentally  by  ultraeentrifuging  and  by 
exposure  to  cyanide  (Zawadowsky,  1926;  Huff  and  Boell,  1936). 
About  90  percent  of  the  respiration  was  sensitive  to  cyanide, 
and  it  seemed  that  ultraeentrifuging  affected  only  the  cyanide 
sensitive  respiratory  mechanism. 

The  respiratory  quotient  of  Farascaris  and  Ascaris  eggs  has 
been  found  to  be  below  1,  and  this  indicates  that,  in  contrast 
to  results  on  tissues  of  the  adult  worm,  no  fermentative  proc 
esses  are  present  in  the  eggs.  The  respiratory  quotient  deter- 
mined at  the  beginning  of  development  was  about  .80,  and. 
with  some  variations  in  the  ease  of  Farascaris,  it  increased 
during  the  later  stages  to  .92.98  (Faure-Fremiet,  1913a,  1913; 
Huff,  1936).  The  total  energy  liberated  by  one  Farascaris  dur- 
ing its  development  was  50  x  10"  cal.  (Faure-Fremiet,  1913). 
Nolf  (1932)  found  that  the  R.  Q.  of  Trichuris  decreased  from 
a  value  of  1.0  for  the  first  5  days  of  development  to  a  value  of 
0.73  for  the  8th  to  ir)th  days.  " 

In  considering  the  chemical  changes  which  occur  in  the  eggs 
of  parasitic  nematodes  during  their  development,  one  must 
distinguish  clearly  between  processes  which  lead  to  the  forma- 
tion of  the  egg  shells  and  ijrocesses  which  liberate  energy. 
The  shells,  as  far  as  they  are  formed  from  the  ovum,  consist 
essentially  of  the  shell  proper  and  the  vitelline  membrane.  The 
shell  is  composed  of  chitin  in  such  species  as  Farascaris,  Ascaris. 
Dioctophyma  and  Enterobius  (Faure-Fremiet,  1913;  Szwejkow- 
ska,  1929 ;  Schmidt,  1936  ;  Wottge,  1937  ;  Chitwood,  1938 ;  Jacobs 
and  Jones,  1939).  The  investigations  of  Faure-Fremiet  (1913) 
and  Szwejkowska  (1929)  have  demonstrated  that  in  Ascaris 
about  half  the  glycogen  stored  in  the  oocytes  was  used  to  form 
the  glucosamine  incorporated  in  the  chitin.  The  latter  has 
shown  in  addition  that  26  percent  of  the  total  nitrogen  of  the 
egg  was  used  during  the  chitin  formation. 

The  vitelline  membrane  of  the  eggs  of  these  and  other  species 
is  of  a  lipoid  nature  (Faure-Fremiet,  1913;  Zawadowsky,  1928). 
Faure  Fremiet  considered  it  to  be  mainly  ascaryl  alcohol, 
Wottge  (1937)  obtained  a  positive  reaction  for  cholesterol. 
and  Chitwood  (1938)  and  Jacobs  and  Jones  (1939)  demon- 
strated that  it  gave  sterol  reactions.  During  the  secretion  of 
this  layer  certain  changes  in  the  chemical  nature  of  the  ether 
soluble  substances,  perhaps  a  saponification,  seemed  to  occur. 
The  necessity  for  further  studies   is   indicated. 

Chemical  analyses  of  the  egg  indicate  that  both  glycogen  and 
fat  are  oxidized,  and  these  data  are  in  accordance  with  the 
above  data  on  the  respiratory  quotient.  Swejkowska  (1929) 
found  in  Farascaris  eggs  jnst  after  fertilization  about  0.46 
percent  volatile  fatty  acid  and  0..53  percent  higher  fatty  acids. 
After  formation  of  the  second  polar  body  these  suli- 
stances  had  diminished  to  0.34  and  0.36  percent  re- 
spectively. For  the  same  period  it  was  calculated  that 
in  addition  to  the  glycogen  used  in  the  formation  of  chitin  an 
amount  of  glycogen  corresponding  to  about  2.7  percent  of  the 
egg  weight  had  disappeared.  From  Faure  Fremiet 's  (1912, 
1913)  experinients  it  would  appear  that  both  fat  and  glycogen 
were  used  during  the  later  developmental  stages.  All  of  these 
experiments  were  conducted  under  aerobic  conditions.  Dyrdowska 
(1931)  found  by  the  use  of  staining  methods  that  the  glycogen 
content  of  Farascaris  eggs  kept  under  anaerobic  conditions  un- 
derwent a  slight  diminution  and  that  there  was  a  marked  de- 
crease in  the  fat  content.  It  seems  desirable  that  this  decrease 
in  fat  content  should  be  verified  with  quantitative  chemical 
methods  since,  as  already  stated  above,  it  is  difficult  to  under- 
stand how  processes  which  liberate  energy  from  fat  could 
occur  in  the  absence  of  oxygen.  It  should,  furthermore,  be 
remembered  that  Faure-Fremiet  (1913)  gained  the  impression 
that  the  amount  of  fat  in  anaerobically  kept  eggs  tended  to 
increase. 

