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Full text of "Protozoan parasites of domestic animals and of man"

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August, 1963 



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PROTOZOAN PARASITES 

OF 

DOMESTIC ANIMALS 

AND 
OF MAN 



PROTOZOAN PARASITES 

OF 



DOMESTIC ANIMALS 
AND 

OF MAN 



by 




NORMAN D. LEVINE. Ph.D. 

Professor of Parasitology 

College of Veterinary Medicine 

University of Illinois, Urbana, Illinois 



^* "^ 



w 



BURGESS PUBUSHING COMPANY 

426 South Sixth Street — Minneapolis 15, Minnesota 



Copyright © 1961 

by 
Norman D. Levine 



All Rights Reserved 
Library of Congress Catalog Card No. 61 9214 



No part of this book may be reproduced in any form 
without permission in writing from the publishers. 



Printed in the United States of America 



DEDICATED TO MY PARENTS: 

To Max Levine, whose example guided me to a 

career in science 
To Adele Levine, whose example helped me to 

an interest in the humanities 



Preface 



The importance of protozoan parasites as causes of disease in domestic animals is 
well recognized, yet the literature on them is still widely scattered and the books now 
available provide little more than an introduction to the subject. The present book was 
written to serve as a text and reference work for veterinarians, protozoologists, para- 
sitologists, zoologists and also for physicians. As our knowledge of the relations be- 
tween human and animal parasites has increased, the list has also increased of parasites 
which were once thought to be confined to domestic and wild animals but which are now 
known to occur also in man. The area of overlap between the fields of human and animal 
disease is becoming continually greater, and the zoonoses are receiving more and more 
attention. For this reason, the protozoan parasites of man are included in this book, 
and their relations to those of lower animals are indicated. 

When this book was begun, it was intended to be a revision of the pioneering 
Veterinary Protozoology by the late Banner Bill Morgan and the late Philip A. Hawkins, 
the second edition of which was published in 1952. However, it soon became apparent 
that far more than this was necessary, and the result has been an entirely new book. 

It is planned to follow this volume with others on veterinary helminthology and en- 
tomology. The first chapter, therefore, deals with the general principles of parasitology, 
while the second is an introduction to protozoology. The different groups of protozoa are 
discussed in the succeeding chapters, and the final chapter deals with laboratory diag- 
nostic technics. This systematic organization based on parasite groups is used rather 
than one based on host animals because it is more efficient, avoids repetition, and makes 
the subject easier to present and to understand. However, it is also useful to know which 
parasites one can expect to find in each host. Lists of parasites by host have therefore 
been prepared and are incorporated in the index. E. A. Benbrook (1958. Outline of 
parasites reported for domesticated animals in North America. 5th ed. Iowa State Univ. 
Press) has listed the parasites both by host and by location in the host. 

The world today is too small to permit a provincial approach to parasitism and 
disease. Katanga and Uttar Pradesh, Kazakhstan and Luzon are only a step from New 
York and San Francisco, and their problems and their diseases are becoming more and 
more our concern. The scope of this book, therefore, is world-wide, and parasites are 
discussed regardless of where they occur. However, major attention is given to the 
parasites of those domestic animals which occur in the temperate zones, and relatively 
little is included on parasites of animals like the elephant, camel, llama, reindeer and 
yak, even tho they are important domestic animals in some regions. 

When C. M. Wenyon wrote his classic Protozoology in 1926, he remarked that one 
of his chief difficulties had been that hardly a week passed without the publication of some 
paper of importance; that difficulty is far greater today than it was then. The number of 
published papers has been increasing exponentially, and there is no sign that the loga- 
rithmic phase of the curve is near its end. Even if one tries to read the current journals 
faithfully and to use the abstract journals assiduously, important papers may escape his 
notice. I am sure that some have escaped mine, and I should appreciate having them 
called to my attention. In addition, to help me in preparing future editions, I should ap- 
preciate receiving reprints of pertinent papers. 

- i - 



A favorite saying of Jean Baer is that textbooks perpetuate errors by copying them 
from one to another. I have tried to avoid this by going to the original papers as much 
as possible, but in so doing I may well have introduced some errors of my own. I should 
appreciate having these called to my attention also. 

Papers are appearing so fast that, unless one is forced to it, he cannot take the 
time to read and ponder those outside his own immediate field of interest and to try to 
integrate them into a coherent whole. Writing this book has made me do so, and the 
process has taught me a great deal. Not only have I learned many things which I did not 
know, but I have come to realize more clearly how much information we still lack, even 
about parasites which have been studied extensively. This book reflects that situation. 
The reader will find at least one question, one gap in our knowledge on each page. Each 
is a challenge for future research which I hope will be accepted by many who read this 
book. 

I should like to express appreciation to Drs. Carl A. Brandly, John O. Corliss, 
William R. Horsfall, Francis J. Kruidenier, R. N. Mohan and Miss Virginia Ivens for 
reading and commenting on various chapters; to Mrs. Helen V. Olson for preparing fig- 
ures 6, 13A, 18, 19, 20K-1, 24 and 31; to Miss Ada Price for typing the greatest part of 
the manuscript; to Mesdames Marion Corzine, Mardell Harris, Kathryn Hill, Janet 
Manning, Lucille Rice, Carolyn Seets and Misses Eileen Bourgois and Beverly Seward 
for proof-reading the manuscript; to Drs. E. R. Becker, J. F. Christensen, H. Christl, 

F. P. Filice, D. M. Hammond, C. A. Hoare, R. R. Kudo, J. Ludvik, E. R. Noble, 

G. A. Noble, Muriel Robertson, R. M. Stabler, E. E. Tyzzer and D. H. Wenrich, to 
Balliere, Tindall & Cox, Cambridge University Press, Charles C Thomas, the Common- 
wealth Agricultural Bureaux, Gustav Fischer Verlag, Iowa State University Press, Johns 
Hopkins Press, Springer-Verlag, University of California Press, Williams & Wilkins Co. 
and The Wistar Institute, and to the Annals of Tropical Medicine and Parasitology, Iowa 
State Journal of Science, Journal of Morphology, Journal of Parasitology, Journal of 
Protozoology, Parasitology, Quarterly Journal of Microscopic Science, Quarterly Re- 
view of Biology, University of California Publications in Zoology, Veterinary Reviews 
and Annotations, Zeitschrift fur Parasitenkunde, and Zentralblatt fur Bakteriologie for 
permission to reproduce some of their illustrations; and, not the least, to the Burgess 
Publishing Company for its patience and understanding during the time this manuscript 
was in preparation. 

NORMAN D. LEVINE 



University of Illinois 
Urbana 
November, 1960 



- 11 - 



^ -"- Contents 

Page 

Preface i 

Chapter 

1 Introduction to Parasitology 1 

2 Introduction to the Protozoa 18 

3 The Hemoflagellates 40 

4 Histomonas 74 

5 The Trichomonads 82 

6 Other Flagellates 107 

7 The Amoebae 129 

8 The Telosporasida and the Coccidia Proper 158 

9 Klossiella and Hepatozoon 254 

10 Plasmodium, Haemoproteus and Leucocytozoon 259 

11 The Piroplasmasida 285 

12 Sarcocystis, Toxoplasma and Related Protozoa 317 

13 The Ciliates 347 

14 Laboratory Diagnosis of Protozoan Infections 377 

Appendix Scientific and Common Names of Some Domestic 

and Wild Animals 395 

Index and Host-Parasite Lists 399 



81589 



- Ill 



Parasitology is the science which 
treats of parasites. The word "parasite" 
is derived from the Greek and means, 
literally, "situated beside. " It was used 
by the ancient Greeks originally for 
people who ate beside or at the tables of 
others, and referred both to sycophants 
or hangers-on and to priests who col- 
lected grain for their temples. While the 
social meaning of the term has been par- 
tially retained, it has been given a new 
connotation by scientists. Parasites are 
defined as organisms which live on or 
within some other living organism, which 
is known as the host. Parasitism is the 
association of two such organisms. 

Parasites may be either animals or 
plants--viruses, rickettsiae, spirochetes, 
bacteria, yeasts, fungi, algae, mistletoe, 
dodder, protozoa, helminths, arthropods, 
molluscs, and even certain vertebrates 
such as the cuckoo. The general prin- 
ciples of parasitology apply to all. How- 
ever, in this book we shall deal primarily 
with animal parasites, leaving the plant 
parasites to textbooks of microbiology. 

In our everyday thinking we consider 
that animals can live in three main hab- 
itats--land, fresh water and sea water. 
A fourth habitat is the parasitic one, 
which is quite different from the other 
three. As a matter of fact, there are 
quite a few different parasitic habitats, 
each with its own characteristics. Para- 
sites are found in the lumen of the intes- 
tinal tract, on the outside of the body, in 
the skin, in various tissues, in the blood 
plasma, inside different types of cells, 
and even inside cell nuclei. 

Parasites have arisen from free- 
living animals. Some parasites closely 
resemble their free-living relatives, but 
others have undergone structural changes 
which make them more suited to their 
changed environment. Since these 
changes have in many cases been the loss 
of some power which their free-living 
relatives possess, parasites have some- 



C/iapter 1 



IHTROdUCTm 

TO 
PARASITOLOGY 



- 1 



INTRODUCTION TO PARASITOLOGY 



times been considered degenerate crea- 
tures. The opposite is true. Parasites 
are highly specialized organisms. Those 
powers which were unnecessary, they 
have lost. For instance, the adults of 
most parasitic worms have relatively 
little ability to move around. But they 
don't need it. Too much activity might 
even lead to their reaching the point of no 
return and being discharged from their 
host's body. 

As another example, tapeworms have 
no intestinal tract. But, since they ob- 
tain their nourishment directly thru the 
body wall, an intestine would be super- 
fluous. Thus, in the case of parasites as 
with all other animals and plants, the use- 
less has been eliminated in the course of 
evolution. 



being confronted by odds of this sort and 
are continually surmounting them. 

Life of one sort or another seems to 
have flowed into every possible niche. 
Parasites live in some of the most diffi- 
cult niches, and it is remarkable how they 
have succeeded in surviving in them. 
Parasites have tremendous problems to 
solve--problems of nutrition, of respira- 
tion, of excretion, of getting from one 
host to another--and the different and 
often ingenious ways in which different 
parasites have solved these problems are 
amazing. Some of their adjustments are 
almost perfect; others are less satisfac- 
tory. In general, we may say that the 
more satisfactory the solution, the more 
abundant are the parasites. The rare 
ones are the less successful ones. 



In contrast, the reproductive system 
of parasites is often tremendously devel- 
oped. Since the chances of an egg or 
larva leaving one host and infecting an- 
other are very small, the numbers of 
eggs produced must be very large. Many 
parasitic worms produce thousands of 
eggs a day. The female of Ascaris suum, 
the large roundworm of swine, lays about 
1, 400, 000 eggs per day (Kelley and Smith, 
1956). Assuming that she lives 200 days, 
which is not an excessive life, she will 
have laid 280 million eggs in her lifetime. 
Since the number of Ascaris in the world 
is staying more or less the same, we can 
conclude that on the average only two of 
these eggs will produce adult worms--a 
male and a female. The chance of any 
particular egg ever becoming a mature 
worm is thus about 1 in 140 million, 
which is much less than a man's chance of 
being struck by lightning. 

The broad fish tapeworm of the dog, 
man and other animals, Diholliriocephalus 
laliis, will produce over 4 miles of seg- 
ments containing 2 billion eggs during a 
10-year life span, and again the number 
of these tapeworms is not increasing. 
Since these tapeworms are hermaphro- 
dites, each egg can become an egg-laying 
worm, but its chances of doing so are a 
hundred times less than those of the 
Ascaris egg. Parasites are continually 



We can think of parasitism as related 
basically to the solution of the problem of 
nutrition, and we can think of the other 
problems as somewhat secondary. This 
is obviously an incomplete and defective 
view, but nevertheless it has some value. 

Living organisms have four general 
types of nutrition. Holophytic nutrition is 
typical of plants; it involves synthesis of 
carbohydrates by means of chlorophyll. 
Holozoic nutrition is animal-like; it in- 
volves ingestion of particulate food thru a 
permanent or temporary mouth. Sapro- 
zoic or saprophytic nutrition (the choice 
of term depending upon whether the organ- 
ism is an animal or plant) involves ab- 
sorption of nutrients in solution thru the 
body wall. The fourth type of nutrition is 
that employed by viruses, which synthe- 
size their proteins directly from the host's 
amino acids and do not have a true body 
wall during their parasitic phase. 

The terms saprophyte and saprophytic 
are often used by bacteriologists in an- 
other sense also, to refer to non-patho- 
genic, non-parasitic organisms. The 
terms saprozoite and saprozoic are also 
similarly used with reference to free- 
living animals, but much less frequently. 

Coprozoic or coprophilic organisms 
are animals which live in feces. They 



INTRODUCTION TO PARASITOLOGY 



may be either saprozoic or holozoic or 
both, and are sometimes mistaken for 
true parasites. 

Parasites resemble predators in some 
respects; indeed, one grades into the 
other. In general, we think of predators 
as larger than or as large as their prey, 
while we think of parasites as consider- 
ably smaller. A lion seizing an antelope 
is a predator, as is a spider capturing a 
fly. But there is a distinction only in size 
of prey between a predatory assassin bug 
capturing another insect and sucking out 
its juices and the closely related, para- 
sitic kissing bug sucking blood out of a 
man. And a mosquito is just as much a 
predator as the kissing bug. The distinc- 
tion is one of degree. As Elton (1935) put 
it, "The difference between a carnivore 
and a parasite is simply the difference be- 
tween living upon capital and income, be- 
tween the burglar and the blackmailer. 
The general result is the same although 
the methods employed are different." 



TYPES OF PARASITISM 

There are several types of parasitism. 
Parasitism itself is defined as an associa- 
tion between two specifically distinct or- 
ganisms in which one lives on or within 
the other in order to obtain sustenance. 

SvDibiosis is the permanent associa- 
tion of two specifically distinct organisms 
so dependent upon each other that life 
apart is impossible under natural condi- 
tions. The relation between many ter- 
mites and their intestinal protozoa is 
symbiotic. The termites eat wood, but 
they cannot digest it; the protozoa can di- 
gest wood, turning it into glucose, but 
they have no way of obtaining it; working 
together, the termites ingest wood par- 
ticles, the protozoa break the cellulose 
down to glucose, and the termites then 
digest the glucose. Lichens furnish an- 
other example of symbiosis. They are 
composed of certain species of algae and 
fungi living together. 

Many insects, ticks and mites have 
symbiotic bacteria and rickettsiae. The 



symbiotic organisms are found either in 
special cells, the mycetocytes, in modi- 
fied parts of the Malpighian tubules, or 
in special organs, the mycetomes. It is 
significant that, among blood-sucking 
arthropods, symbiosis occurs in those 
which live on blood thruout their life cy- 
cles (ticks, lice, bedbugs, kissing bugs, 
tsetse flies, hippoboscid flies) but not in 
those in which only the adults suck blood 
while the larvae are free-living (fleas, 
mosquitoes, phlebotomines, tabanids and 
stable flies). Blood lacks some metabo- 
lites which the arthropods are unable to 
synthesize themselves and for which they 
depend on their symbiotes. These meta- 
bolites appear to include vitamins of the 
B group and probably other substances as 
well (Buchner, 1953; Koch, 1956; Weyer, 
1960). 

Mutualism is an association of two 
organisms by which both are benefited. 
It differs from symbiosis in that it is not 
obligatory for both partners. One exam- 
ple often cited is that of a sea anemone 
living upon the back of a crab. The anem- 
one is benefited by being moved to new 
hunting grounds and by obtaining morsels 
of food torn off by the crab, while the crab 
is protected by the bulk and stinging ten- 
tacles of the anemone. Another marine 
example is that of the scorpion fish of 
Indo-Malaya. It lives on the bottom of the 
sea, where it lies in wait for passing fish. 
It is covered with a crust of hydroids 
which camouflage it so that it can seize 
its unwary prey more easily. The hydroids 
presumably benefit by being moved to new 
sources of food and by being provided with 
a dwelling-place. However, since they 
can live other places beside the scorpion 
fish's back, their relation is mutualistic. 

Another example of mutualism, and 
one closer to us, is the relationship be- 
tween ruminants and the cellulose-digest- 
ing bacteria and other micro-organisms 
in their rumens. The latter are furnished 
a favorable home by their hosts and aid 
them by breaking down cellulose to usable 
compounds. The rumen-dwelling bacteria 
which produce B group vitamins and thus 
make an outside source of them unneces- 
sary for ruminant nutrition probably 



INTRODUCTION TO PARASITOLOGY 



belong here too, altho they verge on the 
symbiotic. The bacteria which produce 
these vitamins in the large intestine of 
swine are more nearly mutualistic, since 
the pigs cannot absorb the vitamins thru 
the colon wall but must re-ingest their 
feces to obtain them. The same is true 
of rabbits, and is undoubtedly responsible 
for their coprophagy. 

The bizarre protozoa which swarm 
in the rumen and reticulum are almost 
certainly mutualistic. Their host can get 
along without them, but they may benefit 
it by providing a better type of protein 
than it ingests. In addition, they are an 
important source of volatile fatty acids, 
and they smooth out the carbohydrate fer- 
mentation process. 

Commensalism is an association be- 
tween host and parasite in which one part- 
ner is benefited and the other is neither 
benefited nor harmed. Many intestinal 
bacteria such as Escherichia coli are 
normally commensals, as are many in- 
testinal protozoa such as Entamoeba coli 
and Trichomonas spp. 

The next two terms both refer to po- 
tentially pathogenic parasites. Parasito- 
sis is the association between two organ- 
isms in which one injures the other, 
causing signs and lesions of disease. 
Parasitiasis is the association between 
two organisms in which one is potentially 
pathogenic but does not cause signs of 
disease. 

The difference between parasitosis 
and parasitiasis is quantitative. In para- 
sitiasis the host is able to repair the 
damage caused by the parasite without 
noticeable injury, while in parasitosis it 
cannot. As Whitlock (1955) put it, "Para- 
sitiasis is a state of balance. Parasitosis 
is a state of imbalance. " Applying the 
concept to ruminant helminths, Gordon 
(1957) said, "Helminthiasis is almost uni- 
versal and continuous, helminthosis is 
more restricted and sporadic. However, 
one shades imperceptibly into the other in 
subclinical infestations." The same or- 
ganism can cause either parasitosis or 
parasititiasis, depending upon the number 



present or upon the nutritional condition, 
age, sex, immune state, etc. of the host. 
Failure to recognize this distinction may 
cause many false diagnoses--the mere 
presence of a potentially pathogenic spe- 
cies of parasite does not necessarily 
mean that it is causing disease. 

The carrier state furnishes a good 
example of parasitiasis. Carriers are 
animals which have a light infection with 
some parasite but are not harmed by it, 
usually due to immunity resulting from 
previous exposure, but which serve as a 
source of infection for susceptible ani- 
mals. Thus, adult sheep and cattle may 
be lightly infected with gastrointestinal 
nematodes without noticeable effect, but 
their lambs and calves may become heav- 
ily parasitized from grazing with them. 
The condition in the adults is parasitiasis; 
that in the young is parasitosis. Adult 
chickens rarely suffer from coccidiosis 
because they have recovered from a clin- 
ical or subclinical attack when young. 
However, they are usually still lightly in- 
fected and continue to shed a few oocysts; 
they have coccidiasis. Cattle which have 
aborted as a result of Brucella infection 
may continue to shed the bacteria in their 
milk without ordinarily suffering further 
clinical attacks. The aborting cow has 
brucellosis, while the carrier has bru- 
celliasis. 

These endings can also be applied to 
the names of the disease agents, as has 
already been done above. Thus, Haenion- 
chiis coiitortus may cause haemonchosis 
or haemonchiasis, Taenia may cause 
taeniosis or taeniasis, Histomo>ias mel- 
eagridis may cause histomonosis or his- 
tomoniasis, depending on the circum- 
stances. 

It was mentioned earlier that the so- 
lutions different parasites have made of 
their problems of living have varied in 
satisfactoriness. We might consider this 
in regard to type of parasitism. Symbio- 
sis is a highly specialized type of associ- 
ation which occurs only in certain groups. 
Mutualism is a much looser association, 
also fairly uncommon. It could well be a 
step on the road to symbiosis. The most 



INTRODUCTION TO PARASITOLOGY 



common types of parasitism are the last 
three. Of these, commensalism is 
clearly the most desirable, both from the 
standpoint of the host (which isn't harmed) 
and of the parasite. Parasitosis, which 
harms the host, is in the long run harm- 
ful to the parasite also. By injuring their 
hosts, parasites harm their environment, 
and if they are so indiscreet as to kill 
their hosts, they die too. Parasitiasis 
is intermediate between parasitosis and 
commensalism in some cases, but not in 
all. 



HOST- PARASITE 
RELATIONS 

Depending on their species, para- 
sites may live in any organ or tissue of 
the host; they may live on its surface, or 
they may spend most of their time away 
from it. Special terms have been applied 
to these relationships. An endoparasite 
is a parasite that lives within the host's 
body. An ectoparasite is one that lives 
on the outside of the body. An erratic 
{oT aberrant) parasite is one that has 
wandered into an organ in which it does 
not ordinarily live. An incidental para- 
site is a parasite in a host in which it does 
not usually live. A facultative parasite is 
an organism that is capable of living 
either free or as a parasite. An obliga- 
tory parasite is an organism which must 
live a parasitic existence. A periodic 
parasite is one which makes short visits 
to its host to obtain nourishment or other 
benefits. A pseudoparasite is an object 
that is mistaken for a parasite. Para- 
sites may themselves be parasitized by 
hyperparasites . 

An organism which harbors a para- 
site is its host. There are several types 
of host. A definitive host is the host 
which harbors the adult stage of a para- 
site. An intermediate host is the host 
which harbors the larval stages of the 
parasite. A first intermediate host is 
the first host parasitized by the larval 
stages of the parasite. A second inter- 
mediate host is the host parasitized by 
the larval stages at a later period in the 
life cycle. A paratenic or transport host 



is a second (or third) intermediate host 
in which the parasite does not undergo any 
development but usually remains encysted 
until the definitive host eats the paratenic 
host. 

The vector of a parasite or disease 
agent is an arthropod, mollusc or other 
agent which transmits the parasite from 
one vertebrate host to another. If the 
parasite develops or multiplies in the 
vector, it is called a biological vector. 
If the parasite does not develop or mul- 
tiply in it, it is called a mechanical vec- 
tor. 

Intermediate hosts of helminths are 
biological vectors, but biological vectors 
are not necessarily intermediate hosts. 
Indeed, the latter term has no applica- 
tion to protozoa, bacteria, rickettsia or 
viruses, none of which have larvae. Mos- 
quitoes are biological vectors of malaria 
and of yellow fever, and the tsetse fly is 
a biological vector of Trypanosoma 
brucei, for the parasites must develop in 
them to become infective for the next ver- 
tebrate host. However, tabanid flies are 
merely mechanical vectors of Trypano- 
soma evansi, since the parasites undergo 
no development in them. 

The terms infection and infestation 
are used by different people in different 
ways. The former term originally re- 
ferred to internal agents of disease, 
while the latter was used with reference 
to external harassing agents, including 
not only ectoparasites but also rodents, 
pirates and thieves. This usage was cur- 
rent during the latter part of the nine- 
teenth century. Later on, it was felt de- 
sirable to distinguish between parasites 
which multiplied in their hosts and those 
which did not. "Infection" was then used 
for the former type of parasitism, and 
"infestation" for the latter. This usage 
was popular for a time, but it was never 
universally accepted. More recently 
there has been a trend toward the older 
usage. Most American parasitologists 
have accepted it, but most British ones 
prefer to speak of helminth infestations. 
In this book infection will be used to refer 
to parasitism by internal parasites, and 



INTRODUCTION TO PARASITOLOGY 



infestation to parasitism by external para- 
sites. 

The term life cycle refers to the de- 
velopment of a parasite thru its various 
forms. It may be simple, as in an organ- 
ism which multiplies only by binary fis- 
sion, or it may be extremely complex, 
involving alternation of sexual and asexual 
generations or development thru a series 
of different larval forms. A )>ionogenetic 
parasite is one in which there is no alter- 
nation of generations. Examples of this 
type are bacteria, flagellate protozoa 
such as Trichomonas , nematodes such as 
Ascaris and Ancylostoma, and the ecto- 
parasitic fish trematodes of the order 
Monogenorida (= Monogenea). A hetero- 
genetic parasite is one in which there is 
alternation of generations. Examples of 
this type are malarial parasites and coc- 
cidia, in which sexual and asexual gen- 
erations alternate, the endoparasitic 
trematodes of higher vertebrates of the 
order Digenorida (= Digenea), in which 
there may be several larval multiplicative 
stages before the adult, and the nematode, 
Strongyloides, in which one generation is 
parasitic and parthenogenetic while an- 
other is free-living and sexual. 

Depending on their type, parasites 
may live in only one or in a number of 
different types of hosts during the course 
of their normal life cycles. A monoxen- 
ous parasite has only one type of host-- 
the definitive host. Examples are coc- 
cidia, amoebae, hookworms, fish trema- 
todes, horse bots, streptococci and most 
pox viruses. A heteroxenous parasite 
has two or more types of host in its life 
cycle. Examples are the malarial para- 
sites, most trypanosomes, trematodes of 
higher vertebrates, filariae, tapeworms, 
the rickettsiae, yellow fever virus and 
various encephalitis viruses. 

These two pairs of terms are inde- 
pendent of each other. Parasitic amoebae 
and hookworms are monogenetic and 
monoxenous. Filariid and spirurid nema- 
todes are monogenetic and heteroxenous. 
Strongyloides and most coccidia are het- 
erogenetic and monoxenous. Malarial 
parasites and trematodes of birds and 



mammals are heterogenetic and hetero- 
xenous. 

Another group of terms deals with 
host range, i.e. , the number of host spe- 
cies in which a particular parasite may 
occur. These parasites can be either 
monoxenous or heteroxenous, monogen- 
etic or digenetic. Indeed, there may be 
a difference in host-restriction between 
the definitive and intermediate hosts of 
the same parasite. For example, the 
blood fluke, Schistosoma japoniciini, can 
become adult in a rather wide range of 
mammals, but its larval stages will de- 
velop in only a few closely related species 
of snails. 

The term, monoxenous parasite, is 
used by some authors for a parasite which 
is restricted to a single host species. 
Such parasites undoubtedly exist, but they 
are fewer than our present records indi- 
cate. The human malarial parasites were 
once thought to be monoxenous in this 
sense of the word, but they have more re- 
cently been found capable of infecting 
apes, and it is now known that chimpan- 
zees in West Africa are naturally infected 
with P. malariae, the cause of quartan 
malaria in man (Garnham, 1958). Many 
species of coccidia are also known from 
but a single host, but for the most part 
closely related wild hosts have not been 
examined nor have cross transmission ex- 
periments been attempted with them. Be- 
cause of this and because of the confusion 
arising between this usage of monoxenous 
and the one defined above, this usage 
should be avoided. 

A stenoxenoiis parasite is one which 
has a narrow host range. Among the 
coccidia, members of the genus Eimeria 
are generally stenoxenous, as are the 
human malaria parasites and cyclophyl- 
lidorid tapeworms. Many nematodes such 
as the hookworms, nodular worms, fila- 
riids and spirurids tend to be stenoxenous. 
Both biting and sucking lice are steno- 
xenous, and many are even limited to 
specific areas on their host. Relatively 
few bacteria are stenoxenous, but Strep- 
tococcus agalactiae, Mycobacterium 
leprae, Vibrio, Mycoplasma, the spiro- 



INTRODUCTION TO PARASITOLOGY 



chete, Treponema, the rickettsiae, Ana- 
plasma, Eperythrozoon, Haemobartonella 
and Cowdria, and the viruses of hog chol- 
era, duck hepatitis and yellow fever are 
stenoxenous. 



5. 7% of its mammals. If all these pos- 
sible hosts were to be examined, one 
might expect to find some 3500 species of 
Eimeria in mammals and 34,000 in chor- 
dates. 



An euryxenous parasite is one which 
has a broad host range. Among the coc- 
cidia, members of the genus Isospora 
are often euryxenous. So are most try- 
panosomes, most Plasmodium species 
(but not those affecting man), and many 
species of Trichomonas. Most trema- 
todes are euryxenous, as are Trichinella, 
Dracunculns and Dioctophyma among the 
nematodes. Fleas, chiggers and many 
ticks are euryxenous. Most parasitic 
bacteria are euryxenous; examples are 
most species of Salmonella, Escherichia, 
Brucella, Erysipelothrix and Listeria. 
Among euryxenous rickettsiae are 
Rickettsia, Coxiella and Miyagawanella 
psittacii. Among euryxenous viruses are 
those of rabies and many encephalitides. 
Leptospira and Borrelia are euryxenous 
spirochetes. 

The use of these two terms, however, 
may be deceptive. There exist in nature 
all intergrades between them, and all we 
have done has been to pick out the two 
extremes of a continuum and give them 
names. 

Actually, the host range of most 
parasites is broader than generally sup- 
posed. The fact is that most animal 
species have not been examined for para- 
sites. For example, the genus Eimeria 
is one of the commonest and best known 
among parasitic protozoa. Becker (1956) 
listed 403 species, of which 394 were 
from chordates and 202 from mammals. 
This is quite impressive, especially to 
someone who wishes to study their tax- 
onomy. However, according to Muller 
and Campbell (1954), there are 33,640 
known living species of chordates and 
3552 of mammals. Some hosts have 
more than one species of Eimeria, but 
some coccidian species occur in more 
than one host. Assuming that these more 
or less cancel out, we can calculate that 
Eimeria has been described from only 
1. 17% of the world's chordates and from 



So far only the qualitative aspect of 
the host range has been discussed. How- 
ever, altho a parasite may be capable of 
living in more than one host, it is much 
more common in some hosts than in 
others. The principal hosts of a parasite 
are those hosts in which it is most com- 
monly found. The supplementary hosts 
are those of secondary importance, and 
the incidental hosts are those which are 
infected only occasionally under natural 
conditions. To these should be added 
experimental hosts, which do not normally 
become infected under natural conditions 
but which can be infected in the laboratory. 
This last category may include both inci- 
dental and supplementary hosts and also 
hosts never infected in nature. 

In order to take into account this 
quantitative aspect of the host-parasite 
relationship, the terms quantitative host 
spectrum or quantitative host range are 
used. These give the amount of infection 
present in each infected species. 

Several factors affect the quantita- 
tive host spectrum. One is geographic 
distribution. The natural quantitative 
spectrum may be quite different in one 
locality than in another. The species of 
animals present may be different, or the 
incidence of infection may be different. 
For example, a number of nematodes 
parasitize both domestic and wild rumi- 
nants. However, since the wild rumi- 
nants of North America and Africa are 
not the same, the quantitative host spec- 
tra of the same parasites on the two con- 
tinents are different. The spectrum is 
still different in Australia, where there 
are no wild ruminants but where wild 
rabbits are susceptible to infection with 
a few ruminant nematodes. 

A second factor is climate. Many of 
the same host species may be present in 
different areas but climatic conditions in 
one area may prevent or favor a para- 



INTRODUCTION TO PARASITOLOGY 



Site's transmission. For instance, the 
common dog hookworm in most parts of 
the United States is Ancylostoma caninum, 
but in Canada it is Uncinaria slenocephala. 
This is due to a difference in temperature 
tolerance of the free-living larval stages. 

Local conditions such as ground cover 
are also important. If the vegetation is 
open so that the sunlight can get down to 
the surface of the soil where a parasite's 
eggs, cysts or free-living stages are 
found, survival will be much less, trans- 
mission will be reduced and the numbers 
of affected hosts will be fewer than if the 
vegetation is thick and protective. Or the 
kinds and numbers of parasites in a herd 
of animals confined to a low, moist pas- 
ture may be quite different from those in 
a herd kept on a hill pasture or on drylot. 

A fourth factor is that of the distribu- 
tion of acceptable intermediate hosts. 
Trypanoso7na briicei occurs only in Africa 
because its tsetse fly intermediate hosts 
occur only there. The fringed tapeworm 
of sheep, Thysanosoma actinioides, is 
found in the western United States but not 
in the east despite the fact that infected 
sheep have repeatedly been introduced 
onto eastern pastures. A suitable inter- 
mediate host does not occur on these 
pastures, so the parasite cannot be trans- 
mitted. 

A fifth factor is that of chronologic 
time. The quantitative host spectrum may 
be quite different in the same locality at 
different periods, particularly if an erad- 
ication campaign has been carried out in 
the interim. Echinococcosis is a case in 
point. At one time it was extremely com- 
mon in the dogs, sheep and people in Ice- 
land, but it has now been eradicated. 
Gapeworms were once common in poultry 
in the United States, but as the result of 
modern poultry management practices 
they are now exceedingly rare in chickens 
and turkeys, altho they are not uncommon 
in pheasants. 

A sixth factor is that of the ethology 
or habits of the host. A species may be 
highly susceptible to infection with a par- 
ticular parasite, yet natural infections 



may seldom or never occur. The habits 
of the host may be such that it rarely 
comes in contact with a source of infec- 
tion even tho both exist in the same local- 
ity. For example, wild mink in the mid- 
western United States are not infrequently 
infected with the lung fluke, Paragonimus 
kelUcotti. It is easy to infect dogs with 
this fluke experimentally, yet it is ex- 
tremely rare in midwestern dogs. The 
reason is that dogs rarely eat the cray- 
fish which are the fluke's intermediate 
host. 

Because of these factors, we must 
speak of «a///rrt/ and potential host spec- 
tra. The latter term refers to the abso- 
lute infectability of potential hosts and not 
to the natural situation. The natural host 
spectrum is an expression of the actual 
situation at a particular time and place. 
The two spectra may be quite different, 
and of course the natural one will vary 
considerably, depending on the circum- 
stances. The complete host spectrum has 
not been worked out for any parasite, and 
to do so would be a very time-consuming 
process. However, it will have to be 
done, at least for the more important 
parasites, before we can fully understand 
their ecology and the epidemiology of the 
diseases they cause. 

Certain parasites and diseases occur 
in man alone, others in domestic animals 
alone, and others in wild animals alone. 
Still others, including some important 
ones, occur in both man and domestic 
animals, man and wild animals, domestic 
and wild animals, or in all three. A 
knowledge of their host relations is im- 
portant in understanding their ecology and 
epidemiology. 

A disease which is common to man 
and lower animals is known as a zoo)iosis. 
Zoonoses were redefined in 1958 by the 
Joint WHO FAO Expert Committee on 
Zoonoses as "those diseases and infec- 
tions which are naturally transmitted be- 
tween vertebrate animals and man" (World 
Health Organization, 1959). Less than 20 
years ago it was said that there were 50 
zoonoses, but in the above report the 
World Health Organization listed more 



INTRODUCTION TO PARASITOLOGY 



than 100, of which 23 were considered of 
major importance. Many more are cer- 
tain to be revealed by future investigations. 

Our thinking about parasites and dis- 
eases is ordinarily oriented toward either 
man or domestic animals. In this context, 
it is convenient to have a special term for 
hosts other than those with which we are 
primarily concerned. A reservoir host 
is a vertebrate host in which a parasite or 
disease occurs naturally and which is a 
source of infection for man or domestic 
animals, as the case may be. Wild ani- 
mals are reservoirs of infection for man 
of relapsing fever, yellow fever and moist 
Oriental sore, while domestic animals are 
reservoirs for man of trichinosis and 
classical Oriental sore. Wild animals are 
reservoirs of infection for domestic ani- 
mals of many trypanosomes, while man is 
a reservoir for domestic animals of Enta- 
moeba histolytica. 

Parasites and diseases may continue 
to exist indefinitely in their reservoir 
hosts, and man or domestic animals may 
become infected when they enter the local- 
ity where the parasites or diseases exist. 
Such a locality is known as a nidus (liter- 
ally, "nest"). This term is used primarily 
in connection with vector-borne diseases, 
altho it need not be restricted to them. 



epidemiology, taxonomy, evolution, etc. 
(see Hoare, 1955). A dei)ie is a natural 
population within a species. It lies more 
or less below the subspecies level, but it 
is not a formal taxon and is not given a 
Latin name. There are different types of 
deme. Nosodemes differ in their clinical 
manifestations. One example is Leish- 
mania donovani, which has five nosodemes, 
Indian, Mediterranean, Sudanese, Chinese 
and South American, which produce differ- 
ent types of disease. Serodemes differ 
serologically. These are best known 
among the bacteria and viruses, but also 
occur among the animal parasites. Tri- 
trichonionas foetus, for example, has 
several serological types or serodemes. 
Xenodemes differ in their hosts, and topo- 
demes differ in geographic distribution. 

There are also other types of demes. 
The population of a parasite species within 
a single host animal is a i)io)iodenie, and 
that in a single flock or herd is an agele- 
deme. Thus, a population of the stomach 
worm, Haemouchus contortus, in a single 
sheep is a monodeme, the population in 
all the sheep of a single flock is an agele- 
deme, that in all sheep is a xenodeme. 
The population in all cattle is another 
xenodeme and that in all goats is a third, 
the population of H. contortus in all hosts 
in North America is a topodeme, etc. 



Natural nidi may be elementary or 
diffuse (Palovsky, 1957). An elementary 
nidus is confined within narrow limits. 
A rodent burrow containing rodents, arga- 
sid ticks and relapsing fever spirochetes 
or a woodrat nest containing woodrats, 
kissing bugs and Trypanosoma cruzi is an 
elementary nidus. In a diffuse nidus the 
donors, vectors and recipients are distrib- 
uted more widely over the landscape. A 
wooded region in which ticks circulate 
Rickettsia rickettsii among the rodents 
and lagomorphs is a diffuse nidus of 
Rocky Mountain spotted fever, as is an 
area where tsetse flies transmit trypan- 
osomes among wild game. The nidality 
of a disease refers to the distribution and 
characteristics of its nidi. 

The concept of the deme is useful in 
discussing host-parasite relationships, 



Each of these demes may differ mor- 
phologically and physiologically, and a 
large part of the taxonomist's work con- 
sists in determining the limits of their 
variation and deciding whether they are 
really demes or different species. Since 
the judgments of all taxonomists do not 
agree, there is some variation in the 
names which different parasitologists use. 
Demes are advance guards in the march 
of evolution, and no sharp line can be 
drawn beyond which they become subspe- 
cies or species. Taxonomists have been 
able to arrive at no better statement of 
how species are defined than to say that a 
species is what a specialist on its group 
says it is. And since some scientists are 
splitters and others are lumpers, their 
definitions vary with their temperaments. 
For most of us, the best rule is the prag- 
matic one of using those names which 



10 



INTRODUCTION TO PARASITOLOGY 



make for the greatest understanding of the 
organisms we study and of their relations 
with each other and with their hosts. 

Parasite evolution : Parasites have 
evolved along with their hosts, and as a 
consequence the relationships between the 
parasites of different hosts often give val- 
uable clues to the relationships of the 
hosts themselves. Certain major groups 
of parasites are confined to certain groups 
of hosts. Sucking lice are found only on 
mammals. Biting lice occur primarily on 
birds, but a few species are found on 
mammals. The monogenetic trematodes 
are found almost without exception on fish; 
some of the more highly evolved digenetic 
trematodes are found in fish, but more 
occur in higher vertebrates. There is a 
tendency, too, for the more advanced di- 
genetic trematodes to occur in the higher 
host groups. 

One would expect that, as evolution 
progressed in different host groups, there 
would develop in each one its own group 
of parasites. This has often occurred. 
Thus, of the 48 families of digenetic 
trematodes listed by Dawes (1956), 17 
occur only in fish, 8 only in birds, 3 only 
in mammals, 2 in fish and amphibia, 3 in 
reptiles and birds, 6 in birds and mam- 
mals, 1 in fish, amphibia and reptiles, 
2 in reptiles, birds and mammals, 1 in 
amphibia, reptiles and birds, 3 in all but 
fish, and 2 in all five classes of verte- 
brates. Of the 11 classes of tapeworms 
recognized by Wardle and McLeod (1952), 
4 are found only in elasmobranch fish, 3 
only in teleosts, 1 only in birds, 1 in 
teleosts, amphibia and reptiles, 1 in tel- 
eosts, birds and mammals, and 1 in am- 
phibia, reptiles, birds and mammals. 

This same tendency is apparent even 
in parasitic groups which are quite widely 
distributed. For example, many reptiles 
and mammals (but not birds) have pin- 
worms of the family Oxyuridae, but each 
group has its own genera. Iguanas have 
Ozolaimus and Macrae is, other reptiles 
have Thelandros , Pharyngodon and sev- 
eral other genera, rodents have Asfiicu- 
liiris, Syphacia and Wellcomia, rabbits 
have Passalurus, equids have Oxyuris, 



ruminants have Skrjabinema, and man and 
other primates have Enlerobius . 

On the other hand, there are many 
exceptions to this general rule, and it 
cannot be used without corroboration as 
the sole criterion of host relationship. 
Many fish-eating birds and mammals have 
the same species of trematodes for which 
fish act as intermediate hosts. And the 
fact that the pig and man share a surpris- 
ing number of parasites is no proof of 
their close relationship despite their sim- 
ilarity of character and personality; it 
simply reflects their omnivorous habits 
and close association. 

Adaptation to parasitism : Adaptation 
to a parasitic existence has required many 
modifications, both morphological and 
physiological. Locomotion, at least of the 
parasitic stages, has often become re- 
stricted. Certain organs and organ sys- 
tems may be lost. Tapeworms lack an in- 
testine altho their ancestors presumably 
had one, and adult trematodes have no eye- 
spots altho their turbellarian ancestors 
and many of their larvae have them. 
Parasitic amoebae have no contractile 
vacuoles altho their free-living relatives 
do. 

In contrast, many structures are 
modified or hypertrophied for the para- 
sitic life. Many helminths have hooks and 
suckers to help them hold their position. 
The protozoon, Gianiia, has turned most 
of its ventral surface into a sucking disc. 
The mouthparts of many insects and mites 
have become highly efficient instruments 
for tapping their hosts' blood supply. The 
chigger, which does not suck blood, has 
developed a method of liquefying its hosts' 
tissues. The food storage organs of many 
parasites have been enlarged. Many blood- 
sucking arthropods which are unable to ob- 
tain all the nutrients they need from blood, 
have established symbiotic relationships 
with various microorganisms and have 
formed special organs for them. 

The reproductive system of many 
parasites has been hypertrophied to pro- 
duce tremendous numbers of eggs. Other 
parasites, such as the trematodes, have 



INTRODUCTION TO PARASITOLOGY 



11 



developed life cycles in which the larvae 
also multiply. 

In the parasites with high reproduc- 
tive rates, infection is left largely to 
chance. Many other parasites, however, 
have developed life cycles in which chance 
is more or less eliminated. In these, the 
reproductive rate is low. The larva of 
the sheep ked, Melophagns ovinus, devel- 
ops to maturity in the body of its mother 
and pupates immediately after emerging. 
The pupa remains in its host's wool. The 
female tsetse fly, too, produces fully de- 
veloped larvae. The tropical American 
botfly, Derinaiobia honiinis, captures a 
mosquito and lays her eggs on it. These 
hatch when the mosquito lights to suck 
blood, and the larvae enter the host. 

Morphological and developmental 
modifications are the most obvious ones, 
but biochemical ones are even more im- 
portant. How do parasites survive in 
their hosts without destruction? What 
keeps those which live in the intestine 
from being digested along with the host's 
food? Why is it that morphologically sim- 
ilar species are restricted to different 
hosts which themselves may be morpho- 
logically quite similar? 

The second question has been an- 
swered by saying that the same mecha- 
nism operates which prevents the hosts 
from digesting themselves, that the para- 
sites protect themselves by producing 
mucus or that mucoproteins in their in- 
tegument protect them, that they secrete 
antienzymes, or that the surface mem- 
brane of living organisms is impermeable 
to proteolytic enzymes. However, much 
more research must be done before a 
satisfactory answer can be given. An- 
swers given to the first and third ques- 
tions are vague. Compatibility of host 
and parasite protoplasm is invoked, but 
all this does is put a name to the beast. 
The question of how this compatibility is 
brought about remains unanswered, and a 
great deal of biochemical and immuno- 
chemical research must be done before it 
can be answered (see Becker, 1953; Read, 
1950; von Brand, 1952). 



Injurious effects of parasites on their 
hosts . Parasites may injure their hosts 
in several ways: 

1. They may suck blood (mosquitoes, 
hookworms), lymph (midges) or exu- 
dates (lungworms). 

2. They may feed on solid tissues, either 
directly (giant kidney worms, liver 
flukes) or after first liquefying them 
(chiggers). 

3. They may compete with the host for 
the food it has ingested, either by in- 
gesting the intestinal contents (asca- 
rids) or by absorbing them thru the 
body wall (tapeworms). In some cases 
they may take up large amounts of cer- 
tain vitamins selectively, as the broad 
fish tapeworm does with Vitamin B12. 

4. They may cause mechanical obstruc- 
tion of the intestine (ascarids), bile 
ducts (ascarids, fringed tapeworm), 
blood vessels (dog heartworm), lymph- 
atics (filariids), bronchi (lungworms) 
or other body channels. 

5. They may cause pressure atrophy 
(hydatid cysts). 

6. They may destroy host cells by grow- 
ing in them (coccidia, malaria para- 
sites). 

7. They may produce various toxic sub- 
stances such as hemolysins, histoly- 
sins, anticoagulants, and toxic prod- 
ucts of metabolism. 

8. They may cause allergic reactions. 

9. They may cause various host reac- 
tions such as inflammation, hyper- 
trophy, hyperplasia, nodule forma- 
tion, etc. 

10. They may carry diseases and para- 
sites, including malaria (mosquitoes), 
trypanosomosis (tsetse flies), swine 
influenza (lungworms), salmon poison- 
ing of dogs (flukes), heartworms (mos- 
quitoes) and onchocercosis (blackflies). 

11. They may reduce their hosts' resis- 
tance to other diseases and parasites. 

A great deal more could be said about 
this subject. Additional information is 
given in the symposium on mechanisms of 
microbial pathogenicity of the Society for 
General Microbiology (Howie and O'Hea, 
1955). 



12 



INTRODUCTION TO PARASITOLOGY 



Resistance and Immunity to Para - 
sites . This is such a tremendous sub- 
ject that its facets can only be hinted at. 
The general principles of immunology 
apply to animal parasites as much as they 
do to bacteria, viruses and other micro- 
organisms. However, since the associ- 
ation of many of the larger parasites with 
their hosts is not as intimate as that of 
microorganisms, the hosts' immune res- 
ponses may not be as great. This is 
especially true with regard to the forma- 
tion of circulating antibodies. 

Immunity or resistance may be either 
natural {innate) or acquired. Natural re- 
sistance is the basis of host-parasite 
specificity, but, as mentioned above, 
little is known of its mechanism. Ac- 
quired immunity may be either active or 
passive. Active immunity results from 
the body's own action. It follows expo- 
sure to living or dead disease agents, and 
can result from natural infection or arti- 
ficial administration of virulent, attenu- 
ated or killed organisms. 

One type of active immunity is pre- 
munition. This is immunity due to the 
continued presence of the disease agent. 
It occurs in such diseases as babesiosis 
and anaplasmosis. 

Passive immunity results from the 
introduction of antibodies produced by 
some other animal. It may be acquired 
naturally, thru the colostrum or milk in 
mammals or thru the egg yolk in birds, 
or artificially by injection of antiserum. 
Passive immunity is seldom as long- 
lasting as active immunity. 

Immunity against parasites and dis- 
ease agents generally increases with age. 
There are exceptions, however. Young 
cattle, for instance, are more resistant 
to Babesia and Anaplasnia than are adults. 
Age immunity may be either developed as 
the result of previous exposure or it may 
be natural. Not all the factors operating 
in the latter case are known. An impor- 
tant one is that very young animals can- 
not mobilize their body defenses against 
invasion as efficiently as adults. For in- 
stance, they do not produce antibodies at 



first, depending on those acquired from 
their mothers. Another factor, discov- 
ered by Ackert and his co-workers (cf. 
Ackert, Edgar and Frick, 1939) to explain 
the relative resistance of older chickens 
to Ascaridia galli, is that these birds have 
more intestinal goblet cells than do young 
birds. The goblet cells secrete mucus 
which inhibits the development of the 
worms. For further information on im- 
munity in parasitic infections, see Talia- 
ferro (1929), Culbertson (1941) and Soul- 
sby (1960). 

Genetic constitution is also important 
in determining resistance to parasites. 
For instance, Ackert el al. (1935) showed 
that Rhode Island Red and Plymouth Rock 
chickens are more resistant to Ascaridia 
galli than are Buff Orpingtons, Minorcas 
and White Leghorns. Cameron (1935) 
found that in a mixed flock of sheep. Chev- 
iots were less heavily parasitized with 
gastrointestinal nematodes than Shetlands 
and Scottish Blackface, and that these in 
turn were less heavily parasitized than 
Border Leicesters. Stewart, Miller and 
Douglas (1937) found that Romney sheep 
were markedly resistant to infection with 
Ostertagia circunicincta. while Rambouil- 
lets were less so and Southdowns, Shrop- 
shires and Hampshires were least resist- 
ant. Certain individuals among the more 
susceptible breeds, however, were just as 
resistant as the Romneys. Whitlock(1958) 
has studied genetic resistance to tricho- 
strongylidosis in sheep in some detail. 

The nutritional status of the host may 
affect its resistance. Poorly nourished 
animals are usually more susceptible to 
infection and suffer more severely from 
its effects. Protein depletion or protein 
starvation is particularly important. 
Lack of specific vitamins and minerals 
generally decreases resistance, but there 
are cases in which lack of a certain vita- 
min which the parasite requires may af- 
fect the parasite adversely. Thus, Becker 
and Smith (1942) found that when calcium 
pantothenate was added to a ration con- 
taining restricted vitamins B,, Bg and pan- 
tothenate, the number of oocysts produced 
hy Einteria nieschulzi infections in the rat 
was increased. 



INTRODUCTION TO PARASITOLOGY 



13 



Geographic Distribution . Some para- 
sites, particularly those of man and his 
domestic animals, are worldwide in dis- 
tribution, but others are much more re- 
stricted. But even a widely distributed 
species may be much more prevalent in 
one region than another. Many factors 
are responsible, some of which have al- 
ready been discussed (pp. 7-8). A para- 
site which originated in a particular place 
in a particular host species may never 
have been introduced into some other lo- 
cality or host where it could develop per- 
fectly well. It may have been introduced 
but may have died out because a suitable 
vector was lacking or because the climate 
was not suitable. The ox warble has not 
been able to establish itself in the south- 
ern hemisphere because the reversal of 
seasons has prevented it from completing 
its life cycle. 

Whenever domestic animals are in- 
troduced into a new region, there is a 
good possibility that they will pick up 
some of the parasites of their wild rela- 
tives there. The parasite spectrum of 
cattle in Africa differs from that in North 
America, both of these differ from the 
spectrum in Europe, and all three differ 
from the spectrum in Australia. Wild 
animals, too, may acquire parasites 
from domestic ones or from other wild 
species. Hence, the parasite spectrum 
of animals in zoos may be quite different 
from that in their normal habitat, and the 
success of an attempt to introduce a new 
game bird or mammal into a region may 
depend in part on the parasites and dis- 
eases that it encounters. 

The importance of wildlife as a para- 
site reservoir for domestic animals is 
well illustrated by the report of Longhurst 
and Douglas (1953) on the interrelation- 
ships between the parasites of domestic 
sheep and Columbian black-tailed deer in 
the north coastal part of California, 
where the two live on the same range. 
They found in their survey of 63 sheep 
and 81 deer that 1 species of trematode, 
5 of cestodes, and 13 out of 18 species 
of nematodes were common to both 
hosts. 



Origin of Parasitism . Parasites 
originated from free-living ancestors. 
The process probably began soon after 
the first living forms appeared. The 
change from a free-living to a parasitic 
habitat has taken place many times in the 
course of evolution. It has occurred as 
new major groups appeared, it has taken 
place independently many times in each 
group, and it is undoubtedly still occur- 
ring. Once established, the parasites 
evolved along with their hosts. 

In some cases, the parasites first 
invaded the host thru the integument, like 
Pelodera and related rhabditid nematodes. 
In other cases, the parasites were swal- 
lowed along with their host's food. Para- 
sites with life cycles involving two or 
more hosts became established first in 
one host, and later on developed their 
more complicated life cycles. The try- 
panosomes, for instance, were originally 
gut parasites of insects and only later be- 
came blood parasites of vertebrates. 

Preadaptation was necessary for 
parasites to become established. They 
must have had the ability to survive and 
reproduce in the host before they entered 
it. By far the great majority of free-liv- 
ing forms which entered the alimentary 
canal of some larger animal were killed 
and digested, but some of them were able 
to resist this process and a few were able 
to live there. Some of the factors involved 
have already been discussed (p. 10). 

Economic Importance . Parasites 
are responsible for heavy economic losses 
to the livestock industry. These are due 
in part to death, but even more important 
are the losses due to illness, reduced 
growth rate, decreased meat, milk, egg 
and wool production and, in working ani- 
mals, loss of working energy. It is im- 
possible to quantitate these losses accu- 
rately, but rough estimates can be made. 
The U. S. Department of Agriculture 
(1954) made such an estimate for losses 
in agriculture during the ten-year period, 
1942-1951. The figures on parasite losses 
in Table 1 are taken from this publication. 
Further details are given in the publication 
itself and by Schwartz et al. (1955). 



14 



INTRODUCTION TO PARASITOLOGY 



TABLE 1 

ANNUAL LOSSES DUE TO PARASITES OF 

LIVESTOCK IN THE U.S., 1942-1951 

(from USDA, 1954) 



Class of 
Livestock 


Average Annual 
Value of 
Production 


Annual Losses 


DoUais 


% of 
Production 


Cottle 

Sheep 

Goats 

Swine 

Hoises and 
Mules 

Poultry 

All Livestock 
(screw-worms 
only) 


$3,431,539,000 

404, 162, 000 

16,375,000 

3,473,817,000 

835, 852, 000* 
3, 149, 002, 000 


$420, 658, 000 

64, 626, 000 

1, 886, 000 

279, 826, 000 

26, 320, 000 
126,532,000 

20, 000, 000 


12.3 

16.0 

11.5 

8.1 

3.1 
4.0 


TOTAL 


$11,310,747,000 


$939, 848, 000 


8.3 



♦Average annual value of animals. 



Parasites caused an estimated loss of 
$939, 848, 000 per year. All other dis- 
eases, both infectious and nutritional, were 
estimated to cause a total annual loss of 
$1,748, 594,000, so parasites are consid- 
ered to be responsible for about 35% of the 
losses in the American livestock industry. 
A billion dollars a year is a sizeable fig- 
ure. We can hardly expect to eliminate 
this loss completely, but if every animal 
owner took advantage of our present know- 
ledge, a half billion dollars a year, or 
even more, could be saved. 

Scientific Names . There are several 
million species of animals in the world. 
Many of them are well enough known and 
easy enough to recognize to have received 
common names. However, these names 
vary from one language to another and 
from one locality to another among people 
who speak the same language. Further- 
more, the same common name is often 
applied to different species in different 
regions. 

In the United States, "cattle" refers 
to the ox. Box laiirus, but in India it re- 
fers to the zebu. Bus indiciis, and in Eng- 
land and some other countries (and in the 



Bible) to domestic livestock in general. 
"Fowl" has more than one meaning. It 
may refer to the chicken, Gallns domesti- 
cus, but it may refer to any bird raised 
for food, including the turkey, Meleagris 
gallopavo , and ducks. Most domestic ducks 
are Anas platyrhynchos, but the Muscovy 
duck is Cairina moschata. One of the worst 
offenders is "rabbit" which is applied in- 
discriminately to many quite different spe- 
cies. Rabbits are not rodents, but lago- 
morphs; they have four upper incisors, 
whereas rodents have only two. The do- 
mestic rabbit is the common wild rabbit of 
Europe, Oryctolagus cunicitlus. The com- 
mon wild rabbit of North America, however, 
is the cottontail, Sylvilagiis, of which there 
are 13 species. In addition, there are sev- 
eral species of jack rabbits belonging to the 
genus Lepiis. A list of scientific names of 
domestic and common wild animals is given 
in Appendix I. 

In order to prevent the confusion which 
would be inevitable in dealing with these 
myriad species, a system of scientific 
names has been worked out. This system 
was first established by Linnaeus in the 
eighteenth century, and the starting point 
for the names of animals is the tenth edition 
of Linnaeus' Syste»ia Naturae, which was 
published in 1758. An International Code of 
Zoological Nomenclature was adopted in 
1904; it was reviewed at a colloquium held 
in Copenhagen in 1953, and a new, revised 
code was adopted by another colloquium 
held in London in 1958. This code estab- 
lishes rules for naming animal species and 
for indicating their relationships. 

In the system of binomial nomenclature 
used for scientific names, each species is 
given two names. The first name, which 
is capitalized, is used for a group of closely 
related species; this group is called a 
and its name is the generic name. The sec- 
ond name, which is not capitalized, is used 
for a single species within the genus and is 
called the specific name. A particular gen- 
eric name can be used for only a single 
group of species in the animal kingdom, but 
the same specific name can be applied to 
species in different genera. The generic 
and specific names are often derived from 
Latin or Greek, but they may also be based 



INTRODUCTION TO PARASITOLOGY 



15 



on the names of persons, geographic lo- 
calities, etc. They must, however, have 
latinized endings. Both names are writ- 
ten in italics. 

The name of the person who first 
named each species and the date when he 
did it are also part of its scientific name, 
altho these are often omitted in non-taxo- 
nomic writing. If the namer assigned the 
species to a different genus from the one 
which is accepted as correct, then his 
name and date are enclosed in parentheses 
and are followed outside the parentheses 
by the name of the person who assigned 
the species to its present genus with the 
date when he did it. If there has been no 
change in the genus designated by the or- 
iginal author, parentheses are not used. 
Thus, the common large roundworm of the 
dog, Toxocara canis, was first described 
by Werner in 1782, but he assigned it to 
the same genus as the earthworm, Lum- 
bricus. In 1905, Stiles established a new 
genus, Toxocara, for this species. The 
original name, then, was Lumbricus canis 
Werner, 1782, and the presently accepted 
name is Toxocara canis (Werner, 1782) 
Stiles, 1905. Similarly, in the early days 
of parasitology almost all tapeworms were 
assigned to a single genus, Taenia. As 
knowledge increased, more and more gen- 
era were split off from it. The common 
sheep tapeworm was called Taenia expansa 
by Rudolphi in 1805, but in 1891 Blanchard 
established a new genus, Moniezia, for it, 
so that its correct name is now Moniezia 
expansa (Rudolphi, 1805) Blanchard, 1891. 

Genera are grouped together into 
families, families are grouped into orders, 
orders into classes, and classes into phyla. 
Each of these categories, and also each of 
the lower ones, is known as a taxon (pi. , 
taxa). Subfamilies and superfamilies, sub- 
orders and superorders, etc. are often 
used, and in some cases so many relation- 
ship levels are recognized that it is neces- 
sary to introduce cohorts, tribes, etc. 

Each family is based on one of its 
genera, known as the type genus, and the 
name of the family is obtained by attach- 
ing the ending, -idae, to the root of the 
name of the genus. Thus, Strongylus be- 



longs to the family Strongylidae, and 
Trichomonas to the family Trichomonad- 
idae. The subfamily ending is -inae. 

While the botanists long ago adopted 
a system of uniform endings for the names 
of their higher taxa, the zoologists have 
never been able to agree on one. As a 
consequence, it is impossible to determine 
the ranks of the higher taxa with certainty 
from their names. In the present book, 
however, the system of uniform endings 
proposed by Levine (1959) is used, so this 
problem does not arise. These are: 
Superclass, -asica; Class, -asida; Sub- 
class, -asina; Superorder, -orica; Order, 
-orida; Suborder, -orina; Supercohort, 
-icohica; Cohort, -icohida; Subcohort, 
-icohina; Superfamily, -icae; Family, 
-idae; Subfamily, -inae; Supertribe, 
-ibica; Tribe, -ibida; Subtribe, -ibina. 

Many scientific names appear quite 
formidable at first glance. They have def- 
inite meanings, however, and it helps in 
remembering them to know what these 
meanings are. Since most scientific names 
are based on Latin or Greek, a knowledge 
of some of the descriptive words from 
these languages is helpful. Much informa- 
tion can be obtained from a dictionary of 
derivations such as that of Jaeger (1955). 
The thorny -headed worm of swine is 
MacracantJiorhynchus hirudinaceus. This 
name is derived from the Greek. The gen- 
eric name means "large {macr-) thorny 
{acantho-) proboscis {-rhynchus)." The 
specific name is derived from the scien- 
tific name of the leech (Hirudo) and means 
"leechlike"; it was given because the worm 
is firmly attached to the intestinal wall and 
looks vaguely like a leech. The name of 
the whipworm, Trichuris, commemorates 
an error. This nematode looks a good 
deal like a buggy-whip, with a sturdy body 
and a long, whip-like anterior end about as 
thick as a hair. T'' . ne, however, 
means hair-tail an ' "tir-head. This 

mistake was so offe. some scien- 

tists that they propos . to substitute 
Trichocephaliis for j.richuris. This is 
not permissible according to the rule of 
priority of the International Code of Zoo- 
logical Nomenclature, so the error re- 
mains. 



16 



INTRODUCTICN TO PARASITOLOGY 



It is often discouraging to students 
and scientists alike to see the many 
changes in scientific names which continue 
to be made. These, however, appear to 
be inevitable. As new knowledge is 
gained, some species must be split up, 
others recombined and still others shifted 
from one genus to another. It is some- 
times found that a name which has been 
long used and accepted must be dropped 
in favor of an unfamiliar one, either be- 
cause it had been used first for some other 
species or because the less familiar name 
had been given earlier but overlooked. 

Another reason for these changes lies 
in human nature itself. No satisfactory 
criteria have ever been established for 
the definition of species, and some taxo- 
nomists go into finer differences than 
others in separating them. 

The taxonomists' difficulties arise 
because what they are dealing with are 
individual organisms, and all taxonomic 
schemes are the result of man's attempts 
to arrange these individuals in a system 
which shows their relationships. All 
taxa, whether species, subspecies, gen- 
era, families or whatnot, are products 
of this abstraction process and have no 
real existence outside the human mind. 
Many taxonomists, however, refuse to 
accept this idea, believing that species 
are real and external, and that their task 
is simply to discover and differentiate 
them. It is easy to understand why they 
do not like to believe that they are devot- 
ing their lives to figments of the imagin- 
ation. 

Without the labors of the systema- 
tists we should be in a state of hopeless 
confusion. Their scientific names and 
their taxonomic schemes are absolutely 
necessary if we are to carry out repro- 
ducible experimental work or understand 
practically all biological phenomena. 



Becker, E. R. and L. Smith. 1942. Iowa St. Col. ). Sci. 

16:443-449. 
von Brand, T. 1952. Chemical physiology of endoparasitic 

animals. Academic Press, New York. 
Buchner, P. 1953. Endosymbiose der Tiere mit pflanzlichen 

Mikroorganismen. Birkhauser, Basel/Stuttgart. 
Cameron, T. W. M. 1935. Proc. 12th Intern. Vet. Congr. 

3:44-62. 
Culbeitson, J. T. 1941. Immunity against animal parasites. 

Columbia Univ. Press, New York. 
Dawes, B. 1956. The Trematoda. Cambridge Univ. Press, 

Cambridge, England. 
Elton, C. 1935. Animal ecology. Macmillan, New York. 
Gamham, P. C. C. 1958. ]. Trop. Med. Hyg. 61:92-94. 
Gordon, H. M. 1957. Adv. Vet. Sci. 3:287-351. 
Hoare, C. A. 1955. Refuah Vet. 12:258-263. 
Howie, J. W. and A. ]. O'Hea, eds. 1955. Mechanisms 

of microbial pathogenicity. Fifth symposium of the 

Society for General Microbiology held at the Royal In- 
stitution, London, April 1955. Cambridge Univ. Press, 

Cambridge, England. 
Jaeger, E. C. 1955. A source -book of biological names 

and terms. 3rd ed. Thomas, Springfield, Illinois. 
Kelley, G. W. and L. J. Smith. 1956. J. Pamsit. 42:587. 
Koch. A. 1956. Exper. Parasit. 5:481-518. 
Levine, N. D. 1959(1958). System. Zool. 7:134-135. 
Longhuret, W. M. and ]. R. Douglas. 1953. Trans. N. Am. 

Wildlife Conf. 18:168-187. 
Muller, S. W. and A. Campbell. 1954. Syst. Zool. 

3:168-170. 
Pavlovsky, Y. N. 1957. Natural nidality of disease in re- 
lation to the ecology of the zoonoses. WHO Regional 

office for Europe, Seminar on Veterinary Public Health. 

EURO-85. 2/20 Rev. 1, pp. 30. 
Read, C. P., Jr. 1950. Rice Inst. Pamph. 37(2):l-94. 
Schwartz, B. et al. 1955. Proc. U. S. Livestock San. 

Assoc. 58:303-308. 
Stewart, M. A., R. F. Miller and J. R. Douglas. 1937. 

J. Ag. Res. 55:923-930. 
Taliaferro, W. H. 1929. The immunology of parasitic 

infections. Century, New York. 
U. S. Dept. of Agriculture. 1954. Losses in agriculture. 

A preliminary appraisal for review. USDA Agr. Res. 

Serv. ARS-20-1, Washington, D. C. 
Wardle, R. A. and J. A. McLeod. 1952. The zoology of 

tapeworms. Univ. of Minnesota Press, Minneapolis. 
Whitlock, J. H. 1955. Proc. Am. Vet. Med. Assoc. 

92:123-131. 
Whitlock, J. H. 1958. Cornell Vet. 48:127-133. 
World Health Organization. 1959. Joint WHO/FAO Expert 

Committee on Zoonoses. Second Report. Tech. Rep. 

Ser. No. 169, Geneva, pp. 83. 



GENERAL REFERENCES 



CHAPTER REFERENCES 

Ackert, J. E. , S. A. Edgar and L. P. Frick. 1939. Trans. 

Am. Micr. Soc. 58:81-89. 
Ackert, J. E. , L. L. Eisenbrondt, J. H. Willmoth, B. 

Glading and I. Pratt. 1935. J. Agr. Res. 50:607-624. 
Becker, E. R. 1953. J. Parasit. 39:467-480. 
Becker, E. R. 1956. Iowa St. Col. J. Sci. 31:85-139. 



The following general references are a supple- 
ment to the chapter references given above, 
some of which are also general in nature. 

Antipin, D. N. , V. S. Ershov, N. A. Zolotarev and V. A. 
Salycev. 1959. Parasitologiya i invazionnye bolezni 
sel'skokhozyaistvennykh zhivotniykh. 2nd ed. Gos. hdat. 
Sel'skokh. Liter. , Moscow. 



INTRODUCTION TO PARASITOLOGY 



17 



Audy, J. R. 1958. The localization of disease with special 
reference to the zoonoses. Trans. Roy. Sec. Trop. Med. 
Hyg. 52:308-328. 

Baer, J. G. 1951. Ecology of animal parasites. Univ. of 
111. Press, Urbana. 

Baer, J. G. , ed. 1957. First symposium on host specificity 
among parasites of vertebrates. Univ. Neuchatel, Swit- 
zerland. 

Baker, E. W. , T. M. Evans, D. J. Gould, W. B. Hull and 
H. L. Keegan. 1956. A manual of parasitic mites of 
medical or economic importance. Nat. Pest Control 
Assoc. , New York. 

Baker, E. W. and G. W. Wharton. 1952. An introduction 
to acorology. Macmillan, New York. 

Ball, G. H. 1943. Parasitism and evolution. Am. Natur- 
alist 78:345-364. 

Becker, E. R. 1933. Host specificity and specificity of 
animal parasites. Am. J. Trop. Med. 13:505-523. 

Belding, D. H. 1952. Textbook of clinical parasitology. 
2nd ed. Appleton-Century-Crofts, New York. 

Benbrook, E. A. 1958. Outline of parasites reported for 
domesticated animals in North America. 5th ed. Iowa 
St. Coll. Press, Ames, Iowa. 

Benbrook, E. A. and M. W. Sloss. 1955. Veterinary Clin- 
ical Parasitology. 2nd ed. Iowa State Univ. Press, Ames, 
Iowa. 

Biester, H. E. and L. H. Schwarte, eds. 1959. Diseases of 
poultry. 4th ed. Iowa State College Press, Ames, Iowa. 

Borchert, A. 1958. Lehrbuch der Parasitologie fur Tierarzte. 
2nd ed. S. Hirzel, Leipzig. 

Brumpt, E. 1949. Precis de parasitologie. 6th ed. 2 vols. 
Masson et Cie. , Paris. 

Cameron, T. W. M. 1952. The parasites of domestic 
animals. 2nd ed. Lippincott, Philadelphia. 

Cameron, T. W. M. 1956. Parasites and parasitism. 
Wiley, New York. 

CauUery, M. 1950. Le parasitisme et la symbiosis. 2nd 
ed. G. Doin, Paris. 

Chandler, A. C. 1923. Speciation and host relationships 
of parasites. Parasitol. 15:326-339. 

Chandler, A. C. 1948. Factors modif>'ing host resistance 
to helminthic infections. Proc. 4th Intern. Congr. Trop. 
Med. Malaria 2(6):975-983. 

Chandler, A. C. 1953. The relation of nutrition to para- 
sitism. J. Egypt. Med. Assoc. 36:533-552. 

Chandler, A. C. 1953a. Immunity in parasitic diseases. 
J. Egypt. Med. Assoc. 36:811-834. 

Chandler, A. C. 1955. Introduction to parasitology. 9th 
ed. Wiley, New York. 

Chitwood, B. G. and M. B. Chitwood. 1950. An introduc- 
tion to nematology. Rev. ed. B. G. Chitwood, Balti- 
more, Md. 

Clunies Ross, I. and H. McL. Gordon. 1936. The internal 
parasites and parasitic diseases of sheep. Angus S Robert- 
son, Sydney, Australia. 

Cole, W. H. , ed. 1955. Some physiological aspects and 
consequences of parasitism. Rutgers Univ. Press, New 
Brunswick, N. J. 

Faust, E. C. 1955. Animal agents and vectors of human 
disease. Lea S Febiger, Philadelphia. 



Faust, E. C, P. F. Russell and D. R. Lincicome. 1957. 
Craig and Faust's clinical parasitology. 6th ed. Lea & 
Febiger, Philadelphia. 

Hall, M. C. 1930. The wide field of veterinary parasitol- 
ogy. J. Parasitol. 16:175-184. 

Herms, W. B. 1950. Medical entomology. 4th ed. Mac- 
millan, New York. 

Kotldn, S. 1953. Parazitologia. Mezogazdasagi Kiado, 
Budapest. 

Lapage, G. 1951. Parasitic animals. Cambridge Univ. 
Press, Cambridge, England. 

Lapage, G. 1956. Veterinary parasitology. Charles C 
Thomas, Springfield, 111. 

Lapage, G. 1956. Monnig's veterinary helminthology and 
entomology. 4th ed. Williams G Wilkins, Baltimore. 

Markell, E. K. and Marietta Voge. 1958. Diagnostic 
medical parasitology. W. B. Saunders, Philadelphia. 

Martini, E. C. W. 1952. Lehrbuch der medizinischen 
Entomologie. 4th ed. G. Fischer, Jena. 

Matheson, R. 1950. Medical entomology. 2nd ed. Corn- 
stock, Ithaca, N. Y. 

Morgan, B. B. and P. A. Hawkins. 1949. Veterinary hel- 
minthology. Burgess, Minneapolis. 

Most, H. , ed. 1951. Parasitic infections in man. Colum- 
bia Univ. Press, New York. 

Neveu-Lemaire, M. 1936. Traite d'helminthologie 
medicale et veterinaire. Vigot Freres, Paris. 

Newsom, I. E. 1952. Sheep disease. Williams S Wilkins, 
Baltimore. 

Orlov, N. P. 1958. Veterinamaya parazitologiya. Gosud. 
Izdat. Sel'skokh. Liter, Moscow. 

Pearse, A. S. 1942. Introduction to parasitology. Thomas, 
Springfield, 111. 

Reichenow, E. , H. Vogel and F. Weyer. 1952. Leitfaden 
zur Untersuchung der tierischen Parasiter des Menschen 
und der Haustiere. 3rd ed. J. A. Barth, Leipzig. 

Rothschild, Miriam and Theresa Clay. 1957. Fleas, flukes 
and cuckoos. A study of bird parasites. 2nd ed. Collins, 
London. 

Smith, Theobald. 1934. Parasitism and disease. Princeton 
Univ. Press, Princeton, N. J. 

Soulsby, E. J. L. 1960. Immuirity to helminths--recent 
advances. Vet. Rec. 72:322-328. 

Strong, R. P. 1935. The importance of ecology in relation 
to disease. Science 82:307-317. 

Stunkard, H. W. 1929. Parasitism as a biological phenom- 
enon. Sci. Mon. 28:349-362. 

Taliaferro, W. H. 1940. The mechanism of acquired im- 
munity in infections with parasitic worms. Physiol. Rev. 
20:469-492. 

U. S. Dept. of Agriculture. 1956. Animal diseases. Year- 
book of Agriculture, Washington, D. C. 

Univ. of Illinois. 1952. Microscopic diagnosis of parasitism 
in domestic animals. 111. Ag. Exper. Sta. Circ. No. 
698. pp. 135. 

Watson, J. M. 1960. Medical helminthology. Balliere 
Tindall and Cox, London. 

Weyer, F. 1960. Biological relationships between lice (Ano- 
pluro) and microbial agents. Ann. Rev. Ent. 5:405-420. 

Whitlock, J. H. 1960. Diagnosis of veterinary parasitisms. 
Lea & Febiger, Philadelphia. 



Chapter 2 



iNTRODUCTION 
TO 

THE PROTOZOA 



Protozoa form the most primitive 
group in the animal kingdom. The bodies 
of all other animals are composed of 
many units, or cells, but those of the 
protozoa are a single cell. No matter 
how complex their bodies may be, and 
many of them are very much so, all the 
different structures are contained in a 
single cell. This complexity has made 
some investigators maintain that, instead 
of being considered single cells, protozoa 
should be thought of as non-cellular (see, 
for example, Boyden, 1957). This argu- 
ment is essentially a verbal issue--a 
matter of how one wants to define "cell. " 

Protozoa are microscopic in size, 
only a few being visible to the naked eye. 
They differ from the Metazoa in being 
unicellular, but this difference is not as 
clearcut as might be supposed. Some 
protozoa have a syncytial stage in their 
life cycle in which there are no cell walls 
between the nuclei, and some species form 
colonies which swim as a unit and which 
contain somatic and reproductive organ- 
isms which look different. The difference 
between these and Metazoa is again partly 
a matter of definition, and gives a clue to 
how the Metazoa could have arisen. 

The boundary between the Protozoa 
and certain one-celled plants, too, is not 
clearcut. For example, the whole group 
of slime molds are considered by proto- 
zoologists to be protozoa and assigned to 
the order Mycetozoorida in the class 
Sarcodasida, but botanists consider them 
fungi and assign them to the class Myxo- 
mycetes. 

A still more confusing situation in- 
volves the plant-like protozoa which con- 
tain chlorophyll. Protozoologists assign 
them to the subclass Phytomastigasina, 
but botanists consider them green algae. 
The problem is that there are many spe- 
cies of colorless protozoa which differ 
from green ones only in that they lack 
chromatophores. Loss of chromatophores 
can be produced experimentally. It has 



18 - 



INTRODUCTION TO THE PROTOZOA 



19 



been done in Euglena, for instance, by 
treatment with streptomycin or simply by 
growing the organisms at 34 to 35° C 
(Pringsheim and Pringsheim, 1952). This 
change of a plant into an animal would be 
just as astounding as the metamorphosis 
of Cinderella's pumpkin into a golden 
coach if the differences between the lower 
forms were as great as those between 
higher plants and animals. However, the 
principal difference is one of nutrition, 
and many species are quite plastic, their 
form of nutrition depending on circum- 
stances. Indeed, many of the metabolic 
pathways of the phytoflagellate, Ochro- 
monas Dialhaniensis, aside from those in 
which its chlorophyll takes part, are so 
similar to those of men that Hutner has 
facetiously called it a humanoid! 

In recognition of this situation, Ernst 
Haeckel proposed that the name Protista 
be applied to all single-celled organisms 
and that the group be considered inter- 
mediate between the animal and plant 
kingdoms. Relatively few modern taxon- 
omists subscribe to this idea, perhaps 
less because of any defect in the idea itself 
than because they have been trained either 
as botanists or zoologists and not as biol- 
ogists. 

Since their discovery by Leeuwenhoek, 
some 30,000 species of protozoa have been 
described. They occur in practically all 
habitats where life can exist and are among 
the first links of the food chain on which 
all higher life depends. Floating in the 
plankton of tropic seas, they cause the 
luminous glow of waves and ship-wakes. 
Blooming off our coasts, they cause the 
red tide which deposits windrows of dead 
fish on shore. They abound in ponds and 
streams and in the soil. Their role in 
sewage purification is just beginning to be 
understood. Their skeletons cover the 
ocean floor and form the chalk we use in 
classrooms. 

As parasites, protozoa play a double 
role. Malaria is still the world's most 
important disease. Trypanosomes have 
interdicted vast African grazing lands for 
livestock. Amoebae cause dysentery in 
man, and coccidia cause it in his domes- 



tic animals. But other protozoa, packing 
the termite's hind-gut almost solidly, di- 
gest the cellulose that it eats and feed it 
with their wastes and dead bodies. Fabu- 
lous numbers of protozoa swarm in the 
rumen and reticulum of cattle and sheep 
and in the cecum and colon of the horse, 
but their role is still not clear. 

In this book we are concerned with the 
protozoan parasites of domestic animals. 
Our understanding of these forms can be 
enhanced by knowledge of the parasites of 
other animals and of free-living forms. 
For further information on the protozoa in 
general, reference is made to Doge'l (1951), 
Grasse (1952-53), Grell (1956), Hall (1953), 
Hyman (1940), Kudo (1954), Reichenow 
(1949-53) and Wenyon (1926). 



STRUCTURES 

The structures of protozoa are not 
referred to as organs as in higher animals 
but as organelles, organs being composed 
of cells and organelles being differentiated 
portions of a cell. 

NUCLEI 

Protozoa contain one or more nuclei, 
which may be of several types. In the 
protozoa other than ciliates, the nucleus 
is vesicular, and all the nuclei in the same 
individual look alike. There are two types 
of vesicular nuclei. In one type, an endo- 
some is present. The endosome is a more 
or less central body with a negative Feul- 
gen reaction and therefore without deoxy- 
ribonucleic acid. The chromatin, which 
is Feulgen positive and which forms the 
chromosomes, lies between the nuclear 
membrane and the endosome. This type 
of nucleus is found in the trypanosomes, 
parasitic amoebae and phytoflagellates. 
In the other type of vesicular nucleus, 
there is no endosome, but there may be 
one or more Feulgen-positive nucleoli. 
In these, the chromatin is distributed thru- 
out the nucleus. This type of nucleus is 
found in the Telosporasida, hypermasti- 
gorid flagellates, opalinids, dinoflagel- 
lates, and radiolaria. 



20 



INTRODUCTION TO THE PROTOZOA 



In the ciliates there are two types of 
nucleus which look different, and each 
individual has at least one of each. The 
niicronucleiis is relatively small; it di- 
vides by mitosis at fission and apparently 
controls the reproductive functions of the 
organism. The ))iac runnel ens is relatively 
large; it divides amitotically at fission and 
apparently has to do with the vegetative 
functions of the organism. Both these 
nuclei appear quite homogeneous in com- 
position in contrast to the vesicular nuclei 
of other protozoa. 



LOCOMOTION 

Protozoa move by means of flagella, 
cilia or pseudopods. A flagelhim is a 
whip-like organelle composed of a central 
axoneme and an outer sheath. The axo- 
neme arises from a basal granule or 
blepharoplast in the cytoplasm. The axo- 
neme has been shown by electron micro- 
scopy to be composed of 9 peripheral and 
2 central fibrils. In some species a fla- 
gellum may pass backward along the body, 
being attached to it along its whole length 
or at several points to form an nndulating 
membrane. Flagella are found in the 
Mastigasida and in the flagellate stages of 
the Sarcodasida and Telosporasida. 

A cilium is an eyelash-like organelle 
resembling a small flagellum. It has a 
sheath, basal granule and axoneme. In 
Paramecium and other forms, the axo- 
neme is composed of 9 peripheral and 2 
central fibrils. Cilia are found in the 
Ciliasida. The less specialized ciliates 
have large numbers of cilia which are 
arranged in rows and beat synchronously. 
In the more specialized ciliates, special 
locomotory organelles have been devel- 
oped by fusion of cilia. A cirrus is a tuft 
of fused cilia embedded in a matrix. A 
membranelle is a more or less triangular 
flap formed by the fusion of two or more 
transverse rows of cilia; membranelles 
are found especially around the mouth. 
An undulating membrane (not to be con- 
fused with the undulating membrane of 
flagellates) is formed by the fusion of one 
or more longitudinal rows of cilia; they 
occur in the oral groove of some ciliates. 



A pseudopod is a temporary locomo- 
tory organelle which can be formed and 
retracted as needed. There are four types 
of pseudopod. A lobopod is a relatively 
broad pseudopod with a dense outer layer 
and a more fluid inner zone; lobopods are 
found in the amoebae and some flagellates. 
Afilopod is a slender, hyaline pseudopod 
which tapers from its base to its pointed 
tip; filopods tend to anastomose and may 
fuse locally to produce thin films of cyto- 
plasm; they contain no cytoplasmic gran- 
ules. A tnyxopod [rhizopod, reticnlupod) 
is a filamentous pseudopod with a dense 
inner zone and a more fluid outer layer 
in which cytoplasmic granules circulate; 
myxopods branch and anastomose to form 
complex networks which are used for 
trapping food and also for locomotion; 
they are found in the Foraminiferorida. 
An axopod is a slender pseudopod which 
projects from the body without branching 
or anastomosing; it is composed of a thin 
outer layer of fluid cytoplasm and an axial 
filament composed of a fibrillar tube con- 
taining a homogeneous core; axopods are 
found in the Heliozoorida and Radiolari- 
orida. 

Locomotion can also be effected by 
bending, snapping or twisting of the whole 
body. A number of protozoa employ this 
method. 

There is still another type of locomo- 
tion, gliding, exemplified by Toxoplasma, 
Sarcocystis, coccidian merozoites, greg- 
arines and Labyrintlinla, in which the body 
glides smoothly along without benefit of 
any apparent locomotor organelles, change 
in shape or other visible cause. Kummel 

(1958) found by means of electron micro- 
graphs that the outer surface of certain 
gregarines {Gregarina cuneata, G. poly- 
morpfia, Beloides sp.) is thrown into a 
series of deep, microscopic folds which 
he thought produce mucus. Beneath these 
folds in the pellicle are fibrils which he 
thought contract to move the organism 
along a mucous track. Jarosch (1959) 
thought that the gliding of Gregarina, 
Euglena and various single-celled plants 
is caused by superficial fibrils thrusting 
against extruded mucus. Beams et at. 

(1959) found numerous ultramicroscopic 



INTRODUCTION TO THE PROTOZOA 



21 



folds in the surface membrane and an 
ultramicro^scopic network of fibrils about 
50 to 200 A in diameter in the ectoplasm 
of the trophozoites of Gregarina rigida 
from the grasshopper. They believed that 
gliding is probably accomplished by move- 
ment of the body surface in contact with 
the substrate and that the mucus which is 
secreted may possibly provide a suitable 
surface for locomotion. Ludvik (1958) 
observed superficial, longitudinal fibrils 
in electron micrographs of Sarcocystis 
tenella. However, a definitive explana- 
tion of the mechanism of gliding still 
eludes us. 



EXCRETORY ORGANELLES 

Excretion in the Protozoa is either 
thru the body wall or by means of a con- 
tractile vacuole which may be simple or 
may be associated with a system of feeder 
canals or vacuoles. Contractile vacuoles 
are probably more important as osmoreg- 
ulatory organelles than for excretion. 
They maintain water balance by removing 
excess water from the cytoplasm and 
passing it out of the body. They are found 
in fresh-water protozoa but are absent in 
most marine and parasitic protozoa. How- 
ever, some of the latter, including Balan- 
tidiuni and trypanosomes, contain them. 



ORGANELLES ASSOCIATED 
WITH NUTRITION 



OTHER ORGANELLES 



Nutrition among the protozoa may be 
of several types. Rather elaborate clas- 
sifications have been proposed by some 
authors, but three types are sufficient for 
our purposes. In holophytic nutrition, 
which is characteristic of the phytoflagel- 
lates, carbohydrates are synthesized by 
means of chlorophyll which is carried in 
chroiuatophores , which vary consider- 
ably in size, shape and number. 

In holozoic nutrition, particulate food 
material is ingested thru a temporary or 
permanent mouth. A temporary mouth is 
formed by amoebae when they engulf their 
food. A permanent mouth is a cytostome. 
It may be simple or it may lead into a 
cytopharynx. In many ciliates the area 
around the cytostome forms a peristome, 
and there may be a number of other spe- 
cialized structures associated with it. 
Particulate food passes into a. food vacuole 
in the cytoplasm, where it is digested. 
The indigestible material may be extruded 
from the body either thru a temporary 
opening or thru a permanent cytopyge. 

In saprozoic nutrition, no specialized 
organelles are necessary, nutrients being 
absorbed thru the body wall. This type is 
found in many protozoa, and may be pres- 
ent along with holophytic or holozoic nu- 
trition. 



Protozoa have many other specialized 
organelles which are found in different 
groups. These will be described in the 
appropriate places below. 



REPRODUCTION AND LIFE CYCLES 

Reproduction in the Protozoa may be 
either asexual or sexual. The commonest 
type of asexual reproduction is binary 
fission, i.e., each individual divides into 
two. The plane of fission is longitudinal 
in the flagellates and transverse in the 
ciliates. Cytoplasmic division follows 
nuclear fission and separation of the 
daughter nuclei. Vesicular nuclei and 
micronuclei divide mitotically; macronu- 
clei divide amitotically. 

Multiple fission or schizogony is 
found mostly in the Telosporasida. In this 
type of fission, the nucleus divides several 
times before the cytoplasm divides. The 
dividing cell is known as a schizont, 
agamont or segmenter, and the daughter 
cells are merozoites or schizozoites. 
Nuclear division, again, is mitotic. 

A third type of asexual division is 
budding. In this process, a small daugh- 
ter individual is separated off from the 



22 



INTRODUCTION TO THE PROTOZOA 



Side of the mother and then grows to full 
size. 

Internal budding or endodyogeny has 
been described in Toxoplasma and Bes- 
noitia. Two daughter cells are formed 
within the mother cell and then break out, 
destroying it (Goldman, Carver and Sul- 
zer, 1958). 

Several types of sexual reproduction 
have been described, but only two occur 
in parasitic protozoa. In conjugation, 
which is found among the ciliates, two in- 
dividuals come together temporarily and 
fuse along part of their length. Their 
macronuclei degenerate, their micronu- 
clei divide a number of times, and one of 
the resultant haploid pronuclei passes 
from each conjugant into the other. The 
conjugants then separate, and nuclear re- 
organization takes place. 

In syngamy, two gametes fuse to form 
a zygote. If the gametes are similar in 
appearance, the process is called isogamy; 
if they are different, it is anisogamy, the 
smaller gamete being the microgamete 
and the larger one the macrogamete. The 
gametes may be produced by special cells, 
the microgametocytes and macrogamet- 
ocytes, respectively. These are also 
sometimes called gamonts. The zygote 
may or may not then divide by multiple 
fission to form a number of sporozoites. 
The process of gamete formation is known 
as gametogony. It may differ in different 
groups, and will be described in the ap- 
propriate places below. 

Some protozoa form resistant cysts 
or spores. A cyst results from the for- 
mation of a heavy wall around the whole 
organism. Spores are produced within the 
organism by the formation of heavy walls 
around a number of individuals which have 
been produced by multiple fission or other- 
wise. This process, known as sporogony, 
ordinarily follows syngamy. Each spore 
may contain one or more individual organ- 
isms or sporozoites. 

The vegetative, motile stage of a 
protozoon is known as a tropliozoite. 



HISTORY 

The first person to see protozoa was 
the Dutch microscopist, Antony van Leeu- 
wenhoek (1632-1723). He used simple 
lenses which he ground himself and which 
gave magnifications as high as 270 times. 
His letters to the Royal Society are a 
classic of biology. Between 1674 and 1716, 
Leeuwenhoek described many free-living 
protozoa, among them, according to Dobell 
(1932), being Euglena, Volvox and Vorti- 
cella. Huygens in 1678 was the first to 
describe Paramecium. Classic work on 
free-living protozoa was done by O. F. 
Milller (1786), Ehrenberg (1830, 1838) and 
Dujardin (1841). 

The first parasitic protozoon to be 
discovered was Eimeria stiedae; Leeuwen- 
hoek found its oocysts in the gall bladder 
of an old rabbit in 1674. Later, in 1681, 
Leeuwenhoek found Giardia lamblia in his 
own diarrheic stools, and in 1683 he found 
Opalina and Nyctotherus in the intestine of 
the frog. 

The first species of Tricfiomonas, 
T. tenax, was found by O. F. Miiller in 
1773 in the human mouth; he named it 
Cer carta tenax. Donne found T. vaginalis 
in the human vagina in 1837, and Davaine 
found Trichomonas and Chilomastix in the 
stools of human cholera patients in 1854. 

The first trypanosome was discovered 
in the blood of the salmon by Valentin in 
1841, and the frog trypanosome by Gluge 
and Gruby in 1842. Lewis found the first 
mammalian trypanosome, T. lewisi, in the 
rat in 1878. Evans discovered the first 
pathogenic one, T. eva>isi, in 1881 in India, 
where it was causing the disease known as 
surra in elephants. Bruce discovered T. 
brucei in Africa in 1895 and described its 
life cycle and transmission by the tsetse 
fly in 1897. In 1902, Dutton discovered 
that African sleeping sickness of man was 
caused by T. gambiense. Leishmania 
tropica was first seen by Cunningham in 
India in 1885 and was first described and 
identified as a protozoon by Borovsky in 
Russia in 1898. Leishman and Donovan 
independently discovered Leishmania 
donovani in India in 1903. 



INTRODUCTION TO THE PROTOZOA 



23 



Histomonas meleagridis , the cause of 
blackhead of turkeys, was discovered by 
Theobald Smith in 1895. Its transmission 
in the eggs of the cecal worm was discov- 
ered by Tyzzer and Fabyan in 1922 and 
described in detail by Tyzzer in 1934. 

The first parasitic amoeba, Enta- 
moeba gbtgivalis, was found in the human 
mouth by Gros in 1849. Lewis found E. 
coli in India in 1870, and Losch found E. 
histolytica in Russia in 1875. 

Balantidium coli was discovered by 
Malmsten in 1857. 

It was not until 154 years after Leeu- 
wenhoek saw Eimeria stiedae that any 
other telosporasids were found. Then, in 
1828, Dufour described gregarines in the 
intestines of beetles, and in 1838 Hake 
rediscovered the oocysts of E. stiedae. 
The most extensive early study of the coc- 
cidia was that of Eimer (1870), who des- 
cribed a number of species in various 
animals. Schaudinn and Siedlecki (1897) 
described the gametocytes and gametes of 
coccidia and showed that they formed 
zygotes. Further studies on the life cycle 
of coccidia were published by Schaudinn 
in 1898 and 1899. Classic work on the 
coccidia of gallinaceous birds was done by 
Tyzzer (1929) and Tyzzer, Theiler and 
Jones (1932). 

The human malaria parasite was dis- 
covered in 1880 by the French army doctor, 
Alphonse Laveran. Golgi (1886, 1889) re- 
ported on its schizogony and distinguished 
the types of fever caused by the different 
species. MacCallum (1897), working with 
the closely related Haemoproteiis of birds, 
recognized that the exflagellation which 
had been seen by Laveran was microgamete 



formation, and later observed fertilization 
and zygote formation in Plasmodium fal- 
ciparum. 

Ross worked out the life cycle of the 
bird malaria parasite, Plasmodium re- 
lictum {P. praecox), in India in 1898, 
showing that it was transmitted by the 
mosquito, Culex fatigans . Working inde- 
pendently in Italy, Grassi and his collab- 
orators (1898) almost immediately after- 
ward found that human malaria is trans- 
mitted by Anopheles mosquitoes. 

Babesia bovis was discovered by 
Babes in 1888. Theobald Smith and Kil- 
borne described the cause of Texas fever 
of cattle, B. bigemina in 1893; they showed 
that it was transmitted by the tick, Boo- 
philus annulatus, being passed thru its 
eggs to the next generation of ticks which 
then infected new cattle. This was the 
first demonstration of arthropod trans- 
mission of a protozoon. 

The present century has seen many 
advances in protozoology, but there are 
many more ahead. Several times more 
species of parasitic protozoa have been 
described since 1900 than were known be- 
fore, but these are only a fraction of the 
total number. Exciting new discoveries 
are being made every year on the physi- 
ology and nutritional requirements of pro- 
tozoa (Lwoff, 1951; Hutner and Lwoff, 
1955), and the life cycles, host-parasite 
relations, and pathogenesis of many spe- 
cies are only now being worked out. The 
electron microscope and the phase micro- 
scope have opened up a whole new field 
for morphologic study, chemotherapy is 
progressing rapidly, and new discoveries 
are being made even in taxonomy, which 
most people used to consider a dead field. 



CLASSIFICATION 

Various classifications have been proposed for the Protozoa. They have been dis- 
cussed by Hall (1953) and also by Biocca (1957). The classification used in the present 
book is based on those used by Jahn and Jahn (1949) and Hall (1953), with certain mod- 
ifications; the classification of the Ciliasida is based on Corliss (1956, 1959). The uni- 
form endings for the names of higher taxa proposed by Levine (1959) are used. Most of 
the groups not of veterinary or medical interest are omitted. In addition, some genera 



24 INTRODUCTION TO THE PROTOZOA 

once thought to be protozoa but now known to be otherwise are not included. Among these 
are AnafilasDia, Eperyllirozooii and Haeniohartonella, all of which are rickettsiae; Bar- 
tonella, which is a bacterium; and Pneumocystis, which is a yeast. 

Class MASTIGASIDA 

With 1 or more flagella. Nucleus vesicular. 

Subclass PHYTOMASTIGASINA 

Typically with chromatophores. Nutrition typically holophytic. 

Order CHRYSOMONADORIDA 

With 1 to 3 flagella. Chromatophores, if present, yellow, brown, 
orange, or occasionally blue. Stored reserves include leucosin (pre- 
sumably a polysaccharide) and lipids, but no starch. 

Suborder EUCHRYSOMONADORINA 

Flagellate stage dominant. Without siliceous skeleton or peri- 
pheral zone of coccoliths. 

Family CHROMULINIDAE 
With 1 flagellum. 

Caviomonas 

Oikomonas 

Sphaeromonas 

Family OCHROMONADIDAE 

With 1 long and 1 short flagellum. 

Monas 

Family PRYMNESIIDAE 
With 3 flagella. 

Prymnesium 



INTRODUCTION TO THE PROTOZOA 2S 



Order EUGLENORIDA 

With 1 to 4 flagella. Chromatophores, if present, green. 
Stored reserves composed of paramylum. 



Suborder EUGLENORINA 

Pellicle rigid. Flagellar sheath not swollen at base. 
Seldom holozoic. 



Family ASTASHDAE 

Without chromatophores or stigma. With 1 flagellum. 
Body highly plastic, altho usually elongate spindle-shaped. 



Copromonas 

Order DINOFLAGELLORIDA 

With 2 flagella, 1 of which is transverse. Marine forms. 

Suborder GYMNODINIORINA 

Unarmored dinoflagellates (without theca). 

Family GYMNODINIIDAE 

With well-developed girdle and sulcus. Transverse fla- 
gellum typically flattened. Tentacle and ocellus absent. 

Gymnodinium 

Suborder PERIDINIORINA 

With a theca of a cellulose-like material, composed of separate 
plates. 

Family GONYAULACIDAE 

Thecal plates distinct. One antapical plate is characteristic. 

Gonyaulax 



26 INTRODUCTION TO THE PROTOZOA 



Order PHYTOMONADORIDA 

With 1 to 8 flagella. Typically with 1 green chromatophore. 
Body wall contains cellulose. Starch and lipids stored as food. 



Family CHLAMYDOMONADIDAE 

Solitary, with a well-developed membrane. 

Polytoma 

Subclass ZOOMASTIGASINA 

Without chromatophores. Nutrition holozoic or saprozoic. 

Order RfflZOMASTIGORIDA 

With both flagella and pseudopods. 

Family MASTIGAMOEBIDAE 

With 1 to 3, rarely 4 flagella. 

Histomonas 

Order PROTOMASTIGORIDA 
With 1 or 2 flagella. 

Family TRYPANOSOMATIDAE 

With 1 flagellum. Body characteristically leaf -like but 
may be rounded. With a single nucleus and a kinetoplast. 
With a basal granule from which a flagellum arises. Ex- 
clusively parasitic. 



Blastocrithidia Leptomonas 

Crilhidia Phytomonas 

Herpelo»ioiias Tyypa>ioso)ua 
Leisliuiaiiia 



Family BODONIDAE 

With 2 flagella originating anteriorly, one directed anter- 
iorly and the other posteriorly. Anterior end more or less 
drawn out. With 1 to several contractile vacuoles. 



INTRODUCTION TO THE PROTOZOA 27 



Bodo 

Cercomonas 
PleuroDionas 
Proteroinonas 



Family AMPfflMONADIDAE 

Body naked or loricate, with 2 equal flagella. 

Spiromonas 



Order POLYMASTIGORIDA 

With 3 to about 12 flagella (2 in Retortamonas) and 1, 2 or several 
nuclei. Without costa, axostyle (except in some Hexamitidae and Poly- 
mastigidae) or parabasal body. 



Family TETRAMITIDAE 

With 4 flagella, 1 or 2 of which may be trailing. 



Enteromonas 
Tetrmnitus 



Family RETORTAMONADIDAE 

With 2 or 4 flagella, of which 1 is trailing. With 1 nucleus. 
Cytostome with supporting fibrils present. 



Chilomastix 
Retortamonas 



Family CALLIMASTIGIDAE 

With a compact antero-lateral group of flagella which beat 
as a unit. With 1 nucleus. 



Callimastix 
Selenonwnas 



Family POLYMASTIGIDAE 

With 4 anterior flagella and axostyle. With 1 nucleus. 
Apparently without parabasal body. 



Monocercomonoides 



28 



INTRODUCTION TO THE PROTOZOA 



Family COCHLOSOMATIDAE 

With 6 anterior flagella, 1 axostyle and a single nucleus. 
Apparently without parabasal body. 



Cochlosoma 



Family HEXAMITIDAE 

With 6 or 8 flagella, 2 nuclei and sometimes axostyles and 
median or parabasal bodies. Bilaterally symmetrical. 



Giardia 
Hexaniila 
Octomilus 
Trepomonas 



Order TRICHOMONADORIDA 

With 3 to 6 flagella, of which 1 is trailing and may form part of an un- 
dulating membrane. With 1 or many nuclei (the forms in vertebrates 
have only 1 nucleus), but not with 2. With axostyle and parabasal body. 



Family MONOCERCOMONADIDAE 

With either a free or an adherent trailing flagellum but no 
undulating membrane or costa. 



Chilomitus 
Hexamastix 
Monocercomonas 
Protrichomonas 



Family TRICHOMONADIDAE 

With an undulating membrane and a costa. Sometimes with 
a pelta. 



Pentatrichomonas 

Trichomonas 

Tritrickomonas 

Order HYPERMASTIGORIDA 

With many flagella, 1 nucleus and often multiple axostyles and para- 
basal bodies. Intestinal parasites of termites and roaches. 

Trichonynipha 



INTRODUCTION TO THE PROTOZOA 29 

Class SARCODASIDA 

With pseudopods but without flagella or cilia. Nucleus vesicular. 

Subclass RfflZOPODASINA 

With lobopods, filopods or myxopods but without axopods. 

Order AMOEBORIDA 

With lobopods. Without test. 

Family NAEGLERIDAE 

With amoeboid and flagellate stages. 

Naegleria 
Trimastigamoeba 



Family AMOEBIDAE 

Free-living or coprozoic amoebae without a flagellate 
phase. 



Acanthamoeba Sappinia 

Hartmannella Vahlkampfia 



Family ENDAMOEBIDAE 

Parasites in the digestive tract of vertebrates and inverte- 
brates. 



Dientamoeba Entamoeba 

Endamoeba lodamoeba 

Endolimax 



Order TESTACEORIDA 

With a single-chambered test. 

Family ARCELLIDAE 

Test simple and membranous. Pseudopods filose or sim- 
ply branched. 

Chlamydophrys 



30 INTRODUCTION TO THE PROTOZOA 



Class TELOSPORASIDA 

With simple spores containing 1 to many sporozoites but without polar filaments. 
Without pseudopods, cilia or flagella (except for flagellated microgametes in some 
groups). Locomotion by body flexion or gliding. Reproduction both sexual and 
asexual. All parasitic. 



Subclass GREGARINASINA 

Mature trophozoite extracellular, large. Parasites of digestive tract and 
body cavity of invertebrates. 



Subclass COCCIDIASINA 

Mature trophozoite ordinarily intracellular, small. 

Order EUCOCCIDIORIDA 

Parasites of epithelial and blood cells of vertebrates and invertebrates. 
Life cycle involves both sexual and asexual phases. Schizogony present. 

Suborder ADELEORINA 

Macrogamete and microgametocyte associated in syzygy during 
differentiation. Microgametocyte usually produces few micro- 
gametes. Sporozoites enclosed in an envelope. Monoxenous or 
heteroxenous. 

Superfamily ADELEICAE 

Zygote inactive, may or may not develop a typical oocyst. 

Family ADELEIDAE 

Sporocysts formed in oocyst. In epithelium of gut 
and its appended organs. Chiefly in invertebrates. 

Klossia 

Family KLOSSIELLIDAE 

Typical oocyst not formed; a number of sporocysts, 
each with many sporozoites, develops within a mem- 
brane which is perhaps laid down by the host cell. 
Two to 4 non-flagellate microgametes formed by 
microgametocyte. Monoxenous, gametogony and 
schizogony occurring in different locations in the same 
host. In kidney and other organs of host. 

Klossiella 



INTRODUCTION TO THE PROTOZOA 31 



Superfamily HAEMOGREGARINICAE 

Zygote active (ookinete), secreting a flexible membrane which is 
stretched during development. Heteroxenous. Life cycle in- 
volves 2 hosts, one vertebrate and the other invertebrate. In 
cells of circulatory system of vertebrates and digestive system 
of invertebrates. 



Family HAEMOGREGARINIDAE 

Oocysts small, without sporocysts. 

Haemogregarina 

Family HEPATOZOIDAE 

Oocysts large, containing many sporocysts, each with 4 to 
12 or more sporozoites. Microgametes non-flagellate. 

Hepatozoon 



Family KARYOLYSIDAE 

Sporoblasts become sporokinetes which invade the egg of a 
mite before secreting sporocyst membrane. Sporocysts 
with numerous sporozoites. Gametocytes in erythrocytes 
of vertebrate host. 



Karyolysus 



Suborder EIMERIORINA 

Macrogamete and microgametocyte develop independently. 
Syzygy absent. Microgametocyte typically produces many micro- 
gametes. Zygote not motile. Sporozoites typically enclosed in 
a sporocyst. Monoxenous or heteroxenous. 



Family EIMERIIDAE 

Development in host cell proper. Oocysts and schizonts 
without attachment organ. Oocysts with 0, 1, 2, 4 or many 
sporocysts, each with 1 or more sporozoites. Monoxenous. 
Schizogony in the host, sporogony typically outside. Mi- 
crogametes with 2 flagella. 

Dorisiella Tyzzeria 

Einieria Wenyonella 

Isospora 



32 INTRODUCTION TO THE PROTOZOA 



Family CRYPTOSPORIDIIDAE 

Development on the surface of the host cell or within its 
striated border and not in the cell proper. Oocysts and 
schizonts with a knob-like attachment organ at some point 
on their surface. Oocysts without sporocysts. Monoxenous. 
Microgametes without flagella. 

Crxptospu)-idii(7n 



Family AGGREGATIDAE 

Development in host cell proper. Oocysts typically with 
many sporocysts. Heteroxenous. Schizogony in one host, 
sporogony in another. 

Merocystis 



Family LANKESTERELLIDAE 

Development in host cell proper. Oocysts without sporo- 
cysts, but with 8 or more sporozoites. Heteroxenous, with 
schizogony, gametogony and sporogony in a vertebrate host. 
Sporozoites in blood cells, transferred without developing 
by an invertebrate (mite or leech). Microgametes with 2 
flagella, so far as is known. 

Lankesterello 
Schellackia 



Suborder HAEMOSPORORINA 

Macrogamete and microgametocyte develop independently. Syzygy 
absent. Microgametocyte produces moderate number of micro- 
gametes. Zygote motile (ookinete). Sporozoites naked. Heter- 
oxenous. Schizogony in vertebrate host, sporogony in inverte- 
brate. Pigment (hematin) formed from host cell hemoglobin. 



Family PLASMODIIDAE 

With the characters of the suborder. 

Haemoproteus Leucocytozoon 

Hepatocystis Plasmodium 

Class PIROPLASMASIDA 

Small, piriform, round, amoeboid or rod-shaped parasites of vertebrate erythro- 
cytes and also in some cases of leucocytes or histiocytes. Pigment (hematin) not 



INTRODUCTION TO THE PROTOZOA 33 



formed from host cell hemoglobin. Without spores. Nucleus vesicular. Without 
flagella or cilia. Locomotion by body flexion or gliding. Reproduction asexual, 
by binary fission or schizogony. Existence of sexual reproduction dubious. All 
parasitic. Heteroxenous. Vectors (if known), Lxodid or argasid ticks. 

Order PIROPLASMORIDA 

With the characters of the class. 



Family BABESHDAE 

Relatively large, piriform, round or oval parasites occur- 
ring in erythrocytes of vertebrate host. Asexual reproduc- 
tion in erythrocytes by binary fission or schizogony. 

Aegyptianella 

Babesia 

Echinozoon 



Family THEILERIIDAE 

Relatively small, round, oval, irregular or rod-shaped 
parasites of erythrocytes and lymphocytes or histiocytes of 
vertebrate host. The forms in the erythrocytes may or 
may not reproduce; in the former case they divide into 2 or 
4 daughter cells. Asexual reproduction by schizogony (or 
a series of binary fissions) in lymphocytes or histiocytes 
followed by invasion of erythrocytes. 

Cytauxzoon 
Gonderia 
The Her ia 



Class TOXOPLASMASIDA 

Without spores. With cysts or pseudocysts containing many naked trophozoites. 
Nucleus vesicular. Without flagella or cilia. Locomotion by body flexion or glid- 
ing. Reproduction asexual, by binary fission or endodyogeny (and possibly by 
schizogony in young cysts). All parasitic. Monoxenous. 



Order TOXOPLASMORIDA 

With the characters of the class. 



Family SARCOCYSTIDAE 

With cysts. Multiplication by binary fission, and possibly 
also by schizogony in young cysts. 

Sarcocystis 



34 INTRODUCTION TO THE PROTOZOA 



Family TOXOPLASMATIDAE 

With pseudocysts and probably true cysts as well. Multi- 
plication by binary fission or endodyogeny and possibly by 
schizogony in young pseudocysts. 

Besnoitia 

Encephalilozoon 

Toxoplasma 



Class CNIDOSPORASIDA 

With spores containing polar filaments. Nucleus vesicular. All parasitic. 

Order MYXOSPORORIDA 

Spores comparatively large, with bivalve shell and 1 to 4 polar cap- 
sules. Parasites of lower vertebrates, especially fish. 

Order MICROSPORORIDA 

Spores comparatively small, with 1 -piece shell and 1 or 2 polar fila- 
ments. Typically parasites of invertebrates and fish. 



Class CILIASIDA 

With two types of nucleus--macronucleus and micronucleus. With cilia at some 
stage of the life cycle. 



Subclass HOLOTRICHASINA 

Without or with poorly developed adoral zone of membranelles (except in 
Peritrichorida). 



Order GYMNOSTOMORIDA 

Cytostome opens directly at surface or else into a slight depression 
which lacks well-developed peristomial ciliature. 



Family BUETSCHLIIDAE 

Cytostome usually at anterior end. Anterior concretion- 
vacuole (possibly a statocyst), one or more contractile 
vacuoles and posterior cytopyge present. Cilia uniformly 
distributed over body or restricted to certain areas. 

Alloiozona Bundleia 

Ampullacula Didesmis 



INTRODUCTION TO THE PROTOZOA 



35 



Blepharoconus Holophryoides 

Blephah'oprosthium Parnisotrichopsis 

Blephayosphaera Polymorphella 

Blepharozoum Prorodonopsis 

BuetschUa Sulcoarcus 



Family PYCNOTRICHIDAE 

Body completely ciliated. A long groove usually leads to 
the cytostome, which may lie near the middle or at the 
posterior end of the body. 



Bnxtouello 
Infuiidibiiloriiiui 



Order SUCTORIORIDA 

Young with cilia; adults with tentacles. 

Family ACINETIDAE 

With endogenous budding. Tentacles capitate, usually ar- 
ranged in groups. Lorica often present. Stalk present or 
absent. 

Allantosoma 

Order TRICHOSTOMORIDA 

Cytostome usually at base of well-defined oral groove or pit, the wall 
of which bears 1 or more dense fields of adoral cilia; in some primi- 
tive forms the cytostome is almost at the anterior end, but more often 
it is shafted posteriorly on the ventral surface. Spiral torsion of the 
body occurs in some genera. 

Family BLEPHAROCORYTHIDAE 

Somatic ciliation reduced to a few anterior and posterior 
fields, with 1 or 2 groups of anal cilia near the cytopyge 
and 2 or 3 distinct anterior groups. Cytostome antero- 
ventral, opening into a long ciliated pharynx. 

Blepharocorys Qchoterenaia 

Charonina 

Family CYATHODINIIDAE 

Cilia limited to anterior half of body. Peristome a non- 
ciliated, rather long triangular groove. Slender trichites 



36 INTRODUCTION TO THE PROTOZOA 



extend from a row of papillae along left rim of peristome, 
and an adoral cilium arises from each papilla. 

Cyathodinium 



Family ISOTRICHIDAE 

Mouth terminal or subterminal. Pharynx ciliated, with 
longitudinal striations in its wall. Somatic ciliation com- 
plete and practically uniform. 

Dasytriclia 
Isotricha 



Family PARAISOTRICHIDAE 

Mouth subterminal, opening just posterior to concretion 
vacuole. Somatic ciliation complete, with an anterior tuft 
of longer cilia. 

Paraisotricha 



Family BALANTIDIIDAE 

Somatic ciliation complete, with cilia arranged in approx- 
imately longitudinal rows. Peristome a pouch with a tri- 
angular opening, thru which the short adoral band of mem- 
branelles is not easily seen from the outside. Numerous 
long fibrils extend into the endoplasm from the basal gran- 
ules of cilia and membranelles. Concretion vacuole absent. 

Balantidium 



Order HYMENOSTOMORIDA 

Adoral cilia fused in membranes, the number, size and arrangement 
of which vary in different genera. 



Family OPHRYOGLENIDAE 

With a ciliated vestibule (peristome), an invagination of the 
body wall, and a pharynx which opens into the vestibule. A 
retractile body ("body of Lieberkiihn", "watch-glass body") 
lies just to the left of the vestibule. Reproduction takes 
place within a cyst. The resultant young ciliates (tomites) 
leave the cyst, develop into trophic therontes and then into 
large trophonts which encyst. 

Ichthyophthirius 



INTRODUCTION TO THE PROTOZOA 37 



Family PARAMECIIDAE 

With oral groove extending from the anterior end toward 
the middle of the body. Somatic ciliation complete and 
essentially uniform. Adoral ciliature including a dorsal 
zone of long cilia (quadripartite membrane) and 2 peniculi 
(dense bands of cilia extending in a shallow spiral toward 
the cytostome). 

Paramecium 



Family TETRAHYMENIDAE 

Adoral ciliature composed of 3 membranelles lying to the 
left in the oral pouch; a fourth, paroral membrane extends 
along its right margin. One or more stomatogenous rows 
of cilia end at the posterior margin of the oral pouch. 

Tetrahymena 



Subclass SPIROTRICHASINA 

Bases of adoral zone membranelles usually at right or oblique angle to long 
axis of adoral zone; this series of membranelles extends anteriorly from the 
left margin of the cytostome; the basal plate of each membranelle contains 
2, 3 or rarely 4 rows of basal granules. 



Order HETEROTRICHORIDA 

Somatic ciliation usually complete. Peristome usually elongated and 
fairly narrow, with adoral zone of membranelles along left wall. An 
undulating membrane often extends for some distance along right mar- 
gin of peristome. 



Family PLAGIOTOMIDAE 

Body densely ciliated. Adoral zone of membranelles well 
defined. Undulating membrane at right margin of peri- 
stome. 



Nyctotherus 



Order ENTODINIORIDA 

Ciliation may be limited to the adoral zone; there may be 1 or more 
additional bands or groups of membranelles. Skeletal plates usually 
present. 



38 



INTRODUCTION TO THE PROTOZOA 



Family OPHRYOSCOLECIDAE 

With not more than 1 band of membranelles in addition to 
adoral zone. 



Amphacanthus 

Caloscolex 

Cunhaia 

Diplodinium 

Diploplastron 

Elytroplastron 



Enoploplastron EiuUplodinuim 



Enlodiniiim 

Eodinium 

Epidinimn 

Epiplastron 

Eremoplastron 



Meladiniujn 

Ophryoscolex 

Opisthotriclmm 

Ostracodinium 

Polyplastron 



Family CYCLOPOSTHIIDAE 

With 2 or more bands of membranelles in addition to 
adoral zone. 



Cochliatoxum 

Cycloposthium 

Ditoxuni 

Elepliantophilus 

Polydiniella 



Prototapirella 

Spirodinium 

Tetratoxuni 

Tlioracodinium 

Triadinium 



Trifasciciilaria 
Tripalmaria 
Tripliimaria 
Troglodytella 



Class PROTOCILIASIDA 

With cilia. Nucleus vesicular. 



Opalina 



REFERENCES 

The following list includes not only the papers cited in 
this chapter but also a number of general references on the 
Protozoa and on veterinary and medical protozoology. 

Beams, H. W. , T. N. Tahmisian, R. L. Devine and E. 

Anderson. 1959. J. Protozool. 6:136-146. 
Becker, E. R. 1959. Protozoa. Chap. 36inBiester, H. E. 

and L. H. Schwarte, eds. Diseases of poultry. 4th ed. 

Iowa St. Univ. Press, Ames. pp. 828-916. 
Biocca, E. 1957(1956). Alcune considerazioni suUq sis- 

tematica dei protozoi e Sulla utilita di creare una nuova 

closse di protozoi. Rev. Brosil. Malariol. 8:91-102. 
Boyden, A. 1957. Are there any "acellular animals"? 

Science 125:155-156. 
Corliss, J. O. 1956. On the evolution and systematics of 

ciliated protozoa. Syst. Zool. 5:68-91, 121-140. 
Corliss, ]. O. 1959. An illustrated key to the higher 

groups of the ciliated protozoa, with definitions of terms. 

J. Protozool. 6:265-284. 
Craig, C. F. 1948. Laboratory diagnosis of protozoan dis- 
eases. 2nd ed. Lea & Febiger, Philadelphia, pp. 384. 



Curasson, G. 1943. Traite de protozoologie veterinaire et 

comparee. Vigot Freres, Paris. 3 vols. pp. xcv + 1268. 
Dobell, C. 1932. Anthony van Leeuwenhoek and his "little 

animals. " Harcourt, Brace, New York. pp. vii + 435. 
Dogiel, V. A. 1951. Obshchaya protistologiya. Gosud. 

Izdat. Sovet. Nauka, Moscow, pp. 603. 
Dujardin, F. 1841. Histoire noturelle des zoophytes infus- 

oires. etc. Roret, Paris, pp. xii + 684. 
Ehrenberg, C. G. 1830. Organisation, systematik und geo- 

graphisches Verhaltniss der Infusionsthierchen. Konig. 

Akad. Wissenschaft, Berlin, pp. 108. 
Ehrenberg, C. G. 1838. Die Infusionsthierchen als voUkom- 

mene Organismen, etc. L. Voss, Leipzig, pp. xviii 

+ 547. 
Goldman, M. , R. K. Carver and A. J. Sulzer. 1958. Re- 
production of Toxoplasma gondii by internal budding. 

J. Parasit. 44:161-171. 
Crosse, P. -P. , ed. 1952-53. Traite de zoologie. Vol. I, 

Fuse. 1, 2. Masson, Paris, pp. xii + 2231. 
Grell, K. G. 1956. Protozoologie. Springer, Berlin, pp. 

vii + 284. 
Hall, R. P. 1953. Protozoology. Prentice-Hall, New York, 

pp. 682. 



INTRODUCTION TO THE PROTOZOA 



39 



Hoare, C. A. 1949. Handbook of medical protozoology. 

Balliere, Tindall G Cox, London, pp. xv + 334. 
Hutner, S. H. and A. Lwoff, eds. 1955. Biochemistry and 

physiology of protozoa. Vol. 2. Academic Press, New 

York. pp. xiii + 388. 
Hyman, L. H. 1940. The invertebrates. Vol. 1. Protozoa 

through Ctenophorc. McGraw-Hill, New York. pp. xii 

+ 726. 
John, T. L. and F. F. Jahn. 1949. How to know the pro- 
tozoa. Brown, Dubuque, la. pp. 234. 
Jarosch, R. 1959. Zur Gleitbewegung der niederen Organ- 

ismen. Protoplasma 50:277-289. 
Jirovec.O. , K. Wenig, B. Pott, E. Bartos, J. Weiser and 

R. Sramek-Husek. 1953. Protozoologie. Nak. Cesk. 

Akad. Ved, Prague, pp. 643. 
Kirby, H. 1950. Materials and methods in the study of 

protozoa. Univ. Calif. Press, Berkeley, pp. x + 72. 
Kudo, R. R. 1954. Protozoology. 4th ed. Thomas, 

Springfield, 111. pp. xi + 966. 
Kummel, G. 1958. Die Gleitbewegung der Gregarinen. 

Elektronmikroskopische und experimentalle Unteisuch- 

ungen. Arch. Protist. 102:501-522. 



Levine, N. D. 1959(1958). Uniform endings for the names 
of higher taxG. Syst. Zool. 7:134-135. 

Ludvik, J. 1958. Elektronenoptische Befunde zur Morphol- 
ogie der Sarcosporidien (Sarcocystis tenella Railliet 1886). 
Zbl. Bakt. I. Orig. 172:330-350. 

Lwoff, A., ed. 1951. Biochemistry and physiology of pro- 
tozoa. Vol. 1. Academic Press, New York. pp. x 
+ 434. 

Morgan, B. B. and P. P. Hawkins. 1952. Veterinary proto- 
zoology. 2nd ed. Burgess, Minneapolis, pp. vii 
+ 187. 

Mullet, O. F. 1786. Animalcule Infusoria fluviatilia et 
marina, quae detexit, systematice descripsit et ad vivum 
delineari curavit, etc. Typis N. MoUeri, Hauniae. pp. 
Ivi -I- 367. 

