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STUDIES on ISOSPORAN COCCIDIA of MAMMALS, INCLUDING MAN by Miles Berkeley Markus, B.Sc., M.Sc. (Pretoria), M.Sc. (Medical Parasi

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STUDIES on ISOSPORAN COCCIDIA of MAMMALS, INCLUDING MAN by Miles Berkeley Markus, B.Sc., M.Sc. (Pretoria), M.Sc. (Medical Parasi STUDIES ON ISOSPORAN COCCIDIA OF MAMMALS, INCLUDING MAN by Miles Berkeley Markus, B.Sc., M.Sc. (Pretoria), M.Sc. (Medical Parasitology) (London) Thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy of the University of London Imperial College Field Station, Ashurst Lodge, Sunninghill, Ascot, Berkshire November 1975 2 To my parents w 3 ABSTRACT Toxoplasma, Sarcocystis and Isospora are three of the six described genera of Coccidia (Phylum Protozoa, Subphylum Sporozoa or Apicomplexa) having oocysts of the "isosporan" type, containing two sporocysts, each with four sporozoites. Aspects of the life-cycles and transmission of these organisms that have not previously been studied or have received scant attention were examined in relation to human infections and infections in other mammals. Part I of the thesis deals with the parasite outside the host and Part II with the parasite inside the host. Toxoplasma gondii and Isospora fells were isolated from soil in urban areas, emphasising the key role played by the oocyst in transmission. Experiments were conducted on the survival of I. felis in soil. It was found experimentally that coccidian oocysts of vertebrates can pass undamaged through the digestive tracts of invertebrates; and that wild flies can carry isosporan oocysts. These observations, together with others on the movement of coprophagous flies in the field have thrown new light on ways in which oocysts might reach animals and man. The discussion includes a section on the risk of human infection by Toxoplasma oocysts. The results of attempted infection of cats (successful) and chimpanzees (unsuccessful) with Sarcocystis are discussed in conjunction with a review of the life-cycle and relationships of Sarcocystis. Phenomena hitherto unexplained are clarified and taxonomic comments are made. The causative organisms in an outbreak of disease in a herd of cattle in Canada in the early 1960's (named "Daimeny disease") and unidentified Protozoa involved in some other infections of mammals recorded in the literature, are considered to have been Sarcocystis spp. 4 It is concluded that insufficient information is currently available on antibody production in Sarcocystis infections to enable serological tests to be used for diagnosis of intestinal infections in man or carnivorous mammals, as has been attempted by some workers. The question of common antigenicity between Toxoplasma and other isosporan coccidia is discussed in relation to the interpretation of serological tests for human toxo- plasmosis. Studies of I. felis in cats and in normal and immunosuppressed mice and chickens have elucidated aspects of the life-cycle: small mammals and birds might serve as intermediate hosts; and infection of cats can take place through carnivorism. Twenty-one printed contributions on various subjects, written sub- sequent to the author's registration for the Ph.D. degree, are submitted as subsidiary matter. 5 CONTENTS Page Abstract .0* 00. .00 0.0 0.0 ... * • • 3 Acknowledgements *00 0** *** a** 0.* *** 0.0 • • • 7 Introduction 000 O.* 000 0.0 000 0.0 *** • • • 9 Materials and Methods ... *00 • • • • • • ... • • • 000 00* 11 Part I: Survival and dissemination of oocysts in the environment Historical review 00. 0** 000 00* 00* • • • 00. 0.0 21 Environmental contamination by isosporan oocysts • 0 4. 21 Invertebrates as transport hosts for coccidian oocysts • 00 25 Results ... 000 0.0 000 ... 000 000 ... 29 Isolation of Toxoplasma gondii from soil 000 000 000 29 Isolation of Isospora felis from soil 000 0.0 0.0 0.0 40 Survival of Isospora felis in soil in the laboratory ... *00 50 Infectivity of oocysts from the gut of earthworms and worm casts ... ..# 52 Survival of sporocysts of Sarcocystis in flies in the laboratory 0.. 00. *00 00* .0* .00. 000 55 Occurrence of oocysts in wild-caught flies 00* 000 56 Movements of flies in relation to the transport of oocysts 61 Movement to human food from cat faeces 00* 000 61 Movement to cattle from dog/human faeces 62 Discussion ... ... ... ... ... 000 .00 .00 67 Significance for man of the occurrence of oocysts of Toxo- plasma gondii in the environment *0. 000 0.* 0.0 67 Earthworms and Toxoplasma gondii oocysts ... ... 00. 000 73 The role of filth flies in the transmission of bovine sarcosporidiosis and other coccidial infections ... .0. 75 Part II: Development of Sarcocystis and Isospora in tissues of their vertebrate hosts Historical review ... ... ... 00. 000 000 *** 0.0 92 Life-cycle of Sarcocystis 00* 000 000 0.0 000 00* 92 Intestinal isosporan coccidia of non-human Primates ... ... 112 Development of coccidia of mammals in "abnormal" hosts ... 115 6 Ems Results • a • 0.00 *00 .00 O.. 00* .0. 