With  the  exception  of  the  above  mentioned  shifting  of  nitro 
gen  from  the  ovum  to  the  chitin  shell,  nothing  is  known  about 
the  nitrogen  metabolism  of  eggs.  Szwe.ikowska  (1929)  found 
no  change  in  the  total  nitrogen  content  during  the  time  of 
maturation,  and  Kosmin  (1928)  found  the  same  nitrogen  con 
tent  (1.78  percent)  in  undeveloped  and  developed  eggs.  She 
points  out  that  this  may  be  caused  by  the  impermeability  of 
the  vitelline  membrane  for  protein  degradation  products  which 
consequently  might  accumulate  in  the  interior  of  the  egg  shells. 

The  fully  developed  embryo  of  Ascaris  contains  glycogen, 
even  in  eggs  which  have  been  stored  for  6  months  (Stepanow- 
Grigoriew  and  Hoeppli,  1926).  This  observation  has  a  bearing 
on  Pintner's  theory  (1922)  concerning  the  physiological  reason 
for  the  migration  of  parasitic  worms  through  the  host  body 
prior  to  life  in  the  intestine.  Pintner  was  of  the  opinion  that  the 
chief  function  of  the  migration  was  to  allow  the  worms  to  live 
for  a  time  under  aerobic  conditions.  This  would  allow  them 
to  accumulate  a  glycogen  reserve  which  later  on  would  enable 
them  to  begin  life  in  the  anaerobic  intestine.  The  above  men- 
tioned observation  of  Stepanow-Grigoriew  and  Hoeppli   (1926) 


is  not  what  one  might  expect  on  the  basis  of  this  theory.  How- 
ever, StepanowGriegoriew  and  Hoeppli  (1926)  and  Giovannola 
(1936)  found  a  definite  accumulation  of  glycogen  during  the 
migration. 

The  fact  that  glycogen  is  still  present  in  old  embryos  also 
indicates  that  the  rate  of  metabolism  in  fully  developed  eggs 
is  probably  very  much  lower  than  in  the  developing  eggs,  and 
this  problem  seems  worthy  of  quantitative  consideration. 

The  young  larvae  of  Ascaris,  on  the  other  hand,  have  a  high 
level  of  metabolism,  as  evidenced  by  the  investigation  of  Fen- 
wick  (1938).  He  found  a  preliminary  phase  of  about  half  an 
hour  during  which  the  newly  hatched  larvae  showed  a  low 
oxygen  consumption.  This  he  explained  on  the  assumption 
that  they  had  not  yet  become  sufficiently  adjusted  to  the  new 
environment.  Then  followed  an  intermediate  phase,  lasting 
about  an  hour,  in  which  1,000  larvae  consumed  ]3er  hour  9.3  cmm 
oxygen  at  37°  C.  After  this  the  oxygen  consumption  decreased 
to  a  third  level  (0.928  cmm  per  1,000)  which  was  about  1/10 
that  of  the  second  level.  This  new  rate  of  oxygen  consumption 
was  maintained  throughout  the  rest  of  the  exjicriments.  Fen- 
wick  explained  the  high  rate  of  the  intermediate  stage  on  the 
assumption  that  It  was  caused  by  the  removal  of  an  oxygen 
debt  which  the  larvae  had  contracted  while  living  within  the 
egg  shells.  An  investigation  of  the  respiratory  quotient  of 
eggs  containing  infective  embryos  should  prove  helpful  in  an- 
swering this  question. 