Reichenow, E. 1949-53. Lehrbuch der Protozoenkunde. 
6th ed. 3 vols. Fischer, Jena. pp. viii + 1213. 

Richardson, U. F. and S. B. Kendall. 1957. Veterinary 
protozoology. 2nd ed. Oliver G Boyd, Edinburgh, pp. 
xii + 260. 

Wenyon, C. M. 1926. Protozoology. 2 vols. Wood, New 
York. pp. xvi + 1563. 



Chapter 3 



THE 
HBmHAGEUATBS 



The flagellates belong to the class 
Mastigasida. They have 1 or more fla- 
gella, and a few have pseudopods as well. 
Their nutrition is holophytic, holozoic or 
saprozoic. They multiply by longitudinal 
binary fission, and many produce cysts. 

The class is divided into 2 subclasses, 
Phytomastigasina and Zoomastigasina. 
The former contains the phytoflagellates, 
the great majority of which are free-living 
and holophytic. Those of parasitic interest 
will be discussed in Chapter 6. 

It is convenient for our purposes to 
divide the Zoomastigasina into 2 groups, 
the hemoflagellates which live in the blood, 
lymph and tissues, and the other flagel- 
lates which live in the intestine and other 
body cavities. 



FAMILY TRYPANOSOMATIDAE 

The hemoflagellates all belong to the 
family Trypanosomatidae. Members of 
this family have a leaf-like or sometimes 
a rounded body containing one nucleus. 
They have a single flagellum which arises 
from a basal granule or blepharoplast 
posterior to the end of an elongate blind 
pouch or reservoir and passes anteriorly, 
usually extending beyond the body. A con- 
tractile vacuole opens into the reservoir, 
but both of these structures can be seen 
only with the phase microscope and not 
with the ordinary light microscope (Ket- 
terer, 1952; Cosgrove and Kessel, 1958; 
Clark, 1959). The flagellar axonenie is 
composed of 9 peripheral and 2 central 
fibrils (Anderson, Saxe and Beams, 1956). 
An undulating membrane is present in 
some genera; the flagellum lies in its outer 
border. Posterior to the basal granule is 
a rod-shaped or spherical kinetoplast con- 
taining deoxyribonucleic acid. The struc- 
ture of the kinetoplast as seen in electron 
micrographs has been interpreted in dif- 
ferent ways. According to Anderson, Saxe 
and Beams (1956), it consists of lamellae 
oriented at right angles to its long axis; 



- 40 



THE HEMOFLAGELLATES 



41 



Meyer and Queiroga (1960) called it an 
apparently lamellar mass located in a 
vacuole-Iike space; Hans Ris (unpublished) 
said that the lamellae represent sections 
of a continuous spiral; Clark and Wallace 
(1960) considered the kinetoplast to be a 
mitochondrion containing antero-posteriorly 
oriented anastomosing fibers. Under the 
ordinary light microscope, the kinetoplast 
and blepharoplast may appear to be fused. 
Mitochondria and volutin granules have also 
been seen in electron micrographs. 

Members of this family were originally 
parasites of the intestinal tract of insects, 
and many are still found only in insects. 
Others are heteroxenous, spending part of 
their life cycle in a vertebrate and part in 
an invertebrate host. 

In the course of their life cycles, mem- 
bers of one genus may pass thru forms 
morphologically similar to those of other 
genera. These stages are named for the 
genera which they resemble. In the tryp- 
anosome form, which is perhaps the most 
advanced, the kinetoplast and basal granule 
are near the posterior end and the undulat- 
ing membrane runs the length of the body. 
In the crithidial form, the kinetoplast and 
basal granule are just anterior to the nu- 
cleus and the undulating membrane runs 
forward from there. In the leptomonad 
form, the kinetoplast and basal granule are 
still further forward in the body and there 
is no undulating membrane. In the leish- 
manial form, the body is rounded and the 
flagellum has degenerated into a tiny fibril 
which remains inside the body (Fig. 1). 
Further information on life cycles and 
morphology is given by Noble (1955). 

There are several genera in the fam- 
ily Trypanosomatidae. Members of the 
genus Trypanosoma are heteroxenous and 
pass thru leishmanial, leptomonad, cri- 
thidial and trypanosome stages in their 
life cycle. In some species, only trypan- 
osome forms are found in the vertebrate 
host, while in other, more primitive ones, 
both leishmanial and trypanosome forms 
are present. 

Members of the genus Blastocrithidia 
are monoxenous in arthropods and other 




B 



D 



Fig. 1. Forms of the Trypanosomatidae. 
A. Leishmanial form. B. Lep- 
tomonad form. C. Crithidial 
form. D. Trypanosome form. 
(Original) 

invertebrates. They pass thru crithidial, 
leptomonad and leishmanial stages in 
their life cycle. This generic name was 
introduced by Laird (1959) for the crithi- 
dial species commonly and erroneously 
assigned to the genus Crithidia. As both 
Laird (1959), Wallace (1943) and Clark 
(1959) have shown, the type species of 
Crithidia. from mosquitoes, C. fascicu- 
lata, is a short, truncate form with a 
stiff flagellum emerging from a funnelled 
anterior depression, and never has an 
undulating membrane. However, the term 
crithidial is so deeply Embedded in our 
terminology as referring to forms with an 
undulating membrane that it is best to re- 
tain it. 

Members of the genus Crithidia are 
monoxenous in arthropods. Despite their 
name, they have only a leptomonad stage. 

Members of the genus Leptonionas 
are monoxenous in invertebrates. They 
pass thru leptomonad and leishmanial 
stages in their life cycle. 

Members of the genus Leishmania 
are heteroxenous, passing thru the leish- 
manial stage in their vertebrate host and 
the leptomonad stage in their invertebrate 
host or in culture. 

Members of the genus Herpetomonas 
are monoxenous in invertebrates. They 
pass thru trypanosome, crithidial, lepto- 
monad and leishmanial stages in their life 
cycle. The trypanosome form in this 
genus differs from that of Trypanosoma 



42 



THE HEMOFLAGEUATES 



in that the undulating membrane lies in a 
long reservoir which runs the whole length 
of the body and opens at the anterior end, 
whereas in Trypanosoina the reservoir is 
very short and opens laterally near the 
posterior end so that the undulating mem- 
brane runs along the side of the body 
(Clark, 1959). 

Members of the genus Phylomonas 
are heteroxenous in the latex of plants and 
hemipterous insects, passing thru lepto- 
monad and leishmanial stages in their life 
cycle. They are found in milkweeds and 
related plants, and cause the normally 
milky sap to become colorless. 

The only genera parasitic in domestic 
animals and man are Trypanosoma and 
Leishmania. Since, however, their 
stages in the invertebrate vector are mor- 
phologically similar to those of the genera 
confined to invertebrates, one cannot be 
positive, when he finds an infected inver- 
tebrate, whether it is infected with a para- 
site of vertebrates or with one of its own. 
It is possible, too, that some of the forms 
which we now think are confined to inverte- 
brates may actually be normal parasites 
of some wild vertebrates. 



make it practically impossible to raise 
livestock in many parts of the tropics 
which would otherwise be ideal. Accord- 
ing to Hornby (1949), "Trypanosomiasis 
is unique among diseases in that it is the 
only one which by itself has denied vast 
areas of land to all domestic animals 
other than poultry. The areas of complete 
denial are all in Africa and add up to per- 
haps one quarter of the total land surface 
of this continent. " Some, but not all, of 
the African species are transmitted by 
tsetse flies. These flies occupy almost 
4 million square miles, an area larger 
than the United States, and this whole re- 
gion is under the threat of trypanosomosis. 

In a recent Hollywood epic on South 
African history, there is a scene in which 
a line of Boer covered wagons on the Great 
Trek to the north is attacked by Zulus. 
The warriors pour over the hills, the wag- 
ons form a circle with the women and chil- 
dren in the center, and the Boer men pre- 
pare to fight. It is just like a scene from 
the American Wild West, with the Indians 
attacking a wagon train of pioneers. But 
there is one difference- -the Zulus had no 
horses, and made their attack on foot. 
The reason? Trypanosomosis. 



Genus lITfPANOSOmA Gruby, 1843 

Members of this genus occur in all 
classes of vertebrates. They are para- 
sites of the circulatory system and tissue 
fluids, but some, such as T. cruzi, may 
actually invade cells. Almost all are 
transmitted by blood-sucking invertebrates. 
Most species are probably non-pathogenic, 
but the remainder more than make up for 
their fellows. 

Trypanosomosis is one of the world's 
most important diseases of livestock and 
man. Trypanosomes cause African sleep- 
ing sickness and Chagas' disease in man 
and a whole series of similar diseases in 
domestic animals. They are relatively 
unimportant in North America, but they 



A large number of species of Trypano- 
soma has been named. At one time it 
was customary, and still is to some extent, 
to give different names to trypanosomes 
from different hosts. Many of these names 
are still valid, but as we learn more and 
more about the host-parasite relations and 
epidemiology of the trypanosomes, many 
other names have fallen into synonymy. 
No attempt will be made here to list all 
the synonyms of each species, but the more 
important ones will be mentioned. 

Trypanosomes are classified in groups 
on the basis of their morphology, life cy- 
cles and other biological characteristics. 
The validity of this grouping is shown by 
the fact that their metabolic characteris- 
tics, which vary widely, fall into the same 
groups. 



THE HEMOFLACELLATES 43 



The following outline classification of trypanosomes of veterinary and medical im- 
portance is based on Hoare (1957, 1959). Sections on metabolism based on von Brand 
(1956), Ryley (1956) and von Brand and Tobie (1959), and a section on avian trypanosomes 
have been added. 



I. PARASITES OF MAMMALS 

A. Morphology in Mammal 

Kinetoplast not terminal, large. Free flagellum always present. Posterior 
end of body pointed. Division in crithidial, leishmanial or trypanosome stages. 

Biology 

Multiplication in mammal typically discontinuous. Development of metacyclic 
trypanosomes in hind gut (posterior station) of vector (in T. raiigeli also in 
salivary glands: anterior station). Transmission contaminative thru feces (in 
T. rangeli also inoculative). Except for T. cruzi. trypanosomes slightly or not 
pathogenic. 

Metabolism 

Blood forms have high respiratory quotient and low sugar consumption, produc- 
ing acetic, succinic and lactic acids aerobically and succinic, lactic, acetic and 
pyruvic acids anaerobically. Cyanide markedly inhibits oxygen consumption. 
Sulfhydryl antagonists moderately inhibit oxygen consumption. Culture forms 
have high respiratory quotient and moderately high sugar consumption, produc- 
ing acetic and succinic acids aerobically and succinic and acetic acids anaero- 
bically; cyanide markedly inhibits oxygen consumption; sulfhydryl antagonists 
moderately to markedly inhibit oxygen consumption. Cytochrome pigments, 
cytochrome and succinic oxidase activity are present in T. cruzi and T. lewisi. 

1. LEWISI GROUP 

a. Mode of reproduction unknown. 
T. nielophagium of sheep. 

b. Reproduction by binary fission in crithidial stage. 
T. theileri of cattle. 

c. Reproduction by multiple fission in crithidial stage. 
T. lewisi of rats. 

T. duttoni of mice. 

d. Reproduction by binary fission in leishmanial stage. 
T. cruzi of man, dog, opossum, monkeys. 

e. Reproduction by multiple fission in leishmanial stage. 
T. nabiasi of rabbits. 

f. Reproduction by binary fission in trypanosome stage. 
T. rangeli of man, dog, opossum, monkeys. 



44 THE HEMOFLAGELLATES 



B. Morphology in Mammal 

Kinetoplast terminal or subterminal. Posterior end of body blunt. Division in 
trypanosome stage. 

Biology 

Multiplication in mammal continuous. Development of metacyclic trypanosomes 
in proboscis or salivary glands (anterior station) of vector (except evansi sub- 
group). Transmission inoculative, thru bite (except T. equip erduni). Trypano- 
somes pathogenic. 

1. VIVAX GROUP 

Morphology in Mammal 

Monomorphic forms. Posterior end of body typically rounded. Free fla- 
gellum always present. Kinetoplast large, terminal. Undulating mem- 
brane inconspicuous. 

Biology 

Development in Glossina, in proboscis only. T. vivax is also transmitted 
mechanically by tabanids. 

Metabolism 

Blood forms have high respiratory quotient and high sugar consumption, 
producing pyruvic, acetic, lactic acids and glycerol aerobically and glycerol, 
pyruvic, lactic, and acetic acids anaerobically. Cyanide does not inhibit 
oxygen consumption. Sulfhydryl antagonists markedly inhibit oxygen con- 
sumption. Cytochrome and succinic oxidase activity are present. 

a. Long forms 

T. vivax oi cattle, sheep, goats, antelope. 

b. Short forms 

T. uniforme of cattle, sheep, goats, antelope. 

2. CONGOLENSE GROUP 

Morphology in Mammals 

Monomorphic or polymorphic forms. Free flagellum absent or present. 
Kinetoplast medium, typically marginal. 

Biology 

Development in Glossina, in midgut and proboscis. 

Metabolism 

Blood forms have high respiratory quotient and high sugar consumption, 
producing acetic acid, succinic acid, glycerol and pyruvic acid aerobically 



THE HEMOFLAGELLATES 45 



and succinic acid, glycerol, acetic acid and pyruvic acid anaerobically. 
Cyanide and sulfhydryl antagonists moderately inhibit oxygen consumption. 
Cytochrome pigments are absent but cytochrome and succinic oxidase ac- 
tivity are present. Culture forms of T. co)igoleuse have R. Q. of 0.9, 
produce pyruvate, acetate and smaller amounts of lactate, succinate and 
glycerol aerobically, and pyruvate, acetate and succinate with small amounts 
of glycerol and no carbon dioxide anaerobically. Cyanide and sulfhydryl 
antagonists (iodoacetate and sodium arsenite) inhibit oxygen consumption, 
but Krebs cycle inhibitors (fluoro acetate and malonate) do so only slightly. 

a. Monomorphic (free flagellum absent or short, undulating membrane in- 
conspicuous). 

(1) Short forms (means 12.2-14.4 (n). 

T. congolense of cattle, equids, swine, sheep, goat, dog. 

(2) Long forms (means 15.3-17.6 i^). 

T. dimorphon of horse, cattle, sheep, goat, pig, dog. 

b. Polymorphic (short forms without free flagellum, and long forms, of 
which some are stout, with conspicuous undulating membrane and some 
are slender with inconspicuous undulating membrane; free flagellum 
absent or present). 

T. si))iiae of swine, camels, cattle, horse, warthog. 

3. BRUCEI GROUP 

Morphology in Mammal 

Monomorphic or polymorphic forms. Free flagellum present or absent. 
Kinetoplast small, subterminal (absent in T. equinutn). Undulating mem- 
brane conspicuous. 

Biology 

Development in Glossina, in midgut and salivary glands (except evansi sub- 
group). 

Metabolism 

Blood forms have very low respiratory quotient and very high sugar con- 
sumption, producing pyruvic acid and sometimes glycerol aerobically and 
pyruvic acid and glycerol anaerobically. Cyanide does not inhibit oxygen 
consumption. Sulfhydryl antagonists markedly inhibit oxygen consumption. 
Culture forms have high respiratory quotient and moderately high sugar 
consumption, producing acetic, succinic, pyruvic and lactic acids aero- 
bically. Cyanide moderately inhibits oxygen consumption. Sulfhydryl 
antagonists markedly inhibit oxygen consumption. Cytochrome pigments 
have not been found in T. rhodesiense or T. equiperdum , but cytochrome 
and succinic oxidase activity are present in T. rhodesiense. 

a. Monomorphic (stout forms with short free flagellum). 
(1) SUIS SUBGROUP 
T. suis of swine. 



46 



THE HEMOFIACELLATES 



b. Polymorphic (slender, intermediate and stumpy forms). 

(1) BRUCEI SUBGROUP 

Polymorphism constant (stumpy forms always present). 
T. brucei of all domestic animals, antelope. 
T. rhodesiense of man, bushbuck and probably antelope. 
T. gambiense of man. 

(2) EVANSI SUBGROUP 

Polymorphism inconstant (stumpy forms rare or sporadic); no 
cyclic development in vector host. 

(a) Transmission mechanical by insects. 

T. efflnsi of cattle, camels, equids, dogs, etc. 
T. equinum of equids. 

(b) Transmission by contact (coitus) from mammal to mammal. 
T. equiperdum of equids. 

II. PARASITES OF BIRDS 

Very polymorphic, sometimes attaining great size. Relatively easy to cultivate. 
Cyclic development probably in biting arthropods. 

AVIUM GROUP 

T. avium of various birds. 
T. calmettei of chickens. 
T. gallinarum of chickens. 
T. hannai of pigeons . 
T. numidae of guinea fowl. 





Fig. 2. Species of Trypanosoma. A. T. llwilcri. B. T. cnizi. C. T. coiigoleiise. 
D. T. vivax. E. T. equiperduvi . F. T. bnicei. X 2800. (Original) 



THE HEMOFLAGELLATES 



47 



In the discussion which follows, each 
trypanosome species is taken up separ- 
ately, but special attention is paid to 
T. briicei and T. criizi as representatives 
of different types. 



TRYPANOSOMA BRUCEI 
PLIMMER AND BRADFORD, 1899 

Synonym : T. pecaudi. 

Disease : Trypanosomosis, nagana. 

Hosts : Horse, mule, donkey, ox, 
zebu, sheep, goat, camel, pig, dog, and 
many wild game animals. Antelopes are 
the natural hosts of T. brncei and serve 
as reservoirs of infection for domestic 
animals. Experimental attempts to infect 
man have failed (Ashcroft, 1959a). 

Location : Blood stream, lymph, 
cerebrospinal fluid. 

Geographic Distribution : Widely dis- 
tributed in tropical Africa between 15^ N 
and 25° S latitude, coinciding with the dis- 
tribution of its vector, the tsetse fly. 

Prevalence : T. brucei is one of the 
commonest and most important parasites 
of domestic animals in Africa. It has pre- 
vented the raising of livestock in vast 
areas. 



Morphology : Polymorphic, with 
slender, intermediate and stumpy forms. 
Undulating membrane conspicuous. Ki- 
netoplast small, subterminal. Slender 
forms average 29 /i in length but range up 
to 42 (i; posterior end usually drawn out, 
tapering almost to a point, with kineto- 
plast up to 4jj, from posterior end, with a 
long, free flagellum. Stumpy forms stout, 
averaging 18 ju in length with a range of 
12 to 26 /i; posterior end broad, obtusely 
rounded, with kinetoplast almost terminal; 
free flagellum typically absent. Interme- 
diate forms average 23 jj. in length; body 
of medium thickness, with blunt posterior 
end; moderately long free flagellum al- 
ways present. A fourth form with a 
posterior nucleus often appears in labor- 
atory animals. 



Life Cycle : When it is first intro- 
duced into the body, T. bnicei multiplies 
in the blood and lymph by longitudinal 
binary fission in the trypanosome stage, 
being particularly common in the lymph 
glands. Later the trypanosomes pass into 
the cerebrospinal fluid and multiply here 
and between the cells of the brain. Leish- 
manial forms have also been reported 
from the heart muscle of infected monkeys 
(Noble, 1955). 

The vector is a tsetse fly of the genus 
Glossina. T. brucei is generally trans- 
mitted by members of the iiiorsifans group 
of this genus, i.e., G. uiorsilaiis, G. 
sivynnertoni and G. pallidipes. Both males 
and females feed on blood and act as vec- 
tors. Only a small percentage of the tsetse 
flies which feed on an infected animal be- 
come infected, most being apparently re- 
sistant. In experimental studies, 10% or 
less become infected, while less than 1% 
of wild flies caught in endemic areas are 
infected. 

When ingested by a tsetse fly, T. bru- 
cei localizes in the posterior part of the 
midgut and multiplies in the trypanosome 
form for about 10 days. At first the try- 
panosomes are relatively broad, up to 
35/i long, with a kinetoplast about halfway 
between the posterior end of the body and 
the nucleus, with a less pronounced undu- 
lating membrane than the blood form, and 
with a free flagellum. On the 10th to 12th 
day, slender forms appear and migrate 
slowly toward the proventriculus, where 
they are found on the 12th to 20th days. 
They then migrate forward into the esopha- 
gus and pharynx, thence into the hypopharynx 
and finally into the salivary glands. Here 
they attach themselves to the walls by their 
flagella or lie free in the lumen, and turn 
into the crithidial form. These multiply 
further and then transform into the meta- 
cyclic trypanosome form, which is small, 
stumpy, and may or may not have a short 
free flagellum. 

The metacyclic trypanosomes are the 
infective forms. They are injected into the 
blood with the saliva when the fly bites; up 
to several thousand may be introduced by 
the bite. The whole life cycle in the tsetse 



48 



THF. HIMOFLACELLATES 



fly takes 15 to 35 days, and the flies are 
not infective until the metacyclic trypano- 
somes have appeared in the salivary glands. 

This type of development, in which the 
trypanosomes are found in the anterior 
part of the vector and are introduced by 
its bite, is known as development in the 
anterior station to contrast it with devel- 
opment in the posterior station or hindgut. 
In the latter, exemplified by the lewisi 
group, infection is by contamination with 
feces. 

In addition to the cyclical transmis- 
sion described above, T. briicei may oc- 
casionally be transmitted mechanically by 
tsetse flies or other biting flies. In this 
case, the trypanosomes remain alive in 
the proboscis for a short time and are 
transferred to a new host if the fly bites it 
soon enough after having bitten an infected 
one. 




mrtacjclic 



crithUiat* 



Fig. 3. Simplified life cycle of Trypano- 

sotna briicci. (From Noble, 1955) 



Pathogenesis : The signs and patho- 
genesis of the trypanosomoses of domestic 



animals are more or less similar. Dif- 
ferent hosts are affected to different de- 
grees. Horses, mules and donkeys are 
very susceptible to T. briicei. Affected 
animals have a remittent fever, edema- 
tous swellings of the lower abdomen, gen- 
italia and legs, a watery discharge from 
the eyes and nose, and anemia. The ani- 
mals become emaciated altho their appe- 
tite is good. Muscular atrophy sets in, 
and eventually incoordination and lumbar 
paralysis develop, followed by death. The 
course of the disease is 15 days to 4 
months, and untreated animals rarely re- 
cover. 

The disease in sheep, goats, camels 
and dogs is also severe. The signs are 
much the same as in horses. In the dog, 
fever may appear as shortly as five days 
after infection, and the parasites often 
cause conjunctivitis, keratitis and blind- 
ness. 

The disease is usually more chronic 
in cattle. There is remittent fever with 
swelling of the brisket, anemia, gradual 
emaciation, and discharge from the eyes 
and nose. The animals may survive for 
several months. Swine are more resistant 
than cattle and usually recover. 

Following infection, the trypanosomes 
appear first in the blood and lymph, caus- 
ing fever, edema, anemia, etc. and only 
later on are they able to invade the central 
nervous system, causing incoordination, 
paralysis and meningo-encephalitis. 

The exact way in which they act to kill 
their victims is unknown, altho several 
theories have been advanced. It is known 
that they have a high glucose metabolism, 
and one theory was that they rob the body 
of glucose so that death is due to hypo- 
glycemia. In experimental animals, life 
can be prolonged by feeding glucose and 
shortened by injecting insulin. This 
theory, however, has been discredited. 

It is known that the serum potassium 
level increases in trypanosomosis, and 
another theory was that the effects are due 
to the high potassium level. However, the 
latter is a result of the disease and not a 



THE HEMOFLAGELLATES 



49 



cause. It is due to the destruction of red 
cells with consequent release of potassium 
into the plasma, and the observed levels 
are not too harmful. 

Epidemiology : The epidemiology of 
the diseases caused by T. briicei and other 
tsetse-borne trypanosomes depends upon 
the bionomics and distribution of their 
vectors. This is such a vast subject that 
no attempt will be made to cover it here. 
In general, tsetse flies occupy almost 4 
million square miles of Africa. They 
occur in woodlands, bush or forested areas 
where there is ample rainfall and where 
the mean annual temperature is above 
about 70° F. Not all species are good vec- 
tors, and trypanosomosis does not occur 
every place that tsetse flies do. For fur- 
ther information on tsetse flies and the 
epidemiology of trypanosomosis, see 
Buxton (1948, 1955, 1955a), Hornby (1949, 
1952), Davey (1958) and Ashcroft (1959). 

Diagnosis : In the acute or early stage 
of the disease, trypanosomes can be found 
in the peripheral blood. Thick blood 
smears are preferable to thin ones. The 
protozoa are found even more often in the 
lymph glands. They can be detected in 
fresh or stained smears of fluid obtained 
by puncture of the glands. In the later 
stages of the disease, trypanosomes can 
be found in the cerebrospinal fluid. Lab- 
oratory animals such as the rat can also 
be inoculated. The complement fixation 
test can also be used; it is not specific 
for T. brucei infections, but also reacts 
in a number of other trypanosomoses. 

Cultivation : Trypanosomes can be 
successfully cultivated in a number of 
media. A common one is NNN medium, 
which is essentially a 25% blood agar 
slant. Another medium is that of Weinman 
(1946), which contains beef extract, pep- 
tone, washed erythrocytes and plasma. 
Still another is that of Tobie, von Brand 
and Mehlman (1950). A discussion of 
problems of cultivation and diagnosis is 
given by Weinman (1953). 

Trypanosomes can also be cultivated 
in developing chick embryos or in tissue 
culture. See Pipkin (1960) for a review 
of this subject. 



Treatment : Many different drugs have 
been used in the treatment of trypanoso- 
mosis. Indeed, the first synthetic organic 
compound of known composition ever used 
to cure an experimental disease was try- 
pan red, which was developed by Ehrlich 
and Shiga (1904). Since that time thousands 
of drugs have been found to show some ac- 
tivity, but the number of satisfactory ones 
is very small. The chemotherapy of try- 
panosomiasis has been reviewed by Findlay 
(1950), Ing (1953), Browning (1954), Good- 
win and RoUo (1955), Davey (1957), and 
others. 

Altho much of the earlier work on 
chemotherapy was done on members of 
ihebyncei subgroup, most of that since 
World War n on trypanosomosis of live- 
stock has dealt with the vivax and coiigo- 
lense groups. 

Antrycide methyl sulfate is perhaps 
the drug of choice for T. brucei in horses. 
It is injected subcutaneously at the rate 
of 5 mg/kg body weight; two treatments 
may be given 4 days apart. Antrycide is 
also effective against T. brucei in dogs, 
cattle and other animals. 

Suramin (Germanin, Naganol, Antry- 
pol, Moranyl, Bayer 205, Fourneau 309, 
etc. ) has been used for many years. A 
single dose of 4 g per 1000 lb body weight 
is given intravenously to horses, but it 
may be toxic in some animals. In dogs, 
5 mg/kg is given intravenously. 

The diamidines, pentamidine and 
stilbamidine, have been used extensively 
against T. ga)iibie)2se and T. rhodesiense 
in man, but have been used very little in 
veterinary medicine. Another diamidine, 
Berenil, appears promising against T. 
brucei, but needs more study. 

Control: Preventive measures 
against trypanosomosis include measures 
directed against the parasite, measures 
directed against the intermediate hosts, 
livestock management, elimination of 
reservoir hosts, and avoidance of acci- 
dental, mechanical contamination. 

Measures directed against the para- 
site include continuous survey and treat- 



so 



THE HEMOFIAGEXLATES 



ment or slaughter of all affected animals 
and periodic mass prophylactic treatment 
of all animals. The latter is discussed in 
the section on treatment of T. congolense. 

Fly traps and fly repellents have been 
used without much success in attempting 
to control tsetse flies. Elimination of 
breeding places has been practiced on a 
wide scale in many areas. Since the tsetse 
flies breed under brush along streams or 
in other localities, such measures consist 
essentially of brush removal. Two meth- 
ods are used: 

Eradicative clearing aims at eradica- 
tion of tsetse flies thruout an area. All 
the species of trees and shrubs under which 
the flies survive thru the dry season are 
removed. When this is done thoroughly 
over a large area, the flies disappear com- 
pletely. 

Protective clearing is more limited. 
It is designed to break the contacts between 
tsetse flies and domestic animals and man 
at the places where transmission is taking 
place. Fly-free belts wide enough so that 
the flies cannot cross them are established. 
In addition, inspection stations known as 
deflying houses may be set up on traffic 
routes to remove flies which may be car- 
ried across on vehicles or animals. 

Bush clearing can be quite successful. 
The incidence of trypanosomosis was re- 
duced by 92% between 1938 and 1944 in the 
Kamba area of Africa by this means 
(Morris, 1946). However, it is expensive, 
requires a large amount of labor, and the 
initial clearing must be followed up faith- 
fully as new growth occurs. 

A potentially much more satisfactory 
control measure is the spraying of insec- 
ticides on fly breeding places by means of 
aircraft. DDT and benzene hexachloride 
are highly effective for this purpose. 
Glossina pallidipes was eradicated from 
Zululand by airplane spraying with these 
insecticides at a total cost of 2. 5 million 
pounds, or slightly less than 2 shillings 
per acre (DuToit, 1959). 

Since tsetse flies bite only in the day- 
time, night grazing has been practiced by 



African natives to avoid their bites. The 
animals are held in a protected corral 
during the day. 

Cattle can be sprayed with DDT or 
another insecticide in order to kill any 
tsetse flies which light on them. 

The elimination of reservoir hosts, 
e. g. , wild game in Africa, has been ad- 
vocated and practiced in some regions 
despite the protests of many people inter- 
ested in game preservation. The Trypan- 
osomiasis Committee of Southern Rhodesia 
(1946) has described and defended the prac- 
tice. It claims that if a zone 10 miles 
wide with its ends in fly-free country is 
fenced off and all the game within it is 
killed, Glossina morsitans will disappear 
in less than 10 years. The fences can 
then be removed and the game allowed to 
return into the area. 

Since trypanosomes can be transmitted 
mechanically by inoculation of infected 
blood or lymph, there is danger of its 
transmission by the use of contaminated 
instruments in bleeding, castrating, etc. 

A great deal has been written on try- 
panosomosis control. For further infor- 
mation, see Hornby (1949, 1952), Morris 
(1946), Buxton (1948, 1955) and the pro- 
ceedings of the meetings of the International 
Scientific Committee for Trypanosomiasis, 
which held its sixth meeting in 1956. 



TRYPANOSOMA GAMBIENSE 
DUTTON, 1902 

TR Y'PANOSOMA RHODESIENSE 
STEPHENS AND FANTHAM, 1910 

These two species cause African 
sleeping sickness in man. T. rliodesiense 
is thought to occur also in antelopes 
(Hoare, 1955) and was isolated once from 
a bushbuck (Heisch, McMahon and Manson- 
Bahr, 1958). T. ganibiense does not occur 
in wild game. Neither occurs in domestic 
animals. They are morphologically indis- 
guishable from each other and'from T. 
brucei, and for this reason some people 
prefer to consider all three as subspecies 
of T. brucei. However, the biological and 



THE HEMOFLAGELLATES 



51 



epidemiologic differences between them 
make it more convenient to retain separ- 
ate names. Whatever the names used, it 
is clear that these species arose from 
strains of T. brucei which became adapted 
to man. 

Human trypanosomosis occurs in 
tropical Africa, roughly between 15° N 
and 15° S latitude. T. yliodesiense, which 
causes an acute form of the disease, 
occurs in Rhodesia, Tanganyika, Nyasa- 
land, Bechuanaland and Portuguese East 
Africa, while T. gambiense, which causes 
a chronic form of the disease, occurs in 
a large part of the remainder of the area. 
Kunert (1953) prepared a map of the dis- 
tribution of human sleeping sickness in 
Africa together with climatologic and 
other information. Ashcroft (1959a) and 
Morris (1960) reviewed its epidemiology. 

In general, T. gambiense causes a 
"domesticated" type of disease, trans- 
mitted by tsetse flies from man to man in 
regions of human habitation, while T. 
rhodesiense causes more of a woodland 
disease and people become infected with 
it away from their village areas. 

Altho it is certain that some wild ani- 
mals must serve as reservoirs of Trypano- 
soma rhodesiense, it has been isolated 
from them only once. Heisch, McMahon 
and Manson-Bahr (1958) isolated it from 
a bushbuck ( Tragelaphus scriptus) in 
Kenya by inoculation of a human volunteer. 

Epidemiologic evidence for a wild 
animal reservoir is exemplified by the ob- 
servation that every year fishermen and 
honey hunters become infected with T. 
rhodesiense near the Ugalla River in the 
Western Province of Tanganyika, yet this 
is an uninhabited region, and no people 
are there at all during the 6-month rainy 
season. The Ugalla River is part of the 
Malagarasi river system of the Western 
Province. It runs thru a sparsely popu- 
lated, woodland region inhabited by many 
wild animals and infested with Glossina 
morsitans . Jackson (1955) described 25 
cases of sleeping sickness in fly-boys 
stationed in remote outposts in this area 
between 1935 and 1939, and concluded 



that there was strong evidence that game 
was acting as a reservoir. Over half the 
cases of T. rhodesiense infection diag- 
nosed in Africa in 1953, 1954 and 1955 
were contracted in this region (Ashcroft, 
1958); 2069 cases were reported in the 
Western Province in these years (Apted, 
1955). 

The only way to be positive that a 
brucei-Hyie strain of trypanosome isolated 
from wild animals is actually T. rhodesi- 
ense is to inoculate human volunteers with 
it, and very few such attempts have been 
made. In one of the latest of these, Ash- 
croft (1958) inoculated a strain which he 
had isolated from a Coke's hartebeest 
{Alcelaphus cokei) in Tanganyika into 2 
African volunteers, but no infection re- 
sulted and he concluded that the organism 
was T. brucei. 

The life cycles of the human trypano- 
somes are the same as that of T. brucei. 
The vectors are species of tsetse flies of 
the genus Glossina. The chief vectors of 
T. gambiense are the riverine tsetse flies, 
G. palpalis and G. tachinoides, while 
those of T. rhodesiense are the game 
tsetse flies, G. morsitans, G. swynner- 
toni and G. pallidipes. 

Human trypanosomosis is similar to 
nagana in its manifestations. For further 
information, any human parasitology text 
may be consulted. 



TRYPANOSOMA EVANSI 
(STEEL, 1885) BALBIANI, 1888 

Synonyms : T. soudanense, T. 
elepfiantis, T. annamense, T. cameli, 
T. marocanum, T. ninae kohl-yakimov, 
T. aegyptum, T. hippicum, T. venezue- 
lense. 

Disease : Trypanosomosis due to 
T. evansi has been given different names 
in different localities. The most widely 
used name, surra, is applied to the dis- 
ease in all hosts. The disease in camels 
is called el debab in Algeria and mbori in 
Sudan. That in horses is called murrina 
in Panama and derrengadera in Venezuela. 



52 



THE HEMOFLAGELLATES 



Hosts : Camels, horse, donkey, ox, 
zebu, goat, pig, dog, water buffalo, ele- 
phants, capybara, tapir, and (in Mauri- 
tius) deer. 

Location : Blood, lymph. 

Geographic Distribution : Northern 
Africa (north of 15 N latitude in the west 
and central part of the continent, but ex- 
tending almost to the equator in the east), 
Asia Minor, U.S.S.R. from the Volga 
River east into Middle Asia, India, Burma, 
Malaya, Indochina, parts of southern 
China, Indonesia, Philippines, Central 
America, South America. Hoare (1956) 
has shown how the original distribution of 
T. evansi coincided with that of the camel. 
In Africa, its southern boundary coincides 
roughly with the northern boundary of 
tsetse fly distribution. It now extends far 
to the east of the camel's range in the Old 
World. It is often associated with arid 
deserts and semi-arid steppes, but may 
occur in other types of climate as well. 
In India, it is most common in the Punjab, 
which is mostly in the northwestern dry 
region (Basu, 1945; Basu, Menon and Sen 
Gupta, 1952). It was probably introduced 
into the New World in infected horses by 
the Spanish conquerors during the 16th 
century. 

Prevalence : T. evansi is an impor- 
tant cause of disease over a large part of 
its range. 

Morphology : The morphology of the 
Old World strains of T. evansi has been 
studied intensively by Hoare (1956). The 
mean length of different host and geo- 
graphic strains varies considerably. How- 
ever, the typical forms are 15 to 34 ji 
long, with a mean of 24 |i. Most are slen- 
der or intermediate in shape, but stumpy 
forms occur sporadically. All forms are 
morphologically indistinguishable from 
the corresponding ones of T. briicei. 
Strains which lack a kinetoplast have oc- 
casionally arisen spontaneously or can be 
produced by treatment with certain dyes 
(Hoare, 1954). 

Life Cycle : T. evansi is transmitted 
mechanically by biting flies. No cyclic 



development takes place in the vectors, 
the trypanosomes remaining in the pro- 
boscis. The usual vectors are horseflies 
of the genus Tabanus, but Stomoxys, 
Haematopola and Lyperosia can also trans- 
mit it. In Central and South America, the 
vampire bat is a vector, the disease in 
this case being known as murrina. 

Pathogenesis : Surra is nearly always 
fatal in horses in the absence of treatment; 
death occurs in a week to six months. The 
disease is also severe in dogs and elephants. 
It is less severe in cattle and water buffalo. 
Cattle may carry the parasites without 
showing signs of disease for months. How- 
ever, occasional outbreaks of acute disease 
occur in cattle and water buffalo. Surra in 
camels is similar to the disease in horses 
but more chronic. In dogs, T. evansi 
causes a chronic disease with a high mor- 
tality rate; untreated dogs usually die in 1 
to 2 months (Gomez Rodriguez, 1956). 

The signs of surra include intermittent 
fever, urticaria, anemia, edema of the legs 
and lower parts of the body, loss of hair, 
progressive weakness, loss of condition 
and inappetence. Conjunctivitis may occur, 
and abortion is common in camels. 

The lesions include splenomegaly, en- 
largement of the lymph glands and kidneys, 
leucocytic infiltration of the liver paren- 
chyma, and petechial hemorrhages and 
parenchymatous inflammation of the kidneys. 

Diagnosis: Same as for T. brucei. 

Cultivation : Same as for T. brucei. 

Treatment : Treatment of T. evansi 
is similar to that of T. brucei. Antrycide 
methyl sulfate is less toxic than suramin 
for horses; a single subcutaneous dose of 
5 mg/kg or even less is effective. A dose 
of 3 mg/kg has given good results in cattle. 
A single injection of 2 g is effective in 
camels. 

The dose of suramin for horses is 4 g 
per 1000 lb body weight intravenously. 
Camels tolerate suramin well, and a single 
intravenous injection of 4 to 5 g is effective 
against surra in these animals. Tartar 



THE HEMOFLAGELLATES 



53 



emetic, which has been largely superseded 
in other animals, is still used in treating 
surra in the camel; a single intravenous 
injection of 200 ml of a 1% solution is 
given. This drug is also widely used in 
cattle in India because of its cheapness. 

Control : Essentially the same meas- 
ures used in the control of T. brncei. ex- 
cept of course those directed against the 
tsetse fly, can be used in the control of 
T. evansi infections. Control of horse- 
flies and other biting flies is important. 

Remarks : Hoare (1956, 1957) has 
discussed the phytogeny of T. evansi. 
This species undoubtedly arose from T. 
briicei, being introduced into camels when 
they entered the tsetse fly belt and then 
becoming adapted to mechanical transmis- 
sion by tabanids. 



TRYPANOSOMA EQUINUM 
VOCES, 1901 

This species occurs in South America, 
where it causes a disease known as mal de 
Caderas in horses. The disease is similar 
to surra. T. equimim differs morpholog- 
ically from T. evansi only in lacking a 
kinetoplast. However, strains of T. evansi 
without a kinetoplast have appeared in the 
laboratory, and T. eqidnuni undoubtedly 
originated in this way. 

T. equimim is transmitted mechan- 
ically by tabanids. Both antrycide methyl 
sulfate and suramin can be used in treat- 
ing it. The former is less toxic. A single 
subcutaneous dose of 5 mg/kg or less of 
antrycide methyl sulfate or a single intra- 
venous dose of 4 g per 1000 lb body weight 
of suramin can be used. Control measures 
are the same as for T. evansi, 



TRYPANOSOMA EQUIPERDUM 
DOFLEIN, 1901 

'I'his species is morphologically indis- 
tinguishable from T. evansi. It causes a 
disease of horses and asses known as 
dourine. This is a venereal disease, 
transmitted by coitus. Dourine is similar 



to nagana, but runs a more chronic course 
of 6 months to 2 years. The incubation 
period is 2 to 12 weeks. 

The first sign of the disease is edema 
of the genitalia and often of the dependent 
parts of the body. There is slight fever, 
inappetence, and a mucous discharge from 
the urethra and vagina. Circumscribed 
areas of the mucosa of the vulva or penis 
may become depigmented. 

The second stage of the disease, 
characterized by urticaria, appears after 
4 to 6 weeks. Circular, sharply circum- 
scribed, urticarial plaques about 3 cm in 
diameter arise on the sides of the body, 
remain 3 or 4 days, and then disappear. 
They may reappear later. Muscular pa- 
ralysis later ensues. The muscles of the 
nostrils and neck are affected first, but 
the paralysis spreads to the hind limbs 
and finally to the rest of the body. Inco- 
ordination is seen first, and is followed 
by complete paralysis. Dourine is usually 
fatal unless treated, altho mild strains of 
the parasite may occur in some regions. 

T. equiperdum is found in Asia, North 
and South Africa, southern and eastern 
Europe and the U. S. S. R. It was once 
common in western Europe and North 
America, but has been eradicated from 
these regions. The last place where it 
was known to occur in North America, the 
Papago Indian Reservation in Arizona, was 
released from quarantine in 1949. 

Dourine can be diagnosed by finding 
the parasites in smears of fluid expressed 
from the urticarial swellings, lymph, the 
mucous membranes of the genitalia or 
blood. The signs of the typical disease are 
characteristic enough to permit diagnosis 
in endemic areas. Inoculation of mice, 
rats, rabbits or dogs may also be prac- 
ticed, but it is often difficult to demonstrate 
the parasites on the first passage. The 
complement fixation test is invaluable in 
detecting early or latent infections, and it 
was only by its use that dourine was erad- 
icated from North America. All horses 
imported into the United States must be 
tested for dourine before they are ad- 
mitted. 



S4 



THE HEMOFLAGELLATES 



To treat dourine in horses, a single 
subcutaneous dose of 5 mg/kg antrycide 
methyl sulfate or two intravenous injec- 
tions of 2 g suramin each 15 days apart 
can be used. 



TRYPANOSOMA SUIS 
OCHMANN, 1905 

This species, which was once thought 
to be the same as T. siniiae, was redis- 
covered in the Belgian Congo by Peel and 
Chardome (1954). It is a member of the 
brute i group, but differs from the others 
in being monomorphic, having only stout 
forms 14 to 19 ji long, with a short, free 
flagellum. The kinetoplast is very small 
and marginal. 

T. si</s occurs in pigs, causing a 
chronic infection in adults and a more 
acute disease with death in less than 2 
months in young pigs. Peel and Chardome 
attempted without success to transmit 
T. suis to the goat, sheep, dog, white rat, 
guinea pig, Cricetomys gambianus , Den- 
drohyrax, chimpanzee, cat, rabbit, cattle, 
monkey and ass. It is transmitted by the 
tsetse fly, Glossina brevipalpis, in which 
it develops first in the intestine and pro- 
ventriculus and then in the salivary 
glands. Metacyclic infectious trypano- 
somes appear in the hypopharynx on the 
28th day. 



TR YPANOSOMA 
BRODEN, 1904 



CONGOLENSE 



Synonyms : Trypanosoma nanum, 
T. confiisiun, T. pecorimi, T. somaliense, 
T. cellu, T. frobeniusi, T. monlgomeryi, 
T. ruandae. 

Disease : The South African disease 
of cattle known as nagana is ordinarily 
caused by T. cotigolense. Other names 
which have been given to the disease are 
paranagana, Gambia fever, ghindi and 
gobial. 

Hosts : Cattle, equids, sheep, goats, 
camels, dogs and, to a lesser extent, 
swine. Antelopes, giraffes, zebras. 



elephants and wart hogs are also infected 
and act as reservoirs. 

Location: This species develops 
almost exclusively in the blood. It does 
not invade the lymph or central nervous 
system. 

Geographic Distribution : Widely 
distributed in tropical Africa between 15° 
N and 25" S latitude, coinciding with the 
distribution of the tsetse flies which act 
ad its vectors. 

Prevalence : T. co>igolense is the 
commonest and most important trypano- 
some of cattle in tropical Africa. 

Morphology : This species is small, 
being 8 to 20|:i long; the mean lengths of 
different populations range from 12.2 to 
14.4|i (Hoare, 1959). It lacks a free 
flagellum or has a short one, has an in- 
conspicuous undulating membrane, and a 
medium-sized kinetoplast which lies some 
distance from the posterior end and is 
typically marginal. 

Life Cycle : The vectors of T. con- 
golense are various species of Glossina, 
including G. morsitans, G. palpalis, G. 
longipalpis, G. pallidipes and G. austeni. 
After the trypanosomes have been ingested 
by the tsetse flies, they develop in the 
midgut as long trypanosomes without a 
free flagellum. They then migrate to the 
proventriculus and thence to the proboscis, 
where they assume a crithidial form with- 
out a free flagellum. These are attached 
at first to the wall of the proboscis and 
multiply for a time. Later they pass into 
the hypopharynx, where they turn into 
metacyclic, infective trypanosomes sim- 
ilar in appearance to the blood forms. 
These are injected into the blood stream 
when the flies bite. 

T. congolense can also be transmitted 
mechanically by other biting flies in tsetse- 
free areas. 

Pathogenesis : Many strains which 
differ markedly in virulence and also in 
antigenic properties are united under T. 
congolense (Fiennes, 1950). In cattle. 



THE HEMOFLAGELLATES 



55 



the parasite may cause an acute, fatal 
disease resulting in death in about 10 weeks, 
or a chronic condition with recovery in 
about a year, or a mild, almost asympto- 
matic condition (Hornby, 1949). The dis- 
ease is similar in sheep, goats, camels 
and horses. Swine are more resistant. 

The signs of trypanosomosis due to 
this species are similar to those caused 
by other trypanosomes, except that the 
central nervous system is not affected. 

Fiennes (1953) described the lesions 
observed in untreated T. coiigolense in- 
fections of cattle. The lymph nodes are 
edematous, the liver is congested, the 
marrow of the long bones is largely des- 
troyed, and there are hemorrhages in the 
heart muscle and renal medulla. In cattle 
treated with antrycide or dimidium, the 
lesions are more chronic. The spleen is 
enlarged, the liver is swollen and some- 
times fibrous, the lymph nodes are hyper- 
trophied, edematous and somewhat fibro- 
tic, the kidneys show chronic degenera- 
tion, the hemolymph tissue is hyperplas- 
tic, and the marrow of the long bones is 
largely destroyed. 

Fiennes (1950), described a cryptic 
form of trypanosomiasis in cattle, usually 
following drug prophylaxis or unsuccessful 
drug therapy, in which severe lesions 
occur in the heart. These lesions were 
associated with degenerate or lysed try- 
panosomes, but some normal forms were 
also present. This is probably similar to 
the condition described by Curasson (1943) 
and Reichenow (1952), in which masses of 
degenerating trypanosomes plug the capil- 
laries. 

Diagnosis : This disease can be diag- 
nosed by detection of the parasites in blood 
smears. Repeated examinations may be 
necessary in chronic cases. Inoculation 
of rats or guinea pigs may give positive 
results when blood examinations are neg- 
ative. 

Cultivation: Same as for T. brucei. 



T. vivax until after World War II. Several 
drugs have been introduced since then, and 
active research is still going on. The gen- 
eral pattern has been similar. Each new 
drug was introduced with glowing accounts 
of its effectiveness, later its limitations 
were discovered, and it was either dropped 
or assumed its place in the trypanocidal 
armamentarium while the search passed 
on to a new field. The review articles 
listed under treatment of T. brucei may be 
consulted for further information, but 
progress is being made so rapidly that both 
they and some of the recommendations be- 
low may soon be out of date. 

Ethidium is the most effective and 
safest of several phenanthridinium deriv- 
atives which have been used. Cattle are 
treated by intramuscular injection of 
1 mg/kg ethidium bromide or chloride. 
The tiypanosomes disappear from the 
blood within 2 days. The earlier phenan- 
thridinium compounds caused photosen- 
sitization and liver damage, but Ethidium 
apparently does not. 

Antrycide methyl sulfate is also effec- 
tive against T. coiigolense. Cattle are 
treated with a single subcutaneous injection 
of 4. 5 to 5.0 mg/kg, while 3 to 5 mg/kg is 
used in horses and dogs. Antrycide causes 
a painful local reaction when given subcu- 
taneously, and may sometimes also cause 
increased salivation, sweating and tremors. 
In addition, there are a number of reports 
of drug-fastness developing to antrycide. 

The diamidine, Berenil, has been used 
with success in preliminary experiments, 
but has yet to be completely evaluated. The 
dosage for cattle is about 2 mg/kg subcu- 
taneously or intramuscularly. 

The above recommendations deal with 
curative treatment. A great deal of work 
has also been done on chemical prophylaxis 
of trypanosomosis. The idea here is to 
inject drugs in relatively insoluble form so 
that they will be released slowly over a 
long period of time and will protect animals 
for months. 



Treatment : No effective treatment 
was known for either T. coiigolense or 



Antrycide chloride, which is much less 
soluble than antrycide methyl sulfate, is 



56 



THE HEMOFIAGELLATES 



used for prophylaxis. In actual use, a 
mixture of 3 parts of the methyl sulfate 
and 4 of the chloride, known as Antrycide 
prosalt, is employed. The methyl sulfate 
eliminates any trypanosomes that might 
be present at the time of treatment, and 
the chloride provides the prophylaxis. The 
prosalt is injected subcutaneously in 
amount sufficient to give 5 mg/kg of the 
methyl sulfate. In areas where there are 
relatively few tsetse flies (defined as an 
apparent density (AD) of less than 10 flies 
caught per 10,000 yards of patrol, using a 
standardized catching technic), treatment 
every 2 months is effective, but under 
heavy challenge (defined as an AD of 40 or 
more) this protection may break down. 

Prothidium (R.D. 2801), which con- 
tains the pyrimidine moiety of Antrycide 
linked to a phenanthridinium instead of a 
quinoline nucleus, was introduced in 1956 
as a prophylactic agent. According to 
Robson and Cawdery (1958), it is better 
than Antcycide prosalt, a single subcutan- 
eous dose of 4 mg/kg protecting zebus 
naturally exposed to T. congolense, T. 
vivax and T. brucei injections for 110 or 
more days. 

Complexes or salts of suramin with 
Ethidium, Antrycide and other trypano- 
cides were introduced by Williamson and 
Desowitz (1956) for prophylactic use. 
They obtained more than 7 months' pro- 
tection against T. congolense and T. vivax 
by subcutaneous injection of Ethidium sur- 
aminate. However, Robson and Cawdery 
(1958) considered that the local reactions 
which it produced were so severe as to 
preclude its use even tho at 5 mg/kg it 
protected naturally exposed zebus for 113 
days or more. Further work with such 
complexes may be rewai'ding. 

Pentamidine has been used extensively 
in prophylaxis of human trypanosomosis, 
but is not used in domestic animals. 

Whenever a drug is used continuously 
for prophylaxis, there is danger that drug- 
fast strains of parasites may appear be- 
cause the blood level becomes so low that 
relatively resistant individuals can survive. 
This has happened particularly with Antry- 



cide and also with the phenanthridinium 
derivatives. Unfortunately, too, strains 
which have become resistant to Antrycide 
are also resistant to phenanthridinium 
compounds. No drug resistance has ap- 
peared so far to Berenil. 

Control: Same as for T. brucei. 



TRYPANOSOMA DIMORPHON 
LAVERAN AND MESNIL, 1904 

This species was once thought to be a 
synonym of T. congolense, but Hoare 
(1959) restudied Laveran and Mesnil's 
original slides, measuring 1200 individuals 
and analyzing the data statistically, and 
showed that it differs in length. T. di- 
morphon is 11 to 24 jj, long with a mean of 
16. 2 (i; the means of different populations 
ranged from 15. 3 to 17. 6|n . Despite its 
name, Hoare (1959) found that it is actually 
monomorphic. It is slender, without a 
free flagellum, and its undulating membrane 
is not pronounced. The posterior end is 
rounded (chiefly in the shorter forms) or 
pointed (chiefly in the longer forms). The 
nucleus is in the middle or posterior part 
of the body. The kinetoplast is fairly large 
and typically subterminal and marginal. 

T. dimorphon occurs in Gambia, French 
Guinea, Ivory Coast, Belgian Congo, Sudan, 
Somalia, Southern Rhodesia, Portuguese 
East Africa, Zululand and possibly Nigeria, 
and has been found in the horse, sheep, 
goat, cattle, pig and dog. It is transmitted 
by tsetse flies in the same way as T. con- 
golense. 



TRYPANOSOMA SIMLAE 
BRUCE ET AL. , 1912 

Synonyms : T. ignotum, T. rodhaini, 
T. porci. 

T. simiae was first found in a monkey, 
but its natural reservoir host is the wart- 
hog {Phacophoerus aethiopiciis). It is 
highly pathogenic for the pig and camel, 
causing a peracute disease with death 
usually in a few days. This is the most 
important trypanosome of domestic swine. 



THE HEMOFLAGELIATES 



57 



It is only slightly pathogenic for sheep 
and goats, and apparently non-pathogenic 
for cattle, horses or dogs, altho it may 
infect them. The rabbit appears to be the 
only susceptible laboratory animal. There 
is a great deal of variation in pathogenicity 
between strains, and indeed marked 
changes can occur in the pathogenicity of 
a single strain. 

T. slniiae occurs mostly in East 
Africa and the Belgian Congo, but it has 
also been found in other parts of Africa 
where T. co)igolense occurs. 

T. simiae differs morphologically 
from T. congolense in being polymorphic 
instead of monomorphic. It varies in 
length from 12 to 2^\i. About 90% of its 
forms are long and stout, with a conspicu- 
ous undulating membrane, about 7% are 
long and slender with an inconspicuous un- 
dulating membrane, and about 3% are 
short, with an inconspicuous undulating 
membrane. A free flagellum is usually 
absent, but has been reported in from 1 to 
4% of different strains. 

This species is transmitted in the 
warthog reservoir host by tsetse flies, in- 
cluding Glossliia morsitans and G. brevi- 
palpis, in which it develops in the midgut 
and proboscis. Tsetse flies also transmit 
it to swine, but once it has been introduced 
into a herd, it can apparently be trans- 
mitted mechanically by horseflies and 
other blood-sucking flies (Unsworth, 1952). 

T. simiae is more resistant to drugs 
than the other African trypanosomes. 
Antrycide methyl sulfate is probably the 
best drug, but it may not be completely 
effective. It is injected subcutaneously 
at the rate of 5 mg/kg; more than one in- 
jection is probably necessary. 

Control measures are the same as 
for T. briicei. In addition, horseflies and 
other biting flies should be controlled. 



Disease : Souma. T. vivax is also 
sometimes found in mixed infections of 
cattle with T. congolense and T. briicei. 

Hosts : Cattle, sheep, goats, camels, 
horse. Antelopes and the giraffe are res- 
ervoir hosts in Africa, and the deer (Odo- 
coileiis g\'))inolis) in Venezuela (Faisson, 
Mayer and Pifano, 1948). The pig, dog 
and monkey are refractory to infection. 
The small laboratory rodents are difficult 
to infect. 

Location : Blood stream, lymph. Cen- 
tral nervous system infections have been 
described in sheep. 

Geographic Distribution : T. vivax 
is found thruout the tsetse fly belt in Africa. 
It has, however, spread beyond this region 
to other parts of Africa and to Central 
America, South America, the West Indies 
and Mauritius. 

Morphology : T. vivax is 20 to 27 ji 
long and monomorphic. The posterior end 
is typically rounded, a free flagellum is 
always present, the kinetoplast is large 
and terminal, and the undulating membrane 
is inconspicuous (Fairbairn, 1953). 

Life Cycle : The original vectors of 
T. vivax and still the most important in 
Africa are tsetse flies, including Glossina 
morsitans, G. tachinoides and other spe- 
cies. Development takes place only in the 
proboscis. The trypanosomes turn into 
the crithidial form, multiply in this form 
and then turn into metacyclic, infective 
trypanosomes which pass to the hypopharynx 
and infect new hosts when the tsetse flies 
bite. The flies become infectious as early 
as 6 days after they themselves were in- 
fected. 

Horseflies and other tabanids may act 
as vectors; they are the only ones in the 
New World and in Africa outside the tsetse 
zone. In this case transmission is mechan- 
ical. 



TRYPANOSOMA VIVAX 
ZIEMANN, 1905 

Synonyms : T. cazalboui, T. viennei, 
T. bovis, T. angolense, T. caprae. 



Pathogenesis : T. vivax is most im- 
portant in cattle, in which the disease is 
similar to that caused by T. congolense. 
According to Fairbairn (1953), T. vivax 
infections of cattle in East Africa usually 



58 



THE HEMOFLAGELLATES 



cause a mild disease, but in West Africa 
they are usually fatal in some types of 
cattle. Virulent strains may also occur 
in East Africa. Unsworth (1953) found 
that T. L'ivax is highly pathogenic for zebu 
cattle in laboratory infections, and that 
when these cattle were exposed to infec- 
tion under natural conditions in Nigeria, 
all of them died. 

Camels are less seriously affected 
than cattle. T. vivax is apparently more 
pathogenic for sheep than other trypano- 
somes, and may be found in the central 
nervous system. It is apparently less 
pathogenic for goats. It causes a chronic 
disease, often with spontaneous recovery, 
in horses. It is not pathogenic for dogs, 
pigs and monkeys, and only slightly so for 
the common laboratory rodents. 

The signs of disease are similar to 
those caused by T. coiigolense. There is 
a wide variation in virulence between dif- 
ferent strains, but the virulence of any 
particular strain tends to remain constant. 

Diagnosis : T. vivax is detected most 
readily in lymph node smears. Large 
numbers are found in the blood only in 
early infections. Inoculation of laboratory 
animals is not particularly satisfactory; 
inoculation of sheep or goats is better, 
the trypanosomes appearing in 7 to 10 days. 



being smaller. It is 12 to 20 ji long, with 
an average of about 16/j.. It occurs in 
cattle, sheep, goats and antelopes, causing 
a disease similar to that caused by T. vivax 
(Wilson, 1949). Laboratory rodents are 
refractory to infection. T. uniforme 
occurs only in Uganda and the Belgian Congo. 
It is transmitted by tsetse flies in the same 
way as T. vivax. 



TRYPANOSOMA CRUZI 
CHAGAS, 1909 

Synonyms : Schizotrypanum cruzi. 

Disease : American human trypano- 
somosis, Chagas' disease. 

Hosts : Many species of wild and do- 
mestic animals have been found naturally 
infected with Trypanosoma cruzi, and 
probably most mammals are susceptible. 
Man is also susceptible, infants and young 
children being most often affected. The 
most important wild reservoir hosts are 
probably armadillos (Dasypus) in South 
America, opossums (Didelphis) in South 
and Central America and the United States, 
and woodrats {Neotoma) and possibly rac- 
coons (Procyo)i) in the United States. The 
dog, cat and possibly the pig are consid- 
ered of some importance as reservoirs of 
infection for man in South America. 



Cultivation : Same as for other try- 
panosomes. 

Treatment : T. vivax can be success- 
fully treated with the same drugs and in 
the same dosages as T. congolense. It is 
perhaps slightly more resistant, but not 
significantly so. 

Control : Control measures are the 
same as those for T. coiigolense infections. 
In areas where tabanids are the vectors, 
measures directed against these flies 
should be practiced. 



TR YPANOSOMA UNIFORME 
BRUCE et al. , 1911 

This species is similar to T. vivax, 
differing from it morphologically only in 



Location : The trypanosomes are 
found in the blood early in an infection. 
Later, they invade the cells of the reticulo- 
endothelial system, heart and striated 
muscles and other tissues. In central nerv- 
ous system infections, they are found in 
the neuroglial cells. Trypanosome forms 
occur in the blood, and leishmanial forms 
within the cells. 

Geographic Distribution : T. cruzi 
occurs in South America from Argentina 
north, in Central America and in southern 
United States. Dias (1953) published maps 
of the distribution of Chagas' disease in 
South and Central America together with 
climatologic and other information. 

In the United States, T. cruzi had been 
thought until recently to be confined to the 
southwestern states, including Texas, 



THE HEMOFLAGELLATES 



59 



Arizona, New Mexico and southern Califor- 
nia, but Walton et al. (1956) discovered it 
in raccoons in Maryland, and it appears 
that it may be rather widely distributed in 
the southeastern states. McKeever, Gor- 
man and Norman (1958) found it in 17% of 
552 opossums, 2% of 118 grey foxes {Uro- 
cyon cinereoaygentens), 1. 5% of 608 rac- 
coons and 1% of 306 striped skunks {Me- 
phitis mephitis) from Georgia and Florida. 
Walton et al. (1958) found it in 5 of 400 
raccoons from Maryland. Norman et al. 
(1959) reported that their strains were 
typical T. criizi of relatively low virulence 
for mice. 

Morphology : The forms in the blood 
are monomorphic, 16 to 20 /i long, with a 
pointed posterior end and a curved, stumpy 
body. The kinetoplast is subterminal and 
larger than that of any other trypanosome 
of domestic animals or man, often causing 
the body to bulge around it. The undulating 
membrane is narrow, with only 2 or 3 un- 
dulations. There is a moderately long 
free flagellum. The leishmanial forms in 
the muscle and other tissue cells are 1. 5 
to 4. 0|i in diameter and occur in groups. 
Electron microscope studies of this spe- 
cies have been made by Meyer and Porter 
(1954), Meyer, Musacchio and Mendonca 
(1958) and Meyer and Queiroga (1960). 




Fig. 4. Successive stages in the transfor- 
mation of a leishmanial form of 
Trypanosoma criizi into a meta- 
cyclic trypanosome form. The 
metacyclic trypanosome (lower 
right) is from a Giemsa stained 
smear; the other stages are from 
living preparations of culture ma- 
terial viewed with the phase mi- 
croscope. (From Noble, 1955) 



Life Cycle : Altho the trypanosome 
form of T. cruzi is common in the blood 
in the early stages of Chagas' disease, it 
does not multiply in this form. The try- 
panosome forms enter the cells of the 
reticulo-endothelial system, striated mus- 
cles and especially of the heart muscle, 
where they round up and turn into leish- 
manial forms. These multiply by binary 
fission, destroying the host cells and 
forming cyst-like nests of parasites. 
There does not appear to be conclusive 
proof that they turn into the crithidial 
form in mammals, as was once believed. 
The leishmanial forms turn into trypano- 
some forms which re-enter the blood. 
Among recent studies or reviews of the 
life cycle of T. cruzi in the vertebrate host 
are those of Elkeles (1951), Noble (1955), 
Romana (1956) and Wood (1951, 1951a, 
1953). 



The vectors of T. cruzi are kissing 
bugs or conenose bugs, members of the 
hemipteran family Reduviidae. Natural 
infections have been found in at least 36 
species of these bugs. They get their first 
name from the fact that in sucking blood 
they prefer to attack the thinner parts of 
the skin such as the lips or eyelids. 

The most important vector in South 
America is probably Panstrongylus (syn. , 
Triatoma) megistus. Other important 
vectors in South and Central America are 
P. geniculatus, Eutriatoma sordida, Tri- 
atoma infestans, Rliodnius prolixiis and 
Eratyrus cuspidatus. 

According to Faust (1949), 15 naturally 
infected species of reduviids have been 
found in the United States. Dias (1951, 



60 



THE HEMOFLACELLATES 



1951a) listed Triatoma pro Ir acta, T. san- 
giiisiiga (= T. gerstaeckeri), T. lecliilar- 
ius, T. longipes, T. neolomae and T. 
rubida as having been found infected in the 
U. S. Mehringer and Wood (1958) found 
T. C7-uzi in 24% of 383 Triatuma prolracta 
collected in the Boy's and Girl's Camp 
areas in Griffith Park, Los Angeles, 
Calif. Most of the conenose bugs were 
taken in human habitations. 

Both the nymphs and adults of these 

reduviids can be infected and can transmit 
the disease. In addition, it is possible to 
infect sheep keds (Rodhain and Brutsaert, 
1935), ticks {Orinthodorus){Bv\im'()i, 1939) 
and bedbugs (Wood, 1951a) experimentally. 

After they have been ingested by the 
triatomids along with a blood meal, the 
trypanosomes pass to the midgut. Here 
they turn into leishmanial forms which 
multiply by binary fission and turn into 
either metacyclic trypanosomes or cri- 
thidial forms. The crithidial forms multi- 
ply further by binary fission, and extend 
into the rectum. Here they turn into meta- 
cyclic trypanosomes, which are unable to 
divide until they enter a vertebrate host. 
The life cycle in the invertebrate host takes 
6 to 15 days or longer, depending on the in- 
sect species or stage and on the temperature. 

The infective trypanosome forms pass 
out in the feces. They can penetrate the 
mucous membranes or skin actively. 
Triatomids commonly defecate after feed- 
ing, and most human infections occur when 
feces are rubbed into the eyes or mucous 
membranes following a bite. Animals can 
become infected by licking their bites or 
by eating infected bugs or rodents. 

Epidemiology : Human infections 
with T. cnui are common in many parts 
of tropical America, including Brazil, 
Bolivia, northern Chile, northern Argen- 
tina, French Guiana, Paraguay, Uruguay 
and Venezuela. In some localities 10 to 
20% or even 507o of the inhabitants are 
positive to the complement fixation 
(Machado) test, but in other localities 
where exposure to the vectors is minimal, 
there are very few positive reactions. As 
mentioned below, acute Chagas' disease 



occurs primarily in infants and children, 
and the number of acute cases is far lower 
than the numbers of chronic and unrecog- 
nized infections. 

Chagas' disease becomes increasingly 
uncommon to the north of the endemic area 
even tho infected reservoir hosts and vec- 
tors may be common. Less than 140 cases 
of Chagas' disease had been reported from 
Guatemala, Salvador, Nicaragua, Costa 
Rica and Panama according to Dias (1952a) 
while only 9 cases were known from Mexico 
(Mazzotti and Dias, 1950). Only a single 
indigenous case has been reported from 
the United States, by Woody and Woody 
(1955) in Texas. 

Chagas' disease is a zoonosis, infec- 
tions occurring widely in animals and man. 
The armadillo is thought by Hoare (1949) 
to be the original source of the human dis- 
ease in South America, but the opossum 
and many other wild animals are also in- 
fected. The most important wild reser- 
voirs in the United States are woodrats of 
the genus Neotoitia. Natural infections 
have been found in the southwestern states 
and southern California in jV. fuscipes, 
N. albigida, N. micropus, in the deer- 
mouse, Peromyscus boylii, and also in 
the opossum, house mouse and nine -banded 
armadillo {Dasypus novemcbictus). The 
recent discovery of T. criizi infections in 
raccoons {Procyon lotor), opossums, gray 
foxes and skunks in Maryland, Georgia and 
Florida (Walton t^/ «/. , 1956, 1958; Mc- 
Keever, Gorman and Norman, 1958) 
raises the question how widespread the in- 
fection is in these animals. 

Cats and dogs are often naturally in- 
fected in South America, and, because of 
their closer association with man, are 
probably more important as sources of 
human infection than wild animals. Natur- 
ally infected pigs have been found in South 
America, and sheep and goats can be in- 
fected experimentally with these South 
American strains. 

In a study of the possible role of farm 
animals as reservoirs of North American 
strains of T. criizi. Diamond and Rubin 
(1958) established low-grade infections in 



THE HEMOFLAGELLATES 



61 



young pigs, lambs, kids and calves with 
a strain isolated from a raccoon in Mary- 
land. The infections persisted at least 
57 days in the pigs, 53 to 85 days in the 
lambs, 38 days in a kid and 21 days in a 
calf. 

Infection is common in the triatomid 
vectors of Chagas' disease. In the endemic 
regions of South and Central America, 40 
to 60% of them are infected, while 20 to 
25% are infected in Mexico and southwest- 
ern United States. The triatomids infest 
armadillo burrows and woodrat nests, and 
thus maintain the infection in these animals. 
They also infest houses, where they live 
like bedbugs; it is these triatomids which 
are responsible for the vast majority of 
human infections. 

Because triatomids are rare in south- 
eastern U. S. where T. criizi is common 
in the opossums, and because they iso- 
lated the organism from the urine of in- 
fected opossums, McKeever, Gorman and 
Norman (1958) believed that infections may 
be passed from mammal to mammal by 
contact with infected urine. 

For further information on the epide- 
miology of T. cruzi infections see Dias 
(1951, 1951a, 1951b, 1952, 1952a, 1952b), 
Dias and Chandler (1951), Dias and Laranja 
(1948), Dias, Laranja and Nobrega (1946) 
and other papers by these authors. For 
information on the epidemiology of T. 
cruzi in southwestern United States, see 
Elkins (1951) and particularly Wood (1950, 
1953a, 1958), and Mehringer and Wood 
(1958). 

Pathogenesis : Chagas' disease may 
be either acute or chronic in man. The 
great majority of acute cases occur in 
infants and young children. The first sign 
of disease is often swelling of the eyes and 
conjunctiva. This swelling may affect 
either one or both sides of the face. The 
tear glands become inflamed, and the 
cervical lymph nodes swell. Later on, 
swellings may appear in other parts of the 
body. Each swelling, known as a chagoma, 
is due to an inflammatory exudate in the 
region where the parasites are invading 
the tissue cells. In addition to this edema, 



there may be anemia, more or less con- 
tinuous fever, prostration and severe 
headache. 

If the patient survives the acute phase, 
the disease becomes more or less chronic. 
Some authorities believe that it persists 
for life. The lymph nodes are edematous 
and inflamed, and the liver and spleen are 
enlarged. The heart is affected in many 
cases. Electrocardiographic abnormal- 
ities are common. Inflammatory infiltra- 
tion by phagocytes, fibrosis, separation of 
the muscle cells and partial destruction of 
the fibers by the multiplying parasites are 
present. The death rate due to cardiac 
conditions is increased in endemic areas. 

T. cruzi may cause an acute or chronic 
disease in laboratory animals, depending 
on the strain of the parasite and the age of 
the host. Puppies and kittens are most 
susceptible, followed in order by mice and 
guinea pigs. The reservoir hosts are ap- 
parently not seriously affected, nor are 
farm animals. No clinical signs were ob- 
served in the infected young pigs, lambs, 
kids and calves studied by Diamond and 
Rubin (1958). 

Diagnosis : In the acute stage of the 
disease, T. cruzi can be found in thick 
blood smears. In chronic or light infec- 
tions, other methods must be used. One 
of the most important is xeuodiagiios is, 
the inoculation of susceptible vector hosts. 
Laboratory-reared, parasite-free triato- 
mids are allowed to feed on suspected in- 
dividuals, and their droppings or intestines 
are examined 7 to 10 days later for devel- 
oping trypanosomes. Rhodnius prolixus 
is often used for this purpose (Pifano, 1954a). 

Laboratory animals can also be inoc- 
ulated. In descending order of suscepti- 
bility, these are puppies, kittens, mice 
and guinea pigs. The trypanosomes can 
be cultivated in NNN medium, Weinman's 
(1946) medium, Diamond and Herman's 
(1954) SNB-9 (serum -neopeptone-blood) 
medium, or in a number of other media. 
The trypanosomes can also be found in 
biopsy examinations of affected lymph 
glands or, on necropsy, in sections of 
heart muscle. 



62 



THE HEMOFLAGELLATES 



A complement fixation test, the 
Machado reaction, has been used, but it is 
also positive in Leislunaitia infections and 
weakly positive in a number of other con- 
ditions. Other serologic tests which have 
been used are the precipitin reaction, an 
intradermal skin test and a slide agglu- 
tination test. T. cruzi can be differenti- 
ated from the non-pathogenic T. rmigeli 
by its smaller size and large kinetoplast. 

Treatment : No satisfactory drug is 
known for the treatment of T. criizi infec- 
tions, altho Bayer 7602 Ac is used. 

Control : Prevention of human T. 
cruzi infection depends upon eliminating 
triatomids from houses. This will also 
largely prevent infections among domestic 
dogs and cats. Dusting or spraying houses 
with residual lindane or dieldrin has given 
good results. 



TR YPANOSOMA RANGELI 
TEJERA, 1920 

Synonyms : Tr\'pa>ioso))ia guaterna- 
lense, T. ariarii. 

T. yaiigeli was first found in the tri- 
atomid, Rhodnius prolixus, in Venezuela. 
It was later found in children in Guatemala 
and still later in Colombia, Chile and El 
Salvador. It is quite common in dogs, 
cats and man in certain areas of Venezuela, 
Colombia and Guatemala, and is sometimes 
found in mixed infections with T. cruzi. 
Groot, Renjifo and Uribe (1951) found it in 
67 of 183 persons in the Ariari Valley and 
Groot (1951) found it in 1 of 30 persons, 2 
of 27 dogs and an opossum in the Mira- 
flores region of Colombia. It has also been 
found in the monkey, Cebiis fatiiellns. 
Young mice, rats and rhesus monkeys can 
be infected experimentally. 

The trypanosomes in the blood are 
considerably larger than T. cruzi, being 
26 to 36 )i long. The nucleus is anterior 
to the middle of the body, the undulating 
membrane is rippled and the kinetoplast 
is small and subterminal. 

The most common vector is Rhodnius 
prolixus, but Triatoma dimidiata and other 



triatomids have also been found infected. 
A piriform stage about 1 ji long has been 
found in the foregut, and crithidial and 
metacyclic trypanosome forms develop in 
the hindgut. The crithidial stages may be 
extremely long, ranging from 32 to 70 or 
even over 100 /i in length. The metacyclic 
trypanosome forms have a well-developed 
undulating membrane and a long free fla- 
gellum. They may pass into the hemolyniph 
and thence to the salivary glands. They 
can be transmitted either by bite or by 
fecal contamination. 

T. rangeli does not appear to be path- 
ogenic for vertebrates, but Grewal (1957) 
found that it was pathogenic for R. prolixus 
and also for experimentally infected bed- 
bugs. 

The blood forms of T. ra)igeli can be 
readily differentiated from those of T. 
cruzi by their larger size and their much 
smaller kinetoplast. The forms in the in- 
sect hosts can be distinguished by their 
small kinetoplast and giant crithidial forms. 

T. rangeli can be easily cultivated in 
a modified NNN medium containing glucose, 
peptone and macerated meat (Pifano, 1948). 
The culture forms are similar to those in 
the triatomid intestine. For further infor- 
mation regarding this species, see Groot, 
Renjifo and Uribe (1951), Groot (1954), 
Pifano (1948, 1954) and Zeledon (1954). 



TR YPANOSOMA 
LAVERAN, 1902 



THEILERI 



Synonyms : Trypanosoma franki, 
T. ivrublewskii, T. himalayanum, T. 
indiciim, T. muktesari, T. falsliaici, T. 
scheini, T. americanum, T. rulherfordi. 

T. theileri occurs in the blood of cat- 
tle. It is worldwide in distribution. It is 
probably quite common, but is rarely found 
in blood smears. Crawley (1912) found it 
in blood cultures from 74% of 27 cattle 
around Washington, D. C. and Glaser (1922) 
found it in blood cultures from 25% of 28 
New Jersey cattle. Neither found it in 
direct blood smears. Atchley (1951) found 
it in the blood of 1% of 500 South Carolina 
cattle. 



THE HEMOFLACELLATES 



63 



T. theileri is relatively large, being 
ordinarily 60 to 70 ;i long, but forms up 
to 120jLi long and smaller ones 25|i long 
often occur; those found by Levine et al. 
(1956) in an Illinois heifer were 34 to 40 /i 
long exclusive of the flagellum. The pos- 
terior end is long and pointed. There is 
a medium -sized kinetoplast some distance 
anterior to it. The undulating membrane 
is prominent, and a free flagellum is pres- 
ent. Both trypanosome and crithidial forms 
forms may occur in the blood. Multipli- 
cation occurs by binary fission in the 
crithidial form in the lymph nodes and 
various tissues. 

T. theileri is transmitted by various 
tabanid flies, including Tabamis and 
Haeinatopota. It reproduces in the fly 
intestine by binary fission in the crithidial 
stage. 

T. theileri is ordinarily non-patho- 
genic, but under conditions of stress it 
may cause serious signs and even death. 
It has caused losses in cattle being im- 
munized against rinderpest and other 
diseases, and has occasionally been 
accused of causing an anthrax-like dis- 
ease. Carmichael (1939) found masses of 
T. theileri in the brain of a cow which had 
died with signs of "turning sickness" in 
Uganda. 

T. theileri may also be associated 
with abortion, altho it has not proved that 
it causes this condition. Levine et al. 
(1956) found it in an Illinois heifer which 
had aborted, and Dikmans, Manthei and 
Frank (1957) found it in the stomach of 
an aborted bovine fetus in Virginia. Lund- 
holm, Storz and^McKercher (1959) found 
it as a contaminant in a primary culture 
of kidney cells from a bovine fetus in 
California. This was further evidence 
that intrauterine transmission may occur. 

Ristic and Trager (1958) found T. 
theileri in three Florida dairy cattle with 
depressed milk production; it was not 
found in cows in the same herd with nor- 
mal milk production. The affected cows 
had a marked eosinophilia. 

Since T. theileri is rarely seen in 
the blood, diagnosis ordinarily depends on 



cultivation. It can be cultivated in NNN 
and other media at room temperature. 
Ristic and Trager (1958) also cultivated 
it at 37"" C in a blood-lysate medium. 
Both crithidial and trypanosome forms 
were present in their cultures. Lundholm, 
Storz and McKercher (1959) found that it 
grew well in tissue culture medium con- 
taining 10% lamb serum, but better if 
bovine kidney cells were present. 

No treatment is known for T. theileri. 
Infections can be prevented by elimination 
of the tabanid vectors. 



TRYPANOSOMA MELOPHAGIUM 
(FLU, 1908) 

This parasite is very common in sheep 
thruout the world. It is non-pathogenic, 
and infections are so sparse that it can or- 
dinarily be found only by cultivation. The 
trypanosomes in the blood resemble T. 
theileri and are 50 to 60 |i long. 

T. nielophagimn is transmitted by the 
sheep ked, Melophagns oviuiis, and can 
readily be found in its intestine. Its life 
cycle has been described by Hoare (1923). 
Crithidial forms are abundant in the mid- 
gut, and leishmanial forms occur here 
also. Both multiply by binary fission. 
The crithidial forms change into small, 
metacyclic trypanosome forms in the hind- 
gut. Nelson (1956) found that T. melo- 
phagiiim may kill the ked by blocking the 
midgut. Sheep are infected when they 
bite into the keds and the trypanosomes 
pass thru the intact buccal mucosa. Be- 
cause infections in sheep are so sparse, 
it has been suggested that no multiplication 
occurs in this host. 



TRYPANOSOMA THEODORI 
HOARE, 1931 

This non- pat ho genie species was 
found in goats in Palestine. It resembles 
T. melophagiHui and has a similar life 
cycle, except that its intermediate host 
is another hippoboscid fly, Lipoptena 
capriiia. T. tJieodori may be a synonym 
of T. nielophagiuni. 



64 



THE HEMOFLACELLATES 



TRVPAXOSUMA NABIASI 
RAILLIET, 1895 

This species occurs in the wild 
European rabbit, Oryctolagns cuniculiis. 
It has been found sporadically in England, 
France and other European countries. It 
is 24 to 28 fi long. Its intermediate host 
is the flea, Spilopsyllus cuniculi, in which 
it develops in the gut. The metacyclic 
infective forms occur in the rectum. In- 
fection is presumably by ingestion. Grewal 
(1956) described its life cycle briefly. 



TRYPANOSOMA LEWISI 

CKENT, 1880) 

LAVERAN AND MESNIL, 



1901 



This species occurs quite commonly 
in the black rat, Norway rat and other 
members of the genus Ralliis thruout the 
world. It is not normally transmissible 
to mice. It is 26 to 34 ^t long. Its vector 
is the rat flea, Nosopsyllus fasciatus, in 
which it develops in the gut, and in which 
the metacyclic, infective forms occur in 
the rectum. Rats become infected by 
eating infected fleas or flea feces. T. 
lewlsi is non-pathogenic. 

A great deal of research has been 
done on this species, since it is easy to 
handle and its host is a convenient one. 



TRYPANOSOMA DUTTONI 
THIROUX, 1900 

This species occurs in the house 
mouse and other species of Alus thruout 
the world. It is not normally transmis- 
sible to rats. It is 28 to 34 ^ long. Its 
vector is the flea, Nosopsyllus fasciatus, 
and its life cycle is the same as that of 
T. lewisi. It is non-pathogenic. 



TRYPANOSOMES OF BIRDS 

Trypanosomes have been reported 
under a large number of names from 
many species of birds. They all look 
very much alike and probably belong to 
relatively few species. However, exten- 



sive cross transmission studies are 
needed to establish their relationships, 
and, until these are carried out, it is 
probably best to refer to them by the names 
under which they were first described. 

Trypanosoma avium Danilew sky, 1885 
was first described from owls (scientific 
name not given) and roller-birds {Coracias 
garrulus) in Europe, and has since been 
reported from a wide variety of birds, in- 
cluding crows (Baker, 1956) and Canada 
geese (Diamond and Herman, 1954). Baker 
(1956 a, b) transmitted it from the rook 
[Corvus frugilegns) and jackdaw (C. mone- 
dula) to canaries, but failed to transmit it 
to a single 3-day-old chick. 

T. calmettei Mathis and Leger, 1909 
was described from the chicken in south- 
east Asia; it is about 36 |i long. T. gal- 
linarum Bruce et al. , 1911 was described 
from the chicken in central Africa; it is 
about 60 /i long. T. Iiannai was described 
from the pigeon, and T. numidae from the 
guinea fowl. 

Avian trypanosomes are very poly- 
morphic, sometimes attaining great size. 
They may be 26 to 60j:x long or even longer. 
The kinetoplast is generally a long distance 
from the posterior end. There is a free 
flagellum, and the body is often striated. 

Blood-sucking arthropods such as 
mosquitoes and hippoboscids are believed 
to be the vectors of avian trypanosomes, 
but the only complete life cycle was worked 
out by Baker (1956, a, b) for T. avimn from 
rooks and jackdaws. He found that in Eng- 
land the hippoboscid fly, Oniilhoiiiyia 
avicularia, acts as the vector. Upon in- 
gestion with a blood meal, the trypanosomes 
change into the crithidial form in the mid- 
gut, multiply by binary fission in this form, 
and pass to the hindgut. They multiply fur- 
ther and then turn into a piriform stage 
which develops in turn into a small, meta- 
cyclic trypanosome form. Birds become 
infected when they eat infected insects. 
The metacyclic trypanosomes penetrate 
the membranes of the mouth, esophagus 
and/or crop and probably invade the lymph- 
atic system, developing into large forms 



THE HEMOFLAGELLATES 



65 



which first appear in the blood 18 to 24 
hours after infection. 

According to Baker, there is no mul- 
tiplication in the avian host, the trypano- 
somes simply becoming larger. This 
would account for their sparse numbers in 
the blood. They persist in the rook and 
jackdaw over-winter, being more or less 
restricted to the bone marrow, and re- 
appear in the peripheral blood in the spring 
Diamond and Herman (1954), too, found 
that T. avium could be isolated from the 
bone marrow of Canada geese much more 
readily than from the blood. 

Nothing is known of the pathogenicity 
of the avian trypanosomes. They are pre- 
sumably non-pathogenic. 

Avian trypanosomes can be readily 
cultivated on several media, including 
NNN medium and the SNB-9 (saline-neo- 
peptone-blood) medium described by 
Diamond and Herman (1954). 



Genus LEISHMANIA Ross, 1903 

Members of this genus occur primar- 
ily in mammals. They cause disease in 
man, dogs and various rodents including 
gerbils and guinea pigs. Leishiiiaiiia is 
heteroxenous, being transmitted by sand- 
flies of the genus Phlebotoiuiis. It is 
found in the leishmanial stage in the cells 
of its vertebrate hosts and in the lepto- 
monad stage in the intestine of the sandfly 
and in culture. 

Morphology : All species of Leish- 
mania look alike, altho there are size dif- 
ferences between different strains. The 
leishmanial stage is ovoid or round, 
usually 2. 5 to 5. by 1 . 5 to 2. p. , altho 
smaller forms occur. Only the nucleus 
and kinetoplast are ordinarily visible in 
stained preparations, but a trace of an in- 
ternal fibril representing the flagellum 
can sometimes be seen. This flagellum 
and the basal granule from which it arises 
can also be seen in electron micrographs 
(Chang, 1956; Pyne and Chakraborty, 
1958). The leptomonad forms in culture 
and in the invertebrate host are spindle- 



shaped, 14 to 20 |i long and 1. 5 to 3. 5(i 
wide. 

Life Cycle : In the vertebrate host, 
Leishmauia is found in the macrophages 
and other cells of the reticulo-endothelial 
system in the skin, spleen, liver, bone 
marrow, lymph nodes, mucosa, etc. It 
may also be found in the leucocytes, es- 
pecially the large mononuclears, in the 
blood stream. It multiplies by binary 
fission in the leishmanial form. 

The invertebrate hosts of Leishmauia 
are sandflies of the genus Phlebotomus . 
When the sandflies suck blood they ingest 
the leishmanial forms. These pass to the 
midgut, where they assume the leptomonad 
form and multiply by binary fission. They 
may be either free in the lumen or attached 
to the walls. 

Their further development varies with 
the particular species of Pldebotomiis and 
strain of Leislniiaitia. In good vectors like 
P. argentipes, P. papatasii and P. sergenti, 
they begin to extend their range forward to 
the esophagus and pharynx by the fourth or 
fifth day. They continue to multiply to 
such an extent that they plug up the esopha- 
gus and interfere with blood- sucking. When 
an infected sandfly bites, it clears the pas- 
sage by injecting some of the leishmanial 
forms into its victim and thus transmits the 
parasite. Leishmauia may also be transmit- 
ted when sandflies are crushed on the skin. 

In other cases, the parasites remain 
in the sandfly midgut and do not pass for- 
ward into the pharynx. These can then be 
transmitted only by crushing the sandflies. 
A third type of development was described 
by Shoshina (1953), who found leptomonads 
in the hindgut of P. )nini(tiis var. arpark- 
leiisis in Russia and suggested that feces 
containing them might be rubbed into the 
bite while scratching it. 

In addition to transmission by sand- 
flies, it has been suggested that direct 
infection by means of excretions of infected 
individuals might occur in kala azar. 

Species of Leishmania : The specia- 
tion of Leislimaiiia has been discussed by 



66 



THE HEMOFLACELLATES 



Hoare (1949), Kirk (1949, 1950) and Biaga 
(1953) among others. While some 22 dif- 
ferent specific or subspecific names have 
been given to mammalian leishmanias, and 
while different strains are associated with 
different types of disease, neither morpho- 
logic, cultural nor immunologic characters 
can be used to differentiate the species of 
Leishiiia)iia. In practice, the species are 
separated on the basis of pathologic and 
epidemiologic differences and, since most 
studies have been made by parasitologists 
oriented toward human disease, the patho- 
logic characters used for each strain have 
been those seen in man. In the earlier 
days of our knowledge, when relatively few 
types were known, it was quite easy to de- 
lineate their characteristics and set up 
separate species, but as more studies 
were made, intermediate types were found 
and the boundaries between species tended 
to disappear. 

Some parasitologists consider that all 
the leishmanias of man and dogs should be 
assigned to a single species. Others pre- 
fer to assign them to two species, and 
still others to three. One can justify each 
of these schemes, but in all of them each 
species is still composed of a number of 
strains or demes. 

In this book, two species of Leish- 
mania are recognized: L. doiiovani, 
causing various visceral forms of disease, 
and L. tropica, causing various cutaneous 
and mucocutaneous forms. The third spe- 
cies recognized by some authorities is 
L. hrasiliensis, which causes a mucocu- 
taneous form of the disease. 

Maps of the world distribution of 
leishmanioses together with climatologic 
and other information have been published 
by Piekarski (1952), Piekarski and Sibbing 
(1954), Piekarski, Hennig and Sibbing 
(1956, 1958a), the American Geographical 
Society (1954) and May (1954). 



LEISHMANIA DONOVANI 
(LAVERAN AND MESNIL, 1903) 
ROSS, 1903 

Synonyms : Piroplasma donovani, 
Leishmania infantum, L. canis, L. chagasi. 



Disease : Kala-azar; dum-dum fever; 
visceral leishmaniosis. 

Hosts : Man and the dog are the prin- 
cipal hosts of L. donovani. Infections have 
also been reported in the cat by Sergent 
el at. (1912) and Bosselut (1948), in the 
sheep by De Paolis (1935) and in the horse 
by Richardson (1926). 

Location : L. donovani occurs in the 
cells of the reticulo -endothelial system, 
including both the endothelial cells and the 
circulating monocytes and polymorphonu- 
clear leucocytes. The parasites are found 
thruout the body, but particularly in the 
endothelial cells of the blood and lymph 
vessels of the spleen, liver, bone marrow, 
lungs, kidneys, mesenteric lymph nodes 
and skin. 

Types of Disease, Geographic Distri - 
bution and Epidemiology : 

Five types of visceral leishmaniosis can 
be recognized: 

1. Indian kala-azar or dum-dum fever is 
the classical type of the disease. It is 
found in India and affects young adults 
(60%) and children 5 to 15 years old. 

It does not occur naturally in dogs altho 
they can be infected experimentally. It 
is transmitted by Phlebotoums argen- 
tipes. 

2. Sudanese kala-azar is found in the 
Sudan and Abyssinia. It affects people 
of the same ages as Indian kala-azar 
and does not occur naturally in dogs. 
It was found once in a horse (Kirk, 
1956). Oral lesions are frequently 
present, and this type of the disease is 
relatively refractory to treatment with 
antimony compounds. It is transmitted 
by P. orientalis. A similar form oc- 
curs in small, isolated pockets scat- 
tered thru Africa south of the Sahara. 
It may cause skin lesions in addition 

to the visceral ones. It is a zoonosis, 
and has been found in a gerbil ( Tatera 
vicina) and a ground squirrel {Xenis 
)7<////fs)(Manson-Bahr, 1959). 

3. Chinese kala-azar is found in northern 
China. It is more common in children 



THE HEMOFLAGELLATES 



67 



than in adults, and also occurs com- 
monly in dogs. It is transmitted by 
P. cliiiieiisis and P. 



sergeiiti. 



4. Mediterranean or infantile kala-azar 
is found in countries of the Mediter- 
ranean basin including southern 
Europe and in parts of tropical Africa. 
Dogs are much more commonly in- 
fected than man, and 90% of the af- 
fected people are children less than 5 
years old. The incidence in dogs may 
reach 20% in some countries, and in- 
fection rates as high as 40% have been 
reported in Greece and Samarkand. 
Even in such countries, the infection 
rate in children is only 1 to 2%. 
Mediterranean kala-azar is transmitted 
principally by P. perniciosus and P. 
major. 

5. South American kala-azar is found 
from Mexico to northern Argentina. 

It attacks human beings of all ages and 
also occurs in dogs and cats. In a 
monographic review of visceral leish- 
maniosis in Brazil, Da Silva (1957) 
stated that it is endemic and at times 
epidemic in certain areas, that it is 
transmitted by Plilebotonius longipal- 
pis from a natural reservoir host such 
as the dog, and that it occurs mostly 
among persons with a low economic 
status and particularly among the 
children of that group. According to 
Deane (1956, 1958), the dog is the 
principal urban reservoir and the most 
important source of human infection, 
while the "bush-dog" {Lycalopex vet- 
uliis) is probably the principal rural 
one. The disease is also transmitted 
by P. iiitermedius. 

Two cases of visceral leishmaniosis 
have been reported in dogs in the United 
States, one in Alabama by Thorson et al. 
(1955) and the other in Washington, D. C. 
by Gleiser, Thiel and Cashell (1957). 
Both dogs had been imported into this 
country from Greece. 

Of the five types of visceral leish- 
maniosis, the Mediterranean, Chinese 
and South American are zoonoses while 
the Indian and Sudanese are not. The 



reasons for this are not clear, since dogs 
can be infected experimentally with the 
Indian and Sudanese denies of L. cloiiovani. 
Adler and Theodor suggested that it may 
be because the Mediterranean type is trans- 
mitted by sandfly bites whereas the Indian 
type is transmitted when the sandfly is 
crushed on the skin. Since dogs and infants 
are not good flyslappers, they are not so 
likely to get Indian kala-azar. 

Pathogenesis : Kala-azar is an im- 
portant and highly fatal disease of man, 
particularly in India. After an incubation 
period of several months, it starts with an 
irregular fever lasting weeks to months. 
The spleen and liver hypertrophy. In ad- 
vanced cases, there is ulceration of the 
digestive tract (mouth, nose, large intes- 
tine) resulting in diarrhea, and ulceration 
of the skin. There is great emaciation, 
but the abdomen is swollen. In untreated 
cases, the mortality is 75 to 95%, being a 
little higher in adults than in infants. 
Death occurs in a few weeks to several 
years, often resulting from intercurrent 
disease. In treated cases, 85 to 95% re- 
cover. Following recovery, whitish spots 
which develop into lentil-sized nodules may 
appear in the skin, particularly of the face 
and neck. This condition is known as post- 
kala-azar dermal leishmanoid. 

Mediterranean kala-azar in children 
is similar to the above, but the disease 
usually runs a shorter course. 

Kala-azar is essentially a reticulo- 
endotheliosis. The reticulo-endothelial 
cells are increased in number and invaded 
by the parasites. The cut surface of the 
enormously enlarged spleen is congested, 
purple or brown, with prominent Malpig- 
hian corpuscles. The liver is enlarged 
and there is fatty infiltration of the Kupf- 
fer cells. The macrophages, myelocytes 
and neutrophiles of the bone marrow are 
filled with parasites. The lymph nodes 
are usually enlarged and the intestinal 
submucosa is infiltrated with macrophages 
filled with parasites; these are especially 
numerous around the Peyer's patches. In- 
testinal ulceration, if present, is usually 
a secondary condition. There is progres- 
sive leucopenia accompanied by monocytosis. 



68 



THE HEMOFLAGELLATES 



There may be anemia due to blockage of 
the reticulo-endothelial system. 

In dogs and also in the Brazilian bush- 
dog, L. duiiova)ii may cause either vis- 
ceral or cutaneous lesions, but the latter 
are much more common. The disease is 
usually chronic with low mortality, altho 
an acute, highly fatal type is known. 
There may be emaciation and anemia. 
There is an abundant scurfy desquamation 
of the skin, and in some dogs more or 
less numerous cutaneous ulcers. In 
Chinese kala-azar, cutaneous lesions occur 
especially around the nose and ears. The 
hair is shed on parts of the body, particu- 
larly the head. The parasites occur in the 
macrophages in the subcutaneous tissues 
or in nodular lesions in the skin. They 
have also been recovered from healthy 
appearing skin. The visceral type of the 
disease is similar to that in man. 

Diagnosis : The only sure diagnostic 
method is the demonstration of the para- 
sites themselves, altho serologic and 
other tests have also been used and are of 
suggestive value. Smears made from 
biopsy samples of spleen pulp, liver pulp, 
superficial lymph nodes, bone marrow or 
thick blood smears can be stained with 
Giemsa's stain and examined microscopi- 
cally. In visceral leishmaniosis, the 
spleen is most often positive, but a certain 
amount of danger is associated with punc- 
turing a soft, engorged, enlarged spleen. 
Thick blood smears are more often posi- 
tive in man than in dogs. 

Examination of bone marrow obtained 
by sternal puncture is becoming increas- 
ingly popular. In the cutaneous form of 
the disease, scrapings should be made 
for staining from the lesions or from the 
dermis with as little bleeding as possible. 
This is probably the method of choice for 
dogs, since the cutaneous disease is more 
common than the visceral form in them. 
L. donovaiii can often be found in appar- 
ently normal skin in dogs and also, in the 
Sudanese and Middle Asiatic forms of the 
disease, in man (Manson-Bahr, 1959). 
Examination of the superficial lymph 
nodes is also valuable. 



Leishmania can be cultivated readily 
in NNN medium or a similar medium. The 
medium is inoculated with spleen, lymph 
node or liver juice, bone marrow, blood, 
or excised dermis and incubated for a week 
to a month at 22 to 24"^ C. Leptomonad 
forms are present in culture. Leishmania 
can also be grown in chicken embryos 
(Trincao, 1948) and in tissue culture 
(Hawking, 1948); see Pipkin (1960) for a 
review of this subject. 

Animal inoculation can also be prac- 
ticed, but is not usually done because it 
takes several months. The golden hamster 
is the most susceptible laboratory animal. 

The complement fixation test has been 
used with some success, particularly in 
man. It is often positive before the para- 
sites themselves can be found. 

The formol gel test (Napier's aldehyde 
test) is positive in more advanced cases. 
It is carried out by adding a drop of com- 
mercial formalin to 1 ml of serum. In a 
positive reaction the serum turns into a 
milky white gel; a clear gel is not positive. 
Organic antimony compounds, resorcinol, 
and many other compounds will also pro- 
duce this reaction. It is due to an increase 
in euglobulin and decrease in albumin in 
the serum. It also occurs in diseases 
other than kala-azar. 

Treatment: Leishmanial infections 
can be treated successfully with various 
organic antimony compounds. The cheap- 
est is tartar emetic, which is administered 
intravenously. In man, at least 25 or 30 
doses totaling at least 2. 5 g must be ad- 
ministered daily or on alternate days. 
Pentavalent antimony compounds are more 
expensive, but they are less toxic, act 
more quickly, and most of them can be in- 
jected intramuscularly as well as intra- 
venously. Even so, 10 or 12 doses total- 
ing 2. 7 to 4. g are needed. Among these 
compounds are neostibosan, neostam, 
solustibosan and urea stibamine. The 
aromatic diamidines, pentamidine and stil- 
bamidine, have been used in treating hu- 
man leishmaniosis, but they are appar- 
ently not very effective in dogs. Goodwin 



THE HEMOFLAGELLATES 



69 



and Rollo (1955) reviewed the chemother- 
apy of leishmaniosis briefly. 

Control : Prevention of leishmanial 
infections depends on breaking the life 
cycle by elimination of sandflies. This 
can be done by residual spraying of houses, 
barns and outside resting places with DDT 
or other chlorinated hydrocarbon insecti- 
cides (Hertig, 1949; Corradetti, 1954; 
Deane, 1958). In addition, insect repel- 
lents such as dimethylphthalate can be 
rubbed on the skin, houses can be screened 
with very fine mesh wire, and decaying 
vegetation and other breeding places can 
be cleaned up. 

In regions where kala-azar is a 
zoonosis, treatment of infected dogs and 
destruction of strays will eliminate the 
reservoir of infection for man. 



LEISHMANIA TROPICA 
(WRIGHT, 1903) 
LUHE, 1906 

Synonyms : Helcosoma tropicnm, 
Sporozoa furuncidosa, Ovoplas»ia orien- 
tale, Plasmosoma jericiiaense, Leish- 
mania wrighti, L. Cunningham i, L. nilo- 
tica, L. recidiva, L. brasilieiisis, L. 
peruviana. 

Disease : Cutaneous leishmaniosis, 
mucocutaneous leishmaniosis, Oriental 
sore, Aleppo button, Jericho boil, Delhi 
boil, espundia, uta, chiclero ulcer, buba, 
plan bois, American forest leishmaniosis. 

Hosts : The usual hosts are man, the 
dog and, in parts of the Old World, gerbils 
{Rhombomys opimus) and other wild ro- 
dents. 

Location : L. tropica occurs in the 
monocytes and other cells of the reticulo- 
endothelial system, in cutaneous lesions 
and in the skin. It may also occur in the 
lymph nodes and in the mucous membranes. 

Types of Disease, Geographic Distri - 
bution and Epidemiology : 

Two forms of cutaneous leishmaniosis 
have been described in man in the Old 



World and 4 in the New. Separate sub- 
specific names have been given to some 
of them: 

1. Classical Oriental sore is found in 
regions with a hot, dry climate from 
the Mediterranean basin to central and 
northern India. It is caused by L. 
tropica minor. The incubation period 
is several months. The lesions are 
circumscribed, "dry" sores in the 
skin. They heal spontaneously and do 
not extend to the mucous membranes. 
The lymph nodes are involved in about 
10% of the cases. Dogs are commonly 
infected, and the disease is urban in 
distribution. In Teheran, Iran, for 
example, 40 to 50% of the dogs have 
skin ulcers. The disease is transmit- 
ted by Phleboto)}ins papatasii, P. ser- 
genti, P. perfiliewi and P. tongicuspis. 

2. "Moist" or "wet" Oriental sore is found 
in Central Asia and southern USSR. It 
is caused by L. tropica major; there is 
no cross-immunity between this sub- 
species and L. t. minor. The incuba- 
tion period is 1 to 6 weeks. The lesions 
are wet and ulcerative, but do not ex- 
tend to the mucous membranes. They 
heal spontaneously. The lymph nodes 
are often involved. The disease is rural 
in distribution. The reservoir hosts 
are various desert rodents, the gerbil 
{Rhombomys opimus) being the most 
important. The vector is P. caucasicus, 
which lives in the gerbil burrows. 

3. Mucocutaneous leishmaniosis or espun- 
dia is found in the Brazilian rain for- 
ests. It is caused by L. tropica bra- 
siliensis, which many authors consider 
a separate species, L. brasiliensis. 
The skin lesions are chronic and spread- 
ing, often invading the mucous mem- 
branes either by metastasis or extension, 
and sometimes causing great disfigure- 
ment. Spontaneous recovery is rare. 
The lymph nodes are seldom involved. 
Dogs and occasionally cats have been 
found naturally infected, but the true res- 
ervoir hosts have not been discovered; 
they are probably wild jungle mammals. 
The retus monkey and various squirrels 
can be readily infected, but the golden 
hamster is refractory. The vectors are 



70 



THE HEMOFLAGEUATES 



Phlebotomus intermedins (syn. , Pllittzi), 
and also probably P. iiiigonei, P. whit- 
niani and P. pessoai. 

4. Uta occurs in the mountains of Peru. 
It is a benign form of the disease, 
with numerous small skin lesions. Its 
reservoir hosts and vectors are ap- 
parently unknown. 

5. American forest leishmaniosis, pian 
bois or buba is found in Panama, Costa 
Rica, the Guianas and other parts of 
northern South America. It is caused 
by L. Iropica gidaneiisis. The skin 
lesions are moderately ulcerated, and 
ordinarily heal spontaneously unless 
they involve the nose. About 5% of the 
patients have lesions of the mucous 
membranes which have arisen by ex- 
tension rather than by metastasis. 
The lymph nodes are involved in about 
10%. Dogs may be naturally infected, 
but the wild reservoirs are unknown. 
The vectors in Venezuela are believed 
to be PlilebutoDius evansi, P. niigoiiei, 
P. parasinensis and P. siiis. 

6. Chiclero ulcer or bay sore is found in 
Guatemala, southeastern Mexico and 
British Honduras. It gets its name 
because it is common among chicle 
and rubber hunters in rain forests. It 
is caused by L. tropica mexicaiia. The 
skin lesions are small. They heal 
spontaneously in a few weeks to a few 
months unless they involve the ear. In 
this location they cause chronic, dis- 
figuring nodular ulcers which may per- 
sist many years. There is no metas- 
tasis to the mucous membranes, and 
cutaneous metastases are rare. The 
lymph nodes are involved in about 2%. 
Nothing is known of the wild reser- 
voirs or of the vectors, altho the dis- 
ease is clearly a zoonosis (Garnham 
and Lewis, 1959). 

Both the Old World types of cutaneous 
leishmaniosis are zoonoses, but their 
epidemiology is quite different. The dry 
type is an urban disease common to dogs 
and man, while the moist type is a rural 
disease of gerbils and other rodents which 
affects man more or less incidentally. 



The American forms, too, occur primarily 
in wild animals, mostly unknown, of the 
tropical rain forests; both man and dogs 
are secondary hosts. 

Pathogenesis : The ulcers or sores 
of classical, dry Oriental sore are found 
on exposed parts of the body in man. At 
first they resemble mosquito bites, but 
they do not go away. The lesion grows 
slowly, becoming covered with thick brown 
scales. It itches a great deal, and scratch- 
ing produces a small ulcer which is covered 
with a crust. This enlarges slowly, and 
may finally be several centimeters in diam- 
eter. After some months or a year, con- 
nective tissue is formed, but a permanent 
scar is left. The disease is very seldom 
fatal. 

In the central Asian form of the dis- 
ease, the lesions are moist. They develop 
more rapidly, becoming ulcerative in one 
or two weeks, and then heal spontaneously. 
Relatively few parasites can be found in 
them. 

In espundia, the ulcers are often worse 
than those of Oriental sore and may last 
much longer. They usually heal in 7 to 8 
months, but sometimes last more than 20 
years. In addition, in some cases they may 
extend to the mucosa of the mouth or nose 
either directly or by metastasis. When 
they do this, they may cause a great deal of 
disfigurement; in extreme cases the nose 
may even be completely eaten away. 

The lesions in the dog are similar to 
those in man. They are probably confined 
to the skin. Visceral leishmaniosis due to 
L. tropica has been reported in dogs, but 
many observers believe that these are due 
to concurrent infections with L. donovani. 
In infected gerbils, cutaneous sores occur 
on the ears. 

Immunity : Persons who have recov- 
ered spontaneously from classical Oriental 
sore have a solid immunity. This fact is 
so well known among the natives that they 
vaccinate themselves on the arm in order 
to avoid natural, disfiguring ulcers on the 
face. There is no cross-immunity between 
the wet and dry Old World types of the 



THE HEMOFLAGELLATES 



71 



disease, between these and the New World 
forms, or between L. tropica and L. dono- 
vani infections. 

Diagnosis : The same methods are 
used in diagnosing L. tropica as L. dono- 
vaiii infections, except for the tissues ex- 
amined. The parasites are usually abun- 
dant in dry Oriental sore, but are scanty 
in wet Oriental sore and New World muco- 
cutaneous leishmaniosis. 

A skin test, the Montenegro intrader- 
mal reaction, is used with considerable 
success in diagnosing American muco- 
cutaneous leishmaniosis. A suspension of 
killed organisms from NNN culture is in- 
jected intradermally. In positive cases, 
an erythematous wheal appears in 48 hours 
and lasts 4 or 5 days. A small sterile 
papule which becomes vesicular or pustu- 
lar develops in the center of the wheal. 

Treatment : Organic antimony com- 
pounds are effective against cutaneous 
leishmaniosis. The same ones are used 
as for kala-azar. 

Control : The same measures used 
to prevent kala-azar are effective against 
cutaneous leishmaniosis. 



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Wood, 


s 


F. 


1951a 


Wood, 


s. 


F. 


1953. 


Wood, 


s. 


F. 


1953a 


Wood, 


s. 


F. 


1958. 



Chapter 4 



HISTOMOHAS 



Histomonas belongs to the order 
Rhizomastigorida, members of which 
possess both flagella and pseudopods. 
Within this order it belongs to the family 
Mastigamoebidae, members of which have 
1 to 4 flagella. Histo»ionas is the only 
genus in this order occurring in domestic 
animals. 

Genus HISTOMONAS 
Tyzzer, 1920 

The body is actively amoeboid, 
usually rounded, sometimes elongate, 
with a single nucleus, and with 1 to 4 ex- 
tremely fine flagella arising from a basal 
granule close to the nucleus. A single 
species, H. meleagridis is recognized. 



HISTOMONAS MELEAGRIDIS 
(SMITH, 1895) TYZZER, 1920 

Disease : Histomonosis, infectious 
enterohepatitis, blackhead. 

Hosts : Chicken, turkey, peafowl, 
guinea fowl, pheasant, ruffed grouse, 
quail, chukar partridge. 

Location : Ceca, liver. 

Geographic Distribution : Worldwide. 

Prevalence : This parasite is prac- 
tically ubiquitous in chickens, altho it 
seldom causes disease in them. It is one 
of the most important causes of disease 
in turkeys. Before control measures were 
developed, it drove many turkey raisers 
out of the business, and even now the United 
States Department of Agriculture (1954) has 
estimated that it causes an annual loss of 
$3,815,000 in turkeys and Sl49,000 in 
chickens due to mortality alone. 

Morphology : This parasite was first 
recognized by Theobald Smith in 1895. He 
thought it was an amoeba and named it 
accordingly. It was later confused with a 
number of other microorganisms. Some 
workers thought that it was one of the forms 



74 - 



HISTOMONAS 



75 



assumed by a pleomorphic Trichomonas, 
others that it was part of the life cycle of 
a coccidium, and still others confused it 
with the budding fungus, Blastocyslis. 
Finally Tyzzer (1919, 1920, 1920a) showed 
that the organism was a flagellate and des- 
cribed it in detail. His observations have 
been confirmed by DeVolt and Davis (1936), 
Bishop (1938) and Wenrich (1943) among 
others. 

H. meleagridis is pleomorphic, its 
appearance depending upon its location and 
the stage of the disease. The forms in the 
tissues have no discernible flagella, altho 
there is a basal granule near the nucleus. 
Tyzzer described three stages. The in- 
vasive stage is found in early cecal and 
liver lesions and at the periphery of older 
lesions. It is extracellular. It is 8 to 
ITjLL long and is actively amoeboid, with 
blunt, rounded pseudopods. Its cytoplasm 
is basophilic with an outer zone of clear 
ectoplasm and finely granular endoplasm. 
Food vacuoles containing particles of in- 
gested material but no bacteria are pres- 
ent. 

The vegetative stage is found near the 
center of the lesions and in slightly older 
lesions than the invasive stage. It is 
larger, measuring 12 to 15 by 12 to 21 jj,. 
It is less active than the invasive stage 
and has few if any cytoplasmic inclusions. 
Its cytoplasm is basophilic, clear and 
transparent. The vegetative forms are 
often packed tightly together, and cause 
disruption of the tissues. 

Tyzzer called the third form the re- 
sistant stage, but it is actually no more 
resistant than the other stages. There 
are no cysts. This form is 4 to 11 fi in 
diameter, compact, and seems to be en- 
closed in a dense membrane. The cyto- 
plasm is acidophilic and filled with small 
granules or globules. These forms may 
be found singly or they may be packed to- 
gether so that their outlines appear rather 
angular. They, too, are extracellular, 
but they may be taken up by phagocytes or 
giant cells. 

A fourth form of the parasite is fla- 
gellated and occurs in the lumen of the 



ceca. The same form is found in cultures. 
Its body is amoeboid and may be 5 to 30 [^ 
in diameter. Wenrich (1943) found that 




Fig. 5. Histoiiionas meleagridis tropho- 
zoites from cecum. A. Living 
trophozoite. B. , C. , D. Tropho- 
zoites fixed in Schaudinn's fluid 
and stained with iron-alum hema- 
toxylin. X 2300 (From Wenrich, 
1943, J. Morph. 72:279) 

400 individuals from the ceca of 2 phea- 
sants measured 9 to 28 /i in diameter with 
a mean of 13.9fi, and that 400 individuals 
from the ceca of 2 chickens measured 5 to 
18 JJ, in diameter with a mean of 7. 9 |j. . 
The cytoplasm is usually composed of a 
clear, outer ectosarc and a coarsely gran- 
ular endosarc. It may contain bacteria, 
starch grains and other food particles, in- 
cluding an occasional red blood cell. The 
nucleus is often vesicular, with a single 
dense karyosome, or it may contain as 
many as 8 scattered chromatin granules. 
Near the nucleus is a basal granule or 
blepharoplast from which the flagella a- 
rise. There is typically a single, short 
flagellum, but as many as 4 may be pres- 
ent. Movement may be amoeboid, and 
there may be a pulsating, rhythmic, 



76 



HISTOMONAS 



intracytoplasmic movement. The flagella 
produce a characteristic, jerky, oscillat- 
ing movement resembling that of tricho- 
monads, but Hislomonas can be differen- 
tiated from them because it lacks an 
undulating membrane and cixostyle. 
Wenrich (1943) found peculiar, cylindrical 
feeding tubes in about 15"( of the individuals 
from one of the 2 pheasants he examined 
and also in some individuals from a chicken. 
These sometimes extended out as much as 
the body diameter and often had internal 
extensions as long or longer. 

This form is sometimes present in 
large numbers in the lumen of the ceca, 
but it is ordinarily absent or very difficult 
to find. 

Life Cycle : Reproduction is by binary 
fission, and there is no evidence of a sex- 
ual cycle. Wenrich (1943) considered the 
larger, 4-flagellate forms in the ceca to 
be adult. There are no cysts. 

The naked trophozoites are delicate 
and do not survive more than a few hours 
when passed in the feces. Turkeys can be 
infected by ingesting trophozoites, and this 
mode of infection plays a part in transmit- 
ting the parasites once disease has ap- 
peared in a flock (Tyzzer and Collier, 
1925). However, large numbers of the 
parasites must be ingested. Tyzzer (1934) 
pointed out that oral infection with infected 
liver tissue or cecal discharges is some- 
what unreliable because of the death of the 
protozoa during their passage thru the al- 
imentary tract. Lund (1956) found that 
oral administration of 10,000 to 100,000 
protozoa in saline caused infections in 
about 40% of 6- to 9-week-old poults, and 
illness in about 20%. However, when di- 
gestible materials were added to the inoc- 
ulum, the infection and morbidity rates 
fell sharply. The protozoa remained in 
the gizzard and upper intestine longer in 
the presence of food, and were destroyed 
before they reached the cecum. Horton- 
Smith and Long (1956a) found that infections 
with trophozoite suspensions could be pro- 
duced only in starved chickens or, in 
chickens that were feeding, by giving them 
an alkaline mixture just before dosing 
them. They believed that successful in- 



fection depends on the pH of the gizzard 

and possibly upper intestine. The pH of 
the starved gizzard is 6. 3 to 7. 0, that of 
chickens on feed is 2. 9 to 3. 3, and that of 
chickens on feed which have received 
alkali is 6. 2 to 6. 5. 

By far the most important mode of 
transmission is in the eggs of the cecal 
worm, Heterakis galli)iariim. Its discov- 
ery by Smith and Graybill (1920) was a 
milestone in the history of parasitology. 
This mode of transmission has been amply 
confirmed by many workers, and is the 
preferred method of producing experimental 
infections (Tyzzer and Fabyan, 1922; Tyzzer, 
1926; Swales, 1948; McKay and Morehouse, 
1948; Lund and Burtner, 1958). The para- 
sites are carried inside the Heterakis eggs; 
eggs treated with disinfectants or other 
chemicals which do not kill them are still 
infective. 

Infection of Heterakis eggs is so wide- 
spread that Histouionas infections can be 
produced with batches of eggs taken from a 
very high percentage of turkeys or chickens 
even if the hosts do not appear sick. Not 
every egg is infected, however. Lund and 
Burtner (1957) found that less than 0. 5% of 
the embryonated eggs from experimentally 
infected chickens contained the protozoa, 
that less than half of the cecal worms they 
examined from these birds contained Hist- 
o)iiuiias -iniected eggs, and that positive 
worms contained an average of only 2 in- 
fected eggs each. 

The Heterakis eggs must hatch and 
liberate larvae in order to transmit the 
protozoa. Histomonas has never been seen 
in the infective eggs, its presence being 
inferred from the experimental results. 
However, Tyzzer (1926) found the protozoa 
in half-grown Heterakis from birds with 
histomonosis, and (1934) in the cells of the 
intestinal wall of 10-, 12-, and 21 -day old 
worms from experimentally infected birds, 
and Kendall (1959) found them in a 4-day - 
old H. galluiarum larva. 

The possibility that arthropods may 
transmit histomonosis has been considered 
by a number of authors. Mechanical trans- 
mission by flies and even grasshoppers is 



HISTOMONAS 



77 



possible (Frank, 1953), but it is of minor 
importance. 

Epidemiology: Histomonas is ex- 
tremely common in Heterakis-irdecieA 
chickens, and these birds constitute the 
principal reservoir of infection for turkeys. 
This accounts for the fact that it is almost 
impossible to raise turkeys successfully 
on the same farm with chickens. In addi- 
tion, wild gallinaceous birds such as the 
wild turkey, pheasant, quail and ruffed 
grouse may be infected, but their role as 
reservoirs of infection for domestic tur- 
keys has not been properly assessed. 

Birds become infected most commonly 
by ingesting infected Heterakis eggs. In- 
fective eggs can survive for one to two 
years or even longer in the soil. Farr 
(1956) infected chickens and turkeys with 
Hisfonioiias from eggs which had been in 
the soil in Maryland for 66 weeks. 

Pathogenesis : Histomonosis can 
affect turkeys of all ages; the course and 
mortality of the disease vary with age. 
Poults less than 3 weeks old are refrac- 
tory according to Swales and Frank (1948), 
but from this age to about 12 weeks, the 
disease is acute and may cause losses 
averaging 50% of the flock and ranging up 
to 100%. The birds often die 2 or 3 days 
after showing the first signs of disease. 
In older birds, the disease is more chronic, 
and recovery may take place. The mortal- 
ity decreases with age, and losses in these 
birds rarely exceed 25%. However, even 
birds of breeding age may be affected. 

Chickens are much less susceptible 
than turkeys. They ordinarily show no 
signs of disease, but serious outbreaks 
may occur in young birds. Histomonosis 
occasionally occurs in the peafowl (Gray- 
bill, 1925; Dickinson, 1930), guinea fowl 
(Graybill, 1925) and quail (GraybiU, 1925). 
Serious outbreaks may occur in captive 
ruffed grouse (Tyzzer and Fabyan, 1920; 
Graybill, 1925) and chukar partridges 
(Honess, 1956). Altho the parasite occurs 
in pheasants, it is apparently not very 
pathogenic for them. 

When the histomonads are released 
in the cecum, they enter the wall and 



multiply, causing characteristic lesions. 
Later they pass by way of the blood stream 
to the liver. 

The incubation period is 15 to 21 days. 
The first sign of disease is droopiness. 
The birds appear weak and drov/sy, and 
stand with lowered head, ruffled feathers 
and drooping wings and tail. There is a 
sulfur-colored diarrhea. The head may 
or may not become darkened. This sign, 
which is responsible for the name black- 
head, may also occur in other diseases, 
so the term is a misnomer. 

The principal lesions of histomonosis 
occur in the cecum and liver. One or both 
ceca may be affected. Small, raised pin- 
point ulcers containing the parasites are 
formed first. These enlarge and may in- 
volve the whole cecal mucosa. Sometimes 
the ulcers perforate the cecal wall and 
cause peritonitis or adhesions. The mu- 
cosa becomes thickened and necrotic. It 
may be covered with a characteristic, foul- 
smelling, yellowish exudate which may 
consolidate to form a dry, hard, cheesy 
plug that fills the cecum and adheres 
tightly to its wall. The ceca are markedly 
inflamed and often enlarged. 

The liver lesions are pathognomonic o 
They are circular, depressed, yellowish 
to yellowish green areas of necrosis and 
tissue degeneration. They are not encap- 
sulated, but merge with the healthy tissue. 
They vary in diameter up to a centimeter 
or more and extend deeply into the liver. 
In older birds the lesions are often con- 
fluent. 