The  rate  of  metabolism  of  Trichinella  larvae,  according  to 
the  data  of  Stannard,  McCoy  and  Latchford  (1938),  was  about 
as  high  as  that  of  Ascaris  larvae  in  the  third  of  Fenwick's 
stages.  At  body  temperature  in  T.vrode  solution  the  Trichinella 
larvae  consumed  2.24  cmm  oxygen  per  mgm  dry  weight  per 
hour.  In  saline  the  value  was  1.70,  and  in  Tyrode  without 
bicarbonate  it  was  1.78.  The  figures  for  1,000  larvae  in  these 
solutions  can  be  calculated  to  be  about  1.12,  O.S,")  and  0.88  cmm 
oxygen  per  hour,  respectively.  The  respiration  was  independent 
of  the  oxygen  tension  in  the  range  of  1  to  100  percent  oxygen. 
It  was  very  sensitive  to  cyanide,  but  was  stimulated  by  carbon 
monoxide  and  paraphenylene  diamine.  The  respiratory  quotient 
of  the  Trichinella  larvae  was  always  above  1,  and  the  averages 
were  from  1.13  to  1.17.  It  seems  probable  that  under  aerobic 
conditions  some  fermentations  may  take  place,  liut  most  of  the 
oxidative  processes  apparently  proceed  to  completion.  Fer- 
mentation alone  was  sufficient  to  keep  the  worms  alive  under 
anaerobic  conditions,  but  apparently  oxygen  was  necessary  for 
enabling  them  to  move. 

The  fermentation  processes  of  the  Trichinella  larvae  are 
very  interesting,  since  they  lead  not  only  to  the  formation  of 
carbon  dioxide  but  to  the  formation  of  other  as  yet  unidentified 
substances  which  are  known  to  be  non  acidic.  In  this  respect 
they  differ  from  all  the  other  helminths.  It  is  remarkable,  fur- 
thermore, that  substances  like  iodoacetate  and  others,  which 
rapidlj'  inhibit  alcoholic  fermentation  or  muscle  glycolysis,  were 
quite  slow  in  their  action  on  the  anaerobic  carbon  dioxide  pro- 
duction of  these  larvae  (Stannard,  McCoy  and  Latchford,  19,38). 
McCoy,  Downing  and  A'an  Voorhis  (1941)  showed  that  radio- 
active phosphorus  fed  to  tlie  host  penetrates  rapidly  into  the 
larvae.  This  observation  indicates  that  tlie  larvae  may  have  an 
active  metabolism  inside  the  cyst. 

The  Trichinella  larvae  are  clearly  aerobic  rather  than  an- 
aerobic organisms.  This  is  also  true  for  the  larvae  of  Enstron- 
(/i/lidcs,  investigated  by  v.  Brand  (1938).  He  found  that  these 
worms  survived  much  longer  under  aerobic  than  under  anaero- 
bic conditions.  One  hundred  grams  of  worms  in  the  presence 
of  oxygen  consumed  0.3  gm  of  glycogen  in  24  hours  at  37°  C, 
and  no  organic  acids  could  be  found.  ITnder  anaerobic  condi- 
tions 0.9  gm  glycogen  was  consumed  and  organic  acids  equiva- 
lent to  30  ce  n/10  acid  were  produced.  The  ratio  between  aero- 
bically  and  anaerobically  consumed  glycogen  was  1:3,  a  ratio 
which  places  these  worms  intermediate  between  most  free- 
living  worms  which  have  ratios  of  about  1  :■"  and  Ascaris  with 
one  of  1.0:1.3. 

The  experiments  mentioned  so  far  were  performed  with  larvae 
which  had  been  living  under  natural  conditions  in  a  host.  From 
free-living  stages  of  parasitic  nematodes  data  are  only  avail- 
able for  Ancfilostonm  caninnni.  McCoy  (1930)  found  that  the 
oxygen  consumption  of  infective  larvae  varied  greatly  with 
the  temperature.  At  7°  C.  it  was  imperceptible,  but  in  the 
range  of  17°  C.  to  42°  C.  the  oxygen  consumption  increased 
about  9  percent  for  every  degree  rise  in  temperature,  and  fol- 
lowed an  exponential  curve,  the  b  constant,  of  which  was 
1.0879.  The  actual  oxygen  consumption  at  37°  C.  corresponded 
to  0.47  cmm  per  1,000  larvae  per  hour,  a  figure  somewhat 
lower,  but  of  the  same  order  of  magnitude  as  those  mentioned 
above  for  Ascaris  and  Trichinella  larvae. 