Other organs such as the kidney and 
lung may occasionally be affected. P. P. 
Levine (1947), for example, described 
numerous white, round areas about 1 mm 
in diameter in the kidneys of an affected 
turkey. 

The parasites can be readily found on 
histologic examination of the lesions. Hy- 
peremia, hemorrhage, lymphocytic infil- 
tration, and necrosis occur, and macro- 
phages and giant cells are present. The 
pathology of histomonosis in turkeys has 
been described by Malewitz, Runnels and 
Calhoun (1958) among others. 



78 



HISTOMONAS 



McGuire and Cavett (1952) studied the 
effect of histomonosis on the blood picture 
of experimentally infected turkeys. The 
non-protein nitrogen, uric acid and hemo- 
globin levels declined progressively, but 
tended to recover just before death. The 
blood sugar rose during the incubation 
period but decreased during development 
of the liver lesions; severe hypoglycemia 
was present just before death. The total 
leucocyte count rose as the result of pro- 
liferation of heterophils, myelocytes and 
monocytes. 

If the birds recover, the protozoa dis- 
appear from the tissues, and repair takes 
place. The exudate and necrotic tissue in 
the ceca are incorporated into the cecal 
plug, which becomes smaller and is finally 
passed. U the lesions were not too severe, 
the ceca may eventually appear entirely 
normal, but in other cases there may be 
so much scarring that the lumen is oblit- 
erated. In the repair process, the lesions 
are invaded by blood vessels, lymphoid 
cells and connective tissue. The liver 
lesions may be completely repaired or 
there may be extensive scar tissue. 

Immunity : Birds which recover from 
histomonosis are immune to reinfection. 
In addition, as mentioned above, suscep- 
tibility decreases with age. 

Lund (1959) found that infection of tur- 
keys with a nonpathogenic strain of Histo- 
monas did not protect the birds against 
subsequent infection with a pathogenic 
strain introduced by feeding Heterakis eggs, 
altho it did afford some protection against 
rectally introduced pathogenic histomonads. 

Diagnosis : Histomonosis can be di- 
agnosed from its lesions. Those in the 
liver are pathognomonic. In case of doubt 
and in order to differentiate the liver le- 
sions from those caused by tumors, tuber- 
culosis or mycotic infections, histologic 
examination is desirable. The cecal le- 
sions can be distinguished from those 
caused by coccidia by microscopic exam- 
ination of scrapings from the mucosa. 

Cultivation : Histomonas was first 
cultivated by Drbohlav (1924) in a diphasic 
medium consisting of coagulated egg white 



slants overlaid with blood bouillon contain- 
ing 1% peptone. It has since been culti- 
vated in a number of other media, both di- 
phasic and monophasic (Tyzzer, 1934; 
De Volt and Davis, 1936; Bishop, 1938). 
Delappe (1953, 1953a) found that addition 
of penicillin or streptomycin or both to 
Laidlaw's culture medium facilitated the 
initial isolation of the protozoa, but he was 
unable to obtain axenic cultures. When the 
bacteria disappeared, the protozoa did 
likewise. 

Treatment: Since histomonosis can 
be prevented by proper management, drug 
therapy should be regarded as a secondary 
line of defense against the disease. The 
chemotherapy of this disease has been re- 
viewed by Wehr, Farr and McLoughlin 
(1958). 

While a number of phenylarsonic acid 
and quinoline derivatives have been used 
with some success in the past, the only 
one of them which is now used to any extent 
is 4-nitrophenylarsonic acid. When fed as 
0.0125 to 0.075% of the mash or 0.006 to 
0. 04% of the drinking water for 3 days be- 
fore and 21 days after experimental infec- 
tion, this compound prevents death. How- 
ever, there is a high relapse rate following 
cessation of treatment. Hence, to be effec- 
tive this compound must be fed continuously 
until 5 days before slaughter. Mashes con- 
taining 0.01 to 0.03% of this compound 
stimulate growth, but 0.02% in the drinking 
water decreases egg production of adults 
and growth and livability of poults (Moreng 
and Bryant, 1956). 

Thiazole derivatives are used most 
commonly against histomonosis. Three of 
these are enheptin, acetylenheptin, and 
nithiazide (Hepzide). The first is 2-amino- 
5-nitrothiazole, and the other two are de- 
rivatives of it. Enheptin was introduced 
by Waletzky, Clark and Marson (1950), 
and its activity was confirmed by a number 
of workers, including McGregor (1953), 
Jungherr and Winn (1950), DeVolt, Tromba 
and Hoist (1954), and Joyner and Kendall 
(1955). Acetylenheptin (2-acetylamino-5- 
nitrothiazole) was found by Grumbles, 
Boney and Turk (1952, 1952a, 1952b) to be 
just as effective as enheptin; it was also 
studied by Brander and Wood (1955) and 



HISTOMONAS 



79 



Cooper and Skulski (1957) among others. 
Nithiazide (l-ethyl-3-[ 5-nitro-2-thiazolyl] 
urea) was introduced by Cuckler et al. 
(1956, 1957) and Cuckler and Malanga 
(1956). 

These drugs have both prophylactic, 
suppressive and therapeutic value. En- 
heptin is usually fed continuously in the 
mash at the rate of 0.05% for prevention 
and suppression. If feeding is begun 
within 2 days after the infective dose of 
Histomonas is given in an experimental 
infection, it will almost completely pre- 
vent the disease. If it is begun later than 
this, it will suppress the disease as long 
as it is continued, but after it is withdrawn, 
histomonosis will reappear in the flock. 
If enheptin is to be used in treating turkeys 
which already show signs of disease, 0. 1 
to 0. 2% of the drug is mixed in the feed. 
Not all the birds will recover, but quite a 
high percentage do. Acetylenheptin is 
used in much the same way. The preven- 
tive level of nithiazide in the feed recom- 
mended by the manufacturer in 1958 was 
0.03%. 

Potential hazards are often associ- 
ated with feeding drugs continuously. 
Hudson and Pino (1952) and Pino, Rosen- 
blatt and Hudson (1954) found that enheptin 
prevented or delayed sexual maturity in 
chickens and turkeys. When fed in the 
ration to chickens, it produced complete - 
sexual involution or inhibition in both 
males and females. In young birds, sex- 
ual development did not take place, while 
in older ones the testes, ovary and oviduct 
atrophied. The effect was less marked in 
turkeys, altho 0.1% enheptin in the ration 
reduced the level of reproductive perform- 
ance. This effect was found to be due to 
inhibition of gonadotropin secretion by the 
pituitary, and could be counteracted, at 
least in part, by simultaneous administra- 
tion of gonadotropic hormone. Shellabar- 
ger and Schatzlein (1955) found that enhep- 
tin caused rats to have larger thyroid 
glands and to accumulate less iodine than 
normal rats. They suggested that these 
antithyroid properties might explain why 
enheptin inhibits the secretion of pituitary 
gonadotropin in the chicken. 



Grumbles, Boney and Turk (1952) 
and Cooper and Skulski (1957) compared 
enheptin with acetylenheptin. The former 
found that 0. 1% enheptin in the feed reduced 
production, fertility and hatchability in tur- 
keys, but that acetylenheptin had no such 
effect. The latter found that enheptin de- 
creased spermatogenesis and egg produc- 
tion and increased embryo mortality when 
fed to chickens at preventive levels. Acet- 
ylenheptin was less toxic. It had no effect 
on egg production, fertility or embryo 
mortality, and reduced sperm production 
only slightly. 

According to Cuckler, Porter and Ott 
(1957), 0.1% nithiazide in the feed did not 
interfere with growth, maturation or re- 
production of chickens or turkeys. 

The nitrofuran, furazolidone (NF-180, 
Furoxone), was found by McGregor 
(1953a, 1954), Horton-Smith and Long 
(1955, 1956) and Costello and DeVolt (1956) 
to suppress histomonosis when fed at the 
rate of 0. 01 to 0. 04% in the feed. Even 
with the higher doses, however, some re- 
lapses occurred after medication was 
stopped, and slight lesions were found in 
treated birds killed during the experiments. 

Cooper (1956) reported that feeding 
0. 02% furazolidone to pullets for 12 weeks 
had no effect on body weight, egg produc- 
tion, fertility or hatchability, but Cooper 
and Skulski (1955, 1956) found that feeding 
this drug to cockerels and roosters re- 
duced the number of spermatozoa and de- 
creased weight gains. 

Control : Histomonosis can be pre- 
vented by good management. Turkeys 
should be kept separate from chickens, 
since chickens are carriers. Young tur- 
keys should be kept separate from adults. 
The same attendants should not care for 
chickens and turkeys. Persons who go 
from one flock to another should take care 
not to carry the infection on contaminated 
shoes or equipment. 

Young birds should be raised on hard- 
ware cloth, and the droppings should be 
removed regularly. When the poults are 



80 



HISTOMONAS 



old enough to move onto range, they should 
be placed on clean ground where neither 
turkeys nor chickens have been kept for 2 
years. The length of time infective cecal 
worm eggs survive in the soil depends upon 
soil type, weather and amount of cover 
provided by vegetation. They will survive 
only a few weeks on barren soils in warm, 
dry regions, but may remain alive for 
several years in heavy soils in moist cli- 
mates. 



roughage. The medicated ration is given 
for 5 to 7 days, the regular ration is fed 
for about 15 days, the medicated ration is 
then given again and alternated as before 
with regular feed until about 3 weeks be- 
fore the birds are to be marketed. Pheno- 
thiazine should not be fed during these 3 
weeks. 



LITERATURE CITED 



The range should be rotated at regular 
intervals. Different farmers use different 
intervals. Many of them move the birds 
along every week, not returning to the 
same place during the same season. An- 
other rotation system which has been rec- 
ommended is to move the birds thru a 
series of 4 lots, allowing them to remain 
on each for a month. The frequency of ro- 
tation depends on the climate. In cool, 
damp climates the birds should be moved 
at least every 10 days, but in hot, dry 
climates they need be moved less frequent- 
ly, and it is even possible to raise turkeys 
successfully without changing the range if 
the area around the feeders, waterers, 
roosts and shelters is kept dry. 

Low areas and streams that drain 
poultry yards should be fenced off. 

The feeders and waterers should be 
placed on wire platforms. Most of the 
droppings are deposited around them, and 
this practice keeps the turkeys from getting 
at them. Wire should also be used beneath 
roosts and in shelters to keep the birds 
from their droppings. 

Treating the birds with phenothiazine 
to prevent histomonosis by killing the 
cecal worms has been suggested. It is in- 
effective in controlling active outbreaks, 
but may help prevent future ones. Pheno- 
thiazine kills the cecal worms, but does 
not prevent their eggs from hatching and 
releasing the histomonads (Wehr and 
Olivier, 1946). 

To eliminate Heterakis, 0. 5% pheno- 
thiazine is mixed with the feed if the birds 
are not getting roughage, and 1.0% if they 
are on good range or getting supplementary 



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81 



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18:397-400. 
McGuire, W. C. and]. W. Cavett. 1952. Poult. Sci. 

31:610-617. 
McKay, F. andN. F. Morehouse. 1948. ]. Parasit. 

34:137-141. 
Moreng, R. E. and R. L. Bryant. 1956. Poult. Sci. 35: 

406-409. 
Pino, ]. A., L. S Rosenblatt and C. B. Hudson. 1954. 

Proc. Soc. Exp. Biol. Med. 87:201-207. 
Shellabarger, C. J. and F. C. Schatzlein. 1955. Proc. Soc. 

Exp. Biol. Med. 90:470-473. 



Smith, T and H. W, Graybill. 1920. ]. Exp. Med. 32: 

143-152. 
Swales, W. E. 1948. Canad. J. Comp. Med. 12:97-100. 
Swales, W. E. and J. F. Franl<. 1948. Canad. ]. Comp. 

Med. 12:141-143. 
Tyzzer, E. E. 1919. ]. Med. Res. 40:1-30. 
Tyzzer, E. E. 1920. J. Parasit. 6:124-131. 
Tyzzer, E. E. 1920a. J. Med. Res. 41:219-237. 
Tyzzer, E. E. 1926. Proc. Soc. Exp. Biol. Med. 23:708-709. 
Tyzzer, E. E. 1934. Proc. Am. Acad. Arts Sci. 69:189-264. 
Tyzzer, E. E. and]. Collier. 1925. ]. Inf. Dis. 37:265-276. 
Tyzzer, E. E. andM. Fabyan. 1920. ]. Inf. Dis. 27:207-239. 
Tyzzer, E. E. andM. Fabyan. 1922. J. Exp. Med. 35:791-812. 
U. S. Dept. of Agriculture. 1954. Losses in agriculture. A 
preliminary appraisal for review. USDA Ag. Res. Serv. 
ARS-20-1. pp. 190. 
Waletzky, E. , ]. H. Clark and H. W. Marson. 1950. Science 

3:720-721. 
Wehr, E. E. , M. M. Farr and D. K. McLoughlin. 1958. 

]. Am. Vet. Med. Assoc. 132:439-445. 
Wehr, E. E. and L. G. Olivier. 1946. Poult. Sci. 25:199-203. 
Wenrich, D. H. 1943. ]. Morph. 72:279-303. 



Chapter 5 



WE 
TRICHOmUdS 



The trichomonads belong to the family 
Trichomonadidae within the order Trich- 
omonadorida. The body is usually piriform, 
with a rounded anterior end and a pointed 
posterior end. There is a single nucleus 
in the anterior part of the body. Anterior 
to the nucleus is a blepharuplasl composed 
of several basal granules . Two to five 
anterior flagella and a posterior flagellum 
arise from the blepharoplast. The posterior 
flagellum passes along the border of an iin- 
dHlati)ig me»ibrane which extends along the 
side of the body; a secondary or accessory 
filament may be associated with it. The 
posterior flagellum may or may not extend 
beyond the undulating membrane as a free 
flagellum. A filamentous costa arises from 
the blepharoplast and runs along the base of 
the undulating membrane. A parabasal 
body arises from the blepharoplast; there 
may or may not be a parabasal filament 
at its posterior end. A clear, rod-like 
axostyle also arises from the blepharoplast 
and passes thru the center of the body to 
emerge from the posterior end. The an- 
terior end of the axostyle is enlarged to 
form a capitulum. There may or may not 
be a chromatic ring at the point of emer- 
gence of the axostyle. There may or may 
not be a cytostome near the anterior end. 
Just anterior to the blepharoplast and lying 
along the anterior margin of the body is a 
pelta which stains with silver. In addition 
to these structures, there may be various 
granules within or along the axostyle, 
along the costa, or in other locations. 



An electron micrograph study of 
Tritrichomonas muris by Anderson (1955) 
revealed the fine structures of these or- 
ganelles which may be taken to represent 
the group. He found that the blepharoplast 
appears to be limited by a membrane and 
to contain basal granules for each organelle. 
The anterior and posterior flagella are 
composed of 2 central and 9 peripheral 
fibrils. The accessory filament is com- 
posed of two differentiated meshwork 
areas. The undulating membrane is com- 
posed of a series of lamellae 300 to 400 A 
thick; it is attached to the outer surface of 
the body by fine fibers 167 to 300 A thick. 



82 - 



THE TRICHOMONADS 



83 



PARABASAL BODY 
COSTA 



PARABASAL 

FILAMENT 




UNDULATING 
MEMBRANE 



FREE FLAGELLUM 



CHROMATIC RING 



TRICHOMONAS 
Fig. 6. Structures of Tyicliomonas. (Original) 

The costa consists of a series of discs 
about 370 A thick and 490 A apart, em- 
bedded in a matrix; it is attached to the 
inner surface of the body wall by exten- 
sions of the discs. The axostyle is lim- 
ited by a double, corrugated membrane. 
The chromatic ring is composed of a series 
of rods about 640 A thick. The parabasal 
body consists of a series of filaments about 
190 A thick. The chromatic granules along 
the costa, inside the axostyle and scattered 
in the cytoplasm are irregular in shape and 
vacuolated. The mitochondria are spher- 
ical and contain a varying number of pro- 
jections internally. 

Trichomonads are divided into sev- 
eral genera on the basis of the number of 
their anterior flagella. Ditrichomonas 
has 2, Tritrichomonas has 3, Trichomonas 
has 4, and Pentatrichonionas has 5. These 
genera are closely related; Mehra, Levine 
and Reber (1960), for example, found in a 
column chromatographic study of the hy- 
drolysates of Tritrichomonas foetus , T. 
suis, Trichomonas gallinae, T. galli- 
narum and T. buttreyi, that they are all 
composed of the same amino acids but that 
there are some differences in the amounts 



of each amino acid present in the different 
species. 

Gabel (1954) established the genus 
Paratrichomonas for P. marmotae from 
the woodchuck and possibly T. batrachorum 
from the frog. Paratrichomonas differs 
from Tritrichomonas orincipally in having 
a ring-shaped parabasal body. T. buttreyi 
of the pig resembles it, but has 4 anterior 
flagella. There does not seem to be suf- 
ficient justification for accepting this genus, 
at least at present. 

Morgan (1943, 1946) and Trussell (1947) 
have given host-parasite lists of the trich- 
omonad species. 

There are several species of tricho- 
monads in domestic animals and man, but 
the nomenclatorial status and host-parasite 
relations of many of them are not yet clear. 
They have been found in the cecum and 
colon of practically every species of mam- 
mal or bird that has been examined for 
them, and they also occur in reptiles, am- 
phibia, fish and many invertebrates. Those 
in the termite gut are particularly well 
known. Many of the cecal trichomonads 
look alike, and cross-transmission studies 
have shown that many of them can be easily 
transmitted from one host species to an- 
other. Some mammalian trichomonads 
have even been transmitted successfully to 
day-old chicks, altho they will not become 
established in older birds. Further and 
extensive studies are needed to establish 
the correct names and host spectra of all 
but a few trichomonads. 

Most trichomonads are non- pathogenic 
commensals, but a few are important path- 
ogens. None of the cecal trichomonads has 
ever been proven to be pathogenic, altho 
some people have thought that they were 
because they were found in animals which 
had enteritis or diarrhea. However, the 
mere presence of an organism in a diseased 
animal does not mean that the organism 
caused the disease. The latter may have 
set up conditions favorable to the organism's 
growth and multiplication. This is espe- 
cially true of the cecal trichomonads, which 
flourish in a fluid or semi-fluid habitat. 



84 



THE TRICHOMONADS 



The life cycle of trichomonads is sim- 
ple. They reproduce by longitudinal binary 
fission. No sexual stages are known. 
There are no cysts, altho degenerating or 
phagocytized individuals (or entirely dif- 
ferent organisms such as Blaslocyslis) 
have been mistaken for them. 

Genus TRITRICHOMONAS 
Kofoid, 1920 

Members of this genus have 3 anterior 
flagella. 



TRITRICHOMONAS FOETUS 

(RIEDMULLER, 1928) 

WENRICH AND EMMERSON, 1933 

Synonyms : Trichomonas utero- 
vaginalis vilulae, T. bovis, T. genitalis, 
T. bovinus, T. mazzanti. 

Disease : Bovine trichomonad abor- 
tion, bovine genital trichomonosis. 

Hosts : Ox, zebu, possibly pig, 
horse, roe deer. 



productive disorders in cows bred by in- 
fected western range bulls may amount to 
about S800 annually per infected bull. On 
this basis, the 23 infected bulls they found 
in their survey would cost their owners 
about $18,000 a year. The annual loss due 
to an infected bull in an artificial insemin- 
ation ring would be considerably greater 
than this. 

Morphology : The morphology of T. 
foetus has been studied by Wenrich and 
Emmerson (1933), Kirby (1951) and Ludvik 
(1954), among others. The body is spin- 
dle- to pear-shaped, 10 to 25/i long and 
3 to 15|U wide. It has 3 anterior flagella 
and a posterior flagellum which trails as 
a free flagellum about as long as the an- 
terior flagella. The undulating membrane 
extends almost the full length of the body 
and has an accessory filament along its 
margin. The costa is prominent. The 
axostyle is thick and hyaline, with a cap- 
itulum containing endoaxostylar granules 
and a chromatic ring at its point of emer- 
gence from the posterior end of the body. 
The parabasal body is sausage- or ring- 
shaped. A cytostome is present. There 
is no pelta. 



Location : Genital tract. 

Geographic Distribution : Worldwide. 
Morgan and Beach (1942) mapped the geo- 
graphic distribution of bovine trichomon- 
osis. 



Prevalence : Altho T. foetus is 
known to be widely distributed, few studies 
have been made of its incidence. It is 
especially common in southern Germany 
and Switzerland, up to 30% of the cattle 
having been found infected in some areas. 
In the U. S. , it is probably third to brucel- 
losis and leptospirosis as a cause of abor- 
tion in cattle. In a survey of 383 beef 
bulls in Utah, Idaho and Colorado, Fitz- 
gerald et at. (1958) found 6% to be infected. 

The USDA Agricultural Research Serv- 
ice (1954) estimated that bovine trichomon- 
osis causes an annual loss of $750,000 in 
the United States. This figure is probably 
low. Fitzgerald et at. (1958) estimated 
that losses in production because of re- 



Fig. 7. 



Tyilrichomonas foetus. X 3400 
(From Wenrich and Emmerson, 
1933, J. Morph. 55:193) 



Pathogenesis : A great deal has been 
written about bovine trichomonosis. 



THE TRICHOMONADS 



85 



Morgan's (1946) review listed 447 refer- 
ences, and many more papers have been 
published since then. Among more recent 
papers on its pathogenesis are those of 
Morgan (1947), Bartlett (1947), Bartlett 
and Dikmans (1949), Bartlett, Moist and 
Spurrell (1953), Laing (1956) and Gabel 
et al. (1956). 

Bovine trichomonosis is a venereal 
disease, transmitted by coitus. It can 
also be transmitted by artificial insemin- 
ation. Non-venereal transmission is very 
rare under natural conditions. After in- 
fection of the female, the trichomonads 
multiply at first in the vagina, causing a 
vaginitis. They are most numerous here 
14 to 18 days after infection (Hammond 
and Bartlett, 1945). They invade the 
uterus thru the cervix. They may disap- 
pear from the vagina or they may remain 
there, producing low-grade inflammation 
and catarrh. 

Early abortion is characteristic of 
bovine trichomonosis. Abortion usually 
occurs 1 to 16 weeks after breeding. The 
foetus is often so small that it is not ob- 
served by the owner, and he does not 
realize that abortion has occurred, be- 
lieving that the animal failed to conceive 
and that its heat periods are irregular. 
Morgan and Hawkins (1952) knew of only 
6 reports in the literature of abortion due 
to T. foetus after 6 months gestation. 

If the placenta and fetal membranes 
are completely eliminated following abor- 
tion, the animal usually recovers spon- 
taneously. This is the most common 
course. If, however, part of the placenta 
or membranes remain, a chronic catar- 
rhal or purulent endometritis results which 
which may cause permanent sterility. 

Sometimes the animal does not abort, 
but the fetus dies and becomes macerated 
in the uterus. Pyometra results, and the 
uterus may contain several quarts of a 
thin, greyish white fluid swarming with 
trichomonads. In the absence of bacteria, 
this fluid is almost odorless. The cervi- 
cal seal may remain intact or it may allow 
a small amount of fluid to escape when the 
animal is lying down. Animals with pyo- 



metra seldom come in heat, and the owner 
may believe them to be pregnant. In long- 
standing cases, the trichomonads may 
disappear from the uterine fluid. 

Occasionally normal gestation and 
calving may occur in an infected animal, 
but this is rare. 

In the bull, the most common site of 
infection is the preputial cavity, altho the 
testes, epididymis and seminal vesicles 
may sometimes be involved. Spontaneous 
recovery is rare; bulls remain infected 
permanently unless treated. The numbers 
of trichomonads fluctuate, the intervals 
between peaks being 5 to 10 days according 
to Hammond el al. (1950). 

Immunology: Cows or heifers which 
recover from infection are usually rela- 
tively immune, altho reinfections can occur. 

A number of investigators have studied 
various immunological responses to trich- 
omonad infection. Kerr and Robertson 
(1945) showed that there is more than one 
serological strain of T. foetus. McEnte- 
gart (1956) found that T. foetus var. belfast 
and T. foetus var. )uaiiley differed sero- 
logically from each other and from T. 
vaginalis. Menolasino and Hartman (1954) 
were unable to distinguish T. foetus from 
T. vaginalis serologically, but McDonald 
and Tatum (1948) and Schoenherr (1956) 
were able to do so. Both also found sero- 
logical differences between T.foetus and 
Pentatyicho>no)ias lioiiiiiiis, and the latter 
between T. /oe/;(S and T richonionas gal- 
liuae. Sanborn (1955) found that T. foetus 
differed serologically from the large pig 
cecal trichomonad, T. suis and from the 
pig nasal trichomonad. 

Kerr and Robertson (1941, 1943) and 
Pierce (1947) studied the agglutination test 
in cattle, and Feinberg (1952) described a 
capillary agglutination test. Kerr (1943) 
felt that his test was positive in about 60% 
of all infected cattle, but Morgan (1943a) 
considered it impractical. The wide dis- 
tribution in the animal kingdom of non- 
specific antibodies against T. foetus was 
brought out by Morgan (1944), who showed 
that the sera of the carp, horned lizard 



86 



THE TRICHOMONADS 



and leopard frog agglutinated T. foetus at 
1:2, those of the gold fish, pigeon and 
domestic rabbit at 1:4, those of the guinea 
fowl and chicken at 1:8, those of the turkey 
and sheep at 1:16, those of deer and goat 
at 1:32, that of the cow at 1:128 and that 
of the horse at 1:1024. 

Nakabayasi (1952) distinguished be- 
tween agglutination and agglomeration. 
With immune rabbit and infected guinea 
pig sera, agglomeration reached its max- 
imum within 30 minutes and then decreased 
gradually as the agglomerated individuals 
separated. On the other hand, the agglu- 
tination reaction reached its maximum 
within about an hour and did not reverse. 
Levine et al. (unpublished) have seen ag- 
glomeration of T. foetus following mixture 
with fresh culture media containing inac- 
tivated serum. 

Kerr and Robertson (1954, 1956) 
found "normal agglutinin" in the blood of 
calves which they apparently acquired in 
the colostrum; this agglutinin disappeared 
after 17 to 55 days. Injection of calves 
less than 4 weeks old did not induce anti- 
body formation, but instead caused im- 
pairment of antibody production (immuno- 
logical paralysis) which persisted for 
about 2 years. 

Complement fixation and precipitin 
reactions have been studied, but with un- 
satisfactory results (Svec, 1944; Morgan, 
1948). 

Kerr (1944) developed an intradermal 
test, using a trichloracetic acid-precip- 
itated extract of T. foetus called "tricin. " 
Positive reactions appear in 10 minutes, 
reach their peak within 30 minutes and 
disappear in about 6 hours. Fifty of 592 
cows at an abattoir were positive to this 
test, and trichomonads were found in 11 
of them on direct examination. Tricho- 
monads were also found in 11 of 34 bulls 
which were positive to the skin test. 
Morgan (1948) obtained negative results 
with skin tests with a number of different 
antigens. Kerr, McGirr and Robertson 
(1949) found that cattle could be desensi- 
tized to the skin test by injecting antigen 
intramuscularly, instilling it into the 



uterus of non-pregnant cows, or by inject- 
ing adreno-cortical hormone or sphingo- 
myelin at parturition. Absorption of 
antigen from acute uterine infections also 
desensitized the animals. 

A local immune reaction takes place 
in the vaginal mucosa of infected animals. 
In addition, the uterine mucosa is sensi- 
tized (Kerr and Robertson, 1953). The 
presence of agglutinins in the vaginal 
mucus prompted the development of a 
mucus agglutination diagnostic test by 
Pierce (1947a, 1949) and Florent (1947, 
1948, 1957). This test is considerably 
better than the blood agglutination test, 
but, according to Pierce (1949), must still 
be regarded as only a herd test because a 
number of infected animals fail to react. 
Unsatisfactory results are obtained with 
estral and post-estral vaginal mucus and 
with purulent uterine mucus containing 
trichomonads. Mucus from pregnant an- 
imals sometimes gives a false positive 
reaction. Schneider (1952), too, consid- 
ered the mucus agglutination test simply 
an adjunct to other means of diagnosis. 

Morgan (1947a) found that a series of 
16 intramuscular or intravenous injec- 
tions with living T. foetus over a period of 
3 months apparently protected heifers 
temporarily against genital infection, but 
6 intramuscular injections over a period 
of 3 weeks did not. This does not appear 
to be a practical method of prevention. 

Epidemiology : Bovine trichomonosis 
is a venereal disease transmitted at coitus. 
T. foetus is known to occur in cattle, but 
whether it is also present in other animals 
and whether it may be transmitted from 
them to cattle by a non-venereal route re- 
main to be determined. 

With the introduction of the technic of 
preserving bovine semen by freezing in 
the presence of glycerol, the question arose 
whether T. foetus would survive in frozen 
semen. Several investigators have studied 
the problem, and have found that the pro- 
tozoa may or may not survive freezing in 
the presence of glycerol, depending on the 
conditions (see Levine, Mizell and Houla- 
han, 1958 for a review of the literature). 



THE TRICHOMONADS 



87 



They survive in some media but not in 
others. Rapid freezing and high salt con- 
centration are deleterious (Levine and 
Marquardt, 1955; Levine, Mizell and 
Houlahan, 1958). The stage of the popu- 
lation growth curve is important, the pro- 
tozoa being much more sensitive to injury 
when frozen during the initial and logarith- 
mic phases than at the peak of the curve 
and for some time thereafter (Levine, 
McCaul and Mizell, 1959). Temperature 
fluctuation during storage is deleterious 
(Fitzgerald and Levine, 1961). 

A particularly interesting fact is that 
glycerol appears to be toxic at refrigerator 
temperatures but not at either sub-freezing 
or incubator (37° C) temperatures (Joyner, 
1954; Joyner and Bennett, 1956; Fitzgerald 
and Levine, 1961). It may be possible to 
develop a technic for freezing semen which 
would be sure to kill the protozoa, but at 
present the use of frozen semen from in- 
fected bulls cannot be recommended. 

Many different laboratory animals 
can be infected experimentally in various 
ways with T. foetus (see Morgan, 1946 for 
review). Leaving aside other routes of 
infection, successful vaginal infections 
with T. foetus have been established in 
the rabbit by Witte (1933) and others, in 
the guinea pig by Riedmuller (1928) and 
several others, in the golden hamster by 
Kradolfer (1954) and Uhlenhuth and 
Schoenherr (1955), in the dog by Trussell 
and McNutt (1941), in the goat by Wittfogel 
(1935) and Hammond and Leidl (1957), in 
the sheep by Wittfogel (1935) and Andrews 
and Rees (1936), and in the pig by Ham- 
mond and Leidl (1957). The golden ham- 
ster is the laboratory animal of choice for 
experimental vaginal infections. Abortions 
were produced in some of the infected 
guinea pigs. Laboratory mice and rats 
are refractory to vaginal infection. 

Kijst (1936) found trichomonads simi- 
lar to T. foetus in the genital tract and 
aborted fetuses of swine and horses in 
Germany. Petersen (1937) cultured trich- 
omonads resembling T. foetus from the 
genital tracts of 13 mares with pyometra. 
He also found an infected stallion which 
had transmitted trichomonads to mares. 



Schoop and Oehlkers (1939) also found 
trichomonads in the genital tract of horses. 
Schoop and Stolz (1939) found trichomonads 
resembling T. foetus in the uteri of 4 out 
of 5 roe deer in Germany. The infections 
were associated with sterility, and the 
trichomonads produced vaginitis in guinea 
pigs. Schoop (1940) suggested that if the 
trichomonads from deer were T. foetus, 
deer might be a source of infection for 
cattle. 

The relation of T. foetus to the trich- 
omonads of swine still remains to be elu- 
cidated. The pig nasal trichomonad, 
TritricJioiuoiias suis, greatly resembles 
T. foetus morphologically (Buttrey, 1956) 
and in metabolic characteristics (Doran, 
1957, 1959), and vaginal infections were 
readily established in cattle with it by 
Switzer (1951) and Fitzgerald et at. (1958). 
The infection reported by Switzer lasted 3 
weeks and was accompanied by a mild 
catarrhal vaginitis. Those reported by 
Fitzgerald et al. lasted 46 to 133 days, 
and some infections appeared to interfere 
with breeding efficiency. 

Vaginal infections of cattle with trich- 
omonads from the cecum and stomach of 
swine have also been readily established 
(Switzer, 1951; Hammond and Leidl, 
1957a; Fitzgerald e/ aZ. , 1958), and the 
latter two authors reported that bulls be- 
came infected by breeding infected heifers 
and then transmitted their infections to 
other heifers. The bulls later recovered 
spontaneously in both studies. Kerr (1958), 
too, infected heifers intravaginally with 
trichomonad from swine, using both strains 
obtained from Hammond and a strain of 
T. suis isolated in England. He found that 
the vaginal mucus agglutination test of 
heifers infected with porcine trichomonads 
was positive with T. suis and Belfast strain 
T. foetus antigens but not with Manley 
strain T. foetus antigen. 

In the other direction, Fitzgerald et al. 
(1958) produced cecal infections with T. 
foetus in young pigs. 

Robertson (1960) made a serologic 
comparison of the Belfast and Manley 
strains of T. foetus and Strains S2 and 414 



88 



THE TRICHOMONADS 



of T. siiis, isolated by Hammond and 
Leidl from the ceca of pigs in Germany 
and Utah, respectively. Using both the 
tube agglutination and precipitin tests and 
especially the gel diffusion precipitin test, 
she found considerable cross-reaction be- 
tween the 4 strains. All had the same 
major protein antigens, but they shared 
their major polysaccharide antigens only 
partially. The 2 bovine strains were 
readily distinguished from each other, 
while the 2 porcine strains were very 
closely related but not identical. The por- 
cine strains were more closely related to 
the Belfast than to the Manley strain of T. 
foetus. Robertson concluded that the 
serologic distinctions between the 4 strains 
did not justify separating them into 2 spe- 
cies, and she called them all T. foetus. 

Diagnosis : Altho the mucus aggluti- 
nation test and a number of other sero- 
logical procedures have been suggested 
for diagnosing T. foetus infections, the 
only sure method is to demonstrate the 
protozoa microscopically either directly 
or in culture. Diagnostic procedures have 
been described by Hammond and Bartlett 
(1945), Morgan (1945), Bartlett (1949), 
Fitzgerald et at. (1952) and Thorne, Shupe 
and Miner (1955), among others. 

In heavy infections, particularly of 
females, the trichomonads can be seen 
by direct examination of mucus or exudate 
from the vagina or uterus, amniotic or 
allantoic fluid, fetal membranes, placenta, 
fetus stomach contents, oral fluid or other 
fetal tissues, or, in bulls, of washings 
from the preputial cavity and rarely sem- 
inal fluid or semen. If trichomonads can- 
not be found on direct microscopic exam- 
ination, cultures should be made in 
CPLM, BGPS or Diamond's media (see 
below). 

Samples can be obtained from the 
vagina by washing with physiological salt 
solution in a bulbed douche syringe. They 
can be obtained from the preputial cavity 
with a cotton swab or, better, by washing 
with physiological salt solution in a bulbed 
pipette or syringe. The washings should 
be allowed to settle for 1 to 3 hours or 
centrifuged before examination. 



The external genitalia should be cleaned 
thoroughly before the samples are taken in 
order to avoid contamination with intestinal 
or coprophilic protozoa which might be mis- 
taken for T. foetus. Among these are 
Tritrichomonas enteris, Monocercotnonas 
noninaniiuni, Protriclwmonas niminantiutn, 
Bodo foetus, B. glissans, Spiromonas 
atigusta, Cercomonas crassicauda, Poly- 
tonia uvella, Monas obliqua and Lenibus 
pusillus. In identifying T. foetus, ii must 
be distinguished from these. 

Trichomonads are most numerous in 
the vagina 2 to 3 weeks after infection. 
Their numbers fluctuate in bulls, the in- 
terval between peaks being 5 to 10 days 
(Hammond et at. , 1950). 

A single examination is not sufficient 
to warrant a negative diagnosis. A cow can 
be considered uninfected if, after at least 3 
negative examinations, she has 2 normal 
estrus periods and subsequently conceives 
and bears a normal calf; she should be bred 
by artificial insemination to avoid infecting 
the bull. A bull can be considered negative 
if, after at least 6 negative examinations at 
weekly intervals, he is bred to 2 or more 
virgin heifers and they remain negative. 

Cultivation : T. foetus can be readily 
cultivated in a number of media. Among 
them are CPLM (cysteine-peptone-liver ex- 
tract-maltose-serum) medium (Johnson and 
Trussell, 1943), BGPS (beef extract-glu- 
cose-peptone-serum) medium (Fitzgerald, 
Hammond and Shupe, 1954) and Diamond's 
(1957) trypticase -yeast extract-maltose- 
cysteine-serum medium. 

T. foetus was first cultivated in tissue 
culture by Hogue (1938). It was cultivated 
in the chorio-allantoic sac of chicken em- 
bryos by Nelson (1938) and independently 
by Levine, Brandly and Graham (1939) and 
Hogue (1939). 

Treatment: Since trichomonosis is 
ordinarily self-limiting in females, treat- 
ment is unnecessary. No satisfactory 
treatment is known for these infections. 

Many investigators have reported on 
treatment of T. foetus infections in bulls, 



THE TRICHOMONADS 



89 



including Bartlett (1948), Bartlett, Moist 
and Spurrell (1953), Mahoney, Christen- 
sen and Steere (1954), Thorne, Shupe and 
Miner (1955), Gabel et al. (1956) and 
Brodie (1960). Treatment is expensive, 
tedious and time-consuming; unless a bull 
is exceptionally valuable, it is best to sell 
it. Bartlett (1948) found that the German 
proprietary preparation, Bovoflavin-Salbe, 
cured 7 out of 8 infected bulls, and later 
workers have confirmed its effectiveness. 
This salve, which contains trypaflavine 
and surfen in an ointment base, is rubbed 
into the penis and prepuce following pu- 
dendal nerve block or relaxation of the re- 
tractor penis muscles with a tranquilizer. 
Brodie (1960) injected 200 to 1000 mg 
promazine hydrochloride intravenously 
for the latter purpose, and found that its 
ease of administration and quieting effect 
made it preferable to nerve block. 

Massage is continued for 15 to 20 
minutes, using 120 ml of the ointment. 
In addition, 30 ml of 1% acriflavine solu- 
tion is injected into the urethra. Repeated 
treatment may be necessary. If the epid- 
idymis or testis are affected, this treat- 
ment will be ineffective. 

For reasons which have not been de- 
termined, American bulls are much more 
refractory to treatment and much more 
difficult to infect experimentally than 
European bulls. Treatment with silver 
nitrate or by injecting 10 1 of 3% hydrogen 
peroxide into the preputial cavity under 
pressure with the apparatus described by 
Hess (1949), which is successful in Ger- 
many and Switzerland (Jondet and Guilhon, 
1957), has been found unsatisfactory in 
the United States. 

Control : Control of bovine tricho- 
monosis depends on proper herd manage- 
ment. Most infected bulls should be 
slaughtered. Infected cows should be 
given breeding rest, and should then be 
bred by artificial insemination to avoid 
infecting clean bulls. 

Proper management of bulls used for 
artificial insemination is especially im- 
portant, since they may spread the infec- 
tion widely. They should be examined for 



T. foetus before purchase, and the herds 
from which they originated should be stud- 
ied at the same time. In addition, they 
should be examined repeatedly while in use 
(Bartlett, Moist and Spurrell, 1953). 
Freezing the semen in the presence of glyc- 
erol cannot be expected to kill the trich- 
omonads. 



TRITRICHOMONAS SUIS 
(GRUBY AND DELAFOND, 1843) 

Synonym: Trichomonas suis Gruby 
and Delafond, 1843. 

Common Name : Large pig tricho- 
monad, pig nasal trichomonad. 

Disease : None . 

Hosts : Pig. 

Location : Nasal passages, stomach, 
cecum, colon, occasionally small intestine. 

Geographic Distribution : Worldwide. 

Prevalence : Switzer (1951) found 
this species in the nasal passages of 80% 
of swine affected with atrophic rhinitis and 
in only 3% of nonrhinitic pigs in Iowa. 
Shuman et al. (1953) found it in 27% of 36 
pigs with atrophic rhinitis and in 17% of 32 
unaffected pigs in a herd near Washington, 
D. C. Levine, Marquardt and Beamer 
(1954) found it in 91% of 11 pigs with atro- 
phic rhinitis and in 39% of 23 pigs with 
normal nasal passages in Illinois. Ham- 
mond, Fitzgerald and Johnson (1957) found 
it in the nasal passages of 56% of 64 pigs 
from Utah, Nebraska and Idaho. Hibler 
et al. (1960) found it in the nasal passages 
of 55% of 100 pigs, the stomach of 8% of 
512, the cecum of 43% of 496 and the small 
intestine of 3% of 100 pigs in Utah. 

Morphology : This species was des- 
cribed in detail by Hibler et al. (1960), 
Marquardt (1954) and Buttrey (1956); the 
latter described it under the name Tri- 
tricfiomonas sp. from the nasal passages. 
T. suis is characteristically elongate or 
spindle-shaped, occasionally piriform or 
rotund, 9 to 16 by 2 to 6ju,, with a mean of 



90 



THE TRICHOMONADS 




Fig. 8. Trichomonads of swine. A. Trtlrichoiiionas siiis. X 7700. B. Trilriclioiii- 
onas rotunda. X 5100. C. Trichomonas buUrexi. X 5700. (From Hibler 
et ai., 1960) 



11.3 by 3.4^1. Buttrey described a cyto- 
stome, but Hibler et al. did not see one. 
The 3 anterior flagella are about equal in 
length, 7 to 17 /i long with a mean of about 
12.6^L, and end in a round to spatulate 
knob. The blepharoplast is composed of 
several granules. The undulating mem- 
brane runs the full length of the body and 
has 4 to 6 subequal folds. Its marginal 



filament continues as a posterior free fla- 
gellum 5 to 11 ji long. An accessory 
filament is present. The costa runs the 
full length of the body, and fine subcostal 
granules are present. The axostyle is a 
hyaline rod 0. 6 jj. in diameter with a bulb- 
ous capitulum 1. 7 p. in diameter. It ex- 
tends 0. 6 to 1. 7fi beyond the body as a 
cone-shaped projection narrowing abruptly 



THE TRICHOMONADS 



91 



to a short tip. There is a chromatic ring 
around its point of exit. The parabasal 
body is usually a single, slender, tube- 
like structure 2 to 5jn long. The nucleus 
is oval or elongated, 2 to 5 by 1 to 3 /li , 
with a large, conspicuous endosome sur- 
rounded by a relatively clear halo. 

Pathogenesis : The discovery of this 
trichomonad by Switzer (1951) in a high 
percentage of cases of atrophic rhinitis 
and in a relatively low percentage of nor- 
mal pigs raised the question whether it 
was the cause of the condition. Spindler, 
Shorb and Hill (1953) produced the disease 
in young pigs with nasal washings contain- 
ing trichomonads from pigs with atrophic 
rhinitis, but Switzer (1951), Levine, 
Marquardt and Beamer (1954) and Fitz- 
gerald, Hammond and Shupe (1954a), 
among others, were unable to do so with 
axenic cultures of the protozoon. It is 
now generally agreed that this trichomonad 
is not pathogenic. Several other agents, 
including Pasteiirella tnultocida and Myco- 
plasDia hyorhinis, have been incriminated 
as causes of atrophic rhinitis, but their 
roles require further elucidation (see 
Switzer, 1955 for review). 

While T. suis is not pathogenic for 
pigs in its natural locations, it may cause 
abortion in heifers with experimental in- 
fections of the reproductive tract (see 
below). 

Cultivation : This trichomonad can 
be readily cultivated in any of the media 
used for T. foetus. In mixed cultures 
with other species of porcine trichomon- 
ads, it survives while the others die out, 
so that it sometimes seems as tho one 
species has taken on the appearance of 
another (Hibler et al. , 1960). Because of 
this fact, cultures of pig cecal trichomonad 
heretofore used in cross-transmission 
studies have most probably been this spe- 
cies. 

Switzer (1959) cultivated T. suis from 
the nasal passages in pig kidney, nasal 
mucosa and lung tissue cultures. 

Remarks : Uncertainty has existed 
for many years regarding which of the 



trichomonads known to occur in swine was 
T. suis. This specific name was origi- 
nally given by Gruby and Delafond (1843) 
to a form found in the stomach. Since 
that time, trichomonads have been found in 
the cecum and nasal passages, but it was 
not certain what their relationship was to 
the form which Gruby and Delafond had 
named. However, Hibler et al. (1960) 
found that the species described above is 
the only one which occurs in the stomach 
and that it also occurs in the nasal pas- 
sages, cecum and small intestine. They 
found the other 2 trichomonad species of 
swine only in the cecum. 

The relationship between T. suis and 
T. foetus requires further study. Buttrey 
(1956) and Hibler et al. (1960) pointed out 
their great morphological similarity. 
Doran (1957, 1959) concluded on the basis 
of metabolic studies that T. suis is a 
highly adapted strain of T. foetus. The 
other way around would be more likely in 
terms of evolution, i.e., T. foetus may 
well have arisen from T. suis or may be 
an adapted strain of it. 

Fitzgerald et al. (1958) produced 
vaginal infections in 3 heifers with T. suis 
from the pig nose; the infections lasted 46 
to 133 days. They also produced vaginal 
infections in 2 heifers with T. suis from 
the pig cecum which lasted 33 and 84 days, 
respectively, and in another heifer with 
T. suis from the pig stomach which lasted 
88 days. They produced abortion in a 4- 
month-pregnant heifer by intrauterine 
inoculation of T. suis from the pig cecum. 
In addition, a bull became infected by 
breeding an infected heifer. He remained 
positive for 4 months and transmitted the 
infection to a virgin heifer by coitus. 
Hammond and Leidl (1957a) infected the 
preputial cavity of bulls with T. suis from 
the pig cecum and found that the infections 
were transmissible by coitus. Kerr (1958) 
produced vaginal infections in heifers with 
Hammond's strains and also with a strain 
of T. suis which he isolated from pigs in 
England. 

Hammond and Leidl (1957) produced 
vaginal infections with T. suis from the 
pig cecum in 4 of 5 sows; the infections 



92 



THE TRICHOMONADS 



lasted 3 to 42 days. Fitzgerald el al. 
(1958) produced nasal and cecal infections 
in young pigs with cultures of T. suis from 
the pig nose, and they produced nasal, gas- 
tric and cecal infections with T. sicis from 
the pig stomach and from the pig cecum. 

Shaw and Buttrey (1958) were able to 
infect young chickens with T. siiis from 
the pig nose by rectal inoculation but not 
by mouth. 

Kerr (1958) found that the vaginal 
mucus agglutination test of heifers infected 
with T. suis was positive with T. suis and 
Belfast strain T. foetus antigens but not 
with Manley strain T.fuelus antigen. 
Sanborn (1955) found by microagglutination 
tests that a strain of T. suis from the pig 
nose was antigenically different from a 
strain of T. foetus and that both differed 
from a pig cecal trichomonad. 

As mentioned above under the discus- 
sion of T. foetus, Robertson (1960) found 
that the Belfast and Manley strains of T. 
foetus and Strains S2 and 414 of T. suis 
were serologically related and concluded 
that the differences between them did not 
justify separating them into 2 species. 

Cattle and swine are often raised to- 
gether, and the broad host ranges and mor- 
phologic, metabolic and serologic similar- 
ity between T. suis and T. foetus suggest 
that they may have had a common origin if 
they are not indeed the same. Robertson 
(1960) believed that they are the same and 
called them all T. foetus, but the correct 
name, as Hibler et al. (1960) pointed out, 
would be T. suis. Even so, however, it 
might still be worth-while to retain both 
names, simply as a matter of convenience. 



TRITRICHOMONAS ROTUNDA 
HIBLER, HAMMOND, CASKEY, 
JOHNSON AND FITZGERALD, 1960 

Synonym : Tritrichomonas suis pro 
parte. 

Common Name : Medium -sized pig 
cecal trichomonad. 



Disease : None. 

Hosts: Pig. 

Location : Cecum, colon. 

Geographic Distribution : This spe- 
cies has been recognized so far only in 
North America, but presumably occurs 
thruout the world. 

Prevalence : Hibler et al. (1960) 
found T. rotunda in the ceca of 10. 5% of 
496 pigs in Utah. 

Morphology : This species was des- 
cribed in detail by Hibler et al. (1960) and 
by Buttrey (1956); the latter referred to it 
as "T. s«/s -like." T. rotunda is typically 
broadly piriform, and only occasionally 
ovoid or ellipsoidal. It measures 7 to 11 
by 5 to 7 (i with a mean of 9. by 5. 8 p. . 
Hibler et al. saw no cytostome. Cyto- 
plasmic inclusions were frequently pres- 
ent. The 3 anterior flagella are about 
equal in length, being 10 to 17/j. long with 
a mean of 14.9|j,, and terminate in a knob 
or spatulate structure. The blepharoplast 
appears to consist of a single granule. 
The undulating membrane is relatively 
low. It and the costa extend about 1/2 to 
2/3 of the length of the body according to 
Hibler et al. (the full length of the body, 
according to Buttrey), and its undulation 
pattern varies from smooth to tightly 
telescoped or coiled waves (with 3 to 5 in- 
distinct folds, according to Buttrey). The 
accessory filament impregnates heavily 
with silver. The posterior free flagellum 
is generally shorter than the body. The 
axostyle is a narrow, straight, non-hya- 
line rod with a crescent- or sickle-shaped 
capitulum. It extends a relatively long 
distance beyond the body (0. 6 to 6. 3 /i with 
a mean of 4. 3fi). There is no chromatic 
ring at its point of exit from the body. 
The nucleus is practically spherical, 2 to 
3 fi in diameter, with an endosome sur- 
rounded by a clear halo. The parabasal 
body measures 2. 3 to 3. 4 by 0. 4 to 1.3/1. 
It is composed of 2 rami which form a V; 
each ramus has a parabasal filament. 

Pathogenesis : Non- pathogenic. 



THE TRICHOMONADS 



93 



Cultivation : T. rotunda grows read- 
ily on primary culture in standard tricho- 
monad media, but dies out on subculture 
and can no longer be found after the 4th or 
5th subculture. However, it can be main- 
tained indefinitely in a cecal extract- 
serum medium provided that Pseudonionas 
aeruginosa is present (Hibler et al. , 1960). 



TRITRICHOMONAS ENTERIS 
(CHRISTL, 1954) nov. comb. 

Synonym : Trichomonas enteris 
Christl, 1954. 

Hosts : Ox, zebu. 

Location : Cecum, colon. 

Geographic Distribution : Germany, 
India, probably worldwide. 

Prevalence : Common in Bavaria, 
according to Christl (1954). 

Morphology : The body is 6 to 12jLi 
long and 5 to 6fi wide. Three anterior 
flagella of equal length arise from a single 
blepharoplast. The flagellum at the edge 
of the undulating membrane is single, 
without an accessory filament. The un- 
dulating membrane extends 3/4 of the body 
length, and a free flagellum extends be- 




Fig. 9. 



Tritrichomonas enteris. X 1950. 
(From Christl, 1954 in Zeitschrift 
fiiy ParasitenkiDide, published by 
Springer- Verlag). 



yond the undulating membrane. The axo- 
style is straight, slender, bent like a 
spoon around nucleus, and extends at the 
most 1/4 of the body length beyond the 
body. Subcostal granules are present. 



TRITRICHOMONAS SP. 

Host: Ox. 

Location : Feces. 

Geographic Distribution : North 
America (Maryland). 

Morphology : Diamond (1957) culti- 
vated this form from calf feces. He did 
not describe it except to say that it resem- 
bled T. batrachorum. 



TRITRICHOMONAS EQUI 
(FANTHAM, 1921) 

Synonyms : Trichomonas equi. 

Host: Horse. 

Location : Cecum, colon. 

Geographic Distribution : Presum- 
ably worldwide, altho it has been reported 
specifically only from South Africa and 
the U.S. (Iowa). 

Prevalence : Fantham (1921) found 
T. equi very rarely and in very small num- 
bers in horses in South Africa. Hsiung 
(1930) found it on several occasions in 
Iowa. 

Morphology : According to Hsiung 
(1930), T. equi measures about 11 by 6fx 
and seems to possess 3 anterior flagella 
and an undulating membrane. The axo- 
style is slender. 



TRITRICHOMONAS FECALIS 
CLEVELAND, 1928 

This species was isolated once from 
human feces by Cleveland (1928). It has 
3 very long flagella, a heavy undulating 



94 



THE TRICHOMONADS 



membrane, a long, coarse axostyle and a 
costa with 2 rows of granules. Like T. 
hiitlreyi and the form cultured from a calf 
by Diamond (1957), it resembles T. balra- 
churiDn. The relationship between the 
small trichomonads of mammals requires 
study. 



TRITRICHOMONAS EBER THI 
(MARTIN AND ROBERTSON, 1911) 
KOFOID, 1920 

Synonyms : Trichomonas eberthi. 

Hosts : Chicken, turkey. Kotlan 
(1923) reported T. eberthi from the duck. 

Location : Ceca. 

Geographic Distribution : Worldwide. 

Prevalence : Common. McDowell 
(1953) found T. eberthi in 35% of a large 
number of chickens in Pennsylvania. 

Morphology : The body is carrot- 
shaped, 8 to 14 by 4 to 7|ii , with vacuo- 




Fig. 



10. Tritrichoinonas eberllu. X 4700. 
(From Martin and Robertson, 1911) 



lated cytoplasm, and 3 anterior flagella. 
The undulating membrane is prominent, 
extending the full length of the body. The 
posterior flagellum extends about half of 
the body length beyond the undulating mem- 
brane. An accessory filament is present. 
The cytostome is difficult to demonstrate. 
The blepharoplast is composed of 4 equi- 
distant granules, but tends to stain as a 
single body. Five to 12 or more subcostal 
granules are present. The axostyle is 
massive, hyaline, with its anterior end 
broadened to form a capitulum which con- 
tains siderophilic, argentophilic granules. 
Other endoaxostylar granules are also 
present. A ring of chromatic granules 
surrounds the axostyle at its point of emer- 
gence from the body. The parabasal body 
is shaped like a flattened rod, sometimes 
lumpy, of variable length. There are 5 
chromosomes. 

Pathogenesis : Non- pathogenic. 

Cultivation : Diamond (1957) culti- 
vated T. eberthi axenically for the first 
time in Diamond's medium. 



OTHER SPECIES OF TRITRICHOMONAS 

Tritrichomonas muris (Grassi, 1879) 
occurs in the cecum, colon and sometimes 
small intestine of the Norway rat, black 
rat, house mouse, golden hamster and a 
large number of wild rodents. It measures 
16 to 26 by 10 to 14^l. 

T. minuta (Wenrich, 1924) occurs in 
the cecum and colon of the Norway rat, 
house mouse and golden hamster. It meas- 
ures 4 to 9 by 2 to 5 jli . 

T. wenyoni (Wenrich, 1946) occurs in 
the cecum and colon of the Norway rat, 
house mouse, golden hamster, rhesus 
monkey and Chacma baboon. It measures 
4 to 16 by 2.5 to 6 fi. 

T. caviae (Davaine, 1875) occurs in 
the cecum and colon of the guinea pig. It 
measures 10 to 22 by 6 to 11 ji . 

Tritrichomonas sp. Nie, 1950 occurs 
in the cecum of the guinea pig. It meas- 
ures 6 to 13 by 4. 5 to 6. 5 |i. 



THE TRICHOMONADS 



95 



Tritrichomonas criceti (Wantland, 
1956 emend. ) nov. comb. (syn. , Tri- 
chomonas cricetus Wantland, 1956)occurs in 
the cecum and colon of the golden hamster. 
It measures 12 to 25 by 5 to 10 /i. 



Genus TRICHOMONAS Donne, 1837 

Members of this genus have 4 anter- 
ior flagella. 



TRICHOMONAS TEN AX 
(MULLER, 1773)DOBELL, 1939 

Synonyms : Cercaria tenax, Tetra- 
tyiclio)iioiias buccaUs, Trichomonas biic- 
calis, Trichomonas elongata. 

Disease : None. 

Hosts : Man, monkeys [Macaco 
nmlatta. Papio sphinx). 

Location : Mouth, especially between 
gums and teeth. 

Geographic Distribution : Worldwide. 

Prevalence : Common. T. tenax has 
been found in 4% to 53% of persons exam- 
ined in different surveys (Wenrich, 1947). 

Morphology : The morphology of T. 
tenax has been studied by Wenrich (1947) 
and Honigberg and Lee (1959). The latter 
remarked on the close morphological re- 
semblance of this species to T. gallinae. 
The body is ellipsoidal, ovoid or piriform, 
4 to 16 (i long and 2 to 15(a wide. Different 
strains differ in size; the smallest of 5 
strains studied by Honigberg and Lee (1959) 
averaged 6. by 4. 3 /i and the largest 8. 4 
X 6. 0|U . The 4 anterior flagella are 7 to 
15fx long. They originate in a basal gran- 
ule complex anterior to the nucleus and 
terminate in little knobs or rods. The un- 
dulating membrane is shorter than the body; 
it ranged from 40 to 100% and averaged 
from 69 to 82% of the body length in the 5 
strains studied by Honigberg and Lee (1959). 
An accessory filament is present. There 
is no free posterior flagellum. The costa 
is slender and accompanied by a group of 



large paracostal granules. The parabasal 
apparatus consists of a typically rod- 
shaped body and a long filament extending 
posteriorly from it. The axostyle is slen- 
der and extends a considerable distance 
beyond the body. There is no periaxostylar 
ring at its point of exit nor is it accompa- 
nied by paraxostylar granules. The capi- 
tulum of the axostyle is somewhat enlarged 
and spatulate. The pelta is of medium 
width. Wenrich (1947) said that a cyto- 
stome was present, but Honigberg and Lee 
(1959) found no evidence of one. Honigberg 
and Lee (1959) described the division proc- 
ess in detail. 

Pathogenesis : None. 

Cultivation : Honigberg and Lee (1959) 
cultivated T. tenax in Balamuth's yolk in- 
fusion medium. Diamond (1960) cultivated 
it axenically in a complex medium contain- 
ing chick embryo extract. 

Remarks : Hinshaw (1928) infected a 
dog which had gingivitis with T. tenax. 



TRICHOMONAS EQUIBUCCALIS 
SIMITCH, 1939 



Disease : None . 

Hosts : Horse, donkey. 

Location : Mouth, around gums and 
teeth^ 

Geographic Distribution : This species 
has apparently been reported only from 
Jugoslavia. 

Prevalence : Simitch (1939) found T. 
eqidbuccalis by culture in 7 out of 22 
horses and 2 out of 4 donkeys in Jugoslavia. 

Morphology : The body is piriform or 
ovoid, 7 to 10 /i long. It has a single ble- 
pharoplast and 4 anterior flagella 10 to 
15;i long. The undulating membrane is 
relatively short, rarely reaching the pos- 
terior end. There is no free posterior 
flagellum. The costa is slender and not 
always visible. The axostyle is apparently 
slender and extends beyond the body. 



96 



THE TRICHOMONADS 



Pathogenesis : Non- pathogenic. 

Remarks : Simitch (1939) transmitted 
T. eqiiibiiccalis readily from the horse to 
the donkey and vice versa, but was unable 
to infect cattle, sheep and goats with it. 



length of the body. The free posterior fla- 
gellum is about half as long as the body. 
The costa is apparently slender. The axo- 
style is thread-like, staining black with 
hematoxylin, and extends a considerable 
distance beyond the body. Subcostal gran- 
ules are absent. 



TRICHOMONAS FELISTOMAE 
HEGNER AND RATCLIFFE, 1927 

Hosts : Cat. 

Location : Mouth. 

Geographic Distribution : United 
States. 

Prevalence : Hegner and Ratcliffe 
(1927) found this species in 2 out of 28 
cats examined in Baltimore, Md. 

Morphology : The body is piriform, 
6 to 1 1 by 3 to 4 (I with a mean of 8 by 3 ji , 
and has 4 anterior flagella longer than 
body. The costa is illustrated as promi- 
nent. The undulating membrane extends 
most of the body length. There is a free 
posterior flagellum. The axostyle extends 
a considerable distance beyond the body. 

Pathogenesis: Non-pathogenic. 



TRICHOMONAS CANISTOMAE 
HEGNER AND RATCLIFFE, 1927 



Pathogenesis : Non- pathogenic. 

Remarks : An old dog with advanced 
gingivitis was infected with T. leiiax by 
Hinshaw (1928); the infection was still 
present 14^ months later. Simitch and 
Kostitch (1938) were unable to infect hu- 
mans with T. caiiistoDiae or to infect dogs 
with T. tenax. The morphological differ- 
ence described between the two species 
indicates that they are different. T. can- 
istomae and T. felistomae, however, may 
well be the same; further study is needed 
to determine this. 



TRICHOMONAS VAGINALIS 
DONNE, 1836 

Hosts: Man. 

The golden hamster can be infected 
intravaginally (Uhlenhuth and Schoenherr, 
1955). Mice can be infected subcutaneously 
(Honigberg, 1959). 

Location : Vagina, prostate gland, 
urethra. 



Hosts : Dog. 

Location : Mouth. 

Geographic Distribution : 
States, Europe. 



United 



Prevalence : Hegner and Ratcliffe 
(1927a), found this species in 22 out of 23 
dogs examined in Baltimore, Md. 

Morphology : The following descrip- 
tion is based on Hegner and Ratcliffe 
(1927a). The body is piriform, 7 to 12|j, 
long and 3 to 4/i wide. Four anterior 
flagella about as long as the body arise in 
pairs from a large blepharoplast. The 
undulating membrane extends almost the 



Geographic Distribution : Worldwide. 

Prevalence : T. vaginalis has been 
reported in 2% to as high as 80 to 90% of 
women and in 1 to 47% of men in various 
surveys (Wenrich, 1947; Kucera, 1957; 
Burch, Rees and Reardon, 1959). 

Morphology : The body is piriform, 
7 to 23 by 5 to 12 ;i, and has 4 anterior 
flagella about as long as the body. The un- 
dulating membrane has 3 or 4 waves and 
extends a little more than half the body 
length. There is no free posterior flagel- 
lum. An accessory filament is present. 
The costa is very narrow. The parabasal 
body is long, cylindrical, and has a para- 
basal filament extending posteriorly from 



THE TRICHOMONADS 



97 




Fig. 11. Trichonionads of man. 1. Trichomonas 
vaginalis. 2. Trichomonas lenax. 
3. Pentatrichomonas hominis. X 2500. 
(From Wenrich, 1947) 

it. Paracostal and extra- axostylar gran- 
ules are numerous; other siderophil gran- 
ules are scattered in the cytoplasm. Four 
chromosomes are present. The axostyle 
is rather slender. The cytostome is in- 
conspicuous. 

Pathogenesis : T. vaginalis infec- 
tions are often asymptomatic in womena 
and are usually so in the male. Tricho- 
monad vaginitis is characterized by leu- 
korrhea and vaginal and vulvar pruritis. 
T. vaginalis may occasionally cause pur- 
ulent urethritis and prostato-vesiculitis 
in the male. Concomitant bacteria and 
yeasts may exacerbate the symptoms and 
lesions. 

Epidemiology : T. vaginalis infec- 
tions are essentially venereal in origin, 
the organism being transmitted during 
sexual intercourse. In exceptional cases, 
infants have been infected from their 
mothers. Transmission thru contamina- 
ted towels, underwear or toilet seats is 
extremely rare. 

Diagnosis : T. vaginalis infections 
can be readily identified by microscopic 



examination of vaginal secretions or scrap- 
ings, sedimented urine or prostate secre- 
tions obtained by massaging the prostate 
gland. 

Cultivation : T. vaginalis can be 
readily cultivated in any of the media used 
for trichonionads, such as CPLM medium. 

Treatment : A number of preparations 
are used in treating trichomonad vaginitis. 
Among them are suppositories containing 
chiniofon, diodoquin, vioform, carbarsone 
or oxytetracycline. Lactic acid douches 
are often used to make the vaginal pH acid 
and provide conditions unsuitable for the 
protozoa. Infections in the male may be 
treated by introducing oxytetracycline 
ointment into the urethra or irrigating 
with a sulfonamide or antibiotic. To pre- 
vent reinfection, both husband and wife 
should be treated. 

Remarks : Trussell (1947) has writ- 
ten a definitive monograph on this species. 



TRICHOMONAS PAVLOVI 
NOM. NOV. 

Synonym : Trichomonas bovis Pavlov 
and Dimitrov, 1957, non Trichomonas 
bovis Riedmiiller, 1930. 

Host : Ox. 

Location : Large intestine. 

Geographic Distribution : Bulgaria. 

Morphology : This species was des- 
cribed by Pavlov and Dimitrov (1957). The 
trophozoites are piriform and usually meas- 
ure 11 to 12 by 6 to 7 (jL . The 4 anterior 
flagella are about the same length as the 
body. The undulating membrane is well de- 
veloped, with 2 to 4 waves, and extends al- 
most to the posterior end of the body. A 
posterior free flagellum, an accessory fil- 
ament and a costa are present. The nucleus 
is round-oval or oval. The axostyle is rel- 
atively weak and slender, broadening to 
form a capitulum at the anterior end, and 
extending about 1/4 of its length from the 
posterior end of the body. There are many 
food vacuoles in the cytoplasm. 



98 



THE TRICHOMONADS 



PathoRenesis : Pavlov and Dimitrov 
(1957) found this species in the feces of 
calves 5 days to 4 months old, all of which 
had diarrhea. They thought that the pro- 
tozoa were the cause of the diarrhea, bas- 
ing their opinion on their inability to find 
another cause and on the fact that the 
trichomonads disappeared from the feces 
when the diarrhea ceased. Needless to 
say, this is not sufficient justification for 
their view. 

Remarks : Further study is necessary 
to be sure whether this species is valid. 
Pending such a study, it is considered best 
to retain it. 

Pavlov and Dimitrov (1957) named 
this species Trichomonas bovis. This 
name is a homonym of Tyichomonas bovis 
Riedmiiller, 1930, which is in turn a syn- 
onym of TritrichoHiuiias foetus (Ried- 
miiller, 1928). Hence I am renaming it 
Trichomonas pavlovi nom. nov. 



r. bultreyi is ovoid or ellipsoidal, 4 
to 7 by 2 to 5 (i with a mean of about 5. 9 
by 3.4p.. Cytoplasmic inclusions are 
frequently present, but Hibler et al. saw 
no cytostome. There are 4 or 3 anterior 
flagella which vary in length from a short 
stub to more than twice the length of the 
body and end in a knob or spatulate struc- 
ture. The undulating membrane runs the 
full length of the body and has 3 to 5 un- 
dulations. The accessory filament is 
prominent and the costa relatively deli- 
cate. A posterior free flagellum is pres- 
ent. The axostyle is relatively narrow, 
with a spatulate capitulum, and protrudes 
3 to 6|i beyond the body. There is no 
chromatic ring at its point of exit. A 
pelta is present anteriorly. The nucleus 
is frequently ovoid but varies consider- 
ably in shape; it measures 2 to 3 by 1 to 
2 /J, and has a small endosome. The para- 
basal body is a disc 0. 3 to 1. 1 /i in diam- 
eter. 

Pathogenesis: Non- pathogenic. 



TRICHOMONAS BUTTREYI 
fflBLER, HAMMOND, CASKEY, 
JOHNSON AND FITZGERALD, 1960 

Common Name : Small pig cecal 
trichomonad. 

Disease: None. 

Host : Pig. 

Location : Cecum, colon, rarely 
small intestine. 

Geographic Distribution : This spe- 
cies has been recognized so far only in 
North America, but presumably occurs 
thruout the world. 

Prevalence : Hibler et al. (1960) 
found T. biittreyi in the ceca of 25. 4% of 
496 pigs and in the small intestine of 1% 
of 100 pigs in Utah. 

Morphology : This species was des- 
cribed in detail by Hibler et al. (1960) and 
by Buttrey (1956); the latter referred to it 
as a Paralricho>nonas-like form resem- 
bling P. (or Trichomonas) batrachorum. 



Cultivation : According to Hibler 
et al. , T. biittreyi grows readily on pri- 
mary culture in standard trichomonad 
media, but dies out on subculture; they 
maintained it indefinitely in a cecal ex- 
tract-serum medium provided Pseiido- 
monas aeruginosa was present. Diamond 
(1957) however, established it in axenic 
culture. 

Remarks : Doran (1958) studied the 
metabolism of this species, using Strain 
PC-287. It could not oxidize Krebs cycle 
intermediates, but produced carbon diox- 
ide and other gas not absorbed by KOH 
anaerobically. It resembled T. siiis 
more than other trichomonads, but dif- 
fered in carbohydrate utilization and in 
having a generally lower respiratory 
rate. 



TRICHOMONAS GALLINAE 
(RIVOLTA, 1878) STABLER, 1938 

Synonyms : Cercomonas gallinae, 
Cercomonas hepaticiim. Trichomonas 
columbae, Trichomonas diversa, Tri- 
chomonas halli. 



THE TRICHOMONA DS 



99 



Disease : Avian trichomonosis, upper 
digestive tract trichomonosis. 

Hosts : The domestic pigeon is the 
primary host of T. gallinae. but it also 
occurs in a large number of other birds, 
including hawks and falcons which feed on 
pigeons. Its natural hosts besides the 
pigeon include the mourning dove {Zen- 
aidura macroura), Indian dove ( Turtiir 
siiratensis), wood pigeon [Columba pa- 
lumbiis), band-tailed pigeon (C. fasciata), 
ring dove {Streptopelia risoria), white- 
winged dove {Zenaida asiatica), turkey, 
chicken, Cooper's hawk {Accipiter cooperi), 
golden eagle {Aquila chrysaetos), duck 
hawk [Falco peregrinus anatiini), Java 
sparrow {Miinia oryzivora), zebra finch 
and orange-cheeked waxbill. 

A number of other birds have been 
experimentally infected. They include the 
bobwhite quail, canary, English sparrow 
(Levine, Boley and Hester, 1941), barn 
swallow, goldfinch and song sparrow 
(Stabler, 1953), and Tovi parakeet and 
Verraux's dove (Callender and Simmons, 
1937). Parenteral infections have also 
been produced experimentally in mammals 
--by Bos (1934) in mice and guinea pigs, 
by Wagner and Hees (1935), Wittfogel 
(1935), Miessner and Hansen (1936), 
Schnitzer, Kelly and Leiwant (1950) and 
Honigberg (1959) in mice, and by Rakoff 
(1934) in rats and kittens. 

Prevalence : T. gallinae is extremely 
common in domestic pigeons, in which it 
often causes serious losses. It is fairly 
common in the turkey; the U.S. Dept. of 
Agriculture (1954) estimated that it causes 
an annual loss of $47,000 in these birds. 
It is rare in chickens. It is common in 
mourning doves, and may cause serious 
losses among them (Stabler and Herman, 
1951). According to Stabler (1954), it was 
common in trained hawks during the hey- 
day of falconry; they became infected be- 
cause they were fed largely on pigeons. 
Stabler and Herman (1951) and Stabler 
(1954) give further information on incidence 
in domestic and wild birds. 

Morphology : The following description 
is based on Stabler (1941, 1954). The body 




Fig. 12. Trichomonas gallinae 
(From Stabler, 1947) 



X 3400. 



is roughly piriform, 6 to 19 by 2 to 9 |j,. 
Four anterior flagella 8 to ISfi long arise 
from the blepharoplast. The axostyle is 
narrow and protrudes a short distance 
from the body. There is no chromatic 
ring around its point of emergence. The 
parabasal body is sausage-shaped, about 
4|i long, with a parabasal filament. The 
costa runs 2/3 to 3/4 of the body length. 
The undulating membrane does not reach 
the posterior end of the body. An acces- 
sory filament is present. A free trailing 
flagelium is absent. A cytostome is 
present. There are 6 chromosomes. 

Pathogenesis : In the pigeon, tricho- 
monosis is essentially a disease of young 
birds; 80 to 90?o of the adults are infected 
but show no signs of disease. The sever- 
ity of the disease varies from a mild con- 
dition to a rapidly fatal one with death 4 to 
18 days after infection. This is due in 
part to differences in virulence of different 
strains of the trichomonad (Stabler, 1948). 
Severely affected birds lose weight, stand 
huddled with ruffled feathers, and may fall 
over when forced to move. A greenish 
fluid containing large numbers of tricho- 
monads may be found in the mouth. 

Lesions are found in the mouth, si- 
nuses, orbital region, pharynx, esophagus, 
crop and even the proventriculus. They do 
not involve the digestive tract beyond the 



:oo 



THE TRICHOMONADS 



proventriculus. They often occur in the 
liver and to a lesser extent in other organs, 
including the lungs, air sacs, heart, pan- 
creas, and more rarely the spleen, kid- 
neys, trachea, bone marrow, navel re- 
gion, etc. 

The early lesions in the mouth are 
small, yellowish, circumscribed areas in 
the mucosa. They increase in number and 
become progressively larger, finally de- 
veloping into very large, caseous masses 
which may invade the roof of the mouth and 
sinuses and may even extend thru the base 
of the skull to the brain. The early lesions 
in the pharynx, esophagus and crop are 
small, whitish to yellowish caseous nod- 
ules which also grow. They may remain 
circumscribed and separate, or they may 
form thick, caseous, necrotic masses 
which may occlude the lumen. The cir- 
cumscribed, disc-shaped lesions are 
often described as "yellow buttons". Those 
in the esophagus and crop may have central, 
spur-like projections. A large amount of 
fluid may accumulate in the crop. The le- 
sions in the liver, lungs and other organs 
are solid, yellowish, caseous nodules 
ranging up to a centimeter or more in di- 
ameter. 

In the turkey and chicken, the lesions 
occur mostly in the crop, esophagus and 
pharynx, and are relatively uncommon in 
the mouth and liver. The lesions in the 
mourning dove are similar to those in the 
pigeon. 

Immunology : As mentioned above, 
different strains of T. gallinae differ 
greatly in virulence (Stabler, 1948; Flor- 
ent, 1938; Gloor, 1943). Previous infec- 
tion bestows more or less immunity; adult 
pigeons which have survived infection as 
squabs are symptomless carriers. Infec- 
tion with a relatively harmless strain pro- 
duces immunity against virulent strains 
(Stabler, 1948a, 1951). According to 
Florent (1938), pigeons are particularly 
susceptible at the time of weaning and of 
the first molt. Stabler (1953) found that 
immunity did not increase with age of un- 
infected birds. Certain breeds or strains 
of birds may be more sensitive than others. 
Miessner and Hansen (1936) felt that roller 



and tumbler pigeons were such, and Levine 
and Brandly (1940) were able to infect 
chicks from one source readily while chicks 
from other sources were very resistant. 

Epidemiology : In pigeons and mourn- 
ing doves, trichomonosis is transmitted 
from the adults to the squabs in the pigeon 
milk which is produced in the crop. The 
squabs are infected within minutes after 
hatching. Hawks and other wild raptors 
become infected by eating infected birds. 
Turkeys and chickens are infected thru 
contaminated drinking water. Feral pig- 
eons and other columbid birds are the or- 
iginal source of infection. The trichom- 
onads pass into the water from the mouths 
of infected birds, and not from the drop- 
pings (Stabler, 1954). T. gallinae has no 
cysts and is very sensitive to drying, so 
direct contamination is necessary. 

Diagnosis : Upper digestive tract 
trichomonosis is readily diagnosed by ob- 
servation of the lesions together with dem- 
onstration of the protozoa. It must be 
differentiated from other conditions which 
may cause more or less similar lesions, 
including fowl pox, vitamin A deficiency 
and moniliosis (thrush). 

Cultivation : T. gallinae can be cul- 
tivated readily in any of the customary 
trichomonad media. Diamond (1954) com- 
pared 28 culture media for it and (1957) 
introduced a trypticase-yeast extract- 
maltose-cysteine-serum medium for it and 
other trichomonads. 

Treatment : A number of workers 
have recommended the use of copper sul- 
fate for 20 days or more in the drinking 
water to eliminate T. gallinae (see Stab- 
ler, 1954) but this is not particularly sat- 
isfactory. The optimal concentration for 
non-breeding pigeons is 1-1000 and that for 
breeding pigeons with squabs is 1-3000 
according to Jaquette (1948), but it tends 
to make the birds sick, and Jaquette felt 
that all the treated birds may have suffered 
liver damage. Turkeys will not drink 
1-2000 copper sulfate. 

The best treatment for T. gallinae is 
2-amino-5-nitrothiazole (enheptin). 



THE TRICHOMONADS 



101 



Stabler and Mellentin (1953) recommended 
7 daily doses of 28 mg/kg for homing pi- 
geons and 45 mg/kg for commercial birds. 
This treatment cures both acute cases and 
carriers. Stabler, Schmittner and Harman 
(1958) used 6. 3 g enheptin soluble per gal- 
lon of drinking water for 7 to 14 days in 
non-breeding pigeons. The birds consumed 
9 to 27 mg of the drug per day--operation 
of the peck order may have cut down water 
consumption by some birds--and 53 of 61 
infected birds were freed of their infec- 
tions. Zwart (1959) obtained promising 
results with 0. 125% enheptin in the drink- 
ing water of a Dutch aviary where the in- 
fection had been found in zebra finches 
and an orange-checked waxbill. 

Control : Control of trichomonosis 
in pigeons depends upon elimination of the 
infection from the adults by drug treat- 
ment. Prevention in turkeys and chickens 
is based upon preventing wild pigeons and 
doves from drinking from their watering 
places. 



TRICHOMONAS GALLINARUM 
MARTIN AND ROBERTSON, 1911 

Synonym : Trichomonas pullorum. 

Disease : None . 

Hosts : Chicken, turkey, guinea fowl, 
and possibly other gallinaceous birds such 
as the quail, pheasant and chukar par- 
tridge. Diamond (1957) found a T. gal- 
linarum -like form in the Canada goose 
{Branta canadensis). 

Location : Ceca, sometimes liver. 

Geographic Distribution : Worldwide. 

Prevalence : Common. McDowell 
(1953) found T. gallinarum in over 60%of 
a large number of chickens in Pennsyl- 
vania. 

Morphology : The body is piriform, 
7 to 15 by 3 to 9 jj, , with 4 anterior fla- 
gella and a posterior flagellum which runs 
along the undulating membrane and ex- 
tends beyond it. An accessory filament is 



present. The axostyle is long, pointed 
and slender, without a chromatic ring at 
its point of emergence. The cytostome is 
prominent. Supracostal granules but no 
subcostal or endoaxostylar granules are 
present. The pelta is elaborate, ending 
abruptly with a short ventral extension 
more or less free from the ventral edge 
of the axostyle, according to McDowell 
(1953); Marquardt (1954), however, did 
not find a pelta in his cultures of a strain 
from a turkey. The shape of the para- 
basal body is highly variable, but it is 
usually a ring of variously spaced gran- 
ules plus 1 or 2 fibrils or rami. The 
chromosome number is apparently 5. A 
rather uniform perinuclear cloud of ar- 
gentophilic granules is usually present 
(McDowell, 1953). 

The form originally described by 
Martin and Robertson (1911) had 4 anterior 
flagella. Allen (1940) described a trichom- 
onad from the ceca and liver of chickens 
and turkeys which she considered to be this 
species but which had 5 anterior flagella. 
Walker (1948), too, illustrated the trichom- 
onad he isolated from turkey livers with 5 
anterior flagella. Further study is needed 
to determine the relationship of this form 
to T. gallinarum. McDowell (1953) in- 
sisted on the fact that the usual number of 
anterior flagella is 4, rarely 3 and in even 
rarer cases 5. He studied 1000 slides from 
a large number of chickens. Marquardt 
(1954), too, found only 4 anterior flagella 
in a culture strain from a turkey. 

Pathogenesis : Allen (1936, 1941), 
Olsen and Allen (1942) and Walker (1948) 
isolated a trichomonad from turkey liver 
lesions resembling those of histomonosis 
and considered that the trichomonad had 
caused them. The disease they described 
resembled histomonosis, with cecal and 
liver lesions, pale yellow, cecal diarrhea, 
inappetance, loss of weight, and a mor- 
tality of to 44%. The cecal lesions were 
said to be the same as those of histomo- 
nosis, but the liver lesions were said to 
be smaller, to have irregular outlines and 
to be raised or level with the liver surface 
instead of depressed below it. Wichmann 
and Bankowski (1956) described a similar 
condition in chukar partridges. However, 



102 



THE TRICHOMONADS 



the mere presence of an organism in a 
lesion is no proof that it caused the lesion. 
There is no satisfactory proof that T. gal- 
liiutru))! by itself is capable of causing 
disease, and the weight of evidence is 
against it. Delappe (1957) infected chick- 
ens and turkeys experimentally with a 
strain of T. galliiianiDi isolated from 
liver lesions of a turkey with histomonosis, 
but was unable to produce either symptoms 
or lesions. The possibility has still not 
been completely eliminated, however, that 
a Penlalrichomonas may exist which is 
pathogenic (see below). 

Epidemiology: Birds become infected 
by ingestion of trichomonads in contamin- 
ated water or feed. McLoughlin (1957) 
found that one-week-old turkey poults were 
more susceptible than 9-week-old ones. 
He also found that T. gcilliiiarnni survived 
for 24 hours but not for 48 hours in cecal 
droppings at 37" C, and for 120 hours at 
6' C. 

Cultivation : T. gnlUnanuv is readily 
cultivated in the usual trichomonad media. 



TRICHOMONAS ANATIS 
(KOTLAN, 1923) 

Synonym : Tetratrichomonas anatis. 

Host : Domestic duck. 

Location : Posterior part of intes- 
tinal tract. 

Geographic Distribution : Europe 
(Hungary). 

Morphology : The body is broadly 
beet-shaped, 13 to 27 by 8 to 18 fx, with 4 
anterior flagella, an undulating membrane 
extending most of the length of the body, a 
free trailing flagellum, a costa and a 
fibrillar axostyle. 



TRICHOMONAS ANSERI 
HEG^fER, 1929 

Hosts : Domestic goose, baby chick 
(experimental). 



Morphology : The body is oval, 6 to 
9 by 3. 5 to 6. 5(i with a mean of 8 by 5jx . 
Four anterior flagella appear to arise in 
pairs from 2 blepharoplasts. The undulat- 
ing membrane extends almost the full 
length of the body. A free trailing flagel- 
lum and a costa are present. The axo- 
style is broad and hyaline, extending a 
considerable distance beyond the body. 
There is no chromatic ring at its point of 
emergence from the body. The nucleus is 
characteristic, completely filled with min- 
ute chromatin granules and also with a 
single large karyosome usually at one 
side. The cytostome is prominent. Many 
specimens have large bacteria in the en- 
doplasm. 

Location : Ceca. 

Geographic Distribution : United 
States (Maryland). 

Prevalence : Unknown. 

Remarks : Hegner (1929) found a very 
few of these trichomonads in cecal material 
from a goose. He inoculated 3-day-old 
chicks with the material /»(?r os and per 
rectimi and the above description is based 
on material from the chicks. 



OTHER SPECIES OF TRICHOMONAS 

Trichomonas macacovaginae Hegner 
and Ratcliffe, 1927 occurs in the vagina 
of the rhesus monkey. It measures 8 to 16 
by 3 to 6 ^ and has a free posterior flagel- 
lum, a feature which differentiates it from 
T. vaginalis. 

T. w^/cro// Wenrich and Saxe, 1950 
occurs in the cecum of the Norway rat, 
house mouse, goldfen hamster, vole {Mi- 
croliis peniisylL'a)iici<s) and other wild ro- 
dents. It is 4 to 9 ji long. Simitch, Petro- 
vitch and Lepech (1954) transmitted it from 
the white mouse to the laboratory rat, guin- 
ea pig, ground squirrel (Citellus citelliis), 
dog and cat, but were unable to infect the 
chicken and a human volunteer. Wenrich 
and Saxe (1950) transmitted if from the vole 
to the laboratory rat, hamster and guinea 
pig, but could not infect a human volunteer. 



THE TRICHOMONADS 



103 



Genus PENTATRICHOMONAS 
Mesnil, 1914 

Members of this genus have 5 anter- 
ior flagella. 

PENTATRICHOMONAS HOMINIS 
(DAVAINE, 1860) 

Synonyms : Cercomonas hominis, 
Monocercomonas hominis, Trichomonas 
intestinalis. Trichomonas confusa, Pen- 
tatrichomonas ardin delteili, Tricliom- 
onas felis, Trichomonas parva, Pentatri- 
chomonas canis auri. 

Disease : None . 

Hosts : Man, gibbon, chimpanzee, 
orang-utan, rhesus monkey, pigtailed 
monkey {Macaca nemestrina), brown 
capuchin (Cebus fatuellus), weeping 
capuchin (C. apella), white-throated 
capuchin (C. capucinus), black spider 
monkey {Ateles ater), white-crested titi 
monkey (Callicebus amictus), Guinea 
baboon {Papio papio), Humboldt's woolly 
monkey {Lagothrix lagotricha), vervet 
monkey {Cercopithecus pygerythrus), dog, 
cat, rat, mouse, golden hamster. The 
primates were listed by Flick (1954). 

Kessel (1928) infected kittens with 
trichomonads from man, the monkey and 
rat. Simitch (1932, 1932a, 1933) trans- 
mitted P. hominis from the rat to the cat, 
dog and man. Saxe (1954) transmitted it 
from the golden hamster to the laboratory 
rat and from the rat to the hamster. 
Simitch, Petrovitch and Lepech (1954) in- 
fected the white mouse, laboratory rat, 
guinea pig, ground squirrel (Citellus ci- 
telliis ), dog, cat and chicken with P. ho- 
minis from man. 

Location: Cecum, colon. 

Geographic Distribution : Worldwide. 

Prevalence : Common. 

Morphology : The following descrip- 
tion is based primarily on Wenrich (1947) 
and Kirby (1945). The body is usually 



piriform, 8 to 20 by 3 to 14 /i. Five an- 
terior flagella are ordinarily present, al- 
tho some organisms may have 4 and a few 
3. Flick (1954) found in a study of more 
than 13,000 individuals from 13 P. hominis 
strains from 13 hosts that 77% had 5 fla- 
gella, 17% had 4, 5% had 3, and 1% had 6 
or more anterior flagella. Four of the 
anterior flagella are grouped together and 
the fifth is separate and directed poster- 
iorly. A sixth flagellum runs along the 
undulating membrane and extends beyond 
it as a free trailing flagellum. The undu- 
lating membrane extends the full length 
of the body. An accessory filament, a 
costa and paracostal granules are present. 
The axostyle is hyaline, thick, with a 
sharply pointed tip but without a chromatic 
ring at its point of exit. The parabasal 
body is small and ellipsoidal. The bleph- 
aroplast is composed of 2 granules. The 
pelta is crescent-shaped, prolonged dor- 
sally in a filament which passes posteriorly 
in the cytoplasm dorsal to the nucleus. A 
cytostome is present. There are 5 or 6 
chromosomes. 

Pathogenesis : Non- pathogenic. 

Cultivation : P. hominis is readily 
cultivable in the usual trichomonad media. 



PENT A TRICHOMONAS 
SP. ALLEN, 1936 

Synonym : Pentatrichomonas gal- 
linarum auct. 

Hosts : Chicken, turkey, guinea fowl. 

Location: Ceca, liver. 

Geographic Distribution : Probably 
worldwide. 

Prevalence : Unknown. 

Morphology : Pentatricliomonas sp. 
resembles T. gallinarum morphologically 
except that it has 5 anterior flagella. Four 
of these are of equal length and the fifth is 
about half as long as the others. The body 
is usually spherical, sometimes more or 
less pear-shaped, fixed specimens 



104 



THE TRICHOMONADS 



measuring 3 to 7 by 5 to 8 |i with a mean 
of 5 by 7 ji. The undulating membrane ex- 
tends the full length of the body, with a 
free flagellum at its end. A costa is pres- 
ent (Allen, 1940 called it a parabasal body). 
A row of paracostal granules runs between 
the costa and the undulating membrane. 
The axostyle is slender, projecting from 
the posterior end, but not discernible in 
rounded-up specimens. A cytostome is 
present. The blepharoplast is composed 
of a group of small granules. 

Pathogenesis : As mentioned in the 
discussion of Trichomonas galli)iaru))i , 
Allen and others isolated this form from 
turkey liver lesions resembling those of 
histomonosis and attributed the disease to 
it. However, post hoc reasoning is not 
enough, and there is as yet no acceptable 
proof that this trichomonad is pathogenic. 

Remarks : Allen (1936) first assigned 
this species to the genus Pentatrichomonas 
without naming it. She later (1940) des- 
cribed it as a five-flagellate "Trichom- 
onas galli>iarum Martin and Robertson, 
1911". Later authors such as Morgan and 
Hawkins (1952) called it Pentatrichomonas 
gallinaritm. The species described by 
Martin and Robertson has 4 anterior fla- 
gella, as does the form described by 
McDowell (1953). Further study is needed 
to determine the relationship between the 
two forms. 

Genus DfTR/CHOMONAS 
Cutler, 1919 

Similar to Trichomonas, but with 2 
anterior flagella. 



DITRICIiOMONAS OVIS 
ROBERTSON, 1932 

Host : Sheep. 

Location : "Gut. " 

Geographic Distribution : England. 

Prevalence : Robertson (1932) found 
this species in 1 out of 86 sheep in a Lon- 
don abattoir. 



Morphology : The protozoa were des- 
cribed from cultures. The body is slightly 
ovoid or nearly spherical, 3 to 14 by 3 to 
10 ji, with 2 anterior flagella, one 12 to 
16. 5/i and the other 7. 5 to 10. 5^ long. 
The undulating membrane is poorly devel- 
oped but extends the whole length of the 
body. A free flagellum was described as 
present, but was absent in 7 out of 9 draw- 
ings. A costa is present. The axostyle 
extends beyond the body. Three blepharo- 
plasts and another granule described as a 
parabasal body are present. 

Pathogenesis : Non- pathogenic. 

Cultivation : Robertson (1932) culti- 
vated D. ovis in Tanabe's medium with or 
without added rice starch. 

Remarks: Robertson's paper was 
apparently overlooked by Grasse, Reich- 
enow and others who discussed the validity 
of the genus Ditricho)nonas. Robertson 
insisted that there are only 2 anterior fla- 
gella except when the protozoa are divid- 
ing. No one else appears to have studied 
the intestinal trichomonads of sheep care- 
fully, altho they are more common in the 
United States than Robertson found them 
to be in England. Whether they are the 
same species remains to be determined. 



LITERATURE CITED 

Allen, EnaA. 1936. Trans. Am. Micr. Soc. 55:315-322. 
Allen, EnaA. 1940. Proc. Helm. Soc. Wash. 7:65-68. 
Allen, EnaA. 1941. Am. J. Vet. Res. 2:214-217. 
Anderson, E. 1955. J. Protozool. 2:114-124. 
Andrews, J. and C. Rees. 1936. J. Parasit. -22:108. 
Bartlett, D. E. 1947. Am. ]. Vet. Res. 8:343-352. 
Bartlett, D. E. 1948. Am. J. Vet. Res. 9:351-359. 
Bartlett, D. E. 1949. ]. Am. Vet. Med. Assoc. 114:293-305. 
Bartlett, D. E. and G. Dikmans. 1949. Am. J. Vet. Res. 

10:30-39. 
Bartlett, D. E. , K. Moist and F. A. Spurrell. 1953. J.Am. 

Vet. Med. Assoc. 122:366-370. 
Bos, A. 1934. Zbl. Bakt. I. Grig. 132:453-458. 
Brodie, B. O. 1960. J. Am. Vet. Med. Assoc. 136:501-504. 
Burch, T. A., C. W. Rees and L. V. Reardon. 1959. Am. 

J. Trop. Med. Hyg. 8:312-318. 
Buttrey, B. W. 1956. J. Protozool. 3:8-13. 
Callender, G. R. and J. S. Simmons. 1937. Am. J. Trop. 

Med. 17:579-585. 
Christl, H. 1954. Ztschr. Parasitenk. 16:363-372. 
Cleveland, L. R. 1928. Am. J. Hyg. 8:232-255. 
Delappe, I. P. 1957. Exp. Parasit. 6:412-417. 
Diamond, L. S. 1954. Exp. Parasit. 3:251-258. 



THE TRICHOMONADS 



105 



Diamond. L. S. 1957. J. Parasit. 43:488-490. 
Diamond, L. S. 1960. J. Parasit. 46(sup. ):43. 
Doran, D. J. 1957. J. Protozool. 4:182-190. 
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THE TRICHOMONADS 



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In this chapter is discussed a miscel- 
lany of flagellates, most of which are 
found in the digestive tract. Only a few 
are pathogenic, the great majority being 
commensal. Some are not parasitic at all 
but are coprophilic or have been found as 
contaminants in washings from the sheath 
of bulls; these are mentioned because they 
must be differentiated from parasitic 
forms. A few other species are free-liv- 
ing toxin-producers. 



TOXIC MARINE PHYTOFLAGELLATES 

The great majority of phytoflagellates 
are free-living and holophytic. Some of 
them produce powerful toxins which may 
kill fish or even man. 

Gonyaulax catanella is a marine dino- 
flagellate, found particularly off the coast 
of California, which causes a fatal dis- 
ease of man known as mussel poisoning. 
Its toxin is one of the most powerful known. 
Under conditions still largely unknown, the 
protozoa multiply tremendously, forming 
a luminescent "bloom" in the ocean. Mus- 
sels and certain other shellfish feeding on 
plankton are not harmed by the toxin but 
accumulate it in their internal organs. 
People who eat these mussels may then be 
killed by the toxin. 

The blooming of other dinoflagellates, 
including several species of Gymnodinium, 
cause the "red tide" or "red water" which 
sometimes kills huge numbers of fish, de- 
positing them in rotting windrows on the 
shore. This condition is particularly 
common off the coast of Florida, where it 
is associated with the discharge of phos- 
phates into the ocean, but it also occurs 
off the Texas coast and elsewhere (Hutner 
and McLaughlin, 1958). 

A third marine phytoflagellate, the 
chrysomonad Prymnesium parvmn, has 
killed fish en masse in brackish fish ponds 
in Israel, and has formed blooms accom- 
panying fish kills in Holland and Denmark 
(McLaughlin, 1958). 




,RY 






Chapter 6 



OTHER 
HAGBUATES 



- 107 



108 



OTHER FLAGELLATES 



A few phytoflagellates are coprophilic 
and may be mistaken for true parasites, 
and still fewer are parasitic. These will 
be discussed below. 



PARASITIC FLAGELLATES 

The parasitic mode of life has arisen 
independently a number of times in this 
group. Free-living species or genera in 
distantly related or unrelated families 
have found suitable living conditions in 
various hosts. Many of these were pre- 
viously inhabitants of stagnant water. 
The fact that so few of them are pathogenic 
effectively refutes the notion that para- 
sites tend to be pathogenic in their first 
association with a new host and that later 
on the host and parasite adjust to each 
other, the latter becoming less pathogenic 
and eventually commensal. 



FAMILY MONOCERCOMONADIDAE 

This family, like the Trichomonadidae, 
belongs to the order Trichomonadorida. 
Its members have either a free or adherent 
trailing flagellum, but lack the undulating 
membrane and costa found in the Trichom- 
onadidae. Four genera, Monocercomonas , 
Hexamastix, Protrichomonas and Cliilo- 
mitus, occur in the intestinal tracts of 
domestic animals. 



Genus MONOCERCOMONAS Grassi, 1879 

In this genus the body is piriform, 
with a rounded anterior end. There is a 
pelta. The cytostome and nucleus are 
anterior. There are 3 anterior flagella 
and a trailing one. The axostyle projects 
beyond the posterior end of the body. 
Travis (1932) showed that Trichomastix 
Blochmann, 1884 and Entrichomastix 
Kofoid and Swezy, 1915 are synonyms of 
Monocercomonas . Morgan (1944) gave a 
checklist of species of the genus; it in- 
cluded 20 species, of which 4 were from 
mammals, 4 from birds, 2 from reptiles, 
1 from amphibia, 2 from fish and 7 from 
insects and other arthropods. Others 
have been described since. 




Fig. 13. Monocercomonas. 
(Original) 



X 2800. 



Monocercomonas ruminantium 
(Braune, 1914) nov. comb, occurs in the 
rumen of cattle. In addition, Morgan and 
Noland (1943) found what was probably the 
same organism in material from the sheath 
of bulls. 

The body is about S/i long, with 3 an- 
terior flagella about 8)i long and a trailing 
flagellum a little longer. The axostyle is 
curved and does not extend beyond the 
body, altho the posterior end is pointed. 
A line of granules runs beside the convex 
side of the axostyle. This species is non- 
pathogenic, but must be distinguished from 
Tri trichomonas foetus. 

Synonyms of this species are Tri- 
chomonas noiiiiiaiitiiiiii Braune, 1914; 
Tricercomitus ni)>iiiiaiitiii»i (Braune, 1914) 
Christl, 1954; and Tritrichomonas rumin- 
antium (Braune, 1914); but not Tricho- 
))iastix ruminantium Braune, 1914. Altho 
Braune (1914) assigned this species to the 
genus Trichonioiias and succeeding work- 
ers have followed him in this or at the 
most have changed the generic name of 
Tritrichonionas. Christl (1954) pointed out 
that the absence of an undulating membrane 
made this assignment incorrect. Christl 
transferred it to the genus Tricercomitus, 
but it belongs more properly to the genus 
Monocercomonas . 



OTHER FLAGELLATES 



109 



Monocercomouas cuniculi (Tanabe, 
1926) occurs in the cecum of the domestic 
rabbit. It is piriform, 5 to 14 ji long. 
Its axostyle is slender, hyaline, and pro- 
jects from the body. 

Monocerco))io)ias gaUinaritm (Martin 
and Robertson, 1911) Morgan and Hawkins, 
1948 is said to occur in the ceca of the 
chicken. Kotlan (1923) reported it from a 
single domestic duck. Its body is piri- 
form, 5 to 8 by 3 to 4 fj, . There is some 
question whether this is a valid species. 
It has been reported by Martin and Robert- 
son (1911) in England, Kotlan (1923) in 
Hungary, and Morgan and Hawkins (1952) 
in Wisconsin, but McDowell (1953) failed 
to find it in 1000 slides from a large num- 
ber of chickens in Pennsylvania. McDowell 
believed, along with Minchin (1917), 
Wenyon (1926), Doflein and Reichenow 
(1929) and others, that it is simply a de- 
generate Trichomonas eberthi. 



Genus HEXAMASHX 
Alexeieff, 1912 

In this genus the body is piriform, 
with a rounded anterior end. The cyto- 
stome and nucleus are anterior. There 
are 6 flagella, of which 1 trails. (Ac- 
cording to Nie, 1950, the number of an- 
terior flagella varies in this genus from 
2 to 6. ) A pelta is present, the axostyle 
is conspicuous, and the parabasal body 
prominent. Members of this genus have 
been found in mammals, amphibia and 
insects. Hexamastix caviae Nie, 1950 
and H. robustus Nie, 1950 occur in the 
guinea pig cecum, and H. muris (Wen- 
rich, 1924) in the cecum of the Norway 
rat, golden hamster and other rodents. 



Genus CHILOMITUS 
Da Fonseca, 1915 

The body is elongate, with a convex 
aboral surface. The pellicle is well de- 
veloped. The cuplike cytostome is near 
the anterior end. Four flagella emerge 
thru it from a bilobed blepharoplast. The 
nucleus and parabasal body are just below 
the cytostome. An axostyle is present but 



may be rudimentary. Cysts may occur. 
Only a few species have been described, 
all in mammals. Cliilo»nlus caviae da 
Fonseca, 1915 and C. coiiexits Me, 1950 
occur in the guinea pig cecum. 



Genus PROTRICHOMONAS 
Alexeieff, 1912 

The body is piriform or beet- shaped, 
with 3 anterior flagella of equal length 
arising from an anterior blepharoplast, 
an anterior nucleus and an axostyle. Three 
species have been named, from birds, 
mammals and a fish. 

Protrichomonas niniinantiiiDi (Braune, 
1914) nov. comb, was originally assigned 
by Braune (1914) to the genus TrichoDias- 
tix (now Monocerconionas), but the absence 
of a trailing flagellum makes this assign- 
ment incorrect. Its description agrees 
with that of Protricho))wiias, altho it must 
be said that this genus is badly in need of 
redescription. P. ru)ninaiitium occurs in 
the rumen of cattle and sheep. It is about 
8/i long. Its nucleus is often surrounded 
by a clear zone. No cytostome was seen. 

Protrichomonas anatis Kotlan, 1923 
has been described from the large intes- 
tine of the domestic duck and other water 
birds. It is 10 to 13|Li long and 4 to 6ju 
wide. Two distinct fibrillae arise from 
the anterior blepharoplast and pass back 
thru the body, separating to pass around 
the nucleus and finally passing out of the 
body as a pointed axostyle. The nucleus 
is often triangular. 



ORDER POLYMASTIGORIDA 

Members of this group have 2 to about 
12 flagella and 1, 2 or several nuclei. 
They lack a costa, axostyle (except in some 
Hexamitidae and Polymastigidae) and para- 
basal body. 



FAMILY TETRAMITIDAE 

In this family there is a single nucleus 
and 4 flagella, 1 or 2 of which may be 



no 



OTHER FLAGELLATES 



trailing. Eiiferonionas is parasitic in 
domestic and laboratory animals, and 
Tetramitus is coprophilic. 



Genus TETRAMITUS Perty, 1852 

In this genus the life cycle involves 
flagellate and amoeboid forms; there are 
also uninucleate cysts. In the flagellate 
stage the body is ellipsoidal or piriform, 
with a large, trough-shaped cytostome at 
the anterior end, a vesicular nucleus with 
a large endosome, 4 anterior flagella, 
and a contractile vacuole. Nutrition is 
holozoic. 

Tetramitus rostratus Perty, 1852 
(syn. , Copromastix prowazeki Aragao, 
1916) is found in stagnant water and is 
also coprophilic. It has been found in 
human and rat feces. The flagellate stage 
is 14 to 18 /i long and 7 to IOjll wide. The 
amoeboid stage is 14 to 48 jm long and 
usually has a single lobose pseudopod. 
The cysts are spherical, thin-walled, and 
6 to 18 fi in diameter. The life cycle of 
this species has been studied by Bunting 
(1926), Bunting and Wenrich (1929) and 
Hollande (1942). 



Genus ENTEROMONAS 
Da Fonseca, 1915 

The body is spherical or piriform and 
is plastic. It has 3 short anterior flagella, 
1 of which may be difficult to see, and a 
4th, long flagellum which runs along the 
flattened body surface and extends free for 
a short distance at the posterior end of 
the body. A strand-like funis arises from 
the blepharoplast and extends posteriorly 
along the body surface; it stains faintly 
with iron hematoxylin and strongly with 
protargol. The nucleus is anterior, vesi- 
cular, with or without an endosome. There 
is no cytostome. The cysts are ovoid, and 
are tetranucleate when mature. A syno- 
nym of this genus is TricercoDionas Wen- 
yon and O'Connor, 1917. This genus has 
been reported from a number of mammals. 

E>itero»io)ias hu»iinis da Fonseca, 
1915 (synonyms, Octomitus hominis, 



Tricercomonaa intestinalis, Diplucerco- 
monas soudanensis, Enteromonas beiiga- 
lensis) occurs in the cecum of man, maca- 
ques (Macaca »iHlatta, M. sinica, M. 
nemestrina) the golden hamster and prob- 
ably other animals thruout the world. 
Wantland (1955) reported it in l%of 500 
golden hamsters in the United States. 
Saxe (1954) transmitted it from the golden 
hamster to the laboratory rat. Dobell 
(1935) was unable to infect himself with a 
culture of £. liominis from the macaque, 
M. sinica, but believed that future work 
would show that the human and macaque 
forms are the same species. Simitch 
et at. (1959) reported failure to transmit 
E. hominis to 2 young pigs. 

The trophozoite is oval, 4 to 10 by 3 
to 6|:x, and has many food vacuoles con- 
taining bacteria. The cysts are ovoid or 
ellipsoidal; they are usually binucleate 
but have 4 nuclei when mature. E. hominis 
is readily cultivated on the usual media 
for enteric protozoa such as LES medium; 
cysts form in the cultures. It is non-path- 
ogenic. 





Fig. 14. A. Enteromonas. B. Retorta- 
iiionas. X 2800. (Original) 



Enteromonas suis (Knowles and Das 
Gupta, 1929) Dobell, 1935 (syn. , Tricer- 
comonas suis) was described from the 
cecum of a pig in India. It was cultivated 
easily in Dobell and Laidlaw's medium. 
It is shaped like a broad, ovate leaf with 
a more or less rounded anterior end and 
a pointed posterior end, and is 9 to 20ju 
long and 6 to 14/i wide. It moves slug- 
gishly more or less directly forward and 
does not rotate like Trichomonas. The 
three anterior flagella are 8 to ISji long 



OTHER FLAGELLATES 



111 



With a mean of 14fi, and the posterior 
flagellum is 9 to 26|j, long with a mean of 
17jLt. Simitch et al. (1959) found it in 
2% of 1800 pigs in Yugoslavia. 



FAMILY RETORTAMONADIDAE 

Members of this family have 2 or 4 
flagella, of which 1 is trailing, a single 
nucleus and a cytostome with supporting 
fibrils. There are 2 genera of veterinary 
interest, Retortamonas and Chilomastix . 



Genus RET0RTAA10NAS 
Grassi, 1879 

The body is usually piriform or fusi- 
form, drawn out posteriorly, and plastic. 
There is a large cytostome near the an- 
terior end containing in its margin a 
cytostomal fibril which extends across 
the anterior end and posteriorly along 
each side. An anterior flagellum and a 
posteriorly directed, trailing flagellum 
emerge from the cytostomal groove. The 
cysts are piriform or ovoid, have 1 or 2 
nuclei, and retain the cytostomal fibril. 
A synonym of this genus is Embadonionas 
Mackinnon, 1911. Species occur in var- 
ious insects, amphibia, reptiles and mam- 
mals. (Ansari, 1955, 1956). 

Retortamonas intestinalis (Wenyon 
and O'Connor, 1917) Wenrich, 1932 (syns. , 
Embadomonas intestinalis, Waskia intes- 
tinalis) occurs in the cecum of man and 
probably also in the chimpanzee, macaques 
and other monkeys. Dobell (1935) was un- 
able to infect a Macaca mulatta and a M. 
sinica with cultures of R. intestinalis from 
man, but nevertheless believed it likely 
that the Retortamonas of man and maca- 
ques belong to the same species. It is not 
common in man, and is non- pathogenic. 

The trophozoites oi R. intestinalis 
are elongate piriform, 4 to 9|i.long and 3 
to 4/i wide. The cysts are uninucleate, 
piriform, 4. 5 to 7fj, long and 3 to 4. Sjj. 
wide and have a rather thick wall. This 
species can be cultivated in the usual cul- 
ture media for intestinal protozoa. 



Retortamonas ovis (Hegner and Schu- 
maker, 1928) (syn. , Einbadoi)iO)ias ovis) 
was described from trophozoites and cysts 
in cultures from sheep feces in Maryland. 
The trophozoites are piriform and average 
5.2 by 3.4^L. 

Retortamonas cuniculi (Collier and 
Boeck, 1926) (syn. , Embadomonas cuni- 
culi) occurs in the cecum of the rabbit. 
The trophozoites are generally ovoid but 
occasionally have a tail-like process; they 
measure 7 to 13 by 5 to 10 |U . The cysts 
are oval and measure 5 to 7 by 3 to 4 ji . 
Collier and Boeck (1926) found this species 
in 1 of 50 rabbits. It is apparently non- 
pathogenic. 



Genus CHILOMASTIX 
Alexeieff, 1912 

The body is piriform and plastic, with 
a large cytostomal groove near the anterior 
end containing in its margin a cytoplasmic 
fibril which extends across the anterior end 
and posteriorly along each side. The nu- 
cleus is anterior. There are 3 anteriorly 
directed flagella and a short fourth flagel- 
lum which undulates within the cytostomal 
cleft. Cysts are formed. Synonyms of this 
genus are Macrostoma Alexeieff, 1909 and 
Fanapepea Prowazek. Chilomastix is 
found in mammals, birds, reptiles, am- 
phibia, fish, insects and leeches. All spe- 
cies are apparently non- pathogenic. 

Chilomastix mesnili (Wenyon, 1910) 
Alexeieff, 1912 (syns. , Macrostoma 
mesnili, Chilomastix suis, Chilomastix 
hominis) is found in the cecum and colon of 
man, the orang-utan, chimpanzee, a num- 
ber of monkeys {Macaca, Cercopithecus, 
Cebus, Pithecus) and the pig. It is quite 
common in man, having been found in 1 to 
28% in various surveys; according to 
Belding (1952), it was found in 3. 4% of 
35, 577 persons in recent surveys in the 
United States, and in 6. 1% of 19, 006 per- 
sons elsewhere in the world. Frye and 
Meleney (1932) found it in 3 of 127 pigs in 
Tennessee. Kessel (1928) found it in pigs 
in California, and Reichenow (1952) in 
Hamburg, Germany. Simitch et al. (1959) 



112 



OTHER FLAGELLATES 



found it in 1. 1% of 1800 pigs in Yugosla- 
via. 

Kessel (1924) transmitted C. mesnili 
from man to monkeys, and Deschiens 
(1926) from the chimpanzee to Macaca 
siiiicci. However, Simitch el al. failed to 
transmit C. iiiesiiili from man to 2 young 
pigs and consequently named the pig form 
C. sitis. 





Fig. 15. Chiloniastix. A. Trophozoite. 
B. Cyst. X 2800 (Original) 



The trophozoites of C. mesnili are 
asymmetrically piriform, with a spiral 
groove running thru the middle half of the 
body. The posterior end is drawn out 
when the protozoa are moving. The 
trophozoites are 6 to 24ji long and 3 to 
10|i wide. The cytostomal cleft is about 
6 to 8|i long and 2\i wide. A complex of 
6 minute blepharoplasts lies anterior to 
the nucleus; from them come the 3 free 
anterior flagella (of which 2 are short and 
the third is relatively long), the cytostomal 
flagellum, and the 2 cytostomal fibrils. 
The cysts are lemon-shaped, 6. 5 to lOfi 
long, and contain a single nucleus and the 
organelles of the trophozoite. 

C. mesnili is ordinarily considered 
non- pathogenic. However, Mueller (1959) 
suggested that it might possibly be a mild 
pathogen occasionally. He referred to an 
outbreak of watery diarrhea in very young 
children in Czechoslovakia and to his own 



experience with watery diarrhea accom- 
panied by swarms of Cliiloinaslix following 
a visit to Mexico. This species can be 
cultivated in the usual media used for in- 
testinal protozoa. 

C. cuniciili da Fonseca, 1915 occurs 
in the cecum of the domestic rabbit. It is 
morphologically similar to C. mesnili. 
The trophozoite is ordinarily 10 to 15pL 
long, but may range from 3 to 20fi . 

C. ca/>rae da Fonseca, 1915 was re- 
ported from the rumen of the goat in Bra- 
zil. Das Gupta (1935) found it in India. It 
is morphologically very similar to C. mes- 
nili and is 8 to 10 ^L long and 4 to 6(1 wide. 

C. gallinarum Martin and Robertson, 
1911 occurs in the ceca of the chicken and 
turkey. McDowell (1953) found it in 40% 
of a large number of chickens in Pennsyl- 
vania. The body is pear- or carrot-shaped, 
11 to 20 by 5 to 12/1 . The nucleus is 
pressed against the anterior end of the 
body. The cytostomal pouch is 8-shaped, 
spirals toward the left on the ventral side, 
and extends 1/2 to 2/3 of the body length. 
Cysts are rare in cecal material but com- 
mon in culture. They are lemon-shaped, 
measure 7 to 9 by 4 to 6 jj. , and have a 
single nucleus. McDowell (1953) cultiva- 
ted C. gallinarum easily in Ringer's solu- 
tion with 0.2% gastric mucin at 39 to 40 C. 

C. intestinalis Kuezynski, 1914 and 
C. wenrichi Nie, 1948 occur in the cecum 
of the gunea pig, and C. bettencoiirti da 
Fonseca, 1915 in that of the laboratory 
rat, domestic mouse and golden hamster. 



FAMILY CALLIMASTIGIDAE 

Members of this family have a single 
nucleus and a compact antero-lateral group 
of flagella which beat as a unit. There are 
2 genera, Callimastix and Selenomonas. 



Genus CALLIMASTIX 
Weissenberg, 1912 

The body is ovoid, with a compact 
central or anterior nucleus. There are 



OTHER FLAGELLATES 



113 



12 to 15 long flagella near the anterior end 
which beat in unison. One species occurs 
in the body cavity of copepods and the 
others in ruminants and equids. They are 
non- pathogenic. 

CaUi)Jiastix frontalis Braune, 1913 
occurs in the rumen of cattle, sheep and 
goats thruout the world. Becker and Tal- 
bot (1927) reported it in Iowa. The body is 
spherical or ovoid, about 12 to 14 fi in di- 
ameter. The nucleus has a large central 
endosome. The 12 flagella are about 30 /i 
long; they arise from a row of basal gran- 
ules on the anterior margin of the body 
and join to form a single unit distally. 
This species has been found in material 
submitted for diagnosis of Tritrichomonas 
foetus infections (Morgan and Hawkins, 
1952). 

Callimastix eqiii Hsiung, 1929 occurs 
in the cecum and colon of the horse. The 
body is kidney- shaped with the hilus at its 
anterior third; it is 12 to 18 ^l long and 7 
to 10 fi wide with a mean of 14 by 8 /i . 
Just behind the hilus is a clear, granule- 
free area on the margin of which are 12 to 
15 basal granules which give rise to fla- 
gella 25 to 30 ^ long; these unite distally 
and function as a unit. The rest of the 
cytoplasm is filled with deeply staining 
granules. The nucleus \s Zii in diameter 
has a large endosome and lies near the 
center of the body. 



Genus SEUNOMONAS 
Von Prowazek, 1913 

The body is kidney- to crescent- 
shaped, with blunt ends. One or more 
flagella are attached to the middle of the 
concave side. The flagella are thicker at 
the base than at the free end and are 
usually 1 to 1. 5 times as long as the body. 
The nucleus is highly retractile and lies 
on the concave side near the base of the 
flagella. Reproduction is by transverse 
binary fission thru the flagellar region. 
This genus has been placed by many au- 
thors in the Spirillaceae among the bac- 
teria, but Jeynes (1955, 1956) showed 
that it is actually a protozoon. It is not 
pathogenic. 



Selenomonas ruminantium (Certes, 
1889) Wenyon, 1926 (syns., Ancyromonas 
ri())iiiiantiii»i. Seleiioniastix rioiiinantium) 
occurs in the rumen of cattle, sheep, 
goats and various wild ruminants including 
the gazelle, giraffe, antelope (CepJialoplins 
)uaxivelli) in Africa and the pronghorn an- 
telope (A)itilocapra ainericmia), deer 
(Odocoileus hemionus) and elk {Cervus 
iianiiodes) in the United States (California). 
It was also found in the blood of the African 
antelope by Kerandel (1909), of the prong- 
horn antelope by Chattin, Herman and 
Kirby (1944) and of the deer (O. lieii/ioiiKs) 
by Herman and Sayama (1951) in California. 
According to Lessel (1957), S. rii»iinan- 
tiiu)i is the predominant organism found on 
microscopic examination of the rumen 
juices. 

The body of S. ru})ii)iautii(>n is cres- 
cent-shaped, 9. 5 to 11 by 2 to 3 li , with a 
tuft of flagella arising from the center of 
the concave side. The nucleus is in the 
center of the concave side. There are no 
cysts. This species has not been culti- 
vated. 




Fig. 16. Selenomonas ruminantium. 
X 2800. (Original) 



Selenomonas palpitans Simons, 1922 
occurs in the cecum and upper part of the 
colon of the guinea pig. 

S. spidigeua (Flugge, 1886) Dobell, 
1932 occurs in the mouth of man. It grows 
well in thioglycollate broth. 



FAMILY POLYMASTIGIDAE 

Members of this family have 4 anter- 
ior flagella, an axostyle and a single 



114 



OTHER FLAGELLATES 



nucleus. They apparently lack a para- 
basal body. The only genus found in do- 
mestic animals is Monocerconiunoides . 



Genus MONOCERCOMONOfDES 
Travis, 1932 

Members of this genus have 4 anterior 
flagella in 2 pairs, a pelta and an axostyle 
which is generally filamentous. Nie (1950) 
described 1 to 4 strand-like funises which 
stain with protargol in 4 species of this 
genus from the guinea pig. The funis is 
a costa-like structure extending backwards 
just beneath the body surface. Members 
of this genus occur in insects, amphibia, 
reptiles and a number of mammals. They 
are non-pathogenic. 

Monocercomonoides caprae (Das 
Gupta, 1935) (syn. , Monocercomonas 
caprae) was described from the rumen of 
the goat in India. The body is ovoid, 6 to 
12(1 long and 4 to 8 p. wide. 

Monocercomonoides caviae (Cunha 
and Muniz, 1921) Nie, 1950, M. qiiadri- 
funilis Nie, 1950, Al. ivenrichi Nie, 1950 
andM. exilis Nie, 1950 occur in the cecum 
of the guinea pig. 

MonocercoDionoides sp. was found by 
Saxe (1954) in the laboratory rat and 
golden hamster. He transmitted it from 
the hamster to the rat. This species 
awaits morphologic study and specific 
characterization. 



Genus COCHLOSOMA 
Kotlan, 1923 

The body is ovoid, broadly rounded 
anteriorly and narrowly rounded poster- 
iorly. Six flagella of unequal length arise 
from a blepharoplastic complex at the an- 
terior end; 2 of them are trailing and lie 
in a longitudinal groove. The nucleus is 
near the middle of the body. A slender, 
fibrillar axostyle and a more lateral costa 
arise from the blepharoplastic complex. 
On the anteroventral surface is a large 
sucker which opens on the left side and 
has a marginal filament. A parabasal 
body is present. 

Cochlosoma anatis Kotlan, 1923 (syn. , 
Cochlosoma roslratn»i) occurs in the cloaca, 
large intestine and sometimes the ceca of 
the domestic duck, Muscovy duck and also 
in the wild mallard and various other wild 
ducks. It has been reported in Hungary by 
Kotlan (1923), in California by Kimura 
(1934), in Iowa by Travis (1938), and is 
probably worldwide in distribution. Kimura 
(1934) found it in 23 of 30 White Pekin and 
Muscovy ducks in central California. 

The body of C. anatis is beet-shaped, 
6 to 12^1 long and 4 to Yfi wide. The sucker 
covers 1/3 to 12 the body length. The or- 
ganism swims forward with an erratic, 
jerky motion, rotating on its long axis but 
with very little of the dipping motion of 
Giardia. The parabasal body is sausage- 
shaped. Reproduction is by longitudinal 
fission. C. anatis has not been cultivated. 



FAMILY COCHLOSOMATIDAE 

In this family there are 6 anterior 
flagella, an axostyle, an anteroventral 
sucker, and a single nucleus. There may 
or may not be a parabasal body. The only 
genus so far reported from domestic ani- 
mals is Cochlosoma, but Cyathostonia 
Tyzzer, 1930 and Ptychostoma Tyzzer, 
1930 have been described from the ruffed 
grouse (Bonasa iimbellus) in North Amer- 
ica. 