The  free-living  larvae  of  Xecator  aniericanns,  and  Ancj/losio- 
ma  canininn  seem  to  derive  their  energy  primarily  from  fatty 
substances  stored  in  their  body  (Payne,  1923,  Rogers,  1939), 
and      the      amount      of      fat      demonstrable      seems      to      be 


366 


etiaractcristic  of  the  physiological  age  of  the  larvae 
(Payne,  1923;  Cort,  1925).  A  decrease  in  the  amount  of  fat 
granules  was  also  observed  by  Giovannola  (1936)  in  the  filari- 
form larvae  of  several  species,  especially  'f"  f'^J'  were  kept  at 
37°  C. 

It  seems,  however,  that  these  larvae  also  consume  glycogen. 
Giovannola  (1936)  found  small  amounts  of  glycogen  in  young 
rhabditiform  larvae  of  Necator,  Anci/lostoma  and  Nippostrongy- 
lus,  but  none  in  the  filariform  stages.  A  comparable  observa- 
tion was  made  by  Stepanow-Grigoricw  and  Hoeppli  (1936)  who 
found  glycogen  in  one-  or  two-day  old  filariform  larvae  of 
Strongyloidcs,  but  never  in  three-  to  nine-day  old  larvae. 

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Physiol.,  V.  10:681-697. 

Meier,  W.  1931. — Neuere  Untersuchungen  iiber  die  Warmeent- 
wicklung  der  Spuhviirmer.     Ztsehr.  Biol.,  v.  91:459-474. 

Mueller,  J.  F.  1928-29. — Studies  on  the  microscopical  anato- 
my and  physiology  of  Ascaris  lumbricoides  and  Ascaris 
megalocephala.     Ztsehr.  Zellforsch.,  v.  8:361-403. 

Oesterlin,  M.  1937. — Die  von  oxybiotisch  gehaltenen  Ascari 
den  ausgeschiedenen  Fettsauren.  Ztsehr.  Vergleich.  Physiol., 
v.  25:88-91. 

SCHIMMELPPBNNIG,  G.  1903. — Uber  Ascaris  megalocephala. 
Beitrage  zur  Biologic  uud  physiologischen  Cliemie  dersel- 
ben.  Arch.  Wiss.  &  Prakt.  Tierheilk.,  v.  29:332-376. 

ScHULTE,  H.  1917. — Versuche  iiber  Stoffwechselvorgange  bei 
Ascaris  lumbricoides.     Pfliiger's  Archiv.,  v.  166:1-44. 

Slater,  W.  K.  1925. — The  nature  of  the  metabolic  processes 
in  Ascaris  lumbricoides.    Biochem.  J.,  v.  19:604-610. 

1928. — Anaerobic  life  in  animals.  Biol.  Rev.,  v.  3 : 
303-328. 

ToRTU,  Y.  1934. — Contributions  to  the  physiology  of  the  As- 
caris. II.  The  respiratory  exchange  in  the  Ascaris,  As- 
caris megalocephala  Cloq.  Sc.  Rpt.  Tohoku  Imp.  Univ., 
4th.  Ser.,  v.  9:61-70. 

1935. — Idem.  III.  Survival  and  glycogen  content  of 
the  Ascaris,  Ascaris  megalocephala  Cloq.  in  presence  and 
absence  of  o.xygen.    Ibid.,  v.  10:361-375. 

1936a. — Idem.  IV.  Products  from  glycogen  during 
anaerobic  and  aerobic  existence  of  the  Ascaris,  Ascai'is 
megalocephala  Cloq.     Ibid.,  v.  10:687-696. 

1936b. — Idem.  V.  Survival  and  respiratory  exchange 
of  the  Ascaris,  Ascaris  megalocephala  Cloq.  intercepted 
from  light  in  presence  and  absence  of  oxygen.  Ibid.,  v. 
11:1-17. 


Waechter,  J.  1934.— Uber  die  Natur  der  beim  Stoffwechsel 
der  Spuhviirmer  ausgeschiedenen  Fettsauren.  Ztsehr.  Biol., 
V.  95:497-501. 

Weinland,  E.  1901. — tJber  Kohlehydratzersetzung  ohne  Sauer- 
stoffaufnahme  bei  Ascaris,  einen  tierischen  Garungsprozess. 
Ztsehr.  Biol.,  v.  42:55-90. 