The pathogenicity of C. anatis in water- 
fowl is unknown. Kimura (1934) found it in 
both healthy and sick birds, but the condi- 
tion of the latter was due to bacterial or 
nutritional disturbances, and even in heavy 
Cochlosonia infections there was no intes- 
tinal inflammation. Travis (1938) found 
no lesions in the infected domestic and 
wild ducks which he examined. 

McNeil and Hinshaw (1942) reported 
finding a Cochlosoma morphologically in- 
distinguishable from C. anatis in turkeys 



OTHER FLAGELLATES 



115 



in California. In young poults it was pres- 
ent thruout the intestinal tract, and in 
adults in the region of the cecal tonsil. 
Campbell (1945) found Coclilosonia in 
large numbers in the intestinal tracts of a 
flock of young turkeys in Scotland affected 
with a disease clinically and pathologically 
indistinguishable from infectious catarrhal 
enteritis due to Hexa»iita meleagridis. 
Both McNeil and Hinshaw and Campbell 
considered the turkey form to be the same 
species found in ducks, but experimental 
and further morphological studies are 
needed to be sure of this. 

It has not been established whether 
this form is pathogenic for turkeys. 
Campbell believed that it was the cause of 
the enteritis which he saw, but Hexamita 
was also usually detectable in his affected 
birds. In the turkey poults studied by 
McNeil and Hinshaw, Cochlosoma was al- 
ways found in association with Hexamita 
or with Hexamita and SalDionella. 



FAMILY HEXAMITIDAE 

Members of this family are bilaterally 
symmetrical, with 2 nuclei, 6 or 8 fla- 
gella and sometimes with axostyles and 
parabasal bodies. Three genera are of 
veterinary interest: Hexamita, Giardia 
and Trepomonas. 



Genus HEXAMITA 
Dujardin, 1838 

The body is piriform, with 2 nuclei 
near the anterior end, 6 anterior and 2 
posterior flagella and 2 independent axo- 
styles (which may possibly be hollow tubes 
rather than rods). The body is quite sym- 
metrical, three anterior flagella and 1 
posterior one arising on each side. Free- 
living forms have 1 or 2 contractile vac- 
uoles. The cytostome is obscure if pres- 
ent. Some species form cysts. Some 
members of this genus are free-living, 
while others are parasitic in insects, 
other invertebrates and all classes of ver- 
tebrates. The taxonomic relations of the 
various species are greatly confused, and 
much work is needed before they will be 



understood. Reasons why some workers 
use the spelling Hexamitus are given by 
Kirby and Honigberg (1949). 



HEXAMITA MELEAGRIDIS 
McNEIL, fflNSHAW AND 
KOFOID, 1941 

Disease : Hexamitosis, infectious 
catarrhal enteritis. 

Hosts : Turkey, peafowl, California 
valley quail, Gambel's quail, chukar par- 
tridge, ring-neck pheasant, golden pheas- 
ant. See Levine, Beamer and McNeil 
(1952) for references. H. meleagridis 
has been transmitted from the turkey to 
the chicken, quail and domestic duck, and 
from the ring-neck pheasant, quail and 
chukar partridge to the turkey. 

Location : Duodenum and small in- 
testine of younger birds; some occur in 
the cecum and bursa of Fabricius, espe- 
cially in adults. 

Geographic Distribution : United 
States, Canada, Great Britain, South 
America (Uruguay). The distribution of 
hexamitosis in California has been dis- 
cussed by Hinshaw, McNeil and Kofoid 
(1938). It has been reported from Con- 
necticut by Jungherr and Gifford (1944), 
from Indiana by Doyle, Cable and Moses 
(1947), from Virginia by Farr, Wehr and 
Jaquette (1948), from Alberta by Vance 
and Bigland (1956), from Scotland by 
Campbell (1945) and from England by 
Slavin and Wilson (1953). It also occurs 
in Illinois. 

Prevalence : The published reports 
of outbreaks of hexamitosis are too few to 
give a true picture of its importance. It 
occurs in all major turkey producing areas 
in the United States and in other countries 
as well. It appears to be particularly im- 
portant in California. The U. S. Dept. of 
Agriculture (1954) estimated that it causes 
an annual loss of $667,000 in turkeys in 
the United States. 

Morphology : The body is 6 to 12/i 
long and 2 to 5/j, wide, with a mean of 9 



llfi 



OTHER FLAGELLATES 



by 3/i. The two nuclei contain round endo- 
somes 2/3 the diameter of the nucleus. 
Anterior to each nucleus is a large blephar- 
aroplast or group of blepharoplasts from 
which 2 anterior and 1 anterolateral fla- 
gella arise. Just behind this blepharoplast 
is another from which the caudal flagellum 
arises. The caudal flagella pass poster- 
iorly in a granular line of cytoplasm to 
their points of emergence near the poster- 
ior end of the body. Hexamita moves ra- 
pidly without the spiralling characteristic 
of trichomonads. 




Fig. 17. Hexamita iiieleagridis. 
(Original) 



X 2800. 



Life Cycle : Multiplication is by 
longitudinal binary fission. Slavin and 
Wilson (1953) and Wilson and Slavin (1955) 
described what they believed to be schizog- 
ony and cyst formation, but Hoare (1955) 
considered their idea to be purely specu- 
lative and inacceptable. 

Pathogenesis : Hexamitosis is a dis- 
ease of young birds; adults are symptom- 
less carriers. The mortality in a flock 
may be as high as 70 to 80%, but heavy 
losses seldom occur in poults over ten 
weeks old. Affected poults appear nervous 
at first, have a stilted gait, ruffled, un- 
kempt feathers, and a foamy, watery 
diarrhea. They usually continue to eat, 
but chirp continually. They lose weight 
rapidly, become listless, weak and finally 
die. Birds often do not appear to be ill 
until shortly before death, but examination 



will reveal that they are thin and have 
lowered temperatures. Birds which re- 
cover grow poorly, and an outbreak may 
leave many stunted birds in its wake. 

The incubation period is 4 to 7 days. 
Poults may die within a day after signs 
appear. In acute outbreaks, the mortality 
reaches a peak in the flock in 7 to 10 days 
after the first birds die; in other flocks, 
deaths may continue for 3 weeks. 

The principal pathological changes 
are found in the small intestine. Catarrhal 
inflammation with marked lack of tone is 
present in the duodenum, jejunum and 
ileum. The intestinal contents are usually 
thin, watery and foamy, with localized 
bulbous swellings filled with watery fluid. 
The small intestine, especially the anter- 
ior part, is inflamed and edematous. The 
cecal contents are usually fluid, and the 
cecal tonsils are congested. 

Epidemiology : Hexamita is trans- 
mitted thru contaminated feed and water. 
Carrier adult birds which have survived 
earlier attacks are the most important 
source of infection for turkey poults. 
Sometimes the disease does not appear in 
the earlier hatches but strikes the later 
ones after the adults have been sold. This 
may come about because the infections in 
the earlier hatches were very light or per- 
haps because the virulence of the strains 
was too low to cause noticeable disease. 
According to Hinshaw (1959) it may take 
several passages in poults of a strain from 
carrier turkeys before an acute outbreak 
occurs. 

Wild quail, pheasants and chukar par- 
tridges sharing the range with turkeys may 
also be a source of infection. 

Hot weather and overcrowding may 
also contribute to the severity of an out- 
break. In addition, the role of flies de- 
serves study. Turkey poults are excellent 
fly-catchers, and these insects might carry 
the protozoa from one pen to another. 

Diagnosis : Hexamitosis can be diag- 
nosed by finding the protozoa in scrapings 
from the small intestine, and particularly 



OTHER FLAGELLATES 



117 



from the jejunum and duodenum. The 
smears should be mixed with physiological 
salt solution and examined while fresh. 
Hexanilta can be readily differentiated 
from TrichoDionas, Giardia or Cochlosoma 
by its small size, absence of a sucker or 
undulating membrane, and characteristic 
motion. Impression smears can also be 
made of cross sections of fresh small in- 
testine, dried rapidly and stained with 
Giemsa's stain; the protozoa are often 
found in groups in the crypts. Hexaiiiita 
can also be found in the bursa of Fabricius 
and cecal tonsils in carrier birds. 

Cultivation : Hexamita nieleagridis 
has not been cultivated in artificial culture 
media, but Hughes and Zander (1954) cul- 
tured it axenically in the chorioallantoic 
fluid of chick embryos. 

Treatment : No treatment has appar- 
ently been uniformly successful for hexa- 
mitosis. McNeil (1948) recommended 
replacing the drinking water for several 
days with a mixture of 3% dried whey in 
1-2000 aqueous copper sulfate solution. 
It must be begun early in an outbreak to be 
effective, and Wilson and Slavin (1955) did 
not find it to be of value in their studies. 

Almquist and Johnson (1951) found in 
preliminary tests that streptomycin was 
ineffective, but that penicillin, chlortetra- 
cycline and oxytetracycline were of some 
value. Enheptin also gave good results 
when fed as 0.1% of the mash for 14 days. 
Wilson and Slavin (1955) said that they 
tested every antiprotozoal drug available 
commercially in England (including anti- 
malarials, trypanocides, amoebicides and 
antiluetics) without success. Enheptin was 
only about 50% effective in experimentally 
infected poults. The most promising drug 
was di-n-butyl tin dilaurate, which ap- 
peared to control mild field outbreaks and 
to lower the death rate in more severe 
ones. 

Mangrum et al. (1955) reported that 
furazolidone reduced mortality in exper- 
imentally infected turkey poults. McNeil 
(1958) mentioned that nithiazide had been 
used successfully by Merck, Sharp & 
Dohme Research Laboratories in a com- 



bined outbreak of histomonosis and hexa- 
mitosis. 

Prevention and Control : Hexamitosis 
can be prevented by proper management 
and sanitation. Poults should be separated 
from adults, and separate caretakers should 
be used for the two groups. If feasible, 
breeding birds should be sold 2 weeks before 
any poults are hatched. Separate equipment 
should be used for different groups of birds. 
Attendants should keep out of the pens, and 
the feeders and waterers should be placed 
where they can be reached from the outside. 
Feeders and waterers should be placed on 
wire platforms. Young birds should be kept 
on wire. Ranges frequented by pheasants, 
quail and chukar partridges should be 
avoided. General sanitation and fly control 
should be practiced. 



OTHER SPECIES OF HEXAMITA 

Hexamita columbae (NoUer and Butt- 
gereit, 1923) (syn. , Octo»iitus coliiuibae) 
occurs in the duodenum, jejunum, ileum 
and large intestine of the pigeon. It is 5 
to 9|u long and 2. 5 to 7 p. wide. It is path- 
ogenic, causing a catarrhal enteritis. 
Noller and Buttgereit (1923) found it in 
great masses from the gizzard to the anus 
in a pigeon with catarrhal enteritis in Ger- 
many, and McNeil and Hinshaw (1941) 
found it in affected pigeons in California. 
They were unable to infect turkeys with 
this species. 

Hexam ita -was found by Kotlan (1923) 
in the intestinal mucus of the domestic 
duck in Hungary. He called it "Hexamitus 
intestinalis (?)". It was usually piriform, 
10 to 13/i long and 4 to 5(u wide. Kimura 
(1934) found Hexamita in the ceca and large 
intestine of domestic ducks in California. 
McNeil and Hinshaw (1941) infected domes- 
tic ducks experimentally with H. melea- 
gridis from the turkey. It is uncertain 
whether the duck form is a separate species. 
It has not been adequately described, and 
its pathogenesis is unknown. 

Hexamita muris (Grassi, 1881) (syns. , 
Octomitus muris, Syndyomita nniris) occurs 
in the posterior small intestine and cecum 



118 



OTHER FLAGELLATES 



of the Norway rat, house mouse, golden 
hamster and various wild rodents. It 
measures 7 to 9 by 2 to 3 (i . 

Wenrich (1933) described Hexamita 
sp. from the feces of a rhesus monkey. 
It measured 4 to 6 by 2 to 4 jj, . 



Genus OCTOMIlUi 
Von Prowazek, 1904 

The body is piriform, with 2 nuclei 
near the anterior end, and 6 antenior and 
2 posterior flagella. The body is quite 
symmetrical, 3 anterior flagella and 1 
posterior one arising on each side. There 
are 2 axostyles which originate at the an- 
terior end and fuse as they pass poster- 
iorly, emerging as a single central rod 
from the middle of the posterior end. 
This genus differs from Hexamita, of 
which it was formerly considered a syn- 
onym, in the structure of its axostyles 
(Gabel, 1954). 

Octomitus pulcher (Becker, 1926) 
Gabel, 1954 (syn. , O. intestinalis) occurs 
in the cecum of the Norway rat, house 
mouse, golden hamster, ground squirrels 
and other wild rodents. It measures 6 to 
10 by 3 to 7 /i. 



Genus GIARDIA Kunstler, 1882 

The body is piriform to ellipsoidal, 
and bilaterally symmetrical. The anterior 
end is broadly rounded, and the posterior 
end is drawn out. There is a large suck- 
ing disc on the ventral side; the dorsal 
side is convex. There are 2 anterior nu- 
clei, 2 slender axostyles, 8 flagella in 4 
pairs, and a pair of darkly staining median 
bodies. The cysts have 2 or 4 nuclei and 
a number of fibrillar remnants of the 
trophozoite organelles. A synonym of this 
generic name is Lamblia Blanchard, 1888. 

The names given the species of Giardia 
depend on the authorities concerned. Tra- 
ditionally, it has been believed that Giardia 
is highly host-specific, and different names 
have been given to almost all the forms in 
different hosts. Thus, if we accept the 



names in Ansari's (1951, 1952) review, 
the species in cattle is G. bovis, that in 
goats and sheep G. caprae, that in the dog 
G. canis, that in the cat G. cali, that in 
the rabbit G. duodenaiis , that in the guinea 
pig G. caviae, those in the Norway rat G. 
muris and G. simoni, and those in the 
house mouse G. muris a.ndG. microti. 
However, Filice (1952) was unable to find 
any morphological difference between the 
giardias of the laboratory rat and a num- 
ber of wild rodents, and on reviewing the 
literature discovered that almost no ac- 
ceptable cross-transmission studies exist 
between some species. Altho he did not 
discuss them all, he appears to have con- 
cluded that there are only two species of 
Giardia in mammals, each with a number 
of races. G. muris occurs in the mouse, 
rat and hamster, and G. duodenaiis in the 
rabbit, rat, chinchilla, ground squirrel, 
deermouse, pocket mouse, man and pre- 
sumably ox, dog, cat and guinea pig, 
among others. The essential difference 
between these two forms is that the median 
bodies of G. muris are small and rounded 
while those of G. duodenaiis are long, re- 
semble somewhat the claw of a claw-ham- 
mer, and lie approximately transversely 
across the body. 

In this connection, Hegner's (1930), 
Armaghan's (1937) and Haiba's (1956) 
success in infecting laboratory rats with 
Giardia from man suggests that Filice' s 
view may eventually prevail. However, 
careful cross-transmission studies must 
be carried out before a decision can be 
made. In the meantime, it is more con- 
venient to use different specific names for 
most of the forms from different hosts. 

Associated with this nomenclatorial 
problem is an important epidemiological 
one. If it turns out that Giardia can be 
freely transmitted from one host to an- 
other, we shall have to revise our ideas 
about the danger to man of infections in 
laboratory and domestic animals, and of 
infections in one domestic animal to others. 
Here is an area of ignorance which de- 
serves exploration. 

Giardia has not yet been cultivated in 
artificial media, a fact which has hampered 



OTHER FLAGELLATES 



119 



studies both of its epidemiology and path- 
ogenicity. However, Karapetyan (1960) 
cultivated G. lamblia in chicken fibroblast 
tissue cultures. 



GIARDIA LAMBLIA 
STILES, 1915 

Synonyms : CercoiHOiias iiitestinalis, 
Lamblia intestinalis, Giardia intestinalis , 
Megasto))Hi entericiiiii , Giardia enterica. 
European writers still call this species 
Giardia intestinalis, but there was so 
much confusion about the availability of 
the specific names intestinalis and enter- 
ica that Stiles (1915) established the pres- 
ent name. 

Disease : Giardiosis. 

Hosts : Man, Old and New World 
monkeys, pig. Hegner (1930) and Arma- 
ghan (1937) infected laboratory rats and 
Bonestell (1935) infected woodrats (Neo- 
tonia fiiscipes) with G. huiiblia from man. 
Haiba (1956) infected wild and laboratory 
Rattus norvegicus , but failed to infect 
wild R. rattus and laboratory mice with 
G. lamblia from man. 



duodenalis type. The cysts are ovoid, 8 
to 12j;i long and 7 to lO/i wide, and con- 
tain 4 nuclei. 

Pathogenesis : There was considerable 
controversy for many years whether Giardia 
is pathogenic in man, but it is now gener- 
ally agreed that it may be in some individ- 
uals. Most infections are symptomless, 
but in a fairly small number there is a 
chronic diarrhea. The feces contain a 
large amount of mucus and fat but no blood. 
The diarrhea is accompanied by dull epi- 
gastric pain and flatulence. Affected per- 
sons have a poor appetite and lose weight. 
In some cases the gall bladder may be in- 
vaded and cholecystitis may be present, 
but there is no proof that the protozoa 
caused this condition. Pizzi (1957) reviewed 
some of the literature on the pathogenicity 
of G. lamblia and concluded that in heavy 
infections it may also interfere with fat 
absorption and produce a deficiency in fat- 
soluble vitamins. It is more often patho- 
genic in children than adults. 



The pathogenicity of G. 
sv/ine is unknown. 



lamblia for 



Location : Duodenum, jejunum, upper 
small intestine. 

Geographic Distribution : Worldwide. 

Prevalence : G. lamblia is common 
in man. In 86 surveys of 134,966 people 
thruout the world summarized by Belding 
(1952), its prevalence ranged from 2.4 to 
67. 5% with a mean of 10. 4%. It was found 
in 7. 4% of 35, 299 persons in 24 surveys 
in the United States, and in 6. 9% of 65, 295 
persons in 20 surveys in the rest of the 
world. It is about 3 times as common in 
children as in adults. 

G. lamblia was reported from a pig 
in Tennessee by Frye and Meleney (1932). 
Its prevalence in swine is unknown. 

Morphology : The trophozoites are 9 
to 21 ju long, 5 to 15 p. wide and 2 to 4/^ 
thick; they are usually 12 to 15ju long. 
The median bodies are curved bars of the 




Fig. 18. A. Giardia trophozoite. X 2800. 
(After Filice, 1952). B. Giardia 
bovis cyst. X 2900. (From 
Becker and Frye, 1929) 



120 



OTHER FLAGELLATES 



Diagnosis : Giardia infections can be 
diagnosed by recognition of trophozoites 
or cysts in stained fecal smears. Fixation 
with Schaudinn's fluid and staining with iron 
hematoxylin are recommended. Tropho- 
zoites alone are generally found in diarrheic 
stools. The cysts can be concentrated by 
the flotation technic. Zinc sulfate solution 
should be used for flotation; sugar and 
other salt solutions distort the cysts and 
make them unrecognizable. 

Cultivation : Neither G. lamblia nor 
any other species of Giardia has been cul- 
tivated in artificial media. Karapetyan 
(1960) cultured it in chicken fibroblast 
tissue cultures along with the yeast, Can- 
dida guillierniondi. The protozoon did not 
develop without the yeast, which led him to 
believe that there may be a synergistic re- 
lation between the 2 organisms. 

Treatment : Giardia infections in man 
can be successfully treated with either 
quinacrine or chloroquine. Three oral 
doses of 0. 1 g each are given daily for 5 
days. Amodiaquin is considered even 
better than these (Lamadrid-Montemayor, 
1954); a single dose of 0. 6 g is given to 
adults. 

Prevention and Control: These de- 
pend on sanitation. Cerva (1955) found 
that 2 to 5% phenol or lysol would kill G. 
lamblia cysts, but that chloramine, mer- 
curic chloride, formalin and a number of 
other disinfectants were ineffective in the 
concentrations commonly used. The cysts 
were killed by temperatures above 50° C 
and, after 10 hours, by freezing below 
-20° C. They remained viable in water 
for over 3 months. 



GIARDIA CANIS 
HEGhfER, 1922 

Host: Dog. 

Location : Duodenum, jejunum, upper 
small intestine. Tsuchiya (1932) found 
the optimum location to be 10 to 30 inches 
posterior to the stomach in puppies on a 
carbohydrate diet and 25 to 40 inches 
from the stomach in puppies on a high 
protein diet. 



Geographic Distribution : North 
America (United States, Canada), South 
America (Uruguay). 

Prevalence : Catcott (1946) found G. 
canis in 17. 7% of 113 dogs in Ohio. Cho- 
quette and Gelinas (1950) found it in 9.0% 
of 155 dogs in Montreal, Canada. Craige 

(1948) found it in 8. 8% of 160 dogs in Cal- 
ifornia. We have seen it a number of 
times in dogs in Illinois, but have not at- 
tempted a survey. 

Morphology : The trophozoite is 12 
to 17 ;j long and 7 to 10 ji wide. The me- 
dian bodies are curved bars of the duoden- 
alis type. The cysts measure 9 to 13 by 
7 to 9 fi . 

Pathogenesis : The pathogenicity of 
G. canis for the dog has still to be incon- 
trovertibly determined. Catcott (1946) 
noted diarrhea in one-third of his positive 
dogs. Craige (1948) found Giardia in 17 
of 71 dogs with dysentery, but in 13 of them 
other organisms which he considered path- 
ogenic were also present. Choquette (1950) 
found Giardia in several cases of dysentery, 
but some of these were complicated by 
other conditions. Tsuchiya (1931) reported 
that diarrheic stools alternated with formed 
stools in a number of experimentally in- 
fected puppies, but was uncertain whether 
it was due to an existing pathological con- 
dition or to the flagellates. According to 
Tsuchiya (1932), a carbohydrate diet is 
more favorable for G. ca)iis than a high 
protein diet. 

Diagnosis : Same as for G. lamblia. 

Treatment : Quinacrine has been 
found effective against G. canis. Craige 

(1949) gave dogs 50 to 100 mg twice daily 
for 2 or 3 days, repeating if necessary 
after 3 to 4 days. Choquette (1950) gave 
large dogs 0. 2 g three times the first day 
and twice a day for 6 more days; he gave 
small dogs 0. 1 g twice the first day and 
once a day for 6 more days. Chloroquine 
has also been found effective in man; 0. 1 
g is given 3 times a day for 5 days. 

Prevention and Control : The standard 
sanitary measures should be used in pre- 
venting the transmission of Giardia. 



OTHER FLAGELLATES 



121 



GIARDIA CATI 
DESCfflENS, 1925 

Synonym s : Giardia felis . 

Host : Cat. 

Location : Small intestine, large in- 
testine. Hitchcock and Malewitz (1956) 
noted G. cati trophozoites thruout the 
small intestine, cecum and colon (except 
at the pyloric valve) of a naturally infected 
64-day-old kitten in Michigan. They were 
most numerous in the lower part of the 
small intestine. 

Geographic Distribution : North 
America (United States), Europe (France). 

Prevalence : Hitchcock (1953) found 
Giardia in 8 of 14 kittens in Michigan. 

Morphology : It is quite likely that 
this species is a synonym of G. canis. 
The trophozoites are 10 to 18 jj, long and 5 
to 9 jLi wide with a mean of 13 by 7 ji . The 
median bodies are bars of the duodenalis 
type. The cysts are 10. S/jL long and 7/1 
wide. 

Pathogenesis : Unknown. The in- 
fected cats studied by Hitchcock (1953) and 
Hitchcock and Malewitz (1956) apparently 
had no signs of enteritis. 



GIARDIA BOVIS 
FANTHAM, 1921 

Host: Ox. 

Location: Duodenum, jejunum, ileum. 

Geographic Distribution : North 
America (United States), Europe (England, 
Holland, Austria, Italy), South Africa. 

Prevalence : Unknown. Becker and 
Frye (1927) found this species in the feces 
of cattle in Iowa, Nieschulz (1923) saw it 
in a calf in Holland, Graham (1935) found 
it alive and active in the digestive tract of 
6 of 21 female Cooperia oncophora from a 
calf from New Jersey, and we have found 
it from time to time in casual examinations 
in Illinois. 



Morphology : The trophozoites are 
11 to 19 jn long and 7 to lOfi wide. The 
median bodies are curved bars of the duo- 
denalis type. The cysts are 7 to 16fj. long 
and 4 to lOfi wide. 

Pathogenesis : The pathogenicity of 
G. bovis is unknown. Supperer (1952) 
found it in a calf in Austria with a mucous 
diarrhea. The calf was killed for necropsy 
diagnosis and was found to have catarrhal 
duodenitis and jejunitis; the mucosa was 
dark red, thickened and lay in folds. Botti 
(1956, 1956a) found it in calves with hem- 
orrhagic diarrhea in Italy. On the other 
hand, the cattle in which we saw the or- 
ganism in Illinois did not appear to be 
affected by it. 



OTHER SPECIES OF GIARDIA 

Giardia caprae Nieschulz, 1923 (syn. , 
G. ovis) was reported from the anterior 
part of the small intestine of 2 goats in 
Holland. Nieschulz (1924) described it 
further. Its trophozoites are 9 to 17 /i long 
and 6 to 9jj, wide with a mean of 13. 5 by 
7. 5/i. The median bodies are curved bars 
of the duodenalis type. The cysts have 4 
nuclei and measure 12 to 15 by 7 to 9/1 
with a mean of 14 by 8 /j, . 

Giardia caprae was found by Grassi 
(1881) in sheep in Italy and by Turner and 
Murnane (1932) in the small intestine of 
sheep in Australia. The Australian sheep 
had been losing weight gradually for sev- 
eral months. Deas (1959) found it in a 
lamb with enteritis in England. D. A. 
Willigan (unpubl. ) found Giardia in 3 of 24 
iambs brought to the University of Illinois 
Veterinary Diagnostic Service. All came 
from a single flock in which many of the 
lambs were suffering from diarrhea and 
loss of weight, but coccidiosis and sal- 
monellosis were also found. Dissanaike 
(1954) found live and active G. caprae in 
the intestines of 50 female and no male 
Nematodirus filicollis from 5 sheep in 
England. 

Giardia equi Fantham, 1921 was or- 
iginally found in the large intestine of a 
horse in South Africa. Varela and Sal- 
samendi (1958) found it in the feces of a 



122 



OTHER FLAGELLATES 



horse with colic in Venezuela. Its troph- 
ozoites measure 17 to 21 by 9 to 12 jx , and 
its cysts measure 12 to 16 by 8 to 9. 5 fi . 

Giardia duodenalis (Davaine, 1875) 
(syns. , HexuDiila duodenalis, LciDiblia 
cuniciili) occurs in the anterior small in- 
testine of Old and New World rabbits and 
also in Coeiidu uillosus in Brazil. It oc- 
curs sporadically and is apparently not 
pathogenic. Its trophozoites measure 13 
to 19 by 8 to 11 |i with a mean of 16 by 9^t . 
The median bodies are curved bars re- 
sembling the claws of a claw-hammer; th 
they lie transversely across the body. 
The cysts contain 2 to 4 nuclei. 

Giardia simoni Lavier, 1924 occurs 
in the anterior small intestine of the Nor- 
way rat, golden hamster and probably 
various wild rodents. Its trophozoites 
measure 11 to 19 by 5 to 11 jj,. Its median 
bodies are curved bars of the duudenalis 
type. 

G. 7nuris (Grassi, 1879) occurs in 
the anterior small intestine of the house 
mouse, Norway rat, black rat, golden 
hamster and various wild rodents. It is 
common in laboratory rats and mice. Its 
trophozoites measure 7 to 13 by 5 to I0\i. 
Its median bodies are small and rounded. 

G. curiae Hegner, 1923 occurs in the 
anterior small intestine of the guinea pig. 
Its trophozoites measure 8 to 15 by 6. 5 
to lOfi. Its median bodies are curved 
bars of the duodenalis type. 

Giardia chinchillae Filice, 1952 
emend, (syn. , Giardia duodenalis race 
chinchillae Morgan, 1949 of Filice, 1952; 
altho he gave the first description of this 
form, Morgan did not give it a specific 
name; the name chinchillae vfas intro- 
duced by Filice) occurs frequently in the 
chinchilla. It is found thruout the small 
intestine, but more commonly in the duo- 
denum and anterior jejunum. Its troph- 
ozoites measure 11 to 20 by 6 to 12 j:i . 
Its median bodies are curved bars of the 
duodenalis type. This species has been 
accused by various workers of causing 
diarrhea and even death (Shelton, 1954; 
Gorham and Farrell, 1955). Treatment 
with 6 to 9 mg quinacrine for 5 to 7 days 



was found by Hagan (1950) to eliminate the 
infection. Attempts to transmit G. chin- 
chillae to the golden hamster, white mouse, 
domestic rabbit or guinea pig have been un- 
successful (Morgan, 1949; Shelton, 1954). 



Genus TREPOfAONAS Dujardin, 1841 

These are free-swimming protozoa 
with a more or less rounded, bilaterally 
symmetrical body and with a cytostomal 
groove on each side of the posterior half. 
There are 8 flagella, of which 1 long and 
3 short ones are present on each side. A 
horseshoe-shaped structure near the an- 
terior margin contains the 2 nuclei. Mem- 
bers of this genus are free-living in fresh 
water, coprophilic or parasitic in am- 
phibia, fish and turtles. 

Trepomonas agilis Dujardin, 1841 
occurs in stagnant water and the intestine 
of amphibia and is also coprophilic. It is 
7 to 25jj. long and 2 to 15|i wide, with a 
flattened body and with the posterior end 
wider than the rounded anterior end. The 
flagella come off near the middle of the 
body at the anterior end of the cytostome. 



ORDER PROTOMASTIGORIDA 

Members of this order have 1 or 2 
flagella. 



FAMILY BODONIDAE 

Members of this family have 2 fla- 
gella which originate anteriorly; one is 
directed anteriorly and the other poster- 
iorly. The anterior end is more or less 
drawn out. There are 1 to several con- 
tractile vacuoles. There are several gen- 
era of free-living and parasitic forms in 
this family. 



Genus BODO Stein, 1875 

These are small, more or less ovoid, 
plastic forms with an anterior cytostome 
and a central or anterior nucleus. Cysts 
are forme'd. 



OTHER FLAGELLATES 



123 



Bodo caudatus (Dujardin, 1841) Stein, 
1878 is a common coprophilic form and 
also occurs in stale urine and stagnant 
water. It is 8 to 18;U long and 2. 5 to 6)ll 
wide, with a polymorphic body ranging in 
shape from spherical to elongate ovoid. 
It has a tiny contractile vacuole, a single 
vesicular nucleus with a large endosome 
and a rounded parabasal body. This spe- 
cies and also B. foetus and B.glissans 
have been found in material from bulls 
submitted for TritricIiouw>ias foetus diag- 
nosis. 



Genus CBRCOMONAS Dujardin, 1841 

These are small forms with a plastic 
body, one flagellum directed anteriorly 
and the other running backward over the 
body to become a trailing flagellum. The 
nucleus is piriform and is connected with 
the basal granule of the flagella. The 
cysts are spherical and uninucleate. A 
number of freshwater and coprophilic 
species have been described, but it is not 
clear whether all the species are valid. 

Cercomonas longicauda Dujardin, 
1841 is a common coprophilic flagellate. 
Its trophozoites are amoeboid, 2 to 15 /j. 
long, have 2 contractile vacuoles, and 
ingest food by means of pseudopods. Its 
cysts are 4 to 7jj, in diameter. 

Cercomonas heimi (Hollande) is sim- 
ilar to C. longicauda but is piriform and 
has longer flagella. 

Cercomonas equi (Sabrazes and Mur- 
atet, 1908) (syn. , C. asini) was described 
from the large intestine of the horse and 
donkey and also occurs in their feces. 



coprophilic. It has been found in material 
from bulls submitted for examination for 
Tritrichomonas foetus (Morgan and Haw- 
kins, 1952). Its trophozoites measure 10 
to 16 by 7 to 10 /ix. 




Fig. 19. Coprophilic flagellates. A. Cer- 
comonas sp. X 4200. B. Copro- 
nionas subtilis. X 5100. 
C. Moiias sp. X 4200. (From 
Noble, 1956) 

Noble (1956) found Cercomonas sp. 
in fresh bovine and porcine feces, and 
cultivated them in feces in the refrigerator 
at 4° C for 5 months. Noble (1958) found 
that Cerco»io)ms sp. appeared in fecal 
specimens from Wyoming elk, bison, cat- 
tle, horses and sheep after storage at 4°C 
for 6 to 7 days. They persisted for sev- 
eral weeks and then died out. They failed 
to survive in soil alone or in soil mixed 
with boiled feces, nor could they be found 
in soil samples taken from areas where 
elk, sheep or horses were present. Noble 
concluded that this and other coprophilic 
protozoa may require certain essential 
metabolites produced by bacteria. 



Cercomonas faecicola (Woodcock and 
Lapage, 1915) (syn., Helkesimastix fae- 
cicola) was found in the feces of the goat. 
It is ovoid, with a rigid, pointed anterior 
end. The anterior flagellum is very short 
and easily overlooked. The trophozoites 
are 4 to 6jLt long and the cysts 3 to 3. 5 /i 
in diameter. 

Cercomonas crassicauda Dujardin, 
1841 occurs in fresh water and is also 



The Cercomonas sp. trophozoites ob- 
served by Noble (1958) were 5. 4 by 2. 5jj,, 
somewhat tadpole-shaped, with a broad 
anterior end tapering to a highly flexible 
tail-like posterior end. An extremely 
short anterior flagellum, visible only with 
phase contrast, extended from a minute 
subterminal cytostome. Another flagellum 
arose from the anterior region, passed 
thru the cytoplasm ventral to the nucleus, 
emerged about 2/3 of the body length from 



124 



OTHER FLAGELLATES 



the anterior end, and continued as a long 
trailing whip. Eight to 10 large, dark 
cytoplasmic granules were arranged along 
this flagellum. The cytoplasm contained 
a large contractile vacuole and many food 
vacuoles. The nucleus was vesicular. 



Genus PLEUROMONAS Perty, 1852 

The body is somewhat amoeboid. 
The 2 flagella often appear to emerge 
separately from the body. The anterior 
flagellum is very short and often rolled 
up into a ring. The posterior flagellum 
is very thick and more than 2 to 3 times 
the length of the body. There is a single 
vesicular nucleus. The cyst is spherical, 
and 4 to 8 young individuals apparently 
emerge from it. 

There is a single species in this 
genus, Pleuromonas jacidans Perty, 1852, 
which occurs in stagnant water. It is 6 to 
lOfi long and about Sfi wide. Uribe(1921) 
found large numbers of this protozoon in 
the ceca of young chickens which he had 
fed Heterakis material, and believed that 
it could become adapted to parasitism. 



Genus PROTEROMONAS 
Kunstler, 1883 

The body is spindle-shaped. An an- 
terior and a free trailing flagellum arise 
from 2 blepharoplasts at the anterior end. 
The nucleus is anterior to the middle of 
the body and contains scattered chromatin 
granules but no endosome. A rhizoplast 
runs from the blepharoplast to a centro- 
some on the nuclear membrane. A peri- 
rhizoplastic ring surrounds the rhizoplast 
a short distance behind the blepharoplast; 
this is considered a parabasal body. A 
paranuclear body the same size as the 
nucleus lies beside the nucleus; it divides 
when the nucleus divides, and stains with 
hematoxylin but not with protargol. All 
the species are parasitic. They are com- 
mon in the intestines of reptiles and am- 
phibia. Synonyms of this genus are 
Prowazekella Alexeieff, 1912 and Sc/ii2o- 
bodo Chatton, 1917. 



Proteromonas brevifilia Alexeieff, 
1946 occurs in the cecum of the guinea 
pig- 



FAMILY AMPHIMONADIDAE 

Members of this family have a naked 
or loricate body with 2 equal flagella. 
There are several genera, mainly in fresh 
water. 



Genus SPIROMONAS Perty, 1914 

Members of this genus have an elon- 
gate, spirally twisted body with 2 anterior 
flagella. They form spherical cysts in 
which division into 4 daughter individuals 
takes place. They live in fresh water. A 
synonym is Alphanwnas Alexeieff. 

Spiromonas miffusta (Dujardin) Alex- 
eieff lives in stagnant water or is copro- 
philic. It has also been found in bull 
sheath washings. It is spindle-shaped and 
about lOfi long. 



SUBCLASS PHYTOMASTIGASINA 

Members of this subclass typically 
have chromatophores and holophytic nu- 
trition. Some are colorless but closely 
resemble other holophytic forms and are 
derived from them or from a common 
ancestor. A few are coprophilic and still 
fewer are parasitic. In each group the 
parasitic mode of life has undoubtedly 
arisen anew. 

ORDER CHRYSOMONADORIDA 

In this order the chromatophores, if 
present, are yellow, brown, orange or 
occasionally blue. The stored reserves 
include leucosin (presumably a polysac- 
charide) and lipids, but no starch. There 
are five suborders in the Chrysomonador- 
ida, but only one of them, Euchrysomon- 
adorina, contains forms of veterinary or 
medical interest. In this suborder the 
flagellate stage is dominant, and neither 
a siliceous skeleton nor a peripheral zone 



OTHER FLAGELLATES 



125 



of coccoliths is present. This suborder 
contains 4 families, 2 of which contain 
parasitic or coprophilic species. 



FAMILY CHROMULINIDAE 

Members of this family have a single 
flagellum. 



Genus OIKOMONAS Kent, 1880 

Members of this genus lack chromato- 
phores, lorica or test. They are solitary. 
The nucleus is near the center of the body. 
The single flagellum arises from a basal 
granule near the body surface. Cysts are 
formed, at least in the free-living species. 
This genus is the colorless homolog of 
Chroninlina. Its parasitic species are 
poorly known. 

Oikomonas communis Liebetanz, 
1910 and Oikomonas mini)>ia Liebetanz, 
1910 were both described from the rumen 
of cattle. They are said to differ in size, 
the former being up to 11 /i long and the 
latter more than 4(i long; this is probably 
not a valid difference. Das Gupta (1935) 
found 0. communis in the rumen of goats 
in India. 

Oikomonas equi Hsiung, 1930 was 
found in the cecum of 8 horses in Iowa. 
It is usually spherical or ovoid and swims 
in a jerky manner. The nucleus has a 
large, central endosome and the cytoplasm 
is filled with small, dark-staining gran- 
ules. The body is 3. 5 to 1 [i long and 3 to 
5. 5/1 wide. The flagellum is about 20 /i 
long. 



Genus SPHAIROMONAS 
Liebetanz, 1910 

The body is spherical or ellipsoidal, 
with a more or less central nucleus. A 
single, long flagellum arises from a basal 
granule on the nuclear membrane. This 
genus is poorly known and has apparently 
not been studied by modern methods. It 
is closely related to Oikomonas and may 
even be a synonym of that genus. Several 



species have been named, all parasitic, 
but most of them are probably the same. 

Sphaeromonas communis Liebetanz, 
1910 (syns. , S. minima, S. maxima, S. 
liebeta)izi, S. rossica) occurs in the rumen 
of the ox and goat and in the cecum and 
feces of the guinea pig. It may also be 
coprophilic. Liebetanz (1910) and Braune 
(1914) found it in the rumen of cattle in 
Europe, Becker and Talbott (1927) found 
it in the rumen of a few cattle in Iowa 
(calling it, however, Monas communis), 
and Fonseca (1916) found it in cattle and 
goats and also in the guinea pig in Brazil. 
Yakimoff et al. (1921) found it in the 
guinea pig in Russia. The body is spher- 
ical or ellipsoidal, 3 to Mfi in diameter. 
The cytoplasm contains many dark-staining 
granules. 



Genus CAVIOMONAS Nie, 1950 

The body is naked, without chromato- 
phores and with a vesicular nucleus at the 
anterior end. One flagellum arises from 
the nuclear membrane. A band-like peri- 
style arises from the nuclear membrane 
opposite to the origin of the flagellum and 
extends posteriorly along the periphery of 
the body surface; it stains with hematoxylin 
and protargol. Cytostome and contractile 
vacuoles are absent. 

Caviomonas mobilis Nie, 1950 occurs 
in the cecum of the guinea pig. The body 
is ovoid to elongate carrot-shaped and the 
posterior end is often pointed. It measures 
2 to 7 by 2 to 3 n with a mean of 4 by 3 /j. . 



FAMILY OCHROMONADIDAE 

Members of this family have 1 long 
and 1 short flagellum. 



Genus MONAS Muller, 1773 

The body is active and plastic. Chrom- 
atophores are absent. This genus is the 
colorless homolog of Ochromonas . Reyn- 
olds (1934) recognized 13 free-living spe- 
cies, and in addition there is at least 1 
coprophilic one. 



126 



OTHER FLAGELLATES 



Noble (1956) cultivated Monas sp. in 
bovine feces at 4" C in the refrigerator 
for 5 months. He also (1958) found that 
Motias sp. appeared in fecal samples from 
Wyoming elk, bison and bear after storage 
at 4° C for 7 to 27 days. The protozoa 
persisted for several weeks and then died 
out. They failed to survive in soil or in 
soil mixed with boiled feces, nor could 
they be found in soil samples taken from 
areas whei-e elk, sheep or horses were 
present. Noble concluded that this and 
other coprophilic protozoa may require 
certain essential metabolites produced by 
bacteria. The form which Noble studied 
was spherical and 4(i in diameter. He 
assigned it to the "Moiias coiiininnis" re- 
ported by Becker and Talbott (1927) from 
the rumen of cattle, but the latter had 
only a single flagellum and was Spliaeyo- 
ntuiias co>iii)iH)iis. 

Moiias obliqua Schewiakoff has been 
found in material from bulls submitted 
for Trilricliomonas foetus diagnosis 
(Morgan and Hawkins, 1952). 



ORDER EUGLENORIDA 

In this order the chromatophores, if 
present, are green. The stored reserves 
include lipids and paramylum. There is 
a reservoir or "gullet" from the posterior 
or postero-dorsal wall of which the fla- 
gella arise. There are 3 suborders in the 
Euglenorida, of which the Euglenorina in- 
cludes one genus containing coprophilic 
forms. 



nucleus is vesicular, with a large endo- 
some. Permanent fusion followed by en- 
cystment takes place. Nutrition is holo- 
zoic on bacteria. 

Copromonas subtilis Dobell, 1908 
(syn. , Copromonas ruminantium) was first 
described from the feces of frogs and 
toads, but has since been found in the feces 
of man and various domestic and wild mam- 
mals, Wenyon (1926) and Noble (1956) 
found it in pig feces. Woodcock (1916) 
found it in goat feces. Noble (1958) found 
that it appeared in fecal samples from 
Wyoming elk, bison, cattle, horses, sheep 
and moose after storage at 4 ' C for 7 to 11 
days. It persisted from 2. 5 months in the 
bison samples to more than 18 to 24 months 
in the elk and cattle samples. It failed to 
survive in soil or in soil mixed with boiled 
feces, nor could it be found in soil samples 
taken from areas where elk, sheep or 
horses were present. 

The trophozoites of C. subtilis are 7 
to 20 (i long. They are usually ovoid, but 
can change from spindle-shaped to almost 
round. The flagellum is 1 to 2 times the 
length of the body. When the animal 
swims straight, only the tip of the flagellum 
moves; the flagellum is sometimes used 
like a highly flexible probe. The cysts are 
ovoid or spherical and 7 to 8)j. long. They 
have a thin wall and clear contents with a 
single vesicular nucleus. 

Reichenow (1952) and Grasse' (1952) 
considered that Copromonas subtilis is a 
synonym of Scytomoiias piisilla Stein, 1878, 
which was incompletely described by Stein. 



FAMILY ASTASilDAE 

Members of this family have a single 
flagellum. They lack chromatophores or 
a stigma. 



Genus COPROMONAS Dobell, 1908 

The body is elongate ovoid, with an 
elongate reservoir at the anterior end into 
which a contractile vacuole discharges. 
The single flagellum arises from a bleph- 
aroplast at the base of the reservoir. The 



ORDER PHYTOMONADORIDA 

In this order a single large green 
chromatophore is typical. The stored re- 
serves are starch and sometimes lipids. 
No members of this order are parasites of 
domestic animals or man, but one species 
deserves mention. 

Polytoma uvellaEhrenberg, 1838 
occurs in infusions and stagnant water, 
and has been found in bull sheath washings 
submitted for Tritrichomonas foetus 



OTHER FLAGELLATES 



127 



diagnosis (Morgan and Hawkins, 1952). 
Its body is ovoid to piriform, 15 to 30 by 
9 to 20 |i, without chromatophores and 
with numerous starch granules in the 
posterior part of the body. A red or pink 
stigma may or may not be present. There 
are 2 anterior flagella of equal length. 

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The amoebae belong to the class Sar- 
codasida. Members of this class move by 
means of pseudopods. They have no cilia 
and, except in rare instances, no flagella. 
The group is named for sarcode, a term 
introduced by Dujardin for what was later 
called protoplasm. Most sarcodasids are 
holozoic, ingesting their prey by means 
of their pseudopods. Their cytoplasm is 
usually divided into endoplasm, containing 
the food vacuoles, nucleus, etc., and rel- 
atively clear ectoplasm. The fresh water 
forms contain one or more contractile 
vacuoles; these are absent in the salt water 
and parasitic species. With a few excep- 
tions, reproduction is asexual, by binary 
fission or rarely by multiple fission, by 
budding or by plasmotomy. Most species 
form cysts. 

The Sarcodasida originated from the 
Mastigasida. The group did not arise 
from a single progenitor, but is polyphyle- 
tic. One line, for example, passes from 
Tetramitus thru Naegleria to Vahlkampfia. 
In Tetramitus, which is usually classified 
among the flagellates, the life cycle in- 
cludes flagellate and amoeboid stages, 
and the flagellate stage has a permanent 
cytostome. In Naegleria, which is usually 
classified among the amoebae, the life 
cycle also includes flagellate and amoeboid 
stages, but there is no permanent cyto- 
stome. In Vahlkampfia, there is no fla- 
gellate stage, but the amoebae are very 
similar to those of Naegleria. Another 
line passes from the amoeboid flagellate, 
Histomonas, to the very similar but non- 
flagellate amoeba, Dientamoeba. 

Only a few of the Sarcodasida are 
parasitic. The free-living forms include 
the most beautiful protozoa of all, the 
pelagic Radiolaria with their delicate, 
latticework siliceous skeletons. One 
group of Radiolaria has skeletons of stron- 
tium sulfate- -perhaps some day proto- 
zoologists will be asked to develop ways 
of using them to eliminate strontium 90 
pollution. Another marine group, the 
Foraminifera, has calcareous shells. 



Chapter 7 



THE 
AMOEBAE 



129 - 



130 



THE AMOEBAE 



Their skeletons form our chalk, and they 
and the Radiolaria are of great geological 
interest. They are used, too, as indica- 
tors in oil well drilling. More species of 
Foraminifera have probably been named 
than of all the other protozoa put together; 
493 new species and 53 new genera of 
Foraminifera were listed in the Zoological 
Record for 1956, and of these, 470 species 
and 48 genera were fossil. In contrast, 57 
new species and 4 new genera of parasitic 
protozoa were listed. And this was not an 
exceptional year. 



ORDER AMOEBORIDA 

Members of this order have lobopodia 
and are naked, without a test. All of the 
parasitic and all but one of the coprophilic 
Sarcodasida are found in this order. 



FAMILY NAEGLERIIDAE 

This family is transitional between 
the Mastigasida and the Sarcodasida. 
Both amoeboid and flagellate stages occur 
in its life cycle. 



ORDER TESTACEORIDA 

Members of this order have a single- 
chambered shell or test. 



FAMILY ARCELLIDAE 

The test is simple and membranous, 
without foreign bodies, platelets or scales. 
The pseudopods are filose or simply 
branched and do not anastomose. There 
are many genera and species of free-living 
protozoa in this family. They are found 
commonly in fresh water, swamps, etc. 
One species is coprophilic. 



Genus CHLAMYDOPHRYS 
Cienkowski, 1876 

The test is rigid and circular in cross 
section. The nucleus is vesicular, with a 
prominent endosome. The cytoplasm is 
differentiated into distinct zones, and re- 
fractile waste granules are present in it. 
The pseudopods are branching. 

Chlamydophrys slercorea Cienkowski, 
1876 has an oval, white porcelaneous, thin, 
smooth shell open at the pointed end. It 
measures about 20 by 14 /i. The pseudo- 
pods are filose. Somewhat smaller naked 
amoebae may also be seen. The cysts are 
uninucleate, 12 to l'b\i in diameter, with 
thick, irregular, brownish walls. Multi- 
plication is by budding. C. slercorea is 
coprophilic and may also be found in fresh 
water. 



Genus NAEGLERIA Alexeieff, 
1912 emend. Calkins, 1913 

The flagellate stage has 2 flagella. 
The amoeboid stage has lobopodia and re- 
sembles Vahlkanipfia. The nucleus is 
vesicular, with a large endosome. The 
contractile vacuole is conspicuous. The 
cysts are uninucleate. Naegleria lives on 
bacteria and is free-living in stagnant 
water or coprophilic. 

Naegleria gruberi (Schardinger) (syn. , 
Dimasligamoeba gruberi) is found in stag- 
nant water and is also coprophilic. The 
active amoebae are 10 to 36 by 8 to 18 p. 
and have a single vesicular nucleus 3 to 
4fj, in diameter. The nucleus has a cen- 
tral endosome and sparse granules of 
peripheral chromatin. The flagellate stage 
is 18 by 9 (i, ovoid, and has 2 equal anter- 
ior flagella. It can be produced from the 
amoeboid stage by flooding the culture with 
distilled water and exposing it to air. The 
cysts are spherical, 8 to 12 /i in diameter, 
translucent, with a single nucleus and sev- 
eral large spherical chromatoid bodies 
when first formed. The cyst wall is double, 
and the outer wall is perforated by 3 to 8 
pores. 



Genus TRIMASTIGAMOEBA 
Whitmore, 1911 

The nucleus is vesicular, with a large 
endosome. The flagellate stage has 3 fla- 
gella (4 according to Bovee, 1959) and the 



THE AMOEBAE 



131 



amoeboid stage is relatively small. The 
cysts are uninucleate, with a smooth wall. 

Triiuastigamoeba philippinensis Whit- 
more, 1911 was first found in human 
feces. Bovee (1959) rediscovered it in 
sewage-seepage into a spring in Florida 
and redescribed it. According to Whit- 
more (1911), the flagellate stage has 3 
(occasionally 2 or 4) anterior flagella and 
measures 16 to 22 by 6 to 8 j:i . Bovee, 
however, found that there are actually 4 
anterior flagella which arise in pairs from 
2 basal granules adjacent to the nucleus. 
The flagella lie in an anterior, gullet-like, 
cylindrical invagination and extend 20 to 
25 [x beyond it. According to Bovee, the 
fully formed flagellate stage is 17 to 20 |i 
long, its larger rear end is 6. 5 to 7. 5 ji 
in diameter, the narrower anterior end 
is 4. 5 to 5. 5|U in diameter and the anter- 
ior pocket is 1 ji deep. 

The amoeboid stage was said by 
Whitmore (1911) to be 16 to 18 ii in diam- 
eter. Bovee (1959) said that it is 12 to 
18fi in diameter when at rest and 30 to 
40 (i long and 14 to 20 )i wide during rapid 
locomotion. It moves quickly by means 
of rapidly-extruded eruptive waves at its 
frontal margin. It feeds principally on 
bacteria and has a contractile vacuole 
which is formed by the union of several 
small vacuoles in about 2 minutes. The 
cysts are oval to subspherical. Whitmore 
(1911) gave their dimensions as 13 to 14 
by 8 to 12 fi. 



FAMILY AMOEBIDAE 

Members of this family are free-living 
or coprophilic. They have no flagellate 
phase. This family contains, besides 
Amoeba and a number of other free-living 
genera, several coprophilic species and 
one which can produce disease with a little 
human help. 



Genus ACANTHAMOEBA 
Volkonsky, 1931 

These are relatively small amoebae 
without well developed ectoplasm. The 
nucleus is vesicular, with a large endo- 



some. During mitosis, the nuclear mem- 
brane disappears at prophase. The mi- 
totic figure at the end of metaphase is a 
straight or concave spindle with sharply 
pointed poles. The cysts are angular and 
polyhedric, with 2 membranes, the outer 
one being highly wrinkled and mammillated. 

Acanthamoeba hyalina (Dobell and 
O'Connor, 1921) Volkonsky, 1931 (syn. , 
Hartnianiiella hyalina) is a common copro- 
philic form. It occurs in soil and fresh 
water and is easily cultivated from old 
human and animal feces. Its trophozoites 
are 9 to 17 fi in diameter when rounded. 
It has a single contractile vacuole and a 
single vesicular nucleus with a central 
endosome and peripheral chromatin. The 
cysts are spherical, 10 to 15fi in diam- 
eter, with a thin, smooth inner wail and 
a thick, wrinkled, brownish outer wall. 

Walker (1908) described an amoeba 
from the intestinal tract of the turkey in 
Massachusetts under the name A»ieba 
gallopavoiiis which Chatton (1953) listed 
as Acanthamoeba gallopavonis Walker. 
It had angular cysts and may be synony- 
mous with A. hyalina. 

Acanthamoeba has occasionally been 
encountered as a contaminant of tissue 
cultures and, because of its pathogenicity 
on injection and the resistance of its cysts 
to virucidal agents, it is a potential haz- 
ard in vaccines prepared from viruses 
grown in tissue culture. 

Jahnes, Fullmer, and Li (1957) and 
Culbertson, Smith and Minner (1958) 
isolated an Acanthamoeba sp. from tissue 
cultures of trypsinized monkey kidney 
cells. The latter first recognized the 
amoebae in the lesions of monkeys which 
had died following inoculation of tissue 
culture fluid thought to contain an unknown 
virus but later shown to contain only 
Acanthamoeba. Following intracerebral 
and intraspinal inoculation into cortison- 
ized monkeys, the amoebae caused ex- 
tensive choriomeningitis, destructive 
encephalomyelitis and death in 4 to 7 days. 
Following intracerebral inoculation into 
mice, they caused destructive encepha- 
litis and death in 3 to 4 days. Following 
intranasal instillation into mice, they 



132 



THE AMOEBAE 



produced ulcers in the nasal mucous mem- 
brane and invaded the adjacent base of the 
skull, involving the frontal lobes of the 
brain and causing death in about 4 days. 
Following intravenous inoculation into 
mice, they caused perivascular granulo- 
matous lesions in the lungs. These were 
associated with severe pneumonia, exten- 
sive fibrinopurulent exudate containing 
polymorphonuclear leucocytes and mono- 
cytes, hemorrhage, and invasion of the 
pulmonary veins followed by the formation 
of thrombi containing the amoebae. 

McCowen and Galloway (1959) also 
isolated Acanlhamoeba sp. from tissue 
cultures of trypsinized monkey kidney 
cells. They studied the pathogenicity for 
mice of this strain and of others isolated 
from the same source. The average sur- 
vival time of intracerebrally inoculated 
mice was approximately 5 days. Cysts 
remained virulent for mice after storage 
at -67 °C for 15 months. 



Genus SAPPINIA Dangeard, 1896 

In this genus the trophozoites have 2 
closely associated nuclei with large endo- 
somes. The cysts are binucleate also. 

Sappinia diploidea (Hartmann and 
Nagler, 1908) Alexeieff, 1912 is a com- 
mon coprophilic amoeba in the feces of 
man and other animals. Its trophozoites 
are 10 to 60 fi long, with a thick, smooth, 
hyaline pellicle; according to Noble (1958), 
the ectoplasm has fine lines sometimes 
resembling wrinkles in cellophane. Two 
nuclei are present, usually pressed 
tightly together. Each nucleus has a 
large endosome and frequently a crescentic 
mass of granules between the endosome 
and the nuclear membrane. The cytoplasm 
is usually filled with many food vacuoles. 
A contractile vacuole is present, formed 
by the enlargement and coalescence of 
smaller vacuoles. A single, clear, broad 
pseudopod is characteristic, altho occa- 
sionally many pseudopods may be present. 
Cytoplasmic granules and food vacuoles 
are concentrated between the pseudopod 
and the rest of the body. Movement is 
quite sluggish. The cytoplasmic granules 



usually move rapidly. The cysts are typ- 
ically binucleate, 12 to 18/i or more in 
diameter, with thick, uniform walls. The 
cysts are formed from 2 individuals which 
come together and secrete a common cyst 
wall; their nuclei fuse so that each one has 
a single nucleus, their cytoplasm fuses, 
each nucleus gives off reduction bodies, 
and the 2 remaining nuclei come into con- 
tact to make the cyst binucleate. 

Noble (1958) found that 6'. diploidea 
appeared in fecal samples from Wyoming 
elk and bison (but not from cattle, horses 
and sheep) after storage at 4° C for a few 
days to a few weeks. It failed to survive 
in soil or in soil mixed with boiled feces, 
nor could it be found in soil samples taken 
from areas where elk, sheep or horses 
were present. 

S. diploidea is readily cultivated. 
Noble (1958), for example, cultivated it 
both at 4^^ C and at room temperature on 
the surface of agar plates containing 1. 5% 
agar, 0. 05% yeast extract and 0. 05% pep- 
tone. The cultures held at room temper- 
ature became moldy after 6 weeks. Sap- 
pinia was present for 2 to 3 weeks in the 
cultures at 4° C. 

Genus VAHLK4MPF/A Chatton and 

Lalung-Bonnaire, 1912 emend. 

Calkins, 1913 

These are small amoebae with a nu- 
cleus containing a large endosome and 
peripheral chromatin, with polar caps 
during nuclear division. The trophozoites 
have a single broad pseudopod and move 
like a slug. The cysts have a perforated 
wall. The nucleus of this genus closely 
resembles that of Naegleria, but the latter 
has both flagellate and amoeboid stages. 
A number of species have been described 
from fresh water, old feces, lower verte- 
brates and invertebrates, but the taxonomy, 
nomenclature and validity of some of them 
are not certain. 

Vahlkampfia punctata (Dangeard, 1910) 
Chatton and Lalung-Bonnaire, 1912 has 
been found in human feces. Its cysts have 
punctate markings. 



THE AMOEBAE 



133 



Vahlkanipfia lobospinosa (Craig, 1912) 
Craig, 1913 is another coprophilic species. 
Becker and Talbott (1927) found it in the 
rumen of a cow in Iowa. Its trophozoites 
are 10 to 24 ju long. Its cysts have 1 or 2 
nuclei and are 7 to 11 (i in diameter. 

Noble (1958) found that Vahlkampfia 
sp. appeared in fecal samples from Wy- 
oming elk, bison, cattle, horses, sheep, 
moose and marmots after storage at 4^ C 
for a few days to a few weeks. The proto- 
zoa persisted for several months. They 
failed to survive in soil, nor were they 
present in soil samples taken from areas 
where elk, sheep or horses were present. 
The trophozoites were 20 to 40 p. in diam- 
eter, with finely granular cytoplasm 
filled with food vacuoles and other parti- 
cles. A contractile vacuole was present. 
The pseudopods were broad, usually slug- 
gish but sometimes formed almost explo- 
sively; often there was only a single, 
large pseudopod. The nucleus was ves- 
icular, with a large, central endosome 
occasionally appearing to be composed of 
several closely packed granules. Peri- 
pheral chromatin was rarely present, 
altho a ring of minute granules was often 
present just within the nuclear membrane. 
The cysts were 8 to 15 in in diameter and 
almost exclusively mononucleate. The 
nucleus was different from that of the 
trophozoite. Its central endosome was 
usually smaller than in the trophozoite 
and often composed of several granules, 
and the peripheral chromatin was distinct, 
arranged in irregular clumps and often 
forming a crescent. A large vacuole and 
irregular chromatoid bodies, many of 
which resembled those of Entamoeba his- 
tolytica, were present. Noble believed 
that many of the cysts found in animal 
and human feces and described as those 
of Entamoeba are actually of the Vahl- 
kampfia type. 

Noble (1958) cultured this species at 
both 4° C and room temperature on the 
surface of agar- plates containing 1 . 5% 
agar, 0. 05% yeast extract and 0. 05% pep- 
tone. The cultures held at room temper- 
ature became moldy after 6 weeks and 
were discarded, but Vahlkampfia was 
present for 3 months without attention in 
those held at 4° C. 



FAMILY ENDAMOEBIDAE 

Members of this family are parasitic 
in the digestive tract of vertebrates and 
invertebrates. The genera are differen- 
tiated on the basis of nuclear morphology. 
Four genera contain parasites of domestic 
animals and man, but only two of these 
contain pathogenic species. However, it 
is important to be able to identify the var- 
ious species in order to know whether an 
infection with a pathogenic one is present 
or not. 



Genus ENTAMOEBA Casagrandi and 
Barbagallo, 1895 

The nucleus is vesicular, with a com- 
paratively small endosome located at or 
near its center, with or without periendo- 
somal granules around the endosome, and 
with a varying number of granules around 
the periphery of the nucleus. Cysts are 
formed; they contain 1 to 8 nuclei and may 
or may not contain chromatoid bodies 
(rod-like bodies which stain with hema- 
toxylin and which are absorbed and dis- 
appear as the cysts mature). This genus 
occurs in both vertebrates and inverte- 
brates. 

The name of this genus was the sub- 
ject of one of the most famous taxonomic 
controversies in protozoology (Dobell, 
1938; Kirby, 1945). The genus Endamoeba 
was established by Leidy in 1879 for an 
amoeba of the cockroach, Endamoebae 
blattae. In 1895 and in ignorance of this 
name, Casagrandi and Barbagallo intro- 
duced the name Entamoeba for the human 
amoeba, E. coll. The nuclei of these two 
forms are very different, that of the cock- 
roach species lacking a central endosome. 
Since the appearance of the nucleus is the 
most important differentiating character 
between genera in this family, it is ob- 
vious to a protozoologist that these forms 
belong in different genera. However, the 
first syllable of their names is derived 
from the same Greek root. Hence the In- 
ternational Commission of Zoological 
Nomenclature was asked to decide whether 
the name that had been given second 
should be changed to something else (i.e. , 
whether the two names were homonyms). 



134 



THE AMOEBAE 



The Commission, which had no protozo- 
ologists among its members, went beyond 
this, and decided that £^^/rt»/0(;^/>f/ was a 
synonym of EiidcDiiueba and that both pro- 
tozoa belonged to the same genus. Altho 
the latter is obviously not true, this dic- 
tum was accepted by many protozoologists. 
Finally, after much agitation and several 
long, involved papers by various author- 
ities, the International Commission finally 
reversed itself, and Enlanioeha is now 
universally recognized as the correct 
name for the species occurring in verte- 
brates. 

The nomenclature and taxonomy of the 
species of Eiitamoeha are about as con- 
fused as it is possible to make them. 
Some of the problems are explained below, 
but puzzle addicts are referred to the 
cited papers for the details. 

Members of the genus found in domes- 
tic animals and man can be divided into 4 
groups on the basis of trophozoite and 
cyst morphology. A fifth group includes 
species about which insufficient morpho- 
logical information is available to deter- 
mine which of the other groups they belong 
in. Most of the species within each group 
are morphologically indistinguishable; 
they are differentiated on the basis of size, 
hosts, pathogenicity, etc. Criteria of 
this type are given different weights by 
different taxonomists, and this fact com- 
bined with a lack of cross-transmission 
studies for many species accounts for 
some of the confusion. More is due to 
the fact that the original descriptions of 
some of the species were so poor as to 
make it difficult or impossible to be sure 
what forms the authors were dealing with. 

The groups of Entamoeba will be des- 
cribed first, and then the individual spe- 
cies. 

1. fflSTOLYTICA GROUP. The nucleus 
has a small, central endosome, a 
ring of small peripheral granules and 
a few scattered chromatin granules 
between them. The cysts have 4 nuclei 
when mature, and their chromatoid 
bodies are rods with rounded ends. 
Glycogen vacuoles, when present in 



the cyst, are usually diffuse and ill- 
defined. 

Entamoeba histolytica of man, other 
primates, the dog, cat and rarely 
the pig. 

E)itai)ioeba harliuauiii of man and pre- 
sumably also of the other hosts of 
E. histolytica. 

Entamoeba eqni of the horse. 

Entanioeba anal is of the duck. 

Entamoeba moshkovskii of sewage. 

2. COLI GROUP. The nucleus has a 
somewhat larger, eccentric endosome 
than that of the histolytica group and 
has a ring of coarse peripheral gran- 
ules and some scattered chromatin 
granules between them. The cysts 
have 8 nuclei when mature, and their 
chromatoid bodies are splinter-like. 
Glycogen vacuoles, when present in 
the cyst, may be fairly well defined. 

Entamoeba coli of man, other pri- 
mates, the dog and possibly the pig. 

Entamoeba wenyoni of the goat. 

E)itamoeba nniris of mice, rats, ham- 
sters, and other rodents. 

Entamoeba caviae of the guinea pig. 

Entamoeba cunicnli of rabbits. 

Entamoeba galli)iaynm of the chicken, 
turkey, guinea fowl, duck, and goose. 

3. BO VIS GROUP. The endosome of the 
nucleus varies in size; it may be as 
small as that of the histolytica group, 
but is generally larger than that of the 
coli group. The ring of peripheral 
granules in the nucleus may be fine or 
coarse, evenly or irregularly distrib- 
uted. Periendosomal granules may be 
present. The cysts have 1 nucleus 
when mature, and their chromatoid 
bodies are either rods with rounded 
ends or less often splinter-like. Gly- 
cogen granules, when present in the 
cyst, are usually fairly well defined. 

Entamoeba bovis of cattle. 
Entamoeba ovis of sheep and goats. 
Entamoeba dilimani of goats. 
Entanioeba siiis of the pig and perhaps 

man. 
Entamoeba bubalis of the carabao. 
E)ita»ioeba cliattoni of monkeys and 

probably man. 



THE AMOEBAE 



135 



4. GINGIVALIS GROUP. The nucleus 
has a small, central endosome and a 
ring of small peripheral granules. 
There are no cysts. Members of this 
group are found in the mouth. 

Entamoeba gingivalis of man, other 

primates, the dog and cat. 
E)ita>noeba equibuccalis of the horse. 
Entamoeba suigingivalis of the pig. 

5. INSUFFICIENTLY KNOWN SPECIES. 
This group includes Entamoeba gedo- 
etsti of the horse and E. caudata of 
the dog. The nucleus of E. caudata 
resembles that of E. coli, while the 
nucleus of E. caudata resembles that 
of E. histolytica. The cysts of these 
species are unknown. 

The only species of Entamoeba patho- 
genic for mammals is E. histolytica. The 
fact that it has been recorded in an aver- 
age of about 18% of the people examined in 
various surveys thruout the world and yet 
only about 1/5 of them have signs or symp- 
toms of disease has puzzled epidemiolo- 
gists for many years. Two other facts 
contribute to the problem. One is that 
there are two different sizes of these 
amoebae, the smaller of which is not asso- 
ciated with disease; it has been encountered 
in about 1/3 of the people in these surveys. 
The other is that amoebic dysentery occurs 
mostly in the tropics. Autochthonous cases 
occur so seldom in western Europe that 
many European parasitologists believe that 
cases of amoebic dysentery which occur in 
their countries have been imported from 
the tropics either directly or thru contact 
with infected persons. These parasitolo- 
gists have not had the benefit of the Amer- 
ican experience with the disease. There 
is no question that indigenous cases occur 
in the temperate ZQne of this country. 

Several hypotheses have been advanced 
in explanation (see Hoare, 1958). The 
first theory, suggested about 1913 and still 
held by perhaps the majority of parasitolo- 
gists, is based on an unwillingness to 
assign separate specific names to protozoa 
which differ only in size and pathogenicity. 
According to this view, the species Enta- 
moeba histolytica is composed of a small 



race and a large race. The small race is 
not pathogenic, while the large race may 
or may not be. In its virulent phase the 
latter invades the tissues; the tropho- 
zoites of this phase are large- -the "magna" 
form. In its commensal phase it remains 
in the lumen of the intestine, feeding on 
bacteria and saprozoically. The tropho- 
zoites of this phase are small--the "minuta" 
form. Under proper conditions, this non- 
pathogenic "minuta" form can invade the 
intestinal mucosa and turn into the patho- 
genic "magna" form. The trophozoites of 
the small race of E. histolytica are usually 
12 to 15 |U in diameter and the cysts are 5 
to 9|Li in diameter with a mean of 7 to 8/1. 
The trophozoites of the "magna" form of 
the large race are 20 to 30 jj, and those of 
the "minuta" form 12 to 15 |U. in diameter. 
However, the cysts of both the "magna" 
and "minuta" forms are the same size, 10 
to 20 jj, in diameter, with a mean of about 
12^. 

The second theory was proposed by 
Brumpt in 1925. He recognized 3 species. 
He called the small, non- pathogenic race 
Enta?noeba liartmanni, and divided the 
large race into 2 species. Of these, E. 
dispar is non- pathogenic and occurs thru- 
out the world, while E. dysenteriae is 
pathogenic, altho it may cause no apparent 
symptoms in carriers, and occurs only in 
warm and hot countries. 

The third theory was formulated for- 
mally by Hoare in 1957. It calls the small, 
non- pathogenic race E. hartmanni, but re- 
tains the name E. histolytica for the large 
race of the first theory. It then divides E. 
histolytica into an avirulent race (corres- 
ponding to Brumpt' s E. dispar) and a viru- 
lent race (corresponding to Brumpt's E. 
dysenteriae) which may invade the gut wall 
or live in the lumen without causing symp- 
toms. 

This view has a great deal to recom- 
mend it. By giving the non- pathogenic 
small form a separate name, it makes it 
easier for the physician to interpret lab- 
oratory reports and prevents faulty diag- 
noses and needless treatment. However, 
the question whether there actually are 
completely non- pathogenic strains of E. 



136 



THE AMOEBAE 



histolytica (sensu stricto) which cannot be 
induced to become pathogenic has not yet 
been answered satisfactorily. Concomi- 
tant bacteria, nutritional deficiencies and 
other factors affect the pathogenicity of 
the amoebae. Indeed, Phillips el al. 
(1955) found it impossible to infect bac- 
teria-free guinea pigs with E. histolytica 
at all, altho normal guinea pigs or those 
infected with Escherichia coli or Aero- 
bacter aerogenes could be readily infected 
and subsequently developed intestinal le- 
sions. 

Some of the amoebae reported as E. 
histolytica from domestic animals may 
well have been actually E. hartnianni. but 
unless they were specifically described as 
having small cysts, it is impossible to 
know which they were. 

The above discussion has to do pri- 
marily with a matter of nomenclature. In 
addition, another species morphologically 
identical with E. histolytica has been 
found in sewage. This is E. moshkovskii 
It has not been found in fresh feces, but 
nevertheless its existence must be taken 
into consideration in diagnosis. It is not 
infective for rats, kittens, guinea pigs or 
frog or salamander larvae and its optimum 
temperature is about 24° C, altho it will 
grow poorly at 37° C. 

Before beginning a systematic account 
of the species of Entamoeba, a word is in 
order regarding the bovis group. All of 
these look alike, with minor differences 
which may not be of taxonomic significance. 
Different names have been given to the 
forms in different hosts, but no cross- 
transmission studies have been attempted, 
and it is quite likely that when they are, 
some of these forms will be found to be 
synonyms. In this case. Entamoeba bovis 
will have precedence over the other names. 

The name Entamoeba polecki has 
been used for members of the bovis group 
from the pig and goat, but it is a nomeu 
nudum. Prowazek's (1912) original des- 
cription and figures of it are so poor that 
it is impossible to know whether he was 
dealing with a member of the genus Enta- 
moeba at all. 



Noble and Noble (1952) and Hoare 
(1959) have reviewed the amoebae of do- 
mestic animals. 



ENTAMOEBA IIISTOL YTICA 
SCHAUDINN, 1903 

Synonyms : Amoeba coli, Amoeba 
dysenleriae, Entamoeba tetragena. Enta- 
moeba dispar. Entamoeba venaticum. 

Disease : Amoebic dysentery. 

Hosts : Man, orang-utan, gorilla, 
chimpanzee, gibbon, many species of 
macaques, baboons, spider monkeys and 
other monkeys, dog, cat, pig, rat, pos- 
sibly cattle. The rat, mouse, guinea pig 
and rabbit are often infected experimentally. 

Location : Large intestine, some- 
times liver, occasionally lungs, and rarely 
other organs including the brain, spleen, 
etc. 

Geographic Distribution : Worldwide. 
Maps of the world distribution of amoebic 
dysentery and E. Jiistolytica, together 
with climatological and other information, 
were published by Piekarski and Westphal 
(1952) and Westphal (1955). 

Prevalence : E. histolytica is most 
important as a parasite of man. It also 
occurs in monkeys and higher primates. 
According to Belding (1952), it was found 
in an average of 17.6% of 42,713 persons 
(range, 0.8 to 50%) in 37 surveys thruout 
the world from 1941 to 1948. In 10 surveys 
of 10,867 persons in the United States from 
1941 to 1948, it was found in an average of 
13.6% (range, 0.8 to 38%). 

According to Benson, Fremming and 
Young (1955), it has given considerable 
trouble in their chimpanzee colony at the 
Univ. of Texas. 

Sporadic cases of amoebic dysentery 
have been reported in dogs; these animals 
are generally considered to have acquired 
their infections from human contacts. 
Kartulis (1891, 1913) found £. histolytica 
causing dysentery in 3 dogs in Egypt; in 



THE AMOEBAE 



137 








Q 



Fig. 20. Species of Entamoeba. A. E. hislolylica trophozoite. B. E. histolytica cyst. 
C. E. hartmanni trophozoite. D. E. Iiartmanni cyst. E. E. coli cyst. 
F. E. coli trophozoite. G. E. gallinarum trophozoite. H. E. gallinarum 
cyst. I. E. bovis trophozoite. J. E. bovis cyst. K. E. ovis trophozoite. 
L. E. ovis cyst. M. E. dilimani trophozoite. N. E. dilimani cyst. 
O. E. suis, large trophozoite. P. E. suis, small trophozoite. Q. E. suis, 
large cyst. R. E. snis, small cyst. X 1700. (From Hoare, 1959, in Veter- 
inary Reviews and Annotations) 



138 



THE AMOEBAE 



one of these, a liver abscess was also 
present. Darling (1915) reported a fatal 
infection in a dog in Panama. Ware (1916) 
reported an outbreak in a pack of foxhounds 
in the Nilgiri Hills of India, Boyd (1931) 
reported an outbreak in another pack of 
hounds in India, and more recently Gana- 
pathy and Alwar (1957) reported 2 cases of 
amoebic dysentery in dogs in India. 
Fischer (1918) reported a case of amoebic 
dysentery in a dog in China, Bauche and 
Motais (1920) reported one in Indochina, 
and Morcos (1936) found 5 cases in Egypt. 
In the United States, Faust (1930) found 2 
dogs in New Orleans with amoebic dysen- 
tery, Andrews (1932) found £. histolytica 
in the feces of a diarrheic dog in Baltimore, 
and Thorson, Seibold and Bailey (1956) re- 
ported a case of systemic amoebosis in a 
puppy which also had distemper. E. his- 
tolytica was found in large numbers in the 
lungs and amoebae were also seen in the 
liver, kidneys and spleen. 

In surveys of presumably normal dogs, 
Kubo (1936) found E. histolytica in 8% of 
85 street dogs in Mukden, China, while 
Yamane (1938) found it in 3% of 60 street 
dogs from the same city. Chary et al. 
(1954) stated that amoebic dysentery occurs 
frequently in dogs in Indochina. Eyles 
et al. (1954) found E. histolytica in 8. 4% 
of 143 dogs in the Memphis, Tennessee dog 
pound. The protozoa were so scarce that 
cultural methods were required to reveal 
them. This finding suggests that amoebic 
dysentery may be more common in dogs 
than is generally believed. 

Natural E. histolytica infections are 
apparently rare in cats, but Kessel (1928) 
found the protozoon in 3 of 150 kittens in 
China. 

E. histolytica is rare in swine. Frye 
and Meleney (1932) found it in 1 of 127 
pigs which they examined in Tennessee; 
this animal came from a farm where an 
infected woman lived. 

There are 2 reports of what may have 
been E. histolytica in cattle. Walkiers 
(1930) saw it in the feces of dysenteric 
cattle in the Belgian Congo. Thiery and 
Morel (1956) found it in the lungs of a 



young zebu in Dakar which was slaughtered 
on account of generalized streptothricosis. 

Natural infections in rats have been 
reported by a number of workers. Chiang 
(1925) found E. histolytica in 7 laboratory 
rats. Brug (1919) found it in 2 of 50 wild 
rats in Batavia, Nagahana (1934) found it 
in 3 of 274 wild rats in Mukden, China, 
and Epshtein and Avakian (1937) found it in 
7 of 515 wild Rattiis norvegicus in Moscow. 
In the United States, Lynch (1915) saw it in 
a wild rat, Tsuchiya and Rector (1936) 
found it in 2 of 100 wild rats in St. Louis, 
and Andrews and White (1936) found it in 
28 (1.1%) of 2515 wild rats in Baltimore. 

Morphology : The trophozoites of the 
large, pathogenic race of E. histolytica 
are 20 to 30 ji and those of the small race 
are 12 to 15 ji in diameter. They have a 
thick, clear layer of ectoplasm and gran- 
ular endoplasm. They move rapidly when 
warm, usually moving forward in a straight 
line with a single clear pseudopod at the 
anterior end. When the feces have cooled, 
the amoebae stay in one place and throw 
out large, clear pseudopods from various 
parts of their body. The trophozoites often 
ingest erythrocytes, a feature which differ- 
entiates them from those of other amoebae. 
The nucleus is indistinct in living amoebae. 
When stained with hematoxylin, it has a 
small, central endosome, a ring of small 
peripheral granules and a few scattered 
chromatin granules in between. The cysts 
of both the large and small races are 10 to 
20jLt (average, 12 /i ) in diameter. They 
have 4 nuclei when mature and often con- 
tain rod-like chromatoid bodies with rounded 
ends. Diffuse glycogen is present in the 
young cysts. 

Life cycle : E. histolytica multiplies 
in the trophozoite stage by binary fission. 
It has 6 chromosomes. Before encysting, 
the amoebae round up, became smaller 
and eliminate their food vacuoles. They 
lay down a cyst wall, and the nucleus 
divides into 2 and then into 4 small nuclei. 
After the 4-nucleate amoebae emerge from 
the cyst, both the nuclei and cytoplasm 
divide so that 8 small amoebulae result. 
Each then grows into a normal tropho- 
zoite. 



THE AMOEBAE 



139 



Pathogenesis : As mentioned above, 
only the large forms of E. histolytica are 
generally considered pathogenic, altho 
there are reports of mild disease and 
slight lesions associated with the small 
form (Shaffer et al.^ 1958). They may 
cause diarrhea or dysentery, and may 
invade the wall of the cecum and colon, 
forming ragged, undermining or flask- 
shaped ulcers which may be pinpoint in 
size or may become large and confluent. 
The amoebae invade the mucosa at first 
and multiply to form small colonies. These 
colonies then extend into the submucosa and 
even into the muscularis. In the absence of 
bacterial invasion, there is little tissue re- 
action, but in complicated infections there 
is hyperemia, inflammation and infiltra- 
tion with neutrophiles. 

Some of the amoebae may pass into 
the lymphatics or even the mesenteric 
venules. Those entering the hepatic portal 
system pass to the liver, where they may 
cause abscesses. Those which enter the 
lymph ducts are generally filtered out by 
the lymph nodes. Abscesses may be 
formed in various other organs, including 
the lungs, brain, etc. , depending on the 
host's resistance. 

The relation of parasite strain to 
pathogenicity has already been mentioned. 
The species of concomitant bacteria pres- 
ent may also affect the amoeba's pathoge- 
nicity, as may the nutritional status of the 
host and other environmental factors. 
Dysentery is much more common in the 
tropics than in the temperate zone. 

In most cases, E. histolytica causes 
minor symptoms or none at all. Infections 
may last 40 years or even more. There 
may be recurring mild to severe gastro- 
intestinal symptoms, including intermit- 
tent diarrhea, bowel irregularity, abdom- 
inal pain, nausea and flatulence. Some- 
times affected persons tire easily, have 
headaches or feel nervous. Appendicitis 
or symptoms resembling it may occur. 
These symptoms generally clear up after 
treatment. 

In acute amoebic dysentery, the feces 
consist almost entirely of blood and mucus 



filled with amoebae and blood cells. The 
patient is wracked by waves of severe 
abdominal pain and spends a large part of 
his time on the stool, straining and passing 
blood and mucus every few minutes. In 
contrast to bacillary dysentery, there is no 
fever in uncomplicated cases. 

Epidemiology : As mentioned above, 
E. histolytica is primarily a parasite of 
primates, and man is the reservoir of in- 
fection for his domestic animals. This is 
one of the few zoonoses which man gives 
to his associated animals in return for the 
many which he receives from them. 

Infection is due to ingestion of cysts. 
Since trophozoites alone are passed by 
dysenteric individuals, these are not im- 
portant sources of infection, while cyst- 
producing chronic cases and carriers are. 

The cysts are relatively resistant. 
They are not affected by water chlorina- 
tion, but can be removed by sand filtration. 
They survive for at least 8 days in soil at 
28 to 34° C (Beaver and Deschamps, 1949), 
but live only an hour at 46 to 47° C and 
less than a minute at 52° C (Jones and 
Newton, 1950). They survive longest at 
refrigerator temperatures (40 days at 2 to 
6° C according to Simitch, Petrovitch and 
Chibalitch, 1954; 62. 5 days at 0° C accord- 
ing to Chang, 1955). They will not excyst 
after 24 hours at temperatures of -15° C 
or lower (Halpern and Dolkart, 1954), and 
die in 7. 5 hours or less in the deep freezer 
at -28° C (Chang, 1955). 

The cysts are usually transmitted with 
food or water. Raw vegetables may be a 
source of infection. Flies may transmit 
the cysts also. Pipkin (1949) was able to 
cultivate cysts from the vomitus of filth 
flies {Musca domestica, Lucilia pallescens, 
Cochliomyia macellaria, Phormia regina 
and Sarcophaga ttiisera) 39 to 64 minutes 
after ingestion and from their feces 172 to 
254 minutes after ingestion. 

Faulty plumbing and water systems 
may cause water-borne transmission. The 
most striking case of this kind occurred 
during the Chicago World Fair in 1933. 
An outbreak of amoebic dysentery occurred 



140 



THE AMOEBAE 



among guests at two neighboring hotels 
from which over 1000 cases with 58 deaths 
were tracked down in 44 states and 3 Ca- 
nadian provinces (Bundesen el al. , 1936). 
Cross connections between the water and 
sewage pipes, back siphonage from toilet 
bowls into the water supply and leakage 
from an overhead sewage pipe in the 
kitchen were involved. 

Food handlers may play an important 
role in transmission of amoebae, even tho 
the cysts rarely survive more than 10 
minutes on the hands, except under the 
fingernails (Spector and Buky, 1934). 
Thus, Schoenleber (1940, 1941) reported 
that in a group of Americans living in a 
Standard Oil Co. camp in Venezuela, the 
prevalence of amoebic infection was re- 
duced in 3 years from 25. 6% to 1. 9% and 
the amoebic dysentery rate from 36.84 to 
0.61 per 1000 per year by inspection and 
treatment of food handlers. Winfield and 
Chin (1939), in a comparison of the prev- 
alence of amoebic infection with food hab- 
its in different parts of China, concluded 
that transmission by food handlers is 
probably more important than by other 
means in that country. E. histolytica is 
much commoner in North China than in 
South and Central China. This is corre- 
lated with the serving and eating of cold 
bread with the hands in North China as 
contrasted to the handling of hot rice with 
a serving spoon and chopsticks in South 
and Central China. On the other hand, 
Sapero and Johnson (1939, 1939a) found no 
evidence that carriers were important in 
the transmission of amoebae in a study of 
919 persons in the U.S. Navy. The sani- 
tary habits of American sailors probably 
had something to do with this. 

Diagnosis : The laboratory diagnosis 
of amoebiasis has been discussed in detail 
by Brooke (1958). Live amoebae can be 
found in wet smears made with physiolog- 
ical salt solution. These smears may be 
stained with Lugol's iodine solution diluted 
1:5 to bring out the nuclei of the cysts and 
stain glycogen. However, for accurate 
identification and differentiation from 
other species of amoebae, staining with 
hematoxylin is essential. The smears are 
generally fixed in Schaudinn's fluid and 
stained with Heidenhain's iron hematoxylin. 



Sapero and Lawless's (1953) MIF (merthio- 
late -iodine -formaldehyde) stain -preserva- 
tion technic can also be used. 

For concentration of cysts, flotation 
in zinc sulfate solution (Faust et al. , 1938) 
can be used. The cysts are distorted be- 
yond recognition, however, by the other 
salt and sugar solutions in common use 
for flotation of helminth eggs. For con- 
centration by sedimentation, the FTE 
(formalin- triton-ether) sedimentation 
technic (Ritchie, Pan and Hunter, 1952, 
1953) or MIFC (merthiolate- iodine-formal- 
dehyde-concentration) technic (Blagg el al. , 
1955) can be used. 

Cultivation can be helpful in diagnosis 
of amoebiasis, but only if fresh specimens 
are used and if the laboratory personnel 
are expert. Cultivation is not recommended 
for general use. 

E. histolytica cannot be differentiated 
morphologically from E. haybiuDiiii, and 
its differentiation from other intestinal 
amoebae, and especially from E. coli, is 
not an easy task. There is a surprising 
amount of discrepancy even among those 
who should be qualified. Thus, in an eval- 
uation by the USPHS Communicable Dis- 
ease Center of the diagnostic ability of 42 
state health department laboratories 
(Brooke and Hogan, 1952), an average of 
4. 1 out of 18 £. histolytica infections was 
missed among 98 stool samples sent to the 
laboratories for examination, and an aver- 
age of 4.4 false positive reports was made 
among the 80 negative samples. Further- 
more, in an analysis of responses by mem- 
bers of the American Society of Tropical 
Medicine to a questionnaire on the clinical 
and laboratory diagnosis of amoebiasis, 
Brooke et al. (1953) found a surprising 
lack of agreement in statements concerned 
with the identification of E. histolytica 
cysts and trophozoites. 

Goldman (1959, 1960) was able to dif- 
ferentiate between Entamoeba histolytica, 
E. liart>}ianni, E. nioshkovskii and E. coli 
by a fluorescence antibody technic. Three 
originally invasive strains of E. histolytica 
which he studied differed significantly 
from a non-invasive strain. 



THE AMOEBAE 



141 



Cultivation : E. histolytica was first 
cultivated by Boeck and Drbohlav (1925). 
Their medium was composed essentially 
of a coagulated egg slant overlaid with 
Locke's solution containing serum. Var- 
ious modifications of this medium are 
still in use. Cleveland and Collier (1930) 
used a liver infusion agar slant overlaid 
with serum and physiological salt solution. 
Balamuth (1946) introduced an all-liquid 
egg infusion-liver extract medium. 

Treatment : Amoebiasis can be 
treated with a number of drugs (cf . Bala- 
muth and Thompson, 1955). The old stand- 
ard drug, emetine, is not used as much as 
formerly because of its toxicity. Other 
drugs from which one can choose include 
(1) the arsanilic acid derivatives, carbar- 
sone, glycobiarsol (bismuth glycoarsani- 
late, Milibis) and thiocarbarsone; (2) the 
iodoquinoline derivatives, diodohydroxy- 
quin (Diodoquin), chiniofon (Yatren) and 
iodochlorhydroxyquin (Vioform); (3) the 
antimalarial drug, chloroquine; and 
(4) the antibiotics, erythromycin, fuma- 
gillin, tetracycline, chlortetracycline and 
oxytetracycline. 

The particular drug selected depends 
in part on the type of amoebic infection 
involved. For acute or subacute dysen- 
tery, erythromycin, oxytetracycline or 
chlortetracycline may be used. Erythro- 
mycin is administered to man by mouth at 
the rate of 15 mg/kg daily in divided doses 
for 14 days. The usual human course of 
treatment with oxytetracycline or chlor- 
tetracycline is 0. 5 g 4 times a day by 
mouth for 10 days. 

For chronic cases or to eradicate in- 
testinal infections, one of the arsanilic 
acid or iodoquinoline derivatives may be 
used. The usual adult human course of 
treatment with carbarsone is 0. 25 g 2 or 
3 times a day by mouth for 10 days. That 
with glycobiarsol is 0. 5 g 3 times a day by 
mouth for 8 days. That with chiniofon is 
1. g 3 times a day by mouth for 7 days. 
That with diodohydroxyquin is 0. 65 g 3 
times a day by mouth for 20 days. 



For amoebic hepatitis or liver ab- 
scesses, chloroquine is used. A loading 
dose of 1 g chloi'oquine phosphate (0.6 g 
base) by mouth on each of 2 successive 
days followed by 0. 5 g daily for 2 to 3 
weeks is the recommended adult human 
course of treatment. 

Diodohydroxyquin has also been rec- 
ommended as a prophylactic drug for use 
by travellers in ai-eas of high endemicity. 

While relatively little work has been 
done on the treatment of amoebiasis in 
domestic animals, the same drugs are in 
general effective in them. Benson, Frem- 
ming and Young (1955) found that for chim- 
panzees the most successful drugs were 
carbarsone (0.25 g twice daily for 10 
days) and fumagillin (20 to 30 mg twice 
daily for 10 days) administered in fruit or 
fruit juice. They also frequently gave a 
course of emetine hydrochloride (1 mg/kg 
body weight up to a maximum of 60 mg, 
injected intramuscularly daily for a max- 
imum of 6 days) prior to carbarsone or 
fumagillin therapy (see also Fremming 
et al. , 1955). Herman and Schroeder 
(1939) successfully treated amoebic diar- 
rhea in a 21 -lb. orang-utan with carbar- 
sone. They gave 2 courses of treatment 
11 days apart, each course consisting of 
0. 05 g carbarsone in milk or a slice of 
banana 3 times a day for a week. 

Prevention and Control : Infection 
with amoebae can be prevented by sanita- 
tion. Water supply systems should be 
built without cross connections to sewage 
systems. Water which may be polluted 
should be boiled or filtered thru sand, 
since ordinary chlorination does not kill 
the cysts. Food handlers should wash 
their hands thoroughly after using the toi- 
let. Vegetables grown on polluted ground 
should be cooked, or, if they are to be 
eaten raw, should be scalded or soaked in 
vinegar containing 5% acetic acid for 15 
minutes at 30° C or in vinegar containing 
2. 5% acetic acid for 5 minutes at 45° C 
(Beaver and Deschamps, 1949). Diodohy- 
droxyquin may also be used prophylactically. 



142 



THE AMOEBAE 



ENTAMOEBA HARTMANNI 
VON PROWAZEK, 1912 

As mentioned above, E. kartmanni 
closely resembles the small race of E. 
histolytica. It can be differentiated by 
careful examination of hematoxylin-stained 
preparations. Burrows (1959) compared 
the two species. Most trophozoites of E. 
hartmanni are smaller than those of E. 
histolytica. Rounded trophozoites of E. 
hartmanni range from 3 to 10. Sjix in diam- 
eter, while those of E. histolytica are 
6. 5|i or more in diameter. The tropho- 
zoite nucleus of E. hartmanni is usually 
2. to 2. 5 fi in diameter but may range 
from 1. 5 to 3. 2^ , while that of E. his- 
tolytica is usually 3.0 to 3. 5fj, in diameter 
but may range from 2.8 to 3. 8/i . The 
peripheral chromatin of E. hartmanni is 
more variable in its arrangement than 
that of E. histolytica and may consist of 
discrete granules with wide spaces be- 
tween them, a crescent of granules on one 
side of the nucleus, or a single large bar 
of chromatin with several small granules 
around the membrane; the peripheral 
chromatin of E. histolytica is generally 
distributed uniformly along the nuclear 
membrane. 

Most cysts of E. Itartmanni are 
smaller than those of E. histolytica. They 
range from 3. 8 to 8. Ofi in diameter while 
those of small race E. histolytica are 
5. 5(1 or more in diameter. The cyst nu- 
clei of E. hartmanni are 1. 8 to 3. Ojj, in 
diameter in uninucleate cysts, 1. 3 to 2.0 )i 
in binucleate cysts and 0. 7 to 1. 7 /i in 
tetranucleate cysts; those of small race 
E. histolytica are 2.4 to 2.8 ji in diameter 
in uninucleate cysts, 2. to 2. 8/j, in binu- 
cleate cysts and 1.4 to 2.2 /i in tetranu- 
cleate cysts. The cysts of E. liartmanni 
seldom contain large glycogen bodies, but 
nearly all of them have a few to many 
small vacuoles; the cysts of E. histolytica 
generally have one large glycogen vacuole 
or no vacuoles. The chromatoid bodies of 
the two species are similar. 

Freedman and Elsdon-Dew (1959) 
suggested that, until an accurate, prac- 
tical method of separation is devised, 
mean sizes of 12/i for trophozoites and 



10/i for cysts be used as the dividing line 
between E. histolytica and E. liartmanni. 
The latter criterion has been used for 
some time to distinguish between the cysts 
of large and small race E. histolytica by 
those who do not accept the name E. liart- 
manni (Shaffer et al. , 1958). 

The incidence of E. liartmanni in an- 
imals and man is unknown because in the 
past it has ordinarily been lumped with 
E. histolytica. According to Burrows 
(1957, 1959) about half of the reported 
cases of E. histolytica in the United States 
were actually E. hartmanni. Further 
studies in which the two species are sep- 
arated will throw light on this point, which 
is important because E. hartmanni is non- 
pathogenic. 



ENTAMOEBA MOSHKOVSKII 
CHALAYA, 1941 

This species occurs in sewage. It is 
not a parasite of animals, but of the mu- 
nicipal digestive tract. It was found in 
the sewage disposal plant and sewer sys- 
tem of Moscow by Chalaya (1941, 1947), 
in sewage in Leningrad by Gnezdilov (1947), 
in sewage in Brazil by Amaral and Azzi 
Leal (1949), in sewage in London by Neal 
(1950, 1953), and in sewage in Quebec by 
Lachance (1959). Probably the same or- 
ganism was found in sewage in California 
by Wright, Cram and Nolan (1942), altho 
they did not name it. Chalaya (1947) cul- 
tivated it from the water of 2 ponds and a 
river in Russia. Altho E. moshkovskii 
is not parasitic, the possibility of its ac- 
cidental presence in fecal samples is of 
concern in diagnosis. 

E. moshkovskii resembles E. histo- 
lytica morphologically. The trophozoites 
are active, 9 to 29fi (usually 11 to 13(j.) 
in diameter. The nucleus has a small, 
central endosome and a peripheral layer 
of fine granules. The cysts are generally 
spherical, 7 to 17 /i in diameter. They 
contain a very large glycogen vacuole at 
first which is eventually absorbed as the 
cysts age. The chromatoid bodies are 
large, rather elongate, and have rounded 
ends. The mature cysts have 4 nuclei. 



THE AMOEBA 



143 



The cysts remain viable at 4" C up to 10 
months if they are not allowed to dry out. 

E. nioshkovskii can be cultivated in 
the usual Entamoeba media.. Its optimum 
temperature is about 24° C and it grows 
poorly at 37° C. The ability to grow at 
room temperature differentiates this spe- 
cies from E. histolytica. 

Chalaya (1941) was unable to infect 
kittens with E. moshkovskii, and Neal 
(1953) could not infect rats, frog {Rana 
temporaria ) tadpoles or salamander 
{Salamandra maculosa) larvae by feeding. 



ENTAMOEBA EQUI 
FANTHAM, 1921 

Fantham (1921) found this amoeba in 
the feces of 2 horses with signs of intes- 
tinal disturbance in South Africa. It is 
unusually large, fully extended tropho- 
zoites measuring 40 to 50 by 23 to 29)Lt 
and rounded ones 28 to 35 /i in diameter. 
The nucleus is of the histolytica type, but 
is oval rather than round. Erythrocytes 
are ingested. The cysts are 15 to 24 ju. in 
diameter and contain 4 nuclei and chroma- 
toid bars. 



ENTAMOEBA ANATIS 
FANTHAM, 1924 

Fantham (1924) found this amoeba in 
the feces of a duck which had died of acute 
enteritis in South Africa. It resembles 
E. histolytica morphologically, and its 
trophozoites ingest erythrocytes. The 
cysts are spherical or subspherical, thin- 
walled, 13 to 14 n in diameter, and con- 
tain 1 to 4 nuclei and thin, needle-like 
chromatoid bodies. 



ENTAMOEBA CO LI 
(GRASSI, 1879) 
CASAGRANDI AND 
BARBAGALLO, 1895 

Synonyms : Am,oeba coli, Endamoeba 
hominis. Council-mania lafleuri. 

This is the commonest species of 
amoeba in man. According to Belding 



(1952), it was found in 28% in 19 surveys 
of 17,733 persons thruout the world and 
occurs in about 30% of the population of 
the United States. It also occurs in the 
gorilla, orangutan, chimpanzee, gibbon 
and in various species of macaques and 
other monkeys (Mackinnon and Dibb, 
1938). Smith (1910) saw an amoeba sim- 
ilar to E. coli in pigs, and Kessel (1928a) 
found it in a Chinese pig. Kessel (1928a) 
also infected pigs experimentally with E. 
coli cysts from man, but the infections 
lasted less than 6 weeks. 

Entamoeba coli occurs in the cecum 
and colon. It can be cultivated on the 
usual media. It is non- pathogenic, and 
therefore must be differentiated from E. 
histolytica. 

Its trophozoites are 15 to 50 /i (usually 
20 to 30 jn) in diameter. The cytoplasm is 
filled with bacteria and debris, and the 
ectoplasm is thin. The organism moves 
sluggishly. The nucleus has an eccentric 
endosome larger than that of E. histo- 
lytica, and a row of relatively coarse 
chromatin granules around its periphery. 
There may also be a few scattered chrom- 
atin granules between the endosome and 
the nuclear membrane. The cysts are 10 
to 33 ju in diameter and have 8 nuclei when 
mature. The cysts contain slender, splin- 
ter-like chromatoid bodies with sharp, 
fractured or square ends; these disappear 
as the cysts age. The young cysts also 
may contain a large, well-defined glycogen 
globule; it usually disappears before the 
cyst is mature. 



ENTAMOEBA WENYONI 
GALLI-VALERIO, 1935 

Wenyon (1926) reported that he had 
seen 8-nucleate amoeba cysts of the E. 
coli type in the feces of goats. Galli- 
Valerio (1935) described this form, naming 
it Entamoeba wenyoni. The few tropho- 
zoites which he saw measured 12 by 9j^i, 
their protoplasm was fairly granular with 
no distinction between ectoplasm and endo- 
plasm, and they contained numerous bac- 
teria. They moved very slowly with short, 
rounded pseudopods. The cysts were spher- 
ical, 6 to 9(i in diameter, and contained 8 
nuclei. 



144 



THE AMOEBAE 



ENTAMOEBA MURIS 
(GRASSI, 1879) 

Synonyms : Amoeba miiris. Council- 
mania muris, Councilmania decumani. 

E. muris occurs commonly in the 
cecum and colon of rats, mice and the 
golden hamster thruout the world. An- 
drews and White (1936) found it in 10.4% of 
2515 wild rats in Baltimore. Fry and Mel- 
eney (1932) found it in 48% of 48 wild Rattus 
norvegicus and 24. 1% of 54 grey mice cap- 
tured in a rural area of Tennessee. Tsuchiya 
and Rector (1936) found it in 8% of 100 rats 
in St. Louis. Elton, Ford and Baker (1931) 
reported it in 50% of 440 long-tailed field 
mice (Apodemus sylvaticus), 4l"/o oi 116 bank 
voles {Clelhrionomys glareolus) and 41% 
of 51 short-tailed field mice {Microtus 
hirtus) in England. Wantland (1955) found 
it in 33% of 412 golden hamsters from sev- 
eral American suppliers and laboratories. 
Mudrow-Reichenow (1956) found E. luuris 
in 7% of 14 golden hamsters, 35% of 21 
laboratory rats and 39% of 92 laboratory 
mice in Germany. 

Kessel (1924) transmitted E. muris 
from the rat to the mouse and vice versa. 
Neal (1947, 1950a) and Saxe (1954) infected 
rats with E. uiuris from the golden ham- 
ster and mouse. Saxe (1954) infected the 
golden hamster with E. muris from the rat. 

E. muris is morphologically similar 
to E. coli. Its trophozoites are 8 to 30 /i 
long. Its cysts are 9 to 20jj, in diameter 
and have 8 nuclei when mature. Its nu- 
clear structure and division were studied 
by Wenrich (1940). He found that the nu- 
cleus is intermediate in structure between 
those of E. kislolylica and E. culi but 
more nearly resembles the latter. It var- 
ies in diameter from 3 to 9fi with a mean 
of 4 to 5 |i. In division, approximately 8 
chromosomes are formed. Binucleate 
cysts almost always contain a large gly- 
cogen vacuole, and mononucleate cysts 
very frequently do. 

E. muris is non- pathogenic. It is 
important to the research worker because 
it must be differentiated from other amoe- 
bae introduced in experimental infections. 



ENTAMOEBA CAVIAE 
CHATTON, 1918 

This species is often referred to as 

Entamoeba cobayae (Walker , 1908) Chatton, 
1917. However, the form which Walker 
(1908) called Amoeba cobayae -wcls seen in 
cultures from a guinea pig intestine and 
was not an Enta»ioeba at all. Hoare (1959) 
considered this species a synonym of E. 
muris. 

E. caviae is common in the ceca of 
laboratory guinea pigs. Nie (1950) found 
it in 14% of 84 guinea pigs in Pennsylvania 
and Mudrow-Reichenow (1956) found it in 
46% of 13 guinea pigs in Germany. 

E. caviae resembles E. culi. Its 
morphology has been studied by Nie (1950). 
The trophozoites are 10 to 20 )i in diam- 
eter with a mean of 14.4jj,. The nucleus 
is 3 to 5 (i in diameter. Its endosome var- 
ies in size and shape and may be central 
or eccentric. In some cases it is com- 
posed of several granules. There is a 
ring of coarse chromatin granules inside 
the nuclear membrane. The cysts are 11 
to 17 |i in diameter with a mean of 14^ 
and have 8 nuclei (Holmes, 1923). They 
are rare. 

E. caviae is non- pathogenic. Because 
it is so common, it must be differentiated 
from other amoebae in experimentally in- 
fected animals. 



ENTAMOEBA CUNICULI 
BRUG, 1918 

This species occurs in the cecum and 
colon of the domestic rabbit. It is not 
pathogenic. It resembles^, coli, and 
Kheisin (1938) has even suggested the name 
Entamoeba coli forma cnniculi for it. 
Hoare (1959) considered it a synonym of 
E. muris. It is apparently quite common 
in rabbits, altho there seem to be relatively 
few reports on it. Kheisin (1938) found it 
in 25% of the rabbits he examined in Russia. 
The trophozoites range from 12 to 30 ji in 
length with means of 13 to 17 fi in different 
rabbits. The cysts have 8 nuclei. They 



THE AMOEBAE 



145 



range in diameter from 7 to 21 ji with 
means of 10 to 15ju in different rabbits. 



ENTAMOEBA GALLINARUM 
TYZZER, 1920 

This non-pathogenic species was des- 
cribed from the ceca of the chicken and 
turkey by Tyzzer (1920). By cecal inocu- 
lation of parasite-free baby chicks, 
Richardson (1934) found what appeared to 
be the same species in the ceca of the 
domestic duck, turkey and goose. E. 
galliiiaruni is common. McDowell (1953) 
found it in about 30% of a large number of 
chickens he examined in Pennsylvania. 

E. gallinarmu closely resembles E. 
coli. The trophozoites are 9 to 25jj, in 
diameter, most measuring 16 to 18|i. 
The endoplasm is highly vacuolated and 
contains many food vacuoles. Altho 
Tyzzer (1920) said that E. galliiiaruni 
did not ingest bacteria, McDowell (1953) 
found that bacteria were its main food, 
altho it also ingested Trichouionas among 
other foods. The ectoplasm is clear or 
granular. The nucleus is 3 to 5 ji in di- 
ameter, with an eccentric endosome and 
a row of granules around the outside. 
The mature cysts are 12 to 15/i in diam- 
eter and contain 8 nuclei. 



found it in the feces of 4 gnus ( Conno- 
chaetes taurinus) in the London zoo. It 
has been described most recently by Noble 
(1950) and Noble and Noble (1952). The 
trophozoites are 5 to 20jj. in diameter. 
The cytoplasm is smoothly granular and 
filled with vacuoles of various sizes. The 
nucleus is large, with a large, central 
endosome made up of compact granules 
and a conspicuous row of chromatin gran- 
ules of different sizes around its periphery. 
The cysts are 4 to 14 p. in diameter and 
contain a single nucleus when mature. 
Their chromatoid bodies are irregular 
clumps of varying size and rods, splinters 
or granules. A large glycogen vacuole 
may or may not be present. 

Noble and Noble (1952) found that the 
uninucleate entamoebae from the feces of 
cattle, goats, sheep and swine were mor- 
phologically indistinguishable. However, 
since their physiological characteristics 
have not been studied and cross infections 
have not been attempted, they considered 
it best not to assign them all to the same 
species. If future work should show that 
they are all the same, their correct name 
would be E. bovis. 



ENTAMOEBA OVIS 
SWELLENGREBEL, 1914 



Richardson (1934) transferred infec- 
tion from chick to chick by association in 
the same cage. She found that the mini- 
mum oral infective dose of E. gallinarum 
for the chick was 240 cysts, and observed 
that the cysts remained viable in raw 
feces for 10 days and in feces diluted with 
water for at least 28 days. 



ENTAMOEBA BOVIS 
(LIEBETANZ, 1905) 

Synonym : Amoeba bovis. 

This non- pathogenic species occurs 
commonly in the rumen and feces of cattle 
thruout the world. Noble and Noble (1952) 
found it in the feces of all of 34 cattle 
from California, Pennsylvania, Korea 
and Japan. Mackinnon and Dibb (1938) 



Synonym: Entamoeba debliecki, pro 
parte". 

This non- pathogenic species was first 
described from the intestines of sheep in 
Sumatra, but it is common thruout the 
world. Noble and Noble (1952) found it in 
the feces of all of 25 sheep from California 
and Washington. Triffitt (1926) reported 
it from the feces of the sable antelope 
{Hippotragiis niger) and common water- 
buck ( Cobus ellipsiprymus) in Africa. 

By a historical accident, the name of 
the pig entamoeba rather than that of the 
sheep entamoeba has been used for the 
entamoeba of the goat. Nieschulz (1923) 
gave the first description of E. debliecki 
(a synonym of E. snis) from the pig and 
soon after (1923a) found what appeared to 
be the same species in the large intestine 



146 



THE AMOEBAE 



of the goat in Holland. Hoare (1940) found 
it in the feces of 10 out of 14 goats in 
England and redescribed it under the name 
E. deblieclii. Noble and Noble (1952) 
found it in the feces of 27 out of 28 goats 
in the United States and called it E. fiolecki 
(the name they used for the pig entamoeba). 
However, they considered the uninucleate 
entamoebae of cattle, goats, pigs and 
sheep to be morphologically indistinguish- 
able. Since goats share a great many 
parasites with sheep but relatively few 
with swine, and in the absence of cross- 
infection experiments to the contrary, the 
best name for the goat entamoeba is E. 
ovis . 

The trophozoites of E. ovis measure 
11 to 12 by 13 to 14 ji. The nucleus typ- 
ically contains a large, pale endosome 
generally composed of several granules, 
a ring of peripheral chromatin, and num- 
erous small granules between the endo- 
some and the nuclear membrane. In 
some cases there is very little peripheral 
chromatin and in others the endosome 
may be very small. The cysts are 4 to 
13|Lx in diameter with a mean of 7|j. and 
contain a single nucleus when mature. 
They usually contain numerous chromatoid 
bodies of varying size, shape and abun- 
dance and a glycogen vacuole. 

The cysts of the form from the goat 
are 4 to 13fi in diameter. Hoare (1940) 
found 2 races which differed in size. The 
cysts of one ranged from 5 to 9|j in diam- 
eter with a mode of 6. 7 p. , while the cysts 
of the other ranged from 9 to 13^ with a 
mode of 10.4fi Noble and Noble (1952), 
however, found only a single race with 
cysts ranging in diameter from 4 to 12/:i 
with a mean of 6. 4 /i . 

It is quite likely that E. ovis is a 
synonym of E. hovis, but until cross in- 
fection experiments have been carried 
out, it is thought best to retain it as a 
separate species. 



ENTAMOEBA DILIMANI 
NOBLE, 1954 

Noble (1954) found this species in the 
feces of all of 12 goats he examined on 



Luzon in the Philippines. He saw only 2 
trophozoites. They were 12/1 across, had 
broad, rounded pseudopods whose ends 
had fairly clear ectoplasm, and food vac- 
uoles containing bacteria. The cysts are 
5 to 16/i in diameter with a mean of 9. 7/i , 
and contain a single nucleus. The endo- 
some is usually a small, central dot but 
may be eccentric. Peripheral chromatin 
is often absent or may appear as a few 
large, irregular granules. The entire 
nucleus is filled with fine granules which 
may form a ring around the endosome. 
The cyst contains 1 or more large glycogen 
vacuoles and from one to a large number of 
chromatoid bodies varying in shape from 
small, irregular masses to a single, large, 
sausage-shaped body. Noble considered 
this species to differ from the Entamoeba 
in American goats in that the peripheral 
chromatin rarely forms a heavy ring, the 
endosome is usually a single, small dot, 
and a periendosomal ring of chromatin is 
usually present. 



ENTAMOEBA SUIS 
HARTMANN, 1913 

Synonym : Entamoeba debliecki, pro 
parte. 

A number of authors have used the 
name. Entamoeba polecki Prowazek, 
1912, for this species, but this name must 
be considered a nomen nudum because 
Prowazek' s description was so poor as to 
be unrecognizable (see Hoare, 1940, 1959). 

E. siiis occurs in the cecum and colon 
of swine. Chang (1938) found it in 71% of 
209 pigs in China. Pavloff (1935) found it 
in 26 of 1840 pigs in France and Bulgaria. 
Simitch et al. (1959) found it in 8% of 1800 
pigs in Yugoslavia. Frye and Meleney 
(1932) found it in 63% of 80 pigs, Alicata 
(1932) found it in 43% of 35 pigs, and Noble 
and Noble (1952) found it in all of 30 pigs 
in the United States. Mackinnon and Dibb 
(1938) found it in the European wild boar 
{Stis scrofa), giant forest hog (Hylochoerus 
meinertzliageni) and Indian boar (Sus 
cristatiis) in a London zoo. Kessel and 
Johnstone (1949) and Kessel and Kaplan 
(1949) reported "E. polecki" from the 
rhesus monkey but remarked that it 



THE AMOEBAE 



147 



appeared identical with E. chattoni of 
monkeys; this is the species to which their 
form should be assigned. Ten human in- 
fections have been reported (Kessel and 
Johnstone, 1949; Lawless, 1954; Burrows 
and Klink, 1955). However, altho no 
human cross-infection experiments have 
been attempted, E. suis does not seem to 
be readily transmissible to man. Chang 
(1939) observed that it was not present in 
27 Chinese butchers, altho their methods of 
slaughtering provided ample opportunity for 
infection. Pavloff (1935) was unable to in- 
fect kittens with it by intrarectal inoculation. 

E. suis has been described by a num- 
ber of authors, including Noble and Noble 
(1952) in domestic animals, and by Bur- 
rows (1959) in man. The following des- 
cription is based on Noble and Noble. 
The trophozoites are 5 to 25fi long. Some 
authors (e. g. , Hoare, 1959; Simitch et al. 
1959) have considered the small forms to 
be a separate species, E. debliecki, but 
such a separation does not appear to be 
justified. 

The nucleus varies in appearance. 
The endosome is central and is usually 
quite large. It may sometimes almost fill 
the nucleus, but it may also sometimes be 
small and similar to that of E. histolytica. 
There is a rather homogeneous ring of 
peripheral chromatin within the nuclear 
membrane. There are ordinarily no 
chromatin granules between the endosome 
and the peripheral ring. The cytoplasm 
is granular and vacuolated, and contains 
bacteria in its food vacuoles. The cysts 
are 4 to 17 ju in diameter and have a 
single nucleus when mature. The chroma- 
toid bodies in the cysts vary markedly in 
shape from stout rods with rounded ends 
similar to those of E. histolytica to irreg- 
ular granules of varying size. There may 
or may not be a glycogen vacuole. Cysts 
without chromatoid bodies or glycogen 
vacuoles are also common. 



(1934) observed amoebae associated with 
necrosis in sections of the colon of pigs 
which had died of experimental hog chol- 
era. However, altho E. suis is very 
common in swine, it has never been found 
in sections of intestinal lesions of hundreds 
of swine examined by University of Illinois 
pathologists. 

E. suis can be cultivated in the usual 
media. It is apparently less sensitive 
than E. histolytica to amoebicidal drugs, 
but Frye and Meleney (1932) eliminated it 
from pigs by feeding 50 mg/kg carbarsone 
in the milk daily for 10 days. 



ENTAMOEBA BUBALUS 
NOBLE, 1955 

Noble (1955) found this species in the 
feces of 12 of 15 carabao (Bubalus bubalis) 
from several islands in the Philippines. 
Only 2 trophozoites were seen. They 
averaged 12 /ii in diameter. The cysts are 
5 to 9 fi in diameter with a mean of 8 jll . 
They contain 1 or more vacuoles, but 
usually a single large one which crowds 
the cyst contents to its periphery. The 
chromatoid bodies are usually small and 
irregular in shape but may occasionally 
be large, with rounded ends, similar to 
those of E. histolytica. The cysts contain 
a single nucleus 2. 6ju in diameter with a 
large endosome 1.4jj. in diameter which 
often appears to be a cluster of 4 granules. 
There is usually a distinct peripheral ring 
of chromatin, but the amount of peripheral 
chromatin may vary from practically none 
to a ring of dots to a few isolated clumps. 
There is no periendosomal chromatin. 
Noble (1955) considered E. bubalus to 
differ from other entamoebae with uninu- 
cleate cysts in the character of its nucleus-- 
the heavy, usually uniform outer ring of 
chromatin and the large, prominent endo- 
some. 



E. suis is probably non- pathogenic. 
Smith (1910) found amoebae in sections of 
intestinal ulcers in swine. Hartmann 
(1913), who studied Smith's preparations, 
named the amoeba E. suis. Ratcliffe 



ENTAMOEBA CHATTONI 
SWELLENGREBEL, 1914 



parte. 



Synonym : Entamoeba polecki, pro 



148 



THE AMOEBAE 



This species occurs in the large in- 
testine of macaques and a number of other 
monkeys. It was first seen by Chatton 
(1912), who called it Loeschia sp. , and 
was given its present name by Swellengre- 
bel (1914), who found it in the rhesus 
monkey. This name was thought to be one 
of the many synonyms of E. histolytica 
until Salis (1941) showed that it was not. 
Kessel and Johnstone (1949) found E. 
chattoni and E. polecki to be morphologi- 
cally similar, and used the older name, 
E. polecki, for the species. However, 
in the absence of cross-infection exper- 
iments between pigs and monkeys, it is 
best to retain the name, E. cliattoni, for 
the monkey form. In any case, E. polecki 
is a nomen nudum and should be replaced 
by E. suis. The proper name for the 
forms in the 10 human cases which have 
been reported (see Burrows and Klink, 
1955) is uncertain. Perhaps it should de- 
pend in each case on the source of infec- 
tion, whether pig or monkey, or perhaps 
both these names will eventually be 
dropped in favor of E. bovis. However, 
for the present E. chattoni is preferable. 

E. chattoni is probably much more 
common in monkeys than E. histolytica, 
from which it must be distinguished. 
Mudrow-Reichenow (1956) found it in 6 of 
7 rhesus monkeys in Germany. The 
trophozoites of E. cliattoni are 9 to 25 /i 
long. The cysts are 6 to 18fi in diam- 
eter. Salis described two size races 
with cysts averaging 10. 9 and 13. 1 fj. , 
respectively but other workers have not 
made this differentiation. The nucleus 
varies a great deal in morphology. It 
may be indistinguishable from that of E. 
histolytica, with a small, central endo- 
some and a row of fine, peripheral chro- 
matin granules. On the other hand, the 
endosome may be large or small, central 
or eccentric, compact or diffuse, and 
composed of one to many granules, while 
the peripheral chromatin may be fine or 
coarse, uniform, irregular or diffuse, 
and there may or may not be chromatin 
granules between the endosome and the 
peripheral chromatin. The cysts are 
almost always uninucleate when mature. 
Less than 1% are binucleate, and they are 
never tetranucleate. The chromatoid 



bodies are usually irregular and small, 
but may also be rod-shaped with round or 
pointed ends, oval or round. A glycogen 
vacuole may or may not be present. 

E. cliattoni is generally considered 
non- pathogenic, altho 2 of the human pa- 
tients studied by Burrows and Klink (1955) 
had diarrhea which may or may not have 
been caused by the amoebae. 



ENTAMOEBA GINGIVA LIS 
(GROS, 1849) 
BRUMPT, 1914 

Synonyms : Amoeba gingivalis , 
Amoeba buccalis. Entamoeba buccalis. 
Amoeba dentalis. Amoeba kartulisi, Enta- 
moeba maxillaris. Entamoeba canibuc- 
calis. 

This species occurs commonly in the 
human mouth, where it lives between the 
teeth, in the gingival margins of the gums 
and in the tartar. It has occasionally been 
found in infected tonsils. E. gingivalis 
is present in perhaps 50% of all humans, 
but in up to 95% of those with pyorrhea. 
It was once thought to be the cause of 
pyorrhea, but is now known to be a harm- 
less commensal which finds an ideal home 
in diseased gums. 

Hinshaw (1920) transmitted E. gingi- 
valis to 5 dogs with gingivitis. In one of 
them the infection was still present after 
14 1/2 months, but in the others it died 
out within 4 months. Kofoid, Hinshaw and 
Johnstone (1929) established persistent in- 
fections in 5 of 11 dogs with E. gingivalis 
from cultures. They could not infect dogs 
with healthy mouths, but only those with 
gingivitis, pus pockets or loose gums. 

Goodrich and Moseley (1916) found 
amoebae indistinguishable from E. gingi- 
valis in pyorrheic ulcers in the mouths of 
2 dogs and a cat in England. N6ller(1922) 
found it in dogs in Germany. Simitch 
(1938) found a small amoeba in the saliva 
of 3 out of 165 dogs in Serbia and named 
it E. canibuccalis. The trophozoites 
were 8 to IGja long but became as long as 
2 5 /J in culture. Simitch infected 2 old 



THE AMOEBAE 



149 



dogs with cultured protozoa but failed to 
infect 3 young dogs, a young wolf and 2 
humans. In view of the affection with 
which some dog and cat owners treat their 
pets, there is no reason to believe that the 
entamoebae in the mouths of these animals 
are a different species from that of man. 



no cysts. Simitch (1938a) was unable to 
infect horses with E. gingivalis (syn. , 
E. canibuccalis ) from the dog or to infect 
dogs with the horse form. Hence he con- 
sidered the latter to be a new species. 
Further study is needed to learn whether 
this view is correct. 



Kirby (1928) found E. gingivalis in 
the mouths of 2 chimpanzees with pyorrhea. 
Kofoid, Hinshaw and Johnstone (1929) 
found it in the mouths of Macaco mulatta 
and M. iriis. Deschiens and Gourvil (1930) 
found it in the M. ))ii(latta and Papio 
sphynx. Hegner and Chu (1930) found it in 
the mouths of 37 out of 44 wild M. philip- 
pinensis. 