1902. — Uber  ausgepresste  Extrakte  von  Ascaris  lum- 
bricoides und  ihre  Wirkung.     Ibid.,  v.  43:86-111. 

1904a. — Uber  die  von  Ascaris  lumbricoides  ausgeschie- 
denen Fettsauren.    Ibid.,  v.  45:113-116. 

1904b. — Uber  die  Zersetzung  stickstoffhaltiger  Sub- 
stanz  bei  Ascaris.     Ibid.,  v.  45:517-531. 

Weinland,  E.  and  Ritteb,  A.  1902. — Uber  die  Bildung  vou 
Glykogen  aus  Kohlehydraten  bei  Ascaris.  Ztsehr.  Biol., 
V.  43:490-502. 

Wells,  H.  S.  1931. — Observations  on  the  blood  sucking  activi- 
ties of  the  hookworm.  Aiici/lostoma  caninum..  J.  Parasit., 
V.  17:167-182. 

METABOLISM  OF  EGGS  AND  LARVAE 

Bataillon,  E.  1910. — Contribution  a  1 'analyse  experimentale 
des  phenomenes  karyocinetiques  chez  Ascaris  megaloce- 
phala. Arch.  Entwicklungsmeeh.,  v.  30(l):24-44. 

von  Brand,  Th.  1938. — Physiological  observations  on  a  larval 
Euslrongijlides  (Nematoda).     J.  Parasit.,  v.  24:445-451. 

Brown,  H.  W.  1928. — A  quantitative  study  of  the  influence 
of  oxygen  and  temperature  on  the  embryonic  development 
of  the  eggs  of  the  pig  ascarid  (Ascaris  suum  Goeze).  J. 
Parasit.,  v.  14:141-160. 

Chitwood,  B.  G.  1938. — Further  studies  on  nemic  skeletoids 
and  their  significance  in  the  chemical  control  of  nemic 
pests.     Proc.  Helm.  Soc.  Wash.,  v.  5:68-75. 

CORT,  W.  W.  1925. — Investigations  on  the  control  of  hookworm 
disease.  XXXIV.  General  summary  of  results.  Am.  J. 
Hj'g.,  V.  5:49-89. 

DiNNiK,  J.  A.  and  Dinnik,  N.  N.  1937. — Influence  de  la  tem- 
perature, de  1  'absence  d  'oxygene  et  du  desseehement  sur 
les  oeufs  de  Trichoccphabis  Irichiurtis  (L.).  Med.  Para- 
sit. &  Parasitic  Dis.,  v.  5:603-618.  [Russian  with  French 
summary.  ] 

Dtrdowska,  M.  1931. — Recherehes  sur  le  comportement  du 
glycogene  et  des  graisses  dans  les  oeufs  i' Ascaris  megalo- 
cephala a  I'etat  normal  et  dans  une  atmosphere  d 'azote. 
Comp.   Rend.    Soc.    Biol.,    Paris,   v.    108:593-596. 

Faure-Frbmiet,  E.  1912. — Graisse  et  glycogene  dans  le  de- 
veloppement  de  I'oeuf  de  \' Ascaris  megalocephala.  Bull. 
Soc.  Zool.  France,  v.  37:233-234. 

1913a. — Le  cycle  germinatif  chez  \' Ascaris  megalo- 
cephala.    Arch.  Anat.  Micr.,  v.  15:435-757. 

1913b. — La  segmentation  de  I'oeuf  A' Ascaris  au  point 
de  vue  energetique.  Comp.  Rend.  Soc.  Biol.,  Paris,  v. 
75:90-92. 

Fenwick,  D.  W.  1938. — The  oxygen  consumption  of  newly- 
hatched  larvae  of  Ascaris  sutim.  Proc.  Zool.  Soc.  London, 
Ser.  A,  V.  108,  Part  1:85-100. 

FaiEiDHEiM,  E.  A.  H.  1933. — Das  Pigment  von  Halla  partheno- 
pea,  ein  akzessorischer  Atmungskatalysator.  Biochem. 
Ztsehr.,  V.  259:257-268. 

Giovannola,  a.  1936. — Energy  and  food  reserve  in  the  de- 
velopment of  nematodes.    J.  Parasit.,  v.  22:207-218. 

Huff,  G.  C.  1936. — Experimental  studies  of  factors  influencing 
the  development  of  the  eggs  of  pig  ascarid  (Ascaris  suum 
Goeze).    J.  Parasit.,  v.  22:455-463. 

Huff,  G.  C.  and  Boell,  E.  J.  1936.— Effect  of  ultracentrifug- 
ing  on  oxygen  consumption  of  the  eggs  of  Ascaris  .suum, 
Goeze.     Proc.  Soc.  Exp.  Biol.  &  Med.,  v.  34:626-628. 

Jacobs,  L.  and  Jones,  M.  F.  1939. — Studies  on  oxyuriasis. 
XXI.  The  chemistry  of  the  membranes  of  the  pinworm 
egg.     Proc.  Helm.  Soc.  Wash.,  v.  6:57-60. 

KosMiN,  N.  1928. — Zur  Frage  iiber  den  Stickstoffwechsel  der 
Eier  von  Ascaris  megalocephala.  Tr.  Lab.  Exper.  Biol. 
Zoopark,  Moscow,  v.  4:207-218.  [Russian  with  German 
summary.] 


370 


Looss,  A.  inil.— The  aiiatoniy  and  life  liistoiy  of  Anchylo- 
stoma  diiodcnalc  Duj.  Part  II.  The  aevok)pment  in  the 
free  stage.  Rec.  Egypt.  Govt.  Sch.  Med.,  v.  4:163  613. 
[Not  seen.l 

MoCOT,  O.  R.  1930. — The  iiitlueiice  of  teniiieiatuie,  hydrogen- 
ion  eoncentration,  and  oxygen  tension  on  tlie  development 
of  the  eggs  and  hirvae  of  the  dog  liookworm,  Ancylostoina 
canivtim.     Am.  J.  Hyg.,  v.  11:413-448. 

MoCoY,  Q.  E.,  Downing,  V.  F.  and  V.\N  Voorhis,  S.  N.  1941. — 
The  penetration  of  radioactive  phosjihorus  into  encysted 
Trichiticlla  larvae.  J.  Parasit.,  v.  27;."i3  ."iS. 

NOLF,  L.  O.  1932. — Experimental  studies  on  certain  factors 
influencing  the  development  and  vial)iUty  of  the  ova  of 
the  luiman  Tricliuris  as  compared  with  those  of  the  human 
Ascari.f.     Am.  J.  Hyg.  v.   16:288-322. 

Payne,  F.  K.  1923. — Investigations  on  the  control  of  hook- 
worm disease.  XXX.  Studies  on  factors  involved  in  mi- 
gration of  hookworm  larvae  in  soil.  Am.  .1.  Hyg.,  v.  3: 
547-583. 

PiNTNER,  Th.  1922. — Die  vermutliehe  Bedeutung  der  Hel- 
minthenwanderungen.  Sitzungsb.  Akad.  Wiss.  Wien,  Math.- 
Naturw.  Kl.,  Abt.  I.  v.  131:129-138. 

Rogers,  W.  P.  1939. — The  physiological  ageing  of  Ancylostoina 
larvae.     J.  Helm.,  v.  17:195-202. 

ScHALiMOV,  L.  G.  1931. — A  contribution  to  the  biology  of 
Oxyuris  equi.  Tr.  Dynamics  Develop.,  v.  6:181-196.  [Rus- 
sian with  English  summary.] 

Schmidt,  W.  J.  1937. — Doppelbrechung  und  Feinbau  der 
Eischale  von  Ascaris  megalocephala.  Ein  Vergleich  des 
Feinbaues  faserigen  und  filniartigen  Chitins.  Ztschr.  Zell- 
forseh.,  v.  25:181-203. 

Stannard,  J.  N.,  McCoy,  0.  R.,  and  Latchpord,  W.  B.  1938. 
— Studies  on  the  metabolism  of  Trichinclla  spiralis  larvae. 
Am.  J.  Hyg.,  t.  27:666-682. 


STEPANOW-GBlGORlErvv,  J.  and  HoKiM'Li,  R.  1926. — Ober  Bezie- 
hungen  zwischen  Glykogengehalt  parasitischer  Nematoden- 
larveii  und  ilirer  Wanderung  ini  Wirtskiirper.  Arcli.  Schiffs-u 
Tropen   Hyg.,  v.  30:r)77-5S5. 