E. gingivalis has no cysts. The tro- 
phozoites are usually 10 to 20j:i long, but 
may range from 5 to 35/^. The cytoplasm 
consists of a zone of clear ectoplasm and 
granular endoplasm containing food vac- 
uoles. The amoebae usually feed on leuco- 
cytes, epithelial cells, sometimes on bac- 
teria and rarely on red blood cells. There 
are usually a number of pseudopods. The 
nucleus is 2 to 4 |U in diameter, with a 
moderately small endosome, a peripheral 
layer of chromatin granules and some del- 
icate achromatic strands extending from 
the endosome to the nuclear membrane. 

Reproduction is by binary fission. It 
was described in detail by Child (1926), 
Stabler (1940) and Noble (1947). Child 
said that 6 chromosomes are present, but 
Stabler and Noble found only 5. 



ENTAMOEBA EQUIBUCCALIS 
SIMITCH, 1938 

Synonym : Entamoeba gingivalis va.r . 
eqiii. 

Nieschulz (1924) found this amoeba in 
the mouths of several horses in Holland, 
and Simitch (1938a) cultured it from the 
mouths of 16 out of 22 mares and 3 out of 
4 donkeys in Serbia. It is morphologically 
identical with E. gingivalis, except that 
its trophozoites are somewhat smaller, 
measuring 7 to 14jj, in diameter. It has 



ENTAMOEBA SUIGINGIVALIS 
TUMKA, 1959 

Tumka (1959) found this amoeba on the 
coating of the teeth of 6 out of 32 domestic 
pigs from the vicinity of Leningrad. It re- 
sembles E. gingivalis but is in its lower 
size range, measuring 7 to 12fi with a 
mean length of 9 jj, when fixed and stained. 
It is questionable whether this is a sepa- 
rate species. 



ENTAMOEBA CAUDATA 
CARINI AND REICHENOW, 1949 

This species was found in the feces 
of a dog in Brazil. No cysts were seen. 
The trophozoites were 10 to 36 fi long. 
Their pseudopods and nuclei resembled 
those of E. histolytica, but they differed 
from it in containing many ingested bac- 
teria and in having a sac-like appendage 
at the posterior end containing dense, 
darkly staining cytoplasm and undigested 
bacteria. 



ENTAMOEBA GEDOELSTI 
(HSIUNG, 1930) 

Synonym: Endamoeba gedoelsti. 

Hsiung (1930) found this amoeba in 
the cecum or colon of 7 out of 46 horses 
in Iowa. What was probably the same spe- 
cies had been seen in the horse by Gedoelst 
(1911) in Belgium and Fantham (1920) in 
South Africa. No cysts have been seen. 
The trophozoites are 7 to 13 |i long and 
contain bacteria in their food vacuoles. 
The nucleus is similar to that of E. coli, 
with an eccentric endosome surrounded 
by a halo and a row of peripheral chromatin 
granules. 



ISO 



THE AMOEBAE 











K 



M N 




Q 




Fig. 21. A. Entcniioeha bKlialiis trophozoite. B. E. bnluilus cyst. C. Eiiliimocba 

chattoiii Irophozoite. D. E. clia I loni cyst. E. E)ila»ioeba gingivalis tropho- 
zoite from dog. F. Entamoeba gedoelsti trophozoite. G. Eiilaiiioeba caudata 
trophozoite. H. lodaiiioeba biictschlii trophozoite. I. /. buctschlii cyst. 
J. Entamoeba cqiiibiiccalis trophozoite. K. Eiidolimax nana trophozoite. 
L. E. nana cyst. M. Endolima.x grcgarini/ormis trophozoite. N. E. greg- 
ariniformis cyst. X 1700. (From Hoare, 1959, in Veterinary Reiiens and 
Annotations). O. Vahlkanipfia lobospinosa trophozoite. P. V. lobospinosa 
cyst. X 1050. (From Becker and Talbott, 1927). Q. Dientamoeba fragilis 
trophozoite. X 1700. (From Wenrich, 1944, J. Morph. 74:467) 



THE AMOEBAE 



151 



ENTAMOEBA CAPRAE 
FANTHAM, 1923 

Fantham (1923) described this species 
from the intestine and reticulum of a 
lightly infected goat in South Africa. It is 
very large, one streaming individual 
measuring 34 by 24 jn. The pseudopods 
are short and lobose, and red cells may 
be ingested. The nucleus is oval, 9 to 
10 /i in diameter, with an eccentric endo- 
some. No cysts were seen. The relation- 
ship of this form to other goat amoebae 
remains to be determined. 



papio, kra monkey, green monkey, Anubis 
baboon, Gelada baboon and mandrill, 
(Mackinnon and Dibb, 1938; Wenrich, 1937). 
In addition, Mackinnon and Dibb (1938) 
found this species in the giant forest hog, 
Hyloclioerus meintritz-hageni. Smith 
(1928) infected rats with /. buetschlii 
from man, and Pavloff (1935) did so with 
a strain from the pig. However, Simitch 
et al. (1959) were unable to infect man 
with cysts from fresh pig feces or to infect 
the pig with cysts from fresh human feces; 
they gave no details of their experiments. 

Location: Cecum and colon. 



ENTAMOEBA SP. 

Brenon (1953) tabulated 3 deaths from 
amoebic dysentery among the causes of 
death he observed in 1005 chinchillas in 
California. Since the amoebae of chin- 
chillas have apparently not been described, 
they cannot be assigned to any species. 



Genus lOD AMOEBA Dobell, 1919 

In this genus the nucleus is vesicular, 
with a large endosome rich in chromatin, 
a layer of lightly staining globules sur- 
rounding the endosome, and some achro- 
matic strands between the endosome and 
nuclear membrane. The cysts contain a 
large glycogen body which stains darkly 
with iodine. They are ordinarily uninu- 
cleate. This genus occurs in vertebrates. 
A single species is recognized. 



lOD AMOEBA BUETSCHLII 
(VON PROWAZEK, 1912) 
DOBELL, 1919 

Synonyms : Entamoeba williamsi 
pro parte, Endoliniax williamsi, Endo- 
limax pileonucleatus, lodamoeba wenyoni, 
lodamoeba suis, Endolimax kueneni. 

Hosts : Pig, man, chimpanzee, gor- 
illa, macaques and other monkeys and 
baboons, including Macaca mulatta, M. 
irus, M. sancti-johannis, M. lasiotis, 
M. philippinensis , Cercocebus aethiops, 
Cercopithecus mona, C. ascanius, Papio 



Geographic Distribution : Worldwide. 

Prevalence: /. buetschlii is the com- 
monest amoeba of swine, and the pig was 
probably its original host. Frye and 
Meleney (1932) found it in 24% of 127 pigs 
in Tennessee. Alicata (1932) found it in 
25% of 35 pigs in the U. S. Cauchemez 
(1921) estimated that it was present in 50 
to 60% of the pigs he examined in France. 
Noller (1922) found it in about 20% of those 
he examined in Germany. Pavloff (1935) 
found it in 29% of 530 pigs in France and 
30% of 1310 pigs in Bulgaria. Simitch 
et al. (1959) found it in 8% of 1800 pigs in 
Yugoslavia. Kessel (1928a) found it in 
42% of the pigs he examined in China, and 
Chang (1938) found it in 51% of 209 pigs in 
China. 

According to Belding (1952), I. buet- 
schlii was found in 8. 4% of 17, 568 persons 
in 20 surveys thruout the world, and in 4% 
of the people in American surveys. Wen- 
rich (1937) found it in 44% of 55 apes and 
monkeys which he examined. 

Morphology : Wenrich (1937), among 
others, has studied the morphology of /. 
buetschlii. The trophozoite is usually 9 
to 14/1 long but may range from" 4 to 20 /x. 
It has clear, blunt pseudopods which form 
slowly, and it moves rather slowly. The 
ectoplasm is clear, but not well separated 
from the granular endoplasm. Food vac- 
uoles containing bacteria and yeasts are 
present in the cytoplasm. The nucleus is 
relatively large, and ordinarily contains 
a large, smoothly rounded, central 



152 



THI AMOEBAE 



endosome surrounded by a vesicular space 
containing a single layer of periendosomal 
granules about midway between the endo- 
some and the nuclear membrane. Fibrils 
extend to the nuclear membrane, but 
there are no peripheral granules inside 
the membrane. Stabler (1945) described 
tube-like processes which may be used 
for feeding in 12% and 27%, respectively, 
of the trophozoites of 2 human strains. 

The cysts are often irregular in form. 
They are usually 8 to lOji long, but may 
range from 5 to 14 fi. They contain a 
single nucleus in which the periendosomal 
granules have usually aggregated into a 
crescent-shaped group at one side of the 
endosome, pushing it to one side. They 
contain a large, compact mass of glycogen 
which stains deeply with iodine. The gly- 
cogen disappears after 8 to 10 days in 
feces held at room temperature, and at 
the same time the cysts die and disinte- 
grate (von Brand, 1932). There are no 
chromatoid bodies in the cysts, but they 
may contain small, deeply staining gran- 
ules something like volutin granules. 

Life Cycle : /. buelschlii reproduces 
by binary fission. Pan (1959) studied nu- 
clear division in the trophozoites. He 
considered the process unique; his paper 
should be read for the details. The hap- 
loid number of chromosomes is usually 
more than 10--possibly 12. 

Pathogenesis : /. buelschlii is non- 
pathogenic except under unusual circum- 
stances. These have never been noted in 
the pig, but Andrew (1947) reported symp- 
toms similar to those of chronic E. Iiislo- 
lytica in a few persons, and Derrick (1948) 
described a fatal generalized infection in 
a Japanese soldier captured in New Guinea 
in which there were ulcers in the stomach, 
small intestine, large intestine, lymph 
nodes, lungs and brain. 

Bionomics and Epidemiology : /. 
buelschlii, like other intestinal amoebae, 
is transmitted by cysts. 

Cultivation : This species can be cul- 
tivated in the usual media. 



Treatment : Little is known about 
treatment for /. buelschlii, but it can be 
eliminated by emetine. 

Prevention and Control : The same 
preventive measures recommended for 
E. hislolylica will also prevent /. buel- 
schlii infections. 



Genus ENDOUMAX Kuenen and 
Swellengrebel, 1917 

These are small amoebae. The nu- 
cleus is vesicular, with a comparatively 
large, irregularly shaped endosome com- 
posed of chromatin granules embedded in 
an achromatic ground substance, and with 
several achromatic threads connecting the 
endosome with the nuclear membrane. 
Cysts are present. This genus occurs in 
both vertebrates and invertebrates. 



ENDOLIMAX NANA 

(WENYON AND O'CONNOR, 1917) 

BRUG, 1918 

Synonyms : Amoeba Umax. Enta- 
moeba nana, Endolimax inteslinalis, 
Endolimax cynomolgi, Endolimax suis, 
Councilmania tenuis . 

Hosts : Man, pig, gorilla, chimpan- 
zee, gibbon, macaques and other monkeys 
and baboons, including AJacaca mulalta, 
M. irus, M. sinica, M. sancti-johannis, 
M. lasiotis, M. philippinensis, Papio 
papiu, Cercocebus aethiops, Cercopith- 
ecus asca)iius, Gamadyillns sp. , and 
Erytlirocebns patas (see Mackinnon and 
Dibb, 1938). These authors also reported 
a morphologically indistinguishable form 
from the capybara [Hydrochoerus capybara) 
and tree porcupine (Coendou prehensilis). 

It is quite likely that E. ratti (see be- 
low) may be a synonym of E. nana, so that 
the latter's host range may be even broader 
than that given above. Chiang (1925) con- 
sidered E. ratti a separate species because 
he was unable to infect 14 rats with E. nana 
from man. However, Kessel (1928) suc- 
ceeded in doing so, and Smith (1928) found 



THE AMOEBAE 



153 



an E. naua-\i]^e amoeba in 4 of 63 rats 
which had been fed human feces but did 
not know whether it had already been 
present in the rats. 

Dobell (1933) transmitted E. nana 
from Macaca sinica to a man (himself) 
and from man to M. mulatto. Kessel 

(1928) infected M. irus with E. nana from 
man. However, Simitch et al. (1959) were 
unable to infect 4 young pigs with E. nana 
from man and consequently named the pig 
form E. siiis; they gave no details of their 
experiments. 

Location: Cecum, colon. Hegner 

(1929) and Dobell (1933) found E. nana in 
the vagina of macaques, where it was 
most likely of fecal origin. 

Geographic Distribution : Worldwide. 

Prevalence : E. nana is common in 
man. According to Belding (1952), it was 
found in 20. 5% of 18, 333 persons in 20 
surveys thruout the world and in about 
14% of those examined in the United States. 
Frye and Meleney (1932) found it in 5. 5% 
of 127 pigs in Tennessee, Alicata (1932) 
found it in 1 of 35 pigs in the U.S. , Kessel 
(1928) found it in 14% of the pigs examined 
by him in China, and Chang (1938) found 
it in 15% of 209 pigs in China. Simitch 
et al. (1959) found it in 8% of 1800 pigs 
in Yugoslavia. 

Morphology : The trophozoites are 
6 to 15 p. in diameter with an average of 
10 ju. They move sluggishly by means 
of a few blunt, thick pseudopods. The 
endoplasm is granular, vacuolated and 
contains bacteria and crystals. The nu- 
cleus contains a large, irregular endo- 
some composed of a number of chromatin 
granules. Several achromatic fibrils run 
from the endosome to the nuclear mem- 
brane. There are ordinarily no peripheral 
chromatin granules, but Stabler (1932) 
noted that they are formed after fixation 
in Schaudinn's fluid containing 20% acetic 
acid. The cysts are oval, often irregular, 
and thin-walled; they are usually 8 to 10 ^ 
long but may range from 5 to 14 /i. The 
mature cysts contain 4 nuclei, and they 



may contain ill-defined glycogen bodies. 
They have no chi'omatoid bodies but may 
have small granules resembling volutin 
and occasionally a few filaments of uncer- 
tain nature. 

Life Cycle : Reproduction is by binary 
fission in the trophozoite stage. The 
amoeba which leaves the cyst is multinu- 
cleate, but it divides into uninucleate 
amoebulae which grow into ordinary tropho- 
zoites. 

Pathogenesis : E. nana is non-patho- 
genic. 

Bionomics and Epidemiology : E. nana 
is transmitted in the same way as other 
enteric amoebae. Dobell (1933) found that 
its cysts could live at least 2 weeks at 
room temperature (15-24° C) and at least 
3 weeks at 10° C, while all the trophozoites 
died in 24 hours at both temperatures. 
Frye and Meleney (1932) found E. nana 
cysts in 1 out of 46 lots of flies which they 
examined in Tennessee. 

Cultivation : This species can be cul- 
tivated in the usual media. 

Treatment : Little is known about the 
treatment of E. nana. Dobell (1933) and 
others found that emetine has no effect on 
it. 

Prevention and Control : The same 
preventive measures recommended for 
E. histolytica will also prevent E. nana 
infections. 



ENDOLIMAX RATTI 
CfflANG, 1925 

This species, which may be a synonym 
of E. nana, occurs in the cecum and colon 
of laboratory and wild rats. Andrews and 
White (1936) found it in 1 out of 2515 wild 
rats in Baltimore, and Baldassari (1935) 
found it in 1 of 225 wild rats in Toulon, 
France. Chiang (1925) did not describe it, 
but merely stated that it was morphologi- 
cally identical with E. nana. 



154 



THE AMOEBAE 



ENDOLIMAX CAVIAE 
HEGNER, 1926 

This species occurs commonly in the 
cecum of the guinea pig. Hegner (1926) 
found it in Baltimore and Hegner and Chu 
(1930) found it in the Philippines. Nie 
(1950) found it in 18% of 84 guinea pigs in 
Pennsylvania. It is somewhat smaller 
than E. nana, the trophozoites measuring 
5 to 11 by 5 to 8n , but otherwise resem- 
bles it. Nie saw one specimen with an 
ingestion tube. The cysts are apparently 
unknown. 



ENDOLIMAX GREGARINIFORMIS 
(TYZZER, 1920) 
HEGNER, 1929 

Synonyms: Pygolimax gregarini- 
formis, Endolimax janisae, EndoUtnax 
niimidae. 



large number of chickens he examined in 
Pennsylvania. 

The trophozoites of E. gregariniformis 
are usually 4 to 13 /i long with a mean of 
9 by 5^1 , altho Hegner (1929a) found a 
small race in the guinea fowl. The tropho- 
zoites are oval, often with a posterior pro- 
tuberance, and move sluggishly. The ecto- 
plasm is not clearly separated from the 
endoplasm. The food vacuoles contain bac- 
teria. The nucleus is very similar to that 
of E. nana but tends to have a larger endo- 
some and a more apparent nuclear mem- 
brane, often with chromatin granules at 
the juncture of the achromatic threads with 
the membrane. The cysts have 4 nuclei 
when mature; they measure 7 to 8 by 8 to 
11 /x with a mean of 10 by 7;i (McDowell, 
1953). They tend to be somewhat lima 
bean- shaped instead of truly ovoid, and 
are often highly vacuolated. 



This species is found in the ceca of 
the chicken, turkey, guinea fowl, pheas- 
ant, domestic goose, domestic duck and 
various wild birds, including the black 
duck (Anas riibripes Iristis), black- 
crowned night heron (Nycticorax nycti- 
corax) and screech owl. 

E. gregariniformis was first des- 
cribed by Tyzzer (1920) from the turkey; 
he transmitted it easily to the chicken. 
Hegner (1926) described it from the 
chicken, naming it E. janisae. Hegner 
(1929a) found the same species and an- 
other form which he named E. numidae 
in the guinea fowl. The latter was 
smaller than E. gregariniformis , aver- 
aging 4 by 3/i, but nevertheless fell within 
its size range and did not differ from it 
morphologically. Hegner (1929a) infected 
chicks with both sizes of Endolimax irom 
the guinea fowl and also with Endolimax 
from the domestic goose, domestic duck 
and screech owl. Richardson (1934) in- 
fected chicks with Endolimax from the 
duck, goose, pheasant, black duck and 
black-crowned night heron. 

E. gregariniformis occurs thruout 
the world and is non-pathogenic. 
McDowell (1953) found it in over 50% of a 



Genus DIENTAMOEBA Jepps and 
Dobell, 1918 

These are small amoebae, usually 
with 2 nuclei. The nuclei are vesicular, 
with a delicate membrane and an endosome 
consisting of several chromatin granules 
connected to the nuclear membrane by 
delicate strands. No cysts are known. 
Dobell (1940) considered that this genus 
might be an aberrant flagellate closely 
related to Histomonas . 



DIENTAMOEBA FRAGILIS 
JEPPS AND DOBELL, 1918 

This species occurs in the cecum and 
colon of man and also of some monkeys. 
According to Belding (1952), it was found 
in 4. 2% of 7120 persons in 14 surveys 
thruout the world. Hegner and Chu (1930) 
found D. frag His in 2 out of 44 Macaca 
philippinensis in the Philippines, and 
Knowles and Das Gupta (1936) found it in 
1 out of 4 M. iriis in India. In addition. 
Noble and Noble (1952) mentioned finding 
a Dientamoeba in sheep feces in California. 

Only trophozoites are known for this 
species. They are very sensitive to 



THE AMOEBAE 



155 



environmental conditions, bursting in 
water and becoming degenerate in older 
fecal samples. In order to identify them, 
smears of fresh feces should be fixed in 
Schaudinn's fluid containing 10 to 20% 
acetic acid or in Bouin's fluid and stained 
with iron hematoxylin. Their morphology 
has been studied by Wenrich (1936, 1939, 
1944) and Dobell (1940), whose accounts 
do not always agree. 

The trophozoites range from 3 to 22 jj. 
but are usually 6 to 12 jn in diameter. 
The ectoplasm is distinct from the endo- 
plasm, which contains food vacuoles filled 
with bacteria, yeasts, starch granules, 
and parts of cells. In fresh feces there 
may be a single clear, broad pseudopod. 
About 3/5 of the protozoa contain 2 nuclei 
which are connected by a filament or des- 
mose. This appears to be one of the first 
structures to disappear during degenera- 
tion. Each nucleus is vesicular and has 
an endosome composed of 4 to 8 granules 
from which a few delicate fibers radiate 
to the nuclear membrane. There is no 
peripheral chromatin. 

Reproduction is by binary fission. 
There are 4 chromosomes. 

At one time D. fragilis was thought 
to be non- pathogenic, and this is true in 
most cases. However, in some persons 
it causes a mucous diarrhea and gastro- 
intestinal symptoms. It does not invade 
the tissues, but may cause low-grade ir- 
ritation of the intestinal mucosa, excess 
mucus secretion and hypermotility of the 
bowel. There may be mild to moderate 
abdominal pain and tenderness or dis- 
comfort. There may also be an increase 
in eosinophiles. 

The mode of transmission of D. fra- 
gilis is not clear, since there are no cysts 
and the trophozoites are so delicate. 
Dobell (1940) was unable to infect himself 
by mouth or 2 monkeys by mouth or rec- 
tally and suggested, by analogy with His- 
tomonas, that D. fragilis might possibly 
be transmitted by an intestinal nematode 
such as Trichuris. This idea has been 
partially confirmed by Burrows and 
Swerdlow (1956), who found small, amoe- 



boid organisms resembling D. fragilis in 
the eggs of Enterobius vermicularis and 
suggested that the pinworm might be the 
vector. 

D. fragilis can be readily cultivated 
in the usual culture media. It is sensitive 
to most amoebicidal drugs, including car- 
barsone, diodoquin and erythromycin. 

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156 



THE AMOEBAE 



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Chapter 8 



THE 

TELOSPORASIdA 
AND THE 

cocaviA 

PROPER 



All members of the class Telospo- 
rasida are parasitic. They have simple 
spores, without polar filaments. (The 
spore has been lost secondarily in a few 
genera. ) Each spore contains 1 to many 
sporozoites. Pseudopods, cilia and fla- 
gella are absent, except for flagellated 
microgametes in some groups. Locomo- 
tion is by body flexion or gliding. Repro- 
duction is both sexual and asexual, and 
there may or may not be alternation of 
generations. Most Telosporasida are 
saprozoic, but a few, including the tropho- 
zoites of the malaria parasite, are holo- 
zoic. 

Most of the Telosporasida probably 
arose from the Mastigasida, but some may 
have arisen from the Sarcodasida. How- 
ever, it is difficult to be sure of their 
origin because of their lack of the usual 
organelles of locomotion. 

The classification of this and related 
groups is still the subject of considerable 
difference of opinion among taxonomists, 
and that used in this book is not consid- 
ered definitive. It may require several 
generations of parasitologists to work out 
a universally acceptable one. This class 
is divided into 2 subclasses, of which the 
Gregarinasina parasitize invertebrates 
and the Coccidiasina occur in both verte- 
brates and invertebrates. In the latter 
group, the mature trophozoite is ordinar- 
ily intracellular and comparatively small. 

The coccidia and their relatives belong 
to the order Eucoccidiorida. In this order, 
schizogony is present and the life cycle 
involves both sexual and asexual phases. 
Members of the order are found in the 
epithelial and blood cells of vertebrates 
and invertebrates. 

The coccidia proper belong to the sub- 
order Eimeriorina, which is differentiated 
from the other 2 suborders by several fea- 
tures of its life cycle. The macrogamete 
and microgametocyte develop independently, 
the microgametocyte produces many micro- 
gametes, the zygote is not motile, and the 



158 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



159 



NUMBER 
SPOROCYSTS 
PER OOCYST 



NUMBER SPOROZOITES PER SPOROCYST 
I 2 3 4 8 16 n 







8 



16 



u I); 






^SClV 



^■M^i>' 






: ; II i ! 




CYCLOSPORA 





OCTOSPORELLA 



III;; 



■-iihOii); 













PFEIFFERINELLA 

CRYPTDSPORIDIUy ^?l^,y-*5**'* 
iiZZERlA 




ISOSPORA 00RI51ELLA 

WENYONELLA 







PYTHONELLA 



-'JSa®' 






I I I I \ 



\ ^vy^'' / 



[^^.\\y\[{\l>] iSJii; ^ii'j 








Fig. 22. Numbers of sporocysts per oocyst and of sporozoites per sporocyst in the 

genera of the suborder Eimeriorina. (In the genera without sporocysts, the 
numbers of sporozoites per oocyst are given. ) (Original) 



sporozoites are typically enclosed in a 
sporocyst. All the coccidia of domestic 
animals and man, with one possible ex- 
ception, belong to two families, the 
Eimeriidae and Cryptosporidiidae. An- 
other family, the Lankesterellidae, is of 
considerable interest. Becker (1934) 
wrote a classic review of the coccidia. 
Orlov (1956) discussed those of domestic 
animals, but was seriously handicapped 
by lack of information about non- Russian 
work. Becker (1956) and Pelle'rdy (1956, 
1957) have given checklists of the species 
of coccidia. The coccidia of the avian 



orders Galliformes, Anserlformes and 
Charadriiformes were reviewed by Levine 
(1953). 



FAMILY EIMERIIDAE 

Members of this family have a single 
host. Schizogony and gametogony take 
place within the host cells, and sporogony 
ordinarily occurs outside the host's body. 
The oocysts and schizonts lack an attach- 
ment organ. The oocysts contain 0, 1, 2, 
4 or many sporocysts, each containing 1 



160 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



MICROPYLE CAP 
MICROPYLE 




SPORULATED 
EIMERIA OOCYST 



POLAR GRANULE 
STIEOA BODY 

SMALL REFRACTILE GLOBULE 
IN SPOROZOITE 

LARGE REFRACTILE GLOBULE 
IN SPOROZOITE 

SPOROCYST 

OOCYST RESIDUUM 
SPOROCYST RESIDUUM 
SPOROZOITE NUCLEUS 
SPOROZOITE 

INNER LAYER OF OOCYST WALL 
OUTER LAYER OF OOCYST WALL 



Fig. 23. Structures of sporulated Eiiiicria oocyst. 
(Original) 

or more sporozoites. The microgametes 
have 2 flagella. The genera are differen- 
tiated by the number of sporocysts in their 
oocysts and the number of sporozoites in 
each oocyst. 

Morphology . The morphology of a 
typical oocyst, that of Einieria, is shown 
in Fig. 23. The oocyst wall is composed 
of 1 or 2 layers and may be lined by a 
membrane. It may have a micropyle, 
which may be covered by a micropylar 
cap. Within the oocyst in this genus are 
4 sporocysts, each containing 2 sporozoites. 
There may be a retractile polar granule in 
the oocyst. There may be an oocyst resi- 
duum or a sporocyst residuum in the oocyst 
and sporocyst, respectively; these are com- 
posed of material left over after the forma- 
tion of the sporocysts and sporozoites. The 
sporocyst may have a knob, the Stieda body, 
at one end. The sporozoites are usually 
sausage- or comma-shaped, and may con- 
tain 1 or 2 clear globules. 

Location . Most coccidia are intra- 
cellular parasites of the intestinal tract, 
but a few occur in other organs such as the 
liver and kidney. Each species is usually 
found in a specific location within the in- 
testinal tract; some are found in the cecum, 
others in the duodenum, still others in the 
ileum, etc. They may invade different 
cells in these locations. Some species are 
found in the mucosal cells at the tips of 



the villi, others in the crypts and still 
others in the interior of the villi. Their 
location within the host cell also varies. 
Some species are found above the host 
cell nucleus, while others are found be- 
neath it and a few occur inside it. Some 
species enlarge the host cell only slightly, 
while others cause it to become enormous. 
The host cell nucleus is also often greatly 
enlarged even tho it may not be invaded. 

Life Cycle : The life cycles of the 
Eimeriidae are similar, and can be illus- 
trated by that of Ei»ieyia teiiella, which is 
found in the ceca of the chicken (Fig. 24). 
It was first worked out in a classic paper 
by Tyzzer (1929). The oocysts are passed 
in the feces; at this time they contain a 
single cell, the sporont. They must have 
oxygen in order to develop to the infective 
stage, a process known as sporulation or 
sporogony. The sporont, which is diploid, 
undergoes reduction division and throws 
off a retractile polar body. The haploid 
number of chromosomes is 2 (Walton, 
1959). The sporont divides to form 4 
sporoblasts, each of which then develops 
into a sporocyst. Two sporozoites develop 
within each sporocyst. Sporulation takes 
2 days at ordinary temperatures. The 
oocysts are then infective and ready to 
continue the life cycle. 

When eaten by a chicken, the oocyst 
wall breaks, releasing the sporozoites. 
The factors which cause excystation have 
not been determined. Itagaki and Tsubo- 
kura (1958) found that pancreatic juice did 
not cause excystation of E. lenella, and 
Landers (1960) was unable to induce ex- 
cystation by treating the oocysts of E. 
nieschulzi from the rat with pepsin, tryp- 
sin, pancreatin, pancreatic lipase or bile. 
Ikeda (1960), however, reported that pan- 
creatic juice did cause excystation of E. 
teiiella, and that trypsin was the respon- 
sible enzyme. 

According to Challey and Burns (1959) 
and Pattillo (1959), the sporozoites first 
enter the cells of the surface epithelium. 
Pattillo (1959) observed passageways, 
which he called penetration tubes, in the 
striated border and epithelium thru which 
the sporozoites passed. They deploy along 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



161 




Fig. 24. Life cycle of the chicken coccidium, Eimeria tenella. A sporozoite (1) enters 
an intestinal endothelial cell (2), rounds up, grows, and becomes a first gen- 
eration schizont (3). This produces a large number of first generation mero- 
zoites (4), which break out of the host cell (5), enter new intestinal endothelial 
cells (6), round up, grow, and become second generation schizonts (7, 8). 
These produce a large number of second generation merozoites (9, 10), which 
break out of the host cell (11). Some enter new host intestinal endothelial 
cells and round up to become third generation schizonts (12, 13), which pro- 
duce third generation merozoites (14). The third generation merozoites (15) 
and the great majority of second generation merozoites (11) enter new host 
intestinal endothelial cells. Some become microgametocytes (16, 17), which 
produce a large number of microgametes (18). Others turn into macrogametes 
(19, 20). The macrogametes are fertilized by the microgametes and become 
zygotes (21), which lay down a heavy wall around themselves and turn into 
young oocysts. These break out of the host cell and pass out in the feces (22). 
The oocysts then sporulate. The sporont throws off a polar body and forms 4 
sporoblasts (23), each of which forms a sporocyst containing 2 sporozoites 
(24). When the sporulated oocyst (24) is ingested by a chicken, the sporo- 
zoites are released (1). (Original) 



the basement membrane and then pass 
thru it into the lamina propria. Here 
they are engulfed by macrophages and 
carried by them to the glands of Lieber- 
kuhn. They then leave the macrophages 
and enter the epithelial cells of the glands, 



where they are found below the host cell 
nucleus, i.e. , on the side away from the 
lumen. We do not know how common this 
method of penetration is among the coc- 
cidia; Van Doorninck and Becker (1957) 
first found it in E. necatrix of the chicken. 



162 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



Once in a glandular epithelial cell, 
each sporozoite rounds up and becomes a 
first generation schizont. By a process 
of asexual multiple fission (schizogony), 
each schizont forms about 900 first gen- 
eration merozoites, each about 2 to 4/j. 
long. These get their name from the 
Greek word for mulberry, which they re- 
semble before they separate. They break 
out into the lumen of the cecum about 2. 5. 
to 3 days after infection. Each first gen- 
eration merozoite enters a new host cell, 
and rounds up to form a second generation 
schizont, which lies above the host cell 
nucleus. By multiple fission it forms 
about 200 to 350 second generation mero- 
zoites about IGfi long. These are found 
5 days after infection. Some of them 
enter new intestinal cells, round up to form 
third generation schizonts, which lie be- 
neath the host cell nuclei and produce 4 to 
30 third generation merozoites about 7ji 
long. 

Most of the second generation mero- 
zoites, however, enter new host cells and 
begin the sexual phase of the life cycle, 
known as gametogony. Most of these 
merozoites turn into female gametes (ma- 
crogametes), which simply grow until they 
reach full size. Some of the merozoites 
turn into male gametocytes (microgameto- 
cytes). Both the macrogametes and mi- 
crogametocytes lie below the host cell 
nuclei. Within each microgametocyte a 
large number of tiny biflagellate micro- 
gametes are formed. These break out 
and fertilize the macrogametes. 

The resultant zygote lays down a wall 
around itself in the following way: The 
macrogametes contain one or two layers 
of eosinophilic plastic granules in their 
cytoplasm; these are composed of muco- 
protein (Kheisin, 1958). They pass to the 
periphery, flatten out and coalesce to 
form the oocyst wall after fertilization. 
The formation of this wall marks the 
transition of a fertilized macrogamete into 
an oocyst. According to Monne and Honig 
(1954), the outer layer of the oocyst wall 
is a quinone-tanned protein and the inner 
layer is a lipid coat firmly associated 
with a protein lamella. 



The oocysts then break out of their 
host cells, enter the intestinal lumen, and 
pass out in the feces. The prepatent per- 
iod, from the time of infection to the ap- 
pearance of the first oocysts in the feces, 
is 7 days. Oocysts continue to be dis- 
charged for a number of days thereafter, 
due to the fact that the sporozoites do not 
all enter the host cells immediately but 
may remain in the lumen for some time, 
and also because many of them are retained 
in a plug of material in the ceca for some 
days before they are eliminated. 

In the absence of reinfection, coccidial 
infections are self-limiting. Asexual re- 
production does not continue indefinitely as 
it does, for example, in Plasmodium. In 
E. tenella, 3 generations of merozoites are 
produced; in other species there may be 1, 
2 or 4. After this, the life cycle enters its 
sexual phase; the oocysts are formed, 
eliminated from the body, and the infection 
is over. Reinfection may take place, but 
the host develops more or less immunity 
following primary infection. 

The number of oocysts produced in an 
animal per oocyst fed depends in part on 
the number of merozoite generations and 
the number of merozoites per generation. 
A single oocyst of E. tenella containing 8 
sporozoites is theoretically capable of pro- 
ducing 2, 520, 000 second generation mero- 
zoites (8 X 900 X 350), each of which can 
develop into a macrogamete or micro- 
gametocyte. 

In E. bonis of cattle, there is only a 
single asexual generation, but a giant 
schizont containing about 120,000 mero- 
zoites is formed (Hammond et al. 1946). 
In the rat, E. nieschidzi is theoretically 
capable of producing 1, 500,000 oocysts 
per oocyst fed, E. miyairii 38,016, and 
E. separata only 1536 (Roudabush, 1937). 
In E. nieschulzi there are 4 generations of 
merozoites, while in the latter two species 
there are only 3, and fewer merozoites are 
usually produced in each than in E. nie- 
sclmlzi. In the rabbit, E. magna produces 
800,000 oocysts per oocyst fed, E. media 
produces 150,000 and £. coecicola 100,000 
(Kheisin, 1947, 1947a). 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



163 



The actual numbers of oocysts pro- 
duced per oocyst fed are usually consider- 
ably lower than the theoretical ones. K 
the host is resistant or immune, it des- 
troys many merozoites, and many others 
pass out in the feces before they have time 
to enter host cells. The infecting dose is 
also an important factor in determining 
the number of oocysts produced. The 
greater the infecting dose, the smaller the 
number of oocysts usually produced per 
oocyst fed. For example. Hall (1934) ob- 
tained a yield of 1, 455, 000 oocysts of E. 
nieschulzi per oocyst fed when the infecting 
dose was 6 oocysts, 1, 029, 666 when it was 
150 oocysts, and 144, 150 when it was 2000 
oocysts. If the infecting dose is too small, 
however, smaller numbers of oocysts are 
produced. Hall (1934) found that when only 
a single oocyst was fed, the yield was 
62,000. 

Similarly, Brackett and Bliznick 
(1950, 1952) found that with E. acervuUna 
of the chicken, 9000 oocysts were produced 
per oocyst fed when the infecting dose was 
200 oocysts, 35, 000 to 72, 000 when it was 
2000 oocysts, 35,000 when it was 10,000 
oocysts, and 7,600 when it was 20,000 
oocysts. With E. maxima of the chicken, 
they found that 11, 500 oocysts were pro- 
duced per oocyst fed when the infecting 
dose was 200 oocysts, 2, 250 when it was 
2000 oocysts, and 940 to 2900 when it was 
10, 000 oocysts. With E. necatrix of the 
chicken, they found that 50, 000 oocysts 
were produced per oocyst fed when the in- 
fecting dose was 200 oocysts, and 2400 
when it was 2000 oocysts. With E. tenella 
of the chicken, they found that the maxi- 
mum number of oocysts produced per 
oocyst fed in numerous experiments was 
400,000. However, in one series of 2- 
week-old chicks this figure ranged from 
1200 for chicks fed 40, 000 oocysts to 
80, 000 when the infecting dose was 50 
oocysts. 

All the factors responsible for these 
results are not known. More effective 
mobilization of the host's defenses is 
probably important, but lack of enough 
epithelial cells to parasitize, sloughing of 
patches of epithelium, increased intes- 
tinal motility with resultant diarrhea and 



elimination of merozoites before they can 
reach a cell, and entrapment of merozoites 
in tissue debris and cecal cores may also 
play a part. 

Pathogenesis . While many species 
of coccidia are pathogenic, many others 
are not. Pathogenicity depends on a num- 
ber of factors, some of which are probably 
still unknown. Among those which might 
be mentioned are the number of host cells 
destroyed per infecting oocyst (which de- 
pends upon the number of merozoite gen- 
erations and the number of merozoites per 
generation) and the location of the parasite 
in the host tissues and within the host cells. 
The size of the infecting dose or doses, 
the degree of reinfection, and the degree 
of acquired or natural immunity of the host 
are also important. 

Even with a pathogenic species, the 
final effect on the host depends on the in- 
terplay between many factors; it may range 
from rapid death in susceptible animals to 
an imperceptible reaction in immune ones. 

If disease is present, the signs are 
those of a diarrheal enteritis. There may 
or may not be blood in the feces, depending 
on the parasite species and severity of in- 
fection. Affected animals gain weight 
poorly, become weak and emaciated, or 
may even die, depending again on the para- 
site species and the size of the infecting 
dose. Young animals are much more com- 
monly affected than older ones. Those ani- 
mals which recover develop an immunity 
to the particular species which infected 
them. However, this is not an absolute 
immunity, and recovered adult animals 
are often continuously reinfected so that 
they carry light infections which do not 
harm them but which make them a source 
of infection for the young. In addition, 
under conditions of stress their immunity 
may be broken down and they may suffer 
from the disease again. 

Differentiation of Species . Both 
morphological and biological characters 
are used to separate the species of coc- 
cidia. Both the endogenous and exogenous 
stages of the life cycle may differ morpho- 
logically. However, since the endogenous 



164 



THE TELOSPORASIDA AND THE COCCIDLA PROPER 



stages of many species are unknown, the 
structure of the oocyst is most commonly 
used. The feeling is sometimes expressed 
that the oocysts have so few structures 
that not many species can be distinguished 
morphologically, but conservative calcu- 
lation shows that at least 2, 654, 208 mor- 
phologically different oocysts are possible 
in the genus Eimeria alone (Levine, 1961). 

A second group of criteria is the loca- 
tion of the endogenous stages in the host. 
This has been discussed above. Host 
specificity is a third criterion. This var- 
ies with the protozoan genus and to some 
extent with the species. In general, the 
host range of Isospora and Tyzzeria spe- 
cies is relatively broad. Several mem- 
bers of the same host order may be in- 
fected by the same species of these genera. 
For example, Isospora bigemina occurs in 
the dog, cat, ferret and mink, while 
Tyzzeria anseris has been found not only 
in the domestic goose and several other 
members of the genus Anser, but also in 
the Canada goose and Atlantic brant (both 
Branla) and whistling swan (Olor). On the 
other hand, the host range of Eimeria spe- 
cies is relatively narrow. A single species 
rarely infects more than one host genus 
unless the latter are closely related. 

Cross-immunity studies are also used 
in differentiating the coccidia of a partic- 
ular host species from each other. Infec- 
tion of an animal with one species of coc- 
cidium produces immunity against that 
species but not against other species which 
occur in the same host. 

Diagnosis : Coccidiosis can be diag- 
nosed by finding the coccidia on micro- 
scopic examination. There are several 
pitfalls in diagnosis. Each species of do- 
mestic and laboratory animal has several 
species of coccidia, some of which are 
pathogenic and some of which are not. 
Since an expert is often needed to differ- 
entiate between some of the species, the 
mere presence of oocysts in the feces, 
even in the presence of disease signs, is 
not necessarily proof that the signs are 
due to coccidia and not to some other 
agent. 



Following recovery from a coccidial 
infection, an animal is relatively immune 
to reinfection with the same species. This 
immunity is not so solid that the animal 
cannot be reinfected at all, but it does 
mean that the resultant infection will be 
low-grade (except possibly under conditions 
of stress) and will not harm the host. Such 
low-grade infections are extremely common, 
i.e., the animals have coccidiasis rather 
than coccidiosis. Hence, the presence in 
the feces of oocysts of even highly patho- 
genic species of coccidia does not neces- 
sarily mean that the animal has clinical 
coccidiosis. 

On the other hand, coccidia may cause 
severe symptoms and even death early in 
their life cycle before any oocysts have 
been produced. This occurs commonly, 
for example, with E. tenella of the chicken 
and E. ziirnii of the ox. Consequently, 
failure to find oocysts in the feces in a 
diarrheal disease does not necessarily 
mean that the disease is not coccidiosis. 

The only sure way to diagnose coccid- 
iosis, then, is by finding lesions containing 
coccidia at necropsy. Scrapings of the le- 
sions should be mixed on a slide with a 
little physiological salt solution and exam- 
ined microscopically. It is not enough to 
look for oocysts, but schizonts, mero- 
zoites, gametes and gametocytes inside 
the host cells must be sought for and rec- 
ognized. 

Some species of coccidia can be iden- 
tified from their unsporulated oocysts, 
but study of the sporulated oocysts is often 
desirable. Oocysts can be sporulated by 
mixing the feces with several volumes of 
2. 5% potassium bichromate solution, plac- 
ing the mixture in a thin layer in a Petri 
dish and allowing it to stand for 1 day to 
2 weeks or more, depending on the spe- 
cies. The potassium bichromate prevents 
bacterial growth which might kill the pro- 
tozoa, and the thin layer is necessary so 
that oxygen can reach the oocysts. 

Treatment . The first compound 
found effective against coccidia was sulfur, 
which was introduced by Herrick and 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



165 



Holmes (1936). Later, Hardcastle and 
Foster (1944) introduced borax. Neither 
of these compounds was a satisfactory 
anticoccidial drug. Sulfur interferes with 
calcium metabolism, causing a condition 
known as sulfur rickets in chickens, while 
borax is only partially effective and in 
addition is toxic in therapeutic doses. 

The first practical anticoccidial drugs 
were the sulfonamides, of which the first 
to be used was sulfanilamide, introduced 
by P. P. Levine (1939). Since that time 
many different drugs have been used, 
particularly against Eimeria lenella of the 
chicken. These include not only sulfon- 
amides but also derivatives of phenylar- 
sonic acid, diphenylmethane, diphenyldi- 
sulfide, diphenylsulfide, nitrofuran, tri- 
azine, carbanilide, imidazole and benza- 
mide. Several thousand papers have 
probably been published on coccidiostatic 
drugs, and their use in poultry production 
is so common in the United States that it 
is difficult to obtain a commercial feed 
which does not contain one or another of 
them. They are used to a considerably 
lesser extent for other classes of live- 
stock. 

None of these drugs will cure a case 
of coccidiosis once signs of the disease 
have appeared. They are all prophylactic. 
They must be administered at the time of 
exposure or soon thereafter in order to be 
effective. They act against the schizonts 
and merozoites and occasionally against 
the sporozoites, preventing the life cycle 
from being completed. They are not 
effective against the gametes. Hence, 
since exposure in nature is continuous, 
these drugs must be fed continuously. 
This is usually done by mixing them with 
the feed or water. 

Nowhere is a knowledge of the normal 
course of the disease more important than 
in interpreting the results of treatment of 
coccidiosis, and nowhere is the controlled 
experiment more important than in research 
in this field. This disease is self-limiting 
not only in the individual patient but also in 
a flock or herd. In a typical outbreak of 
coccidiosis, signs of disease appear in 
only a few animals at first, the number of 
affected animals builds up rapidly to a 



peak in about a week, and then the disease 
subsides spontaneously. In the early 
stages, most farmers do little, thinking 
that the condition is unimportant and will 
soon be over. Once more animals become 
affected and losses increase, it takes a 
little time to establish a diagnosis, so 
treatment is often not started until the out- 
break has reached its peak. Under these 
circumstances, it matters little what treat- 
ment is used- -the disease will subside. 
This is the reason why so many quack rem- 
idies used to get glowing testimonials from 
satisfied users. 

A similar course of events is encoun- 
tered by the small animal practitioner. 
The patient with coccidiosis is not brought 
to him until it is already sick. By this 
time it is too late for any anticoccidial 
drug to be of value, altho supportive treat- 
ment and control of secondary infections 
may be helpful. If the patient recovers, 
however, whatever drug happened to be 
used is often given undeserved credit. 
Such drugs are like Samian clay, which 
was Galen's favorite remedy. He said 
that it cured all diseases except those 
which were incurable, in which case the 
patient died. 

Collins (1949) described the "four-pen 
test" which should be used in evaluating 
coccidiostats and other drugs. The birds 
in one pen are infected with coccidia and 
treated with the compound under test. 
Those in the second pen are infected and 
untreated, those in the third pen are un- 
infected and treated, and those in the 
fourth pen are uninfected and untreated. 
Comparison of the first 2 pens determines 
whether the compound has any effect on 
the coccidia; the third and fourth pens are 
used to determine whether the drug has 
any effect on the chickens themselves and 
to make sure that no extraneous infection 
has taken place. 

After an animal has been receiving a 
coccidiostatic drug for some time during 
exposure to infection, it develops an im- 
munity to the coccidia. This occurs be- 
cause the sporozoites are not affected by 
the drug but invade the tissue cells and 
stimulate the host's defenses. 



166 



THE TELOSPORASIDA AND THE COCCIDLA PROPER 



After coccidiostats had been mixed in 
poultry feeds for a number of years, it 
was inevitable that drug resistant strains 
of coccidia would appear. The first report 
of this was by Waletzky, Neal and Hable 
(1954), who found a field strain of Eiiiieria 
tenella resistant to sulfonamides. Cuckler 
and Malanga (1955) reported on 40 field 
strains of chicken coccidia which were re- 
sistant to one coccidiostat or another, and 
drug resistance is now a well-known com- 
plicating factor in the use of these agents. 
A race has developed between the coccidia 
and the pharmaceutical houses, and some 
day, horribile dictu, we may be reduced 
to sanitation to control coccidia. 

Mixed Infections . All domestic ani- 
mals have more than one species of coc- 
cidia. Some are highly pathogenic, others 
less so, and still others practically non- 
pathogenic. Pure infections with a single 
species are rare in nature, so the ob- 
served effect is the resultant of the com- 
bined actions of the particular mixture of 
coccidia and other parasites present, to- 
gether with the modifying effects of the 
nutritional condition of the host and envi- 
ronmental factors such as weather and 
management practices. 

In the remainder of this chapter, each 
species of coccidium in a particular host 
animal will be taken up first, and then a 
general discussion of coccidiosis in the 
host will follow. 



Genus EIMEMA Schneider, 1875 

In this genus the oocyst contains 4 
sporocysts, each of which contains 2 
sporozoites. 



EIMERIA ALABAMENSIS 
CHRISTENSEN, 1941 

Hosts : Ox. 

Location : Posterior half of ileum, 
especially within a few feet forward from 
the ileo-cecal valve. In heavy infections, 
the cecum and upper colon may be in- 
volved. 



Geographic Distribution : 
America. 



North 



Prevalence : Davis, Boughton and 
Bowman (1955) found this species in 93% 
of 102 dairy calves in 6 herds in south- 
eastern United States in a weekly fecal 
survey; they found it in 24% of 135 animals 
from which only a single fecal sample was 
taken; it was present in all of 26 herds 
from which at least 5 animals were ex- 
amined. Hasche and Todd (1959) found it 
in 42% of 355 cattle in Wisconsin. 

Morphology : The oocysts have been 
described by Christensen (1941). They 
measure 13 to 24 by 11 to 16 ji with a mean 
of 18.9 by 13.4jLt. They are typically piri- 
form but may also be subellipsoidal or sub- 
cylindrical. The oocyst wall is thin, 
delicate, homogeneous, transparent, color- 
less to greyish-lavender to pale brownish 
yellow, slightly thinner at the narrow end 
but without a perceptible micropyle. Dur- 
ing sporulation there is a parachute-shaped 
cap at each end of the sporoblasts. Spor- 
ulation takes 4 to 5 days. The sporocysts 
are elongate and gently tapered. Neither 
oocyst nor sporocyst residua are present. 
A polar granule is presumably absent. 

Life Cycle : Davis, Bowman and 
Boughton (1957) described the life cycle of 
E. alabamensis . It is unusual in being an 
intranuclear parasite, occurring within 
the nuclei of the epithelial cells at the tips 
of the villi. Excysted sporozoites were 
seen in the cytoplasm of the intestinal 
epithelial cells 2 days after infection. 
They enter the nuclei and round up, form- 
ing schizonts. These are present as early 
as 2 days after infection and are uncommon 
by the 8th day. They form 16 to 32 mero- 
zoites, which are slender and spindle- 
shaped while still within the parent schizont 
but appear short, with bluntly rounded ends 
in the intracellular spaces and crypts. 
Davis, Bowman and Boughton (1957) thought 
that there is probably more than one gen- 
eration of schizonts. 

Macrogametes and microgametocytes 
first appear 4 days after infection. Most 
are found in the lower third of the small 
intestine, but they may invade the cecum 



THE TELOSPORASIDA AND THE COCCIDLA PROPER 



167 



and upper colon in heavy infections. 
Young oocysts still in the host cell nuclei 
first appear 6 days after infection. Mul- 
tiple infections are common, as many as 
3 schizonts or microgametocytes and 4 or 
5 macrogametes or oocysts having been 
found in a single host cell nucleus. This 
crowding may affect the shape of the 
oocysts in heavy infections, making some 
of them wedge-shaped or asymmetrical. 

The prepatent period in experimentally 
infected calves was found by Davis, Bough- 
ton and Bowman (1955) to range from 6 to 
13 days with a mean of 8 to 9 days. The 
patent period ranged from 1 to 10 days with 
a mean of 4. 6 days in 21 low-grade infec- 
tions, and from 1 to 13 days with a mean 
of 7. 2 days in 72 heavy infections. 

Pathogenesis : Under field conditions, 
E. alabainensis is considered essentially 
non- pathogenic. However, Boughton (1943) 
produced clinical coccidiosis in 5 young 
calves by feeding them 200 million oocysts. 
Within 5 days they developed a severe 
diarrhea, with yellowish feces having a 
characteristic acrid odor. They become 
thin, and 1 calf died on the 8th day and 
another on the 14th. In the first calf the 
lower half of the small intestine was hy- 
peremic and there was massive tissue in- 
volvement with merozoites and macro- 
gametes. In the second calf there was 
enteritis in only the last 3 feet of the 
ileum, and only a few parasites remained 
in the tissues, most of these being within 
1 foot of the ileocecal valve. 

Davis, Boughton and Bowman (1955) 
fed two 14-month-old calves 140 million 
oocysts. One became diarrheic on the 
fifth day. Its feces were watery, yellow- 
ish green, with some bloody mucus and a 
sharp, acrid odor. The diarrhea grad- 
ually subsided. In the second calf the 
feces were soft toward the end of the pre- 
patent period. A 7-month-old heifer which 
had previously been exposed to coccidial 
infection had a slight diarrhea on the 9th 
and 11th days following similar exposure, 
and a 2-year-old cow remained normal. 

Immunity : Reinfection is considered 
common in the field. Davis, Boughton and 



Bowman (1955) reported that in 58 attempts 
to reinfect calves 2 or more times, there 
were 39 high-grade infections, 11 low- 
grade infections and 8 failures. Nine of 
the low-grade infections and 7 of the fail- 
ures followed the third or subsequent in- 
oculations. Some animals were reinfected 
as many as 4 times before reinfection at- 
tempts failed. 



EIMERIA AUBURNENSIS 
CHRISTENSEN AND PORTER, 1939 

Synonym : Eimeria ildefonsoi Torres 
and Ramos, 1939. 

Hosts : Ox. In addition, Bohm and 
Supperer (1956) reported finding this spe- 
cies in a wild roe deer in Austria, but 
gave no morphological information on it. 

Location: Unknown. Oocysts found 
in feces. 

Geographic Distribution : North 
America, South America (Brazil), Europe 
(Austria, Spain, England). 

Prevalence : E. anbiiruensis is one of 
the commonest coccidia of cattle in North 
America. Davis and Bowman (1952) found 
it in all of 20 calves in Alabama. Hasche 
and Todd (1959) found it in 45% of 355 
cattle in Wisconsin. Torres and Ramos 
(1939) found it in 32% of 146 cattle in Brazil. 
Supperer (1952) found it in 3% of 130 cattle 
in Austria. According to Lapage (1956), 
Watkins found it in 91% of the calves he 
examined in Devonshire. 

Morphology : The oocysts have been 
described by Christensen and Porter (1939) 
and Christensen (1941). They measure 32 
to 46 by 20 to 26 fi with a mean of 38. 4 by 
23. 1 ILL. Their length-width ratios range 
from 1 . 32 to 2. 08 with a mean of 1 . 67. 
They are typically elongate ovoid, but vary 
between sub-ellipsoidal and markedly ta- 
pered. The micropyle appears as a thin, 
pale area at the small end in unstained 
specimens, but when stained with iodine- 
eosin in physiological salt solution, a def- 
inite gap covered by a narrow black line 
which may be a flat operculum is seen. 



168 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



A membrane lines the oocyst wall, which 
is illustrated as composed of a single 
layer. The oocyst wall is 1 to 1. 5 /i thick, 
typically smooth, homogeneous, transpar- 
ent and yellowish brown; relatively rarely 
it may be semi-transparent and heavily 
mammillated, and all gradations between 
these two conditions occur. The smooth- 
walled forms are more common than the 
rough. 

The sporulation time at room temper- 
ature in Alabama is 2 to 3 days. There is 
no oocyst residuum or polar granule. The 
sporocysts were illustrated by Christensen 
and Porter (1939) as elongate with one end 
pointed. The sporozoites lie lengthwise, 
head to tail, in them and contain 3 clear 
globules, 1 of which may be the nucleus. 
The sporocyst residuum consists of 
rounded masses or individual granules be- 
tween the sporozoites. 

Christensen and Porter (1939) showed 
that the rough and smooth forms were the 
same species by infecting a calf with rough 
oocysts and recovering all types, but pre- 
dominantly smooth ones, from it. 

Life Cycle : The endogenous stages 
of this species are unknown. Christensen 
and Porter (1939) found that the prepatent 
period in one calf was 24 days. Large 
numbers of oocysts were discharged for 3 
days, and small numbers for the next few 
weeks. 

Pathogenesis : Christensen and Por- 
ter (1939) produced a profuse, watery, 
green diarrhea accompanied by slight apa- 
thy in a 2-week-old calf following admin- 
istration of 8000 sporulated oocysts. The 
signs appeared 9 days after infection (i.e. , 
15 days before the first oocysts appeared 
in the feces) and continued for 5 days. 
According to Davis and Bowman (1952), 
infections with E. aubiiynensis are usually 
accompanied by straining and the passing 
of visible blood and mucus, especially 
following experimental inoculation with 
large numbers of oocysts or in natural 
outbreaks where contamination is heavy. 



EIMERIA BOVIS 
(ZUBLIN, 1908) 
FIEBIGER, 1912 

Synonyms : Coccidium bovis, 
Elmer ia canadensis (pro parte), Eimcria 
smithi, Eimeria thianelhi, Globidiiiiii 
fusiformis (?). 

Hosts : Ox, zebu, water buffalo. 
Wilson (1931) was unable to infect pigs or 
goats with this species. 

Location : The schizonts are mostly 
in the small intestine and the sexual stages 
in the cecum, colon and terminal ileum. 

Geographic Distribution : Worldwide. 

Prevalence : This is one of the com- 
monest coccidia of cattle. Boughton (1945) 
found it in 41% of 2492 bovine fecal samples 
in south-eastern U.S. Hasche and Todd 
(1959) found it in 41% of 355 cattle in Wis- 
consin. Supperer (1952) found it in 66% of 
130 cattle in Austria. Cordero del Cam- 
pillo (1960) reported it and other bovine 
species in Spain. Torres and Ramos (1939) 
found it in 49% of 136 cattle in Brazil. 
Yakimoff, Gousseff and Rastegaieff (1932) 
found it in 40% of 126 cattle in Uzbekistan. 
Yakimoff (1933) found it in 47% of 17 zebus, 
23% of 30 water buffaloes and 39% of 44 
cattle in Azerbaidzhan. Marchenko (1937) 
found it in 54% of 137 cattle in the North 
Caucasus. Rao and Hiregaudar (1954) 
stated that it is common in Bombay State, 
India. Ruiz (1959) found it in 7% of 100 
adult cattle in the San Jose, Costa Rica 
abattoir. 

Morphology : The oocysts of £. bovis 
were described by Christensen (1941). 
Five hundred oocysts measured 23 to 34 
by 17 to 23 n with a mean of 27. 7 by 20. 3 ji . 
Their length-width ratios ranged from 1. 1 
to 1 . 8 with a mean of 1 . 37. They are typ- 
ically stoutly ovoid and somewhat blunted 
across the narrow end, but vary consider- 
ably in shape, especially in heavy infec- 
tions, subellipsoidal, asymmetrical and 
elongated, tapered oocysts also occurring. 



THE TELOSPORASTDA AND THE COCCIDIA PROPER 



169 



The micropyle is a lightened area at the 
small end. The oocyst wall is smooth, 
homogeneous, transparent, pale cloudy, 
greenish brown to yellowish brown, and 
slightly thinner toward the micropylar end. 
The wall is not so delicate as that of E. 
alaba))ieiisis. It is darker than that of E. 
alabai)ieiisis and lighter than that of E. 
aubnriiensis. Christensen (1941) illus- 
trated the wall as composed of a heavy 
inner layer and a very thin, transparent 
outer layer, but he did not mention layers 
in his description. An oocyst residuum 
and polar granule are absent. A sporocyst 
residuum is present. 

The sporulation time is 2 to 3 days. 

Life Cycle : Hammond et al. (1946) 
described the endogenous stages of the 
life cycle of E. bovis in detail. There is 
a single asexual generation. The sporo- 
zoites invade the endothelial cells of the 
lacteals of the villi in the posterior half 
of the small intestine. These cells be- 
come detached from the lacteal lining and 
lie free and greatly swollen in the lumens 
of the lacteals. The schizonts are first 
found 5 days after infection. They grow to 
giant size, becoming mature 14 to 18 days 
after infection. A few may still be found 
as long as 30 days after inoculation, but 
most of these are degenerate. The mature 
schizonts measure 207 to 435 by 134 to 
267 jLi with a mean of 281 by 303 ji and con- 
tain 55,000 to 170,000 (mean, 120,000) 
merozoites. They are easily visible to 
the naked eye as whitish balls, and their 
presence was first pointed out by Boughton 
(1942) as a macroscopic lesion which could 
be used in diagnosing coccidiosis. 

The merozoites are 9 to 15jj, (mean, 
11.6jLi) long and about 2/i wide. They are 
rounded at one end and taper abruptly to a 
point at the other. The nucleus is near 
the pointed end. 

The sexual stages usually occur only 
in the cecum and colon, but in heavy in- 
fections they may be found in the terminal 
3 or 4 feet of the small intestine. They 
occur in the epithelial cells of the intes- 
tinal glands. The cells at the base of the 
glands are invaded first, and later the 



rest of the gland becomes involved. The 
first sexual stages appear 17 days after 
inoculation. The macrogametes contain 
plastic granules in their cytoplasm, there 
being 1 layer of small granules near the 
surface and a less distinct layer of larger 
granules beneath it. Fertilization was not 
seen, but 2 stages in the union of nuclei 
were seen before formation of the oocyst 
wall. 

According to Walton (1959), the hap- 
loid number of chromosomes in E. bovis 
is 2. 

Oocysts appear 16 to 21 days after 
experimental infection. Large numbers 
are discharged for 5 to 7 days, and 
smaller numbers are present in the feces 
for 2 to 3 weeks. In 28 calves studied by 
Senger et al. (1959), oocysts were dis- 
charged for 7 to 15 days with a mean of 
11.5 days. 

Pathogenesis : E. bovis is one of the 
2 most pathogenic of the bovine coccidia. 
Hammond, Davis and Bowman (1944) 
studied its effects in experimentally in- 
fected calves. An infective dose of 
125,000 oocysts or more was generally 
needed to cause marked signs. These 
appeared about 18 days after infection, 
and consisted of diarrhea and/or bloody 
diarrhea, tenesmus, and temperatures as 
high as 106. 6° F. One of 4 calves given 
125,000 oocysts become moribund due to 
coccidiosis, while single calves given 
250, 000 to 1, 000, 000 oocysts all died or 
became moribund 24 to 27 days after in- 
fection. 

The most severe pathologic changes 
occur in the cecum, colon and terminal 
foot of the ileum. They are due to the 
sexual stages of the coccidia. At first 
the mucosa is congested, edematous 
and thickened, with petechiae or diffuse 
hemorrhages. Its lumen may contain a 
large amount of blood. Later, the mucosa 
is destroyed and sloughed, and a patchy 
or continuous membrane forms over its 
surface. The sub mucosa may also be 
destroyed. If the animal survives, 
both mucosa and submucosa are later 
replaced. 



170 



THE TFLOSPORASIDA AND THE COCCIDLA PROPER 



Immunity : Senger et a I. (1959) found 
that inocula of 10, 000, 50, 000 or 100, 000 
oocysts of E. bovis produced a good deal 
of immunity to reinfection. The immunity 
developed rapidly, calves being resistant 
to challenge 14 days after immunization. 
Immunity persisted to a moderate degree 
for 2 to 3 months in young calves, and in 
one group of yearlings there was appar- 
ently a high degree of immunity 7 months 
after the last inoculation. An inoculum 
of 10,000 oocysts did not produce as great 
an immunity as 50,000 or 100,000 oocysts; 
there was no significant difference in the 
degree of immunity produced by the higher 
doses. All these immunizing doses caused 
diarrhea and bloody feces; the greater the 
number of oocysts administered, the more 
severe and longer-lasting the resultant 
disease. 

Hammond el al. (1959) found that this 
immunity was not directed against the 
schizonts but against the sexual stages or 
merozoites. They found no significant 
differences in numbers or size of schi- 
zonts between immunized and non-immu- 
nized calves, but the latter had many more 
sexual stages than the former. 

Remarks : Hassan (1935) described 
the sporozoites and schizonts of an organ- 
ism which he named Globidium fiisiformis 
from 5 zebus with dysentery and rinder- 
pest in India. The schizonts were found 
in the abomasum, duodenum and ileum; 
they often occurred anterior to the ileo- 
cecal valve, but were not found in the 
large intestine. They were whitish and 
measured 0. 4 to 1. by 0. 8 mm. The 
merozoites were elongate, spindle- 
shaped, slightly curved-, with one end 
bluntly rounded and the other finely 
pointed, 13 by 2 to 2. 5 /i . This form may 
well be Eimeria bovis. However, the 
fact that schizonts were found in the abo- 
masum as well as in the small intestine 
made Hammond et al. (1946) hesitate to 
assign it to this species, since they never 
found schizonts of E. bovis in the abo- 
masum. 



EIMERLi BRASILIENSIS 
TORRES AND RAMOS, 1939 

Synonyms : Eimeria boehmi Supperer, 
1952; Eimeria orlovi Basanov, 1952. 

Hosts : Ox, zebu. In addition, Bohm 
and Supperer (1956) reported finding this 
species in several chamois in Austria, 
but gave no morphological information on 
which a comparison could be based. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : North Amer- 
ica, South America (Brazil), Europe(Aus- 
tria), Africa (Nigeria), USSR (Kazakhstan). 

Prevalence : Davis and Bowman (1952) 
stated that this species is uncommon in 
Alabama. Hasche and Todd (1959) found 
it in 6% of 927 cattle in Wisconsin. Torres 
and Ramos (1939) found it in 3% of 146 
cattle in Brazil. Supperer (1952) found it 
in 7% of 130 cattle in Austria. Lee and 
Armour (1958) saw it frequently in cattle 
in Nigeria. Basanov (1952) found it in 
Kazakhstan, USSR. 

Morphology : The oocysts are ellip- 
soidal, colorless to yellowish or pinkish, 
smooth, 31 to 49 by 22 to 33 ji, with a 
mean of 36 to 38 by 26 to 27 j^. The oocyst 
wall is composed of a single layer. The 
micropyle is 5 to 6^ in diameter, and is 
covered by a micropylar cap 8 to 12 [^ wide 
and 1. 5 to 3 (i high; this cap tends to col- 
lapse on storage in unprepared feces in 
the refrigerator. An oocyst polar granule 
is present. An oocyst residuum is absent. 
The sporocysts are elongate ovoid (with a 
fine "operculum", according to Torres and 
Ramos), 16 to 22 by 7 to 9 1^ (Supperer). 
A sporocyst residuum is present. 

The sporulation time is 6 to 7 days at 
27° C (Lee and Armour, 1958) or 12 to 14 
days at 20° C (Supperer, 1952). 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 



THE TELOSPORASIDA AND THE COCCIDLA PROPER 



171 



EIMERIA BUKIDNONENSIS 
TUBANGUI, 1931 

Synonyms : Eimeria ivyomingensis 
Huizinga and Winger, 1942; Eimeria 
khurodensis Rao and Hiregaudar, 1954. 

Hosts : Ox, zebu. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : North 
America, Philippines, USSR, Africa 
(Nigeria), South America (Brazil). 

Prevalence : This species is rela- 
tively uncommon. Baker (1938, 1939) and 
Christensen (1938) reported it in a heifer 
in New York, Christensen (1941) found it 
infrequently in Alabama, Huizinga and 
Winger (1942) found it in 10 cattle in 
Wyoming, and Hasche and Todd (1959) 
found it in 5% of 355 cattle in Wisconsin. 
Tubangui (1931) found it in 1 of 28 zebus 
in the Philippines. Yakimoff, Gousseff 
and Rastegaieff (1932) found it in 2 of 126 
oxen in Uzbekistan. Yakimoff (1933) found 
it in 2 of 17 zebus and 1 of 41 oxen in 
Azerbaidzhan. Marchenko (1937) found it 
in 0. 7% of 137 cattle from the North Cau- 
casus. Yakimoff (1936) found it in 1 of 49 
cattle in Brazil, Torres and Ramos (1939) 
reported it from 8% of 146 cattle in Brazil. 
Lee (1954) found it in a Fulani calf (zebu) 
in Nigeria. 

Morphology : The oocysts are piri- 
form, yellowish brown to dark brown, 33 
to 54 by 24 to 35jj,. Their length-width 
ratio is 1. 3 to 1.8 with a mean of about 
1. 4. The oocyst wall is about 2 to 4 jj. 
thick except at the micropylar end, where 
it is thin. It is composed of 2 layers (3 
according to Yakimoff, 1933), the outer 
one thick and the inner one a tough mem- 
brane. Tubangui (1931), Yakimoff (1933), 
and Lee (1954) described the wall as 
radially striated, but the only American 
author to note this feature was Baker 
(1939). The oocyst wall is speckled, and 
rather rough. The micropyle is conspic- 
uous, 3. 5 to 7jLj, in diameter. An oocyst 
residuum and polar granule are absent. 
The sporocysts are elongate lemon-shaped. 



14 to 22 by 9 to 12 |j.. A Stieda body is 
possibly present. Definite sporocyst res- 
idual material is absent. The sporozoites 
were described by Tubangui as more or 
less roundish or reniform and illustrated 
without refractile globules. According to 
Huizinga and Winger, refractile globules 
are prominent, and it is possible that 
Tubangui mistook these for the sporozoites 
proper. 

Rao and Hiregauder (1954) described 
a new species, E. khurodensis , from zebus 
in India. It failed to sporulate, and there 
is nothing in their description which differs 
from that of E. biikidnonensis. 

The sporulation time is 4 to 7 days 
according to Christensen (1941), 5 to 7 
days according to Huizinga and Winger 
(1942), 24 to 27 days according to Baker 
(1939). 

Life Cycle : Unknown. Baker (1939) 
found that oocysts first appeared in an ex- 
perimentally infected calf on the 10th day. 

Pathogenesis : Baker (1939) observed 
a tendency toward a diarrheic condition 
from the 7th to 15th days after experi- 
mental infection of a 70-day old calf with 
55 oocysts. 



EIMERIA CANADENSIS 
BRUCE, 1921 

Synonyms : Eimeria zurnabadensis . 

Hosts : Ox, zebu. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : North Amer- 
ica, USSR (Azerbaidzhan). 

Prevalence : This species is quite 
common in the United States. Hasche and 
Todd (1959) found it in 35% of 355 cattle in 
Wisconsin. 

Morphology : This species has been 
described by Christensen (1941). The 
oocysts are 28 to 37 by 20 to 27 jm with a 



172 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



mean of 32. 5 by 23.4 /i. Their length- 
width ratio is 1 . 2 to 1 . 6 with a mean of 
1. 39. They are typically ellipsoidal, but 
vary from nearly cylindrical to stoutly 
ellipsoidal and occasionally slightly ta- 
pered. The oocyst wall is transparent, 
about 1 fi thick in the middle, slightly 
thinner at each end, delicately yellowish 
brown (paler toward the ends), normally 
smooth, and apparently composed of a 
single layer lined by a membrane. The 
micropyle is an inconspicuous gap in the 
wall at one end, appearing covered with a 
thin, dark refraction line. An oocyst 
residuum and polar granule are absent. 
The sporocysts were not described by 
Christensen (1941). The sporulation time 
is 3 to 4 days. 

Life Cycle : Unknown. 

Pathogenesis : Apparently slight. 



EIMERIA CYLINDRICA 
WILSON, 1931 

Hosts : Ox, zebu. Wilson (1931) was 
unable to infect pigs or goats with this 
species. 

Location: Unknown. Oocysts found 
in feces. 



a mean of 1. 67. The oocyst wall is thin, 
smooth, homogeneous, transparent, color- 
less to slightly tinted, and presumably 
composed of a single layer. A micropyle 
is absent, altho the wall is slightly paler 
at one end. An oocyst residuum and polar 
granule are absent. A sporocyst residuum 
is present, but there is no sporocyst Stieda 
body. The sporozoites are elongate, lying 
lengthwise in the sporocysts and filling 
them. (According to Rao and Hiregaudar, 
1954, the sporocysts measure 6 to 8 by 2 
to 4/i and the sporozoites are very small, 
rounded bodies. ) The sporulation time is 
2 days. 

The oocysts of E. cylindrica intergrade 
to some extent with those of E. ellipsoidalis 
in size and shape, but other characters in- 
dicate that they are separate species. 

Life Cycle : Unknown. Wilson (1931) 
found oocysts in a calf from the eleventh 
to twentieth days after experimental infec- 
tion. 

Pathogenesis : This species appears 
to be somewhat pathogenic. Wilson (1931) 
observed blood in the feces of an experi- 
mentally infected calf 6 days after infection. 
Rao and Hiregaudar (1954) considered this 
species pathogenic in zebu calves. 



Geographic Distribution : North Amer- 
ica, Europe (Austria), India. 



EIMERIA ELLIPSOIDALIS 
BECKER AND FRYE, 1929 



Prevalence : This species is quite 
common. Hasche and Todd (1959) found it 
in 20% of 355 cattle in Wisconsin. Supperer 
(1952) found it in 4% of 130 cattle in Austria. 
Rao and Hiregaudar (1954) considered it 
quite prevalent in zebu calves in Bombay. 
Ruiz (1959) found it in 1% of 100 adult cattle 
in the San Jose, Costa Rica abattoir. 

Morpholog y: This species has been 
described by Wilson (1931) and Christensen 
(1941). The oocysts are 16 to 28 by 12 to 
16^1 with a mean of about 23 by 14 (i. They 
are typically cylindrical, their sides being 
nearly parallel thruout their middle third, 
but they may vary from ellipsoidal to nar- 
row cylinders twice as long as wide. The 
oocyst length-width ratio is 1. 3 to 2. with 



Hosts : Ox, zebu, water buffalo. 

Location: Small intestine. 

Geographic Distribution : North Amer- 
ica, Europe (Austria, Spain), USSR. 

Prevalence : This species is common 
in cattle. Boughton (1945) found it in 45% 
of 2492 bovine fecal samples from south- 
eastern United States and remarked that 
its oocysts comprised 40 to 50% of the total 
oocyst population in 959 samples from over 
100 calves 3 to 12 weeks old. Christensen 
(1941) found its oocysts more frequently 
than those of any other species in the feces 
of healthy calves in Alabama during early 
natural infection. Hasche and Todd (1959) 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



173 



found it in 43% of 355 cattle in Wisconsin. 
Supperer (1952) found it in 15% of 130 
cattle in A-ustria. Yakimoff, Gousseff and 
Rastegaieff (1932) found it in 23% of 126 
oxen in Uzbekistan. Yakimoff (1933) found 
it in 27% of 41 oxen, 6% of 17 zebus and 
52% of 21 water buffaloes in Azerbaidzhan. 
Marchenko (1937) found it in 16% of 137 
cattle in the North Caucasus. Ruiz (1959) 
found it in 3% of 100 adult cattle in the San 
Jose, Costa Rica abattoir. 

Morphology : The oocysts have been 
described by Becker and Frye (1929) and 
Christensen (1941), among others. They 
are 12 to 27 by 10 to 18 fi with a mean of 
17 by 13|Lt. Their length- width ratio is 
1 . to 1 . 6 with a mean of 1 . 30. They are 
predominantly ellipsoidal, but vary in 
shape from spherical to almost cylindri- 
cal, the spherical and subspherical oocysts 
occurring in the smaller size range. The 
oocyst wall is thin, smooth, presumably 
composed of a single layer, homogeneous, 
transparent, colorless to pale lavender or 
pale yellowish, and slightly thinner and 
paler at one end, suggesting a possible 
micropyie. A true micropyle is apparently 
absent, however. An oocyst residuum and 
polar granule are absent. A sporocyst 
residuum is present. The sporocysts were 
illustrated by Becker and Frye (1929) with- 
out a Stieda body. The sporocysts (in the 
zebu) measure 13 to 14 by 4. 5 fi according 
to Yakimoff (1933). The sporozoites were 
illustrated by Becker and Frye (1929) with- 
out clear globules. 

The sporulation time is 2 to 3 days. 

Life Cycle : Unknown. The endogen- 
ous stages occur in the epithelial cells of 
the small intestine mucosa, according to 
Boughton (1945). 

Pathogenesis : According to Boughton 
(1945), this species often causes nonbloody 
diarrhea in calves 1 to 3 months old. 



EIMERIA PELLITA 
SUPPERER, 1952 

Hosts: Ox. 



Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : Europe 
(Austria). 

Prevalence : Supperer (1952) found 
this species in 5% of 130 cattle in Austria. 

Morphology : This species has been 
described by Supperer (1952). The oocysts 
are 36 to 41 by 26 to 30)ii , ovoid, with a 
flattened small end. There is a micropyle 
at the small end. The oocyst wall is rel- 
atively thick and dark brown. The surface 
of the oocyst bears numerous small, uni- 
formly distributed protuberances in the 
form of small, blunt points which give the 
wall a velvety appearance. An oocyst polar 
granule and residuum are absent. The 
sporocysts are elongate ovoid, 14 to 18 by 
6 to 8|i, without a Stieda body. A sporo- 
cyst residuum is present, usually compact. 
The sporozoites lie lengthwise in sporo- 
cysts, with 2 refractile globules. The 
sporulation time is 10 to 12 days. 

It is possible that E. pellita is a syn- 
onym of E. bukidnonensis . However, it 
differs from it in the velvety appearance 
described for its oocyst wall; the oocyst 
wall of E. bukidnonensis has been des- 
cribed as speckled, and as a matter of fact 
Supperer' s drawing of E. pellita looks 
speckled, too. Other differences are that 
a sporocyst residuum has not been des- 
cribed in E. bukidnonensis, while E. pellita 
has a prominent one, and the sporocysts of 
E. bukidnonensis are somewhat pointed at 
one end (with a Stieda body?), while those 
of E. pellita are not. 

Life Cycle : Unknown. 

Pathogenesis: Unknown. 



EIMERIA SUBSPHERICA 
CHRISTENSEN, 1941 

Hosts : Ox. 

Location : Unknown. Oocysts found 
in feces. 



174 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



Geographic Distribution : 
America. 



North 



Prevalence: 



This species is rela- 
Christensen (1941) 



tively uncommon, 
found it in 6 calves in Alabama, never in 
large numbers. Hasche and Todd (1959) 
found it in 11% of 355 cattle in Wisconsin. 

Morphology : This species has been 
described by Christensen (1941). The 
oocysts are 9 to 13 by 8 to 12 /i with a 
mean of 11. by 10. 4 /J . Their length- 
width ratio is 1 . 00 to 1.3 with a mean of 
1.06. They are typically subspherical, 
but vary from spherical to bluntly ellip- 
soidal. A micropyle is absent. The 
oocyst wall is thin, smooth, homogeneous, 
transparent, of uniform thickness thruout, 
and colorless to faintly yellowish. An 
oocyst residuum and polar granule are 
absent. The sporocysts are pale, spindle- 
shaped, without a sporocyst residuum. 
The sporulation time is 4 to 5 days. 

The oocysts of this species might be 
confused with the smaller, subspherical 
oocysts of E. ellipsoiclalis or E. ziirnii, 
but Christensen (1941) considered that 
they can be differentiated by their more 
fragile appearance, their more delicate 
wall, and by their requiring 2 days longer 
to sporulate. 

Life Cycle : Unknown. 

Pathogenesis: Unknown. 



EIMERIA Z URN II 
(RIVOLTA, 1878) 
MARTIN, 1909 

Synonyms : Cytospermium zurnii, 
Eimeria bovis (pro parte), Eimeria cana- 
densis (pro parte). 

Hosts : Ox, zebu, water buffalo. 
Dahlberg and Guettinger (1956) reported 
E. zurnii in 2 white-tailed deer in Wis- 
consin, and Salhoff (1939) reported it in a 
roe deer in Germany. Wetzel and Enigk 
(1936) found it in a wisent in Germany. 
Honess and Winter (1956) recorded it from 
the elk in Wyoming. 



Location : Cecum, colon, rectum, 
thruout small intestine. 

Geographic Distribution : Worldwide. 

Prevalence : This is one of the com- 
moner coccidia of cattle. Boughton (1945) 
found it in 42% of 2492 bovine fecal sam- 
ples in southeastern U.S. , and Hasche and 
Todd (1959) found it in 26% of 355 cattle in 
Wisconsin. Supperer (1952) found it in 11% 
of 130 cattle in Austria. Yakimoff, Gousseff 
and Rastegaieff (1932) found it in 13% of 
126 oxen in Uzbekistan. Marchenko (1937) 
found it in 20% of 137 cattle in the North 
Caucasus. Yakimoff (1933) found it in 18% 
of 41 oxen, 6% of 17 zebus and 37% of 30 
water buffaloes in Azerbaidzhan. Tubangui 
(1931) found it in 3 of 28 zebus and 1 of 11 
carabaos in the Philippines. Torres and 
Ramos (1939) found it in 38% of 156 cattle 
in Brazil. Ruiz (1959) found it in 1% of 100 
adult cattle in the San Jose, Costa Rica 
abattoir. 

Morphology : The oocysts have been 
described by Christensen (1941) among 
others. They are 15 to 22 by 13 to 18 /i 
with a mean of 17. 8 by 15. 6 ji . Their 
length-width ratio is 1 . to 1 . 4 with a 
mean of 1.14. They are spherical to 
bluntly ellipsoidal, without a micropyle. 
The oocyst wall is thin, homogeneous, 
transparent, and colorless to faint greyish- 
lavender or pale yellow. An oocyst polar 
granule and residuum are absent. The 
sporocysts are 9 to 12 by 6 to 7 fi according 
to Yakimoff, Gousseff and Rastegaieff 
(1932). A sporocyst residuum is absent. 

Complete sporulation occurs in 9 to 
10 days at 12° C, 6 days at 15% 3 days at 
20°, 40 hours at 25° and 23 to 24 hours at 
30 to 32. 5° C; a few oocysts may sporulate 
at temperatures as low as 8° C in several 
months, but sporulation is not normal 
above 32° C (Marquardt, Senger and Seg- 
hetti, 1960). 

Life Cycle : The endogenous stages 
of E. zuniii were described by Davis and 
Bowman (1957). Schizonts are found 2 to 
19 days after experimental infection in the 
epithelial cells of the upper, middle and 
lower small intestine, cecum and colon. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



175 



When mature they measure about 10 by 
13(1 and contain 24 to 36 merozoites. 
They lie distal to the host cell nucleus. 
Merozoites are first seen 7 days after in- 
fection. They are about 5 by 12jll, have 
their nucleus near the tapering end and 
contain 2 refractile globules. Davis and 
Bowman did not determine the number of 
asexual generations, but believed that 
there is more than one. The mature schi- 
zonts late in the cycle are slightly larger 
than the early ones. 

Macrogametes are first seen 12 days 
after infection. They occur in the epithel- 
ial cells of the glands and to a lesser ex- 
tent of the surface of the lower small in- 
testine, cecum, colon and rectum, and 
rarely in the upper small intestine. They 
are about 11 by 14ji and contain 1 or 2 
rows of plastic granules. Microgameto- 
cytes are first seen 15 days after infection 
in the same location as the macrogametes. 
They measure about 10 by I4.fi when ma- 
ture. Immature oocysts are first seen 12 
days after infection. 

Pathogenesis : E. ziirnii is the most 
pathogenic coccidium of cattle. In acute 
infections it causes a bloody diarrhea of 
calves. At first the feces are streaked 
with blood. The diarrhea becomes more 
severe, bloody fluid, clots of blood and 
liquid feces are passed, and straining and 
coughing may cause this mixture to spurt 
out as much as 6 to 8 feet. The animal's 
rear quarters may look as tho they had 
been smeared with red paint. Anemia, 
weakness and emaciation accompany the 
dysentery, and secondary infections, es- 
pecially pneumonia, are common. This 
acute phase may continue for 3 or 4 days. 
If the calf does not die in 7 to 10 days, it 
will probably recover. 

E. zurnii may also be associated with 
a more chronic type of disease. Diarrhea 
is present, but there may be little or no 
blood in the feces. The animals are em- 
aciated, dehydrated, weak and listless, 
with rough hair coats, drooping ears and 
sunken eyes. 

The lesions of coccidiosis have been 
described by Boughton (1945) and Davis 



and Bowman (1952) among others. A gen- 
eralized catarrhal enteritis involving both 
the small and large intestines is present. 
The lower small intestine, cecum and colon 
may be filled with semi-fluid, bloody ma- 
terial. Large or smaller areas of the in- 
testinal mucosa may be eroded and des- 
troyed, and the mucous membrane may be 
thickened, with irregular whitish ridges in 
the large intestine or smooth, dull grey 
areas in the small intestine or cecum. 
Diffuse hemorrhages are present in the 
intestines in acute cases, and petechia;l 
hemorrhages in mild ones. 



EIMERIA BOMBA YANSIS 
RAO AND HIREGAUDAR, 1954 



Host: Zebu. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : India. 

Prevalence : Unknown. Rao and 
Hiregaudar (1954) stated that its preva- 
lence was great in calves in a dairy herd 
near Bombay. 

Morphology : The oocysts measure 
32 to 40 by 20 to 25 |i with a mean of 37 by 
22.4jLL. They are ellipsoidal, tending to- 
ward the cylindrical, some with parallel 
sides and others with 1 side straight and 
the other slightly convex. The micropyle 
is 2 to 4 ji in diameter, with a thickened 
wall around it. The oocyst wall is smooth, 
transparent, homogeneous, pale yellowish 
brown, 1 to 1.5/i thick. The sporocysts 
are 12 to 15(j, long, oval, with 1 end a 
little more pointed than the other. An 
oocyst residuum is absent, but a sporocyst 
residuum is present. The sporozoites are 
4 to 6 |i long. The sporulation time is 2 
to 3 days. 

Pathogenesis : Unknown. 



EIMERIA MUNDARAGI 
fflREGAUDAR, 1956 

Host: Zebu. 



176 



THE TELOSPORASIDA AND THE COCCIDLA PROPER 




J ^<:c^" 





Fig. 25. Coccidia of cattle. A. Eimeria subspherica unsporulated oocyst. B. E. zurnii 
unsporulated oocyst. C. E. ellipsoidalis unsporulated oocyst. D. E. cyliii- 
(/>-;c(7 unsporulated oocyst. E. E. a/a/ja)(u'«s(*- unsporulated oocyst. 
F. E. bukiduouensis unsporulated oocyst. G. E. 6oi7i' unsporulated oocyst. 
H. E. caHarfe«s/s unsporulated oocyst. I. E. n»6io-«e«s/s unsporulated 
oocyst. J. E. aiibiiniensis unsporulated oocyst with maniniillated wall. 
K. Isospora sp. sporulated oocyst from cattle. L. Isospora Incazci sporu- 
lated oocyst from English sparrow; note the close resemblance to Fig. K. 
(A. -J., X 1150, from Christensen, 1941; K. -L. , X 2300, from Levine and 
Mohan, 1960) 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



177 



Location: Unknown. Oocysts found 



in feces. 



Geographic Distribution : India (Bom- 
bay). 

Prevalence : Hiregaudar (1956) des- 
cribed this species from a single calf. 

Morphology : The oocysts are ovoid, 
36 to 38 by 25 to 28 ji . The oocyst wall is 
0.3jn thick, slightly thicker toward micro- 
pylar end, smooth, transparent, and pale 
yellow or yellow. The micropyle is dis- 
tinct, 0.5|j. in diameter. The sporocysts 
are oval, 15 to 9 /j,, thinning at the pointed 
end. The sporozoites are 4 to 6 by 1 to 3/1 
and finely granular. An oocyst residuum 
and polar granule are absent. A sporocyst 
residuum is present. The sporulation 
time is 1 to 2 days during the summer. 
The extremely thin wall and the tiny, dis- 
tinct micropyle may differentiate this 
species from other bovine coccidia. How- 
ever, the possibility must not be over- 
looked that these oocysts may be those of 
a species such as E. bukkliioiiensis from 
which the thick, brittle outer wall has 
cracked off. 

Life Cycle : Unknown. 

Pathogenesis: Unknown. 



COCCIDIOSIS IN CATTLE 

Epidemiology : Infections with a 
single species of coccidium are rare in 
nature; mixed infections are the rule. 
Ei))ieria ziiynii and E. bovis are the most 
pathogenic species, but E. auburnensis 
and the other species may contribute to 
the total disease picture, and some of 
them may cause marked signs by them- 
selves if they are present in large enough 
numbers. 

Bovine coccidiosis is primarily a 
disease of young animals. It ordinarily 
occurs in calves 3 weeks to 6 months old. 
Older calves and even adult animals may 
be affected under conditions of gross con- 
tamination, but they are usually symptom- 
less carriers. 



Calves become infected by ingesting 
oocysts along with their feed or water. 
The severity of the disease depends upon 
the number of oocysts they receive. If 
they get only a few, there are no symptoms, 
and repeated infections produce immunity 
without disease. If they get more, the 
disease may be mild and immunity may 
also develop. It they get a large number, 
severe disease and even death may result. 

Crowding and lack of sanitation greatly 
increase the disease hazard. Successive 
passage of coccidia from one animal to 
another often builds up infection to a patho- 
genic level, since in each passage the re- 
cipient receives more oocysts than in the 
previous one. This is the reason for the 
common observation that calves placed in 
a lot where others are already present may 
suffer more from coccidiosis than those 
which were there first. This successive 
passage from a carrier to a symptomless 
"multiplier" to a sub-clinical case to a 
fatal case was described by Boughton 
(1945) as typical of the transmission of 
bovine coccidiosis. In addition, it is 
likely that recycling by repeated infections 
of a single individual may also play an im- 
portant part. 

A little -understood type of bovine 
coccidiosis is winter coccidiosis. This 
occurs when it is so cold that oocyst spor- 
ulation should be minimal if it occurs at 
all. Presumably there is enough heat in 
the bedding to permit sporulation. Another 
explanation which has been advanced is 
that the stress of winter conditions exacer- 
bates a latent infection. This explanation 
is not easy to validate, however, in view 
of the self-limiting nature of coccidial 
infections. 

Davis, Herlich and Bowman (1959, 
1959a, 1960, 1960a) found that concurrent 
infections of cattle with the nematodes, 
Trichostrotigylus colubrifonnis or Coop- 
eria punctata, exacerbated the effects of 
coccidia in calves, but that Ostertagia 
ostertagi and Strongyloides papillosus had 
no such effect. 

Diagnosis : Bovine coccidiosis can 
be diagnosed from a combination of history, 



178 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



signs, gross lesions at necropsy and mi- 
croscopic examination of scrapings of the 
intestinal mucosa and of feces. Diarrhea 
or dysentery accompanied by anemia, 
weakness, emaciation and inappetance are 
suggestive of coccidiosis in calves. Sec- 
ondary pneumonia is often present. The 
lesions found at necropsy have already 
been described. 

Microscopic examination is necessary 
to determine whether the lesions are due 
to coccidia or to some other agent. How- 
ever, diagnoses will often be missed if 
one relies only on finding oocysts in the 
feces. There may be none there at all in 
the acute stage of zurnii coccidiosis. 
Similarly, the mere presence of oocysts 
in the feces is not proof that coccidiosis 
is present; it may be coccidiasis. To be 
sure of a diagnosis, scrapings should be 
made from the affected intestinal mucosa 
and examined under the microscope. It is 
not enough to look for oocysts, however, 
but schizonts, merozoites and young gam- 
etes should be recognized. 

Treatment: A number of investigators 
(Boughton, 1943; Boughton and Davis, 
1943; Davis and Bowman,- 1952, 1954; 
Hammond et al . . 1956; Senger et al. . 1959) 
have found that the sulfonamides have some 
value against bovine coccidiosis. 

Other types of compounds which are 
used in avian coccidiosis are unsatisfac- 
tory. For example, Hammond el al. (1957) 
found that nicarbazin was effective in pre- 
venting experimental coccidiosis due to 
E. bovis in calves only at doses which 
were toxic to the animals. Gardner and 
Wittorff (1955) found that 0. 1 to 0. 3% 
furacin in the ration was toxic to dairy 
calves, causing nervous signs and reducing 
or preventing weight gains. Even 0.01% 
of the drug had some toxic effect. It in- 
jures the myelin sheaths and causes cere- 
bral damage. 

Gasparini, Roncalli and Ruffini (1958) 
claimed that drenching with 4 g per 100 kg 
ammonium sulfate plus 2 ml lactic acid in 
a liter of milk twice a day for 4 consecu- 
tive days cured coccidiosis due to E. zurnii 
in 2 herds of cattle in Italy, They believed 



that the ammonium sulfate worked by re- 
leasing ammonia, and added the lactic acid 
to prevent release from taking place in the 
stomach. However, their work was im- 
properly controlled, and the efficacy of 
this compound remains to be determined. 

Sulfamethazine and sulfamerazine ap- 
pear to be better than sulfaquinoxaline or 
other suKonamides. They are only par- 
tially effective, however. They do not 
prevent the diarrhea, but they do reduce 
the severity of the disease. Thus, Davis 
and Bowman (1954) found that sulfametha- 
zine reduced the severity of experimental 
infections with E. ziirnii or mixed species 
in calves and that treated calves gained 
slightly more weight than the controls. 
Drug treatment was started before infec- 
tion, and no immunity to subsequent expo- 
sures was produced. Hammond cl al. 
(1956) found that sulfamerazine or sulfa- 
quinoxaline, given to calves at the rate of 
0. 143 g per kg body weight for 2 days and 
0. 072 g per kg for 2 more days, decreased 
the severity of coccidiosis due to E. bovis 
if they were administered between 13 and 
17 days after experimental infection. 
They were not effective earlier or later 
than this. The drugs presumably act on 
the merozoites after their release from 
the schizonts. Senger el al. (1959) found 
that a mixture of equal parts sulfamerazine 
and sulfamethazine given by mouth at the 
rate of 213, 143 and 70 mg per kg body 
weight 13, 14 and 15 days, respectively, 
after inoculation reduced the severity of 
the disease and did not interfere with the 
development of immunity. 

Hammond el al. (1959) found that a 
single treatment with 0. 215 g per kg sulfa- 
methazine or sulfabromomethazine 13 days 
after experimental inoculation with E. bovis 
effectively controlled coccidiosis. Admin- 
istration of either compound on alternate 
days at the rate of 0.0215 g per kg for as 
short a period as 10 to 18 days after inoc- 
ulation also effectively controlled coccid- 
iosis, while in 1 experiment treatment at 
this rate 12 and 14 days after inoculation 
suppressed the disease. This treatment 
did not interfere with the development of 
immunity. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



179 



Since the sulfonamides are generally 
only partially effective, preventive mea- 
sures are more important than curative 
ones. 

Prevention : Sanitation and isolation 
are effective in preventing coccidiosis. 
Beef calves should be dropped and kept on 
clean, well drained pastures. Overstock- 
ing and crowding should be avoided. Feed 
and water containers should be high enough 
to prevent fecal contamination. Feed lots 
should be kept dry and should be cleaned 
as often as possible. Concrete or small 
gravel are preferable to dirt. 

Dairy calves should be isolated within 
24 hours after birth and kept separately. 
Individual box stalls which are cleaned 
daily may be used. Slat-bottom pens are 
also effective and require less cleaning. 
Allen and Duffee (1958) described a simple, 
raised, wooden home-made stall with a 4 
by 2-1/2 foot slatted floor in which dairy 
calves can be raised separately for the 
first 3 months. Davis (1949) and Davis 
and Bowman (1952) described a 5 x 10 x 3 
foot outdoor portable pen which can be 
moved to a fresh site once a week and thus 
eliminates the need for cleaning. It is 
made primarily of net wire and 1x4 lum- 
ber, with a removable roof and siding at 
one end. The pens should not be returned 
to the same ground for a year. 

These methods will not eliminate all 
coccidia, but they will prevent the calves 
from picking up enough oocysts to harm 
them. In addition, they will greatly reduce 
lice, helminth parasites, pneumonia, 
white scours and other diseases. 

The unsporulated oocysts of E. zurnii 
are killed by sunlight in 4 hours or by dry- 
ing at 25% relative humidity or below in 
several days. They are not harmed by 
freezing at -7 to -8° C for as long as 2 
months, and half of them survive as long 
as 5 months; at -30 °C, however, only 5% 
survive 1 day. The oocysts are killed by 
10"^ M mercuric chloride, 0.05 M phenol, 
0. 25 M formaldehyde, 1. 25% sodium hypo- 
chlorite, or 0. 5% cresol (Marquardt, Sen- 
ger and Seghetti, 1960). 



EIMERIA AHSATA 
HONESS, 1942 emend. 

Synonym : Eimeria ah-sa-ia Honess, 
1942. 

Hosts : Sheep, Rocky Mountain big- 
horn sheep. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : North Amer- 
ica (Wyoming, Alabama). 

Prevalence : Unknown. 

Morphology : The oocysts are ellip- 
soidal and faint pink. The oocyst wall is 
faint straw-colored and lined by a mem- 
brane. A micropyle and micropylar cap 
are present. Oocysts from the bighorn 
sheep are 30 to 40 by 20 to 30|Lt with a 
mean of 32. 7 by 23. 7 |j, ; their length- width 
ratio is 1.1 to 1.8 with a mean of 1 . 40; 
the micropylar cap is 0. 4 to 4. 2 jn high and 
2. 1 to 12. 5)n wide with a mean of 2. 1 by 
l.^li. Oocysts from domestic sheep are 
29 to 37 by 17 to 28 ^i with a mean of 33.4 
by 22.6ju; their length-width ratio is 1.2 
to 1 . 8 with a mean of 1 . 48; the micropylar 
cap is 1.7 to 4. 2/i high and 5. 9 to 13. 4jj, 
wide with a mean of 3. by 8. 4 |_i . An 
oocyst residuum is present in some oocysts. 
Oocyst polar (?) granules are almost al- 
ways present. The sporocysts are 15.4 
by 7. 8jj. and have a sporocyst residuum. 

This species is difficult to distinguish 
from E. arlouigi, and Morgan and Hawkins 
(1952) and Lotze (1953) considered it of 
doubtful validity. However, Smith, Davis 
and Bowman (1960) rediscovered it in Ala- 
bama and confirmed its distinctiveness. 

Life Cycle : Unknown. The prepatent 
period is 18 to 20 days according to Smith, 
Davis and Bowman (1960). 

Pathogenesis : Smith, Davis and Bow- 
man (1960) considered this the most patho- 
genic of all sheep coccidia. They produced 
fatal infections in 4 out of 9 lambs 1 to 3 
months old by feeding 100, 000 oocysts. 



180 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



The intestines of infected lambs had thick- 
ened, somewhat edematous areas in the 
upper part. The Peyer's patches and the 
last 8 to 10 inches of the small intestine 
above the ileocecal valve were inflamed. 



EIMERIA ARLOINGI 
(MAROTEL, 1905) 
MARTIN, 1909 

Hosts : Sheep, goat. Rocky Mountain 
bighorn sheep, Ovis »iusl)>ioii, O. polii. 
Copra ibex, Hemmilragus jenilaicus, roe 
deer. 

Location : Small intestine. 

Geographic Distribution : Worldwide. 

Prevalence: This is probably the 
most common coccidium in sheep. Chris- 
tensen (1938a) found it in 90% of 100 sheep 
from Idaho, Maryland, New York and 
Wyoming. Balozet (1932) found it in 52% 
of 63 sheep and 56% of 41 goats in Tunisia. 
Jacob (1943) found it in 58% of 100 sheep 
and 18% of 11 goats in Germany. Svanbaev 
(1957) found it in 52% of 302 sheep and 52% 
of 48 goats in Kazakhstan. 

Morphology : The oocysts are usually 
elongate ellipsoidal, but are sometimes 
asymmetrical, with one side curved more 
than the other, or slightly ovoid. They 
are 17 to 42 by 13 to 27 /i with a mean of 
27 by 18/i; their length-width ratio is 1. 1 
to 1.9 with a mean of 1.49 (Christensen, 
1938a). The oocyst wall is 1.0 to 1. 5 fi 
thick, transparent, almost colorless to 
yellowish-brown, and composed of 2 
layers, the outer one being half as thick 
as the inner, according to Christensen 
(1938a). The oocyst wall is apparently 
lined by a membrane. A micropyle 2 to 
3(1 in diameter is present. A micropylar 
cap is present; it varies from an incon- 
spicuous, flat structure to a prominent, 
transparent, pale yellow to yellowish- 
green rounded cone or crescent, 0.2 to 
2[x high by 3 to 8 fi wide with a mean of 
1.2 by 5/i. This cap is a tough, lid-like 
structure which is easily dislodged and 
may be lost in some specimens. An 
oocyst residuum is absent. An oocyst 



polar granule is present according to 
Balozet (1932). The sporocysts are ovoid, 
13 by 6/1. A sporocyst residuum is pres- 
ent. The sporulation time is 1 to 2 days 
(Christensen, 1938a) to 3 to 4 days (Balo- 
zet, 1932). 

Life Cycle : Lotze (1953a) studied the 
life cycle of E. arloiiigi in experimentally 
infected lambs. The sporozoites emerge 
from the oocysts in the small intestine, 
enter the crypts of Lieberkuehn, and pene- 
trate thru the tunica propria into the in- 
terior of the villi. Here they enter the 
endothelial cells lining the central lacteals 
and grow. The host cell also grows, and 
its nucleus becomes very large. There is 
apparently only 1 generation of schizonts 
and merozoites. The schizonts become 
mature 13 to 21 days after infection. At 
this time they are about 122 to 146 /i in 
diameter and contain a large number 
(probably millions) of merozoites about 
9/i long and 2 /i wide. 

The merozoites break out of the schi- 
zonts and enter the epithelial cells of the 
small intestine. Sometimes only a small 
group of cells at the bottom of the crypts 
is parasitized, but in heavy infections 
practically all the epithelial cells of the 
villi are invaded. The infected villi are 
enlarged and greyish. Some of these 
merozoites become microgametocytes; 
these form many microgametes, leaving 
a large mass of residual material. Most 
of the merozoites become macrogametes, 
which contain large plastic granules when 
mature. 

Following fertilization, the macro- 
gametes turn into oocysts, which break 
out of the host cells and are first seen in 
the feces on the 20th day after infection. 
Their numbers increase for about 5 days 
and then decrease at about the same rate 
for the next 5 days. Thus the prepatent 
period is 19 days and the patent period 
about 10 days following a single exposure. 

Pathogenesis : Lotze (1952) studied 
the pathogenicity of E. arloiiigi in 3- 
month-old lambs experimentally infected 
with 200,000 to 60 million oocysts. No 
visible signs were produced by infections 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



181 



with 1 million oocysts or less. In lambs 
infected with 3 or 5 million oocysts, the 
feces became soft on the 13th day and then 
returned to normal during the next 6 days. 
The health, general condition and weight 
gains of these animals were not affected. 

Severe diarrhea was produced with 
higher doses, but none of the animals 
died altho one was killed in extremis. In 
general, the experimentally infected lambs 
appeared normal up to the 13th day after 
inoculation, when their feces became soft. 
In the more heavily infected lambs the 
feces then became watery, and diarrhea 
was severe beginning on the 15th day. 
Blood-tinged mucus was passed by affected 
lambs only occasionally. The feces began 
to return to normal on the 17th day and 
were usually nearly normal by the 20th 
day. Lambs with marked diarrhea be- 
came weak and refused feed. 

At necropsy, only a few small, 
slightly hemorrhagic areas scattered 
thruout the lining of the small intestine 
were seen up to the 13th day. From the 
13th to 19th days the small intestine was 
more or less thickened and edematous, 
and thick, white opaque patches made up 
of groups of heavily parasitized villi were 
present. 

The villi containing the schizonts be- 
come thin-walled sacs and are presumably 
destroyed. The sexual stages are clus- 
tered in the epithelial cells of the villi 
and destroy these cells when they emerge. 
However, they do not do as much damage 
'as the asexual stages, since the condition 
of affected animals appears to improve 
before oocysts are shed. 

E. arloingi is less pathogenic than 
E. ninakohlyakimovae . 

Epidemiology : This species has 
been reported not only from domestic 
sheep and goats but also from the Rocky 
Mountain bighorn sheep [Ovis canadensis), 
moufflon (O. musimon), argali (O. animon 
polii), ihex {Capra ibex), and Hem )nitra- 
gus jemlaicus (see especially Yakimoff, 
1933a). Ullrich (1930) found it in the roe 
deer. Whether the forms from all these 
animals are really E. arloingi remains to 



and cross-transmission experiments. 
According to Lotze (1953), no cross-trans- 
mission studies, even between domestic 
sheep and goats, have been reported up un- 
til the time of his paper, and he attempted 
none. 



EIMERIA CRANDALLIS 
HONESS, 1942 

Hosts : Sheep, Rocky Mountain big- 
horn sheep. This species was originally 
described from the bighorn sheep, but 
Hawkins (in Morgan and Hawkins, 1952) 
found it in domestic sheep. 

Location: Unknown. Oocysts found 
in feces. 

Geographic Distribution : North 
America (Wyoming, Michigan). 

Prevalence : Unknown. 

Morphology : The oocysts are spher- 
ical to broadly ellipsoidal to ovoid, color- 
less to faint pink or greenish, and are 17 
to 23 by 17 to 22 jj. with a mean of 21. 9 by 
19.4|ji. Their length-width ratio is 1.00 
to 1. 35 with a mean of 1. 11. A micro- 
pyle and micropylar cap are present. The 
micropylar cap measures from a trace to 
1 . 7 |i high and 3. 3 to 6. 6 /ji wide with a 
mean of 0. 8jj, high and 4. 9fi wide. The 
oocyst wall has a distinctly demarcated 
outer edge, a feature which Honess (1942) 
considered to distinguish this species 
from E. arloingi. The sporocysts are 8 
to 11 by 5 to 8 fj. with a mean of 9. 5 by 
6. 4|i . No information is available on 
oocyst polar granule, oocyst residuum or 
sporocyst residuum. 

Lotze (1953) considered that this spe- 
cies was of doubtful validity, since its 
oocysts fall into the size range of E. 
arloingi. but Morgan and Hawkins (1952) 
accepted it, stating that Hawkins had found 
that its peak of infection in Michigan oc- 
curred at a different time from that of E. 
arloi)igi. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 



182 



THF TFLOSPORASIDA AND THF COCCrDIA PROPER 



EIMERIA FAUREI 

(MOUSSU AND MAROTEL, 1902) 

MARTIN, 1909 

Synonym : Einieria aemula. 

Hosts : Sheep, goat. Rocky Mountain 
bighorn sheep, Ovis amnion polii, O. 
musinion, O. orienlalis. Capra ibex, 
Rupicapra rupicapra (chamois), Ammotra- 
gus lervia {Barbary sheep). 

Location : Small intestine. 

Geographic Distribution : Worldwide. 

Prevalence : This species is fairly 
common. Christensen (1938a) found it in 
11% of 100 sheep from Idaho, Maryland, 
New York and Wyoming. Balozet (1932) 
found it in 21% of 63 sheep and 2% of 41 
goats in Tunisia. Jacob (1943) found it in 
40% of 100 sheep and 18% of 11 goats in 
Germany. Svanbaev (1957) found it in 43% 
of 302 sheep and 40% of 48 goats in Kozak- 
hstan. 

Morphology : The following descrip- 
tion is based primarily on those of Chris- 
tensen (1938a) and Balozet (1932). The 
oocysts are ovoid, 25 to 35 by 18 to 24|i , 
with a mean of 28. 9 by 21. Oj^t according to 
Christensen or 31. 5 by 22. 1 ju. according 
to Balozet. The oocyst wall is transparent, 
delicate salmon pink to pale yellowish 
brown, 1 ^ thick at the most according to 
Balozet; with a faint, yellowish-green 
"external coat . . . about half as thick as 
wall" according to Christensen. The mi- 
cropyle is conspicuous, 2 to 3fi in diam- 
eter, at the small end. A micropylar cap 
is absent. An oocyst polar granule was 
illustrated by Balozet (1932). Oocyst and 
sporocyst residua are absent. The sporu- 
lation time is 1 to 2 days according to 
Christensen, 3 to 4 days according to 
Balozet. 

Life Cycle : The life cycle of E. 
faitrei does not seem to have been worked 
out in detail. According to Lotze (1953), 
its schizonts are about 100 (i in diameter 
and contain thousands of merozoites. 



Pathogenesis : 
mildly pathogenic. 



This species is only 
Lotze (1954) found 



that single infections of 3-month-old lambs 
with 5 million oocysts produced only a tem- 
porary softening of the feces without signifi- 
cantly affecting the general health or physical 
condition of the animals, and infections with 
50 million oocysts failed to cause death. 

Epidemiology : This species has been 
reported not only from the domestic sheep 
and goat but also from the Rocky Mountain 
bighorn sheep (Ovis canadensis), moufflon 
(O. am))2on), urial or shapo (O. orienlalis), 
Barbary sheep [Amniulragus lervia), ibex 
(Capra ibex) and chamois (Rupicapra rupi- 
capra) (see especially Yakimoff, 1933). 
Whether the forms from these species are 
all E. fanrei remains to be proven by care- 
ful study of their oocysts and cross-trans- 
mission experiments. According to Lotze 
(1953), no cross-transmission studies, 
even between domestic sheep and goats, 
had been reported up until the time of his 
paper, and he attempted none. 



EIMERIA GILRUTHI 

(CHATTON, 1910) 

REICHENOW AND CARINI, 1937 

Synonyms : Gastrocystis gilruthi, 
Globidimn gilruthi. 

Hosts : Sheep, goat. 

Location : Abomasum, seldom small 
intestine. 

Geographic Distribution : Worldwide. 

Prevalence : This form is very com- 
mon in Europe. Chatton (1910) and Triffitt 
(1928) found it in the abomasa of almost all 
the sheep they examined in France and Eng- 
land, respectively. Alicata (1930) found it 
in 9% of 78 sheep in Indiana, 11% of 101 
sheep from West Virginia and 8% of 72 sheep 
from Idaho. It has also been seen in Mon- 
tana, Wyoming, Michigan (Morgan and 
Hawkins, 1952) and Illinois. Sarwar(1951) 
found it in 34% of the sheep and goats 
slaughtered at the Lahore, Pakistan abattoir, 
and found it in as many as 94% in other parts 
of East Punjab. Soliman (1958) found it in 
18% of 250 sheep and 28%. of 150 goats 
slaughtered in Egypt. Soliman (1960) found 
it in 32% of 425 sheep and 40% of 240 goats 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



183 



in the Sudan. Rac and Willson (1959) re- 
ported it in Australia. 

Morphology : Only the schizonts and 
merozoites of this form have been des- 
cribed. The schizonts occur in the con- 
nective tissue of the abomasal wall. They 
are 300 to 700 ^i long and 300 to 465 |i wide, 
and are easily visible to the naked eye as 
whitish nodules. The host cell nucleus is 
flattened and greatly enlarged. The ma- 
ture schizonts are filled with many thou- 
sands of crescent-shaped merozoites 
about 4. 5 to 7. 5 ;i long and 1. 2 to 2. Opt 
wide. One end of the merozoites is 
rounded and the other pointed. The nucleus 
is near the broad end, and a heavily stain- 
ing granule is in the center. 

These schizonts are undoubtedly 
those of a species of Eimeria presently 
known from its oocysts alone, but we do 
not know which species it is. Reichenow 
(1940) said that it was very probably E. 
intricata. Becker (1956) agreed and, since 
the specific name gilrnthi has priority, 
synonymized E. intricata with it. How- 
ever, Kotlan, Pelle'rdy and Verse'nyi 
(1951, 1951a) found two types of giant 
schizonts in sheep. One type, which 
measured 64 to 256 by 48 to 179/i and con- 
tained straight, slender merozoites 10 to 
12 |i long, they found to be those of E.parva. 
The other type of schizont was larger and 
contained merozoites about 16 fx long which 
were bent like a hoe at one end ("hacken- 
formigen"). These they said were those 
ofE. intricata. However, they saw both 
schizonts in the small intestine and not in 
the abomasum, and they used only 2 lambs 
in their work. Hence, it is felt best for 
the present not to attempt to assign the 
gilruthi schizonts to any other species of 
Eimeria. 



Geographic Distribution: 
America, Europe (Germany). 



North 



Prevalence : This species is rela- 
tively uncommon in sheep. Christensen 
(1938a) found in in 10% of 100 sheep from 
Maryland and New York. Jacob (1943) 
found it in 1% of 100 sheep in Germany. 
Honess (1942) remarked that it was more 
frequent and numerous in bighorn sheep 
than in domestic sheep in Wyoming. 

Morphology : This species has been 
described by Christensen (1938a). The 
oocysts are piriform or shaped like a 
stout, broad-shouldered urn, with the mi- 
cropyle and micropylar cap at the broad 
end; small oocysts are often bluntly ellip- 
soidal. The oocysts are 22 to 35 by 17 to 
25^1 with a mean of 29.4 by 20.9 fi. Their 
length-width ratio is 1 . 2 to 1 . 7 with a 
mean of 1.41. The micropyle is distinct, 
3 to 5jj, in diameter. The micropylar cap 
is prominent, 5 to lQ\i wide and 1 to 2. 5ji 
high with a mean of 7. 5 by l.l \x; it is 
shaped like a broad truncated cone with a 
flat or slightly convex top, and is easily 
dislodged. The oocyst wall is transparent, 
pale brownish-yellow to yellowish-brown, 
and composed of 2 layers, the outer one 
being transparent, pale yellow to yellow- 
ish-green, and half as thick as the inner, 
heavier layer. The oocyst wall is lined 
by a membrane. An oocyst polar granule 
and oocyst residuum are absent. The 
sporocysts are ovoid, with a sporocyst 
residuum. The sporozoites have a re- 
tractile globule at each end. The sporula- 
tion time is 8 to 4 days. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 



EIMERIA GRANULOSA 
CHRISTENSEN, 1938 

Hosts : Sheep, Rocky Mountain big- 
horn sheep. 

Location : Unknown. Oocysts found 
in feces. 



EIMERIA INTRICATA 
SPIEGL, 1925 

Hosts : Sheep, Rocky Mountain big- 
horn sheep, moufflon, roe deer. 

Location: Uncertain, presumably 
abomasum and small intestine. 



184 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



Geographic Distribution : Worldwide. 

Prevalence : This species is fairly 
common. Christensen (1938a) found it in 
14% of 100 sheep from Maryland, New 
York and Wyoming. Jacob (1943) found it 
in 13% of 100 sheep in Germany. Balozet 
(1932) found it in 3% of 63 sheep in Tunisia. 
Svanbaev (1957) found it in 4% of 302 sheep 
in Kazakhstan. 



Morphology : This species has been 
described by Spiegl (1925), Balozet (1932) 
and Christensen (1938a). The oocysts are 
ellipsoidal, 39 to 54 by 27 to 36 (j. with a 
mean of 47.0 by 32.0(:i (Christensen) or 
45.6 by 33.0/1 (Spiegl). Their length- 
width ratio is 1. 3 to 1. 8 with a mean of 
1.47. The oocyst wall, as described by 
Henry (1932), is composed of 3 layers; 
the outer layer is a transparent, colorless 
membrane which is very difficult to see; 
the middle layer is thick, rough, brown, 
transversely striated, 2.0 to 2. 5/i thick, 
and somewhat thinner at the micropylar 
end; the inner layer is colorless, 0.8 to 
1.0 fi thick. The micropyle is prominent, 
6 to 10 /I in diameter; it does not extend 
to the inner layer. The micropylar cap is 
prominent, transparent, colorless to 
yellowish-green, crescent-shaped, de- 
tachable, and 6 to 11 ji wide and 1 to 3j:i 
high with a mean of 9 by 2 jm . An oocyst 
polar granule and residuum are absent. 
The sporocysts are elongate ovoid, 17 to 
18 by 9 to 13 fi, with a small Stieda body 
and a sporocyst residuum. The sporo- 
zoites are wedge-shaped, with several 
refractile globules. The sporulation time 
is 3 to 5 days. 

Life Cycle : The life cycle of E. 
inlricala has not been worked out. As 
mentioned above, Reichenow (1940) and 
Becker (1956) considered that the giant 
schizonts described from sheep under the 
name E. gilruthi are those oiE. inlricala. 
According to Kotlan, Pell^rdy and Versenyi 
(1951), the merozoites of E. inlricala are 
about 16/i long and bent like a hoe at one 
end. 

Pathogenesis : Unknown. These 
oocysts are rarely found in large numbers. 



Epidemiology : Honess (1952) found 
this species in the Rocky Mountain bighorn 
sheep, and Wetzel and Enigk (1936) re- 
ported it from the roe deer in Germany. 



EIMERIA NINAKOHLYAKIMOVAE 
YAKIMOFF AND RASTEGAIEFF, 
1930 emend. 

Synonyms : Eimeria galouzoi (pro 
parte), E. nina-kohl-yakimovi Yakimoff 
and Rastegaieff, 1930. 

Hosts : Sheep, goat. Rocky Mountain 
bighorn sheep, mouflon [Ovis nmsinion), 
0. orientalis, Siberian ibex (Capra ibex 
sibirica), Barbary sheep {Animotragus 
lervia), Persian gazelle {Gazella subgnt- 
turosa). 

Location : Small intestine, especially 
the posterior part,and also cecum and colon. 

Geographic Distribution : Worldwide. 

Prevalence : This species is fairly 
common. Christensen (1938a) found it in 
3% of 100 sheep from Maryland and Idaho. 
Jacob (1943) found it in 5% of 100 sheep in 
Germany. Balozet (1932) found it in 35% 
of 63 sheep and 34% of 41 goats in Tunisia. 
Svanbaev (1957) found it in 52% of 302 sheep 
and 31% of 48 goats in Kazakhstan. 

Morphology : This species has been 
described by Yakimoff and Rastegaieff 
(1930), Balozet (1932) and Christensen 
(1938a). The oocysts are usually ellip- 
soidal, sometimes spherical, occasionally 
slightly ovoid. They are 16 to 27 by 13 to 
22 /i with means of 23. 1 by 18. 3 ^t (Chris- 
tensen) or 19. 8 by 16. 5fj, (Balozet). Their 
length-width ratio is 1. 1 to 1. 5 with a mean 
of 1.27 according to Christensen (1938). 
The oocyst wall is 1 to 1. 5 |i thick, trans- 
parent, almost colorless to pale brownish 
yellow, and composed of two layers of 
which the outer is half as thick as the inner. 
A micropyle is absent or imperceptible 
(occasionally visible under bright light if 
the oocyst is tilted, according to Christen- 
sen). There is no micropylar cap. An 
oocyst polar granule and oocyst residuum 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



185 



are absent. The sporocysts are ovoid, 4 
to 11 by 4 to 6 |u . A sporocyst residuum 
is present. The sporozoites have one end 
slender and pointed and the other thick and 
rounded; they measure 4 to 5 by 2 /j, and 
lie lengthwise, head to tail, in the sporo- 
cysts. The sporulation time is 1 to 2 days 
according to Christensen (1938a) or 3 to 4 
days according to Balozet (1932). 

Life Cycle : The life cycle of this 
species has been described by Balozet 
(1932) in the goat and briefly by Lotze 
(1954) in the sheep. Their accounts differ, 
and are given separately below. 

Lotze (1954) found in sheep that the 
sporozoites enter the epithelial cells ati 
the base of the glands of Lieberkuehn in 
the small intestine, where they form 
schizonts about 300 jj, in diameter contain- 
ing thousands of merozoites. The sexual 
stages occur in the epithelial cells of the 
ileum, cecum and upper part of the large 
intestine, appearing 15 days or more 
after infection. 

Balozet (1932a) found in a kid killed 
39 days after infection that the schizonts 
were only 15 to 35 /j, in diameter and con- 
tained only 40 to 200 merozoites. How- 
ever, these schizonts were found very 
late in the infection. They were asso- 
ciated with macrogametes and microga- 
metocytes, and it is possible either that 
they may have belonged to a second gen- 
eration not mentioned by Lotze or that 
they may have belonged to some other 
species. 

The prepatent period was found by 
Shumard (1957) to be 15 days in lambs 
and by Balozet (1932) to be 10 to 13 days. 

Pathogenesis : This is one of the 
most pathogenic species of coccidium in 
sheep. Lotze (1954) found that as few as 
50,000 oocysts caused diarrhea in a 3- 
month-old lamb, and as few as 500, 000 
oocysts caused death. Dysentery was pro- 
duced in a 2-year-old sheep by inoculation 
with as few as 1 million oocysts. 

Lotze (1954) found that in lambs the 
feces became soft in 12 to 17 days after 



experimental infection. They became 
watery a day or 2 later and remained so 
for a week or more. In the more heavily 
infected lambs, the feces contained blood- 
stained mucus beginning the 15th day after 
infection or soon thereafter. In those ani- 
mals which recovered, the feces remained 
soft for some weeks. 

The lambs with severe diarrhea lost 
their appetites at first, altho they appeared 
to drink more. After about a week they 
drank very little. There was rapid loss of 
weight at the onset of diarrhea. If the 
lambs recovered, they gained weight about 
as rapidly as the controls, but of course 
had taken a setback in growth. About 2 
months after severe coccidiosis, the wool 
began to break off over extensive areas, 
starting on the flanks; this may have been 
due to nutritional disturbance caused by 
the infection. 

The diarrheic feces attracted flies, 
and affected animals quickly became fly- 
struck. Some animals which would other- 
wise have recovered died of flystrike if 
they were not treated for this condition. 

At necropsy, petechial hemorrhages 
were found in the small intestine 3 to 7 
days after infection. The small intestine 
then became thickened and inflamed. Ex- 
tensive hemorrhage was present in the 
posterior part of the small intestine of 
severely affected lambs by the 15th day. 
The cecum and upper part of the large in- 
testine became thickened and edematous, 
and were hemorrhagic by the 19th day. 
In heavily infected lambs, vast areas of 
the posterior part of the small intestine 
were denuded of epithelium. Thus, one 
can say that the lesions consisted at first 
of petechial hemorrhages, followed by 
thickening, edema and inflammation, and 
finally by epithelial denudation. The small 
intestine, especially its posterior part, 
cecum and upper colon were affected. 

Shumard (1957a) studied a somewhat 
less pathogenic strain. He reported 
lowered feed consumption, lassitude, gen- 
eralized incoordination and slight diarrhea 
with some bleeding in lambs experimentally 
infected at 50 days of age with 7 million 



IRfi 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



oocysts of E. ninakohlyakimovae and 
100, 000 oocysts of E. faiirei. There was 
no decrease in water consumption. Clin- 
ical signs appeared on the 9th day after 
infection and ended about the 22nd day. 
One out of the 4 lambs died on the 15th 
day. There were decreases in percentage 
of feed protein digested and inorganic 
serum phosphorus, increases in serum 
globulins and blood glucose, and no sig- 
nificant changes in total serum protein, 
blood hemoglobin and hematocrit values. 
Oocysts of both species appeared in the 
feces on the 15th day, increased until the 
21st day and then decreased gradually. 

Balozet (1932) observed a case of 
muco-sanguineous diarrhea followed by 
death in a naturally affected adult goat, 
and produced the disease experimentally 
in 2 newborn kids. A mucous diarrhea 
appeared on the 22nd day after infection, 
became bloody, and persisted until about 
the 39th day. 

Remarks : In one of the very few 
cross-transmission experiments attempted 
with sheep and goat coccidia, Balozet 
(1932) was unable to infect a recently 
weaned lamb with E. numkohlyakimovae 
from a goat, altho he did infect 2 newborn 
kids. He thought the lamb was too old. 



EIMERIA PALLIDA 
CHRISTENSEN, 1938 



tible and there is no micropylar cap. The 
oocyst wall is thin, homogeneous, color- 
less to pale yellow to yellowish green, 
appears fragile and pallid, and is com- 
posed of 2 layers of which the outer is 
half as thick as the inner, with a single 
dark refraction line marking its inner edge. 
An oocyst polar granule and oocyst resi- 
duum are absent. The sporocysts are 
ovoid, without a sporocyst residuum. The 
sporozoites lie lengthwise, head to tail, 
in the sporocysts, and contain a spherical 
globule at each end. The sporulation time 
is 1 day. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : In describing E. pallida, 
Christensen (1938a) said that it differed 
from E. parva is being narrower, pale, 
inconspicuous and colorless, and in having 
only a single black refraction line on the 
inner surface of the oocyst wall instead of 
2 black refraction lines, one on each side 
of the inner wall. However, Kotlan, Pel- 
lerdy and Versenyi (1951) considered E. 
pallida a synonym of E. parva. 



EIMERIA PARVA 

KOTLAN, MOCSY AND VAJDA, 1929 

Synonyms : Ei»ieria galouzoi {pro 
parte). 



Host : Sheep. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : North 
America. 

Prevalence : Christensen (1938a) 
found this species in 10% of 100 sheep 
from Maryland and Wyoming. 

Morphology : This species has been 
described by Christensen (1938a). The 
oocysts are ellipsoidal, 12 to 20 by 8 to 
15^ with a mean of 14. 2 by 10, O^L . Their 
length-width ratio is 1 . 2 to 1 . 7 with a 
mean of 1. 43. A micropyle is impercep- 



Hosts : Sheep, goat. Rocky Mountain 
bighorn sheep, Barbary sheep {Ammotra- 
gus lervia), Siberian ibex {Capya ibex 
sibirica), roe deer. 

Location : Schizonts are found thru- 
out the small intestine, and gametes and 
gametocytes in the cecum, colon and small 
intestine. 

Geographic Distribution : Worldwide. 

Prevalence : This species is common 
in sheep, less common in goats. Chris- 
tensen (1938a) found it in 50% of 100 sheep 
from Idaho, Maryland and Wyoming. Jacob 
(1943) found it in 52% of 100 sheep and 9% 
of 11 goats in Germany; he also found it in 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



187 



a roe deer. Balozet (1932) found it in 21% 
of 63 sheep and 22% of 41 goats in Tunisia. 
Svanbaev (1957) found it in 9% of 302 sheep 
in Kazakhstan. 

Morphology : This species has been 
described by Kotlan, Mocsy and Vajda 
(1929), Balozet (1932) and Christensen 
(1938a). The oocysts are subspherical, 
ellipsoidal or spherical, 12 to 22 by 10 to 
18/i with a mean of 16. 5 by 14. 1 jj, (Chris- 
tensen) or 17. 2 by 13. 5|u (Balozet). 
Their length width ratio is 1. to 1.5 with 
a mean of 1.18 (Christensen). The oocyst 
wall is smooth, homogeneous, pale yellow 
to yellowish green, and composed of 2 
layers of which the outer is half as thick 
as the inner; there is a heavy, black re- 
fraction line on each side of the inner 
layer, according to Christensen. Accord- 
ing to Balozet, the wall appears to be 
lined by a membrane. The sporont is 
clear. A micropyle is absent; according 
to Christensen, the oocyst wall occasion- 
ally appears slightly paler at one end than 
the other. An oocyst polar granule and 
oocyst residuum are absent. The sporo- 
cysts are oval. The sporocyst residuum 
is indistinct if present at all. The spor- 
ulation time is 1 to 2 days (Christensen) 
or 7 to 8 days (Balozet). 

Life Cycle : The life cycle of E. 
parva in sheep has been described by 
Kotlan, Pelle'rdy and Versenyi (1951). 
The schizonts are found thruout the small 
intestine. They measure up to 185 to 256 
by 128 to 179^1 and are easily visible to 
the naked eye as whitish bodies. They 
lie in the mucosa, usually near the sur- 
face but sometimes as far down as the 
muscularis mucosae. They invade endo- 
thelial cells and enlarge both the host cell 
and its nucleus enormously. They are 
surrounded by a rather thick layer of 
connective tissue which becomes thinner 
as they increase in size. Each schizont 
produced thousands of straight merozoites 
10 to 12^1 long. 

Kotlan, Pellerdy and Versenyi (1951) 
also found a second, much smaller type of 
schizont in the small intestine. It occurred 
in the superficial epithelial cells, was 
10 to 12 fi in diameter and contained about 



10 to 20 merozoites 2. 5 to 3 /i long. They 
were not sure, however, whether it was 
part of the life cycle of E. parva. 

The sexual stages occur mostly in the 
cecum and colon and to a lesser extent in 
the small intestine. They are found in the 
epithelial cells and measure 15 to 19 by 10 
to 16 p.. 

Pathogenesis : This species is appar- 
ently not very pathogenic. Most of the 
damage is caused by the sexual stages in 
the large and small intestines. In a lamb 
killed by Kotlan, Pelle'rdy and Versenyi 
(1951) 16 days after experimental infection, 
the contents of the cecum and colon were 
semifluid, dark and mixed with blood in 
places. The wall was thickened and its 
surface uneven and denuded of epithelium 
in places. By histologic examination of the 
cecum, it was found that the mucosa had 
been stripped from the glandular layer in 
places and the tissue had become necrotic 
and infiltrated with lymphocytes and neu- 
trophiles but no eosinophiles. Sharply 
separated from these necrotic areas were 
other areas in which most of the epithelial 
cells contained microgametocytes, macro- 
gametes or young oocysts. 



EIMERIA PUNCTATA 
LANDERS, 1955 



Synonym : Eimeria honessi Landers, 



1952. 

Host : Sheep. 

Location : Unknown. Oocysts found 
in feces. 



Geographic Distribution : 
America (Wyoming). 



North 



Prevalence : Landers (1952) found 
this species in 2 of 9 sheep in Wyoming. 

Morphology : This species has been 
described by Landers (1952). The oocysts 
are subspherical, 18 to 25 by 16 to 21 fi. 
with a mean of 21.2 by 17.7 j^. Their 
length-width ratio is 1. 1 to 1. 3 with a 
mean of 1. 20. The oocyst wall has 



188 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



conspicuous, uniform, cone-shaped pits 
about 0. 5/jL in diameter. It is 1. 2 to 1. Sfi 
thick (mean, 1.5fi); its outer layer is 
colorless to yellowish, and its inner layer 
greenish, with two dark refraction lines, 
one at either surface. There is a conspic- 
uous micropyle. A micropylar cap is 
present, sometimes imperceptible, up to 
6. 5(i wide and 1.6^ high with a mean of 
4. 1 by 0. 8 )i . An oocyst residuum and 



oocyst polar granule are absent. The 
sporocysts are spherical to ellipsoidal, 
and average 8. 1 |j. in diameter or 10. 4 by 
6. 9 (1 . The presence or absence of a 
sporocyst residuum was not mentioned. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 




Fig. 26. Coccidia of sheep. A. Eimeria pallula unspornl^tedoocysU ^'JJ'^^^J'!^ 
^ sporulated oocyst. C. E. parva unsporulated oocyst D. E. mnakohlyakn 

o.aeunsporulated oocyst. E. E. '"''"■«'" ""fP^^^l^^'^'^o^^'y^'v ^^,„^;,/;;; 
porulated oocyst. G. E. arloinni unsporulated oocyst. H £^ ^~°"' 
Dorulated oocyst. I. £. A'>-«««/osa sporulated oocyst. X 1270. (From 



E. faiirei 



uns 

unsporulated oocyst 

Christensen, 1938) 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



189 



COCCIDiOSIS IN SHEEP AND GOATS 

Coccidiosis in sheep is primarily a 
disease of feedlot lambs. It has been 
studied by Newsom and Cross (1931), 
Deem and Thorp (1939, 1940) and Chris- 
tensen (1940) among others. It appears 
12 days to 3 weeks after the lambs arrive 
in the feedlot. Diarrhea, depression and 
inappetance appear, followed by weakness 
and loss of weight. The diarrhea continues 
for several days up to about 2 weeks, and 
some lambs may die during this period. 
Most, however, recover. The mortality 
varies, but is seldom more than 10%. In 
a group of 16, 000 New Mexico feeder 
lambs studied by Christensen (1940) on a 
Nebraska feedlot, the mortality was 3.4%, 
but another 9. 8% of scouring, emaciated 
lambs were removed to a hospital lot for 
special diet and care. 

Even if there are no deaths, there 
may be loss of weight or reduced weight 
gains. Thus, Shumard (1957) found that 
80 lambs experimentally infected with a 
sublethal mixture of coccidian oocysts 
(mostly E. nlnakohlyakimovae and£. 
arloingi) lost an average of 0.205 pounds 
per pound of feed consumed during the 24 
days following infection, as compared 
with an average gain of 0. 062 pounds per 
pound of feed consumed for 40 control, 
uninfected lambs. 

When lambs are brought into the feed- 
lot, they are usually shedding small num- 
bers of coccidian oocysts. As the result 
of crowding, and under conditions which 
promote fecal contamination of the feed, 
the coccidial infections build up. The 
number of oocysts in the feces rises for 
about a month, remains stationary for 1 
to 3 weeks and then decreases rather 
rapidly, only a few oocysts being present 
at the end of the feeding period. Whether 
or not disease will appear depends upon 
the number and species of oocysts which 
the lambs ingest during the crucial first 
week or two. By the end of the first 
month, there is little danger of coccidio- 
sis. The lambs have been infected, but 
the exposing dose of oocysts has been 
small enough to permit immunity to de- 
velop. In other words, there has been 
coccidiasis but no coccidiosis. 



Feeding of chopped feed in open troughs 
low enough to be contaminated with feces 
promotes coccidiosis. Christensen (1941a) 
found that corn silage provided an amount 
of moisture which favored oocyst sporula- 
tion, while chopped alfalfa, grain and mo- 
lasses also permitted sporulation. 

Dunlap, Hawkins and Nelson (1949) 
followed oocyst production from the time 
of birth in lambs running with their mothers. 
The ewes were the source of infection, and 
lambs became infected by ingesting sporu- 
lated oocysts from the bedding. The first 
oocysts appeared when the lambs were 5 to 
8 weeks old; they built up to a peak which 
lasted 1 to 4 weeks, and then declined. 

Temperature affects oocyst sporula- 
tion. Dunlap, Hawkins and Nelson (1949) 
found the first sporulated oocysts in the 
bedding when the mean temperature was 
49° F. Christensen (1939) found that the 
optimum sporulation temperature for the 
oocysts of E. arloingi was 20-25° C, the 
sporulation time being 2 to 3 days at that 
temperature in a thin layer of water or in 
fecal pellets. The oocysts survived less 
than 4 months in fecal sediment at this 
temperature. Sporulation was slow at 
to 5° C, altho oocysts remained alive for 
at least 10 months in fecal sediment or 
moist pellets. No sporulation took place 
at 40° C and the oocysts were killed within 
4 days. If the fecal sediment was allowed 
to putrefy, however, no sporulation took 
place at any temperature. 

Landers (1953) found that the oocysts 
of E. arloi)igi, E. ninakohlyakiniovae and 
E. parva did not survive 24 hours in sheep 
pellets when frozen directly to -30° C, and 
survived less than 2 days when conditioned 
at -19° C prior to freezing to -30°. They 
survived without essential mortality when 
frozen directly to -25° C for 7 days, but 
only about half of the first two species and 
one quarter of E. parva survived 14 days. 
Repeated freezing and thawing at -19 or 
-25° C up to 6 or 7 times had no significant 
effect on survival. Landers said that in an 
average winter at Laramie, Wyoming the 
minimum soil surface temperature would 
probably be between -15 and -20° C and 
that unsporulated oocysts would not nor- 
mally be killed by such temperatures. 



190 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



Diagnosis : Coccidiosis in sheep and 
goats can be diagnosed from a combination 
of history, signs, gross lesions at necropsy 
and microscopic examination of the intes- 
tinal mucosa and feces. However, recog- 
nition of coccidia in the lesions at necropsy 
is necessary for positive diagnosis. The 
mere presence of oocysts in the feces does 
not necessarily mean that the disease is 
due to coccidia. On the other hand, acute 
coccidiosis may be present before any 
oocysts appear. 

Treatment : Relatively few studies 
have been carried out on the treatment of 
coccidiosis in sheep. A distinction must 
be made between preventive and curative 
treatments. Several sulfonamides and 
sulfur are of value in preventing coccidio- 
sis in lambs, but no drugs are known to 
cure the disease once signs appear. How- 
ever, oxytetracycline and related anti- 
biotics may be of value in controlling sec- 
ondary infections. 



Christensen (1944) found that 0. 5 to 
1. 5% sulfur fed in a ration of chopped al- 
falfa and ground corn held together by 
molasses and water prevented coccidiosis 
in feeder lambs. He fed this amount of 
sulfur for 72 days without ill effects, but 
higher concentrations caused diarrhea and 
decreased weight gains. 

Tarlatzis, Panetsis and Dragonas 
(1955) claimed that furacin was effective 
against coccidiosis in sheep and goats, 
but their work was uncontrolled. 

Prevention : Good sanitation will 
largely prevent coccidiosis in lambs. 
Coccidiosis is not a problem in suckling 
lambs on the western range, but appears 
when the animals are brought together in 
the feedlot. Feedlots should be kept dry 
and clean. Clean water and feed should be 
supplied, and feed troughs should be so 
constructed that they cannot be contamin- 
ated with feces. 



Foster, Christensen and Habermann 
(1941) found that 2 g sulfaguanidine a day 
prevented the acquisition of natural coc- 
cidiosis in 5 lambs and reduced the level 
of oocyst output in 4 subclinical infections 
with unnamed species. Christensen and 
Foster (1943) reported that 0.2% sulfa- 
guanidine in the feed for 20 days beginning 
1 day after an infective feeding with 500,000 
sporulated oocysts from lambs with clin- 
ical coccidiosis prevented severe coccid- 
iosis in lambs, but that 0.45% sulfaguanidine 
failed to affect the course of the disease 
when it was begun the day after clinical 
signs had appeared. Steward (1952) found 
that sulfamethazine and sulfadiazine had 
some value in an outbreak of coccidiosis 
in sheep, reducing the numbers of oocysts 
passed, but that quinacrine was valueless. 
Whitten (1953) found in a controlled exper- 
iment that neither 0.01 g per kg quinacrine 
hydrochloride nor 0.01 g per kg sulfameth- 
azine daily for 3 days had any significant 
effect on oocyst production or weight gains 
in naturally affected lambs. However, 
oocyst production decreased markedly 
markedly in both ireated lambs and controls 
following treatment, so that if no controls 
had been used, it would have been assumed 
that the treatment had been of value. 



Coccidiosis is a potential hazard if 
lambing takes place in a barn or restricted 
area, and the bedding is the most common 
source of infection. Shumard and Eveleth 
(1956) recommended as a practical method 
for raising lambs with their ewes that the 
animals be kept in concrete pens with 
straw bedding, that the pens be cleaned 
twice a week, and that 1 pint of a 3. 45% 
sulfaquinoxaline solution be added to each 
50 gallons of drinking water. In their 
studies, coccidian oocysts did not appear 
in the lambs until 18 days after treatment 
had been discontinued. 



EIMERIA DEBLIECKI 
DOUWES, 1921 

Synonyms : Eimeria bri(»if>ti, Eimeria 
jaliiia, Eimeria suis. 

Host: Pig. 

Location : Small intestine, and, to a 
lesser extent, large intestine. 

Geographic Distribution : Worldwide. 

Prevalence : E. debUecki is the com- 
monest coccidium of swine. De Graff 
(1925) found it in 51% of 500 pigs in the 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



191 



Netherlands. Yakimoff e/ flZ. (1936) found 
it in 92% of 141 pigs in Russia. Yakimoff 
(1936) found it in 27% of 53 pigs from 
Brazil. Novicky (1945) found it in 27% of 
62 pigs in Venezuela. Nieschulz and 
Ponto (1927) found it in all of about 50 
pigs in Java. 

Morphology : The oocysts are ovoid 
to ellipsoidal or subspherical, 13 to 29 by 

13 to 19/1. The oocyst wall is 1.0 to 
1.5ii thick, smooth, colorless to brown- 
ish, and composed of 2 layers. A micro- 
pyle is absent. An oocyst polar granule 
is absent (present according to Paichuk, 
1953). An oocyst residuum is absent. 
The sporocysts are ellipsoidal or ovoid, 

14 to 18 by 6 to 8|:x with a Stieda body. A 
sporocyst residuum is present. 

The sporulation time is 6 to 9 days. 
The sporulation process has been des- 
cribed in detail by de Graaf (1925). 



that pigs experimentally infected with 20 
to 30 million mixed sporulated oocysts of 
E. debliecki and E. scabra developed a 
profuse diarrhea lasting 2 to 15 days, 
inappetance and did not gain weight. 
Swanson and Kates (1940) described an 
outbreak of coccidiosis in a litter of 4. 5 
month old pigs in Georgia. The pigs had 
a profuse diarrhea and gained weight 
poorly despite ravenous appetites, excel- 
lent rations and good care. Novicky (1945) 
described several outbreaks of swine coc- 
cidiosis in Venezuela. The mortality was 
relatively low, but the young animals 
which survived were retarded. 

Immunity : Biester and Schwarte 
(1932) produced complete immunity in pigs 
by feeding them oocysts daily for 100 days 
or more. Light infections produced partial 
immunity. As with other coccidia, adult 
pigs are often carriers, shedding a few 
oocysts in their feces. 



Life Cycle : De Graaf (1925) and 
others have described the endogenous 
stages of this species. The schizonts 
produce 14 to 16 banana-shaped mero- 
zoites. These are 8 to 10 |i long and 3 to 
4. 5ju wide; one end is rounded and the 
other pointed. The nucleus is usually in 
the middle of the merozoites. The micro- 
gametocytes are 7 to 22|U in diameter 
when mature. The microgametes are 
3. 5jLt long and 0. 6;i wide and have 2 fla- 
gella. The macrogametes are similar to 
those of other Eimeria species. 



Remarks : Brug (1946) found E. deb- 
liecki as a pseudoparasite of man in Hol- 
land. Four out of 13 persons in a psychi- 
atric ward passed oocysts in their feces 
on one day. They had probably been in- 
gested with liver sausage, the casing of 
which was made from pig intestines. 



EIMERIA PERMINUTA 
HENRY, 1931 



Host : Pig. 



Biester and Schwarte (1932) found that 
the prepatent period in experimentally in- 
fected pigs was about 7 days and that 
oocysts were present in the feces for 10 
to 15 days in the absence of reinfection. 

Pathogenesis : E. debliecki is only 
slightly pathogenic if at all in adult ani- 
mals, but it may cause diarrhea and even 
death in young pigs. Biester and Murray 
(1929) found that young pigs fed large num- 
bers of sporulated oocysts developed 
severe diarrhea. They became emaciated 
and some even died. Some had constipa- 
tion, but dysentery was never observed. 
The pigs which recovered usually failed to 
do wen. Alicata and Willett (1946) found 



Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : Worldwide. 

t* Prevalence : Yakimoff et al. (1936) 
found this species in 18% of 141 pigs in 
Russia. Yakimoff (1936) found it in 45% 
of 53 pigs in Brazil. 

Morphology : This species was first 
described by Henry (1931) from pigs in 
California. The oocysts are ellipsoidal 
to spherical, 11 to 16 by 10 to 13jj,. The 
oocyst wall is rough, yellowish, and ap- 
parently composed of a single layer. A 
micropyle is absent. An oocyst polar 



192 



THE TELOSPORASIDA AND THE CCXTCIDIA PROPER 



granule is present. No other morphologi- 
cal information is known. The sporulation 
time is 11 days. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

EIMERIA POLITA 
PELLERDY, 1949 

Host : Pig. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : Europe 
(Hungary), North America (Alabama). 

Prevalence : Unknown. 

Morphology : This species has been 
described by Pelle'rdy (1949) in Hungary 
and by Lesser and Davis (1958) in Alabama. 
The oocysts are ellipsoidal, rarely broadly 
ovoid, 17 to 36 by 13 to 24 (J, with a mean of 
23. 8 by 17. 9 |Lt . The oocyst wall is smooth 
or occasionally roughened, yellowish 
brown or pinkish brown, 1.0 to 1.5 /j, thick. 
The micropyle is imperceptible or is seen 
only when the oocyst lies in a favorable 
position. A polar granule is present in 
about half the oocysts. There is no oocyst 
residuum. The sporocysts are ellipsoidal, 
15tol9by6/i. A sporocyst residuum is 
present. The sporulation time is 8 to 9 days. 

Life Cycle : Unknown. Pellerdy (1949) 
found that the prepatent period in 3 exper- 
imentally infected pigs was 8 to 9 days. 

Pathogenesis : Unknown. 

EIMERIA SCABRA 
HENRY, 1931 

Host : Domestic and wild pigs. 

Location : Intestine. The sexual 
stages are found in the epithelial cells of 
the villi. 

Geographic Distribution : Worldwide. 



Prevalence : Yakimoff et al. (1936) 
found this species in 33% of 141 pigs in 
Russia. 

Morphology : The oocysts are ovoid 
to ellipsoidal, 22 to 36 by 16 to 28 ^ . The 
oocyst wall is brown, rough, and 1. 5 to 
2.0ji thick, becoming thinner at the nar- 
row end. A micropyle is present accord- 
ing to Pelle'rdy (1949), but was not men- 
tioned by Henry (1931). An oocyst polar 
granule is present. There is no oocyst 
residuum. The sporocysts are ellipsoidal, 
15 to 19 by 6 jM, and have a sporocyst res- 
iduum. The sporulation time is 9 to 12 
days. 

Life Cycle : The endogenous stages 
of this species have not been described. 
Pelle'rdy (1949) found that the prepatent 
period in 2 experimentally infected pigs 
was 9 days. 

Pathogenesis : Uncertain. Alicata 
and Willett (1946) found that pigs experi- 
mentally infected with 20 to 30 million 
mixed sporulated oocysts of E. debliecki 
and E. scabra developed a profuse diar- 
rhea lasting 2 to 15 days, lost their appe- 
tites and did not gain weight. How much 
of this effect was due to E. scabra is not 
known. 



EIMERIA SCROFAE 
GALLI-VALERIO, 1935 

Host : Domestic pig. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : Europe 
(Switzerland). 

Prevalence : Unknown. 

Morphology : This species has been 
described only by Galli-Valerio (1935). 
The oocysts are cylindroid, with one end 
slightly flattened, and measure 24 by 15fi. 
There is a distinct micropyle. Oocyst and 
sporocyst residua are absent. The sporont 
is finely granular. Pelle'rdy (1949) con- 
sidered this a rather doubtful species 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



193 



resembling E. debliecki. However, the 
absence of a sporocyst residuum and 
presence of a micropyle differentiate it 
from this species. 

Life Cycle : Unknown. 

Pathogenesis : Unknown . 

FIMBRIA SPINOSA 
HENRY, 1931 

Host : Pig. 

Location : Unknown. Oocysts found 
in feces. 



sorted out and their importance assessed. 
Coccidia are among the least known of 
these agents. 

Coccidiosis is primarily a disease of 
young pigs. Adults are carriers. Eiiiieria 
debliecki is probably the most pathogenic 
species, but E. scabra and Isospora suis 
may also cause disease. 

Pigs become infected by ingesting 
sporulated oocysts along with their feed 
or water. The presence or severity of 
the disease depends upon the number of 
oocysts they receive. Crowding and lack 
of sanitation greatly increase the disease 
hazard. 



Geographic Distribution : North 
America (California, Minnesota, Mary- 
land, Georgia), Hawaii, USSR (North 
Caucasus). 

Prevalence : Unknown. This species 
appears to be relatively uncommon. 

Morphology : This species was des- 
cribed by Henry (1931). The oocysts are 
ovoid or ellipsoidal, 16 to 22 by 10 to 
13 ju.. The oocyst wall is brown, opaque, 
and studded with spines about 1 /i long and 
1 iu apart. A micropyle is absent. An 
oocyst polar granule is present. An 
oocyst residuum is apparently absent. 
The sporocysts have a Stieda body. A 
sporocyst residuum is apparently present 
(Henry's description is ambiguous). The 
sporulation time is 11 to 12 days. 

Pathogenesis : This species is only 
slightly pathogenic if at all. Andrews and 
Spindler (1952) observed no diarrhea or 
other signs in an infected pig which passed 
as many as 7 million oocysts per gram of 
feces. 



COCCIDIOSIS IN SWINE 

Epidemiology : Coccidia are common 
in swine, but we know little about the 
prevalence and importance of the disease, 
coccidiosis. Enteritis is so common in 
young pigs and is caused by so many dif- 
ferent agents that they have not all been 



Avery (1942) found that the oocysts of 
E. debliecki and E. scabra could survive 
and remain infective in the soil for 15 
months. The soil surface temperature 
varied between -4. 5° and 40° C during 
this period. Unsporulated oocysts with- 
stood continuous freezing at -2^ to -7° C 
or alternate freezing and thawing at 0. 5° 
and -3° C for at least 26 days, altho sub- 
sequent sporulation was somewhat de- 
creased. 

Immunity : Repeated infections over 
a period of time confer immunity to coc- 
cidiosis. Blester and Schwarte (1932) 
produced complete immunity in pigs by 
feeding oocysts daily for 100 days or 
more. Light infections produced partial 
immunity. 

The coccidia of swine are not trans- 
missible to other farm animals, and pigs 
cannot be infected with their coccidia. 

Diagnosis : Coccidiosis in swine can 
be diagnosed by finding the endogenous 
stages in lesions in the intestine. The 
presence of oocysts in the feces does not 
necessarily mean that coccidiosis is 
present, nor does their absence necessar- 
ily mean that it is absent, since oocysts 
may not be produced until 2 or 3 days 
after the first signs of disease appear. 

Treatment : Little is known about 
treatment of coccidiosis in pigs. Alicata 
and Willett (1946) found that when 1 g 



194 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



sulfaguanidine per 10 lb body weight was 
administered to pigs daily with their feed 
for 7 or 10 days beginning 2 days before 
experimental infection with 20 to 30 mil- 
lion sporulated oocysts of E. debliecki and 
E. scabva, very few if any oocysts were 
produced and the pigs did not become ill. 
Similar treatment with sulfaguanidine for 
3 days beginning on the 2nd day of oocyst 
discharge reduced the numbers of occysts 
produced and the period of discharge. 
Presumably other sulfonamides would also 
be of value. 

Prevention and Control : Sanitation 
will prevent coccidiosis in swine. Pens 
should be cleaned frequently, overcrowd- 
ing should be avoided, and pigs should be 
raised under conditions which prevent 
them from eating many infective oocysts. 



the hot days of October in India (Hire- 
gaudar). 

Life Cycle : The schizonts and mero- 
zoites of this species have not been des- 
cribed. The sexual stages were described 
most recently by Hemmert-Halswick (1943). 
They are found beneath the epithelium in 
the villi of the small intestine. The mi- 
crogametocytes measure up to 300 by 
170|i when mature. The macrogametes 
contain both eosinophilic and basophilic 
plastic granules which later form the wall 
of the oocyst. 

Pathogenesis : Diarrhea, loss of 
weight and even death have been reported 
in heavily infected animals. Hemmert- 
Halswick (1943) described marked inflam- 
matory changes in the small intestine 
mucosa. 



EIMERIA LEUCKARTI 
(FLESCH, 1883) 
REICHENOW, 1940 

Synonyms : Globidium leuckarti. 

Hosts: Horse, ass. 



Diagnosis : Diagnosis can be made 
by finding the endogenous stages of this 
coccidium in association with lesions in 
the intestine. The oocysts are seldom 
seen in feces because they are so heavy 
that they do not rise to the surface in the 
salt solutions used for flotations. 



Location : Small intestine. 

Geographic Distribution : Europe, 
India. 

Prevalence : Apparently uncommon. 

Morphology : The sporulated oocysts 
have been described by Reichenow (1940a) 
and Hiregaudar (1956a). They are ovoid, 
somewhat flattened at the smaller end, 
and 75 to 88 by 50 to 59 /i. The oocyst 
wall is composed of 2 layers, of which the 
outer is dark brown, 5 to 7)j, thick, opaque 
and granular, and the inner layer is about 
1 [i. thick and colorless. The micropyle is 
distinct. An oocyst residuum is absent. 
An oocyst polar granule is apparently ab- 
sent. The sporocysts are elongate, 30 to 
42 by 12 or \A\x with a Stieda body. A 
sporocyst residuum is present. The 
sporozoites are elongate, up to 35 ji long, 
with a clear globule at the large end. The 
sporulation time is 21 days at 20 to 22° C 
in Germany (Reichenow) or 15 days during 



EIMERIA SOLIPEDUM 
GOUSSEFF, 1935 

Hosts : Horse, ass. 

Location: Unknown. Oocysts found 
in feces. 

Geographic Distribution : USSR 
(Azerbaidzhan, Volga basin, Leningrad). 

Prevalence : Gousseff (1935) found 
this species in 1.4% of 3355 horses, 3% 
of 251 donkeys and 1% of 161 mules in 
Russia. 

Morphology : The oocysts are spher- 
ical, bright orange to yellowish brown, 
and 15 to 28 jn in diameter. The oocyst 
wall is double contoured, without a micro- 
pyle. An oocyst residuum and polar gran- 
ule are absent. The sporocysts are 
ellipsoidal or oval, 5by3fi. The sporo- 
zoites are piriform. The presence or 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



195 



absence of a sporocyst residuum could 
not be determined. 

Life Cycle ; Unknown. 

Pathogenesis : Unknown. 

EIMERIA UNIUNGULATI 
GOUSSEFF, 1935 

Hosts : Horse, ass. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : USSR 
(Azerbaidzhan, western RSFSR, Volga 
region, Leningrad, Siberia, Tadzhikistan, 
Uzbekistan). 

Prevalence : Gousseff (1935) found 
this species in 0. 8% of 3355 horses, 3% 
of 251 donkeys and 1% of 161 mules in 
Russia. 

Morphology : The oocysts are oval 
(ellipsoidal?), bright orange, and 15 to 
24 by 12 to 17 )n . The oocyst wall is 
double contoured. A micropyle, oocyst 
residuum and polar granule are absent. 
The sporocysts are 6 to 11 by 4 to 6 jn . 
A sporocyst residuum is present. 

Life Cycle : Unknown. 

Pathogenesis: Unknown. 



Geographic Distribution : Europe 
(England, Holland), North America (Ne- 
braska, Quebec), Australia. 

Prevalence : This form is uncommon. 
It was found by Brown and Stammers (1922) 
and Wenyon (1923) in England, Nieschulz 
(1924) in Holland, Skidmore and McGrath 
(1933) in Nebraska and Bearup (1954) in a 
dingo in Australia. Choquette and Gelinas 
(1950) reported it in 10% of 155 dogs in 
Quebec. 

Morphology : The oocysts are ovoid 
or ellipsoidal, 17 to 45 by 11 to 28/i, 
pink, red or colorless. The oocyst wall 
is fairly thick, rough, and composed of 2 
layers. A micropyle is present. The 
sporocysts measure 9. 5 by 2. 5|u. The 
sporulation time is 1 to 4 days. 

Remarks : It is far from certain that 
this is a valid species. Wenyon (1926) 
remarked that in many respects E. canis 
resembles a mixture of E. stiedae and E. 
perforans of the rabbit, and Goodrich 
(1944) considered it to be a rabbit form 
which the dogs had eaten. 



EIMERIA CATI 
YAKIMOFF, 1933 

Hosts: Cat, dog. 

Location: Intestine. 



COCCIDIOSIS IN HORSES, 
ASSES AND MULES 

Coccidiosis is such a rarity in horses, 
asses and mules that little can be said 
about it. The same measures which are 
effective in cattle should control coccid- 
iosis in equids. 

EIMERIA CANIS 
WENYON, 1923 

Hosts :. Dog, cat, dingo. 

Location : Unknown. Oocysts found 
in feces. 



Geographic Distribution : USSR. 

Prevalence : Rare. 

Morphology : The oocysts are ovoid 
or spherical; the ovoid oocysts are 18 to 
24 by 14 to 20 ji with a mean of 21 by 17 fj,; 
the spherical oocysts are 16 to 22 jj. in 
diameter with a mean of 18jj, . A micro- 
pyle is absent. An oocyst polar granule 
is present. An oocyst residuum is absent. 
A sporocyst residuum is present. 

Life Cycle: Unknown. 

Pathogenesis: Unknown. 



196 



TlIF TELOSPORASIDA AND THE COCCIDIA PROPER 



EIMERIA FELINA 
NIESCHULZ, 1924 

Hosts : Cat, lion. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : Europe 
(Holland). 

Prevalence : Rare. 

Morphology : The oocysts are ellip- 
soidal, 21 to 26 by 13 to 17 ji with a mean 
of 24 by 14. 5ji. The oocyst wall is about 
1 ^t thick, smooth, colorless, and double 
contoured. A definite micropyle is ab- 
sent. An oocyst polar granule is absent. 
An oocyst residuum is present. The 
sporocysts are elongate ovoid, with a 
Stieda body. A sporocyst residuum is 
present. The sporozoites are comma- 
shaped, with a large vacuole at the large 
end and usually a small one at the small 
end. 

Life Cycle : Unknown. 

Pathogenesis: Unknown. 



EIMERIA STIEDAE 

(LINDEMANN. 1865) 

KISSKALT AND HARTMANN, 1907 

Synonyms : Monocystis stiedae, 
Cocciditu)! ovi/orme, Coccidium cimicidi. 

Hosts : Domestic rabbit, European 
hare (Lepus europaeiis), varying hare 
(L. aniericanHs), black-tailed jack rabbit 
(L. calif or nic us), alpine hare (L. tini- 
idus), L. variabilis, cottontails {Sylvil- 
agus floridanus , S. nuttalli). 

Location : Liver. The coccidia are 
found in the bile duct epithelial cells. 

Geographic Distribution : Worldwide. 

Prevalence : This is the most com- 
mon and most important coccidium of 
domestic rabbits. It also occurs in hares 
{Lepus), but is less common in cottontails 
than other species. 



Morphology : The oocysts are ovoid, 
sometimes ellipsoidal, with a flat micro- 
pylar end, and measure 28 to 40 by 16 to 
25 ji with a mean of 37 by 21 /i . The 
oocyst wall is smooth and salmon-colored. 
A micropyle is present. An oocyst polar 
granule and oocyst residuum are absent. 
The sporocysts are elongate ovoid, 18 to 
10 |i, with a Stieda body. A sporocyst 
residuum is present. The sporulation 
time is 3 days. 

Life Cycle : The life cycle of this 
species has been studied by a number of 
workers (see Becker, 1934, for a review). 
The sporulated oocysts excyst in the small 
intestine. The sporozoites penetrate the 
intestinal mucosa, enter the hepatic portal 
system, and pass to the liver. Here they 
enter the epithelial cells of the bile ducts. 
The liver parenchyma cells are only rarely 
invaded. Development takes place above 
the host cell nucleus. Each sporozoite 
rounds up and becomes a schizont which 
produces 6 to 30 or more (usually 8 to 16) 
merozoites which measure about 8 to 10 
by 1. 5 to 2. 0(1 . The number of asexual 
generations is not known. Later, some 
merozoites become microgametocytes 
which produce large numbers of comma- 
shaped, biflagellate microgametes, while 
others become macrogametes. These are 
fertilized, lay down an oocyst wall, break 
out of their host cell, pass into the intes- 
tine with the bile and thence out of the 
body. The prepatent period is 18 days. 

Pathogenesis : In mild cases of liver 
coccidiosis there may be no signs, but in 
more severe ones the animals lose their 
appetites and grow thin. There may be 
diarrhea, and the mucous membranes may 
be icteric. The disease is more severe in 
young animals than in old. It may be 
chronic, or death may occur in 21 to 30 
days. 

Some of the symptoms are due to in- 
terference with liver function. The liver 
may become markedly enlarged, and white 
circular nodules or elongated cords appear 
in it. At first they are sharply circum- 
scribed, but later they tend to coalesce. 
They are enormously enlarged bile ducts 
filled with the developing parasites. 
There is tremendous hyperplasia of the 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



197 



bile duct epithelial cells. Instead of form- 
ing a simple, narrow tube, the epithelium 
is thrown into great, arborescent folds, 
and each cell contains a parasite. 

Dunlap, Dickson and Johnson (1959) 
found that infection with E. stiedae in- 
creased the serum /3- and y-globulin and 
i3-lipoprotein and decreased the a-lipo- 
protein. 



EIMERIA MAGNA 
PERARD, 1925 

Synonyms: Eimeria p erf or ans var. 
magna. 

Hosts : Domestic rabbit, California 
jack rabbit {Lepus calif ornicus), varying 
hare (L. tiniidus), European hare (L. 
europaeus), cottontail (Sylvilagus flori- 
danus) (experimental). 

Location : Jejunum, ileum. 

Geographic Distribution : Worldwide. 

Prevalence : This species is quite 
common. Kessel and Jankiewicz (1931) 
found it in 19% of over 2000 rabbits in 
California. 

Morphology : The oocysts are ovoid 
or ellipsoidal, becoming subspherical 
toward the end of the patent period, 
smooth, orange-yellow or brownish, and 
27 to 41 by 17 to 29 ;j with a mean of 35 
by 24jLL. The micropyle is large and sur- 
rounded by prominent shoulders. An 
oocyst polar granule is absent. An oocyst 
residuum is present. The sporocysts are 
elongate ovoid, with a Stieda body. A 
sporocyst residuum is present. The 
sporulation time is 2 to 3 days. Oocyst 
variation was studied carefully by Kheisin 
(1947). 

Life Cycle : Rutherford (1943) des- 
cribed the life cycle of this species. The 
endogenous stages are found below the 
epithelial cell nuclei of the villi and also 
in the submucosa. There are 2 asexual 
generations of merozoites followed by 
microgamete and macrogamete production. 



It takes 7 days for completion of the endo- 
genous cycle, and the prepatent period is 
7 to 8 days. According to Kheisin (1947), 
E. magna produces 800,000 oocysts per 
oocyst fed. 

Pathogenesis : This is one of the 
most pathogenic of the intestinal coccidia 
of the rabbit. Only a few hundred oocysts 
of some strains may produce symptoms, 
and 300,000 may cause death (Lund, 1949). 
Other strains are less pathogenic, 1 mil- 
lion oocysts not causing death. The prin- 
cipal signs are loss of weight, inappetance 
and diarrhea. A good deal of mucus may 
be passed. The animals lose their appe- 
tites and grow thin. The intestinal mucosa 
is hyperemic and inflamed, and epithelial 
sloughing may occur. 



EIMERIA PERFORANS 

(LEUCKART, 1879) 

SLUITER AND SWELLENGREBEL, 1912 

Synonyms : Coccidium perforans, 
Eimeria exigiia, E. Jugdunumensis. 

Hosts : Domestic rabbit, varying 
hare {Lepus americanus), east Greenland 
hare (L. arcticus groenlandicus), Califor- 
nia jack rabbit (L. calif ornicus), European 
hare {L. europaeus), Brazilian cottontail 
{Sylvilagus brasiliensis), cottontail {Syl- 
vilagus floridanus) (experimentally). 

Location : Thruout small intestine 
and also in cecum. 

Geographic Distribution : Worldwide. 

Prevalence : Common. Kessel and 
Jankiewicz (1931) found it in 30% of over 
2000 rabbits in California. 

Morphology : The oocysts are 
ellipsoidal, sometimes ovoid, smooth, 
colorless to pinkish, 24 to 30 by 14 to 
20jLi with a mean of 26 by lOju . A 
micropyle is absent. An oocyst polar 
granule is absent. An oocyst residuum 
is present. The sporocysts are ovoid, 
with a Stieda body. A sporocyst residuum 
is present. The sporulation time is 
2 days. 



198 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



Life Cycle : Rutherford (1943) des- 
cribed the life cycle of this species. The 
endogenous stages are found above the 
nuclei of the epithelial cells of the intes- 
tine. There are 2 asexual generations of 
merozoites, followed by microgamete and 
macrogamete production. Completion of 
the endogenous cycle takes 5 days, and 
the prepatent period is 5 to 6 days. 

Pathogenesis : E. perforans is one 
of the less pathogenic intestinal coccidia 
of rabbits, but it may nevertheless cause 
mild to moderate signs if the infection is 
heavy enough. The duodenum may be en- 
larged and edematous, sometimes chalky 
white; the jejunum and ileum may contain 
white spots and streaks, and there may 
be petechiae in the cecum. 



production. Completion of the endogenous 
cycle takes 6 days, and the prepatent per- 
iod is 5 to 6 days. According to Kheisin 
(1947), E. media produces 150, 000 oocysts 
per oocyst fed. 

Pathogenesis : This species is moder- 
ately pathogenic (Pelle'rdy and Babos, 1953). 
It may cause the usual signs of intestinal 
coccidiosis. The affected parts of the in- 
testine may be edematous, with greyish 
foci. 



EIMERIA IRRESIDUA 

KESSEL AND JANKIEWICZ, 1931 

Hosts : Domestic rabbit, California 
jack rabbit {Lepus calif ornicus), white- 
tailed jack rabbit (L. loivnsendii). 



EIMERIA MEDIA 
KESSEL, 1929 

Synonym: Eimeria flavescens. 

Hosts : Domestic rabbit, California 
jack rabbit (Lepus californicus), cotton- 
tail {Sylvllagiis floridamis), Wyoming 
cottontail (S. niiltallii grangeri). 

Location: Thruout small and large 
intestines. 

Geographic Distribution : Worldwide. 

Prevalence : Quite common. Kessel 
and Jankiewicz (1931) found it in 12% of 
over 2000 rabbits in California. 

Morphology : The oocysts are ovoid, 
smooth, 19 to 33 by 13 to 21 jii . A micro- 
pyle is present. An oocyst polar granule 
is absent. An oocyst residuum is present. 
The sporocysts are elongate ovoid, with a 
Stieda body. A sporocyst residuum is 
present. The sporulation time is 2 days. 

Life Cycle : Rutherford (1943) and 
Pellerdy and Babos (1953) described the 
life cycle of this species. The endogenous 
stages are found above or below the epi- 
thelial cell nuclei of the intestinal villi 
and also occur in the submucosa. There 
are 2 asexual generations of merozoites 
followed by microgamete and macrogamete 



Location : Thruout small intestine. 

Geographic Distribution: Worldwide. 

Prevalence : Quite common. Kessel 
and Jankiewicz (1931) found this species 
in 10% of over 2000 rabbits in California. 

Morphology : The oocysts are ovoid, 
smooth, and 38 by 26 jm. The micropyle 
is prominent. An oocyst polar granule 
and oocyst residuum are absent. The 
sporocysts are elongate ovoid, with a 
Stieda body. A sporocyst residuum is 
present. The sporulation time is 2 to 2. 5 
days. 

Life Cycle : Rutherford (1943) des- 
cribed the life cycle of this species. The 
endogenous stages are found above or be- 
low the epithelial cell nuclei of the intes- 
tinal villi and also occur in the submucosa. 
There are 2 asexual generations of mero- 
zoites followed by microgamete and macro- 
gamete production. Completion of the 
endogenous cycle takes 9 to 10 days, and 
the prepatent period is 9 to 10 days. 

Pathogenesis : This is one of the 
more pathogenic of the intestinal coccidia 
of rabbits. It causes the usual signs of 
intestinal coccidiosis. The affected areas 
are hyperemic, there may be extravasation 
of blood, and the epithelium may slough 
and become denuded. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



199 



EIMERIA PIRIFORMIS 
KOTLAN AND POSPESCH, 1934 

Host : Domestic rabbit. 

Location: Small and large intestines. 



Geographic Distribution : 
(France, Hungary). 



Europe 



Prevalen ce: 
This species 



Relatively uncommon. 



has been found in both wild 
and captive domestic rabbits. 

Morphology : The oocysts are piri- 
form to ovoid, smooth, yellowish brown, 
26 to 32 by 17 to 21 ji with a mean of 29 
by 18jn. A micropyle is present. An 
oocyst polar granule and oocyst residuum 
are absent. A sporocyst residuum is 
present. The sporulation time is 2 days. 

Life Cycle : The life cycle of this 
species does not appear to have been 
worked out in detail. The life cycle des- 
cribed by Pellerdy (1953) for "E. piri- 
fovDiis" is actually that of E. intestinalis. 
The prepatent period is 9 days. 

Pathogenesis: Unknown. 



The sporozoites are elongate ovoid, with 
a Stieda body. The sporulation time is 2 
to 3 days. 

Life Cycle : The endogenous cycle of 
this species has not been described. 

Pathogenesis : This species is 
slightly to markedly pathogenic, depending 
upon the extent of the infection. The af- 
fected intestinal mucosa is inflamed and 
hyperemic, and caseous necrosis may be 
present. 

Remarks : Pelle'rdy (1954a) found a 
coccidium which he believed to be E. 
neoleporis in domestic rabbits in Hungary 
and described its pathogenic effects. He 
believed that E. coecicola was a synonym 
of this species and he may be right. 
Carvalho (1942) transmitted E. neoleporis 
from the cottontail to the domestic rabbit. 
However, for the present I am using the 
name E. neoleporis for the cottontail form 
alone. 



EIMERIA COECICOLA 
CHEISSIN, 1946 

Host: Domestic rabbit. 



EIMERIA NEOLEPORIS 
CARVALHO, 1942 

Hosts : Cottontail (Sylvilagus flori- 
danus), domestic rabbit (experimentally). 

Location : Posterior part of small 
intestine, large intestine. 

Geographic Distribution : North 
America. 

Prevalence : Common in cottontails. 
Ecke and Yeatter (1956) found this species 
in 31% of 32 cottontails in Illinois. 



Location : Posterior ileum, cecum. 

Geographic Distribution : Europe 
(Hungary), USSR. 

Prevalence : This species is appar- 
ently rare in captive domestic rabbits, but 
is common in wild ones. 

Morphology : The oocysts are ovoid, 
sometimes ellipsoidal, smooth, light yel- 
low, 25 to 40 by 15 to 21 |j, . A micropyle 
is present. An oocyst polar granule is 
absent. Oocyst and sporocyst residua are 
present. The sporulation time is 3 days. 



Morphology : The oocysts are sub- 
cylindrical or elongate ellipsoidal to ovoid, 
smooth, pinkish yellow, 33 to 44 by 16 to 
23 [I with a mean of 39 by 20 jix . A micro- 
pyle is present. An oocyst polar granule 
is absent. An oocyst residuum is usually 
absent. A sporocyst residuum is present. 



Life Cycle : Kheisin (1947) described 
the life cycle of this species. The schi- 
zonts are found in the epithelial cells of 
the villi of the posterior ileum, and the 
gametes and gametocytes are below the 
host cell nuclei of the crypt cells of the 
cecum. The prepatent period is 9 days, 



200 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



and 100,000 oocysts are produced per 
oocyst fed. 

Pathogenesis : According to Kheisin 
(1947), this species is slightly if at all 
pathogenic. He saw small white spots in 
the cecum which were groups of developing 
oocysts. 



EIMERIA ELONGATA 
MAROTEL AND GUILHON, 1941 

Synonym : Eimeria neoleporis 
Carvalho, 1942 (?). 

Host : Domestic rabbit. 

Location : Unknown, presumably in- 
testine. 

Geographic Distribution : Europe 
(France). 

Prevalence : Unknown. 

Morphology : The oocysts are slightly 
greyish, elongate ellipsoidal with almost 
straight sides, 35 to 40 by 17 to 20 fi . The 
oocyst wall is thin. The micropyle is 
broad and easily visible. An oocyst polar 
granule and oocyst residuum are absent. 
The sporocysts are elongate. A sporo- 
cyst residuum is present, and almost as 
long as the sporocysts. The sporulation 
time is 4 days. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : Becker (1956) believed 
that this species and E. neoleporis from 
the cottontail might be the same, and I 
agree. However, it is probably best to 
retain both names pending further research. 



EIMERIA INTESTINALIS 
KHEISIN, 1948 

Synonyms : Eimeria agnosia, 
Eimeria piri/or)nis Gwelessiany and 
Nadiradze, 1945; non E. piriformis Kotlan 
and Pospesch, 1934. 



Host: Domestic rabbit. 



Location: Small intestine except 



anterior duodenum. 

Geographic Distribution : 
(Hungary), USSR. 



Europe 



Prevalence : Relatively uncommon. 

Morphology : The oocysts are piri- 
form, smooth, yellowish, 21 to 36 by 15 
to 21/i. A micropyle is present. An 
oocyst polar granule is absent. An oocyst 
residuum is present. The sporulation 
time is 1 to 2 days. Kheisin (1958) made 
a cytochemical study of the oocysts and 
endogenous stages of this species. 

Life Cycle : Pelle'rdy (1953) des- 
cribed the life cycle of this species under 
the name E. piriformis. The endogenous 
stages occur above or sometimes beside 
the nuclei of the epithelial cells of the 
small intestine. There are at least 2 gen- 
erations of merozoites. The prepatent 
period is 9 days. 

Pathogenesis : According to Pellerdy 
(1953, 1954), experimental infections with 
this species cause more or less severe 
intestinal catarrh and diarrhea, and may 
kill young rabbits. At necropsy, edema 
and greyish-white foci which may coalesce 
to form a homogeneous, sticky, purulent 
layer may be found in the intestine. 



EIMERIA MATSUBAYASHII 
TSUNODA, 1952 

Host : Domestic rabbit. 

Location : Primarily ileum. 

Geographic Distribution : Japan. 

Prevalence : Unknown. 

Morphology : The oocysts are 
broadly ovoid, 22 to 29 by 16 to 22 ^l with 
a mean of 25 hy IS^i . A micropyle is 
present. An oocyst residuum is present. 
The presence or absence of an oocyst 
polar granule and a sporocyst residuum 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



201 



are unknown, 
to 2 days. 



The sporulation time is 1. 5 



Life Cycle : Unknown. 

Pathogenesis : According to Tsunoda 
(1952), this species may be slightly to 
moderately pathogenic, causing a diphther- 
itic enteritis. 



COCCIDIOSIS IN DOMESTIC RABBITS 

Epidemiology : The most important 
species of rabbit coccidium is Eimeria 
stiedae, which occurs in the liver. All 
the other species are found in the intestine. 
Of these, the most important are E. 
residua, E. magna, E. media a.nd E. per- 
f oralis. Kheisin (1957) has assembled in- 
formation on the localization of the intes- 
tinal species. 

Coccidiosis is primarily a disease of 
young rabbits; adults are carriers. Rab- 
bits become infected by ingesting oocysts 
along with their feed or water. The se- 
verity of the disease depends upon the 
number of oocysts they ingest and also 
upon the species involved. Mixed infec- 
tions are the rule, infections with a single 
species usually being seen only under 
laboratory conditions. Crowding and lack 
of sanitation greatly increase the disease 
hazard. 

Some of the coccidia of the domestic 
rabbit {Oryctolagus cnniculiis) also occur 
in cottontails {Sylvilagiis spp. ). Some 
have also been reported from jack rabbits 
and hares (Lepus spp. ). However, after 
reviewing the cross-transmission studies 
carried out to date, Pelle'rdy (1956a) con- 
cluded that, except for E. stiedae, none 
of the coccidia of jack rabbits and hares 
occur in domestic rabbits and cottontails, 
and none of the coccidia of the latter two 
genera occur in Lepus. If this conclusion 
is confirmed, the listing above of Lepus 
as a host of E. niagna, E. perforans, 
E. media and E. irresidua would be in- 
correct. Further cross-transmission 
experiments are needed to settle this 
matter. 



Diagnosis : Liver coccidiosis can be 
diagnosed by finding the characteristic 
lesions containing coccidia. Intestinal 
coccidiosis can be diagnosed by finding 
the coccidia on microscopic examination. 
However, the mere presence of these 
parasites in a case of enteritis does not 
mean that they caused it. Many rabbits 
carry a few coccidia without suffering any 
noticeable effects. In a 3-year study of 
mortality among hutch-raised domestic 
rabbits in California, Lund (1951) consid- 
ered coccidiosis to be the cause of enter- 
itis in only 80 out of 1541 affected animals. 

Treatment : Some of the sulfonamides 
have been found helpful in preventing coc- 
cidiosis if given continuously in the feed 
or drinking water. Succinylsulfathiazole, 
sulfamerazine or sulfamethazine mixed 
with the feed at the rate of 0.5% have been 
recommended (Horton-Smith, 1947; Ger- 
undo, 1948), as have been 0.02 to 0.05% 
sodium sulfaquinoxaline or sodium sulfa- 
merazine in the drinking water. Lund 
(1954) found that the administration of 
0. 03% sulfaquinoxaline in the feed con- 
trolled E. stiedae infections effectively if 
begun not more than 4 days after exper- 
imental infection. The drug was not com- 
pletely effective at this level, but it did 
give practical control. Lund stated further 
that this drug had not been found to harm 
rabbits when fed continuously. 

However, long-term, continuous feed- 
ing of such drugs is not particularly de- 
sirable, nor is it usually necessary. It 
has been the usual experience with poultry, 
and there is evidence that the same thing 
is true with rabbits (see Horton-Smith, 
1947), that if the hosts are exposed to 
coccidiosis during the drug-feeding period 
(as they usually are), an aborted infection 
occurs which is sufficient to induce immun- 
ity. The drug can then be safely stopped. 

Prevention : Coccidiosis can be pre- 
vented by proper management (see Lund, 
1949). Feeders and waterers should be 
designed so that they do not become con- 
taminated with droppings, and should be 
kept clean. Hutch floors should be self- 
cleaning or should be cleaned frequently 



202 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



and kept dry. Manure should be removed 
frequently. The animals should be han- 
dled as little as possible, and care should 
be taken not to contaminate either the 
animals themselves or their food, utensils 
or equipment. In addition, the rabbitry 
should be kept as free as possible of in- 
sects, rodents and other pests. 



EIMERIA TEN ELLA 
(RAILLIET AND LUCET, 1891) 
FANTHAM, 1909 

Synonyms : Eimeria avium, Coccid- 
ium teiiellion, Coccidiu»i globosum, 
Eimeria bracheti. 

Host : Chicken. 

Location: Ceca. 



Geographic Distribution : Worldwide. 

Prevalence : Very common. 

Morphology : The oocysts are broadly 
ovoid, smooth, 14 to 31 by 9 to 25 ^t with 
a mean of 22. 9 by 19. 1 p. . A micropyle is 
absent. An oocyst polar granule is pres- 
ent. An oocyst residuum is absent. The 
sporocysts are ovoid, without a sporocyst 
residuum. 



The sporulation time is 1 to 2 days. 
Edgar (1954) found that the minimum spor- 
ulation time is 18 hours at 29° C, 21 hours 
at 26. 5 to 28 and 24 hours at 20, 24 and 
32 . Maximum sporulation was reached 
in 22 to 24 hours at 29 , the optimum 
temperature. Some sporulation took place 
at 41 ° . When the oocysts were kept at 8° 
they failed to sporulate in 8 weeks and 
most were killed, so that only a few spor- 
ulated when they were subsequently held 
at 28°. 

Life Cycle : The life cycle of E. 
tenella has already been described as an 
example of coccidian life cycles (p. 160). 

Pathogenesis : This is the most 
pathogenic of the chicken coccidia and is 
responsible for heavy losses. Together 
with the other species, it was estimated 



by the USDA (1954) to cause an annual loss 
of $38, 229, 000 in the United States due to 
death and disease alone. To this should be 
added the cost of the medicated feeds which 
are generally fed to poultry, and various 
labor and other costs entailed by disease 
outbreaks. 

Cecal coccidiosis is found most fre- 
quently in young birds. Chicks are most 
susceptible at 4 weeks of age, while chicks 
1 to 2 weeks old are more resistant (Gardi- 
ner, 1955). However, day-old chicks can 
be infected (Gordeuk, Bressler & Glantz, 
1951). Older birds develop immunity as 
the result of exposure. 

Coccidiosis due to E. tenella may vary 
in severity from an inapparent infection to 
an acute, highly fatal disease, depending 
upon the infective dose of oocysts. The 
pathogenicity of different strains of E. 
tenella varies, and it is affected also by 
the breed and age of the chickens and their 
state of nutrition. Thus, Jankiewicz and 
Scofield (1934) found that less than 150 
sporulated oocysts produced no signs, 150 
to 500 oocysts produced slight hemorrhagic 
diarrhea, 1000 to 3000 oocysts produced 
moderate hemorrhage and a few deaths, 
3000 to 5000 oocysts produced marked 
hemorrhage and moderate mortality, and 
more than 5000 oocysts produced severe 
hemorrhage and high mortality. However, 
Horton-Smith(1949) found that infections 
with 15,000 oocysts caused no mortality 
in week-old birds, 30,000 oocysts caused 
32% mortality and 60, 000 oocysts caused 
45% mortality. Swales (1944) found that 
in 6-week-old chickens 15,000 oocysts 
caused 40% mortality, 30,000 oocysts 
caused 44%i moi'tality and 200, 000 oocysts 
caused 80% mortality, while in 4. 5-week- 
old chicks 120,000 oocysts caused 90% 
mortality and in 12-week-old chicks 
100,000 oocysts caused 50'( mortality. 
Waletzky and Hughes (1949) found that in 
one experiment 20.000 oocysts produced 
18-'; mortality and 100. 000 oocysts 36%. 
mortality in 4-weck-old chicks, while in 
other experiments 50, 000 oocysts produced 
45*'( mortality in 7-week-old chicks, 
100,000 oocysts produced 67'r mortality in 
4- to 5-week-old chicks and 500,000 
oocysts produced 48% mortality in 3- to 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



203 



6-week-old chicks. Gardiner (1955) found 
that 200, 000 oocysts were required to pro- 
duce mortality in 1- to 2-week-old chicks, 
while 50,000 to 100,000 oocysts produced 
mortality in older birds. 

Cecal coccidiosis is an acute disease 
characterized by diarrhea and massive 
cecal hemorrhage. The first signs appear 
when the second generation schizonts be- 
gin to enlarge and produce leakage of 
blood into the ceca. Blood first appears 
in the droppings 4 days after infection. 
At this time the birds appear listless. 
They may become droopy and inactive, 
and eat little, altho they still drink. The 
greatest amount of hemorrhage occurs on 
the 5th and 6th days after infection. It 
then declines, and oocysts appear in the 
feces 7 days after infection if the birds 
live that long. The oocysts increase to a 
peak on the 8th or 9th day and then drop 
off very rapidly. Very few are still being 
shed by the 11th day. A few oocysts may 
be found for several months. 

Coccidiosis is self-limiting, and if 
the birds survive to the 8th or 9th day 
after infection, they generally recover. 

The lesions of cecal coccidiosis de- 
pend upon the stage of the disease. They 
have been described by Tyzzer (1929), 
Tyzzer, Theiler and Jones (1932) and 
Mayhew (1937). On the fourth day after 
infection, hemorrhage is present thruout 
the cecal mucosa. On the fifth day, the 
cecum is filled with large amounts of un- 
clotted or only partly clotted blood. This 
increases on the sixth day. Cecal cores 
of fibrinous and necrotic material begin 
to form on the 7th day. They adhere 
tightly to the mucosa at first, but soon 
come loose and lie free in the lumen. 

About 7 days after infection, the wall 
of the cecum changes color from red to 
mottled reddish or milky white due to the 
formation of oocysts. It is greatly thick- 
ened. The cecal core, which was at first 
reddish, becomes yellowish or whitish. 
If it is small enough, it may be passed in- 
tact in the feces, but usually it is broken 
up into small pieces. In a few days the 
cecum becomes normal in appearance or 



at most slightly enlarged and thickened. 
Occasionally the cecum may rupture or 
adhesions may form. 

About the 4th day, when the second 
generation schizonts are developing, the 
lamina propria becomes infiltrated with 
eosinophiles, there is marked congestion, 
and the cecal wall is thickened. The 
epithelium may be torn and coccidia, blood 
and tissue cells may be released into the 
lumen in areas where there are large 
numbers of parasites. On the 5th day, 
when the second generation merozoites 
are released, their host cells are ruptured 
and there is extensive epithelial sloughing. 
The sloughed material and cecal contents 
consolidate to form the cecal core, which 
loosens from the wall as the epithelium is 
regenerated. 

Epithelial regeneration is complete in 
light infections, but in severe ones it may 
not be. There is a marked inflammatory 
reaction, with extensive lymphoid and 
plasma cell infiltration, and there may be 
some giant cells. Connective tissue is in- 
creased. The epithelium may not be re- 
placed between the glands, and cysts 
formed by constriction of the glands during 
the inflammatory stage may persist. 

The loss of blood into the ceca causes 
anemia. Using the microhematocrit tech- 
nic, Joyner and Davies (1960) found that 
the packed red cell volume decreased 
markedly beginning 5 days after experi- 
mental infection. From an original level 
of 26 to 29% it decreased to 18% and 14%, 
respectively, 7 days after infection with 
2000 and 10,000 oocysts. It had returned 
to normal 5 days later. 

Natt (1959) found that E. tenella 
causes marked changes in the leucocyte 
picture. He observed lymphopenia and 
heterophilia on the 5th day, and eosino- 
philia on the 10th day after infection. A 
marked leucocytosis began on the 7th day 
and persisted thru the recovery phase. 

Birds which recover from coccidiosis 
may suffer ill effects for some time or 
even permanently. Gardiner (1954) found 
an inverse correlation between growth 



204 



THE TELOSPORASIDA AND THE CCXTCIDIA PROPER 



rate and severity of cecal coccidiosis. 
Chicks which recovered following severe 
infection made much poorer weight gains 
than mildly affected ones. Mayhew(1932, 
1932a, 1934) found that it took 10 weeks 
to 6 months after recovery before in- 
fected birds regained the weight they had 
lost in comparison with uninfected con- 
trols. He found, too, that pullets which 
had been infected when 6 to 8 weeks old 
laid 19.25% fewer eggs than the controls. 
In addition, severely affected birds began 
to lay 6 to 7 weeks later than the controls. 
Davidson, Thompson and Morre (1936) 
compared a group of chickens which was 
passing oocysts with another group which 
was not. Over a period of 11 months, the 
positive group had a 12. 1% higher mor- 
tality, while the negative group averaged 
0. 44 pounds heavier than the positive one 
and had a 15.2% higher egg production. 
Bressler and Gordeuk (1951) found, in a 
flock of Single Comb White Leghorn chick- 
ens which had survived a mortality of 
8. 3% due to cecal coccidiosis, that weight 
gains were slightly less than in a "control" 
group fed 0.0125% sulfaquinoxaline con- 
tinuously which had not suffered an out- 
break of the disease, but that neither egg 
production nor hatchability were impaired. 



EIMERIA NECATRIX 
JOHNSON, 1930 

Host : Chicken. 

Location: The first and second gen- 
eration schizonts are found in the small 
intestine and the third generation schizonts, 
gametes and gametocytes in the ceca. 

Geographic Distribution : Worldwide. 

Prevalence : Common. 

Morphology : The oocysts are oblong 
ovoid, 12 to 29 by 11 to 24/1 with a mean 
of20byl7/i (Becker e/ aZ. , 1956). The 
oocyst wall is smooth and colorless, with- 
out a micropyle. An oocyst polar granule 
is present. An oocyst residuum is absent. 
The sporocysts are elongate ovoid, with 
a Stieda body. A sporocyst residuum is 
absent. The sporulation time is 2 days 



(18 hours at 29'' C according to Edgar, 
1955). 

Life Cycle : Chickens become in- 
fected by ingesting sporulated oocysts. 
When the sporozoites emerge. Van Door- 
ninck and Becker (1957) found that they 
first enter the epithelial cells of the villi 
in the small intestine, pass thru the 
epithelium into the lamina propria or core 
of the villus and migrate toward the mus- 
cularis mucosae. Most of them are en- 
gulfed by macrophages en route and are 
transported by them to the epithelial cells 
of the fundus. The macrophages invade 
these cells and appear to disintegrate 
during or after the invasion process, leav- 
ing the sporozoites unharmed. These then 
round up to form first generation schizonts. 

The remainder of the life cycle has 
been studied by Johnson (1930) and Tyz- 
zer, Theiler and Jones (1932). Both the 
first and second generation schizonts are 
found above the host cell nuclei in the 
epithelial cells of the gland fundi. The 
first generation merozoites are liberated 
2. 5 to 3 days after infection and enter ad- 
jacent epithelial cells. The second gen- 
eration schizonts are relatively large, 
measuring 39 to 66 by 33 to 54 fi with a 
mean of 52 by 38 /n . Most of the second 
generation merozoites are liberated 5 to 
8 days after infection, but a few may still 
be liberated as long as 23 days after in- 
fection. They measure 8 to 11 by 1. 5 to 
2. /J with a mean of 9 by 2 /ii . They pass 
to the cecum, where they penetrate the 
epithelial cells, coming to lie below the 
host cell nuclei, and turn into third gen- 
eration schizonts. Most of them are 
found in the surface epithelium, but some 
enter the glandular epithelium. Multiple 
infections of a cell with 3 or 4 schizonts 
may occur. These third generation schi- 
zonts are relatively small and contain only 
6 to 8 or a maximum of 16 third genera- 
tion merozoites. It is not certain whether 
there is more than one asexual generation 
in the cecum. 

The third generation and some of the 
second generation merozoites enter other 
cecal epithelial cells and become macro- 
gametes or microgametocytes. These 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



205 



also lie below the host cell nuclei. Micro- 
gametes develop from the microgameto- 
cytes, fertilization takes place, and 
oocysts form and are released. The pre- 
patent period is 7 days, and the patent 
period is about 12 days. 

Brackett and Bliznick (1952a) reported 
that the number of oocysts produced by E. 
necatrix per oocyst fed ranged from 1 5 in 
a group of chicks infected with 35,000 
oocysts each to 58,000 in another group in 
which the infective dose was 50 oocysts. 

Pathogenesis : Next to E. teiiella, 
this is the most pathogenic and important 
species of chicken coccidium. Indeed, 
with the decrease in importance of E. 
tenella due to the use of coccidiostatic 
drugs, E. necatrix has come to the fore 
in many areas as the cause of more losses 
than E. tenella. 

E. necatrix is often said to cause a 
more chronic type of coccidiosis than E. 
tenella. This is not because it runs a 
longer course, but because it produces so 
much scar tissue in the small intestine 
that its effects are more lasting. 

The pathogenesis of E. necatrix has 
been studied especially by Tyzzer, Theiler 
and Jones (1932). The principal lesions 
are in the small intestine, the middle 
third of which is most seriously affected. 
Small, white, opaque foci are found here 
by the fourth day after infection. They 
are composed of second generation schi- 
zonts developing deep in the mucosa. 
They are so deep that they can be seen 
thru the serosa but not from the mucosal 
surface of the intestine. They are seldom 
more than a millimeter in diameter, but 
may coalesce and thus appear larger. 
Severe hemorrhage may appear on the 
5th or 6th days. The small intestine may 
be markedly swollen and filled with clotted 
or unclotted blood. Its wall is greatly 
thickened, dull red, and many petechial 
hemorrhages appear in the white, opaque 
foci which by now contain second genera- 
tion merozoites. The gut wall may lose 
contractility, become friable and even 
appear gangrenous. The epithelium may 
slough, and by the end of the 6th day a 



network of fibrin containing mononuclear 
cells appears in the destroyed areas. 
This is later replaced by connective tissue, 
and permanent scarring results which in- 
terferes with intestinal absorption. 

There is less anemia than in E. 
tenella infections. Using the microhema- 
tocrit technic, Joyner and Davies (1960) 
found that the packed red cell volume de- 
creased from 28% to 23% seven days after 
experimental infection with 20, 000 oocysts, 
and to 25%) after infection with 10, 000 
oocysts, but that there was no significant 
decrease after infection with 1000 oocysts. 
The hematocrit levels had not returned to 
the original level 12 days after infection. 

The ceca are not seriously affected. 
They may be contracted and their contents 
may be dehydrated. 

Death usually occurs 5 to 7 days after 
infection. Many of the birds which recover 
remain unthrifty and emaciated. The 
after-effects of this type of coccidiosis are 
often so long- lasting that it is not worth- 
while to keep birds which have recovered 
from severe attacks. 

Brackett and Bliznick (1950, 1952) 
found that inoculation with 25,000 to 
50,000 oocysts (a relatively small number) 
caused a high degree of mortality in young 
chickens. Following inoculation with equal 
numbers of oocysts, young birds are more 
severely affected than older ones, but if 
the inocula are calculated on a weight basis, 
older birds may be more severely affected 
than younger ones. In 3-week-old chicks, 
25, 000 oocysts caused a mortality of 87%, 
while in 4-week-old chicks, 18,000, 37,000, 
75,000 and 150,000 oocysts caused mor- 
talities of 8, 75, 85 and 61%, respectively. 

EIMERIA BRUNETTI 
LEVINE, 1942 

Host : Chicken. 

Location : First generation schizonts 
occur thruout the small intestine. Second 
generation schizonts, gametes and gameto- 
cytes occur in the posterior small intes- 
tine, rectum, ceca and cloaca. 



206 



THE TEIOSPORASIDA AND THE COCCIDIA PROPER 



Geographic Distribution : North 
America. 



Prevalence : Uncommon. 

Morphology : P. P. Levine (1942) 
described this species, and Becker, Zim- 
mermann and Pattillo (1955) made a bio- 
metric study of its oocysts. The oocysts 
are ovoid, smooth, 14 to 34 by 12 to 26 /j. 
with a mean of 23 by 20 /i. A micropyle 
is absent. An oocyst polar granule is 
present. An oocyst residuum is absent. 
The sporocysts are elongate ovoid, about 
13 by 7. 5(1, with a Stieda body. A sporo- 
cyst residuum is present. The sporulation 
time is 1 to 2 days. Edgar (1955) found 
infective oocysts as early as 18 hours at 
24" C. 

Life Cycle : The life cycle of this 
species was described by Boles and 
Becker (1954). The sporozoites are liber- 
ated in the intestine and invade the epithel- 
ial cells of the villi. They round up to 
become first generation schizonts, which 
lie below the host cell nuclei on the sides 
of the villi of the upper, middle and lower 
small intestines. They are present 51 to 
76 hours after infection, measure 30 by 
20j^L, and contain approximately 200 first 
generation merozoites when mature. 
These invade other cells in the posterior 
small intestine, rectum, tubular part of 
the ceca and cloaca. They are found pri- 
marily at the tips of the villi, and usually 
lie below the host cell nuclei. They turn 
into second generation schizonts, which 
are present 4 days after infection. These 
average 30 by 16/i and contain 50 to 60 
merozoites. Small schizonts about 10 by 
9/j. were also seen on the 4th day, but 
their significance was not determined. 

The second generation merozoites in- 
vade fresh cells in the lower small intes- 
tine, ceca, rectum and cloaca and turn 
into sexual stages. These first appear on 
the 5th day and lie at the tips and sides of 
the villi, either above the host cell nuclei 
or on the basement membrane. The micro- 
gametocytes have a multicentric appear- 
ance, and are larger than the macroga- 
metes, which measure about 25 by 22|:i. 
The macrogametes contain eosinophilic 



plastic granules which later coalesce and 
form the oocyst wall. 

The prepatent period is 5 days. 

Brackett and Bliznick (1952) found 
that E. brunetti could produce a maximum 
of 400,000 oocysts per oocyst fed. This 
figure was obtained in 2- to 3-week-old 
chickens fed 50 oocysts each. With larger 
inocula, relatively fewer oocysts were ob- 
tained. With inocula of 250, 1250, 6250, 
20, 000 and 40, 000 oocysts, respectively, 
150,000, 26,000, 7000, 800 and 400 oocysts 
were produced per oocyst fed. 

Pathogenesis : E. briinelli is mark- 
edly pathogenic, but its effects depend upon 
the degree of infection. In light infections, 
no gross lesions may be seen. In heavier 
infections, Levine (1942) found that the gut 
wall becomes thickened and a pink or blood- 
tinged catarrhal exudate appears 4 or 5 
days after experimental infection: the drop- 
pings are quite fluid and contain blood- 
tinged mucus and many mucus casts. The 
birds become somewhat depressed. These 
signs continue for 5 days and then subside 
if the birds recover. 

In early or light infections, hemor- 
rhagic, ladder-like streaks are present on 
the mucosa of the lower intestine and rec- 
tum. In heavy infections, a characteristic 
necrotic enteritis appears. It may involve 
the entire intestinal tract, but is more often 
found in the lower small intestine, large 
intestine and tubular part of the ceca. A 
patchy or continuous, dry, caseous necrotic 
membrane may line the intestine, and the 
intestine may be filled with sloughed, ne- 
crotic material. Circumscribed white 
patches may be visible thru the serosa, 
and there may even be intestinal perfora- 
tion with resultant peritonitis. 

Boles and Becker (1954) did not ob- 
serve the extensive coagulation necrosis 
described by Levine (1942) in their experi- 
mentally infected chicks, but the other 
lesions were similar to those of his moder- 
ately infected birds. The birds became 
listless 82 hours after infection, and pe- 
techial hemorrhages were found, mostly 
in the lower small intestine but also in the 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



207 



middle and upper small intestine. These 
became more severe the next day but had 
disappeared from the upper and middle 
intestine. The lower small intestine and 
large intestine were hyperemic and hem- 
orrhagic, there was epithelial sloughing, 
and the intestinal contents were watery 
and blood-tinged. The tubular part of the 
ceca was involved, and the dilated portion 
was plugged with dehydrated material. The 
epithelial denudation was most probably 
caused by the asexual stages, and was 
most prominent on the 4th day. Signs of 
illness continued until the 6th day. 

Field outbreaks of the disease were 
studied by Levine (1943). The disease 
occurs most commonly in chicks 4 to 9 
weeks old. The mortality is high, and 
typical necrotic lesions are present. We 
have seen the same condition in field out- 
breaks in Illinois. 



EIMERIA ACERVULINA 
TYZZER. 1929 

Host : Chicken. 

Location : Anterior small intestine. 

Geographic Distribution : Worldwide. 

Prevalence : Common. 

Morphology : The oocysts are ovoid, 
smooth, 12 to 23 by 9 to 17 jii with a mean 
of 16 by 13 p.. A micropyle is absent. An 
oocyst polar granule is present. An 
oocyst residuum is absent. The sporocysts 
are ovoid, with a Stieda body but without a 
sporocyst residuum. The sporulation 
time is 1 day. Edgar (1955) found that the 
minimum sporulation time for this species 
at 28° C was 17 hours. 

Life Cycle : The life cycle of this 
species was described by Tyzzer (1929). 
The schizonts are found in the epithelial 
cells of the villi of the anterior small in- 
testine, where they lie above the host cell 
nuclei. The gland cells may also be in- 
vaded. Sometimes more than one parasite 
is found in a cell. The schizonts produce 
16 to 32 merozoites which measure about 



6 by O.SjLL. There are at least 2 and pos- 
sibly more asexual generations. Asexual 
reproduction lasts longer than in E. teiiella. 



The sexual stages occur above the 
host cell nuclei in the epithelial cells of 
the villi and to a lesser extent in the gland 
cells in the anterior small intestine. They 
first appear 4 days after infection. The 
microgametocytes are relatively small, 
measuring 11 by 9ju. 

The prepatent period is 4 days, and 
oocysts continue to be produced for rela- 
tively longer than with some other chicken 
coccidia. 

Brackett and Bliznick (1950) found 
that the maximum number of oocysts pro- 
duced per oocyst fed in their studies was 
72, 000. This occurred in a group of 3- 
week-old birds fed 2000 oocysts each. In 
another experiment in which similar birds 
were fed the same number of oocysts, 
only 35,000 oocysts were produced per 
oocyst fed. Oocyst production was lower 
with both larger and smaller inocula. 
Following inoculation with 200, 10,000 and 
20,000 oocysts, respectively, 9000,35,000 
and 7, 600 oocysts were produced per oocyst 
fed. 

Pathogenesis : E. acerindina is gen- 
erally considered only slightly pathogenic, 
but very large inocula may cause severe 
signs and even death. Generally, however, 
this species causes only a temporary set- 
back. Dickinson (1941) found that admin- 
istration of as many as 25 million oocysts 
to pullets produced only a temporary drop 
in weight and temporary cessation of egg 
production. Between 4 and 9 days after 
infection, the birds were droopy, ate rel- 
atively little and passed slimy, mucoid 
feces. Peterson (1949) reported losses 
from E. acerindina infection in the Pacific 
Northwest in older birds 3 to 4 weeks after 
they had been brought in off the range and 
placed in houses. The birds lost weight, 
egg production ceased, the combs shriveled 
and keratin pigment disappeared. There 
were few if any deaths. After about 6 
weeks the birds recovered and egg produc- 
tion returned to normal. 



208 



THE TELOSPORASIDA AND THE COCCIDLA PROPER 



Brackett and Bliznick (1950) found 
that inoculation with 500,000 oocysts re- 
duced weight gains of 2-week-old chicks. 
Moynihan (1950) obtained similar results. 
Becker (1959) found that 300,000 oocysts 
produced only loss of appetite for 2 or 3 
days and watery feces on the third day 
after infection in White Leghorn chicks. 
Morehouse and McGuire (1958) found that 
infection of chicks with 100, 000 oocysts 
retarded weight gains somewhat but did 
not affect the final weight. Larger inocula 
produced increasingly severe effects. 
Single and multiple doses of 5 million or 
more oocysts caused 6 to 75% mortality. 

The lesions produced by B.acervulina 
are not as marked as with E. necatrix. 
The intestine may be thickened and a 
catarrhal exudate may be present, but 
hemorrhage is rare. The maturing 
oocysts lie massed in limited areas, and 
form whitish or grey spots or streaks 
running transversely in the intestinal 
mucosa. In heavy infections the entire 
mucosa may be involved and may appear 
greyish, mottled and somewhat thickened. 
Morehouse and McGuire (1958) described 
a severe inflammatory reaction in chicks 
infected with 1 to 20 million oocysts. The 
intestine was edematous and thickened, 
with extensive vasodilation and marked 
reddening of the mucosa, and there was 
also degeneration or necrosis and slough- 
ing of the intestinal epithelium. 



EIMERIA MAXIMA 
TYZZER, 1929 

Host : Chicken. 

Location : Middle and posterior 
small intestine. 

Geographic Distribution : Worldwide. 

Prevalence : Common. 

Morphology : The oocysts are ovoid, 
smooth or somewhat roughened, yellowish, 
21 to 42 by 16 to 30 ji with a mean of 29 by 
23 fx. A micropyle is absent. An oocyst 
polar granule is present. An oocyst resi- 
duum is absent. The sporocysts are 



elongate ovoid, 15 to 19 by 8 to 9 /i , with 
a Stieda body. A sporocyst residuum is 
absent. The sporozoites are 19 by 4ji, 
with a conspicuous retractile globule 
(Long, 1959). The sporulation time is 2 
days. Edgar (1955) and Long (1959) found 
some infective oocysts as early as 30 
hours at 28' C. 

Life Cycle : The life cycle of this 
species has been studied by Tyzzer (1929), 
Scholtyseck (1959) and Long (1959), among 
others. The schizonts are found above the 
host cell nuclei or occasionally beside them 
in the epithelial cells of the tips of the villi 
of the duodenum and upper ileum. There 
are 2 generations of schizonts, both of 
which are relatively small, measuring 
about 10 by 8 p.; they produce only about 8 
to 16 merozoites each. Schizonts may be 
present thru the 5th day. The second gen- 
eration merozoites enter new epithelial 
cells, where they round up and enter the 
sexual phase of the life cycle. 

The sexual stages are found beneath 
the host cell nuclei. As they become 
larger, the host cells are displaced toward 
the center of the villus and come to lie in 
its interior. The mature microgametoc3^es 
measure 30 to 39 by 22 to 33 jj. and form a 
large number of biflagellate microgametes. 
The macrogametes are somewhat smaller, 
averaging 19 by 15fj, (Long, 1959). After 
fertilization, they lay down an oocyst wall, 
break out of the villus and are passed in 
the feces. The prepatent period is 5 to 6 
days, and the patent period is only a few 
days. 

Brackett and Bliznick (1950, 1952) 
reported that the maximum number of 
oocysts produced per oocyst fed in their 
experiments was 12,000. In a series of 
3-week-old chicks, they found that 11,500, 
2250 and 940 to 2900 oocysts were pro- 
duced per oocyst fed when the inoculating 
doses were 200, 2000 and 10,000 oocysts, 
respectively. 

Long (1959) found that the number of 
oocysts produced per oocyst fed varied 
with the age of the birds and the inoculum. 
With an inoculum of 10,000 oocysts it 
averaged 128, 33, 176, 448, 1049 and 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



209 



3294, respectively, in chicks 3, 7, 14, 
21, 28 and 42 days old, while with an in- 
oculum of 80,000 oocysts it was 9, 31 and 
169, respectively in chicks 7, 14 and 21 
days old. 

Pathogenesis : E. maxima is slightly 
to moderately pathogenic. Tyzzer (1929), 
Brackett and Bliznick (1950), Scholtyseck 
(1959) and Long (1959) studied its effects 
on chickens. The asexual stages cause 
relatively little damage, the most serious 
effects being due to the sexual stages. 
Brackett and Bliznick (1950) observed a 
mortality of 35% in one group of young 
chicks infected with 500,000 oocysts each, 
but there were no deaths in another group. 
The survivors lost some weight and then 
gained less than the controls for a time, 
but infection with 100, 000 oocysts had no 
significant effect on weight gains. Long 
(1959) observed no deaths in a group of 
6-week-old chicks infected with 500, 000 
oocysts each or in three 17-day-old chicks 
infected with 1 million oocysts each, altho 
diarrhea was present and the infected 
birds gained less than the controls. Im- 
munity is quickly produced. 

Berg, Hamilton and Bearse (1951) 
found that inoculation of White Leghorn 
laying pullets with 8000 oocysts each pro- 
duced a mild infection and temporary 
cessation of egg-laying. 

The principal lesions are hemorrhages 
in the small intestine. The intestinal 
muscles lose their tone, and the intestine 
becomes flaccid and dilated, with a some- 
what thickened wall. Short, fine, hair- 
like hemorrhages in the intestinal wall are 
sometimes present. There is a catarrhal 
enteritis and the intestinal contents are 
viscid and mucoid, greyish, brownish, 
orange or pinkish, occasionally but not 
usually with flecks of blood. 

Birds which recover soon return to 
normal. 



EIMERIA MITIS 
TYZZER, 1929 

Host: Chicken. 



Location : Anterior small intestine, 
occasionally middle and lower small intes- 
tine or even tubular part of ceca. 

Geographic Distribution : Worldwide. 

Prevalence : Common. 

Morphology : The oocysts are sub- 
spherical, smooth, colorless, 10 to 21 by 
9 to 18|u with a mean of 16 by 13 /i . A 
micropyle is absent. An oocyst polar 
granule is present. An oocyst residuum 
is absent. The sporocysts are ovoid, 10 
by 6(1, with a Stieda body, but without a 
sporocyst residuum. The sporulation time 
is 2 days. Edgar (1955) found some infec- 
tive oocysts as early as 18 hours at 29° C. 

Life Cycle : The life cycle of this 
species has been studied by Tyzzer (1929) 
and Joyner (1958), the latter using a strain 
derived from a single oocyst. The endo- 
genous stages occur in the epithelial cells 
of the villi and occasionally in the glands. 
They lie against the host cell nuclei, and 
below them more often than above accord- 
ing to Tyzzer. However, Joyner stated 
that the schizonts are nearly always super- 
ficial; he illustrated the sexual stages as 
below the host cell nuclei. The schizonts 
produce 6 to 24 or rarely 30 merozoites, 
but the number of schizont generations is 
not known. The merozoites are crescent- 
shaped, with blunt ends, and measure 
about 5 by 1 . 5 /i . 

The microgametocytes are about 9 to 
14 jj, long and the macrogametes are some- 
what larger. In contrast to most other 
coccidian species, in which development 
following a single inoculum is quite syn- 
chronous, both asexual and sexual stages 
occur together. The prepatent period is 
4 to 5 days, and the patent period 10 days 
(Joyner, 1958). 

Joyner (1958) found that chicks in- 
fected with 1000 oocysts produced 61, 709 
oocysts per oocyst fed, while chicks fed 
100,000 oocysts produced 2253 oocysts per 
oocyst fed. 

Pathogenesis : This species is 
slightly pathogenic, but is unlikely to be 



210 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



of pathological significance under normal 
field conditions. Tyzzer (1929) observed 
neither signs nor gross lesions in young 
chickens given tremendous and repeated 
doses of sporulated oocysts. Becker 
(1959) found neither lesions nor diarrhea 
in infected chickens. Joyner (1958) found 
that weight gains of 6- to 26-day-old birds 
fed 500,000 oocysts were reduced, while 
38% of 29 6-day-old chicks died after 
being fed 2. 5 million oocysts. 



praecox is probably no more pathogenic 
than E. mitis. 



EIMERIA HAGANI 
LEVINE, 1938 



Host: Chicken. 



Location: Anterior half of small in- 



testine. 



EIMERIA PRAECOX 
JOHNSON, 1930 

Host : Chicken. 

Location : Upper third of small in- 
testine. 

Geographic Distribution : Probably 
worldwide. 

Prevalence : Common. 

Morphology : The oocysts are ovoid, 
smooth, colorless, 20 to 25 by 16 to 20(1 
with a mean of 21 by 17 /i. A micropyle 
is absent. An oocyst polar granule is 
present. Oocyst and sporocyst residua 
are absent. The sporulation time is 2 
days. 

Life Cycle : Tyzzer, Theiler and 
Jones (1932) studied the life cycle of this 
species. The endogenous stages occur in 
the epithelial cells of the villi, usually 
along the sides of the villi and below the 
host cell nuclei. There are 2 generations 
of schizonts, the second of which appears 
as early as 32 hours after infection. 
Later development is irregular, both sex- 
ual and asexual stages being seen together. 
The prepatent period is 4 days, and the 
patent period is short, 4 days or a little 
more in the absence of reinfection. 

Pathogenesis : This species is essen- 
tially non- pathogenic. Tyzzer, Theiler 
and Jones (1932) were unable to cause 
death with heavy doses of oocysts, altho 
they did observe a mucous cast containing 
large numbers of oocysts at the end of the 
infection. Becker (1959) found that E. 



Geographic Distribution : 
America, India. 



North 



Prevalence : Rare. This species has 
apparently been reported in the United 
States only by P. P. Levine (1938) in New 
York and Edgar (1955) in Alabama. Gill 
(1954a) found it in 2. 5% of 120 chickens in 
India. 

Morphology : The oocysts are broadly 
ovoid, smooth, 16 to 21 by 14 to 19/i with 
a mean of 19 by 18 fj, (18 by 16. 5 jm accord- 
ing to Edgar, 1955). A micropyle is ap- 
parently absent. An oocyst polar granule 
is present. No other morphological data 
are known; this species was differentiated 
from other chicken coccidia by cross-im- 
munity tests. The sporulation time is 1 
to 2 days. Edgar (1955) found sporulated 
oocysts as early as 18 hours at 29" C. 

Life Cycle : Unknown. The prepatent 
period is 7 days according to Levine (1938) 
or almost 6 days according to Edgar (1955). 

Pathogenesis : This species is only 
slightly pathogenic. Levine (1938) ob- 
served pin-head size hemorrhages and 
catarrhal inflammation in the anterior 
half of the small intestine. There were 
also a few hemorrhages in the lower small 
intestine. Later, however, Levine (1942a) 
referred to this species as non- pathogenic, 
stating that 300, 000 oocysts had no effect 
on experimentally infected birds. 



COCCIDIOSIS IN CHICKENS 

Epidemiology : Infections with a 
single species of coccidium are rare, and 
mixed infections are the rule. Eimeria 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



211 




Fig. 27. Morphology and developmental stages of species of Eiiiici'ki from the chukcn. 
1-4. Stages in development of oocysts of Eiiiicyia IcnclUi. 5-7. Stages in 
development of oocysts of Eiiueria initio. 8-9. Stages in development of 
oocysts ol Eiuieria aceyvnlina. 10-13. Stages in development of oocysts of 
Eiiucria maxima. 14-17. Stages in development of oocysts of Eiiiicna 
iiccalyix. 18. Developmental stages in cecal epithelium 7 to 9 days after in- 
fection, oo = oocyst, sch = third generation schizont. nier = third generation 
nierozoite. mi = microgametocyte. ma = macrogamete. (From Tyzzer, 1929 
in the Aincyicaii Junyiial uj Hygiene, published by the Johns Hopkins Press). 



tenella is the most pathogenic and impor- 
tant species. In recent years, however, 
control of this species with coccidiostats 
has revealed more and more coccidiosis 
due to E. )iccalri.x. The other species 
may contribute to the total picture. E. 
brunelli is markedly pathogenic but un- 
common. E. niaxiiiia and E. acerviilina 
are slightly to moderately pathogenic. 
Both are conunon. E. )iiitis and E. 
praecox are common but non- pathogenic. 
E. hagani is rare and only slightly if at 
all pathogenic. Weiiyonella galliiiae is 
rare but moderately pathogenic; it has 



been found so far only in India. Crypto- 
sporidiiiiii tyzzeri is rare and non-patho- 
genic, laospora gallinae is rare if it is a 
chicken parasite at all, and is presumably 
non- pathogenic. 

Coccidiosis is primarily a disease of 
young birds. Older birds are carriers. 
Birds become infected by ingesting oocysts 
along with their food or water. Under 
farm conditions, and even in the laboratory 
unless extreme precautions are taken, it 
is practically impossible to avoid exposure 
to at least a few oocysts. 



212 



THE TELOSPORASIDA AND THE COCCIDL\ PROPER 



^ " 0* 



',9-rTTJ 





mmlff^mS^m 






iLiSjj-i 




3 







Fig. 28. Location of avian coccidia in intestinal epithelium of chicken. 1. Cryplo- 

sporidium tyzzeri. 2. Eimeria aceri'idina. 3. Eiineria iiiilis. 4. Eimeria 
maxima. 5. Eimeria tenella. (From Tyzzer, 1929 in the American Journal 
of Hygiene, published by the Johns Hopkins Press) 



The disease picture depends upon the 
number of oocysts of each species which 
the birds ingest. If they get only a few, 
there are no signs, and repeated infec- 
tions produce immunity without disease. 
If they get more, the disease may be mild 
and the birds will become immune. Only 
if they get a large number of oocysts do 
severe disease and death result. 

Crowding and lack of sanitation greatly 
increase the disease hazard. As the 
oocysts accumulate, the birds receive 
heavier and heavier exposures, and the 
disease becomes increasingly severe in 
each successive batch of birds placed in 
contaminated surroundings. 



Immunity: Coccidiosis is a self- 
limiting disease, and birds which have re- 
covered become immune. The speed with 
which immunity develops depends upon the 
species of Euneria and on the intensity and 
frequency of infection. Immunity develops 
rapidly following infections with E. »iax- 
ima, E. praecox and probably E. hagani, 
somewhat more slowly following infections 
■with E. tenella and E. briiiietli, and is de- 
layed following infections with E. mills, 
E. acervulina and£. necatrix. 

Immunity is species-specific. Chick- 
ens which have become immune to one 
species are susceptible to all the others. 
This fact makes it possible to differentiate 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



213 









Fig. 29. Location of chicken coccidia in regions of the intestinal tract. A. Eiiiivrui 
tenella. B. E. mitis. C. E. acervuliiia. D. E. niaxiiiia. E. E. i/ccalrix. 
F. E. brnnetti. (A-D after Tyzzer, 1929; E after Tyzzer, Theiler and Jones, 
1932; F after Boles and Becker, 1954) 



between species by cross-immunity stud- 
ies, and indeed it was by means of such 
studies that Levine (1938), for instance, 
was able to show that E. hagani was a 
valid species. 

Immunity against coccidia is seldom 
solid. Birds which have recovered may 
be reinfected, but such infections are 
light and do not cause disease. Carriers 
are extremely common and are a source 
of infection for other birds. Thus, Levine 
(1940) found E. mitis, E. acervnlina or 
both in 53%, E. praecox in 33%, E. max- 
ima in 28%, E. necatrix in 38% and£. 
tenella in 23% of 39 pullets 8 months or 
more old, but only 8% of them had gross 
lesions. 

Heredity is a factor in resistance to 
coccidiosis. Herrick (1934) found that 
chicks from resistant parents were about 
100% more resistant to E. tenella than 



unselected chicks. Champion (1954) and 
Rosenberg, Alicata and Palafox (1954) 
established E. teiiella-res\sia.nt and sus- 
ceptible lines of chickens by selective 
breeding. They found that sex linkage, 
passive transfer of immunity thru the egg 
and cytoplasmic inheritance did not play a 
significant part in resistance and suscep- 
tibility. Champion considered that they 
were controlled in large part by non-dom- 
inant, multiple genetic factors which pre- 
sumably act additively. Rosenberg et al. 
also thought that the factor or factors for 
resistance or susceptibility did not show 
marked dominance. 

Immunity in older birds is due mostly 
to previous infection. The birds are ex- 
posed repeatedly and almost continuously, 
and their immunity is continually being 
reinforced. Coccidiasis is thus extremely 
common- -and indeed normal under natural 
conditions- -while coccidiosis is the result 



214 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



of imbalance between infection rate and 
resistance. Actually, the best type of en- 
vironment to control coccidiosis is one in 
which the chickens become infected lightly 
enough to develop an immunity without 
suffering any disease. 

Many workers have studied the devel- 
opment of immunity to coccidiosis (Walet- 
zky and Hughes, 1949; Brackett and 
Bliznick, 1950). Most of this research 
has been done with E. lenella. Farr (1943) 
immunized chickens with 1000 oocysts 
daily for 15 days or with 3 doses of 1000, 
5000 and 9000 oocysts given 5 days apart. 
She also carried out 5 similar experiments 
with differing numbers of oocysts, all of 
which showed that repeated small doses of 
E. lenella oocysts would produce immun- 
ity. Horton-Smith (1949), Waletzky and 
Hughes (1949) and Gordeuk, Dressier and 
Glantz (1951) found that single doses of 
oocysts would also produce immunity, and 
that the degree of protection was propor- 
tional to the intensity of the initial infec- 
tion. Babcock and Dickinson (1954) found 
that a total of 1600 sporulated oocysts, 
given either in one or several doses, 
would produce practical immunity that 
withstood severe challenge. The number 
of individual doses required to make the 
total did not materially affect the immun- 
ity produced. It took 4 days longer for 
immunity to result following exposure to 
1050 sporulated oocysts than to 2125. 
Gordeuk, Bressler and Glantz (1951) found 
that day-old chicks could develop a certain 
degree of immunity. They found, too, that 
feeding the oocysts in the mash resulted 
in higher mortality than when a similar 
dose was given by mouth. 

Many workers have shown that immun- 
ity will develop against coccidiosis in birds 
on suppressive therapy (Waletzky and 
Hughes, 1949; Johnson, Mussell and Diet- 
zler, 1949, 1949a; Grumbles el at. , 
1949; Bankowski, 1950; Kendall and McCul- 
lough, 1952). The drugs are ineffective 
against the sporozoites or first generation 
schizonts, at least in the concentrations 
used, but they do kill the merozoites or 
later stages. The coccidia are thus able 
to invade the host tissues and stimulate 
the development of immunity, but are 



killed before they can multiply enough 
to harm the host. 

A number of workers have attempted 
to produce immunity by infecting birds 
with oocysts attenuated in different ways. 
Jankiewicz and Scofield (1934) heated the 
oocysts to 46" C for 15 minutes before 
sporulation, and found that when they were 
then sporulated and fed to chickens, they 
stimulated the production of immunity 
with a minimum of injury. Waxier (1941) 
produced mild infections with oocysts 
irradiated with 9000 r of x-rays. Follow- 
ing recovery, the chicks were almost as 
resistant as those which had had a severe 
attack after infection with normal oocysts. 
Uricchio (1953) produced marked immunity 
by feeding chicks 100, 000 oocysts which 
had been held at -5^ C for 5 days, and a 
lesser degree of immunity with oocysts 
which had been heated at 45'' C for 12 
hou rs . 

It is well known that cultures slowly 
lose their infectivity upon storage. Bab- 
cock and Dickinson (1954), for example, 
observed reduced pathogenicity in a culture 
of E. tenella after storage for 236 days, 
and reduced immunogenicity at 344 days. 
Using a standard immunizing procedure 
in which 600 oocysts were fed the first 
day and 1000 the second, they found that 
it took 3 days to produce immunity with a 
culture less than 150 days old and 6 days 
with a culture more than 300 days old. 

There is an unanswered question 
whether such treatments produce true at- 
tenuation or whether the observed results 
are due simply to the death of some of the 
oocysts. Invasion must take place for im- 
munity to result, and attempts to immu- 
nize birds with killed antigens have not 
succeeded. 

Most attempts to find circulating anti- 
bodies have failed. However, McDermott 
and Stauber (1954) found agglutinins 
against merozoites in the serum of exper- 
imentally infected chickens and also pro- 
duced them in rabbits and roosters by in- 
jecting formalinized merozoite suspensions. 
Becker and Zimmermann (1953) found that 
infected chicks injected intravenously with 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



215 



an alcoholic horse kidney extract produced 
fewer oocysts than untreated, infected 
controls. Burns and Challey (1959) found 
that when chicks which had been previously 
infected thru a fistula into a cecal pouch 
which had been isolated from the intestine 
were challenged with E. tenella orally, 
they were somewhat more resistant than 
the controls, indicating that there is some 
generalized host response. 

Less research has been done on the 
development of immunity in other species 
of coccidia. Tyzzer, Theiler and Jones 
(1932) found that chickens which had re- 
covered from E. necatrix infections were 
immune, as did Grumbles and Delaplane 
(1947). Dickinson (1941) and Brackett 
and Bliznick (1950) showed that immunity 
developed following infection with E. 
acervulina. The latter found the same 
thing with E. maxima. Similar results 
have been obtained for the other species 
(Brackett and Bliznick, 1950). 

Diagnosis : Avian coccidiosis can be 
diagnosed by finding lesions containing 
coccidia at necropsy. Diarrhea with or 
without blood in the droppings, inappetence 
and emaciation are suggestive, but scrap- 
ings of the affected intestinal mucosa must 
be examined microscopically to determine 
whether coccidia are present. It is not 
enough to look for oocysts, but schizonts, 
merozoites and young gametes should be 
recognized also. 

Coccidiasis is much more common 
than coccidiosis; hence the mere presence 
of oocysts in the feces cannot be relied 
upon for diagnosis. Conversely, the ab- 
sence of oocysts does not necessarily mean 
that coccidiosis is not present, since the 
disease may be in too early a stage to 
produce oocysts. 

Since some species of coccidia are 
highly pathogenic for the chicken while 
others are practically non-pathogenic, 
the species present must be identified to 
establish a diagnosis. This can often be 
done in a rough way from the type and lo- 
cation of the lesions. 

Treatment : Many hundreds of papers 
have been written on the treatment of coc- 



cidiosis in chickens, and there is no space 
here for more than a relatively brief dis- 
cussion. By far the greatest part of the 
research has been done on E. tenella. 

The first compound found effective 
against coccidia was sulfur, which Herrick 
and Holmes (1936) introduced. When 2 to 
5% sulfur is mixed with the feed, coccid- 
iosis is largely prevented in young chicks. 
The use of sulfur had a certain vogue, but 
it was soon found unsatisfactory because 
it causes a condition known as sulfur rick- 
ets. Even tho the chicks are on an ordin- 
arily adequate diet, the sulfur interferes 
with calcium utilization and causes rickets. 

The use of borax in E. tenella coccid- 
iosis was introduced by Hardcastle and 
Foster (1944). Several others have done 
research on it (Wehr, Farr and Gardiner, 
1949), and the consensus is that 0. 3 to 
0. 5% borax in the feed prevents death from 
coccidiosis if administered beginning 1 or 
2 days after experimental infection and 
continued for 3 days or longer. However, 
it does not prevent cecal hemorrhage or 
weight losses. It is also toxic, causing 
loss of weight even when fed alone. 

P. P. Levine (1939) was the first to 
use sulfonamides against coccidiosis. His 
discovery that sulfanilamide was active 
opened up the field. Many different-- 
probably several hundred--sulfonamides 
were tested, and a number of them were 
found of practical value. Sulfaguanidine 
was introduced after sulfanilamide. It 
was followed by sulfamerazine and sulfa- 
methazine (called sulfamezathine in Eng- 
land), and still later by sulfaquinoxaline 
and N'*-acetyl-N'-(4-nitrophenyl) sulfanil- 
amide. All of these compounds are effec- 
tive against E. tenella, the last 2 are 
quite effective against E. necatrix, and 
sulfaquinoxaline and sulfaguanidine are 
quite effective against E. acervulina. 
Sodium sulfadimidine is active against 
E. mitis, but does not completely elim- 
inate it (Joyner, 1958). 

Sulfaguanidine is fed at the rate of 
0. 5% in the mash, sulfamethazine and sul- 
famerazine at 0. 1 to 0.25%, and sulfaquin- 
oxaline at 0.025%. Sodium sulfamethazine 
and sodium sulfadimidine are given in the 



216 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



drinking water at 0. 2%, and sodium sulfa- 
quinoxaline at about 0.04% (see Grumbles, 
el al. , 1949; Farr, 1949; Dickinson, 1949; 
Kendall and McCuUough, 1952; Peterson 
and Munro, 1949; Peterson and Hymas, 
1950; Davies and Kendall, 1954; Bankow- 
ski, 1950; Horton-Smith and Long, 1959; 
and McLoughlin and Chester, 1959 for re- 
views and further information). 

The sulfonamides are in general more 
effective against the schizonts and mero- 
zoites than against the gametes, gameto- 
cytes and sporozoites. Bankowski (1950) 
found that 0. 5% sulfaguanidine was coccid- 
iostatic against the first generation schi- 
zonts of E. tenella but that 2% sulfaguan- 
idine was required to kill the second gen- 
eration schizonts in the lamina propria 
and even this concentration had no effect 
on the sporozoites. He concluded that 
this drug must act against the merozoites 
in the lumen of the ceca, since 0. 5% is 
the usual concentration in the feed. Ken- 
dall and McCullough (1952) found that 0. 25 
to 0. 375% sulfamethazine in the feed af- 
fected the later stages in the life cycle, 
but that 0. 5 to 1.0% was required to affect 
the early stages. Farr and Wehr (1947) 
found that 1% sulfamethazine almost com- 
pletely destroyed the second generation 
schizonts and their merozoites, somewhat 
affected the first generation schizonts but 
did not completely destroy them, and 
either damaged or destroyed the young 
gametes. It did not injure the larger gam- 
etes, oocysts or sporozoites. The action 
of sulfaquinoxaline is similar. 

All of the sulfonamides are coccidio- 
static rather than truly curative. None 
will cure coccidiosis once signs of dis- 
ease have appeared. When fed continu- 
ously in the feed, they abort the disease. 
Sulfaquinoxaline will protect birds when 
given as late as 4 days after experimental 
infection. Since the sporozoites are not 
affected, they invade the intestinal cells 
and stimulate the development of immun- 
ity. However, if too much of a sulfona- 
mide is given, immunity will not develop. 
Thus, Kendall and McCullough (1952) 
found that when 0. 25 to 0. 375% sulfameth- 
azine was given in the feed, immunity de- 
veloped, but when the concentration was 
raised to 0. 5 to 1. 0% it did not. 



When given in the recommended 
amounts, the sulfonamides are not gener- 
ally harmful. Sulfaquinoxaline does not 
depress the growth rate of chicks when fed 
for a long period at rates of 0.01 to 0.02%, 
but 0.03% gives variable results and higher 
concentrations are usually toxic. Dela- 
plane and Milliff (1948) found that when 
0. 05% sulfaquinoxaline was fed continu- 
ously to pullets in egg production, signs 
of poisoning appeared and some birds died. 
They found greyish-white nodules in the 
spleens of most birds and in the livers, 
kidneys, hearts and lungs of some. There 
were also hemorrhages beneath the skin of 
the legs and in the combs. Davies and 
Kendall (1953) found that 0.0645% sodium 
sulfaquinoxaline in the drinking water was 
toxic to chickens when fed for as short a 
period as 5 days. The principal lesions 
were hemorrhages, especially in the 
spleen, and accumulation of fluid in the 
peritoneal cavity. On the other hand, 
Cuckler and Ott (1955) reported that the 
continuous administration of 0. 05% sulfa- 
quinoxaline in the feed or of 0.025% in the 
water for as long as 12 weeks had no ad- 
verse effects on chickens. The blood 
clotting time was prolonged and the pro- 
thrombin time increased slightly by feeding 
0.4% sulfaquinoxaline for 3 to 12 weeks. 



Several organic arsenic compounds 
have been found effective against E. 
tenella, but not against the other species 
(Morehouse and Mayfield, 1946; Goble, 
1949). All are derivatives of phenylarsonic 
acid. All are coccidiostatic, and none will 
cure coccidiosis once signs of disease have 
appeared. The most widely used of these 
is perhaps 3-nitro-4-hydroxyphenylarsonic 
acid, which is generally administered in 



the feed at a concentration of 0. 01' 



It 



apparently acts against the earlier endog- 
enous stages, but not against the sporo- 
zoites, and birds which are exposed while 
under prophylactic treatment become im- 
mune. At the recommended dosage it has 
no harmful effect on the host but is actually 
a growth stimulant. A mixture of this 
compound and N^-acetyl-N'-(4-nitrophenyl) 
suKanilamide is sold under the name Ni- 
trosal to suppress both cecal and intestinal 
coccidiosis. Another active organic ar- 
senic compound is arsanilic acid. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



217 



A number of alkylidenediphenols, 
which are diphenylmethane derivatives, 
are effective against E. tenella, (Johnson, 
Mussell and Dietzler, 1949, 1949a; 
Groschke et al. , 1949). One of these, 
Parabis-90, is 2, 2'-methylene-bis-4- 
chlorophenol. It is used in the starter 
feed at a concentration of 0. 15%, and 
later on, when the chicks are 6 to 8 weeks 
old, in the grower feed at a concentration 
of 0. 12%. These compounds are also coc- 
cidiostatic and will not cure coccidiosis 
once signs of the disease have appeared. 
They appear to act primarily against the 
earlier endogenous stages but not against 
the sporozoites, and birds which are ex- 
posed while getting the drug become im- 
mune. They do not appear to harm 
chickens when fed at the recommended 
levels. 

A diphenyl disulfide derivative which 
has been widely used as a coccidiostat 
against both E. tenella and E. necatrix 
is nitrophenide (Megasul). It is 3, 3'-di- 
nitrodiphenyldisulfide (Waletzky, Hughes 
and Brandt, 1949; Peterson and Hymas, 
1950; Dickinson, Babcock and Osebold, 
1951; Gardiner, Farr and Wehr, 1952; 
Horton-Smith and Long, 1959). It is 
mixed with the feed at the rate of 0. 025 to 
0. 05%. It is coccidiostatic and will not 
cure coccidiosis once signs of the disease 
have appeared. It acts against both the 
sporozoites and later stages, but is more 
effective against the latter and especially 
against the second generation schizonts. 
Immunity does not appear to develop if 
chickens are treated before infection, but 
it does if treatment begins at the time of 
infection or later. Nitrophenide is not 
harmful if fed in therapeutic concentra- 
tions. At higher doses Newberne and 
McDougle (1956) found that it may cause 
postural and locomotor disturbances, 
lowered weight gains, liver degeneration 
and bone marrow changes. 

Another coccidiostat is the diphenyl- 
sulfide derivative, bithionol, or 2,2'- 
dihydroxy-3, 3', 5, 5'-tetrachlorodiphenyl 
sulfide. The commercial coccidiostat, 
Trithiadol, is a mixture of 5 parts bithi- 
onol and 1 part methiotriazamine. The 
latter is 4, 6-diamino-l-(4-methylmer- 



captophenyl)-!, 2-dihydro-2, 2-dimethyl- 
1, 3, 5-triazine. Bithionol is not only coc- 
cidiostatic but also antibacterial and anti- 
fungal. Methiotriazamine is coccidiostatic 
at high concentrations and is also an active 
antimalarial agent. In combination, these 
drugs are effective against coccidia at 
lower concentrations than when used alone. 
A mixture containing 60% active ingredients 
is fed in the feed at the rate of 2 pounds per 
ton. The recommended use level is 0.05% 
bithionol plus 0.01% methiotriazamine. It 
is effective against E. tenella, E. necatrix, 
E. maxima and E. acervulina. Chickens 
fed it develop immunity to these coccidia. 
McLoughlin and Chester (1959) found that 
0. 06% Trithiadol gave relatively good pro- 
tection from mortality due to E. tenella. 
It was not as good as glycarbylamide and 
nicarbazin but was about as effective as 
nitrofurazone and Bifuran and somewhat 
better than sulfaquinoxaline. Trithiadol 
is not harmful to growing chickens when 
fed at the recommended levels (Arnold 
and Coulston, 1959). It does not appear 
to affect egg production or egg shell color 
or quality, but it does affect hatchability 
to some extent and is not recommended 
for use in laying mashes. 

Two nitrofurans are currently used 
as coccidiostats. Nitrofurazone (5-nitro- 
2-furaldehyde semicarbazone) was intro- 
duced by Harwood and Stunz (1949, 1949a, 
1950) and has been studied further by 
Peterson and Hymas (1950), Gardiner and 
Farr (1954), Horton-Smith and Long (1952, 
1959) and McLoughlin and Chester (1959), 
among others. It is mixed with the feed 
at the rate of 0.011%. It is effective 
against E. tenella and to a lesser extent 
against E. necatrix and E. maxima. 
Higher concentrations give better results 
against the intestinal species. Nitrofur- 
azone is coccidiostatic and will not cure 
coccidiosis once signs of the disease have 
appeared. It acts against the schizonts, 
and birds infected while receiving the 
drug develop immunity to reinfection. 

Nitrofurazone is not harmful if fed in 
therapeutic amounts, but 0.04 to 0.05% in 
the feed is definitely toxic, and an adverse 
effect on the growth rate has been noted 
even at 0.022% (Gardiner and Farr, 1954; 



218 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



Peterson and Hymas, 1950). Newberne 
and McEuen (1957) found that 0. 05 to 0. 1% 
of nitrofurazone in the feed produced 
stunted growth, curled-toe paralysis, 
clinical polyneuritis, atrophy of the fol- 
licles of the bursa of Fabricius, renal 
tubular degeneration and pulmonary ossifi- 
cation in young chicks. The blood picture 
remained essentially normal. McLoughlin 
and Chester (1959) found that 0.0055'f 
nitrofurazone was less effective than gly- 
carbylamide or nicarbazin but more effec- 
tive than 0.0125"( sulfaquinoxaline against 
E. tenella. 

Another nitrofuran coccidiostat, Bi- 
furan, was introduced quite recently. It 
is a mixture of nitrofurazone and furazo- 
lidone (NF 180, or N-(5-nitro-2-furfury- 
lidene)-3-amino-2-oxazolidone). The 
final concentrations in the feed are 0.0055% 
nitrofurazone and 0.0008% furazolidone. 
McLoughlin and Chester (1959) found that 
it was less effective than glycarbylamide 
and nicarbazin, about as effective as nitro- 
furazone and more effective than sulfa- 
quinoxaline against E. tenella infections 
in chicks. Horton-Smith and Long (1959) 
found that it was effective against E. 
necatrix when fed at double the above level. 
Kantor and Levine (unpublished) found that 
furazolidone by itself was valueless against 
E. necatrix. 

Both nitrofurazone and furazolidone 
are also antibacterial agents. Furazoli- 
done is used against Salnionella infections 
in poultry, and also has some effect 
against Histomonas meleagridis (Harwood 
and Stun z, 1954) and T)'icho»ioiias gal- 
linae (Stabler, 1957). 

The anticoccidial properties of sub- 
stituted carbanilide complexes were dis- 
covered by Cuckler et at. (1955). They 
introduced nicarbazin, which is an equi- 
molar complex between 4, 4'-dinitrocar- 
banilide and 2-hydroxy-4, 6-dimethylpyri- 
midine. A simple mixture is no better 
than the carbanilide alone. Nicarbazin is 
fed at a concentration of 0.01 to 0.0125% 
in the feed, or 0. 008%) in replacement 
flocks. It is effective against E. tenella, 
E. acerviilina and E. necatrix (Cuckler, 
Malanga and Ott, 1956; Rubin et al. , 1956; 



Cuckler, Ott and Fogg, 1957; Horton-Smith 
and Long, 1959). McLoughlin and Chester 
(1959) found that nicarbazin was about as 
effective as glycarbylamide against E. 
tenella, and more effective than nitrofura- 
zone, Bifuran, sulfaquinoxaline or Trith- 
iadol. 

Nicarbazin is coccidiostatic, and will 
not cure coccidiosis once signs of the dis- 
ease have appeared. It acts against the 
second generation schizonts and their 
merozoites (Cuckler and Malanga, 1956), 
and birds which are infected while receiv- 
ing the drug develop immunity to reinfec- 
tion (Cuckler and Malanga, 1956; Marthe- 
dal and Veiling, 1957; McLoughlin, Rubin 
and Cordray, 1957, 1958). 

Nicarbazin is not recommended for 
laying hens. When fed at the recommended 
level, it makes the egg shells pale (Mc- 
Loughlin, Wehr and Rubin, 1957). At 
higher levels the yolks become mottled, 
blotchy, enlarged and sometimes even 
brown, the whites may become cloudy, 
hatchability is affected, and production 
may be reduced (Snyder, 1956; Sherwood, 
Milby and Higgins, 1956; Baker et al. , 
1956; Lucas, 1958). 

Other pyrimidine derivatives besides 
the one in nicarbazine may have a syner- 
gistic effect on sulfonamide coccidiostats. 
Lux (1954) found that pyrimethamine 
(Daraprim; 2, 4-diamino-5-p-chlorophenyl- 
6-ethyl pyrimidine), which is a powerful 
antimalarial drug, acted synergistically 
with sulfanilamide and other sulfonamides 
against E. tenella. Joyner and Kendall 
(1955) found that as little as 0.0025% pyri- 
methamine allowed the effective concen- 
tration of sulfamethazine against E. tenella 
to be reduced to 1 8 to 1 16 of that nor- 
mally required for protection. Marthedal 
and Veiling (1957) found that pyrimetha- 
mine acted synergistically with two other 
sulfonamides, sulfabenzpyrazine and sul- 
fadimidine, against E. tenella. 

Most recently, a quaternized deriva- 
tive of pyrimidine, amprolium, has been 
introduced. This compound is l-(2-«- 
propyl-4-amino-5-pyrimidinylmethyl)-2- 
methylpyridinium chloride hydrochloride. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



219 



According to Rogers eL al. (1960), 0.0125% 
amprolium in the feed is effective against 
E. tenella, E. necatrix and £. acervuliiia. 
It is a thiamine antagonist, and 0. 003% 
thiamine in the feed markedly decreased 
its activity against coccidia. Another 
name for amprolium is mepyrium, the 
discovery of which was announced by 
Aries (1960). 

According to Rogers et al. (1960), 
many other l-(2-alkyl-4-amino-5-pyri- 
midinylmethyl)-alkyl pyridinium salts have 
marked prophylactic activity in coccidiosis 
of poultry. Analogous 3-thiazolium com- 
pounds are also effective. 

The imidazole derivative, glycarbyla- 
mide (4, 5-imidazoledicarboxamide) was 
introduced as a coccidiostat by Cuckler 
et al. (1958). It is fed in a concentration 
of 0. 003% in the feed. It is effective 
against E. tenella, E. necatrix and E. 
acervulina, but Horton-Smith and Long 
(1959a) found that it is inferior to sulfa- 
quinoxaline against the last. McLoughlin 
and Chester (1959) found that it is about 
as effective as nicarbazin against E. 
tenella, and more effective than nitrofura- 
zone, Bifuran, sulfaquinoxaline or Trithi- 
adol. 

Glycarbylamide is coccidiostatic, and 
will not cure coccidiosis once signs of the 
disease have appeared. It acts against the 
stages prior to the second generation 
schizonts, and birds which are infected 
while receiving the drug develop immunity 
to reinfection. It is apparently non-toxic 
when fed at the recommended level. 

Several benzamide derivatives are 
effective coccidiostats. Morehouse and 
McGuire (1957, 1959) found that 3, 5-di- 
nitrobenzamide and several aliphatic N- 
substituted derivatives are effective 
against E. tenella and somewhat less ef- 
fective against E. necatrix. They found 
that Unistat, a "coccidiostatic growth 
stimulant" mixture containing 30% N"*- 
acetyl-N^-(4-nitrophenyl) sulfanilamide, 
25% 3, 5-dinitrobenzamide and 5% 3-nitro- 
4-hydroxyphenylarsonic acid in an inert 
carrier, when fed at a concentration of 
0. 1% in the feed, prevented death and 



permitted normal or near normal weight 
gains in chicks infected with potentially 
lethal doses of E. tenella, E. necatrix 
and E. acervulina. 