SZWEJKOWSKA,  G.  1929. — Recherehes  sur  la  physiologic  de  la 
maturation  des  oeufs  d' Ascaris.  Bull.  Internatl.  Acad. 
Polon   Sc.  &  Lett.,  Ser.   B,   1928:489-519. 

Wendt,  H.  1936. — Beitrage  zum  Entwicklungszyklus  bei  Oxy- 
uris vcrmicularis.  Ztsclir.  Kinderheilk.,  v.  58:375-387.  [Not 
seen.] 

Wottge,  K.  1937. — Die  stofflichen  Veranderungen  in  der 
Eizelle  von  Ascaris  megalocephala  nach  der  Befruchtung. 
Protoplasma,  v.  29:31-59. 

Zawadowsky,  M.  1916. — Role  de  1 'oxygene  dans  le  processus 
de  segmentation  des  oeufs  de  \' Ascaris  megalocephala. 
(Note  preliminaire.)  Compt.  Rend.  Soe.  Biol.,  Paris  v 
68:595-598. 

1926. — Zum  Mechanismus  der  Wirkung  von  Zyankalium 
auf  die  lebende  Zelle  (Eier  von  A.<icaris  megalocephala'). 
Biologia  Generalis,  v.  2:442-456. 

1928. — The  nature  of  the  egg-shell  of  various  species 
of  Ascaris  eggs  {Toxascaris  limbata  Reillet  et  Henry,  Bel- 
ascaris  my.^tax  Zeder,  Belascaris  marginata  Rud.,  Ascaris 
suilla  Duj.).  Tr.  Lab.  Exper.  Biol.  Zoopark,  Moscow,  v. 
4:201-206.     [Russian  with  English  summary.] 

Zawadowsky,  M.  and  Schalimow,  L.  G.  1929. — Is  autoin- 
vasion  possible  given  the  presence  of  Enterobius  (Oxyuris) 
vermicularis  in  the  intestine?  Tr.  Lab.  Exper.  Biol.  Zoo- 
park,  Moscow,  v.  5:1-42.     [Russian  with  English  summary.] 

Zawadowsky,  M.  and  Orlow,  A.  P.  1927. — Is  there  any  pos- 
sibility of  autoinvasion  during  Ascariasis?  Tr.  Lab.  E::;per. 
Zoopark,  Moscow,  v.  3:99-116.  [Russian  with  English  sum- 
mary.] 

Zviaginzev,  S.  N.  1934. — Contribution  to  the  history  of  devel- 
opment of  Nematodirus  helwetianus.  Tr.  Dynamics  De 
velop.,  v.  8:186-202.     [Russian  with  English  summary.] 


371 


CORRECTIONS 


We  are  indebted  to  Dr.  G.  L.  Graham  for  his  assistance  in 
compiling  this  table  of  errors: 

Page    Column  Line 

1  25 — Strongyles  to  read  Strongiihm. 

2  43 — adherants  to  read  adherents. 
2  oO — Hhabiiias  spp.  to  read  Shabditis. 
1  11-12 — identifield  to   read   identified. 

1  under  Adcnophori,  line  4 — Knoploidrn  to  read  Eno- 
ploidea. 

2  .■)! — Hagmeir  to  read  Hagmeier. 

1   bibliog.    under    Mueller     1927 — Anisakis    to     read 
Anixakis. 

1  8 — macramphidiiim    to   read    macramphirlnm. 

2  27-28 — Critical  studies  are  due. 

1  14 — Iciinl-eli  to  read  l-iincl-eli. 

2  1819 — infecta  to  read  infeetnm. 
1  7 — Comma  between  Chromaelora  and  Mono- 


125 
125 
128 
130 
13-2 

132 
134 

145 
145 
149 
153 
154 

154 
155 
157 

165 
171 
173 

174 
177 
177 
177 
iGG 

177 

177 
178 
179 

183 
183 


posHiia. 
8 — Greeffiela  to  read  Grirfficla 
22 — Insert  asterisk  after  parasitifcra. 


I 

1 

2    under    Schneider,    A.    1858 — Gefass.vstem    to    read 
Gefasssystem. 


36 — Spinonoura  to  read  Spironoitra. 
14-1.) — postcriad   to   read   posteriad. 


1 

1 

1   under   Josepli    1883a — Erkliirengen    to     read     Erk- 
larungen. 