Another benzamide derivative is 
zoalene (3, 5-dinitro-o-toluamide). Hymas, 
Stevenson and Shaver (1960) reported that 
it prevents mortality and weight losses 
from infections with E. tenella, E. neca- 
trix, E. acervulina, E. maxima and E. 
brunetti when fed continuously in the 
ration of chicks at levels ranging from 
0.0025 to 0.015%. They recommended a 
level of 0. 0125% for broilers and lower 
levels for replacement pullets. This com- 
pound is most effective against E. necatrix. 

The benzamide derivatives are coc- 
cidiostatic and will not cure the disease 
once signs have appeared. Birds which 
are infected while receiving them develop 
immunity to reinfection. 

Hemorrhage is an important cause of 
death from cecal coccidiosis, and its con- 
trol will ameliorate the disease. Harms 
and Tugwell (1956) and Tugwell, Stephens 
and Harms (1957) found that the vitamin K 
activity of alfalfa meal or menadione so- 
dium bisulfite complex (Klotogen F) pre- 
vented deaths from cecal coccidiosis in 
birds on a basic vitamin K-deficient diet. 
Otto et al. (1958) confirmed their work, 
finding that 1.0 g of the water soluble 
menadione sodium bisulfite complex per 
ton of feed was just as effective as 3 g per 
ton of menadione. 

Sulfonamides and other coccidiostats 
have been mixed in poultry feed for so 
many years that it was inevitable that drug 
resistant strains of coccidia would develop. 
The first report of this was by Waletzky, 
Neal and Hable (1954), who found that a 
field strain of E. tenella from a Delaware 
broiler flock was more than 40 times as 
resistant to sulfaquinoxaline and 5 times 
as resistant to sulfamethazine as ordinary 
strains. It was unaffected by 1.0% sulfa- 
quinoxaline in the feed. Cuckler and 
Malanga (1955) studied 40 field strains of 
allegedly drug-resistant cecal or mixed 
intestinal and cecal coccidia from chick- 
ens. They found that 43% were resistant 



220 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



to nitrophenide, 45% to sulfaquinoxaline 
and 57% to nitrofurazone. Twenty-two 
percent were resistant to all 3 drugs, 18% 
to 2 and 18"f to 1. None were resistant 
to nicarbazin, which had only recently 
been placed on the market. They produced 
resistance against sulfaquinoxaline in 1 
strain of E. acerviilina and 2 strains of 
E. lenella by exposure to suboptimal dos- 
ages of the drug during 15 serial passages, 
but 1 strain of E. tenella was not rendered 
resistant to nitrophenide, nitrofurazone or 
nicarbazin by the same method for 15 ser- 
ial passages. 

Drug resistance is becoming increas- 
ingly common. It seems to develop with 
especial ease against glycarbylamide. As 
a consequence, we are in a race between 
the discovery of new coccidiostats and the 
development by the parasites of resistance 
against the older ones. In the long run, 
prevention of coccidiosis without reliance 
on drugs appears to hold more promise. 

Prevention and Control : Coccidian 
oocysts are extremely resistant to envir- 
onmental conditions. They may remain 
alive in the soil for a year or more (War- 
ner, 1933; Farr and Wehr, 1949; Koutz, 
1950). They will not sporulate in the ab- 
sence of oxygen, and they are killed in 
time by subfreezing temperatures. Thus, 
Edgar (1954) found that the oocysts of E. 
tenella vieve dead after 7 days at -12° C. 

Ordinary antiseptics and disinfectants 
are ineffective against them. Pe'rard 
(1924), for instance, found that the oocysts 
of rabbit coccidia would sporulate unharmed 
in 5% formalin, 5% phenol, 5% copper sul- 
fate, or 10% sulfuric acid. Horton-Smith, 
Taylor and Turtle (1940) confirmed this 
with E. tenella and added 5% potassium 
hydroxide and 5% potassium iodide to the 
list. Indeed, the standard storage solu- 
tions for coccidian oocysts are 2. 5% 
potassium bichromate or 1% chromic acid 
solution. 

The oocysts may be destroyed by 
ultra-violet light, heat, desiccation or 
bacterial action in the absence of oxygen. 
Long (1959) found that exposure to a tem- 
perature of 52° C for 15 minutes killed 



the oocysts of E. tenella and E. maxima. 
However, Horton-Smith and Taylor (1939) 
found that even a blowtorch did not kill all 
the oocysts on the floors of poultry houses 
unless it was applied long enough to make 
the wood start to char. The problem is 
to reach and maintain a lethal temperature 
at the spot where the oocysts are. 

While formaldehyde fumigation is in- 
effective against coccidia, Horton-Smith, 
Taylor and Turtle (1940) showed that am- 
monia fumigation is of practical value. 
E. tenella oocysts were killed by an 
0.0088% solution of ammonia in 24 hours, 
by an 0. 044% solution in 2 hours and by an 
0.088% solution in 45 minutes. They fu- 
migated poultry houses successfully with 
3 oz. ammonia gas per 10 cu. ft. For 
satisfactory results, the houses should be 
sealed so that the gas does not leak out. 

Boney (1948) found that methyl bro- 
mide is also an effective fumigant. It in- 
activated sporulated oocysts of E. tenella 
in the litter or soil when applied at the 
rate of approximately 1 lb. per 1000 square 
feet (0. 3 ml per sq. ft. ). It prevented in- 
fection in brooder houses using artificially 
contaminated cane pulp litter on wooden 
floors when used as a space fumigant at 
the rate of 2 lb. per 1000 cu. ft. 

Since it is practically impossible under 
farm conditions to prevent chickens from 
picking up at least a few oocysts, preven- 
tion of coccidiosis depends upon preventing 
a heavy enough infection to produce disease 
while at the same time permitting a symp- 
tomless infection (coccidiasis) to develop 
and to produce immunity. This can be 
accomplished by proper sanitation and 
management. Strict sanitation is effective 
alone, but it is usually supplemented by 
the use of a coccidiostatic drug. 

Young chickens should be raised apart 
from older birds, since the latter are a 
source of infection. If birds are raised on 
the floor, each new brood of chicks should 
be placed in a clean house containing clean, 
new litter. The litter should be kept dry, 
stirred frequently and removed when wet. 
The feeders and waterers should be washed 
in boiling water before use, and should be 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



221 



cleaned at least weekly with hot water and 
detergent. The waterers should be placed 
on wire platforms over floor drains, and 
the feeders should be raised high enough 
to prevent their being fouled. Enough 
feeders should be provided so that all the 
birds can feed at once without crowding. 

Chicks raised on wire have much less 
chance of contamination than those raised 
on the floor. However, the wire should be 
cleaned regularly. 

Flies, rats and mice around the poul- 
try houses and yards should be eliminated, 
since they may carry coccidia mechanic- 
ally. Damp areas around the poultry house 
should be filled in or drained. 

Feeding a coccidiostat during times 
when the birds are especially susceptible 
may also be helpful. The drug may be fed 
until the birds are 8 or 9 weeks old, after 
which they have ordinarily become im- 
mune. In addition, it is often recommended 
that a coccidiostat be fed to pullets for the 
first 2 or 3 weeks after they have been 
moved into laying houses. 

If an outbreak of coccidiosis occurs, 
all sick birds should be removed from the 
flock and placed in a separate pen. They 
should be given ample food and water, but 
it is useless to attempt to treat them. The 
remaining, apparently healthy birds should 
be treated with a coccidiostat in the dosage 
recommended by the manufacturer. Birds 
which become ill should be removed. The 
litter should be kept dry and stirred fre- 
quently. 

All dead birds should be burned. The 
litter should also be burned or put some- 
place where chickens will never have 
access to it. 

Care should be taken not to track coc- 
cidia from sick birds to healthy ones. 
Special rubbers or overshoes should be 
put on before entering pens containing sick 
birds, and should be cleaned thoroughly 
after each use. Veterinarians going from 
one farm to another should disinfect their 
boots before leaving each premises. 



The use of old, built-up, deep floor 
litter has been recommended by Kennard 
and Chamberlin (1949) and others to reduce 
losses from coccidiosis. By this method, 
the litter is not changed when new batches 
of birds are placed in a house, but some 
fresh litter may be added from time to 
time as needed to keep it in good condition. 
The litter is stirred every 2 or 3 days for 
the first 8 weeks and every day thereafter. 
Every 2 to 4 weeks, hydrated lime may be 
mixed in with the litter at the rate of 10 to 
15 lb. per 100 square feet of litter, but 
this is not necessary. The litter will keep 
dry for 8 to 16 weeks. Using this method, 
Kennard and Chamberlin (1949) observed a 
mortality of 7% as compared to a mortality 
of 19% in chickens kept on fresh litter re- 
moved and changed every 2 weeks. 

On the other hand, Koutz (1952, 1952a) 
found that many coccidian oocysts and 
nematode eggs remain alive in deep litter. 
Horton-Smith (1954), too, pointed out the 
dangers inherent in its use. He noted, 
however, that the ammonia produced would 
kill many oocysts. Long and Bingstead 
(1959) found that chicks on old, built-up 
litter did not gain as well as chicks on 
wire or new wood shavings, and that coc- 
cidia appeared in them earlier. Because 
of the dust, ammonia fumes, and danger 
of other diseases, the use of built-up litter 
in raising chickens is not recommended. 

Edgar (1955a) developed a coccidiosis 
"vaccine" which is said to be highly suc- 
cessful in immunizing chicks. It is a 
mixture of sporulated oocysts of E. tenella, 
E. necatrix, E. maxima, E. acervulina 
and E. hagani (Libby, Bickford and Glista, 
1959). It is recommended for use when 
the chicks are 3 to 5 days old. They are 
starved for about 3 hours and then given 
feed freshly mixed with the commercially 
prepared oocyst culture. The chicks are 
supposed to develop light infections and 
seed the litter with the oocysts which they 
produce. These oocysts produce reinfec- 
tions in turn. It is recommended that a 
coccidiostat be fed at a low level until 5 
weeks after vaccination, i.e., until the 
birds are 5^ to 6 weeks old. Under these 
conditions, the birds are said to become 



222 



THE TELOSPORASIDA AND THE COCCIDLA PROPER 



immune without suffering disease. While 
this system often works well, failures 
have been encountered too often to justify 
recommending its general use at present. 



EIMERIA MELEAGRIDIS 
TYZZER, 1927 

Hosts : Domestic and wild turkey. 

Altho Steward (1947) and Gill (1954) 
claimed to have transmitted this species 
experimentally to the chicken, Tyzzer 
(1929) was unable to transmit it to the 
chicken, ring-necked pheasant or bob- 
white quail, Hawkins (1952) was unable to 
transmit it to the bobwhite quail or Hun- 
garian partridge, and Moore, Brown and 
Carter (cited by Moore, 1954) and Clark- 
son (1959a) were unable to transmit it to 
the chicken. 

Location : The first generation schi- 
zonts, which are relatively few in number, 
are found only in the small intestine a 
short distance on either side of the yolk 
stalk. They lie below the host cell nuclei 
in the epithelial cells, mostly in those 
near the base of the villi but not in the 
deep glands. 

The second generation schizonts 
occur in the cecum, where they lie above 
the host cell nuclei in the epithelial cells 
of the tips of the villi. 

The sexual stages are found in the 
cecum, rectum and, to a slight extent, 
ileum. They lie above the host cell nuclei 
deep in the glands of the cecum as well as 
in the surface epithelium (Clarkson, 1959a). 

Geographic Distribution : Worldwide. 

Prevalence : Common. Kozicky 
(1948) found "E. meleagridis" in the drop- 
pings of 40% of 95 wild turkeys in Penn- 
sylvania. 

Morphology : This species was first 
described by Tyzzer (1927). The oocysts 
are ellipsoidal, smooth, 19 to 31 by 14 to 
23 ^x with a mean of 24 by 17 (i. The 
oocysts measured by Clarkson (1959a) 



were 22.3 + 2.3 by 16. 25 t 1.23fi. A 
micropyle is absent. One or 2 oocyst 
polar granules are present. An oocyst 
residuum is absent. The sporocysts are 
ovoid, with a Stieda body. A sporocyst 
residuum is present. The sporulation 
time is 1 day. Edgar (1955) found some 
sporulated oocysts as early as 15 hours 
at 28 C. 

Life Cycle : Hawkins (1952) and 
Clarkson (1959a) described the life cycle, 
the latter using a strain which he had de- 
rived from a single oocyst. The first 
generation schizonts are present 2 to 5 
days after infection, being found in great- 
est numbers at 60 hours. They measure 
20 by 15/1 and contain 50 to 100 mero- 
zoites measuring 7 by 1. 5(i. The second 
generation schizonts first appear 60 hours 
after infection, and mature ones are pres- 
ent after 70 hours; they are seen in great- 
est numbers at 84 hours. They are about 
9 (i in diameter and contain 8 to 16 mero- 
zoites which measure 10 by 2;i. Hawkins 
stated that there may be a third asexual 
generation, but that most of the second 
generation merozoites develop into sexual 
stages; Clarkson did not describe third 
generation schizonts. 

Macrogametes and microgametocytes 
appear at 91 hours and become mature 9 
days after infection. They measure about 
18 by 13jLt. The microgametes are bi- 
flagellate. 

According to Hawkins, oocysts appear 
in the feces 5 days after infection; Clarkson 
found that the prepatent period was 108 to 
112 hours. 



Pathogenesis : This species is prac- 
tically non-pathogenic. Hawkins (1952) 
observed only a slight drop in weight in 
poults experimentally infected with 
400,000 to 1 million sporulated oocysts. 
Moore and Brown (1951) infected poults 
with "enormous numbers" of fresh, spor- 
ulated oocysts without producing clinical 
evidence of coccidiosis. Clarkson (1959a) 
found that doses of up to 1 million oocysts 
produced no signs of disease in 2-week- 
old poults. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



223 



The serosal sui'face of the ceca of 
heavily infected birds is cream colored. 
The ceca contain a non-adherent, mucoid 
or caseous, yellow plug on the 5th and 
6th days. Caseous material composed of 
oocysts and epithelial cells is sometimes 
found in the feces on the 6th day, but the 
ceca appear quite normal in another day 
or two. Hawkins noted petechial hemor- 
rhages in the cecal mucosa. 

Immunity : Turkeys which have re- 
covered from an infection with E. mele- 
agyidis have a high degree of immunity 
according to Hawkins (1952). Clarkson 
(1959a) found no cross immunity between 
this species and E. adenoeides. 



EIMERIA MELEAGRIMITIS 
TYZZER, 1929 

Host: Turkey. 

Hawkins (1952) was unable to trans- 
mit this species to the bobwhite quail or 
Hungarian partridge. Gill (1954) claimed 
to have transmitted it to the chicken. 

Location : The asexual stages occur 
mainly in the upper jejunum, but a few 
are present in the duodenum and ileum as 
far as the yolk stalk. The first genera- 
tion schizonts lie below the host cell nuclei 
of the epithelial cells of the glands. The 
second generation schizonts develop in 
colonies in the epithelial cells of the deep 
glands but also spread up the sides of the 
villi. They usually lie just beneath the 
brush border of the cell but are some- 
times found below the host cell nucleus. 
The third generation schizonts are found 
in the epithelial cells of the villi but never 
in the glands. Most of them lie above the 
host cell nucleus, but some are below it. 

The sexual stages are found mainly 
in the epithelial cells at the tips of the 
villi but also spread down the sides. The 
great majority lie above the host cell 
nucleus (Clarkson, 1959). 

Geographic Distribution : Presumably 
worldwide. 



Prevalence : Quite common. Four 
out of 22 outbreaks studied by Clarkson 
and Gentles (1958) in Great Britain were 
due to this species, and 3 to a mixture of 
it and E. adenoeides. 

Morphology : The morphology of this 
species has been studied especially by 
Tyzzer (1929), Hawkins (1952) and Clark- 
son (1959). The oocysts are subspherical, 
smooth, 16 to 27 by 13 to 22 jj. with a mean 
of 19 by 16fi; 150 oocysts measured by 
Clarkson (1959) were 20. li 1.95 by 
17.3tl.7j:i. A micropyle is absent. One 
to 3 oocyst polar granules are present. 
An oocyst residuum is absent. The sporo- 
cysts are ovoid, with a Stieda body. A 
sporocyst residuum is present. The 
sporozoites have a colorless globule at the 
large end. The sporulation time is 2 days 
according to Hawkins (1952), 1 day at 26°C 
according to Clarkson (1959). 

Life Cycle : Tyzzer (1929), Hawkins 
(1952) and Clarkson (1959) studied the life 
cycle of this species, the last using a 
strain derived from a single oocyst. The 
account below is that of Clarkson, which 
is the most complete. The sporozoites 
invade the tips of the villi and migrate 
down the villi in the lamina propria until 
they reach the glands. Young first gener- 
ation schizonts can be found in the gland 
epithelial cells as early as 12 hours after 
infection, and many are mature by 48 
hours. They usually measure 17 by ISfj, 
and enlarge the host cell, pushing its 
nucleus into the gland lumen. They con- 
tain 80 to 100 merozoites which measure 
about 4. 5 by 1. 5jj, and have the nucleus 
at the larger end. 

The first generation schizonts rupture 
and release the merozoites, which invade 
the adjacent epithelial cells, forming col- 
onies of second generation schizonts. 
Most of these are mature by 66 hours 
after infection. They measure 8 by 7 |i 
and contain 8 to 16 merozoites which 
measure about 7 by 1. 5/i and have the 
nucleus near the center. 

Third generation schizonts may be 
recognized as early as 72 hours after 



224 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



infection and reach maturity at about 96 
hours. They measure about 8 by 7/i and 
differ from the second generation schi- 
zonts in having a residuum. They produce 
8 to 16 merozoites which measure about 
7 by 1. 5ju and have the nucleus much 
nearer the large end than do the second 
generation schizonts. 

Macrogametes and microgametocytes 
first appear 114 hours after infection. 
They measure about 15 by 11 /i, and the 
microgametocytes contain a rounded res- 
iduum. The microgametes have 2 long 
flagella. 

According to Hawkins (1952), the 
prepatent period is 6 days. Clarkson 
(1959) found that it ranged from 114 to 118 
hours with an average of 116 hours. 



The duodenal mucosa occasionally seems 
to have undergone coagulation necrosis, 
and pieces of caseous material may be 
scattered in the lumen of the entire intes- 
tine along with a large amount of fluid 
which may have a pinkish tinge. The re- 
mainder of the intestine is congested, and 
petechial hemorrhages may be present in 
the mucosa of most of the small intestine. 

Regeneration of the mucosa begins on 
the 6th or 7th day. A few petechiae are 
present in the duodenum and jejunum, and 
there are a few minute streaks of hemor- 
rhage and spotty congestion in the ileum. 
The posterior part of the jejunum and 
ileum may contain greenish, mucoid casts 
5 to 10 cm long and 3 to 6 mm in diameter, 
and necrotic material may be found in the 
ileum or feces. 



Pathogenesis : This species is mod- 
erately to markedly pathogenic, causing 
catarrhal enteritis. The death rate is 
high in young poults up to 6 weeks of age, 
but older birds are more resistant. Haw- 
kins (1952) found that infection with 
50,000 sporulated oocysts produced a high 
mortality in young poults, in some in- 
stances killing 100% of 2- to 3- week-old 
poults. Clarkson and Gentles (1958) and 
Clarkson (1959) observed mortalities of 
62%, 36% and 0%, respectively, in poults 
1. 5, 3 and 4 weeks old fed 100, 000 oocysts; 
of 40% and 100%, respectively, in 4-week- 
old poults fed 300, 000 and 400, 000 oocysts; 
and of 0% in 5- and 10-week-old poults fed 
200, 000 and 2 million oocysts, respec- 
tively. Food utilization is reduced in in- 
fected birds, and those which recover do 
not gain weight well for some time. 

Lesions first appear at the end of the 
4th day after infection (Hawkins, 1952; 
Clarkson and Gentles, 1958; Clarkson, 
1959). The jejunum is slightly thickened, 
dilated, and contains an excessive amount 
of clear, colorless fluid or mucus contain- 
ing merozoites and small amounts of blood 
and other cells. Five to 6 days after infec- 
tion the duodenum is enlarged, its blood 
vessels are engorged, and it contains a 
reddish brown, necrotic core which ad- 
heres firmly to the mucosa and extends a 
little way into the upper small intestine. 



Feed consumption begins to drop 2 to 
3 days after infection, and 4 days after 
infection the birds huddle together with 
closed eyes, drooping wings and ruffled 
feathers. Their droppings at this time 
are scanty and slightly fluid. At the peak 
of the disease, 5 to 6 days after infection, 
some of the feces form cylinders 1 to 2 
cm long and 3 to 6 mm in diameter. The 
droppings are not bloody, altho a few flecks 
of blood may occasionally be seen. Death 
usually occurs 5 to 7 days after infection. 

The first reaction of the host is local 
infiltration of the whole intestine with 
eosinophiles (Clarkson, 1959). This begins 
within 2 hours after infection, reaches a 
maximum in 1 to 2 days, and persists at 
least 10 days. There are no striking ab- 
normalities at 4 days, but at 5 days many 
of the infected villi appear to have lost 
their tips, all the duodenal blood vessels 
are congested, and many of the epithelial 
cells around the villi stain poorly and ap- 
pear necrotic. These changes are present 
also in birds which die on the 6th or 7th 
days, but resolution is rapid in recovered 
birds, and Clarkson (1959) saw very little 
abnormality by the 8th day except for in- 
creased cellularity of the lamina propria. 

Immunity : According to Hawkins 
(1952), the immunity produced by infections 
with this species is not as solid as that 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



22S 



produced by E. meleagridis , E. dispersa 
and E. gallopavonis , but it is still con- 
siderable. 



EIMERIA DISPERSA 
TYZZER, 1929 

Hosts : Turkey, bobwhite quail, ring- 
necked pheasant, ruffed grouse (?), sharp- 
tailed grouse (?). 

This species was first described by 
Tyzzer (1929) from the bobwhite quail. 
He also found it in the ring-necked pheas- 
ant. Hawkins (1952) first found it in the 
turkey. Boughton (1937) reported it from 
the ruffed grouse (Eonasa umbellus ) and 
sharp-tailed grouse (Pedioecetes pha- 
sianelhis campestris). Tyzzer (1929) 
transmitted it from the bobwhite to the 
turkey, chicken (producing a light infec- 
tion) and possibly to the pheasant. Venard 
(1933) and Patterson (1933) were unable 
to infect chickens with strains from the 
bobwhite. Tyzzer (1929) transmitted it 
from the pheasant to the bobwhite. Haw- 
kins (1952) infected the bobwhite and 
Hungarian partridge [Perdix perdix) with 
E. dispersa from the turkey, but was un- 
able to infect the pheasant or chicken. 
Moore and Brown (1952) infected the bob- 
white with a turkey strain, but, according 
to Moore (1954), were unable to infect the 
pheasant. 

Location : Primarily duodenum, but 
also small intestine. 



Geographic Distribution : 
America. 



North 



Prevalence : Presumably relatively 
uncommon. 

Morphology : The morphology of this 
species was studied especially by Tyzzer 
(1929) and Hawkins (1952). The oocysts 
are broadly ovoid, smooth, 22 to 31 by 18 
to 24 /J, with a mean of 26 by 21 /i . The 
oocyst wall is composed of a single layer 
and lacks a micropyle. An oocyst polar 
granule and oocyst residuum are absent. 
The sporocysts are ovoid, with a Stieda 
body. The sporulation time is 2 days. 



Life Cycle : Tyzzer (1929) and Haw- 
kins (1952) studied the endogenous stages 
of this species. They are found above the 
nuclei of the epithelial cells near the tips 
of the villi. There are apparently two 
types of first generation schizonts. Much 
the commoner is a small type about 6 ji in 
diameter which produces 15 or fewer 
merozoites each 4 to 6jj, long and Ijj, wide. 
The other type measures up to 24 by 18 /j. 
and produces at least 50 merozoites. The 
first generation merozoites are formed by 
the end of the second day of infection. 

The second generation schizonts are 
about 11 to 13/j. in diameter and produce 
18 to 23 merozoites each 5 to 6(i long and 
1. 5 to 2jLL wide about 4 days after infection. 

There are a few third generation schi- 
zonts and merozoites, but most of the sec- 
ond generation merozoites develop into 
sexual stages. The macrogametes are 18 
to 20 ji in diameter when mature, and the 
microgametocytes are slightly smaller. 
The microgametes have 2 flagella. Oocysts 
first appear in the feces late on the fifth or 
on the sixth day after infection. 

Pathogenesis : This species is only 
slightly pathogenic in the turkey. Hawkins 
(1952) found the most severe lesions on the 
fifth and sixth days after experimental in- 
fection. The entire small intestine was 
markedly dilated and the duodenum and 
anterior jejunum were creamy white when 
seen thru the serosal surface. The anter- 
ior half of the small intestine was filled 
with creamy, yellowish, sticky, mucoid 
material. The wall of the anterior intes- 
tine was edematous, but there was little 
epithelial sloughing. The intestinal tract 
was virtually normal by the eighth day 
after infection. 

The only signs Hawkins saw in infected 
turkeys were a slight tendency to produce 
somewhat liquid feces and a slight depres- 
sion in weight gains. 

Immunity; According to Hawkins 
(1952), turkeys which have recovered 
from infection are strongly immune to re- 
infection. 



226 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



EIMERIA GALLOPAVONIS 
HAWKINS, 1952 

Host : Turkey. 

Hawkins (1952) transmitted this spe- 
cies experimentally to the Hungarian 
partridge but not to the pheasant or bob- 
white quail. Gill (1954) claimed to have 
transmitted it from the turkey to the 
chicken. 

Location : Ileum, rectum and, to a 
lesser extent, ceca. 

Geographic Distribution : North 
America, India. 

Prevalence : Uncommon. 

Morphology : This species was des- 
cribed by Hawkins (1952, 1952a), who re- 
marked that its oocysts cannot be differ- 
entiated with any certainty from those of 
E. meleagridis. The oocysts are ellip- 
soidal, smooth, 22 to 33 by 15 to 19 /i 
with a mean of 27 by 17 p., without a 
micropyle. An oocyst polar granule is 
present. There is no oocyst residuum. 
The sporocysts are ovoid, with a Stieda 
body. A sporocyst residuum is present. 
The sporulation time is 1 day. 

Life Cycle : Hawkins (1952) des- 
cribed the life cycle of this species. The 
endogenous stages are found in the epithel- 
ial cells at the tips of the villi, where they 
lie mostly above the host cell nuclei. The 
first generation schizonts occur in the 
ileum and rectum. They produce approx- 
imately 8 merozoites and a residual mass 
3 days after infection. There are appar- 
ently two sizes of second generation schi- 
zonts. The smaller ones occur in the 
rectum, ileum and rarely in the ceca. 
They produce 10 to 12 merozoites and a 
residual mass 4 to 5 days after infection. 
The larger second generation schizonts 
occur only in the rectum. They are 20 ji 
in diameter and produce a large, unde- 
termined number of merozoites 4 days 
after infection. 

There are a few third generation 
schizonts and merozoites in the rectum. 



They produce about 10 to 12 merozoites. 
These and most of the second generation 
merozoites develop into sexual stages. 
These are found primarily in the rectum 
and only occasionally in the ileum and ceca. 
The macrogametes and microgametocytes 
are similar to those of other turkey proto- 
zoa. Some oocysts are passed in the feces 
on the sixth day after infection, but most 
appear on the seventh day. 

Pathogenesis : Little is known of the 
pathogenicity of this species. Hawkins 
(1952) noted marked edema, sloughing and 
lymphocytic infiltration in the intestines, 
but did not have sufficient material to 
make a thoro study. 

Immunity : According to Hawkins 
(1952), infection with E. gallopaionis pro- 
duces a more solid immunity than that 
elicited by £. meleagridis, E. meleagri- 
milis or E. dispersa. 



EIMERIA ADENOEIDES 
MOORE AND BROWN, 1951 

Host: Turkey. 

Moore and Brown (1951) were unable 
to transmit this species to the chicken, 
guinea fowl, ringnecked pheasant or bob- 
white quail. Clarkson (1959a) was unable 
to transmit it to the chicken. 

Location : The first generation schi- 
zonts (Clarkson, 1958) occur in the neck 
of the ceca and in the terminal inch or so 
of the ileum, where 80% of them lie below 
the host cell nuclei of the epithelial cells. 
The second generation schizonts occur 
thruout the ceca, and some are found in the 
rectum and posterior ileum. They lie above 
the host cell nuclei of the epithelial cells, 
just beneath the brush border. The sexual 
stages occur thruout the ceca, rectum and 
posterior third of the small intestine. A 
few are found even more anteriorly, but 
none more than halfway to the yolk sac 
stalk. They invade the epithelial cells of 
the crypts and deep glands, a location which 
distinguishes them from E. meleagridis 
and E. gallopavonis, and also apparently 
the epithelial cells of the villi. Clarkson 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



227 



(1958) illustrated them as lying above the 
host cell nuclei. 



Geographic Disti'ibution : 
America, Great Britain. 



North 



Prevalence : Quite common. Fifteen 
out of 22 outbreaks studied by Clarkson 
and Gentles (1958) in Great Britain were 
caused by this species and 3 by a mixture 
of it and E. iiieleagriniitis. 

Morphology : The oocysts have been 
described by Moore and Brown (1951) and 
Clarkson (1958). They are similar to 
those of E. ))ieleagridis and E. gallopa- 
vonis. They are ellipsoidal, sometimes 
ovoid, smooth, 19 to 31 by 13 to 21 fi with 
a mean of 26 by 17 /i. A micropyle is 
sometimes present. One to 3 oocyst polar 
granules are present. An oocyst residuum 
is absent. The sporocysts are elongate 
ovoid, apparently with a Stieda body. A 
sporocyst residuum is present. The sporo- 
zoites contain a clear globule at the large 
end. The sporulation time is 1 day. Edgar 
(1955) found sporulated oocysts as early as 
18 hours at 29° C. 

Life Cycle : Clarkson (1958) studied 
the life cycle of this species, using a 
strain derived from a single oocyst. First 
generation schizonts can be found in the 
epithelial cells as early as 6 hours after 
infection. They become mature 60 hours 
after infection; by 66 hours most of them 
have released their merozoites, altho a 
few remain up to 84 hours. The mature 
first generation schizonts measure 30 by 
18 |i and contain about 700 merozoites 
measuring 4. 5 to 7 by 1 . 5 fi , with a central 
nucleus. 

The second generation schizonts be- 
come mature 96 to 108 hours after infec- 
tion. They measure 10 by lOjj and contain 
12 to 24 merozoites measuring about 10 by 
3|j., with the nucleus a little nearer the 
rounded than the pointed end. 

Sexual stages can be found as early as 
114 hours and recognized as early as 120 
hours after infection. The mature macro- 
gametes measure about 20 by 18 /i and con- 
tain many large, plastic granules which 



f.tain black with Heidenhain's hematoxylin. 
The mature microgametocytes are about 
the same size as the macrogametes. 

The prepatent period was given by 
Moore and Brown (1951) as 112 hours. 
Edgar (1955) found oocysts in the feces as 
early as 104 hours, and Clarkson (1958) 
found that the prepatent period varied from 
114 to 132 hours in 30 birds. 

The patent period is 7 to 8 days accord- 
ing to Moore and Brown (1951). Clarkson 
(1958) found that very few oocysts were 
passed more than 14 days after infection, 
and none after the 20th day. 

Pathogenesis : This species is highly 
pathogenic. Moore and Brown (1951) were 
able to kill 100% of experimental poults up 
to 5 weeks of age with large doses of spor- 
ulated oocysts. Older poults developed a 
severe enteritis with few or no deaths. 
Clarkson (1958) and Clarkson and Gentles 
(1958) observed mortalities of 0%, 0%, 
45% and 100%, respectively, in 3-week-old 
poults fed 10,000, 25,000, 100, 000 and 
200,000 oocysts; of 33% in 6-week-old 
poults fed 1 million oocysts; and of 0% in 
11 -week-old poults fed 3 million oocysts. 
Birds which did not die had decreased food 
consumption and weight gains. 

Poults develop signs of anorexia, 
droopiness and ruffled feathers during the 
4th day after experimental infection. If 
death occurs, it is usually on the 5th or 
6th days but may be a little later (Moore 
and Brown, 1951). 

The gross lesions have been studied 
by Moore and Brown (1951), Clarkson 
(1958) and Clarkson and Gentles (1958). 
The intestines appear quite normal until 
the 4th day. The walls of the lower third 
of the small intestine, ceca and rectum 
become swollen and edematous, petechial 
hemorrhages which are visible from the 
mucosal but not from the serosal surface 
appear, and the lower intestine becomes 
filled with mucus. 

During the 5th day, most of the ter- 
minal intestine is congested and contains 
large numbers of merozoites and long 



228 



THE TELOSPORASIDA AND THE CCXCIDIA PROPER 



streaks of blood. By the end of the day, 
the intestine contains caseous material 
composed of cellular debris, gametes, 
and a few immature oocysts. A little later 
the caseous exudate is composed largely 
of oocysts. The feces in severe cases are 
relatively fluid and may be blood-tinged 
and contain mucous casts 1 to 2 inches long. 
Caseous plugs are sometimes present in 
the ceca. 



Since E. adenoeides is found in the same 
locations as E. meleagridia and E. gal- 
lopavonis, and since its oocysts are ap- 
parently similar to theirs, this lack of 
reciprocal immunity is an important dif- 
ferentiating criterion. The only other dif- 
ferences are its greater pathogenicity ancj 
its location in the crypts and deep glands 
rather than only in the tips of the villi. 



On the 6th to 8th days in birds infected 
with 10,000 oocysts, the terminal intestine 
contains white, creamy mucus, and pete- 
chiae are present in the mucosa. By the 
9th day the intestinal contents appear nor- 
mal, altho they still contain large numbers 
of oocysts (Clarkson, 1958). 

Infiltration with eosinophiles commen- 
ces as early as 2 hours after infection, 
and enormous numbers of eosinophiles 
may be found in the terminal small intes- 
tine, ceca and rectum from the 3rd to the 
10th days. 

Beginning 4 days after infection, ed- 
ematous changes are seen in the intestine, 
and infected epithelial cells begin to break 
off, leaving the villi denuded. The blood 
vessels become engorged, and cellular 
infiltration of the submucosa and epithel- 
ial denudation increase progressively until 
the 6th day. In birds which recover from 
the disease or which have received rela- 
tively few oocysts, resolution is very 
rapid. Vascularity is greatly reduced, 
the deep glands are almost free of para- 
sites by the 7th day, and the intestine is 
almost normal by the 9th or 10th day 
(Clarkson, 1958). 

Clarkson (1958) found no changes in 
the blood picture of infected poults. 

Immunity : Moore and Brown (1951) 
produced solid immunity to E. adenoeides 
by infecting turkey poults with 25 doses of 
sporulated oocysts over a period of 2 
months. These birds were not immune to 
E. meleagridis . Conversely, poults which 
had been immunized against E. meleagridis 
were not immune to E. adenoeides. Clark- 
son (1959a), too, found no cross immunity 
between E. meleagridis and E. adenoeides . 



EIMERIA INNOCUA 
MOORE AND BROWN, 1952 

Host : Turkey. 

Moore and Brown (1952) were unable 
to infect the chicken, guinea fowl, ring- 
necked pheasant and bobwhite quail with 
E. innocua. 

Location: Thruout the small intestine. 



Geographic Distribution : 
America (New York). 



North 



Prevalence : Apparently uncommon. 

Morphology : The oocysts of this 
species were described by Moore and 
Brown (1952). They are subspherical, 
smooth, 19 to 26 by 17 to 25 ji with a mean 
of 22 by 21 ^t, and without a micropyle or 
oocyst polar granule. No other morpho- 
logical information was given. The sporu- 
lation time is 2 days. 

Life Cycle : Unknown. The endogen- 
ous stages occur in the epithelial cells of 
the villi. The tips of the villi are most 
heavily parasitized, while the crypts and 
deep glands are never affected. According 
to Moore and Brown (1952), oocysts first 
appear in the feces 5 days after infection, 
and the patent period is up to 9 days. 

Pathogenesis : This species is non- 
pathogenic according to Moore and Brown 
(1952). They observed no macroscopic 
lesions, even in heavy infections; poults 
less than 5 weeks old showed no signs of 
illness and had no diarrhea. 

Immunity : Moore and Brown (1952) 
immunized turkey poults by infecting them 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



229 



with 4 to 7 doses of oocysts over a period 
of 22 to 29 days. The immunized birds 
were not immune to E. dispersa, the 
species which E. innocua most closely 
resembles, and turkeys immunized against 
E. dispersa were susceptible to infection 
with E. innocua. 



EIMERIA SUBROTUNDA 

MOORE, BROWN AND CARTER, 1954 

Host : Turkey. 

Moore, Brown and Carter (1954) were 
unable to infect the chicken, guinea fowl, 
ringnecked pheasant or bobwhite quail with 
this species. 

Location: Duodenum, jejunum and 
upper ileum as far as 2 inches anterior to 



the yolk stalk rudiment. 

Geographic Distribution : 
America. 



North 



Prevalence : Apparently uncommon. 

Morphology : This species closely 
resembles E. innocua, according to 
Moore, Brown and Carter (1954). The 
oocysts are subspherical, smooth, 16 to 
26 by 14 to 24 jj. with a mean of 22 by 20 ji , 
without a micropyle or polar granule. No 
other morphological information was given. 
The sporulation time is 48 hours. 

Life Cycle : Unknown. According to 
Moore, Brown and Carter (1954), the en- 
dogenous stages occur in the epithelial 
cells of the tips of the villi, extend along 
the sides of the villi to some extent, but 
never invade the crypts and deep glands. 
Oocysts first appear in the feces 96 hours 
after infection, and the patent period is 12 
to 13 days. 

Pathogenesis : This species is appar- 
ently non- pathogenic. Moore, Brown and 
Carter (1954) observed no signs of infec- 
tion, diarrhea or gross lesions in poults 
less than 5 weeks old which had been in- 
fected with massive doses of sporulated 
oocysts. 



Immunity : Moore, Brown and Carter 
(1954) immunized turkey poults by feeding 
them 10,000 to 15,000 sporulated oocysts 
every 4 days until they ceased to shed 
oocysts; this occurred in less than a month. 
Poults which had been immunized against 
E. subrotunda were not immune to E. 
innocua and E. dispersa, and poults which 
had been immunized against the latter two 
species were not immune to E. subrotunda. 
This was the primary basis for separating 
E. subrotunda from E. innocua. 



COCCIDIOSIS IN TURKEYS 

Epidemiology : Coccidiosis in turkeys 
has been discussed by Morehouse (1949), 
Hawkins (1952), Moore (1954) and Becker 
(1959) among others. The U. S. Dept. of 
Agriculture (1954) estimated that it caused 
an annual loss of $466,000 from 1942 to 
1951, and it is becoming of increasing im- 
portance to the turkey grower. 

Of the 7 species of Eimeria, 1 of 
Isospora and 1 of Cryptosporidium reported 
from turkeys, by far the most important 
are E. meleagriniitis and E. adenoeides. 
The former affects the jejunum and the 
latter the lower ileum, ceca and rectum. 

Coccidiosis is primarily a disease of 
young birds. Older birds are carriers. 
Poults become infected by ingesting 
oocysts along with their feed or water. 
The severity of the disease depends on the 
number of oocysts they receive. If they 
ingest relatively few, they may develop 
immunity without ever showing signs of 
illness, while if they ingest large numbers, 
they may become seriously ill or die. 
Crowding and lack of sanitation greatly 
increase the disease hazard. 

Diagnosis : Coccidiosis of turkeys 
can be diagnosed in the same way as coc- 
cidiosis of chickens by finding endogenous 
stages of the coccidia in scrapings of the 
affected parts of the intestinal tract of 
birds which show signs of the disease. 
The mere presence of coccidia in the ab- 
sence of disease cannot be relied on. Since 
several species of turkey coccidia 



230 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



(E. innociia, E. subyolunda a.nd E. niele- 
agridis in particular) are non- pathogenic 
or nearly so, they must be differentiated 
from the pathogenic E. nieleagriiuUis 
and E. adenoeides. The sporulated oocysts 
of both the latter have polar bodies, which 
differentiates them from all but E. Diele- 
agridis and E. gallopavonis . The oocysts 
of E. »ielecigyi»iilis are ellipsoidal, but 
apparently only pathogenesis and absence 
of cross-immunity differentiates E. 
adenoeides from the other two. This last 
is hardly a practical diagnostic test, since 
it requires a colony of turkeys immunized 
against the various species. 

Treatment : The sulfonamides are 
effective against a number of the turkey 
coccidia. Morehouse (1949a) found that 
only one of 6 sulfonamides was ineffective 
against E. nieleagridis. Peterson (1949a) 
found that several sulfonamides were ef- 
fective against E. nieleagriniitis. Moore 
(1949) found that 0.031% sulfaquinoxaline, 
1% sulfaguanidine or 0. 5% sulfamerazine 
in the feed was effective against turkey 
coccidiosis. Wilson (1951) reported that 
0. 06% sodium sulfaquinoxaline in the 
drinking water stopped losses from E. 
nieleagridis and E. Dieleagriniltis in a 
natural outbreak. (Their cultures oiE. 
nieleagridis may have contained E. 
adenoeides, a species which had not yet 
been named at the time. ) Boyer and 
Brown (1953) found that 0.0175% acetyl- 
sulfaquinoxaline in the feed or 1-1000 to 
1-2000 sulfamethazine in the water was 
effective against E. adenoeides, E. gal- 
lopavonis, E. meleagridis, E. innocua, 
E. subrotunda, E. dispersa andE. mele- 
agrimitis. Horton-Smith and Long (1959) 
found that 0.0125% sulfaquinoxaline in the 
feed was effective against E. nieleagri- 
mitis. 

Other coccidiostats used in treating 
chickens have not been found so useful in 
turkeys. Morehouse (1949) found that 
sodium 4-chlorophenyl arsonate was the 
most effective of 10 organic arsenic com- 
pounds to be tested against E. meleagri- 
dis, but that its effective dose was too 
close to the toxic one. Another organic 
arsenic compound, 3-nitro-4-hydroxy- 
phenyl arsonic acid was of less value. 



Boyer and Brown (1953) found that 
nitrophenide, 2-amino-5-nitrothiazole, 
sulfisoxazole, nitrofurazone and furoxone 
were not effective coccidiostatic agents in 
the turkey. Cuckler et at. (1955) reported 
that nicarbazin was effective against E. 
galloparonis and E. nteleagrimitis, but 
Horton-Smith and Long (1959) found that 
it was ineffective against £. nieleagrimilis 
and in addition found that nitrofurazone and 
glycarbylamide were also ineffective 
against this species. 

Prevention and Control : The same 
measures should be used for the prevention 
and control of coccidiosis in turkeys as in 
chickens. 

EIMERIA TRUNCATA 
(RAILLIET AND LUCET, 1891) 
WASIELEWSKI, 1904 

Synonym : Coccidium truncatum. 

Hosts: Domestic goose, greylag 
goose {Anser anser), Ross's goose {A. 
rossi), Canada goose {Branta ca>iadensis) 
(see Levine, 1953; Hanson, Levine and 
Ivens, 1957). In addition to these, Pavlov 
(1942) reported finding E. truncata in 
domestic ducks in Bulgaria, and Christian- 
sen (1948, 1952) found oocysts resembling 
E. truncata but smaller in the kidneys of 
young swans {Cygniis olor) and common 
eiders [Soniateria niollissima) in Denmark. 

Location : Kidneys. 

Geographic Distribution : Worldwide. 

Prevalence : Relatively uncommon in 
domestic geese, at least in North America. 

Morphology : This species has been 
described by Kotlan (1933) and Lerche 
(1923) among others. The oocysts are 
ovoid, with a narrow, truncate, small 
end, and measure 14 to 27 by 12 to 22 fi. 
The oocyst wall is smooth and delicate, 
shrinking quickly during concentration in 
hypertonic solutions. A micropyle with a 
polar cap is present. An oocyst residuum 
is sometimes present. A sporocyst resi- 
duum is present. The sporulation time is 
1 to 5 days. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



231 



Life Cycle : The endogenous stages 
occur in the epithelial cells of the kidney 
tubules. The life cycle has not been 
studied in detail. The prepatent period is 
5 to 6 days according to Kotlan (1933). 

Pathogenesis : E. truncata is highly 
pathogenic for goslings, sometimes wiping 
out whole flocks within a few days. The 
disease is usually acute, lasting only 2 or 
3 days. Affected birds are extremely 
weak and emaciated. Their kidneys are 
greatly enlarged, light-colored, with 
small, yellowish white nodules, streaks 
and lines on the surface and thruout the 
parenchyma. The infected epithelial cells 
are destroyed, and adjacent, uninfected 
cells are also destroyed by pressure. 
The infected tubules are so filled with 
urates and oocysts that they are enlarged 
to 5 to 10 times the diameter of normal 
tubules. 

Epidemiology : E. truncata occurs 
only sporadically in domestic geese in 
North America. It was first described in 
the United States by McNutt (1929) in 
Iowa, and has since been reported by 
Allen (1933) in Washington, D. C, Adler 
and Moore (1948) in Washington state, 
Levine, Morrill and Schmittle (1950) in 
Illinois, Lindquist, Belding and Hitchcock 
(1951) in Michigan, Farr and Wehr (1952) 
in Maryland, and McGregor (1952) in 
Ontario. It has also been found in New 
York and Quebec. 

The epidemiology of E. truncata in 
wild geese is especially interesting (Han- 
son, Levine and Ivens, 1957). It has 
been found in the greylag goose {Anser 
anser) in Europe by Christiansen and 
Madsen (1948), and in Ross's goose {A. 
rossi) and the Canada goose {Branta cana- 
densis) in North America. However, of 
the 6 wild goose flyways which form ver- 
tical bands across North America, E. 
truncata has been found only in the South 
Atlantic and Pacific flyways, and not from 
the flyways in between. It is common 
among Canada geese of the South Atlantic 
flyway, and has been associated with 
losses at their winter quarters at Pea 
Island, North Carolina (Critcher, 1950). 
Its apparent absence from wild geese in 



the interior flyways does not seem due to 
the examination of too few birds, since 
Hanson, Levine and Ivens (1957) failed to 
find it in 258 wild geese from these fly- 
ways altho they recognized it in birds from 
both coasts. Perhaps E. truncata was 
originally a parasite of greylag and domes- 
tic geese in Eurasia and has reached North 
American wild geese relatively recently, 
entering from both the east and west. 



EIMERIA ANSERIS 
KOTLAN, 1932 

Hosts : Domestic goose, blue goose 
(Anser caerulescens), Richardson's 
Canada goose {Branta canadensis hutch- 
ins i). 

Location : Small intestine, mainly 
posterior part. 

Geographic Distribution : Europe, 
North America. 

Prevalence : E. anser is has been 
reported from domestic geese only in 
Europe (Kotlan, 1933; Cerna, 1956) and 
is apparently not particularly common 
there. Hanson, Levine and Ivens (1957) 
found it in 4% of 73 blue geese from Ft. 
Severn and Weenusk, Ontario and in 33% 
of 6 Richardson's Canada geese from 
York Factory, Manitoba. 

Morphology : This species was des- 
cribed in detail by Hanson, Levine and 
Ivens (1957). The oocysts have the form 
of a sphere surmounted by a truncate 
cone, with a micropyle at the truncate end, 
and measure 20 to 24 by 16 to 19 /i with a 
mean of 22 by 11 \x (16 to 23 by 13 to 18 /i 
according to Kotla'n, 1933). The oocyst 
wall is smooth, colorless, composed of a 
single layer about 1 \i thick, and slightly 
thickened around the micropyle but incised 
sharply to form a plate or shelf across the 
micropyle itself. The oocyst residuum is 
a mass of amorphous material just beneath 
the micropyle and forming a seal beneath 
it. An oocyst polar granule is absent. 
The sporocysts are ovoid and almost com- 
pletely fill the oocyst. The sporocyst 
wall is slightly thickened at the small end. 



232 



THE TELOSPORASIDA AND THE COCCIDW PROPER 



The sporocysts are 10 to 12 by 7 to 9 /i. 
A sporocyst residuum is present. The 
sporozoites often lie more or less trans- 
versely at the anterior and posterior ends 
of the sporocyst. The sporulation time is 
1 to 2 days according to Kotlan (1933). 

Life Cycle : The endogenous stages 
have been described by Kotlan (1933). 
They occur in compact clumps under the 
intestinal epithelium near the muscularis 
mucosae and also in the epithelial cells of 
the villi. The schizonts are spherical, 
12 to 20 ji in diameter, and contain 15 to 
25 slightly curved, crescent-shaped mero- 
zoites. There is probably only a single 
asexual generation. The sexual stages 
are found mostly in the subepithelial tis- 
sues of the villi, but invade the epithelium 
in heavy infections. The macrogametes 
measure 12 to 16 by 10 to 15 /i. The mi- 
crogametocytes are spherical and about 
the same size. Oocysts first appear in 
the feces 7 days after infection, and the 
patent period is 2 to 8 days. 

Pathogenesis : Kotlan (1933) reported 
that experimental infections in 2.5- to 
3-month-old geese were harmless, but 
described two outbreaks of intestinal coc- 
cidiosis in goslings which he considered 
due to a combination of E. anseris and 
E. nocens. 



EIMERIA NOCENS 
KOTLAN, 1933 

Hosts: Domestic goose, blue goose 
{Anser caerulescens). 

Location: Posterior part of small 
intestine. 

Geographic Distribution : Europe, 
North America. 



Morphology : The sporulated oocysts 
were described by Hanson, Levine and 
Ivens (1957). They are ovoid but flattened 
at the micropylar end, 29 to 33 by 19 to 
24 /i with a mean of 31 by 22 /i (25 to 33 by 
17 to 24 |i according to Kotlan, 1933). The 
oocyst wall is smooth and composed of 2 
layers, the outer one 1. Sji thick and pale 
yellow, the inner one 0.9(1 thick and al- 
most colorless. A prominent micropyle 
is present. A true micropylar cap is ab- 
sent, but the micropyle appears to be 
present only in the inner wall and is cov- 
ered by the outer wall. An oocyst polar 
granule and oocyst residuum are absent, 
but part of the oocyst wall often forms one 
or more roundish protuberances just below 
the micropyle. The sporocysts are broadly 
ellipsoidal, with a thin wall and sometimes 
with a very small Stieda body. The sporo- 
cysts are 10 to 14 by 8 to IOjll with a mean 
of 12 by 9 /J.. The sporozoites usually lie 
head to tail in the sporocysts and contain 
2 or more large, clear globules which al- 
most obscure their outline. The sporocyst 
residuum fills the space between sporo- 
zoites. 



Life Cycle : According to Kotlan 
(1933), the endogenous stages are found 
primarily in the epithelial cells at the tips 
of the villi, but they may also occur be- 
neath the epithelium. The younger devel- 
opmental stages lie near the host cell nu- 
clei, but as they grow they not only dis- 
place the nuclei but also destroy the host 
cell and come to lie free and partly be- 
neath the epithelium. The schizonts are 
spherical, 15 to 30 fi in diameter, and con- 
tain 15 to 35 merozoites. The macroga- 
metes are usually ellipsoidal or irregularly 
spherical, uniformly coarsely granular, 
and measure 20 to 25 by 16 to 21 /j, . The 
microgametocytes are spherical or ellip- 
soidal and measure 28 to 36 by 23 to 31 ji. 



Prevalence : E. nocens has been re- 
ported from the domestic goose only in 
Europe (Kotlan, 1933; Cerna, 1956), and 
is apparently not particularly common 
there. Hanson, Levine and Ivens (1957) 
found it in blue geese from Ft. Severn 
and Weenusk, Ontario. 



Pathogenesis : Kotlan (1933) described 
2 outbreaks of intestinal coccidiosis in 
goslings in Hungary in which he found both 
E. nocois and E. anseris. Since the latter 
is apparently non- pathogenic, the disease 
was presumably due to E. nocens. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



233 



EIMERIA PARVULA 
KOTLAN, 1933 

Host : Domestic goose. 

Location : Small intestine, primarily 
posterior part. 

Geographic Distribution : Europe. 

Prevalence : This species is com- 
mon in geese in Hungary, according to 
Kotlah (1933). 

Morphology : This species was des- 
cribed by Kotlin (1933). The oocysts are 
spherical or subspherical, smooth, color- 
less, delicate, 10 to 15 by 10 to 14 p., 
without a micropyle. No other morpho- 
logical details were given. 

Life Cycle : Unknown. According to 
Kotlan (1933), the endogenous stages are 
found almost exclusively in the epithelial 
cells of the villi. Oocysts first appear in 
the feces 5 days after infection. 

Pathogenesis : According to Kotlan 
(1933), this species is non- pathogenic. 



EIMERIA ANATIS 
SCHOLTYSECK, 1955 

Host : Wild mallard (Anas platyrhyn- 
chos). Scholtyseck did not find this spe- 
cies in 6 domestic ducks, which he called 
A. domes tica. 

Location : Small intestine. 

Geographic Distribution : Europe 
(Germany). 

Prevalence : Scholtyseck (1955) found 
this species in 5 of 32 wild mallards. 

Morphology : The oocysts are ovoid, 
14 to 19 by 11 to 16fi with a mean of 17 
by 14 /J.. The oocyst wall is smooth, about 
0. 7 to 1.0 /i' thick, with a thickened ring 
forming shoulders around the micropyle. 
An oocyst residuum and polar granule are 
absent. The sporocysts are elongate 
ovoid or ellipsoidal, with a slight thicken- 



ing at the small end but not a true Stieda 
body. A few sporocyst residual granules 
are present between the sporozoites. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : Tiboldy (1933) reported 
Eimeria sp. oocysts in domestic ducks in 
Hungary. They were ovoid, elongate ovoid 
or occasionally spherical are measured 11 
to 25 by 8 to 13 /i . Their relationship to 
E. anatis is unknown. 



EIMERIA LABBEANA 
PINTO, 1928 

Synonyms : Coccidium pfeifferi, 
Ewieria pfeifferi, Eimeria coliimbarum. 

Hosts: Domestic pigeon, ring dove 
(ColiDuba palumbus), turtle dove (Strep- 
topelia turtur), Streptopelia orientalis 
meena (see Scholtyseck, 1956). 

Location : Small and large intestine. 

Geographic Distribution : Worldwide. 

Prevalence : Common. 

Morphology : The oocysts are sub- 
spherical to spherical, colorless or 
slightly yellowish brown, 13 to 24 by 12 to 
23jLi. The oocyst wall is composed of 2 
layers, the inner one darker than the outer. 
There is no micropyle. An oocyst polar 
granule is present. An oocyst residuum 
is absent. The sporocysts are elongate 
ovoid, with a Stieda body. A sporocyst 
residuum is present. The sporozoites lie 
lengthwise, head to tail, in the sporocysts. 
They are slightly crescent-shaped, with 
one end wider than the other, a vacuole at 
each end and the nucleus near the middle. 

Nieschulz (1935) separated this species 
into two on the basis of size. He retained 
the name E. labbeana for the smaller form, 
which measured 13 to 24 by 12 to 22 jn 
(usually 15 to 18 by 14 to 16jj,) with a mean 
of 18 by 15(i. He named the larger form 
E. columbarum ; it measured 17 to 24 by 



234 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 




Fig. 30. Sporulated oocyst of Eimeria lab- 
beana of the pigeon. X 1700. 
(From Nieschulz, 1935) 

16 to 22 11 (usually 19 to 21 by 17. 5 to 20 fi ) 
with a mean of 20 by 19 ji. On the other 
hand, Duncan (1959), in a study of infec- 
tions in more than 300 pigeons, measured 
a large but unspecified number of oocysts 
at various times during the patent period 
and found that the overall range was 14. 5 
to 24 by 13 to 22. 5 (i with an overall mean 
of 19 by 11 IX . However, smaller oocysts 
appeared early in the infection in 13 birds, 
and in 10 of them they increased in size to 
approximately the overall average by the 
end of the patent period. These small 
oocyst strains averaged 15 to 18 by 14 to 
17ji. It would appear, therefore, that £. 
columbarum is a synonym of E. labbeaiia. 

Life Cycle : Nieschulz (1925a) des- 
cribed the endogenous stages and also gave 
one of the few descriptions extant of early 
sporogony in the coccidia. Soon after the 
macrogametes are fertilized and the 
oocysts are formed, the zygote contracts 
into a ball within the oocyst wall. A fer- 
tilization spindle then forms; it is a clear 
band which passes thru the center of the 
sporont and forms extensions which reach 
to the oocyst wall. This band then dis- 
appears and the sporont rounds up again, 
but a refractile granule is left in the 
oocyst. Altho Nieschulz did not recognize 
it as such, this was undoubtedly reduction 
division with the throwing off of a polar 
granule. Four prominences form on the 
sporont, which then divides to form 4 
spherical sporoblasts. These become 
rather triangular or elongate ovoid, and 
a clear area appears at the pointed end 
(pyramid stage). The sporoblasts round 
up again, and finally elongate to form 
elongate ovoid, pointed sporocysts in 



which the sporozoites develop. The spor- 
ulation time is 4 days or less (Duncan, 
1959a). 

After the sporulated oocysts are in- 
gested, the sporozoites are released and 
invade the epithelial cells of the intestine. 
They round up and grow into mature schi- 
zonts in 3 days. Each schizont produces 
about 15 to 20 merozoites, often leaving a 
residual body. The merozoites are some- 
what crescent-shaped, pointed at the ends, 
and 5. 5 to 9 /J. long. There is a second 
generation of schizonts which Nieschulz 
thought might be extracellular. These are 
elongate, up to 18 by 5 ^i, and form up to 
16 merozoites. 

The microgametocytes form a large 
number of biflagellate microgametes about 
2>\i long with flagella 10/i long. The ma- 
crogametes have a row of large plastic 
granules around their periphery. Nieschulz 
figured what was probably a fertilized ma- 
crogamete in which a microgamete nucleus 
was approaching the macrogamete nucleus 
in a clear pathway thru the cytoplasm. 
After fertilization, the plastic granules 
coalesce to form the oocyst wall. Oocysts 
first appear in the feces 6 days after in- 
fection. 

Pathogenesis : E. labbeatia is 
slightly to markedly pathogenic, depending 
in part upon the age of the birds (Levi, 
1957). Adults are fairly resistant, altho 
fatal infections have been seen. The birds 
become weak and emaciated, eat little but 
drink a great deal, and have a greenish 
diarrhea. The heaviest losses occur 
among squabs in the nest. A high percent- 
age of the squabs may die, and those which 
recover are often somewhat stunted. 

The principal gross lesion is inflam- 
mation thruout the intestinal tract. 

Diagnosis : Diagnosis depends on 
recognizing the oocysts and other stages in 
the intestine in association with the signs 
and lesions of the disease. 

Treatment : According to Lindsay 
(cited by Levi, 1957), sulfaquinoxaline is 
effective against E. labbeana. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



235 



Prevention and Control : The same 
measures used to control coccidiosis in 
chickens are effective against the disease 
in pigeons. General sanitation and dry 
quarters are especially important. 



EIMERIA COLUMBAE 

MITRA AND DAS GUPTA, 1937 

Host : Indian pigeon {Columba livia 
intermedia). 

Location: Intestine. 

Geographic Distribution : India. 

Prevalence : Unknown. 

Morphology : The oocysts of this 
species have not been completely des- 
cribed. They are subspherical, have a 
maximum size of 16 by 14 /j, and differ 
from E. labbeana in having an oocyst 
residuum, according to Mitra and Das 
Gupta (1937). 

Life Cycle : Unknown. 

Pathogenesis: Unknown. 



Genus ISOSPORA Schneider, 1881 

In this genus the oocyst contains 2 
sporocysts, each of which contains 4 
sporozoites. 



ISOSPORA AKSAICA 
BASANOV, 1952 

Host : Ox. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : USSR 
(Kazakhstan). 

Prevalence : Unknown. This species 
was found only in calves 12 to 30 days old. 

Morphology : The oocysts are 26 ii in 
diameter, spherical, dark silver under 



low magnification and light, pinkish grey 
under high. The oocyst wall is 1.6^ thick, 
smooth and double -contoured, with a light 
blue outer layer and a greenish, dingy 
rose inner layer. The sporocysts are el- 
lipsoidal or spherical, 22 by 15 /i. Micro- 
pyle, oocyst residuum and sporocyst resi- 
duum are presumably absent. Polar 
granules are possibly present. The sporo- 
zoites are spherical, bean-shaped or 
ellipsoidal, 1 5 by 1 1 jj, . 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : There is a question 
whether this is actually a valid species of 
bovine coccidium or whether it is a pseudo- 
parasite, i.e., an avian or other foreign 
coccidium which the cattle had ingested 
along with its host's feces. Further work 
will be necessary to decide this point. 
The subjacent discussion of the Isospora 
species found by Levine and Mohan (1960) 
in cattle has a bearing on /. aksaica also. 



ISOSPORA sp. 

LEVINE AND MOHAN, 1960 

Hosts : Ox and ox-zebu hybrids. 

Location : Unknown. Oocysts found 
in feces. 



Geographic Distribution : 
America (Illinois). 



North 



Prevalence : Levine and Mohan (1960) 
found this form in 6 out of 54 beef cattle 
on 3 farms in central Illinois. 

Morphology : The oocysts are usually 
subspherical, occasionally spherical, 21 
to 33 by 20 to 32 ^ with a mean of 27 by 
25 ji. The oocyst wall is smooth, color- 
less, pale lavender or pale yellowish, 
composed of a single layer about 1 ji thick. 
In some oocysts, the wall appeared to be 
lined by a thin membrane. A micropyle 
and oocyst residuum are absent. Several 
oocyst polar granules are present. The 
sporocysts are lemon-shaped, quite thick- 
walled, 14 to 20 by 10 to 12 ^x with a mean 



236 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



of 17 by 11 /i. The sporocyst Stieda body 
is a button-shaped cap, with a dependent, 
globular hyaline mass protruding into the 
interior of the sporocyst. The sporocyst 
residuum is finely granular. The sporo- 
zoites are sausage-shaped, not arranged 
in any particular order in the sporocyst. 
The sporocyst residuum and sporozoites 
are enclosed in a membrane, forming 
more or less of a ball within the sporo- 
cyst. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : Levine and Mohan (1960) 
compared this form with /. lacazei of the 
English sparrow, which they redescribed. 
They found that the 2 forms were practi- 
cally indistinguishable and concluded that 
the oocysts found in bovine feces were 
most likely those of /. lacazei and were 
pseudoparasites of cattle. They calculated 
that, in a steer which produced about 20 
pounds of feces per day, the presence of 
1 oocyst per gram of feces would represent 
contamination of the feed with about 9000 
oocysts, assuming that the oocysts were 
mixed uniformly with the ingesta and 
passed thru the animal unchanged. Assum- 
ing again that a flotation was carried out 
with about 2 g of feces and that about 10% 
of the oocysts present were recovered, 
they calculated that every oocyst found 
might represent an initial contamination 
of a day's feed with about 45, 000 oocysts. 
Since Boughton (1933) quite frequently ob- 
tained counts of 200,000 to 2 million 
oocysts per gram of dried sparrow feces, 
they considered it quite likely that spar- 
row coccidia could be detected in a calf's 
feces if it ingested only a single fecal 
deposit from a single sparrow in the 
course of a day. 



ISOSPORA SUIS 
BIESTER, 1934 

Host : Pig. 

Location : Small intestine, from the 
lower third of duodenum to 2 or 3 feet 
from the ileocecal valve. 



Geographic Distribution : North 
America (Iowa), USSR (Kazakhstan). 

Prevalence : Unknown. 

Morphology : This species has been 
described by Biester (1934) and Biester 
and Murray (1934). The oocysts are sub- 
spherical to ellipsoidal, becoming more 
ellipsoidal on sporulation. The oocyst 
wall is often stretched by the oocysts and 
pinched in between them. It is smooth, 
composed of 2 layers, brownish yellow, 
and 1.5(i thick. A micropyle is absent. 
The unsporulated oocysts measure 20 to 
24 by 18 to 21 fi with a mean of 22. 5 by 
19.4/1. An oocyst polar granule is pres- 
ent. An oocyst residuum is absent. The 
sporocysts are ellipsoidal, 16 to 18 by 
10 to 12 /i with a mean of 16.4 by 11. 2u. 
The sporocyst wall is double, 0. 7|i thick. 
The sporozoites are elongate. A sporo- 
cyst residuum is present. A Stieda body 
is absent. The sporulation time is 4 days. 

Life Cycle : According to Biester and 
Murray (1934), /. suis invades the epithe- 
lial cells of the intestine. Many of these 
invaded cells migrate to a subepithelial 
position, but often both the host cells and 
the parasite appeared to undergo retro- 
gressive changes and to be desquamated. 

The prepatent period after experi- 
mental infection is 6 to 8 days, and oocysts 
continue to be eliminated for about 8 days 
after a single infective feeding. 

Pathogenesis : According to Biester 
and Murray (1934), /. sids causes a catar- 
rhal enteritis. The epithelium of the 
crypts is destroyed except near the intes- 
tinal lumen. The substantia propria of 
the tips of the villi is destroyed, leaving 
a reticular honeycomb without cells or 
nuclei. Interstitial inflammation with 
marked eosinophilic infiltration is present, 
but there is no gross hemorrhage. 

Diarrhea began about the 6th day af 
after experimental infection, continued 
for 3 or 4 days, and was followed by con- 
stipation. /. suis infections are appar- 
ently not fatal, but they may retard growth 
and produce unthriftiness. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



237 



Cross-Transmission Studies : Biester 
and Murray (1934) and Biester (1934) re- 
ported that attempts to transmit /. sids 
to guinea pigs, rats, and dogs were un- 
successful. 



ISOSPORA ALMATAENSIS 
PAICHUK, 1953 

Host : Pig. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : USSR 
(Kazakhstan). 

Prevalence : Unknown. 

Morphology : This species was des- 
cribed by Paichuk (1953). The oocysts 
are short-oval, subspherical or spherical, 
and grey. The short-oval forms are 25 
to 32 by 23 to 29 jj, with a mean of 27. 9 by 
26. \i ; the spherical forms are 26 to 32 [i 
in diameter with a mean of 27. 7 /j. . The 
oocyst wall is smooth, bright yellow, "i^i 
thick, and composed of 3 layers. A mi- 
cropyle is apparently absent. The oocysts 
sometimes have 2 sporoblasts when 
passed. Oocyst polar granules are pres- 
ent. An oocyst residuum is absent. The 
sporocysts are oval or ovoid with a 
pointed end, 12 to 19 by 9 to 12 /i with a 
mean of 15.5 by 10. 8 /i . A sporocyst 
residuum is present. The sporozoites are 
short-oval, 6 by 4jj.. The sporulation 
time is 5 days. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 



ISOSPORA BIGEMINA 
(STILES, 1891) 
LUHE, 1906 

Synonyms : Coccidium bigeminum, 
Liicetina bigemina. 

Hosts : Dog, cat, fox, polecat (Pu- 
toriiis foetidus), mink (Mustela vison), 
man (?). 



Location: Thruout small intestine. 

Geographic Distribution : Worldwide. 

Prevalence : This species is quite 
common in dogs and cats. Gassner (1940) 
found it in 74% of 320 dogs in Colorado. 
Catcott (1946) found it in 3% of 113 dogs 
in Ohio. Choquette and Gelinas (1950) 
found it in 2% of 155 dogs in Montreal. 
Ehrenford (1953) found it in 0.7% of 377 
dogs in Indiana and other midwestern 
states. Hitchcock (1953) found it in 1% of 
147 kittens in Michigan. Levine (1948) 
reviewed reports of this species in Mus- 
telidae. 



Morphology: The oocysts are very 
thin-walled, spherical to ellipsoidal when 
unsporulated, but with the wall stretched 
around the sporocysts and usually con- 
stricted somewhat between them when 
sporulated. The oocyst wall is smooth, 
colorless, and composed of a single layer. 
Two sizes of oocyst have been reported. 
The larger ones measure 18 to 20 by 14 
to 16 |i, and the smaller, more common 
ones 10 to 14 by 7 to 9 ^t. Micropyle, 
oocyst polar granule and oocyst residuum 
are absent. The sporocysts are ellip- 
soidal, 7. 5 to 9 by 5 to 7 |:x, without a 
Stieda body. A sporocyst residuum is 
present. The oocysts are sporulated 
when passed. The oocyst wall is often 
ruptured so that the sporocysts are found 
free in the feces. In acute infections, the 
oocysts may be unsporulated when passed; 
their sporulation time is about 4 days. 

Life Cycle : The life cycle of this 
species has been studied by Wenyon (1926a) 
and Wenyon and Sheather (1925). The 
endogenous stages occur thruout the small 
intestine. Altho the course of infection has 
not been followed consecutively in a series 
of experimentally infected animals, it ap- 
pears that the epithelial cells are invaded 
first, followed later on by the subepithelial 
cells. At any rate, Wenyon and Sheather 
(1925) found coccidia only in the epithelial 
cells of a dog killed during the acute phase 
of the infection. The schizonts of this 
stage contain 8 merozoites. Later on, the 
coccidia are found in the subepithelial 
cells and cores of the villi. The schizonts 



238 



THE TELOSPORASroA AND THE COCCIDIA PROPER 



here contain about 12 merozoites. Sexual 
stages appear to be produced in both loca- 
tions. The oocysts produced in the epithe- 
lial cells during the acute phase are 
unsporulated when passed in the feces. 
They appear 6 to 7 days after infection. 
The oocysts produced in the subepithelial 
cells are sporulated when passed. A 
number of unanswered questions are raised 
by this account, and the whole life cycle 
deserves re-investigation. 

Pathogenesis : This species is mark- 
edly pathogenic for both cats and dogs. 
Its effects on the dog, cat and fox were 
studied by Lee (1934). Puppies and kittens 
are most seriously affected, while adults 
are usually carriers, having developed an 
immunity following earlier infection. 

The first signs usually begin 4 to 6 
days after infection. Their severity de- 
pends on the degree of infection. In 
severe cases, catarrhal or bloody diar- 
rhea, rapid emaciation and anemia occur. 
Affected animals are weak, depressed and 
lose their appetite. There may be a rise 
in temperature or muscular tremors of 
the hind legs. If the animal survives the 
acute phase, the dysentery is replaced by 
mucous stools for 2 to 4 days and the 
other signs subside, disappearing 7 to 10 
days after their onset. Recovered animals 
may continue to shed oocysts for a time. 



from those of /. bigemina, and a number 
of investigators believe that they are the 
same species (Elsdon-Dew and Freedman, 
1953; Routh, McCroan and Hames, 1955; 
Becker, 1956). Cross-transmission ex- 
periments are needed to determine whether 
they are. 



ISOSPORA FEUS 
WENYON, 1923 

Synonyms : Isospora call, Coccidium 
bigeniinuni var. cati, Lucetina cati, 
Lucetina fells. 

Hosts : Dog, cat, lion and possibly 
other carnivores. 

Location : Small intestine, some- 
times cecum, occasionally colon. 

Geographic Distribution : Worldwide. 

Prevalence : This species in common 
in dogs and cats. Gassner (1940) found it 
in 6% of 320 dogs in Colorado. Catcott 
(1946) found it in 3. 5% of 113 dogs in Ohio. 
Choquette and Gelinas (1950) found it in 9% 
of 155 dogs in Montreal. Hitchcock (1953) 
found it in 75% of 147 kittens in Michigan. 
Alves da Cruz, de Sousa and Cabral (1952) 
found it in 10% of 40 stray cats in Lisbon, 
Portugal. 



In severe cases, hemorrhagic enter- 
itis is present thruout the small intestine; 
it is most severe in the lower ileum and 
becomes progressively less so anteriorly. 
Petechiae are present in light infections, 
and diffuse hemorrhages in more severe 
ones. There may be ulcers in addition. 
The mucosa is thickened, and there may 
be extensive desquamation. A circulating 
eosinophilia may be present, and the para- 
sitized region is infiltrated with eosino- 
philes. 

Cross-Transmission : Lee (1934) 
transmitted /. bigemina from the dog to 
the cat and fox, but failed to infect rabbits 
or guinea pigs with it. 

Remarks : The oocysts of /. honiinis 
of man are apparently indistinguishable 



Morphology : The oocysts are ovoid, 
32 to 53 by 26 to 43 ji with a mean of 43 
by 33 jj. . The oocyst wall is smooth and 
colorless, without a micropyle. An oocyst 
polar granule and residuum are absent. 
The sporocysts are ellipsoidal, 20 to 27 
by 18 to 21 /i. A sporocyst residuum is 
present. The sporozoites are 10 to 15;^ 
long. The sporulation time is 3 days or 
less. 

Life Cycle : The life cycle of /. fells 
in experimentally infected kittens was des- 
cribed in detail by Hitchcock (1955) and 
Lickfeld (1959). It is similar in dogs. 
The parasites are found above or beside 
the host cell nuclei of the epithelial cells 
of the villi and sometimes in the subepi- 
thelial tissues. There are 2 asexual gen- 
erations. The first generation schizonts 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



239 



are found in the small intestine and cecum 
from the second to fourth day after experi- 
mental infection. They are ellipsoidal 
and about 20 j^ long. They produce 40 to 
60 merozoites according to Hitchcock, or 
12 or less according to Lickfeld. These 
merozoites are relatively large, measur- 
ing 16 to 18.5 by 5 to 8 ju. 

The second generation schizonts are 
found on the 5th and 6th days after infec- 
tion in the small intestine and less com- 
monly in the large intestine. According 
to Hitchcock, they produce up to 24 mero- 
zoites, but most contain 12 to 16; accord- 
ing to Lickfeld there are 30 to more than 
100 of these merozoites, and they measure 
7. 5 by 2. 5jLt. 

The sexual stages are found on the 
7th and 8th days after infection. They 
occur in the small intestine and less com- 
monly in the cecum. According to Hitch- 
cock (1955), the macrogametes average 
25 to 22 /J,, but other workers have re- 
corded dimensions up to 56 by 48/j, . The 
microgametocytes average 28 by 19jll 
according to Hitchcock, but other workers 
have recorded dimensions up to 50 by 30 ji , 
and Lickfeld said that they are 73 jj, in 
diameter in life. Well over 2000 spindle- 
shaped, curved, biflagellate microgametes 
are formed in each microgametocyte. The 
oocyst wall is laid down following fertiliza- 
tion while the zygotes are still within the 
host cells. The young oocysts then break 
out and are passed in the feces. The pre- 
patent period was found by Hitchcock 
(1955) to be 7 to 8 days. 

According to Walton (1959), the hap- 
loid number of chromosomes in /. felis 
is 2. Lickfeld (1959) described a cryp- 
tomitotic type of schizogony, but saw no 
chromosomes. 

Pathogenesis : This species is 
slightly to moderately pathogenic, depend- 
ing on the host species, age, degree of 
infection, etc. It is less serious in cats 
than in dogs. None of 18 four- to nine- 
week-old kittens infected by Hitchcock 
(1955) with 100,000 sporulated oocysts 
showed signs of disease. Andrews (1926), 



however, observed enteritis, emaciation, 
weakness, depression, dysentery and even 
death in kittens and dogs experimentally 
infected with I. felis. Hitchcock thought 
that these signs and deaths in the kittens 
might well have been due to feline dis- 
temper. 

The gross pathologic lesions are 
similar to those caused by /. bigemina. 
There is hemorrhagic enteritis, frequently 
with ulceration, thickened mucosa and 
epithelial desquamation. 

Immunity : Animals which have re- 
covered from I. felis infections are re- 
sistant to reinfection. 

Cross Transmission : Lee (1934) in- 
fected dogs with /. felis from the cat, and 
a fox with /. felis from the dog. 



ISOSPORA RIVOLTA 

(GRASSl, 1879) 

Synonyms : Coccidiuni rivolta, 
Lucetina rivoltai. 

Hosts : Dog, cat, dingo, and prob- 
ably other wild carjiivores. 

Location: Small intestine. 

Geographic Distribution : Worldwide. 

Prevalence : This species is common 
in dogs and cats. Gassner (1940) found it 
in 20% of 320 dogs in Colorado. Catcott 
(1946) found it in 4% of 113 dogs in Ohio. 
Ehrenford (1953) found it in 72% of 377 
dogs from Indiana and nearby states. 
Choquette and Gelinas (1950) found it in 
13. 5% of 155 dogs in Montreal. Hitchcock 
(1953) found it in 13% of 147 kittens in 
Michigan. 

Morphology : The oocysts are ovoid, 
20 to 25 by 15 to 20 fi. The oocyst wall is 
smooth, with a micropyle at the small 
end. An oocyst polar granule and residuum 
are absent. The sporocysts are 16 by 10 \i. 
A sporocyst residuum is present. The 
sporulation time is 4 days. 



240 



THE TELOSPORASIDA AND THE CCXTCmiA PROPER 



Life Cycle : The endogenous stages 
of /. rivolla are poorly known. They are 
said to resemble those of /. Jelis but to 
be smaller. They are found in the epithe- 
lial cells and sometimes in the subepithe- 
lial tissues of the small intestine. Oocyst 
development ordinarily takes place out- 
side the body, but occasionally occurs in 
the subepithelial tissues. 

Pathogenesis : Altho experimental 
studied on /. rivolla alone have apparently 
not been carried out, it is presumably as 
pathogenic as /. bigeiniiia and /. Jelis. 

Cross Transmission: Lee (1934) in- 
fected a fox with /. rivolla from the dog. 





Fig. 31. 



B 



Sporulated oocysts of coccidia of 

dog and cat. A. Isospora blgem- 

iiia. B. Isospura rivulla. 

C. Isospoya felis. X 850. (From 

Becker, 1934, after Wenyoii, 1926, 

Protozoology) 



COCCIDIOSIS IN DOGS AND CATS 

Epidemiology : Coccidiosis is com- 
mon in dogs and cats, and is a not infre- 
quent cause of diarrhea and even death 
in puppies and kittens. Crowding and 
lack of sanitation promote its spread. 
Coccidia sometimes seed a breeding ken- 
nel, boarding kennel or veterinarian's 
wards so heavily that most of the puppies 
born or brought there become infected. 

Diagnosis : Coccidiosis can be diag- 
nosed at necropsy by finding coccidia in 
the intestinal lesions. It can be diagnosed 
in affected animals by finding oocysts in 



association with diarrhea or dysentery. 
However, care must be taken to differen- 
tiate coccidiosis from coccidiasis, since 
many animals may be shedding oocysts 
without suffering from disease. Other 
disease agents should be searched for and 
found absent. The presence of a wave of 
oocysts during and shortly after an attack 
of enteritis and their marked diminution or 
disappearance soon thereafter would sug- 
gest that coccidia caused the attack. 

The oocysts of Isospora bigemina are 
usually sporulated when they are passed 
in the feces. They are often ruptured, 
releasing the sporocysts. These are very 
small, and will often be overlooked unless 
the high dry power of the microscope is 
used in making a fecal examination. In 
addition, they resemble Cryptospuridium 
oocysts and might be mistaken for them. 

Treatment : There is no good treat- 
ment for coccidiosis in dogs and cats once 
the signs of disease have appeared. All 
the coccidiostatic agents on the market 
are preventive rather than curative in 
action. The fact that coccidiosis is a 
self-limiting disease has often led to the 
belief that some ineffective drug, admin- 
istered at the time natural recovery was 
due to begin, was responsible for the 
cure. Uncontrolled studies on coccidiosis 
therapy, such as that of Duberman (1960) 
with nitrofurazone, are worse than use- 
less, since they may lead to false con- 
clusions regarding a drug's value. 

Craige (1949), a clinician with con- 
siderable experience in handling canine 
coccidiosis, considered treatment in an 
unsatisfactory state. Sometimes the 
animals would respond to sulfonamides, 
but he had better success by combining a 
sulfonamide with quinacrine, sulfocar- 
bolates, tannin-yeast, iodine preparations, 
etc. McGee (1950) used sulfamethazine. 
Altman (1951) used chlortetracycline. 
Supportive treatments such as these, and 
particularly the use of antibiotics such as 
chlortetracycline and oxytetracycline to 
control secondary infections, may be 
helpful even tho they do not act on the 
coccidia themselves. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



241 



Prevention : Sanitation and isolation 
are effective in preventing coccidiosis. 
Animal quarters should be cleaned daily. 
Runways should be concrete. Ordinary 
disinfectants are ineffective against coc- 
cidian oocysts, but boiling water, if it is 
still boiling when it reaches the oocysts, 
will kill them. 



ISOSPORA BELLI 
WENYON, 1923 

Host : Man. 

Location : Presumably small intes- 
tine. Elsdon-Dew, Roach and Freedman 
(1953) found oocysts in material from a 
duodenal intubation. 

Geographic Distribution : Presumably 
worldwide, but more common in the trop- 
ics than in the temperate zone. 

Prevalence : This species is quite 
rare in man. However, Elsdon-Dew and 
Freedman (1953) found it in 32 persons in 
Natal, and considered that it was often 
missed because it was not looked for. 



Pathogenesis : Most infections with 
/. belli appear to be subclinical and self- 
limiting. However, it may cause a mu- 
cous diarrhea. In 31 of the 33 cases of 
Isospora infection studied by Barksdale 
and Routh (1948), anorexia, nausea, ab- 
dominal pain and diarrhea were present. 
Matsubayashi and Nozawa (1948) reported 
that symptoms appeared 1 week after ex- 
perimental infection of 2 human volunteers, 
presumably with /. belli, and that oocysts 
appeared in the feces 10 days after infec- 
tion and persisted for a month. 

Cross-Transmission Studies : Jeffery 
(1956) failed to transmit /. belli from man 
to 2 monkeys, 2 dogs, 2 pigs, 12 mice, 4 
rats, a guinea pig and a rabbit. Robin and 
Fondimare (1960) were unable to transmit 
it from man to the guinea pig, rabbit, 
mouse or rat. 



ISOSPORA HOMINIS 
(RAILLIET AND LUCET, 1891) 
WENYON, 1923 

Synonyms : Coccidiiun bigeminum 
var. hominis, Lucetina hominis. 



Morphology : This species has often 
been confused with /. hominis (see Elsdon- 
Dew and Freedman, 1953), but is clearly 
different. The oocysts are elongate el- 
lipsoidal, 20 to 33 by 10 to 19 fi (mean, 
30 by 12 fi according to Elsdon-Dew and 
Freedman, 1953). One or both ends of 
the oocyst may be somewhat narrow. The 
oocyst wall is smooth, thin, and colorless. 
A very small micropyle is sometimes 
visible. An oocyst polar granule may be 
present in young, incompletely sporulated 
oocysts, but quickly disappears. An 
oocyst residuum is absent. The sporo- 
cysts are subspherical to ellipsoidal, with- 
out a Stieda body, 12 to 14 by 7 to 9 fi 
(mean 11 by 9fi according to Elsdon-Dew 
and Freedman, 1953). A sporocyst resi- 
duum is present. The sporozoites are 
slender, somewhat crescent-shaped, with 
the nucleus at one end. Both immature 
and mature oocysts may be passed in the 
feces. The sporulation time is up to 5 
days. 

Life Cycle : Unknown. 



Host: Man. 



Location: Small intestine. 



Geographic Distribution : Worldwide, 
but more common in the tropics than in 
the temperate zone. 



Prevalen ce: 
rare in man. 
Freedman 

Natal, and thought that it was often missed 
because people did not look for it. 



This species is quite 
However, Elsdon-Dew and 
(1953) found it in 23 persons in 



Morphology : The oocysts are spor- 
ulated when passed. The oocyst wall is 
very thin, stretched around the sporocysts 
and usually constricted between them, and 
sometimes not visible. It is often rup- 
tured, releasing the sporocysts. The 
oocysts are about 20 by 15|j.. Micropyle, 
oocyst polar granule and residuum are 
absent. The sporocysts are ellipsoidal or 
with one side flattened, about 15 by 10 /i, 
without a Stieda body. A sporocyst resi- 
duum is present. 



242 



THi; TELOSPORASIDA AND THE COCCIDLA PROPER 



Life Cycle : Unknown. 

Pathogenesis : Most infections ap- 
pear to be subclinical and self-limiting. 
However, /. Iiominis may cause a mucous 
diarrhea. In 31 of 33 cases of Isuspora 
infection studied by Barksdale and Routh 
(1948), anorexia, nausea, abdominal pain 
and diarrhea were present. 

Remarks : This species resembles 
/. bigetiiina very closely, and it may well 
be the same species (see Becker, 1956, 
Elsdon-Dew and Freedman, 1953; Routh, 
McCroan and Hames, 1955). Elsdon-Dew 
(1954) failed to infect a dog with /. hominis 
from man, but the animal was an adult and 
could have been immune. 



ISOSPORA NATALENSIS 
ELSDON-DEW, 1953 

Host : Man. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : Africa 
(Natal). 

Prevalence : Elsdon-Dew (1953) 
found this species in 2 persons in Natal. 

Morphology : The oocysts are sub- 
spherical, 25 to 30 by 21 to 24^.. The 
oocyst wall is smooth and thin, without a 
micropyle. An oocyst polar granule and 
oocyst residuum are absent. The sporo- 
cysts are ellipsoidal, 17 by 12 /i, without 
a Stieda body. A sporocyst residuum is 
present. The sporulation time is 1 day. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : When Elsdon-Dew and 
Freedman (1953) first saw this form, 
they thought that it was /. rivolla. How- 
ever, it differs morphologically from that 
species. 



COCCIDIOSIS IN MAN 

Coccidiosis is quite rare in man, and 
the relation of the species described from 
man to those in lower animals is still not 
clear. Isospora belli appears to be con- 
fined to man, and /. nataletisis may be 
also. However, further research may 
show that /. lioniinis is a synonym of /. 
bige))iina and that man acquires his infec- 
tions with this parasite from dogs and 
cats. 

In addition to the above species which 
produce infections in man, a number of 
other coccidia have been found in human 
feces and mistaken for parasites of man. 
Perhaps the most famous of these were 
Eimeria wenyoni, E. oxyspora and E. 
snijdersi. which Dobell (1919) described 
as human parasites. The first turned out 
to be E. clupearum, a coccidium of her- 
ring, sprats and mackerel, and the second 
two were both E. sardinae, a parasite of 
sardines, herring and sprats. In addition, 
oocysts of E. stiedae of the rabbit have 
been found in a mental hospital patient who 
liked to eat raw rabbit livers, and oocysts 
of E. debliecki of the pig were found by 
Drug (1946) in several others who probably 
acquired them in sausage casings. 



ISOSPORA GALLINAE 
SCHOLTYSECK, 1954 

Host: Chicken. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : Europe. 

Prevalence : Unknown, presumably 
rare. 

Morphology : The oocysts are ellip- 
soidal, 19 to 27 by 15 to 23)ll with a mode 
of 24 by 19 fi. A micropyle is absent. 
Oocyst polar granules are present. An 
oocyst residuum is absent. The sporo- 
cysts are piriform. 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



243 



Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : The validity of this spe- 
cies is dubious. It is more likely a para- 
site of some wild bird, such as /. lacazei 
of the English sparrow. 



ISOSPORA HEISSINI 
SVANBAEV, 1955 

Host : Domestic turkey. 

Location : Unknown. Oocysts found 
in feces. 

Geographic Distribution : USSR (Ka- 
zakhstan). 

Morphology : The oocysts are spher- 
ical or rarely broadly ovoid, 25 to 33/1 in 
diameter, with a mean of 31 by 30 fx. The 
oocyst wall is greenish, smooth, double 
contoured (illustrated with a single layer), 
and 1.5 to 1.7|i thick. A micropyle is 
apparently absent. An oocyst polar gran- 
ule is present. An oocyst residuum is 
absent. The sporocysts are spherical or 
ovoid and pointed at one end, 15 by 10 jn. 
A sporocyst residuum is absent. The 
sporozoites are oval, 7 to 9 by 4 to 5 /i . 
The sporulation time is 16 to 20 hours at 
20 to 25° C. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : Svanbaev (1955) found this 
species only in turkeys up to 4 months of 
age. 



Genus WENYONELLA Hoare, 1933 

In this genus the oocyst contains 4 
sporocysts, each of which contains 4 
sporozoites. 



WENYONELLA GALLINAE 
RAY, 1945 

Host: Chicken. 



Location : Terminal part of intestine. 

Geographic Distribution : India. 

Prevalence : Uncommon. Gill (1954) 
found this species in 1.7% of 120 chickens 
near Mukteswar. 

Morphology : The oocysts are ovoid, 
rough, punctate, 29 to 34 by 20 to 23 ^i. 
The sporocysts are flask-shaped, 19 by 
8jj,. No other morphological information 
was given. The sporulation time is 28° C 
is 4 to 6 days. 

Life Cycle : Unknown. 

Pathogenesis : According to Ray 
(1945), this species causes a diarrhea 
with blackish-green, semisolid excreta. 
The terminal part of the intestine is thick- 
ened and congested, and there are pinpoint 
hemorrhages in the mucosa. 



Genus TYZZERIA Allen, 1936 

In this genus the oocyst contains 8 
naked sporozoites and no sporocysts. 

TYZZERIA PERNICIOSA 
ALLEN, 1936 

Host: Domestic Pekin duck. 

Location : Thruout the small intes- 
tine, but especially in the upper half. 

Geographic Distribution : North 
America. 

Prevalence : Uncommon. This spe- 
cies has been reported from domestic 
ducks only by Allen (1936) on Long Island. 
However, its relationship to T. alleni, 
which Chakravarty and Basu (1946) des- 
cribed from the cotton teal {Cheniscus 
coromandelianus) in India, to Tyzzeria sp. 
which Farr (1952) reported from the black 
duck {Anas rubripes), to T. anseris re- 
ported by Farr (1959) from the lesser 
scaup duck {Nyroca affinis) in Michigan, 
and to T. anseris from domestic and wild 
geese and the whistling swan (see Hanson, 
Levine and Ivens, 1957) remains to be de- 
termined. 



244 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



Morphology : The oocysts are ellip- 
soidal, 10 to 13 by 9 to 11 (i. The oocyst 
wall is thick, colorless, composed of an 
outer thin, transparent layer and an inner 
thicker layer. A micropyle is absent. 
The sporozoites are curved, with one end 
rounder and broader than the other, about 
10 fi long and 3. 5fx wide at the larger 
end. The oocyst residuum is large, 
usually spherical. The sporulation time 
is 1 day. 

Life Cycle : According to Allen 
(1936), the endogenous stages are found 
in the mucosal and submucosal cells. 
There are at least 3 asexual generations. 
The first generation schizonts are rela- 
tively small, about 12 by Sfi, and contain 
relatively few, small merozoites. The 
later schizonts measure about 15 to 16 by 
14 to 15ji and contain more and larger 
merozoites than the first generation ones. 
Schizogony continues long after the forma- 
tion of gametes. 

The first microgametocytes appear 
2 days after infection. They measure 
about 7. 5 by 6jn and produce a large num- 
ber of tiny microgametes. The macro- 
gametes are somewhat irregular in shape. 
Oocysts first appear in the feces 6 days 
after infection. 

Pathogenesis : According to Allen 
(1936), T. peniiciosa is highly pathogenic 
for ducklings. All of 7 experimentally 
infected, week-old ducklings died. 

Affected birds stop eating, lose 
weight, become weak and cry continuously 
as if in distress. At necropsy, inflamma- 
tion and hemorrhagic areas were found 
thruout the small intestine and especially 
in its upper half. The intestinal wall was 
thickened, and round, white spots were 
visible thru its serosal surface. In se- 
vere cases the lumen was filled with blood 
and often contained a cheesy exudate. The 
intestinal epithelium sloughed off in long 
pieces, sometimes forming a tube which 
could easily be lifted out. 

TYZZERIA ANSERIS 
NIESCHULZ, 1947 

Hosts : Domestic goose, white- 
fronted goose {Anser albifrons), blue or 



snow goose (A. caerulescens), Ross's 
goose (A. rossi), Canada goose {Bfanla 
ca)iadensis), Atlantic brant (B. bernicla 
hrola), whistling swan (Olor colunibianus), 
lesser scaup duck {Nyroca affinis). 

Location : Small intestine. 

Geographic Distribution : North 
America, Europe. 

Prevalence : This species is appar- 
ently rare in domestic geese, having been 
reported in them only by Nieschulz (1947) 
in Holland and by Farr and Wehr (1952) in 
Maryland. It is common, however, in 
wild geese, and has been found in all the 
species from which coccidia have been re- 
ported and from all 6 North American fly- 
ways (Hanson, Levine and Ivens, 1957). 
It is most likely a parasite of wild geese 
which occasionally occurs in domestic 
ones as the result of accidental contam- 
ination. 

Morphology : The oocysts were des- 
cribed by Levine (1952). They are ellip- 
soidal, 10 to 16 by 9 to 12jLL with a mean 
of about 13 by l\ [i . The oocyst wall is 
smooth, colorless, about 0.6(i thick, and 
usually appears to be composed of a sin- 
gle layer altho in some oocysts a second 
inner line is visible; this may perhaps be 
a membrane which has pulled away from 
the wall. A micropyle is absent. The 
sporozoites are banana-shaped. The 
oocyst residuum is large, irregular, gran- 
ular, and often surrounded by the sporo- 
zoites. 

Life Cycle : Unknown. 

Pathogenesis : Unknown in very 
young birds; negligible in adults. 



COCCIDiOSIS IN DUCKS AND GEESE 

Our knowledge of the coccidia of 
ducks and geese is extremely deficient. 
Except for renal coccidiosis of the goose 
caused by E. Irmicata, coccidiosis ap- 
pears to be of little importance in these 
birds, and coccidia have seldom been re- 
ported from them. A few outbreaks of 
intestinal coccidiosis have been reported, 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



245 



however, Jansen (1931), for example-, 
described one in Holland in which more 
than 10% of a flock of 700 ducks died in 2 
days. 

Treatment : Little is known of the 
treatment of coccidiosis of ducks and 
geese. McGregor (1952) reported that E. 
truiicata infections of geese seemed to 
respond to sodium sulfamethazine, and 
the urinary excretion of sulfonamides in 
general would suggest that they should be 
particularly effective against this species. 

Prevention and Control : The same 
measures should be used for the preven- 
tion and control of coccidiosis in ducks 
and geese as in chickens. 



FAMILY CRYPTOSPORIDIIDAE 

Members of this family are mono- 
xenous. Development takes place on the 
surface of the host cells or within their 
striated border, and not in the cells 
proper. The oocysts and schizonts have 
a knob-like attachment organ at some 
point on their surface. The oocysts con- 
tain no sporocysts. The microgametes 
have no flagella. There is a single genus, 
Cryptosporidium . 

Genus CRYPTOSPOMDIUM 
Tyzzer, 1907 

In this genus the oocyst contains 4 
naked sporozoites. 



CRYPTOSPORIDIUM TYZZERI 
NOM. NOV. 

Synonyms : Cryptosporidium parvum 
Tyzzer, 1912 pro parte. 

Host : Chicken. 

Location : All stages occur in the 
striated border (cuticular layer) of the 
surface epithelial cells of the tubular 
part of the ceca. 



Geographic Distribution : 
America (Massachusetts). 



North 



Prevalence : Rare. 

Morpholo gy: Tyzzer (1929) did not 
describe this form in detail, but illustrated 
it and said that it appeared morphologically 
identical with C. parriim of the mouse. 
The following description is based primar- 
ily on that given by Tyzzer (1912) for C. 
parviim. The oocyst is ovoid or spherical, 
4 to 5 by 3|i . The oocyst wall is smooth, 
composed of a single layer, with a small, 
knob-like attachment organ. A micropyle 
is absent. An oocyst residuum is present. 
The sporozoites are slender, bow- or 
boomerang-shaped, 5. 5 to 6/1 long, with 
a rod-shaped, slender nucleus near the 
anterior end. 

Life Cycle : The following description 
is based primarily on that given by Tyzzer 
(1912) for C. parvum, which is morpho- 
logically identical with C. tyzzeri. The 
schizonts are 3 to 5|i in diameter when 
mature and have an attachment organ. 
They are attached to the cell surface or 
embedded in its striated border. They 
form 8 falciform merozoites 2. 5 to 5 by 
0. 5 to 0. 7 /i , with a nucleus near the 
thicker end, and a small residual mass. 
The microgametocytes are smaller than 
the schizonts and also have an attachment 
organ. They give rise to 16 tiny micro- 
gametes and a spherical mass of residual 
material. The microgametes are chroma- 
tin rods about 1 ii long and not more than 
0.4jj, wide, without visible flagella. The 
macrogametes are larger than the schi- 
zonts and microgametocytes, and contain 
tiny, retractile granules. They have a 
thin, dense limiting membrane and an 
attachment organ. 

Pathogenesis : Apparently non-path- 
ogenic. 

Remarks : Tyzzer (1929) thought that 
this was the same species he had pre- 
viously found in mice, but he attempted 
no cross-infection experiments. He said 
that even if such experiments failed, the 
morphological agreement was such that the 
chicken and mouse forms could only be re- 
garded as biological varieties of the same 
species. However, such a narrow species 
concept is no longer held, and it seems 



246 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



best to draw attention to the chicken form 
by giving it a name of its own. Conse- 
quently it is named Cryptosporidium 
tyzzeri. 

In this connection, too, it might be 
mentioned that Tyzzer (1910) was unable 
to infect the laboratory rat with the 
closely related C. niuris from the labor- 
atory mouse. 



CRYPTOSPORIDIUM MELEAGRIDIS 
SLAVIN, 1955 



Pathogenesis : According to Slavin 
(1955), C. »ieleagridis may cause illness 
with diarrhea and a low death rate in 10- 
to 14 -day-old turkey poults. 



CRYPTOSPORIDIUM SP. 

Tyzzer (1929) remarked in passing 
that he had found a Cryptosporidium 
morphologically similar to C. parviim in 
the rabbit's intestine, but did not discuss 
it further. No one else appears to have 
recognized this form. 



Host : Domestic turkey. 

Location : All stages occur on the 
villus epithelium of the terminal third of 
the small intestine. 

Geographic Distribution : Scotland. 

Prevalence : Unknown; found in 1 
flock. 

Morphology : This species was des- 
cribed by Slavin (1955). The oocysts are 
oval, 4. 5 by 4. |i , with very foamy cyto- 
plasm and an eccentric, faint, poorly de- 
fined wisp of nucleus. No sporulated 
oocysts were seen. 

Life Cycle : The young schizonts 
(trophozoites) are attached to the epithe- 
lium of the villi, often in enormous num- 
bers. They have an attachment organ 
which penetrates the striated border of 
the epithelial cells. Slavin also saw 
these forms in the goblet cells, between 
cells as far down as the basement mem- 
brane, and in surface depressions between 
the epithelial cells. The mature schizonts 
measure 5 by 4^ and contain 8 merozoites. 
These are falciform, 5 by 1 ^i. , and taper 
toward the ends, with one end blunter than 
the other. The nucleus is subterminal. 

The microgametocytes are rounded 
or oval, 4 fi in their greatest diameter, 
and contain 16 intensely staining rod-like 
microgametes. These measure 1 by 0.3 n 
and have no flagella. The macrogametes 
are roughly oval, 4. 5 to 5. by 3. 5 to 
4.0ji. 



FAMILY AGGREGATIDAE 

Members of this family are hetero- 
xenous, with two hosts. Schizogony takes 
place in one and sporogony in the other. 
Development takes olace in the host cell 
proper. The oocysts typically contain 
many sporocysts. With one dubious ex- 
ception, the Aggregatidae are parasites of 
marine annelids, molluscs and Crustacea. 



Genus MiROCYSTlS Dalcin, 1911 

In this genus the oocysts contain num- 
erous sporocysts, each with 2 sporozoites. 
A single species, M. kathae, has been 
named. It occurs in the kidney of the 
whelk, Buccinuni undatiim. 

In addition, Paichuk (1953) described 
oocysts in the feces of several pigs in 
Kazakhstan which he called Merocystis 
sp. The oocysts are short-oval, almost 
spherical, 34 to 43 by 30 to 37 ^t with a 
mean of 38.7 by 33. Ojix. The oocyst wall 
is smooth, 2y. thick, composed of 3 layers 
of which the outer is dark brown, the mid- 
dle bright green and the inner yellow-green 
or bright brown. The oocyst wall is very 
fragile. The number of sporocysts is un- 
known, but more than 13. The sporocysts 
are spherical, 9 to 13 /i in diameter with 
a mean of 9. 1 jj, . The presence of an 
oocyst polar granule is unknown. The 
oocyst and sporocyst residua are com- 
posed of dispersed granules. The sporo- 
zoites are spherical, 4.3/i in diameter. 
Altho Paichuk assigned this form to the 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



247 



genus Merocystis, it is much more prob- 
ably Adelea or Adelina, both of which 
occur in arthropods, and it may well be a 
parasite of some arthropod which the 
pigs had eaten. 



FAMILY LANKESTERELLIDAE 

Members of this family are hetero- 
xenous, with 2 hosts. Schizogony, game- 
togony and sporogony all take place in a 
vertebrate host. The sporozoites enter 
the blood cells and are taken up by a 
blood-sucking invertebrate (a mite or 
leech). They do not develop in this host, 
but are transferred to the vertebrate host 
when the latter eats the invertebrate, or 
possibly by injection. In the vertebrate 
host, development takes place in the host 
cells proper. The oocysts contain no 
sporocysts, but have 8 or more sporo- 
zoites, the number depending on the genus. 
The microgametes have 2 flagella so far 
as is known. There are 2 genera in this 
family: Lankesterella, which occurs in 
birds and amphibia, and Schellackia, 
which occurs in reptiles. 



Genus LANKESTERELLA Labbe, 1899 

In this genus the oocysts contain 32 
or more naked sporozoites. The vectors 
are leeches or mites. 

The type species, and the only one 
known for a long time, is L. minima, 
a parasite of the frog. However, Lainson 
(1959) recently showed that the genus 
Atoxoplasma Garnham, 1950 is a synonym 
of Lankesterella, enlarging the genus con- 
siderably and clearing up a question which 
has puzzled parasitologists for years. 

The parasites now known to be sporo- 
zoites of Lankesterella are found fre- 
quently in the lymphocytes and other blood 
cells of wild birds. They had been thought 
to be Haemogregarina or Toxoplasma, but 
Garnham (1950) showed that they were 
definitely not the latter and therefore 
called them Atoxoplasma. 



The names and accepted species of 
the genus are still in a highly confused 
state (Laird, 1959; Lainson, 1959). 

Lankesterella adiei (Aragao, 1933) 
Lainson, 1959 (syns. , L. passeris Raf- 
faele, 1938; L. garnham i Lainson, 1959) 
is a common parasite of the English 
sparrow thruout the world. Lainson 
(1959) found it in all of 99 adult and 150 
fledgling English sparrows in England, 
Manwell (1941) and Manwell et al. (1945) 
reported that it was common in passerine 
birds, and D. D. Myers (unpublished) 
found it commonly in English sparrows in 
Illinois. The sporozoites occur in the 
lymphocytes and monocj^es, and often 
cause a pronounced indentation of the host 
cell nucleus. They are typically sausage- 
shaped with rounded ends, stain weakly 
and lack a well defined periplast, so that 
it is often difficult to differentiate their 
cytoplasm from that of the host cell. 
Their nucleus is diffuse and granular, 
with a tiny karyosome. They measure 4 
to 5 by 2 to 4 fi according to Lainson (1959). 

The life cycle of L. adiei was des- 
cribed (under the name L. garnliami) by 
Lainson (1959). Schizogony takes place 
in the lymphoid-macrophage cells of the 
spleen, bone marrow and liver. There 
are 2 types of schizont, one producing 10 
to 30 (average 16) oval merozoites meas- 
uring 4 by 2 (i , and the other producing a 
smaller number of larger merozoites 
measuring 6 by 3. 5|ll. Gametogony and 
sporogony take place in the lymphoid- 
macrophage cells of the liver, lungs and 
kidney. The microgametocytes resemble 
those of Eimeria and produce 60 to 100 
microgametes. The macrogametes are 
about 14. 5 /J, in diameter when mature and 
produce a large but unspecified number of 
sporozoites measuring about 3.6 by 1.8)i. 
The vector is presumably the common red 
mite, Dermanyssus gallinae, but Lainson 
was unable to prove this because he had 
no uninfected receptor birds. 

According to Lainson (1958), Lanke- 
sterella may cause congestion and hemor- 
rhage of the blood vessels and inflamma- 



248 



THE TELOSPORASHDA AND THE COCCIDLA PROPER 



tory foci in the liver and lungs of infected 
English sparrows. Manwell (1941) stated 
that infections seemed to spread rapidly 
among adult English sparrows from New 
York after they had been captured and 
kept in relatively close quarters in the 
laboratory. He found that the disease was 
not infrequently fatal, but that chronic 
cases also occurred. The liver and spleen 
were greatly enlarged and very dark in one 
bird which he necropsied, but there were 
no hematin granules in either organ. 
D. D. Myers (unpublished) also observed 
deaths from this infection in captured 
English sparrows in Illinois. 

Lankesterella serini Lainson, 1959 
was discovered in canaries when Lainson 
wanted to infect them with L. adici from 
the English sparrow and found that they 
already had an infection of their own. It 
apparently resembles L. acUci. Nothing 
is known about its pathogenicity. Perhaps 
the "x-bodies" or "Einschliisse" which 
occur in the macrophages of the lungs, 
liver and spleen of canaries (Manwell 
eL al. , 1945) belong to this species. 



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Natt, M. P. 1959. Exp. Parasit. 8:182-187. 



2S2 



THE TELOSPORASIDA AND THE COCCIDIA PROPER 



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THE TELOSPORASIDA AND THE COCCIDIA PROPER 



253 



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Chapter 9 



These genera belong to the suborder 
Adeleorina, which is differentiated from 
the Eimeriorina and Haemospororina by 
the fact that the macrogamete and micro- 
gametocyte are associated in syzygy 
(i.e. , they lie up against each other) dur- 
ing development. Correlated with this is 
the fact that the microgametocytes pro- 
duce very few microgametes. The zygote 
may or may not be motile, and the sporo- 
zoites are enclosed in an envelope. 

The great majority of the Adeleorina 
are parasites of lower vertebrates and in- 
vertebrates, but a few occur in domestic 
and laboratory animals. 



KLOSSIBUA 

Am 

HEPATOZOOU 



FAMILY KLOSSIELLIDAE 

In this family, the zygote is not mo- 
tile. A typical oocyst is not formed, but 
a number of sporocysts each containing 
many sporozoites develop within a mem- 
brane which is perhaps laid down by the 
host cell. Each microgametocyte forms 
2 to 4 non-flagellated microgametes. The 
life cycle involves a single host, game- 
togony and schizogony occurring in differ- 
ent locations. There is a single genus, 
Klossiella. 



Genus Ki.OSS\mi\ Smith and 
Johnson, 190:2 

This genus has the characters of the 
family. 

Infection takes place by ingestion of 
sporulated sporocysts, and the sporozoites 
pass into the blood stream and enter the 
endothelial cells of the capillaries and 
arterioles of the kidneys, lungs, spleen 
and other organs. Here they turn into 
schizonts, and these then produce mero- 
zoites. There are probably several 
asexual generations. 

Eventually some merozoites enter the 
epithelial cells of the convoluted tubules 



- 254 



KLOSSIELLA AND HEPATOZOON 



255 



of the kidney, where they become gamonts 
and where gametogony and sporogony take 
place. A macrogamete and microgameto- 
cyte are found together in syzygy within a 
vacuole in the host cell. The microgame- 
tocyte divides to form 2 to 4 microgam- 
etes, one of which fertilizes the macro- 
gamete. The resultant zygote (sporont or 
mother sporoblast) divides by multiple 
fission to form a number of sporoblasts. 
Each of these develops into a sporocyst 
containing 8 to 25 or more sporozoites. 
The sporocysts are enclosed within a 
membrane, but all authorities do not agree 
whether it is a true oocyst or simply the 
remnant of the host cell. 

The sporocysts are released into the 
lumen of the kidney tubules by rupture of 
the host cell, and pass out in the urine. 



KLOSSIELLA EQUI 
BAUMANN, 1946 

Synonym: Einieria utinensls (?). 

Hosts: Horse, ass. 



Location: Kidneys. 

Geographic Distribution : 
Turkey, North America. 



Europe, 



Prevalence : Unknown. This species 
has been encountered only in the course of 
histopathologic examinations of the kidney 
for some other reason. Baumann (1946) 
found it in the kidney of a horse from 
Hungary which had died of pneumonia, 
Seibold and Thorson (1955) found it in the 
kidney of a jackass in Alabama which had 
died of spinal injuries incurred while he 
was being roped. Akcay and Urman(1954) 
found it on histopathologic examination of 
the kidneys of 72 out of 117 donkeys in the 
course of an experiment on infectious 
anemia. 

Morphology : The stages in the kidney 
are the only ones known. These are found 
in the epithelial cells lining the thick 
limbs of Henle's loops in the medullary 
rays. Schizonts and merozoites have not 
been recognized. The macrogametes and 



microgametocytes develop in syzygy. The 
latter form 4 microgametes (Baumann, 
1946). After fertilization, the zygote 
grows to 38 to 46 by 32 to 39 \i and pro- 
duces a large number of sporoblasts by 
multiple nuclear fission followed by bud- 
ding from a large, central residual mass. 
Each sporoblast develops into a sporocyst. 
The fully developed "oocysts" are thin- 
walled sacs 50 to 90 by 35 /i containing as 
many as 40 ovoid sporocysts measuring 
8 to 10 by 4 to 5 (i . Each sporocyst con- 
tains 8 to 12 sporozoites. Seibold and 
Thorson (1955) found 40 sporocysts in a 
cross section of one of the largest sacs 
they saw, so there must have been many 
more actually present. 

Pathogenesis : Apparently non-patho- 
genic. 

Remarks : Pachinger (1886) des- 
cribed parasites resembling EiDieria fal- 
ciformis in the kidneys of 3 horses. These 
were almost certainly K. equi. Selan and 
Vittorio (1924) described a parasite from 
the lungs and gall bladder of a horse in 
Italy which they called Eimeria utinensis. 
Their description was too poor to be sure 
what they actually saw, but it may perhaps 
have been a stage of K. equi. 



OTHER SPECIES OF KLOSSIELLA 

Klossiella muris Smith and Johnson, 
1902 is apparently fairly common in lab- 
oratory mice thruout the world, but has 
been reported only once in wild house 
mice. In the laboratory colonies in which 
it is found, 20 to 100% of the mice are in- 
fected. Each microgametocyte forms 2 
microgametes. Each sporont forms 12 to 
16 sporocysts, each of which contains 
about 25 to 34 banana-shaped sporozoites. 
K. muris is ordinarily non-pathogenic, 
altho in heavy infections the kidneys may 
have minute, greyish, necrotic foci over 
their entire surface, and the epithelium 
of the infected kidney tubules is destroyed 
(Smith and Johnson, 1902). Otto (1957) 
described a perivascular, follicular, 
lymphocytic infiltration in the region of 
the medullary cortex which he considered 
of diagnostic significance. There is no 



256 



KLOSSIELLA AND HEPATOZOON 



inflammatory reaction. No fatal infec- 
tions have been reported. 

Klossiella cobayae Seidelin, 1914 
occurs sporadically in the guinea pig 
thruout the world. Each microgametocyte 
forms 2 microgametes. Each sporont 
forms 30 or more sporocysts, each of 
which contains about 30 sporozoites. K. 
cobayae is apparently non-pathogenic and 
produces slight if any pathologic changes 
in the kidney. However, it may be en- 
countered in sections of the kidney or 
other organs which are being examined 
for something else, as C. C. Morrill and 
I (unpublished) did in some guinea pigs at 
the University of Illinois. 



FAMILY HEPATOZOIDAE 

In this family the zygote is active (an 
ookinete), secreting a flexible membrane 
which is stretched during development. 
The life cycle involves 2 hosts, 1 of which 
is vertebrate and the other invertebrate. 
The parasites are found in the cells of 
the circulatory system of vertebrates and 
of the digestive system of invertebrates. 
The oocysts are large and contain many 
sporocysts, each with 4 to 12 or more 
sporozoites. There is a single genus, 
Hepatozoon. 



Genus HfPATOZOON Miller, 1908 

In this genus schizogony takes place 
in the viscera of a vertebrate, and the 
gametocytes are either in the leucocytes 
or erythrocytes, depending on the species. 
Fertilization and sporogony occur in a 
tick, mite, louse, tsetse fly, mosquito or 
other blood-sucking invertebrate, de- 
pending again on the species. The micro- 
gametocyte forms 2 microgametes. A 
synonym of this generic name is Leucocy- 
togregarina . 

Species of Hepatozoon have been 
described from mammals, reptiles and 
birds. They ai-e especially common in 
rodents. 

The vertebrate hosts become infected 
by eating the invertebrate hosts. The 



sporozoites are released in the intestine, 
penetrate its wall and pass via the blood 
stream to the liver, lungs, spleen or bone 
marrow; different species prefer different 
organs. The sporozoites enter the tissue 
cells and become schizonts, which divide 
by multiple fission to produce a number of 
merozoites. There are several asexual 
generations in the visceral cells, but their 
number is known in only a few cases. The 
last generation merozoites enter the blood 
cells and become gamonts. These look 
alike; presumably the female is a macro- 
gamete and the male a microgametocyte, 
but no evidence is available on this point. 

No further development takes place 
until the parasites reach the alimentary 
tract of the intermediate host. The ga- 
monts then leave their host cells, asso- 
ciate in syzygy, and the microgametocyte 
forms 2 non-flagellate microgametes. 
These are relatively large, but smaller 
than macrogametes. One of them ferti- 
lizes the macrogamete, and the resultant 
ookinete penetrates the intestinal wall and 
comes to lie in the haemocoel. Here it 
grows considerably and becomes an oocyst. 
Several nuclear divisions take place in the 
sporont within the oocyst wall. The daugh- 
ter nuclei migrate to its periphery, and 
each one buds off to form a sporoblast, 
leaving a large residual mass. The sporo- 
blasts then form a wall around themselves, 
becoming sporocysts. Sporozoites develop 
in the sporocysts, their number depending 
on the species. When the vertebrate host 
ingests the invertebrate one, the oocysts 
and sporocysts rupture in its intestine, 
releasing the sporozoites. 

It is possible that trans-placental in- 
fection may also occur, at least in some 
species. At any rate, Clark (1958) found 
a full-blown infection with H. i^riseisciuri 
in a 36-hour-oId grey squirrel which had 
been born in a mite-free environment. 



HEPATOZOON CAMS 
(JAMES, 1905) 

Synonyms : Leucocylozoon cauls, 
Hac'Diogyegarina caiiis, Haeniogregarina 
yolundata, HacDiogregariiia chatloiii, 
Hepatozoon felis . 



KLOSSIELLA AND HEPATOZOON 



2S7 



Disease: Hepatozoonosis. 

Hosts : Dog, cat, jackal, hyena and 
palm civet or musang {Payadoxurns 
herniaphroditns). The forms described 
from the cat, jackal and hyena under the 
names H. felis, H. rotitndata and H. 
cliai/oni. respectively, are practically 
indistinguishable morphologically, and 
are probably all the same species. Laird 
(1959) believed that the form he found in 
the palm civet in Malaya was H. caiiis. 

Location: The schizonts are in the 
spleen, bone marrow and to a lesser ex- 
tent in the liver. The gamonts are in the 
polymorphonuclear leucocytes. 

Geographic Distribution : India, 
Malaya, Singapore, Indochina, Central 
Africa, North Africa, Middle East, Italy. 
This species is well known in dogs, but 
has been reported from cats only by 
Patton (1908) in Madras (Laird, 1959). 

Morphology: The gamonts in the 
leucocytes are elongate rectangular bodies 
with rounded ends measuring about 8 to 12 
by 3 to 6|_L, and with a central, compact 
nucleus. Their cytoplasm stains pale blue 
and their nucleus dark reddish with 
Giemsa stain. They are surrounded by a 
delicate capsule. They may emerge from 
the leucocytes and capsule and lie free in 
citrated blood. Leitao (1945) saw schi- 
zonts in the circulating blood which he 
said were difficult to distinguish from 
platelets. 

Life Cycle : The life cycle of H. 
canis was worked out by Christophers 
(1906, 1907, 1912) and Wenyon (1911). 
Schizogony takes place in the spleen and 
bone marrow, and Rau (1925) saw it in the 
liver also. There are several types of 
schizonts. One type produces a small 
number (usually 3) of large merozoites, 
another type produces a large number of 
small merozoites, and intermediate types 
produce merozoites of intermediate num- 
bers and size. The small merozoites are 
the ones which enter the leucocytes to 
form gamonts. 

The vector is the brown dog tick, 
Rhipiceplialus sanguineus . Both the 



nymph and adult can transmit the infection, 
but there is no transovarian transmission. 
The oocysts are found in the haemocoel. 
They are about 100 fi in longest diameter 
and contain 30 to 50 sporocysts 15 to 16/1 
long, each containing about 16 banana- 
shaped sporozoites and a residual body. 
Dogs become infected by eating infected 
ticks. 

Pathogenesis : H. canis has often 
been found in apparently healthy dogs, but 
it may also cause serious disease and 
death (Rau, 1925; Rahimuddin, 1942). 
The principal signs are irregular fever, 
progressive emaciation, anemia and 
splenomegaly. Lumbar paralysis has 
also been reported. Affected dogs may 
die in 4 to 8 weeks. 

Diagnosis : Hepatozoonosis can be 
diagnosed by identifying the gamonts in 
stained blood smears or in stained smears 
of spleen pulp, bone marrow or liver. 

Treatment: Unknown. 



Prevention and Control : Since//. 
canis is transmitted by the brown dog 
tick, elimination of ticks will eliminate 
the disease. 



OTHER SPECIES OF HEPATOZOON 

Hepatozoon niuris (Balfour, 1905) 
occurs in the wild and laboratory Norway 
rat and black rat thruout the world. 
Schizogony takes place in the parenchymal 
cells of the liver, and the gamonts are 
found in the monocytes and rarely in the 
polymorphonuclear leucocytes. The vector 
is the spiny rat mite, Ecltinolaelaps 
echidninus. Massive infections may cause 
marked degenerative changes in the liver 
and death, but little or no effect has been 
observed in lightly infected wild rats. 

Hepatozoo)! nnisculi (Porter, 1908) 
was reported from the white mouse in 
England. It differs from H. niuris in that 
schizogony takes place only in the bone 
marrow. 

Hepatozoon cuniculi (Sangiorgi, 1914) 
was reported from the domestic rabbit in 



258 



KLOSSIELLA AND HEPATOZOON 



Italy. Its gamonts are found in the leu- 
cocytes and its schizonts in the spleen. 

Hepalozoon griseisciuri Clark, 1958 
is common in the grey squirrel {Scittrus 
carolincnsis) in the United States. Clark 
(1958) described its life cycle. Schizogony 
takes place in the spleen, liver and bone 
marrow, and the gamonts are found in the 
monocytes. The natural vector is the 
mite, Euhaetnogmnasus ambidans, but 
Echinolaelaps echidninus can act as a 
vector experimentally. 



LITERATURE CITED 

Akjay, S. and H. K. Urmon. 1954. Deut. Tierarztl. 
Wchnschr. 61:393. 



Boumann, R. 1946. Wien. Tierarztl. Monatschr. 33:257- 260. 
Chriaophers, S. R. 1906. Sci. Mem. Off. Med. G San. 