1  Acknowledgments — Mantoi'  to  read  Manter. 

1  ."4 — sculptored  to  read  sculptured. 

1  ."iSi — sculptoring  to  read  sculpturing. 

1  caption,   Fig.   135   I. — Si/phaeea  to   read   Sl/phacia. 

1   caption   Fig.   IS.')   R. — riirnrlonumtis  to   read   Pscu- 
rlnnymiis. 

1  caption  Fig.  135  HH. — fiUicolis  to   read  filicollis; 

Also  182,  col.  2,  line  4. 

2  8 — sculptoring  to  read  sculpturing. 

2  44 — Trichostrongylidae. 

2  4th  line  in  next  to  last  paragraph  under  Ovovivi- 
parity — macrocera  to  read  macrncerea. 

1  17 — Thelostomatidae  to  read  Thelastomatidae. 

2  22-33 — Ascaricica  to  read  Ascaridia. 


183 
186 
187 
187 
188 
189 

189 

189 
190 


191 
192 
193 
203 
204 
204 

205 

214 
221 
223 
229 
229 
231 
231 

232 
235 
239 

240 

240 


2  36 — permiable   to    read   permeable. 

1  30 — Gonglonema   to    read   Gongylonema. 

1  1st  line  of  2nd  paragraph — Dioctophymatoidea. 

1  Bibliog.  under  Ackert — Ascaridea  to  read  Ascaridia. 

2  Bibliog.  under  Skinker — salmanoid  to  read  salmoid. 

1  Bibliog.  under  Steiner   1937 — Jubilcm  to  read  Ju- 
bileum. 

1  Bibliog.    under    Zawadowsky    and    Shalimov — En- 

twicklungsbedihungen. 

2  Bibliog  under  Huff— Jour.  Parasit.,  v.  36? 

2   lender   Annelid — Cliaetognath-Xemathelminth    The- 
ory. 
II.  Plathyhelminthes — etc. 

1.  Oblique  cross  fibers  present 

Treniatoda,   etc. 

2.  Oblique  cross  fibers  absent 

Cestoidea,  etc. 

1  footnote — 3rd  line  between   to   read   between. 

2  12 — descendent  to  read  descendant. 

1  40 — cloace  to   read  cloaca. 

2  under  Cholodowsky-Weiblichlen  to  read  Wciblichen. 

1  under  Remane  1928 — Ostee  to  read  Ostsee. 

2  under   Zeder-Naturgeseschichte   to   read   Naturges 

ehichte. 

2    3rd   line    from   bottom — intercallation   to    read    in 
tercalation. 

2  under  Held  1912 — Gesellecsh  to  read  Gesellsch. 

2        77-77 — descendents  to  read  descendants. 

2  footnote — line  3 — divison  to  read  division. 

1  21 — subsequal  to   read  subequal. 

2  18— Fig.   15SJ  to  read  Fig.  157J. 

1  6-7 — Delete    Fig.    15()\V. 

1  Captiou  Fig.  158 — 4th  line  EH — Ancyelostoma  to 
read  Ancylostoma. 

1  12 — Esophagael  to  read  Esophageal. 

1  16-18 — caecae  to  read  ceca. 

2  under  Pai   1928 — Beeintlussing  to   read  Beeinflus- 

sung. 

1  under  Schwartz  and  Alicata  1935 — Longistriati  to 

read  Longistriata. 

2  under  Wehr  1935^superfamily  Filarioidae  to  read 

Filariodea. 


372 


ANNOUNCING  SECTION  II,  PART  III 
AN  INTRODUCTION  TO  NEMATOLOGY 

J.  R.  CHRISTIE,  EDITOR 


Chapter  }  Title  Authors 

XII.        Life  History.  Vagantia  and  Phytopara- 

sitica J-  R-  Christie 

XIII.  Ecology,  symptoms,  control  and  treat- 

ment for  Vagantia  and   Phytopara- 

sitica A.  L.  Taylor, 

W.  L.  Courtney, 
G.  Thorne, 
B.  G.  Chitwood 
and  J.  L.  Bassen 

XIV.  Feeding  habits  of  nematodes.  Vagantia 

and   Phytoparasitica    J-  R-  Christie, 

G.  Thorne  and 
B.  G.  Chitwood 

XV.        Imnmnity  due  to  nematodes Norman  R.  Stoll 

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