Dep. Govt. India, N. S. 26:1-16. 
Christophers, S. R. 1907. Sci. Mem. Off. Med. G Son. 

Dep. Govt. India, N. S. 28:1-11. 
Christophers, S. R. 1912. Parasit. 5:37-48. 
Clarl<, G. M. 1958. J. Parasit. 44:52-63. 
Laird, M. 1959. J. Protozool. 6:316-319. 
Leieao, S. 1945. An. Inst. Med. Trop. 2:217-226. 
Otto, H. 1957. Frankfurt. Ztschr. Path. 68:41-48. 
Pachinger, A. 1886. Zool. Anz. 9:471-472. 
Patton, W. S. 1908. In Ann. Rep. Bact. Sec. King Inst. 

Protect. Med., Guindy, 1907, Madras, (cited by 

Laird, 1959) 
Rahimuddin, M. 1942. Ind. Vet. ]. 19:153-154. 
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Seibold, H. R. and R. E. Thorson. 1955. J. Parasit. 

41:285-288. 
Solan, U. and A. Vittorio. 1924. Clin. Vet. 47:587-592. 
Smith, T. and H." P. Johnson. 1902. J. Exp. Med. 6:303- 316. 
Wenyon, C. M. 1911. Parasit. 4:273-344. 



These genera belong to the suborder 
Haemospororina, which is differentiated 
from the Eimeriorina and Adeleorina by 
the facts that the microgametocyte pro- 
duces a moderate number of microgametes 
and the sporozoites are naked. The gam- 
onts are similar and develop independently. 
The zygote is motile (i.e. , it is an ookinete). 
All species are heteroxenous; schizogony 
takes place in a vertebrate host, and spor- 
ogony in an invertebrate. If the erythro- 
cytes are invaded, pigment (hemozoin) is 
formed from the host cell hemoglobin. 

This suborder was customarily div- 
ided into 2 families, the Plasmodiidae 
containing the genus Plasmodium, and the 
Haemoproteidae containing the genera 
Haenioprotens and Leiicocytozoon. The 
principal difference was that in the Plas- 
modiidae schizogony was thought to take 
place only in the erythrocytes, while in 
the Haemoproteidae it takes place in the 
lungs, liver, spleen, kidneys and other 
internal organs. However, when the com- 
plete life cycles of several species of 
avian and human Plas)}io(lium were worked 
out (Huff and Coulston, 1944, 1946; Shortt 
and Garnham, 1948; Short et al. , 1951; 
Garnham, 1954; Bray, 1957), it was real- 
ized that schizogony may occur both within 
the erythrocytes and exoerythrocytically. 
The distinction between the two families 
is thus an artificial one, and there is no 
point in retaining more than a single fam- 
ily in the suborder. 

It is likely, as Manwell (1955) has 
suggested, that the Haemospororina may 
well have arisen from the coccidia of ver- 
tebrates rather than from those of insects, 
as had been more commonly supposed. 
Genera like Lankesterella and Schellackla, 
in which schizogony, gametogony and 
sporogony all take place in the vertebrate 
host and in which the sporozoites invade 
the blood cells and are transmitted by 
mites or other blood-suckers, could well 
be the starting-point for the transition 
from the Eimeriorina to the Haemospor- 
orina. 



'■4^^ MAiS, 



KY ]^| 



Chapter 10 



PLASMODIUM 
HAEMOPROTEUS 

AND 
LEUCOCYTOZOON 



- 259 



260 



PLASMODHJM, HAEMOPROTEUS AND LEUCOCYTOZOON 



FAMILY PLASMODIIDAE 

This family has the characters of the 
suborder. Its taxonomy has been reviewed 
by Garnhan (1953) and Bray (1957). These 
authors preferred to split the classical 
genus Plasniodtion into several genera, 
based on the life cycles of their species, 
but it is simpler not to do so. 

Genus PLASMODIUM Marchiafava 
and Celli, 1885 

The gametocytes occur in the erythro- 
cytes. Schizogony takes place in the ery- 
throcytes and also in various other tis- 
sues, depending on the species. The exo- 
erythrocytic ("e.e.") schizonts are solid 
or, at the most, vacuolated bodies. Mem- 
bers of this genus are parasites of mam- 
mals, birds and lizards. They are trans- 
mitted by mosquitoes. Anopheles trans- 
mitting the mammalian species, and 
culicines or sometimes Anopheles the 
avian and reptilian ones. 

Members of this genus cause malaria, 
which is still the most important disease 
of man. They also cause a similar dis- 
ease in birds. Coatney and Roudabush 
(1949) have cataloged the species of Plas- 
modium, and other species are discussed 
by Bray (1957). Man has 4 species, higher 
apes 4, lower apes and lemurs 7, rodents 
2, and bats 1. Birds have 14 or 15 valid 
species (Hewitt, 1940; Bray, 1957; Laird 
and Lari, 1958). 

Life Cycle : The life cycle of Plas- 
modluin vivaxoi man is representative. 
The sporozoites enter the blood thru a 
mosquito bite. They stay in the blood less 
than an hour, quickly entering liver par- 
enchymal cells. Here they become schi- 
zonts (known as cryptozoites from their 
location), which enlarge and divide by 
multiple fission to form metacryptozoites 
(a type of merozoite). These enter new 
liver parenchymal cells, undergo multiple 
fission, and form new metacryptozoites. 
This process may go on indefinitely in P. 
vivax, but in another human species, P. 
falciparnni , there is only a single genera- 
tion of metacryptozoites. 



The metacryptozoites break out of the 
liver cells, pass into the blood stream and 
enter the erythrocytes about a week to 10 
days after infection. Here they round up 
and develop a large vacuole in their cen- 
ter. They are called ring stages because 
in Romanowsky stained smears they re- 
semble a signet ring, with a red nucleus 
at one edge and a thin ring of blue cyto- 
plasm around the vacuole. These grow 
and are now called schizonts or tropho- 
zoites. 

The trophozoites were formerly 
thought to obtain their nutriment sapro- 
zoically, but Rudzinska and Trager (1957) 
showed in an electron microscope study 
of P. lophurae of the duck that they are 
holozoic as well. They form food vacuoles 
containing host cell cytoplasm by invagina- 
tion. The hematin pigment granules are 
formed within these food vacuoles by di- 
gestion of the hemoglobin. This study, 
incidentally, settled once and for all the 
question which is raised perennially as to 
whether Plasmodium occurs within or on 
the surface of the host cell; it is within it. 

The trophozoites undergo schizogony 
to produce merozoites, the number depend- 
ing on the species. These break out of the 
erythrocytes, enter new ones, and repeat 
the cycle indefinitely. 

The length of each cycle depends on 
the parasite species. It is 2 days in P. 
vivax and P. falciparum, and 3 days in 
another human species, P. malariae. 
Practically all the parasites are generally 
in the same stage of the cycle at the same 
time, so all the merozoites break out of 
the red cells and pass into the blood at the 
same time. Along with them go the hema- 
tin granules and other waste products pro- 
duced by the parasites' metabolism. These 
are toxic, and cause a violent reaction or 
paroxysm in the host- -the chills and fever 
characteristic of malaria. 

After the infection has been present 
for some time and after an indefinite num- 
ber of asexual generations, some mero- 
zoites entering the erythrocytes develop 
into macrogametes and others develop into 
microgametocytes. The former are 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



261 



customarily called macrogametocytes, 
but this name is incorrect since they are 
haploid from the start (see below). They 
remain in this stage until the blood is in- 
gested by a mosquito. 

In the stomach of the mosquito, micro- 
gametes are produced. The changes in the 
microgametocytes are striking. Within 10 
to 15 minutes the nucleus divides, and 6 
to 8 long, heavy flagellum-like micro- 
gametes are extruded. This process is 
known as exflagellation. The microgam- 
etes break off and swim freely until they 
find a macrogamete. Fertilization takes 
place, and a motile zygote (ookinete) is 
formed. 

The ookinete penetrates into the stom- 
ach wall and grows into an oocyst, which 
forms a ball 50 to 60 /i in diameter on the 
outer surface of the stomach. The oocyst 
nucleus divides repeatedly and a number 
of sporoblasts are formed. The nucleus 
of each sporoblast then divides repeatedly, 
and eventually each oocyst comes to con- 
tain 10,000 or more slender, spindle- 
shaped sporozoites about 15/i long with a 
nucleus in the center. These break out of 
the oocyst into the body cavity and migrate 
to the salivary glands. They are then in- 
jected into a new host when the mosquito 
bites again. The process of sporozoite 
development takes 10 days to 3 weeks or 
longer, depending on the species of Plas- 
modin))i, the species of mosquito and the 
temperature. 

Once infected, a mosquito remains 
infected for life, and can transmit the 
parasites every time it bites. There is a 
case on record (James, 1927) of a mos- 
quito which lived from August 5 to Novem- 
ber 16 and infected more than 40 general 
paresis patients as part of their therapy. 

In vivax and malariae malaria, re- 
lapses are common and may occur for a 
number of years after the individual has 
had his first attack. Between attacks the 
parasites are ordinarily not found in the 
blood. What apparently happens is that 
all the parasites do not leave the liver 
when the metacryptozoites emerge into the 
blood stream, but a few remain there and 



continue to multiply in secret until such 
time as the body's defenses have decreased 
sufficiently so that the parasites can again 
invade the blood. 

There are several variations of the 
above general pattern. In P. falciparimi 
of man, there is only a single generation 
of metacryptozoites in the liver, and re- 
lapses rarely occur. In addition, the 
schizonts and merozoites of this species 
are rarely seen in the peripheral blood. 
Instead, the infected red cells become 
viscid and clump together in the internal 
organs. 

In the avian species, exoerythrocytic 
schizogony does not take place in the liver 
parenchyma, but either in the endothelial 
cells (P. gallinaceiiiii . P. relictum, P. 
catlienieriuDi, P. lophnrae. P. fallax, P. 
circitiii/lexiiiii, P. diirae, P. juxtaimcleare, 
P. hexameriitm) or largely in the haenio- 
poietic cells (P. elo)2gatiau , P. vanghaiii 
and probably P. Imffi and P. rouxi). 

In bird malaria also, but not in mam- 
malian malaria, some of the merozoites 
which have been formed in the erythrocytes 
are able to enter the tissue cells and de- 
velop exoerythrocytically. They are known 
as phanerozoites, but they do not differ 
morphologically from the forms derived 
from sporozoites. 

Plas))todiuiii is haploid thruout its life 
cycle except for a brief period following 
fertilization and zygote formation. In a 
cytologic study of the early oocysts of 7 
species of Plasmodium in mosquitoes, 
Bano (1959) found that the oocysts undergo 
meiosis 2 to 3 days after the infective blood 
meal, the time depending on the species. 
For P. vivax it was 48 hours, for P. gal- 
linaceiDii 53 to 55 hours, and for P. inui 
72 to 79 hours. After that, division is by 
mitosis. 

The haploid number of chromosomes 
is 2 for P. falciparum, P. malariae, P. 
ovale, P. lophurae, P. relictum, P. 
floridense (Wolcott, 1955, 1957), P. vivax, 
P. kiioivlesi, P. berghei (Wolcott, 1955, 
1957; Bano, 1959), and P. gallinaceum 
(Bano, 1959); it is 3 for P. gonderi and 



262 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



4 for P. cynoniolgi and P. inui (Bano, 
1959). 

Cultivation : Various species of 
Plasniodiiun have been cultivated in fluid 
media (Trager, 1947; Anfinsen el al. , 
1946; Geiman el al. , 1946) and in avian 
embryos and tissue culture (see Pipkin 
and Jensen, 1958 for a review). 



HUMAN MALARIA 

The following discussion of human 
malaria is necessarily brief. Further 
details and references can be found in any 
textbook of human parasitology and, in 
more detail, in Boyd (1949) and Mac- 
donald (1957). 

Man has 4 recognized species of 
Plasmodium . P. falciparum (Welch, 
1897) Schaudinn, 1902 is the cause of ma- 
lignant tertian, aestivo-autumnal or fal- 
ciparum malaria. Paroxysms of chills 
and fever occur every other day (i. e. , on 
days 1 and 3, which accounts for the name 
"tertian"). The ring forms are about 
1/6 to 1/5 the diameter of a red blood 
cell. The schizonts and merozoites 
("segmenters") rarely occur in the peri- 
pheral circulation, but are found in 
clumped erythrocytes in the viscera. The 
schizonts are usually compact and 
rounded, with coarse, blackish pigment. 
The segmenters occupy 2/3 to 3/4 of the 
host cell and form 8 to 32 merozoites. 
The host erythrocyte is not enlarged but 
contains reddish clefts known as Maurer's 
dots and may also have bluish stippling. 
The macrogametes and microgametocytes 
are crescent- or bean-shaped, with pig- 
ment granules clustered around a central 
nucleus or scattered except at the poles. 
The microgametocytes have pale blue cyto- 
plasm and a relatively large, pink nucleus 
when stained with Giemsa's stain. The 
macrogametes have darker blue cytoplasm 
and a more compact, red nucleus. 

Plasmodium fif ax (Grass i and Feletti, 
1890) Labbe', 1899 is the cause of benign 
tertian or vivax malaria. Paroxysms 



occur every other day as in falciparum 
malaria. The ring forms are about 1 '3 to 
1/2 the diameter of the host cell. The 
schizonts are highly active and sprawled 
out irregularly over the host cell, with 
small, brown pigment granules usually 
collected in a single mass. The host cell 
is enlarged, pale, and contains red dots 
known as Schuffner's dots. The segment- 
ers nearly fill the host cell and produce 
15 to 20 or occasionally up to 32 irregu- 
larly arranged merozoites. The macro- 
gametes and microgametocytes are 
rounded, 10 to 14fi in diameter (i. e. , 
larger than normal erythrocytes), and have 
fine, brown, evenly distributed pigment 
granules. The microgametocytes have 
pale blue cytoplasm and a relatively large, 
pink nucleus when stained with Giemsa's 
stain. The macrogametes are slightly 
larger, with darker blue cytoplasm and a 
small, red nucleus. 

Plasmodimn malariae (Laveran, 1881) 
Grassi and Feletti, 1890 is the cause of 
quartan or malariae malaria. This species 
also occurs naturally in chimpanzees in 
West Africa (Garnham, 1958). Paroxysms 
occur every 3 days (i. e. , on days 1 and 4). 
The ring forms are similar to those of P. 
vivax. The schizonts are more compact 
and rounded or are drawn out in a band 
across the host cell; their pigment gran- 
ules are blacker and coarser than those of 
P. vivax. The host cell is not enlarged 
and does not contain Schuffner's dots. The 
segmenters nearly fill the host cell and 
produce 6 to 12 (usually 8 or 9) merozoites 
arranged in a rosette. The macrogametes 
and microgametocytes are rounded and 
smaller than those of P. vivax. They do 
not quite fill the host cell and contain 
blacker and coarser pigment granules. 

Plasmodium ovale Stephens, 1922 is 
a rare species which causes a tertian type 
of malaria. Its ring forms are similar to 
those of P. vivax. The schizonts are 
usually round, with brownish, coarse, 
somewhat scattered pigment granules. The 
host cell is oval, often fimbriated, not 
much enlarged, and contains Schuffner's 
dots. The segmenters occupy 3/4 of the 
host cell and produce 8 to 10 merozoites 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



263 



in a grape-like cluster. The macrogametes 
and microgametocytes are rounded, occupy 
3/4 of the host cell and have coarse, black 
evenly distributed pigment granules. 

A vivax-type Plasmodium, P. cyno- 
molgi, occurs in macaques. Eyles, Coat- 
ney and Getz (1960) recently described 
accidental laboratory infections of 2 hu- 
mans with P. c. bastianellii originally 
isolated from Macaca iriis from Malaya. 
They were able to infect 2 other humans 
experimentally by allowing them to be 
bitten by infected Anopheles freeborni 
mosquitoes. This finding and the presence 
of P. malariae in chimpanzees suggest 
that more than one of the human malarias 
may be zoonoses. 

Pathogenesis : The malarial paroxysm 
is highly characteristic. It begins with a 
severe chill. The patient shivers uncon- 
trollably, his teeth chatter, and he has 
gooseflesh, altho his temperature is actu- 
ally above normal. The chill is followed 
by a burning fever, headache and sweating. 
This gradually subsides, the temperature 
falls, and after 6 to 10 hours the patient 
feels much better--UDtil his next paroxysm. 
The destruction of erythrocytes causes 
anemia. 

After a certain number of paroxysms, 
the attack of malaria subsides. Relapses 
may occur over a period of years in vivax 
and malariae malaria, but this is rarely 
the case in falciparum malaria. 

In general, mortality from malaria is 
higher in children than in adults in endemic 
areas, because by the time the people be- 
come adult they have had repeated attacks, 
and those who have survived have devel- 
oped a good deal of immunity. For this 
reason, if one wants to determine the in- 
cidence of malaria in an area, it is better 
to examine children than adults. 

A highly fatal, cerebral form of ma- 
laria may occur in falciparum infections. 
It is due to clogging of the capillaries of 
the brain by agglutinated, infected ery- 
throcytes. If enough clogging takes place 
in the viscera, a severe gastro-intestinal 
disease resembling typhoid, cholera or 



dysentery may occur. Another complica- 
tion of falciparum malaria is blackwater 
fever, which gets its name from the color 
of the urine. There is tremendous des- 
truction of the erythrocytes- -60 to 80% 
may be destroyed in 24 hours--accompanied 
by fever, intense jaundice and hemoglobi- 
nuria. Severe attacks are usually fatal. 
The cause of blackwater fever is not known, 
but it may involve some sort of immuno- 
logical reaction which hemolyzes the ery- 
throcytes. 

Epidemiology : Malaria is transmitted 
by Anopheles mosquitoes. There are about 
200 species of this genus, but not all are 
equally good vectors, and the epidemiology 
of the disease in any particular locality 
depends not only upon the terrain and cli- 
matic conditions, but also upon the partic- 
ular vectors present, their breeding habits, 
food preferences, susceptibility to infec- 
tion, etc. The subject is an extremely 
complex one and cannot be discussed in de- 
tail here. Three examples will suffice. 

The principal malaria vector in south- 
eastern United States is Anopheles quadri- 
maculatus . This species breeds best in 
clean, open water with dense aquatic veg- 
etation and abundant flotage. It prefers 
bovine to human blood, however, so that 
the ratio of livestock to men in an area is 
an important factor in the transmission 
rate. 

The principal malaria vector in the 
Solomon Islands is Anopheles farauti. It 
breeds in small ponds and puddles. During 
the Guadalcanal campaign of World War U, 
the profusion of shell holes, fox holes, 
road ruts, etc. provided ideal conditions 
for its propagation, and the result was an 
explosive outbreak of malaria. It was con- 
trolled by eliminating or draining the breed- 
ing places or spraying them with fuel oil. 

These measures would not work in the 
Philippines, where the principal vector is 
Anopheles minimus flavirostris. This 
species breeds at the edges of slow-moving 
streams in the plains, hence quite different 
measures, such as stream clearing, 
straightening and flushing, must be used 
to prevent its breeding. 



264 



PLASMODRTM, HAEMOPROTEUS AND LEUCOCYTOZOON 



Malaria is primarily a disease of 
warmer climates nowadays, but at one 
time it was common in the temperate zone. 
Nevertheless, malaria is still the most 
important human disease from a global 
standpoint. Of the 1955 world population 
of 2, 653 million, 1070 million lived in 
malarious areas, and 696 million of these 
were protected poorly or not at all from 
malaria. In 1955 there were still 200 to 
225 million cases of malaria in the world, 
with more than 2 million deaths (Diehl, 
1955). 

Malaria control has eliminated or al- 
most eliminated malaria from many parts 
of the world (Pampana and Russell, 1955; 
Russell, 1956, 1958; Anonymous, 1956), 
largely by use of residual spraying with 
DDT and other insecticides. At the end 
of World War II there were about 4 million 
cases of malaria a year in southern Europe 
from Spain to Bulgaria. In 1956 there 
were less than 10,000 cases in the same 
area. 

Malaria was one of the causes of the 
decline of the Roman empire. The swampy 
land of the Roman Campagna made it al- 
most uninhabitable because of the disease. 
There were 411, 602 cases of malaria in 
Italy in 1945. Systematic spraying with 
DDT was begun in 1946, and as a result 
only 12 cases of indigenous malaria (both 
primary cases and relapses) were reported 
in 1953. In 1955 there were only 3. 

During World War I, the British and 
French landed armies at Salonika, Greece, 
with the objective of driving into Germany 
thru the back door. Malaria wrecked 
their plans and immobilized their armies. 
There were 2 million cases of malaria in 
Greece in 1942. In 1950 there were 
50,000, and in 1952 only 408. 

In the Eastern Mediterranean coun- 
tries, with a population of about 170 mil- 
lion, there were about 40 million cases of 
malaria a year in 1949. There are now 
about 14 million, and it has been shown 
that it is technically possible to eliminate 
malaria from the area. 

Malaria has been completely elimina- 
ted from Sardinia and Sicily, and it is 



practically gone from Venezuela, Brazil, 
British Guiana, Argentina, Cyprus, Ceylon 
and parts of India, to mention a few of the 
places. 

In the United States there were a mil- 
lion cases of malaria a year among a pop- 
ulation of 25 million in 12 southern states 
during 1912 to 1915. Before that, malaria 
was an important disease thruout the mid- 
west. Ackerknecht (1945) has given its 
history in that region from 1760 to 1900. 
The decrease of malaria in this country 
was due only in small part to measures 
aimed directly at the disease, but more to 
agricultural development and to other, 
still unknown, factors. It was almost en- 
tirely eliminated from the midwest, for 
instance, by farm land drainage. 

After World War II an intensive cam- 
paign was started to wipe out malaria from 
this country. Residual spraying of dwell- 
ings, outhouses, barns, etc. was practiced 
in malarious areas. Mosquito larval con- 
trol measures were intensified. An attempt 
was made to follow up every case diagnosed 
as malaria, to get a blood smear in order 
to be sure that it actually was malaria, and 
to treat it immediately in order to prevent 
it from being a source of further cases. 

During 1949 less than 5000 cases were 
reported in the U. S. During 1955, 477 
cases were reported. Of these, 64 were 
appraised by the U. S. Public Health Serv- 
ice, and only 29 were confirmed by blood 
smear as malaria. Only 4 were primary 
indigenous cases. Two were in California, 
1 in Arizona, and the fourth--acquired by 
blood transfusion--in Illinois. In 1957, 
157 cases were reported, of which 138 
were appraised by the Public Health Serv- 
ice; 102 were confirmed, and 11 of these 
were primary indigeiious cases (Dunn and 
Brody, 1959). In 1958, 94 cases were re- 
ported, of which 61 were confirmed. Seven 
of these were primary indigenous cases, 4 
of them resulting from blood transfusions, 
and 1 natural case each originating in Cal- 
ifornia, Arizona and possibly Pennsylvania 
(Brody and Dunn, 1959). 

One outbreak of malaria illustrates 
what can happen if conditions are right 
(Brunetti, Fritz and Hollister, 1954). It 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



265 



occurred at a Campfire Girl camp at 
Lake Vera, California. A marine visited 
the camp on July 4, 1952, and spent the' 
night. He had a malarial relapse while he 
was there, and was sleeping without a 
mosquito bar. Within a few weeks the 
first case appeared among the girls, and 
cases continued to appear until January or 
February. A total of 35 cases of vivax 
malaria occurred among that group of 
girls as the result of one night's exposure 
from one infected marine. 

There are no obvious technical or 
economic reasons why malaria could not 
be eradicated from the Americas, Europe, 
Australia and much of Asia during the 
next quarter century, altho the situation is 
not so promising in tropical Africa (Wil- 
liams, 1958). This can be done almost 
entirely by residual spraying of dwellings. 
The cost of protection has been found to 
vary from 11 to 45 cents per capita per 
year. Properly conducted, residual house 
spraying for 2 to 3 years will eradicate 
Plasmodium , altho the mosquito vector 
may persist. Some mosquitoes have de- 
veloped a resistance to DDT, but this has 
always taken at least 6 years, so malaria 
can be eliminated before the mosquitoes 
become resistant. 

New problems result from disease 
control, however. These are well illus- 
trated by the effect of malaria control on 
the population of Ceylon. The birth rate 
on that island was 40 per 1000 in 1920, 
and it was still about the same in 1950. 
But the death rate in 1920 was 32 per 
1000, while in 1950 it was 12 per 1000, 
and this decrease was due primarily to 
the elimination of malaria. This means 
that if both the present birth and death 
rates are maintained, the population of 
Ceylon will double in about 26 years. And 
how can all these additional millions be 
fed? (Stone, 1954). 

Diagnosis : Malaria can be diagnosed 
with certainty only by finding and identify- 
ing the causative organisms in the blood. 
This is done by microscopic examination 
of smears stained with one of the Roman- 
owsky stains; Giemsa's stain is best. At 
one time thin smears were used almost 



entirely, but thick, laked smears are much 
better, since they permit a much larger 
amount of blood to be examined in a given 
time. Identification of the species and 
stages requires skill and practice. An ex- 
cellent guide with outstanding colored illus- 
trations is that of Wilcox (1960). 

Treatment : A number of drugs have 
been used in treating malaria. The first 
one was quinine, the most active ingredi- 
ent of cinchona bark, which was identified 
in 1820 by Pelletier and Caventou. It is 
both suppressive and curative, but does 
not prevent relapses. Chemically it is 
6-methoxy-alpha-(5-vinyl-2-quinuclidyl-4- 
quinoline-methanol). 

Quinacrine (Atebrin, Atabrine, mepa- 
crine) was discovered by Mauss and 
Mietsch (1933) in Germany. It is 2-chloro- 
5-diethylamino-isopentylamino-7-methoxy- 
acridine dihydrochloride. It was used ex- 
tensively during World War II when the 
Indonesian cinchona plantations were taken 
over by the Japanese. It is actually better 
than quinine. It is prophylactic against 
falciparum malaria and suppressive 
against vivax and malariae malarias. It 
cures attacks of the disease, but does not 
prevent relapses. One disadvantage is 
that it is a dye and stains the skin yellow. 

Chloroquine (Aralen) is 7-chloro-4, 
4-dimethylamino-l-methylbutylaminoquin- 
oline. It was developed thru a crash drug- 
testing program during World War II in 
which the Americans tested over 14,000 
compounds and the British about half as 
many. The results of the American effort 
are summarized by Wiselogle (1946). 
Chloroquine appeared too late to be used 
in that war except experimentally. It is 
the most effective drug known for the treat- 
ment and suppression of all types of ma- 
laria. The recommended therapeutic dose 
is 1. 5 g in 3 days. Following its use, fever 
subsides in a day, and the parasites dis- 
appear from the blood in 2 or 3 days. The 
suppressive dose is 0. 3 g weekly. Chlor- 
oquine does not prevent vivax malaria re- 
lapses, however. 

Primaquine appeared even later than 
chloroquine, having been introduced in 



266 



PLASMODIUM, RAEMOPROTEUS AND LEUCOCYTOZOON 



1949. It is 8-(4-amino-l-methylbutyl- 
amino)-6-methoxyquinoline. It is most 
useful as a truly curative agent against 
vivax malaria, since it not only cures 
attacks but prevents relapses. It is best 
used in combination with chloroquine if 
the patient is having an attack, but can be 
used alone in between relapses to prevent 
further relapses. The dosage is 15 mg 
daily for 14 days. The effectiveness of 
this drug in preventing relapses was 
proven in returning Korean veterans. 

Chlorguanide (Paludrine, Proguanil) 
was developed by the British during 
World War H. It is N-p-chlorophenyl-N- 
5-isopropylbiguanide. It showed a great 
deal of promise, but after it had been 
used for a while, resistant strains of 
Plasmodium appeared, and it is no longer 
being used. 

Pyrimethamine (Daraprim, Malocide) 
was introduced by the British in 1951. Its 
discovery grew out of the World War 11 
study. It is 2,4-diamino-5-p-chlorophenyl- 
6-ethylpyrimidine. It is perhaps the best 
suppressive drug known, altho it is not 
recommended for the treatment of malarial 
attacks. In single weekly doses of 25 mg 
it completely suppresses all Plasmodium 
species and is prophylactic against P. 
falciparum and some strains of P. vivax. 
In addition, it destroys P. falciparum 
gametocytes, so that it has value in the 
epidemiological control of this type of 
malaria. It is being mixed with the salt 
for prophylaxis in some parts of the 
Americas. Unfortunately, resistant 
strains have appeared in some areas 
where it has been used, and its eventual 
value is uncertain. 

Many other drugs have been used for 
treating malaria, but these are the most 
important. At present, the ones gener- 
ally recommended are chloroquine, prima- 
quine and pyrimethamine. 



BIRD MAiARIA 

A tremendous amount of work has 
been done on the bird malarias. The 
avian species of Plasmodium lend them- 



selves well to experimentation, and, until 
the discovery of P. bergliei in rodents in 
1948, birds were the only experimental 
animals in which malaria could be conven- 
iently studied. All the drug screening for 
antimalarials in World War II was carried 
out in birds (Wiselogle, 1946). 

About 40 species of Plas»wdii(i)i have 
been described from birds, but only 14 or 
15 are accepted as valid (Hewitt, 1940; 
Bray, 1957; Laird and Lari, 1958). Many 
wild birds are commonly infected. The 
most complete general review of bird 
malaria is that of Hewitt (1940), altho it is 
now somewhat out of date. Herman (1944) 
and Coatney and Roudabush (1949) have 
given catalogs and host-indices of the spe- 
cies of Plasmodium in birds. Levine and 
Hanson (1953) tabulated reports of Plas- 
modium from waterfowl, and Levine and 
Kantor (1959) did the same for birds of 
the order Columbiformes. Other more 
recent general papers are those of Becker 
(1959), Bray (1957), Herman et al. (1954), 
Huff (1954) and Wolfson (1941). 

Bird malaria is not of great veterinary 
importance, but it may occasionally cause 
losses, especially in pigeons. Most of the 
species are not strongly host specific and 
can infect several species of birds. Most 
laboratory studies have been carried out 
with Plasmodium cathemerium and P. 
relictum in the canary, P. gallinaceum in 
the chicken and P. lophurae in the duck. 

The avian species of Plasmodium fall 
into 2 groups, depending upon whether 
their gametocytes are round or elongate. 
Among those with round gametocytes are 
P. cathei)ieriu»i, P. relictum and P- gal- 
linaceum. Among those with elongate 
gametocytes are P. circumflexum , P. 
micleophilum , P. rouxi, P. elongatum, 
P. hexamerium, P. vaughani and P. 
polare. P. lophurae is somewhat different; 
its gametocytes are elongate at first but 
continue to grow and come to fill up the 
whole host cell except for the nucleus. 

Cutting across these morphological 
groups are the two groups based on the 
type of cell invaded by the exoerythrocytic 
forms mentioned on page 261. 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



267 



PLASMODIUM GALLINACEUM 
BRUMPT, 1945 

Disease : Chicken malaria. 

Hosts : Chicken. 

Crawford (1945) thought that jungle 
fowls are the natural hosts of P. gallina- 
cemn. These are Gallus lafayetti in 
Ceylon, G. sonnerati in Sumatra and G. 
bankiva in India. Brumpt (1936), how- 
ever, thought that the natural, wild host 
is still unknown. Jungle fowls are rela- 
tively resistant, but outbreaks of disease 
occur in domestic chickens introduced 
into areas where the parasite is endemic 
in wild birds. 

Pheasants, partridges, peacocks and 
geese have been infected experimentally, 
but the duck, guinea fowl, pigeon, turtle 
dove, quail, buzzard, canary, English 
sparrow, Java sparrow {Padda oryzivora) 
and finch are resistant (Brumpt, 1936). 

Location : Erythrocytes. The exo- 
erythrocytic stages are in endothelial 
cells. 

Geographic Distribution : Southern 
Asia, Indonesia. P. gallinaceuni was first 
seen by Crawford in Ceylon and named by 
Brumpt (1935) from material sent to him 
from Indochina. It has also been found in 
India (Rao, Das and Ramnani, 1951; Das, 
Rao and Ramnani, 1952) and Java, Suma- 
tra and Celebes (Kraneveld and Mansjoer, 
1953). It was reported from Egypt by 
Haiba (1948), but this record requires 
confirmation. 

Morphology : The gametocytes and 
schizonts are round or irregular. The 
host cell nucleus is displaced but seldom 
expelled. The pigment granules in the 
gemetocytes are rather large and not very 
numerous. The schizonts produce 8 to 30 
merozoites. 

Life Cycle : The life cycle is similar 
to that of other Plasmodium species. The 
exo-erythrocytic stages in the endothelial 
or reticulo -endothelial cells of the spleen, 
brain, liver, etc. have been described by 



James and Tate (1937, 1938), James (1939) 
and Huff and Coulston (1944). The natural 
vectors are unknown, but various mosqui- 
toes, including Aedes aegypti, A. albo- 
pictus, A. geniculatus and Culex quinque- 
fasciatiis, are potential vectors (Brumpt, 
1936, 1936a; Vargas and Beltran, 1941). 
Huff (1954) listed 29 susceptible and 1 
questionable species of which 19 are 
Aedes, 5 Armigeres, 2 (possibly 3) Culex, 
1 Anopheles , 1 Culiseta and 1 Mansonia. 

Pathogenesis : P. gallinaceuni causes 
a serious disease with a high mortality 
rate in domestic chickens. The body tem- 
perature fluctuates, and anemia and splen- 
omegaly are present. The birds may be- 
come paralyzed and die due to blocking of 
the brain capillaries by the exoerythrocytic 
stages. 

Remarks : Beltran (1941, 1943a) and 
Crawford (1945) reviewed the history of 
research on this species. Because it lends 
itself well to experimental study and be- 
cause the chicken is such an excellent lab- 
oratory animal, hundreds of papers have 
been written on it--according to Brumpt 
(1949), more than 600 between 1935 and 
1948. 



PLASMODIUM JUXTANUCLEARE 
VERSIANI AND GOMES, 1941 

Disease : Chicken malaria. 

Hosts : Chicken. Versiani and Gomes 
(1941) infected 1 of 3 turkeys experiment- 
ally, but were unable to infect the duck, 
guinea fowl, pigeon, canary, domestic 
sparrow, tico tico, or 3 other species of 
wild birds. 

Location : Erythrocytes. The exo- 
erythrocytic stages are in endothelial cells. 

Geographic Distribution : South Amer- 
ica (Brazil), Mexico. 

Morphology : This species has been 
described from Minas Gerais, Brazil by 
Versiani and Gomes (1941, 1943) and from 
Chiapas, Mexico by Beltran (1941a, 1943). 
The gametocytes and schizonts are round 



268 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



or irregular, relatively small, and usually 
in contact with the red cell nucleus. The 
schizonts produce 3 to 7 (usually 4) mero- 
zoites. The host cell is often distorted. 

Life Cycle : The life cycle has not 
been completely studied. According to 
Beltran (1943), schizogony takes about 24 
hours and its synchronicity is low. The 
prepatent period may vary from 2 to 38 
days. Paraense (1947) saw exoerythro- 
cytic stages in the endothelial cells. Culex 
qiiinqiiefasciatus was found to be a suit- 
able experimental vector by Paraense 
(1944), but Aedes aegypti and A. lepidus 
are not. 



are elongate, at the end or side of the host 
cell, and often displace the host cell nucleus 
when oriented obliquely to it. This tendency 
to take an oblique position differentiates P. 
diirae from other avian species of Plas- 
modium. The pigment granules are usually 
large, round and black. The host cell is 
not enlarged. The trophozoites are more 
or less amoeboid. Presegmenters are 
often at the end of the host cell. The mature 
schizonts rarely displace the host cell nu- 
cleus. The pigment granules are round, 
black, up to 8 in number, and tend to be- 
come clumped together in the mature schi- 
zonts. Six to 14 (usually 8) merozoites 
are formed. The host cell is not distorted. 



Pathogenesis : This species is highly 
pathogenic. The Brazilian strain killed 
75% of the infected young birds and 68% 
of the adults in 15 days to 9 months, and 
the Mexican strain killed 12 of 13 birds in 
1 to 8 months. Affected birds do not show 
any marked signs. Shortly before death 
they appear listless and weak, with pale 
combs. Their temperature is not eleva- 
ted. There are deposits of pigment in the 
liver and spleen. Versiani and Gomes 
(1943) observed a large amount of peri- 
cardial fluid, but Beltran (1943) did not. 



PLASMODIUM DURAE 
HERMAN, 1941 

Disease : Turkey malaria. 

Hosts : Turkey. Purchase (1942) 
produced a transient infection in baby 
chicks. Simpson (1944) infected ducks of 
various ages. This is probably a natural 
parasite of some as yet unknown wild 
African bird. 

Location : Erythrocytes. The exo- 
erythrocytic stages are in endothelial cells. 

Geographic Distribution : Africa 
(Kenya). 

Prevalence : Herman (1941) found P. 
durae in 1 of 75 domestic turkeys in Kenya. 

Morphology : This species was des- 
cribed by Herman (1941). The gametocytes 



Life Cycle : Purchase (1942) and 
Simpson (1944) found exoerythrocytic 
stages of P. durae in the endothelial cells 
of the spleen, liver, lungs and brain of 
turkeys. The prepatent period is 3 days 
to 2. 5 weeks after intravenous injection and 
12 days to 40 days after intramuscular in- 
jection (Herman, 1941). Schizogony in the 
erjTthrocytes apparently takes 24 hours. 
The vectors are unknown (Huff, 1954). 

Pathogenesis : P. durae causes an 
acute, often fatal disease in turkeys less 
than a year old. Twelve out of 14 young 
poults infected by Purchase (1942) died. 
They showed some malaise and ruffled 
feathers, but usually died without any acute 
signs. Two naturally affected adult birds 
showed signs of cerebral involvement, 
emaciation, edema of the legs and high 
blood pressure. 

At necropsy of acute cases (Purchase, 
1942) the liver, spleen and kidneys are dark 
and congested, the lungs slightly edematous, 
and the pericardial cavity contains an excess 
of clear fluid. The lumen of the duodenal 
loop is light chocolate in color and its villi 
are heavily laden with pigment. There is 
injection of the superficial vessels of the 
brain and meninges. 

In chronic, naturally infected birds, 
the spleen is reduced in size, hard and 
fibrous, the liver is firm, with chronic 
congestion and much fibrosis. The villi of 
the duodenal loop are packed with large 
pigment granules. 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



269 



PLASMODIUM RELICTUM 
(GRASSI AND FELETTI, 1891) 

Synonyms : Plasmodium praecox 
Grassi and Feletti, 1890. (Bray, 1957 
considered the correct specific name to 
be praecox, but he continued to use re- 
lictum. ) 

Disease : Pigeon malaria. 

Hosts : Pigeon, mourning dove, pin- 
tail, cinnamon teal, falcated duck, black 
swan, and various passerine and other 
wild birds. This species was first des- 
cribed from the English sparrow. Exper- 
imental infections have been studied in the 
canary, duck, chicken and other birds. 

Location : Erythrocytes. The exo- 
erythrocytic stages are in endothelial cells. 

Geographic Distribution : Worldwide. 

Prevalence : This species is common 
in wild passerine birds. It occurs occa- 
sionally in domestic pigeons, having been 
found in them by Sergent and Sergent 
(1904) in Algeria, Coatney (1938) in Ne- 
braska, Herman et al. (1954), Mathey 
(1955) and Graue (cited by Levi, 1957) in 
California, Becker, Hollander and Pat- 
tillo (1956) in Iowa, Pelaez et al. (1951) 
in Mexico, Cassamagnaghi (1950) in 
Uruguay, Haiba (1946, 1948) in Egypt, and 
Rousselot (1943) in the French Sudan. 

Morphology : The gametocytes and 
schizonts are round or irregular. The 
host cell nucleus is displaced and often 
expelled by the larger forms. The pig- 
ment granules of the gametocytes are rel- 
atively fine and dot-like. The schizonts 
produce 8 to 32 merozoites, the number 
depending on the particular strain. 

Life Cycle : The life cycle of this 
species has been studied extensively 
(Bray, 1957). The exoerythrocytic stages 
occur in the endothelial cells. The asex- 
ual cycle has been reported to take from 
12 to 36 hours in different strains; some 
have a very high and others a low degree 
of synchronicity (Hewitt, 1940). Many 
species of mosquitoes can act as vectors. 



Huff (1954) listed 12 of Culex, 4 of Ano- 
pheles, 3 of Aedes and 2 of Culiseta, and 
remarked that 93% of the species which had 
been tested had been found susceptible. 

Pathogenesis : P. relic turn is highly 
pathogenic for the pigeon but less so for 
the mourning dove and canary. Affected 
squabs become weak and anemic, with en- 
larged and heavily pigmented spleens and 
livers. Pigment may also be deposited in 
the fat. Hill (1942) showed that anemia is 
the principal cause of death. 



PLASMODIUM CIRCUMFLEXUM 
KIKUTH, 1931 

Hosts : This species is quite common 
in a wide variety of hosts. The type host 
is a German thrush, Tiirdus pilaris. It 
was found in the ruffed grouse in Canada by 
Fallis (1945, 1946), and a similar form was 
found in the Canada goose in Illinois by 
Levine and Hanson (1953). 

Location: Erythrocytes. The exo- 
erythrocytic stages are in endothelial cells. 

Morphology : The gametocytes and 
trophozoites are elongate; they tend to en- 
circle the host cell nucleus but are gener- 
ally not in contact with it and do not displace 
it. The schizonts produce 13 to 30 mero- 
zoites (average 19). 

Life Cycle : The life cycle is similar 
to that of other avian species of Plasmodium. 
Exoerythrocytic stages occur in the endo- 
thelial cells. The known vector mosquitoes 
are Culex tarsalis, Culiseta annulata and 
C. melaneura. Two other species of Culex 
and 5 of Aedes have been found insuscepti- 
ble (Huff, 1954). 



PLASMODIUM CATHEMERIUM 
HARTMAN, 1927 

Disease: Canary malaria. 

Hosts: This species was first found 
in the English sparrow. It is common in 
passerine birds and has also been found in 
canaries. 



270 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



Location : Erythrocytes. The exo- 
erythrocytic stages are in endothelial cells. 

Morphology : The gametoc3^es and 
schizonts are more or less round, dis- 
placing and often expelling the host cell 
nucleus. The pigment granules in the 
gametocytes are coarse, often elongate 
and rod-like. The schizonts produce 6 to 
24 merozoites. 



Life Cycle : The life cycle of this 
species has been studied extensively (Bray, 
1957). It is similar to that of other avian 
species of Plasniudiuni. Exoerythrocytic 
stages occur in the endothelial cells. The 
asexual cycle takes 24 hours, and syn- 
chronicity is high. Huff (1954) listed 8 
species of Culex, 3 each of Aedes and 



Anopheles and 1 of Psorophora which can 
act as vectors. However, he remarked 
that only 46% of the mosquito species 
which had been tested were susceptible. 

Pathogenesis : P. cathemerimn 
causes a highly fatal disease in canaries. 
Herman and Vail (1942) reported it in a 
canary in California, and Mathey (1955a) 
described an outbreak in a canary breeding 
establishment in that state in which pos- 
sibly 165 out of 700 birds died. 

Affected canaries have subcutaneous 
hemorrhages, anemia, splenomegaly and 
hepatomegaly. Mathey (1955a) described 
swelling in the region of the eyes. Hewitt 
(1939) found splenic infarcts in 47% of his 
experimentally infected canaries. 





Fig. 32. Avian Plasmodium and Haemoproteus in erythrocytes. A. Plasmodium gal- 

linaceum young trophozoite (ring stage). B. P. galliiiacciim older trophozoite. 
C. P. galliiKiceuiii mature trophozoite (segmenter). D. P. gatlimicfum mac- 
rogamete. E. P. gallinaceum microgametocyte. F. P. reliclum mature 
trophozoite (segmenter). G. P. relictu»i macrogamete. H. Haemoproteus 
colitmbae macrogamete. X 2800. (Original) 



BIRD MALARIA 

Diagnosis : Bird malaria can be diag- 
nosed by finding and identifying the proto- 
zoa in stained blood smears. If schizonts 
or merozoites are present, it is easy to 
differentiate Plasmodium from Haemo- 
proteus, since these stages are not found 
in the peripheral blood in the latter. How- 
ever, if elongate gametocytes alone are 
found, differentiation is usually not possible. 



Treatment : The bird malarias res- 
pond to treatment with quinacrine, chloro- 
quine and other antimalarial drugs. Indeed, 
these were discovered by screening against 
bird malarias. Chloroquine at the rate of 
5 mg per kg, chlorguanide at 7. 5 mg per 
kg and pyrimethamine at 0. 3 mg per kg 
protect chickens against P. gallinaceum 
infections. However, as a practical matter. 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



271 



treatment is usually hardly worthwhile, 
and preventive measures are recommended 
instead. 

Prevention and Control : Since bird 
malaria is carried by mosquitoes, pre- 
vention depends upon mosquito control. 
Residual spraying of poultry houses with 
insecticides such as DDT or lindane should 
be effective. Birds can also be raised in 
screened quarters where mosquitoes can- 
not get to them. 



Genus HAEMOPROTEUS Kruse, 1 890 

The gametocytes occur in the ery- 
throcytes and are usually halter- shaped. 
Schizogony takes place in the endothelial 
cells of the blood vessels, especially in 
the lungs, and not in the erythrocytes. 
The known vectors are louse -flies (Hippo- 
boscidae) and midges {CuUcoides). Mem- 
bers of this genus are parasites of birds 
and reptiles. A synonym of this generic 
name is Halteridium Labbe", 1894. 

Members of this genus are extremely 
common in wild birds and also occur in 
domestic pigeons, ducks and turkeys. 
They are not an important cause of disease. 
Coatney (1936) gave a checklist and host 
index of the species of Haemoproteus , and 
Herman (1944) listed the species reported 
from North American birds. 

Life Cycle : The life cycle of Haemo- 
proteus is similar to that of Plasmodium 
except that schizogony does not take place 
in the erythrocytes but in the endothelial 
cells of the blood vessels, and the vectors 
are not mosquitoes but hippoboscid flies 
or midges. 



HAEMOPROTEUS COLUMBAE 
KRUSE, 1890 

Synonyms : Haemoproteus maccal- 
lumi, Haemoproteus melopeliae, Haemo- 
proteus turtur, Haemoproteus vilhenai (?). 

Hosts : Domestic and wild pigeons, 
mourning dove, turtle dove and a large 
number of other wild columbiform birds. 



Levine and Kantor (1959) tabulated reports 
of Haemoproteus, all of which were prob- 
ably H. columbae, from 45 species belong- 
ing to 19 genera of columbiform birds. 

H. maccallumi was first described 
from the mourning dove {Zenaidura 
macroura). It is morphologically indis- 
tinguishable from H. columbae. Huff 
(1932) transmitted it from the mourning 
dove to the pigeon, but Coatney (1933) was 
unable to transmit it from the pigeon to 
the mourning dove; both used the hippo- 
boscid fly, Pseudolynchia canariensis, 
as the vector. There may be strain dif- 
ferences between the different hosts, but 
until greater differences than these are 
brought out, it is probably better to use 
the name H. columbae for the species 
from columbiform birds. 

Location : The gametocytes are in 
the erythrocytes. Schizogony occurs in 
the endothelial cells of the blood vessels. 

Geographic Distribution : Worldwide. 

Prevalence : Common. Thirty-eight 
reports of H. columbae from the domestic 
pigeon were tabulated by Levine and Kan- 
tor (1959). Among those in which rela- 
tively large numbers of birds were ex- 
amined, Coatney (1935) found it in all of 
about 28 pigeons in midwestern United 
States, Kartman (1949) found it in 82% of 
101 pigeons in the Honolulu zoo, Giovannoni 
(1946) found it in 58% of 159 pigeons in 
southern Curitiba, Brazil, Acton and 
Knowles (1914) found it in all of 75 pigeons 
from the plains of India, and Singh, Nair 
and David (1951) found it in 22% of 214 pig- 
eons in Delhi, India. 

Herman (1938) found it in 8% of 86 
mourning doves {Zenaidura macroura car- 
olinensis) on Cape Cod, Massachusetts, 
Huff (1939) found it in 47% of 188 mourning 
doves, mostly from Illinois, Couch (1952) 
found it in 56% of 213 mourning doves in 
Texas, and Hanson et al. (1957) found it in 
30% of 392 immature and 43% of 72 adult 
mourning doves in Illinois; its incidence 
in this last survey increased steadily from 
7 to 8% in very young doves to 70% in the 
oldest immatures, and varied markedly in 



272 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



different parts of the state and in different 
years. Wood and Herman (1943) found it 
in 93't of 27 western mourning doves in 
Arizona and California. 

Morphology : The only stages found 
in the peripheral blood are macrogametes 
and microgametocytes. When mature, 
these are elongate and sausage -shaped. 
They partially encircle the host cell nu- 
cleus; they may displace it to some extent, 
but they do not push it to the edge of the 
host cell. They contain a variable number 
of dark brown pigment granules. The host 
cell is not enlarged. 

When stained with a Romanowsky 
stain, the cytoplasm of the microgameto- 
cytes is pale blue or almost colorless and 
their nuclei are pale pink and diffuse, 
while the cytoplasm of the macrogametes 
is darker blue and their nuclei are com- 
pact and dark pink or red. 

Life Cycle : The life cycle of H. co- 
lumbae has been studied by Aragao (1908), 
Adie (1915, 1924) and Huff (1942) among 
others. Birds become infected when bit- 
ten by the dipteran vector. The sporo- 
zoites enter the blood stream and invade 
the endothelial cells of the blood vessels 
of the lungs, liver and spleen. Here they 
round up to form schizonts. Each schi- 
zont undergoes multiple fission to form 
15 or more small, unpigmented bodies, 
the cytomeres, each with a single nucleus. 
Each cytomere grows still further, and 
its nucleus undergoes multiple fission. 
Finally, the host cell becomes considerably 
hypertrophied and is filled with a number 
of multinucleate cytomeres. 

The endothelial cells break down, re- 
leasing the cytomeres. These vary in 
size, but may reach 60 ^ in diameter. 
They accumulate in the capillaries, which 
they sometimes block completely. They 
are irregularly shaped and tortuous, and 
may send out branches along the capillar- 
ies, becoming bifurcate, trifurcate or 
even multiradiate. Each cytomere pro- 
duces an enormous number of merozoites, 
which break out and pass into the blood 
stream. 



According to Wenyon (1926), the schi- 
zonts do not necessarily form cytomeres 
but may produce merozoites directly. 
Presumably, too, schizogony is repeated 
a number of times. 

Following schizogony, the merozoites 
enter red blood cells and become macro- 
gametes and microgametocytes. These 
first appear 28 to 30 days after infection. 
At first they resemble ring stages of Plas- 
modiuDi, but grow to the mature, elongate 
form in a few days. Multiple infections of 
erythrocytes with immature parasites are 
not uncommon, sometimes as many as 12 
being found in a single host cell, but in- 
fections with more than 1 mature gamete 
or gametocyte are rare. 

The only proven vector is the hippo- 
boscid fly, Pseudolynchia canariensis 
(syns. , Lynchia maura, L. lividicolor, 
L. capensis). In addition, Arag'ao (1916) 
stated that Alicrolyiichia pus ilia is a vector 
in South America, but gave no experimental 
evidence. Baker (1957) found that H. co- 
limibae from the English wood pigeon 
(Coluniba palumbus) would undergo sporo- 
gony in Ornithomyia aviciilaria, but 6 
attempts to infect domestic pigeons by bite 
or injection of infected louse-flies failed. 

It is highly unlikely that hippoboscids 
are the only vectors of this species, how- 
ever. As Hanson et al. (1957) pointed out, 
hippoboscids are extremely rare on mourn- 
ing doves, yet H. colinnbae is common in 
them. The discovery by Fallis and Wood 
(1957) that biting midges (Ciilicoides) are 
the vectors of H. nettionis of ducks sug- 
gests that they may also transmit H. 
columbae . 

In the stomach of the hippoboscid vec- 
tor, the microgametocytes produce 4 or 
more snake-like microgametes by exfla- 
gellation. They fertilize the macroga- 
metes, and the resultant zygotes are ookin- 
etes which crawl to the midgut wall and 
form oocysts on its outer surface. These 
grow, reaching a diameter of about 36 j^. 
They become mature in 10 to 12 days, pro- 
ducing very large numbers of slender, fal- 
ciform sporozoites up to 10 ^ long and 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



273 



similar to those of Plasmodium. These 
break out of the oocysts into the body cav- 
ity and pass to the salivary glands, where 
they accumulate and are injected into a 
new host when the fly bites it. 

Pathogenesis : U. columbae is only 
slightly pathogenic. Infected birds usually 
show no signs of disease. In relatively 
heavy infections the birds may appear 
restless and go off feed, and anemia may 
result from destruction of erythrocytes, 
but this is unusual. The liver and spleen 
of affected birds may be enlarged and dark 
with pigment. 



HAEMOPROTEUS SACHAROVI 
NOVY AND MacNEAL, 1904 

Hosts : Domestic pigeon, mourning 
dove (Zenaidiira macroura), turtle dove 
{Streptopelia turtiir). This species is 
primarily a parasite of wild doves which 
may also infect pigeons. 

Location : Gametocytes in erythro- 
cytes. Schizogony in endothelial cells of 
blood vessels. 



Geographic Distribution : 
America, Europe (Italy). 



North 



Prevalence : H. sacliarovi is common 
in mourning doves. Levine and Kantor 
(1959) tabulated 12 reports from this host 
from coast to coast in the United States. 
Among those studies in which relatively 
large numbers of birds were examined, 
Herman (1938) found it in 7% of 86 mourn- 
ing doves on Cape Cod, Massachusetts, 
Huff (1939) found it in 56% of 188 mourning 
doves, mostly from Illinois, Coatney and 
West (1940) found it in 67% of 18 mourning 
doves in Nebraska, Couch (1952) found it 
in 27% of 213 mourning doves in Texas, 
Wood and Herman (1943) found it in 41% of 
27 western mourning doves in Arizona and 
California, and Hanson et al. (1957) found 
it in 58% of 392 immature and 43% of 72 
adult mourning doves in Illinois. In this 
last study, its incidence was 31% in very 
young doves and 52% to 69% in older birds. 
Its incidence varied markedly in different 
parts of the state and in different years. 



H. sacliarovi was found in 22% of 50 
domestic pigeons in Nebraska by Coatney 
and West (1940) and in 15% of 20 domestic 
pigeons in Iowa by Becker, Hollander and 
Pattillo (1956). 

Morphology : The macrogametes and 
microgametocytes are found in the erythro- 
cytes. They differ from those of most 
species of Haemoproteus in that when ma- 
ture they completely fill the host cell, en- 
larging and distorting it, and often pushing 
the host cell nucleus to the edge of the cell. 
In addition, they contain very little pig- 
ment. When stained with a Romanowsky 
stain, the microgametocytes have pale blue 
to almost colorless cytoplasm and a light 
pink, diffuse nucleus, while the macroga- 
metes have dark blue cytoplasm and a 
dark pink to red, compact nucleus. 

The young gametocytes are ring-forms, 
and all stages between these and mature 
gametocytes can be found in the blood. 

Life Cycle : Huff (1932) transmitted 
U. sacliarovi from the mourning dove to 
the pigeon by means of the hippoboscid fly, 
Pseiidolyncliia canariensis. However, the 
natural vectors of this protozoon are still 
unknown. In view of its high incidence in 
mourning doves and the extreme rarity of 
hippoboscid flies on these birds, the nat- 
ural vector must be some other ectopara- 
site, possibly Culicoides. 

Pathogenesis : H. sacliarovi is only 
slightly if at all pathogenic in the mourning 
dove. Becker, Hollander and Pattillo (1956) 
considered that it caused the enlarged, pur- 
plish livers which they encountered in 
dressing domestic pigeon squabs from an 
infected flock; there was apparently no 
other evidence of disease. 



HAEMOPROTEUS NETTIONIS 
(JOHNSTON AND CLELAND, 1909) 
COATNEY, 1936 

Synonyms : Haemoproteus anatis, 
Haemoproteus liermani. 

Hosts : Domestic duck, domestic 
white Chinese goose, and over 23 species 



274 



PIASMODIUM. HAEMOPROTEUS AND LEUCOCYTOZOON 



of wild ducks, geese and swans, including 
the Canada goose, whistling swan, wood 
duck, pintail, green-winged teal, Aus- 
tralian teal, blue-winged teal, mallard, 
black duck, white-winged duck, cotton teal, 
Australian sheldrake, wattle duck, shov- 
eller, Baer's pochard, ring-necked duck, 
white-eyed duck, rufous -crested duck, 
baldpate, common goldeneye, surf scoter, 
old squaw and common merganser (Levine 
and Hanson, 1953; Herman, 1954; Fallis 
and Wood, 1957). 



infected birds is 14 to 21 days. Schizogony 
has not been described, and the details of 
sporogony in the midge are still to be 
worked out. Fallis and Wood found ooki- 
netes in the midge stomach 36 hours after 
ingestion; they found structures which they 
regarded as oocysts on the stomach wall, 
and other structures which they regarded 
as sporozoites in the salivary glands. 

Pathogenesis : H. nettionis is only 
slightly if at all pathogenic. 



Location : The gametocytes are in 
the erythrocytes. Schizogony occurs in 
the endothelial cells of the blood vessels. 



HAEMOPROTEUS MELEAGRIDIS 
N. SP. 



Geographic Distribution: Worldwide. 



Hosts : Domestic and wild turkey. 



Prevalence : Common. This species 
is a parasite of wild waterfowl which may 
infect domestic ducks in heavily endemic 
regions. 

Morphology : Only the sexual stages 
are found in the red blood cells. Except 
early in an infection, young stages are 
absent or rare. The mature macroga- 
metes and microgametocytes are elongate 
and sausage-shaped, partially (or some- 
times completely) encircling the host cell 
nucleus, often displacing it. There is fre- 
quently a narrow band of cytoplasm be- 
tween the parasite and the host cell nucleus, 
Free macrogametes and microgametocytes 
may occasionally be found; these are usu- 
ally round. The macrogametes and micro- 
gametocytes contain a few to 30 or more 
(usually 12 to 24) pigment granules which 
are usually coarse and round and tend to 
be grouped at the ends of the cell. The 
host cell is not enlarged. 

When stained with a Romanowsky 
stain, the cytoplasm of the microgameto- 
cytes is pale blue or almost colorless and 
their nuclei are pale pink and diffuse, 
while the cytoplasm of the macrogametes 
is darker blue and their nuclei are com- 
pact and dark pink or red. 

Life Cycle : The vector of H. nettionis 
was first discovered by Fallis and Wood 
(1957). It is the biting midge, Cidicoides. 
The prepatent period in experimentally 



Location : The gametocytes are in 
the erythrocytes. 

Geographic Distribution : North 
America. 

Prevalence : Uncommon. Haemo- 
proteus sp. was reported from 1 out of 4 
domestic turkeys in the District of Colum- 
bia and vicinity by Wetmore (1941), from 
a turkey poult from Texas by Morehouse 
(1945), from 5 of 97 eastern wild turkeys 
(of which 4 had been reared in captivity) 
in Pennsylvania by Kozicky (1948), from a 
flock of turkeys in North Dakota by Goldsby 
(1951), from 3 out of 10 turkeys in South 
Carolina by Atchley (1951), from 1 out of 
2 wild turkeys in Georgia by Love, Wilkin 
and Goodwin (1953) and from 42% of 52 
birds in a flock of domestic turkeys in 
South Carolina by Bierer, Vickers and 
Thomas (1959). 

Morphology : Only Morehouse (1945) 
described the macrogametes and micro- 
gametocytes. They are elongate, sausage- 
shaped, curve around the host cell nucleus 
and occupy about 1 2 to 3 4 of the host cell. 
Their surface is usually in close contact 
both with the host cell nucleus and host cell 
wall. The macrogametes measure 14 to 
19 by 2 to 4 ^ with a mean of 17 by 3 fi . 
They contain 18 to 48 (mean, 27) round or 
irregular pigment granules. Their nuclei 
measure 2 to 6 by 2 to 3 fx with a mean of 
4 by 2(i and are ovoid or irregular in shape. 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



275 



The microgametocytes stain less intensely 
than the macrogametes. They measure 
13 to 18 by 3 to 4 pi with a mean of 16 by 
3|U. They contain 11 to 24 (mean, 18) pig- 
ment granules. Their nuclei measure 5 
to 10 by 2 to 4 jj. with a mean of 8 by 3 ji . 
The host cells are not enlarged. More- 
house also observed occasional extracellu- 
lar macrogametes. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. 

Remarks : Altho Haemoproteiis is 
relatively rare in turkeys, it has been 
seen enough times and has been described 
well enough to warrant having a name of 
its own. I am therefore naming it H. 
meleagridis n. sp. 



species, also in the erythrocytes. Schi- 
zogony takes place in the parenchyma of 
the liver, heart, kidney or other organs, 
the schizonts forming large bodies divided 
into cytomeres. There is no schizogony 
in the erythrocytes or leucocytes. The 
vectors are blackflies {Simulium). Mem- 
bers of this genus are parasites of birds. 

Leucocytozoo)i is common in many 
wild birds and also causes disease in 
ducks, geese, turkeys and chickens. 
Coatney (1937) gave a catalog and host- 
index of the genus, and Herman (1944) 
listed the species occurring in North 
American birds. 



LEUCOCYTOZOON SIMONDI 
MATfflS AND LEGER, 1910 



HAEMOPROTEUS INFECTIONS IN 
BIRDS 

Diagnosis : Haemoproteus infections 
can be diagnosed by finding and identifying 
the protozoa in stained blood smears. 
However, not all infections in which game- 
tocytes alone are found are necessarily 
Haemoproteus infections. Some of them 
may be Plasmodium. 

Treatment : Little is known about 
treatment of Haemoproteus infections. 
According to Coatney (1935), quinacrine 
inhibits the development of young gameto- 
cytes of H. columbae, while pamaquine 
destroys the mature ones. Neither is 
effective against the schizonts. However, 
in view of the slight pathogenicity of 
Haemoproteus, treatment does not seem 
warranted. 

Prevention and Control : Prevention 
of Haemoproteus infections depends on 
control of their hippoboscid and midge 
vectors, or, at least in the latter case, 
in preventing the birds from being bitten. 

Genus LEUCOCYTOZOON 
Danilewsky, 1890 

The macrogametes and microgameto- 
cytes occur in the leucocytes or, in some 



Synonyms : Leucocytozoon anatis, 
Lencocytozoon anseris. 

Disease : Leucocytozoonosis. 

Hosts: Domestic ducks, domestic 
goose and many wild anseriform birds. 
Levine and Hanson (1953) tabulated reports 
of L. simondi from 23 species of wild 
waterfowl, including the grey-lag goose, 
white -fronted goose, Canada goose, wood 
duck, American pintail, green-winged 
teal, teal duck, blue-winged teal, falcated 
teal, mallard, black duck, baldpate, shov- 
eller, scaup, lesser scaup, ring-necked 
duck, redhead, canvasback, American 
goldeneye, old squaw duck, hooded mer- 
ganser, American merganser and red- 
breasted merganser. 

Fallis, Pearson and Bennett (1954) 
transmitted L. simondi from domestic 
ducks to domestic geese, but failed to in- 
fect ruffed grouse, chickens, turkeys and 
pheasants with it. 

Location : The gametocytes are in the 
lymphocytes, monocytes and also erythro- 
cytes. Schizogony takes place in the liver, 
heart, brain, spleen, lungs, lymph nodes 
and pancreas. 



Geographic Distribution : 
America, Europe, Indochina. 



North 



276 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZCXDN 



Prevalence : This species is common 
in northern United States, Canada and 
other mountainous or hilly areas where 
cold, rapid streams permit suitable black- 
fly vectors to breed. 





Fig. 33. Species of Leiicocytozoon in avian 
leucocytes. A. L. smithi macro- 
gamete from turkey. B. L. si- 
tiiondi microgametocyte from duck. 
X 1400. (Original) 



Morphology : The mature macroga- 
metes and microgametocytes are more or 
less elongate, and 14 to 22 fi long. Their 
host cells are ordinarily elongate, up to 
45 to 55 (J, long, with their nucleus form- 
ing a very long, thin, dark band along one 
side and with pale cytoplasmic "horns" 
extending out beyond the parasite and the 
nucleus. In some cases, round macro- 
gametes and microgametocytes in rounded 
host cells have been reported (Fallis, 
Davies and Vickers, 1951; Rawley, 1953; 
Cook, 1954); both types are mature and 
able to exflagellate. Briggs (1960) noted 
that there were approximately equal num- 
bers of round and elongate forms in white 
Pekin ducks but that elongate forms were 
rare in Muscovy ducks, never constituting 
more than 5% of the total number. He 
suggested that this might be due to the in- 
fluence of the host species. 

The cytoplasm of the macrogametes 
is rather dark blue and the nucleus com- 
pact and red when stained with a Roman- 
owsky stain. The cytoplasm of the micro- 
gametocytes is very pale blue and the 
nucleus diffuse and pale pink. The micro- 
gametocytes are more delicate and more 
subject to distortion than the macroga- 
metes. 



A good deal of controversy has existed 
as to the type of cell parasitized by L. 
sii>io)idi. The host cells of the mature 
gametocytes are so distorted that they 
cannot be recognized. Huff (1942) consid- 
ered them to be lymphocytes or stages in 
transformation between them and mono- 
cytes. Levine and Hanson (1953) found 
young and developing forms only in lymph- 
ocytes or monocytes. On the other hand, 
Fallis, Davies and Vickers (1951) and 
Cook (1954) found very young forms in both 
lymphocytes and erythrocytes. Using the 
benzidine-peroxide stain for hemoglobin. 
Cook found no hemoglobin in the host cells 
containing mature gametocytes, but she 
found at least some hemoglobin in all of 
the 191 host cells she saw which contained 
developing gametocytes. She concluded 
that, while the ring stages may invade both 
erythrocytes and lymphocytes, they develop 
to maturity only in cells of the red blood 
series. Whatever the host cell may be, the 
gametes and gametocytes never contain 
hematin pigment granules. 

Life Cycle : The life cycle has been 
studied by O'Roke (1934), Huff (1942), 
Fallis, Davies and Vickers (1951), Fallis, 
Anderson and Bennett (1956) and Cowan 
(1955) among others. Birds become in- 
fected when bitten by a blackfly vector. 
The sporozoites enter the blood stream, 
invade various tissue cells, round up and 
become schizonts. 

Two types of schizont occur in the 
duck. Hepatic schizonts 11 to 18fi in 
diameter occur in the liver cells; they 
form a number of cytomeres which in 
turn form small merozoites by multiple 
fission. 

Megaloschizonts 60 to 164;i in diam- 
eter when mature are found in the brain, 
lung, liver, heart, kidney, gizzard, in- 
testine and lymphoid tissues 4 to 6 days 
after exposure. They are more common 
than the hepatic schizonts. The megalo- 
schizonts develop in cells, possibly lymph- 
oid cells or macrophages, within or out- 
side the blood vessels. They contain 
numerous cytomeres and a large, conspic- 
uous central body which may be either a 
primordium off of which the cytomeres 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZCX5N 



277 



have budded (Cowan) or perhaps a hyper- 
trophied host cell nucleus (Huff). 

According to Cowan, spherical pri- 
mary cytomeres are first formed. Their 
chromatin first diffuses and then prolifer- 
ates to form peripheral clusters, which 
separate to form secondary cytomeres, 
which in turn multiply in the same manner. 
The multiplying cytomeres become smaller 
and more granular, their chromatin be- 
comes more concentrated, and finally 
merozoite-like bodies are formed. These 
reproduce until the central body is greatly 
compressed and the megaloschizont mem- 
brane is ruptured, releasing the mero- 
zoites into the blood. Many thousands of 
bipolar merozoites are produced by each 
megaloschizont. 

In addition to the hepatic schizonts 
and megaloschizonts, small structures 
thought to be schizonts were found by 
R. C. Ritchie (cited by Fallis, Anderson 
and Bennett, 1956) in the Kupffer cells 
of the liver of a duck killed 3 days after 
exposure. 

On the basis of these observations, 
Fallis, Anderson and Bennett postulated 
the following life cycle: The first asexual 
generation occurs in the Kupffer cells of 
the liver. Some of the merozoites from 
these schizonts may develop into gameto- 
cytes; this explains the presence of a few 
large parasites in the blood 5 to 6 days 
after infection. Other merozoites from 
the first generation schizonts develop into 
hepatic schizonts, megaloschizonts and 
perhaps other Kupffer cell schizonts. 
Merozoites arising from megaloschizonts 
and hepatic schizonts develop into gameto- 
cytes which flood into the peripheral circu- 
lation beginning 6 to 7 days after infection. 
Some of these merozoites presumably de- 
velop into another asexual generation. 

The development of the gametocytes 
in the blood cells has already been men- 
tioned in the section on morphology. 
According to Chernin (1952), the gameto- 
cytes may disappear from the blood about 
30 days after they first appear. Following 
this primary parasitemia, which begins in 
mid-summer in northern Michigan, only 



an occasional parasite is seen in the blood 
during the fall and winter (O'Roke, 1934; 
Huff, 1942; Chernin, 1952a). With the 
development of sexual activity in the spring, 
gametocytes reappear in the blood and in 
some cases continue to be present thruout 
the summer. 

It is clear from this account that schi- 
zogony continues in the internal organs for 
an indefinite, long time, altho at a much 
reduced rate. There are about 1000 times 
fewer gametocytes in the relapse phase 
than in the primary infection, and these 
adult birds are not seriously affected. 
However, they serve as the source of in- 
fection for the new crop of ducklings. 

According to Chernin (1952a), the 
early season infections in ducklings are 
comparatively light, but the heavier pool 
of gametocytes provided by these primary 
infections in the first crop ducklings en- 
sures the heavier and highly fatal infec- 
tions which occur during midsummer. 

The vectors of L. simondi are various 
species of blackflies {ShnuUmn). O'Roke 
(1934) showed that S. venustum is the vec- 
tor in Michigan. Fallis, Anderson and 
Bennett (1956) found that S. croxtoni and 
S. euryacbniniculHm are the important 
vectors during the early part of the black- 
fly season (May to June) in Ontario, while 
S. rugglesi is the important vector in late 
June and July. 

In the blackfly's stomach (O'Roke, 
1934; Fallis, Davies and Vickers, 1951; 
Rawley, 1953), 4 to 8 microgametes are 
formed within a few minutes by exflagella- 
tion from the microgametocytes. These 
fertilize the macrogametes to form a mo- 
tile zygote or ookinete about 33 /i long and 
5|Lt wide. Ookinetes are present in the 
blackfly stomach 2 to 6 hours after inges- 
tion of infected blood. They develop into 
oocysts both in the stomach wall and in 
the stomach itself. 

The oocysts are 10 to 13 |i in diameter. 
They can be found 2 to 3 days after infection, 
and complete their development 2. 5 to 4 
days after infection. They produce rela- 
tively few sporozoites compared with 



278 



PI^SMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



Plasmodium . The sporozoites are 5 to 
10(1 long, slender, with one end rounded 
and the other pointed. They break out of 
the oocysts and pass to the salivary 
glands, where they accumulate. Viable 
sporozoites can be found for at least 18 
days after infective feeding. 

Pathogenesis : L. simondi is mark- 
edly pathogenic for ducks and geese. The 
heaviest losses occur among young birds. 
O'Roke (1934) reported mortalities of 
35%, 57% and 85% among young ducks in 3 
different years in Michigan, but noted that 
the death rate among adults was very low. 
Knuth and Magdeburg (1922) and Stephan 
(1922) described serious outbreaks in 
young geese in Germany. According to 
Chernin (1952b), about 68%. of the deaths 
in ducklings occur 11 to 19 days after ex- 
posure. 

Briggs (1960) found that Muscovy 
ducklings were more resistant to L. 
simondi infections than white Pekin duck- 
lings under conditions of natural exposure 
in Michigan. Altho both became readily 
infected, the mortality and number of sex- 
ual forms in the blood were much lower 
among the Muscovies than the white Pekins. 
In addition, deaths were delayed in the 
Muscovies. 

The outstanding feature of an outbreak 
of leucocytozoonosis is the suddenness of 
its onset. A flock of ducklings may appear 
normal in the morning, may become ill in 
the afternoon, and may be dead by the next 
morning. Acutely affected ducklings are 
listless and do not eat. Their breathing 
is rapid and labored due to obstruction of 
the lung capillaries with schizonts. They 
may go thru a short period of nervous ex- 
citement just before death. Adult birds 
are more chronically affected. They are 
thin and listless, and the disease develops 
more slowly in them. If they die at all, it 
is seldom in less than 4 days after the 
appearance of signs. Ducklings which have 
recovered often fail to grow normally. Re- 
covered birds, as mentioned above, re- 
main carriers. 

The principal lesions of leucocyto- 
zoonosis are splenomegaly and liver hy- 



pertrophy and degeneration. Anemia and 
leucocytosis are present, and the blood 
clots poorly. Cowan (1957) described the 
tissue reactions of infected ducks against 
the megaloschizonts. These include des- 
truction by phagocytes and inflammatory 
cells, necrosis and possibly encapsulation. 

Diagnosis : Leucocytozoonosis can be 
diagnosed by finding and identifying the 
gametocytes in stained blood smears or the 
schizonts in tissue sections. 

Treatment : No effective treatment is 
known. Fallis (1948) found that quinacrine, 
sulfamerazine and chlorguanide were in- 
effective. 

Prevention and Control : Prevention 
depends upon blackfly control--ordinarily 
a difficult task--or on raising ducks and 
geese under conditions which prevent them 
from being bitten by blackflies. In black- 
fly areas this means raising them in 
screened quarters. Blackflies pass readily 
thru ordinary, 16 mesh per inch window 
screening, and 32 to 36 mesh screen is 
needed to keep them out. Since this type 
of screening is expensive, a good grade of 
cheesecloth has been recommended for a 
single season's use. 

This disease can be avoided entirely 
by raising ducks and geese in regions 
where blackflies do not occur in significant 
numbers. Since wild ducks and geese are 
reservoirs of infection for domestic birds, 
the latter should not be raised close to 
places where wild waterfowl congregate. 



LEUCOCYTOZOON SMITHI 
LAVERAN AND LUCET, 1905 

Disease : Leucocytozoonosis. 

Hosts: Domestic and wild turkeys. 

Location: The gametocytes are in 
the leucocytes. Schizogony occurs in the 
liver. 

Geographic Distribution : North 
America, Europe (France, Germany, 
Crimea). 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



279 



Pi'e valence : This species is common 
in northern and southeastern United States, 
along the Gulf Coast and Pacific Coast and 
in Canada in mountainous or hilly areas 
wherever cold, rapid streams permit suit- 
able blackfly vectors to breed. It was 
first seen by Smith (1895) in eastern United 
States, and has been encountered in North 
Dakota, Minnesota, Nebraska, Wisconsin, 
Illinois, Virginia, South Carolina, Georgia, 
Alabama, Florida, Pennsylvania, Missouri, 
Texas, California, Ontario and Manitoba 
(Volkmar, 1929; Skidmore, 1932; Johnson, 
1942, 1945; Johnson et al. . 1938; Hinshaw 
and McNeil, 1943; Banks, 1943; Stoddard, 
Humlin and Cooperrider, 1952; Travis, 
Goodwin and Gambrell, 1939; Mosby and 
Handley, 1943; Wehr and Coburn, 1943; 
Kozicky, 1948; West and Starr, 1940; 
Atchley, 1951; Bierer, 1950; Simpson 
Anthony and Young, 1956; Savage and Isa, 
1945; Fallis, Pearson and Bennett, 1954). 

Travis, Goodwin and Gambrell (1939) 
found it in 81% of 357 adult domesticated 
turkeys in Georgia, Florida, Alabama 
and South Carolina. Mosby and Handley 
(1943) found it in 40% of 268 captivity- 
reared wild turkeys, wild turkeys and 
domestic turkeys in Virginia. Kozicky 
(1948) found it in 21% of 92 captivity-reared 
and all of 5 native wild turkeys in Penn- 
sylvania. Atchley (1951) found it in all of 
10 domestic turkeys in South Carolina. 

Morphology : The mature macroga- 
metes and microgametocytes are rounded 
at first but later become elongate, aver- 
aging 20 to 22 |j. in length. Their host 
cells are elongate, averaging 45 by 14|j,, 
with pale cytoplasmic "horns" extending 
out beyond the enclosed parasite. The 
host cell is elongate, forming a long, thin, 
dark band along one side of the parasite; 
often it is split to form a band on each 
side of the parasite. The cytoplasm of the 
macrogametes is rather dark blue and the 
nucleus compact and red when stained 
with a Romanowsky stain. The cytoplasm 
of the microgametocytes is very pale blue 
and the nucleus diffuse and pale pink. 

Life Cycle : The life cycle of L. 
smithi is similar to that of L. simondi, 
but is not known in nearly so much detail. 



The prepatent period is about 9 days. 
Newberne (1955) and Richey and Ware 
(1955) described hepatic schizonts in the 
liver parenchyma of infected turkeys. 
According to Newberne, they measure 10 
to 20 by 7 to 14 /J., with a mean of 13. 5 by 
10. 5ji . The earliest stage he saw con- 
tained round and crescent-shaped, baso- 
philic cytomeres. These developed into 
masses of deeply staining merozoites which 
completely filled the host cell cytoplasm. 
Megaloschizonts have not been seen. 

The vectors of L. siiiitlii are various 
species of blackflies {Siiiinlii(m). Skid- 
more (1932) found that S. occidentale 
transmitted it in Nebraska, Johnson et al. 
(1938) found S. nigroparvuui to be the 
vector in Virginia, and Richey and Ware 
(1955) showed that S. slossonae could 
transmit it in South Carolina. The stages 
in the blackflies are similar to those of 
L. simondi. 

Pathogenesis : L. smithi is markedly 
pathogenic for turkeys, and extremely 
heavy losses have been reported. Savage 
and Isa (1945) described an outbreak in 
Manitoba in which more than 3000 out of 
8000 birds died in 2 months. Not more 
than 10%) of the birds which became ill re- 
covered. Stoddard, Humlin and Cooper- 
rider (1952) described an outbreak in 
Georgia in which 75% of 1600 5-month-old 
turkeys died within a week. Adult birds 
are less seriously affected than poults, 
and the disease runs a slower course in 
them, but even they may die. 

Affected poults fail to eat, appear 
droopy and tend to sit. They move with 
difficulty when disturbed; in the later 
stages there may be incoordination, and 
the birds may suddenly fall over, gasp, 
become comatose and die. If the birds do 
not die within 2 or 3 days after signs of 
disease appear, they recover. 

Recovered birds continue to carry 
parasites in their blood. Some may show 
no serious after-effects, but others de- 
velop a chronic type of the disease. They 
never regain their vigor, and the males 
pay little attention to the females and 
rarely strut. They often have moist 



280 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



tracheal rales, and cough and repeatedly 
try to clear their throats when disturbed. 
They may die suddenly under stress caused 
by undue excitement or handling. 

The spleen and liver of affected birds 
are enlarged, and the duodenum is more 
or less inflamed. This enteritis may 
sometimes extend thruout the small intes- 
tine. The birds are anemic and emaciated, 
their flesh is flabby, and their muscles 
may be brownish. There are no gross 
lesions in adult carriers, but the liver may 
occasionally be icteric, enlarged and cir- 
rhotic. Newberne (1955) saw no local tis- 
sue reaction around the hepatic schizonts, 
but noted hepatic hemosiderosis and lymph- 
ocytic infiltration. 

According to Johnson et al. (1938), 
death is due to obstruction of the circula- 
tory system by large numbers of parasites. 

Diagnosis, Treatment, Prevention and 
Control: Same as for L. sinwndi. 



LEUCOCYTOZOON CAULLERYI 
MATfflS AND LEGER, 1909 

Synonyms : Leucocytozoon andrewsi 
Atchley, 1951; Leucocytozoon schueffneri 
Prowazek, 1912 pro parte. 

Hosts : Chicken. 

Location: The gametocytes are in 
the leucocytes and erythrocytes. 

Geographic Distribution : Indochina, 
Malaya, India, Sumatra, North America 
(South Carolina). 

Prevalence : This species is rela- 
tively uncommon except perhaps in Malaya. 
Atchley (1951) found it in 15% of 400 adult 
domestic chickens in South Carolina, but 
his is the only report of it in North Amer- 
ica. It has been found in Indochina by 
Mathis and Leger (1909), in Sumatra by 
Prowazek (1912), in Malaya by Kuppusamy 
(1936), and in India by Ramanujachari and 



Alwar (1953), Ramaswami (1955), and 
Biswal and Naik (1958). In addition, Ham- 
erton (1929) reported a Leucocytozoon 
without describing it from a domestic 
chicken and a jungle fowl {Callus lajayettei) 
in the London zoo. 

Morphology : The mature gametocytes 
are round, measuring 15. 5 by 15. O/i ac- 
cording to Mathis and Leger (1909). Ac- 
cording to Atchley (1951) the macroga- 
metes are 12 to 14 |j. in diameter with a 
nucleus generally 3 to 4fi in diameter, and 
the microgametocytes are 10 to 12 fi in 
diameter with a nucleus 10 to 12 fj. in diam- 
eter occupying most of the cell. The host 
cell is round, about 20 ji in diameter ac- 
cording to Mathis and Leger and 13 to 11 \x 
in diameter according to Atchley. The 
host cell nucleus forms a narrow, dark 
band extending about a third of the way 
around the parasite. The macrogametes 
stain more darkly with Romanowsky stains 
than the microgametocytes. 

Life Cycle : Unknown. Atchley (1951) 
described exflagellation of the microga- 
metocytes, and figured one with what ap- 
peared to be 6 microgametes. 

Pathogenesis : This species is pre- 
sumably pathogenic, but accounts of it have 
been so mixed up with those of L. sabrazesi 
(see below) that its pathogenicity is uncer- 
tain. 

Remarks : Another species of Leuco- 
cytozoon, L. sabrazesi, with elongate 
gametocytes, has been described from the 
chicken. There has been a good deal of 
uncertainty as to whether L. caulleryi 
may not be merely an immature stage of 
L. sabrazesi. Many of the infections 
which have been seen have been mixed 
ones. However, Mathis and Leger, who 
first described both species, found pure 
infections of each, and Atchley found only 
round forms in the 61 infected chickens 
which he studied, some of which he kept 
under observation for a year. In addition, 
Atchley' s observation of exflagellation 
leaves no doubt that the round forms are 
mature. 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZOON 



281 



LEUCOCYTOZ OON SA BRA ZESI 
MATfflS AND LEGER, 1910 

Synonyms : Lencocylozoon scli/ieff- 
iieri Prowazek, 1912 pro parte. 

Hosts : Chicken. 

Location : The gametocytes are in 
the leucocytes and erythrocytes. 

Geographic Distribution : Indochina, 
Malaya, India, Sumatra, Java. 

Prevalence : Relatively uncommon 
except perhaps in Malaya. L. sabrazesi 
has been found in Indochina by Mathis and 
Leger (1910), in Malaya by Kuppusamy 
(1936), and in India by Ramanujachari and 
Alwar (1953), Ramaswami (1955) and 
Biswal and Naik (1958). In addition, de 
Haan (1911) reported a Leiicocyluzooii in 
the chicken in Java which he assigned to 
L. i/eavei (a species with elongate gameto- 
cytes occurring in the guinea fowl) but 
which was undoubtedly L. sahyazesi. 

Morphology : The mature gametocytes 
are elongate and measure about 24 by 4 (i 
according to Mathis and Leger (1910). 
According to Ramanujachari and Alwar 
(1953), the macrogametes average 22 by 
6. 5|j. and the microgametocytes 20 by 6/j. 
The host cells are spindle-shaped, with 
long, cytoplasmic "horns" extending be- 
yond the parasites, and measure about 67 
by &\i according to Mathis and Leger (1910). 
The host cell nucleus forms a narrow, 
darkly staining band along one side of the 
parasite. The macrogametes stain more 
darkly with Romanowsky stains than the 
microgametocytes, and have a more com- 
pact nucleus. 

Life Cycle : Unknown. 



in the chicken in Sumatra. He saw and 
illustrated both spindle-shaped and round 
host cells, but gave dimensions only for 
the spindle-shaped ones. These ranged in 
length from 45 by 66 /i . He also observed 
granules in the host cell cytoplasm which 
stained red with Giemsa's stain. He stated 
that these granules were partially missing 
in L. caiilleryi and L. sabrazesi and that 
he was establishing his new species because 
of this and also because of the difference in 
size between them and his form. However, 
the dimensions he quoted for L. sabrazesi 
were those of the parasite itself and not 
those of the host cell, and the dimensions 
he gave for L. schiieffiieri were those of 
the host cell and not those of the parasite 
itself. There is actually no significant 
difference in size between the two forms, 
and Prowazek' s name becomes a synonym 
of L. sabrazesi and also, in part, of L. 
caiilleryi. Prowazek also saw Trypano- 
soma in the same chicken, and thought it 
was a stage of Leiicocyiozooi/. 

The type of cell parasitized by Leuco- 
cytozoon has been the subject of some dis- 
cussion (see under L. siiitoiidi, p. 276). 
The host ceils containing mature gameto- 
cytes are so distorted as to be unrecog- 
nizable. Both Ramanujachari and Alwar 
(1953) and Ramaswami (1955) considered 
them to be erythrocytes. In the slide sent 
to me by Biswal, I saw one very young 
parasite in a cell which appeared to be an 
erythrocyte, but the host cells of other, 
somewhat older parasites did not appear 
to be. Further study is needed on this 
point. At any rate, the parasites do not 
form hematin granules from hemoglobin. 



LEUCOCYTOZOON MARCHOUXI 
MATHIS AND LEGER, 1910 



Pathogenesis : According to Kuppus- 
amy (1936), this species causes a disease 
in chickens characterized by anemia, py- 
rexia, diarrhea, paralysis of the legs and 
a ropy discharge from the mouth. Raman- 
ujachari and Alwar (1953) observed similar 
signs in the bird they studied. 

Remarks : Prowazek (1912) gave the 
name L. schueffneri to the forms he found 



Synonyms: Leiicocytozooii tiirtiir. 

Hosts : Various doves and pigeons. 
Levine (1954) and Levine and Kantor (1959) 
assembled reports of Leucocytozoon from 
17 species of 7 genera of columbiform 
birds. All but one were probably L. )}iar- 
cliOHxi. There is only a single report of 
this species in the domestic pigeon, by 
Jansen (1952) in South Africa. 



282 



PLASMODIUM, HAEMOPROTEUS AND LEUCOCYTOZCXDN 



Location : The ganietocytes are in 
the white blood cells. 

Geographic Distribution : Worldwide. 

Prevalence: This species is fairly 
common in wild doves. Hanson el al. 
(1957), for example, found it in 1.2'/c of 
392 immature and 6. 5% of 72 adult mourn- 
ing doves {Zenaidura macroiira) in Illinois. 

Morphology : Levine (1954) redes- 
cribed this species. The macrogametes 
are rounded or elliptical, 8 to 15 by 7 to 
11 fi with a mean of 12 by 9 p.; they stain 
dark blue with Giemsa's stain and have a 
compact, reddish nucleus. The micro- 
gametocytes are often distorted or rup- 
tured by the smearing process, but if not 
badly damaged measure 8 to 15 by 5 to 
11 (1 with a mean of 11 by 8 (i . They stain 
pale blue with Giemsa's stain and have a 
very diffuse, pale pink nucleus. Host 
cell cytoplasm is rarely seen surrounding 
the microgametocytes and was found in 
only 26% of the cells parasitized by macro- 
gametes. When present, it forms a nar- 
row border around part of all of the para- 
site's periphery. The host cell nucleus 
forms a dark-staining band along about 
1/3 of the periphery of the parasite. 

Young gametocytes were seen only in 
lymphocytes or, in one case, in a mono- 
cyte. 

Life Cycle : Unknown. 

Pathogenesis : Unknown. There were 
no signs of illness in the infected mourning 
doves seen by Levine (1954), even though 
4 of them were nestlings and 1 was only 
14 days old. 



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Members of this class constitute a 
fairly cohesive group of blood cell para- 
sites of vertebrates. They are small in 
comparison with the Plasmodiidae. They 
are piriform, round, amoeboid or rod- 
shaped, depending in part on the genus. 
They occur in the erythrocytes, and some 
genera occur in the leucocytes or histio- 
cytes as well. Pigment (hemozoin) is not 
formed from the host cell hemoglobin. 
No spores are formed, and no flagella or 
cilia are present. Locomotion is by body 
flexion or gliding. Reproduction is asex- 
ual, by binary fission or schizogony. 
Budding has also been said to occur, but 
the processes described under this name 
are actually binary fission with the forma- 
tion of 2 daughter cells or schizogony 
with the formation of 4. The existence of 
sexual reproduction is dubious, altho it 
has been described by earlier authors. 
The Piroplasmasida are heteroxenous; the 
known vectors are ixodid or argasid ticks. 

The systematic position of this group 
is still uncertain, and varies with the 
authority. The position given it here 
seems reasonable. 

There is a single order, Piroplas- 
morida. It contains 2 families, both of 
which contain parasites of domestic 
animals. 



Chapter 11 



THE 
mOPLASMASm 



FAMILY BABESIIDAE 

Members of this family are relatively 
large, piriform, round or oval parasites. 
They occur in the erythrocytes, where 
they reproduce asexually by binary fission 
or schizogony. The vectors are ixodid or 
argasid ticks. Binary fission, schizogony 
and sexual reproduction have been des- 
cribed in the tick, but the existence of 
sexual reproduction is dubious, and Reich- 
enow (1953) believed that schizogony is 
simulated by repeated binary fissions. 

By far the most important genus in 
the family is Babesia, species of which 



- 285 



286 



THE PIROPLASM-^SIDA 



cause piroplasmosis or babesiosis, a 
group of highly fatal and economically im- 
portant diseases of livestock. Other gen- 
era are Echinozoon and Aegyptianella. 



Genus BABESIA Starcovici, 1893 



For practical purposes, one can divide 
the genus into 2 groups of species, large 
forms more than 3|i long and small forms 
less than 3(i long. In general, infections 
with the large forms can be successfully 
treated with trypan blue, while infections 
with the small ones cannot. 



In this genus the trophozoites multiply 
by binary fission in the erythrocytes, 
forming pairs, or by schizogony, forming 
tetrads. A "blepharoplast" from which a 
rhizoplast arises has been described in 
the trophozoites. However, Rudzinska 
and Trager (1960) did not report seeing 
either of these structures in electron 
micrographs of Babesia rodhaini irom the 
mouse. 

If present, the blepharoplast and 
rhizoplast may betray a flagellate origin 
for the group (Dennis, 1932). However, 
Reichenow (1953) thought that it originated 
from the amoebae. Another possibility is 
that it is related to PlasniocUiim. This is 
suggested by Rudzinska and Trager's (1960) 
finding in B. rodhaini of structures com- 
posed of concentric membranes (possibly 
representing primitive mitochondria) 
similar to those they had previously seen 
in Plas)>iodimii berghei, and by their ob- 
servation that B. rodhaini apparently en- 
gulfs bits of host cell cytoplasm by phago- 
trophy like Plasmodium . 

There are two opposing schools of 
thought as to the speciation of this genus. 
One breaks it up into several genera or 
subgenera, each with a number of species 
(e. g. , Sergent et al. , 1945; Antipin el al. , 
1959), while the other prefers a single 
genus with a relatively small number of 
species, each of which may include sev- 
eral strains (e.g., Wenyon, 1926; Neitz, 
1956). The second system seems prefer- 
able. The taxonomy of the group has been 
discussed by Reichenow (1953), Poisson 
(1953) and Laird and Lari (1957) in addi- 
tion to the above authors. 

Synonyms of Babesia include Piro- 
plasma, Achro)>ialiciis, Nicollia, Niittal- 
lia, Smithia, Rossiella, Microbabesia, 
Babesiella, Francaiella, Lnlisia, Patton- 
ella, Rangelia, and Gonderiain part. 



Babesia and babesiosis occur in most 
parts of the world where there are ticks, 
except in countries such as the United 
States where they have been wiped out by 
a concerted effort. They are most impor- 
tant in the tropics, where, along with the 
trypanosomoses, they often dominate the 
livestock disease picture. However, they 
also occur in the temperate zone. Bovine 
babesiosis nearly reaches the Artie circle 
in Norway, and Thambs-Lyche (1943) re- 
ported that it was increasing in that coun- 
try. 

Babesiosis was once an extremely 
important disease of cattle in the United 
States, but it has now been eliminated, 
and the only domestic animal species left 
in this country is B. canis, which occurs 
in dogs in Florida, Virginia and Texas. 
However, Babesia is still important in 
livestock in Central and South America. 
It occurs in most of Europe, being espe- 
cially important in the countries bordering 
the Mediterranean Ocean. It is one of the 
most important diseases of livestock in 
the Middle East, thruout Africa, and also 
in parts of India and the Far East. Its 
importance in the USSR, and especially in 
its southern part, is attested by the fact 
that 61 X of the protozoan section of Antipin 
el al. 's (1959) textbook on veterinary para- 
sitology is devoted to it and a related dis- 
ease, theileriosis. It also occurs in Aus- 
tralia. 

Veterinarians and livestock owners 
in the United States today do not know 
what it is to have to contend with babesi- 
osis, but other parts of the world are not 
so fortunate. The disease is of great ec- 
onomic importance in the tropics and sub- 
tropics; indeed, Curasson (1943) believed 
that it was no exaggeration to say that the 
babesioses are the most formidable dis- 
eases of livestock in these regions and 
that they are taking a more and more 



THE PIROPLASMASIDA 



287 



important place in the animal disease 
picture as we discover new manifesta- 
tions of their activity. 

Among recent discussions of babesi- 
osis and its manifestations are those by 
Curasson (1943), Sergent et al. (1945), 
Muromtseva and Dobrokhotova (1955), 
Henning (1956), Malherbe (1956) and 
Antipin et al. (1959). 

Life Cycle : The trophozoites of 
Babesia occur in the erythrocytes, where 
they multiply by binary fission or by schi- 
zogony. In some species, two tropho- 
zoites are formed, which break out of the 
erythrocytes and enter new red cells, 
while in others tetrads composed of 4 
trophozoites are formed. Some authors 
place the latter in a separate genus, 
Nuttallia. The formation of more than 4 
trophozoites by schizogony has also been 
described in the erythrocytes (Dschun- 
kowsky, 1937; Ivanic, 1942; Delpy, 1946), 
but most workers (e. g. , Reichenow, 1953) 
consider that it is merely simulated by 
repeated binary fissions or by multiple 
invasion of a host cell. 

The above asexual cycle continues 
indefinitely, the animals sometimes re- 
maining infected for life. 

Babesia is transmitted by ticks. The 
discovery of this fact--by Smith and Kil- 
borne (1893) for B. bigemi)ia of cattle-- 
was a milestone in the history of para- 
sitology, since it was the first demonstra- 
tion that an arthropod was the vector of 
any disease. 

Dennis (1932) described sexual re- 
production of B. bigemina from cattle in 
the tick, Boophilus annulatus , and Petrov 
(1941) did the same for B. bovis in Ixodes 
ricinus. However, Regendanz and Reich- 
enow (1933) denied its existence in the 
life cycle of B. canis from the dog in 
Derniacentor reticidatus, and Regendanz 
(1936) and Muratov and Kheisin (1959) 
found no evidence of sexual reproduction 
in 5. bigemina in Boophilus microplus 
and B. calcaratus, respectively, nor 
could Polyanskii and Kheisin (1959) for 
B. bovis in Ixodes ricinus . It is likely 



that Dennis and Petrov may have been 
misled by trying to draw an analogy with 
the life cycle of Plasuiodiitiu . Pending 
final settlement of the question, however, 
both accounts are given below. 

According to Regendanz and Reichenow 
(1933), most of the B. canis ingested by 
the female tick die in its intestine. Some 
of them become vermiform and enter the 
intestinal epithelial cells, coming to lie 
against the basal membrane, and grow 
into large amoeboid forms. These then 
multiply by a series of binary fissions, 
producing more than 1000 individuals in 2 
to 3 days. These lie together loosely at 
first, but finally fill the whole host cell. 
They then become vermiform and pass 
into the body cavity. 

The vermiform stages are broadly 
rounded at the anterior end and pointed 
posteriorly, about 16jj, long, and have a 
gliding motion. They enter the ovary, 
where they penetrate the eggs. Here they 
round up and divide a few times, forming 
very small round individuals. They do 
not develop further in the larval tick 
which hatches from the egg, but when it 
molts they enter the salivary glands and 
continue their development. This first 
occurs in the nymphal stage, but is much 
more active in the adults, both male and 
female. The parasites undergo a series 
of binary fissions and enter the cells of 
the glandular acini. Here they multiply 
further, becoming smaller and filling the 
whole host cell, so that it finally contains 
thousands of minute parasites. These 
become vermiform, break out of the host 
cell, come to lie in the lumen of the gland, 
and are injected into the host when the tick 
sucks blood. The developmental process 
in the salivary glands takes 2 to 3 days. 

The tick larvae are not able to infect 
new hosts. The nymphs may do so, but 
generally it takes so long for the parasites 
to reach the salivary glands that most 
transmission, in this species at least, is 
by the adults. 

Regendanz (1936) found that the devel- 
opment of Babesia bigeniiiia from cattle in 
the intestinal wall of Boophilus microplus 



288 



THE PIROPL«iSM.\SIDA 



corresponded completely with that of B. 
canis in Derniacentor reticulaliis. After 
numerous binary fissions, the protozoa 
turn into the motile, vermiform stage and 
enter the developing eggs of the female 
tick, where development continues. He 
found no evidence of sexual stages. 

Muratov and Kheisin (1959) described 
a similar process for B. bigonina in 
Boophilus calcaralus, except that they 
said that schizogony occurs. They studied 
only the stages in the females and their 
eggs. On the day after the tick drops from 
its host, the protozoa begin to reproduce 
in its intestine by binary fission or by 
schizogony, producing club-shaped forms 
which penetrate into the epithelial cells of 
the intestine. Here they develop and un- 
dergo atypical multiple fission, character- 
ized by asynchronous segmentation, into 
amoeboid or round agamonts. These be- 
come club- or cigar-shaped, penetrate 
other intestinal cells and repeat the asex- 
ual cycle. The dividing stages in the intes- 
tinal cells are up to 30 to 45 ji in diameter 
and produce about 250 daughter parasites. 

Some of the club-shaped stages enter 
the body cavity and divide further. They 
penetrate all the organs of the female, 
including the ovary, and continue to divide. 
In the ovary they enter the eggs and divide 
by binary or multiple fission just as in the 
intestine, producing round or amoeboid 
agamonts which turn into club-shaped 
stages. Their number increases as the 
eggs develop, and they are distributed 
thruout the organs of the developing larvae. 
Muratov and Kheisin found no evidence of 
copulation or sexual reproduction. 

Polyanskii and Kheisin (1959) found 
essentially the same pattern for B. bovis 
in Ixodes ricinus. They said that it re- 
produces by binary fission or schizogony 
in the tissues of the tick and in the eggs 
of infected females, and found no stages 
of sexual reproduction or sporogony. 

Quite a different process was des- 
cribed by Dennis (1932) for B. bigemina 
in Boophilus annulatus . According to him, 
when a female tick ingests blood, most of 
the parasites in the blood are destroyed, 
but some of them turn into vermiform bod- 



ies about 6|i long which he considered to be 
gametes and which he called isogametes 
because they all look alike. They move 
actively by bending or gliding. Two of them 
unite to form a motile, club-shaped zygote 
or ookinete 7 to 12/i long. The ookinetes 
pass thru the intestinal wall, enter the 
ovaries and then the eggs. Here they round 
up to form sporonts 7. 5 to 12)i in diameter. 
The sporonts grow, and then divide by mul- 
tiple fission into 4 to 32 amoeboid sporo- 
blasts. The nuclei of the sporoblasts divide 
repeatedly, forming small, multinucleate, 
amoeboid sporokinetes which are distribu- 
ted thruout the tissues of the developing tick 
embryo. The sporokinetes vary in shape, 
being round, elongate, club- or ribbon- 
shaped, and may be as much as 15fi long. 
They contain a varying number of granular 
nuclei 0.4jll in diameter. In the course of 
the embryonal development of the tick, the 
sporokinetes multiply, probably by plasmo- 
tomy. All the tissues of the tick may be 
invaded, and sometimes the cytoplasm of 
a host cell is almost entirely supplanted by 
the parasites, particularly in the salivary 
glands. Toward the end of the tick's de- 
velopment, some sporokinetes produce 
sporozoites, which are the infectious stage. 
Others produce them only after the larva 
has hatched. The sporozoites resemble 
minature trophozoites; they are piriform 
and have a blepharoplast. They are par- 
ticularly numerous in the salivary glands, 
in the coelenchymatous tissue at the base 
of the legs and around the viscera. They 
are inoculated into the blood with the sa- 
liva when the tick feeds. 

Petrov (1941) described a similar 
process for B. bovis in Ixodes ricinus. 
According to him, the isogametes fuse in 
the tick's intestine to form an ookinete 
which passes thru the intestinal wall and 
enters a developing ovum. Here it rounds 
up, forms sporoblasts, and these in turn 
form sporozoites which pass to the sali- 
vary glands. The larvae, nymphs and 
adults of the succeeding generation can all 
transmit the parasite. 

It should be said that Reichenow (1953) 
considered some of the stages described 
by Dennis to be normal, intracellular sym- 
bionts (cf. Buchner, 1953; Koch, 1956) 
rather than Babesia. 



THE PIROPLASMASIDA 



289 



In the life cycles described above, 
the adult tick picks up the infection, but 
does not transmit it. This is done by the 
next generation. Babesia can also be 
transmitted by different stages in the 
same generation; it can be picked up by a 
larval tick and transmitted by the nymph, 
or it can be picked up by the nymph and 
transmitted by the adult. The occurrence 
of this stage-to-stage transmission de- 
pends upon both the species of Babesia and 
the species of tick. Neitz (1956) has as- 
sembled information on this subject, and 
it is given below in the discussion of the 
individual species. 

The life cycle in the tick in stage-to- 
stage transmission was studied carefully 
by Shortt (1936) for B. vogeli {B. canis) 
of the dog in Rliipiceplialus sanguineus in 
India. He saw no evidence of sexual stages. 
After the nymph has taken a blood meal, 
the parasites do not multiply in the gut 
epithelium, but in the phagocytes next to 
the hypodermis in the body cavity. Here 
they reproduce by multiple fission to form 
what Shortt called pseudocysts- -clumps of 
up to 200 organisms contained within the 
envelope of the parasitized host cell. 
These are fully developed about 7 days 
after the nymph has left its host. They 
are 14 to 35 )i in diameter. The stages 
within these pseudocysts are at first more 
or less spherical and 1 . 7 to 3. 3 fi in di- 
ameter. They become club-shaped in 4 to 
8 more days, at which time they measure 
about 9 by 2|i . The club-shaped stages 
then break out of the host cell and migrate 
to the muscles and muscle-sheaths. They 
penetrate the cells, round up, and divide 
by repeated binary fissions to form a 
large number of relatively small, ovoid 
or slightly elongate parasites about 1.2(i 
long. This stage is reached about 20 days 
or more after the nymph has fed. This 
phase of the life cycle corresponds to that 
which takes place in the eggs of the adult. 

The muscles remain unchanged during 
metamorphosis. When the adults begin to 
feed on a dog, the parasites migrate to the 
salivary glands and enter their cells. De- 
velopment then continues as described by 
Reichenow and Regendanz (1933) for B. 
canis. The parasites multiply by repeated 



binary fissions to form large numbers of 
spherical or ovoid infective stages about 
1.9ji or less in diameter. 

Pathogenesis: Babesiosis is a highly 
pathogenic disease in most hosts. It is 
unusual in that the death rate is much 
higher in adults than in young animals. 

The various species of Babesia cause 
a similar disease in different hosts. In 
most cases there are fever, malaise and 
listlessness. Affected animals do not eat, 
or eat little. There is severe anemia, 
and destruction of the erythrocytes is ac- 
companied by hemoglobinuria. The mu- 
cous membranes become pale, and icterus 
develops. The spleen is greatly enlarged, 
with soft, dark red pulp and prominent 
splenic corpuscles. The liver is enlarged 
and yellowish brown. The lungs may be 
slightly edematous. There may be diarrhea 
or constipation, and the feces are yellow 
except in very early or peracute cases. 
Affected animals lose condition, become 
emaciated, and often die. 

The signs of babesiosis may vary 
markedly from this typical picture, how- 
ever. As Malherbe (1956) said, "Anybody 
with extensive experience of these dis- 
eases. . .is forcibly struck by the deviate 
and protean manifestations of the disease 
picture as it is encountered from time to 
time. There is almost no guise under 
which the disease does not masquerade at 
some time or another, and it is therefore 
no accident that the majority of South Af- 
rican veterinarians have a pronounced 
attachment to their microscopes." Mal- 
herbe remarked on the similarity of the 
clinical and pathological manifestations of 
babesiosis to those of malaria, stating 
that "in spite of the differences in the life 
cycle of the parasites, their effect on the 
body is capable of exactly similar poten- 
tialities. " 

Death, if it occurs, is due to organic 
failure which, in turn, is due not only to 
the destruction of erythrocytes with re- 
sultant anemia, edema and icterus, but 
also to the clogging of the capillaries of 
various organs by parasitized cells and 
free parasites (Malherbe and Parkin, 1951; 



290 



THE PIROPD^SM^SIDA 



Malherbe, 1956). The stasis resulting 
from this sludging (Knisely el al. . 1947) 
causes degeneration of the endothelial 
cells of the small blood vessels, anoxia, 
accumulation of toxic metabolic products, 
capillary fragility, and eventually peri- 
vascular escape of erythrocytes and ma- 
croscopic hemorrhage. Purpura may 
result, the great majority of such cases 
in dogs being due to babesiosis. The 
signs of the disease depend in part on the 
location where the most serious stasis 
takes place. Cerebral babesiosis similar 
to cerebral falciparum malaria may occur. 
Gilles, Maegraith and Andrews (1953) 
described liver damage in B. canis infec- 
tions, beginning with early damming of 
the blood in the sinusoids around the cen- 
tral vein, thru centrilobular atrophy and 
degeneration of the hepatic cells, to ne- 
crosis of the cells. Kidney damage is 
also present. 



ported animals usually die. The native 
cattle were infected as calves and are 
premunized. Lambs and puppies, how- 
ever, are highly susceptible. 

There is no cross-immunity between 
the different species of Babesia. 

Treatment : The treatment of babesi- 
osis has been reviewed by Goodwin and 
Rollo (1955), Carmichael (1956) and 
Richardson and Kendall (1957), among 
others. There is an interesting relation- 
ship between the chemotherapy of babesi- 
osis and that of trypanosomosis. Many of 
the compounds effective against Try/jan- 
osoDia are also effective against Babesia. 
This may perhaps indicate a phylogenetic 
relationship, but I hasten to warn that a 
similar line of reasoning was once used to 
suggest a relationship between the trypano- 
somes and the spirochetes. 



Immunity : Cattle which have recov- 
ered from an attack of babesiosis due to 
B. bigeuiiiia remain infected for life, and 
are immune to reinfection. This type of 
immunity, due to continuing low-grade 
infection, is known as premunition. Pre- 
munition in cattle due to species other 
than B. bigeniiiia, and in sheep, swine 
and dogs, lasts up to 2 years. Premu- 
nized animals do not show signs of dis- 
ease except under stress of one sort or 
another. For instance, an attack of foot 
and mouth disease may reactivate babesi- 
osis in cattle, and distemper may do the 
same in dogs. 

The spleen plays an important role 
in maintaining immunity, and it is a com- 
mon observation that splenectomy is often 
followed by a severe or fatal relapse in 
premunized animals. In addition, sple- 
nectomized animals are much more sus- 
ceptible to infection with Babesia and 
much more seriously affected than nor- 
mal ones. 

Calves, foals, young pigs and kids 
are much less seriously affected by 
babesiosis than are adult animals. This 
is the reason that cattle can often be 
raised in highly endemic areas without 
being seriously affected, whereas im- 



Nuttall and Hadwen (1909) introduced 
the first effective drugs, the azo-naphtha- 
lene dyes, trypan red and trypan blue. 
The latter is still used in some areas. It 
is the sodium salt of ditolyl diazo-bis-8- 
amino-l-naphthol-3, 6-disulfonic acid. It 
must be given intravenously, since absces- 
sation and sloughing follow subcutaneous 
injection. It stains the tissues blue-green 
for several months after injection. It does 
not eliminate all parasites, so that recov- 
ered animals are premunized. 

The acridine derivative, acriflavine 
(trypaflavine, gonacrine, flavin, euflavin) 
was introduced by Stephan and Esquibel 
(1929). It is a mixture of 2,8-diamino- 
10-methylacridinium chloride with a small 
amount of 2, 8-diaminoacridinium chloride. 
It, too, is still being used, especially 
against B. eqiii in South Africa and in 
cattle in North Africa. It does not elim- 
inate all parasites, and recovered, 
treated animals are premunized. 

The quinoline derivative, acaprin 
(Acapron, Pirevan, Babesan, Piroparv, 
Zothelone, Piroplasmin) was introduced 
by Kikuth (1935) and also bv Carmichael 
(1935). It is 6,6'-di-(N-methylquinolyl) 
urea dimethosulfate„ It is administered 
subcutaneously. In large doses it elim- 



THE PIROPLASMASIDA 



291 



inates all parasites, but in small ones it 
leaves some so that recovered animals 
are premunized (Kikuth, 1938). It affects 
the parasympathetic nervous system, and 
may cause alarming reactions, including 
salivation, vasodilation, sweating, copious 
urination, diarrhea, panting, a drop in 
blood pressure and even collapse and 
death. Adrenaline and calcium gluconate 
can be given as antidotes. To avoid such 
reactions, the drug is often given in 2 or 
3 divided doses a few hours apart. Dogs 
are much more sensitive than cattle. 
Animals showing reactions usually recover 
rather quickly. Despite these reactions, 
acaprin is still one of the most widely used 
drugs for treating babesiosis in all animals 
thruout the world. 

Lourie and York (1939) found that a 
number of aromatic diamidines were ef- 
fective against Babesia. Adler and 
Tchernomoretz (1940) found that stilbam- 
idine (4, 4'-diamidinostilbene) was effec- 
tive against 5. bigemina, and fi. ovis, 
and it is also used for B. canis and B. 
caballi (Daubney and Hudson, 1941). 
Propamidine (4, 4'-diamidino-l, 3-diphen- 
oxypropane) has been used against B. 
caiiis in dogs (Carmichael and Fiennes, 
1941). Pentamidine (lomidine; 4,4'- 
diamidino-1, 5-diphenoxypentane) is used 
quite widely, especially in North Africa, 
for babesiosis in all animals. Phenami- 
dine (4, 4'-diamidinodiphenyl ether) was 
introduced by Carmichael (1942) for canine 
babesiosis and is now used in cattle and 
other animals as well. Berenil (4,4'- 
diamidino diazoaminobenzene diaceturate) 
was introduced by Bauer (1955), and is 
effective against babesiosis in cattle, dogs 
and other animals. Amicarbalide (M & B 
5062A; 3, 3'-diamidinocarbanilide di- 
isethionate) was introduced by Ashley, 
Berg and Lucas (1960). Preliminary 
studies indicate that it is effective against 
babesiosis in cattle (Beveridge, Thwaite 
and Shepherd, 1960; Lucas, 1960). 

The diamidines are injected subcutan- 
eously or intramuscularly, depending upon 
the compound. Many of them tend to cause 
a fall in blood pressure, but it soon re- 
turns to normal. Subcutaneous injection 
of concentrated solutions may cause ir- 



ritation. Transitory swelling of the face 
and lips which is anaphylactic in nature 
sometimes occurs with phenamidine. 

Prevention and Control : Since babesi- 
osis is transmitted by ticks, prevention 
and control depend primarily on tick elim- 
ination. This can be done by regular dip- 
ping, which should be carried out on an 
area basis for livestock, at least. Dogs 
and riding horses can be treated individ- 
ually. 

Artificial premunization of young an- 
imals has been practiced with a good deal 
of success, especially in North Africa 
(Sergent et al. , 1945). A mild strain of 
the organism is ordinarily used. This 
practice is not necessary if the animals 
are raised in an endemic area where they 
will all become naturally infected at an 
early age, but it is worthwhile in areas 
where only a certain proportion of the 
animals become infected or for animals 
which are destined to be shipped to endemic 
areas later on. 




Fig. 34. Bovine species of Babesia in eryth- 
rocytes. A. , B. , C. , D. Babesia 
bigemina. E. , F. , G. Babesia 
bonis. H. , I. Babesia divergens. 
X 2800. (A., B. , C, D. after 
Nuttall and Graham -Smith, 1908 
in Pavasitology . published by Cam- 
bridge Univ. Press; E. , F. , G., 
H. , I. after Davies, Joyner and 
Kendall, 1958 in Annals of Trop- 
ical Medicine and Hygiene, pub- 
lished by Liverpool School of 
Tropical Medicine). 



292 



THE PIRO°LASM\SlDA 



BABESIA BIGEMISA 

(SMITH AND KILBORNE, 1893) 

Synonyms : Pyrosoma bigeminum, 
Apiosoma bige»iinu»i , Piroplasma 
bigeni ilium, Piroplasnia auslrale, Babesia 
hudsonius bovis. 

Disease : Bovine babesiosis, piro- 
plasmosis, redwater, Texas fever. 

Hosts : Ox, zebu, water buffalo, 
deer (Mazania ainericana reperlicia) 
(syn.,Ay. sarlprii reperlicia), white- 
tailed deer (Odocoelius virginianus chir- 
iquensis (syn. , O. chiriquensis). 

Location : Erythrocytes. 

Geographic Distribution : Central 
America, South America, Europe, North, 
Central and South Africa, Australia, for- 
merly North America (U.S. ). 

Prevalence : This species causes one 
of the most important diseases of cattle 
in the tropics and subtropics. 

Morphology : The trophozoites in the 
erythrocytes are piriform, round, oval or 
irregularly shaped. The piriform tropho- 
zoites occur characteristically in pairs, 
a feature which gives the species its name. 
B. bigemina is relatively large. The 
round forms are 2 to 3 /i in diameter and 
the elongate ones 4 to Sjn long. 

Life Cycle : This has been described 
above (p. 287). The tick vectors are 
Boopliilus aiumlalus in North America, 
B. microplus in South and Central Amer- 
ica, B. auslralis in Australia, B. cal- 
carahis in North Africa and the USSR, B. 
decoloralus in South Africa, Hae»iapliy- 
salis punctata in Europe, Rhipicephaliis 
appendiculatus and R. everlsi in South 
Africa, and R. bursa in North Africa. 
Transmission takes place thru the egg in 
all species; stage-to-stage transmission 
also takes place in Haeniapliysalis and 
Rhipiceplmlus. 

Intrauterine transmission may also 
take place (Enigk, 1942). 



Pathogenesis : B. bigemina is highly 
pathogenic for adult animals but much less 
so for calves. The incubation period is 8 
to 15 days or less. The first sign of dis- 
ease is a rise in temperature to 106 to 
108° F. The temperature persists for a 
week or more. Affected animals are dull, 
listless, fail to eat and stop ruminating. 
The feces are yellowish brown. Severe 
anemia is caused by the invasion and des- 
truction of the erythrocytes; up to 75' ( of 
them may be destroyed. Hemoglobinuria 
is ordinarily present, but may be absent. 
Affected animals become thin, emaciated 
and icteric. In chronic cases the temper- 
ature is not very high and there is usually 
no hemoglobinuria, but diarrhea or con- 
stipation with hard, yellowish feces is 
present. 

The initial febrile response is asso- 
ciated with the appearance of parasites in 
the peripheral blood. 

Death may occur in 4 to 8 days in 
acute cases. The mortality is as high as 
50 to 90% in untreated cases, but treat- 
ment reduces it markedly. Calves less 
than a year old are seldom seriously af- 
fected. 

Chronically affected animals lose con- 
dition quite rapidly and remain thin, weak 
and emaciated for weeks before finally 
recovering. 

The principal lesions are splenomegaly 
with soft, dark red splenic pulp and prom- 
inent splenic corpuscles. The liver is en- 
larged and yellowish brown. The gall 
bladder is distended with thick, dark bile. 
The mucosa of the abomasum and intestine 
is edematous and icteric, with patches of 
hemorrhage. The subcutaneous, subser- 
ous and intramuscular connective tissues 
are edematous and icteric, and the fat is 
yellow and gelatinous. The blood is thin 
and watery, the plasma may be tinged with 
red, and the urine in the bladder is usually 
red. 

Immunity : As mentioned in the gen- 
eral discussion of immunity, recovered 
cattle are premunized, and premunition 
due to latent infection persists for life. 



THE PIROPLASM.'\SIDA 



293 



Diagnosis : Fever associated with 
hemoglobinuria, anemia and icterus is 
suggestive of babesiosis. The diagnosis 
can be confirmed by finding B. bigemina 
by microscopic examination of stained 
blood smears. 

Treatment : Trypan blue was the 
first effective drug used against babesio- 
sis, and is still used in some areas. It 
is administered intravenously in 1 to 2% 
aqueous solution; up to 200 ml may be 
given at a time. Two treatments on suc- 
cessive days may be needed, but 1 is often 
enough. The tissues turn blue, and re- 
covery is relatively slow. 

Acriflavine (trypaflavine) is also used 
to some extent, 50 to 100 ml of a 1% aq- 
ueous solution being given intravenously. 
Neither acriflavine nor trypan blue elim- 
inates all parasites, and recovered an- 
imals remain premunized. 

A number of aromatic diamidines are 
effective against B. bigemina. Stilbami- 
dine was found by Adler and Tchernomoretz 
(1940) to be effective in calves when injec- 
ted subcutaneously at a dosage of 2 to 4 
mg per kg. Phenamidine is used quite 
widely. Randall and Laws (1947) gave 15 
mg per kg phenamidine isethionate sub- 
cutaneously; the drug was well tolerated 
in doses up to 22. 5 mg per kg. Berenil is 
the most recent of these drugs to be intro- 
duced (Bauer, 1955). It is injected intra- 
muscularly at a dosage rate of 1 to 3 mg 
per kg body weight. 

The quinoline derivative, acaprin, is 
also effective. The dosage for cattle is 
0. 02 ml per kg of a 5% aqueous solution 
subcutaneously. 

The diamidines and acaprin eliminate 
all the parasites, so that treated animals 
are no longer premunized. 

Prevention and Control : Since B. 
bigemina is transmitted only by ticks, in- 
fection can be prevented by tick control. 
This can be done by dipping the cattle reg- 
ularly. This is the way in which Texas fe- 
ver was eliminated from the United States. 



Another measure which has been used 
is artificial premunization of young ani- 
mals with a mild strain, especially before 
shipping them to endemic areas. 

Remarks: Spindler et al. (1958) 
found a Babesia which resembled B. bi- 
gemina in a white-tailed deer {Odocoilens 
virginianiis coiiesi) in New Mexico. The 
animal was weak and had lesions charac- 
teristic of babesiosis. Blood smears made 
from several other white-tailed deer, mule 
deer, cattle and a few antelope from the 
same region were negative, but this find- 
ing raises a question as to the existence of 
a possible reservoir of Babesia in wild 
deer in the southwestern states. 



BABESIA BOVIS 
(BABES, 1888) 
STAR