120 Prevalence of Sarcocystis in cattle, sheep, swine and horses in Britain 000 00* 000 *0* 0.0 ..0 00. ... 120 Sporocysts of Sarcocystis of cattle in cats 000 0** 0.0 122 Attempted infection of chimpanzees with cattle Sarcocystis 134 Attempted infection of mice with sporocysts of cattle Sarcocystis from cat faeces 000 0.0 136 Isospora felis in the mesenteric lymph node of the cat 000 142 Isospora felis in normal and immunosuppressed mice and chickens 0.00 *00 000 0** 000 0.0 .0.0. 00* 143 Discussion 000 .00 00* .00 .00 .00 0.0 ... *00 162 Susceptibility of different hosts to intestinal infection with cattle Sarcocystla ... 000 ... 000 0.0 .0, 0 162 Life-cycle of Sarcocystis 00. 000 0.0 000• .00 0** 163 Systematic relationship of Sarcocystis to Hammondia, Besnoitia, Frenkelia and Toxonlasma ... ... ... 000 181 Identification of coccidia in the faeces of naturally infected cats and dogs ... ... ... .00 ... *0* 184 Serology of human sarcosporidiosis ... 0.0 00. 000 000 189 Specificity of serological tests for human toxoplasmosis 000 193 Extra-intestinal infections of Isospora felis ... *00 .040 196 References 0.0 0.0 00* 00* *** 00* 197 Subsidiary matter 000 **0 *0* 000 *00 *** *O0 • • • 244 7 ACKNOWLEDGEMENTS I am most grateful to Dr. E. U. Canning, my supervisor, for her encouragement and support; and for critically reading Part I of the manu- script. I am also indebted to Prof. P. C. C. Garnham, Dr. R. Killick- Kendrick and other colleagues for their interest in this work. Facilities 0 at the Field Station were kindly provided by the Director, Prof. T. R. E. Southwood. In addition to persons mentioned in Markus et al., 1974 (see "Sub- sidiary Matter", No. 18), I wish to thank the following:- Prof. J. K. A. Beverley (Dept. of Medical Microbiology, University of Sheffield), for providing comparative material of Toxoplasma. Dr. C. C. Draper and Mr. S. Thayer (Ross Institute, London School of Hygiene and Tropical Medicine), for bleeding the chimpanzees and for assistance in carrying out the indirect fluorescent antibody tests. Dr. R. Fayer (Animal Parasitology Institute (U.S. Dept. of Agriculture), Beltsville) and Dr. A. J. Johnson (Division of Pathology, Walter Reed Army Institute of Research, Washington, D.C.), who kindly provided Prof. P. C. C. Garnham with comparative material of Sarcocystis for use in Markus et al., 1974, the photomicrographs from which have been included here. Dr. D. G. Fleck (Public Health Laboratory, St. George's Hospital), for carrying out the dye-tests for Toxoplasma. Dr. L. P. Joyner (Central Veterinary Laboratory, Weybridge), for supplying Eimeria tenella oocysts. The Meat Inspectors (Reading Abattoir), for their cooperation. 4 8 Mr. J. P. Nicholas (Imperial College Field Station), for the patience he showed in holding cats and in assisting with proof-reading over the past few years. Mr. A. C. Pont (Department of Entomology, British Museum (Natural History)), for assistance with the identification of flies. I am grateful to Carole Collins for her efficient typing of the thesis; and to Glynis Carter for transferring many of the references for the thesis from my reprints on to sheets for subsequent alphabetical arrangement. Dr. R. Killick-Kendrick and Antonia Reeve kindly assisted with the printing of photomicrographs. This work was supported by the South African Medical Research Council, The British Council and the S.A. Council for Scientific and Industrial Research (travel grant). 9 INTRODUCTION Sporulated oocysts of the "isosporan" type contain two sporocysts, each with four sporozoites, and have been known for many years to occur in the faeces of vertebrates. The mammals in which these disporocystid, tetrazoic oocysts are formed, are mainly carnivorous. Until the discovery by Hutchison et al. (1969, 1970, 1971), Frenkel et al. (1970), Dubey et al. (1970a) and other authors of an isosporan phase in the life-cycle of Toxo- plasma gondii, coccidial infections in which isosporan oocysts were produced had been regarded as restricted to the intestines of the hosts. The discovery of the oocyst of T. gondii indicated the probability that coccidian - type gametogony would also be found to occur in closely related genera. It was soon shown (Rommel et al., 1972) that Sarcocystis had an intestinal phase culminating in production of isosporan oocysts. Besnoitia also undergoes gametogony in carnivorous mammals (Peteshev et al., 1974; Wallace and Frenkel, 1975). It would seem, from the descriptions of Besnoitia oocysts given by these authors, that oocysts found in experi- mental cats and dogs by Rommel (1975) were those of Besnoitia. To date, an oocyst stage of the related Frenkelia has not been reported,* although attempts have been made to ascertain whether gametogony take place (Tadros, 1970). Closer study of small isosporan oocysts in faeces of carnivores resulted in the isolation in the U.S.A. of undescribed organisms from cat faeces which showed similarities to both Toxoplasma and Sarcocystis (Wallace, 1973a, 1974, 1975; Frenkel et al., 1974) and have been designated as a new genus, Hammondia (see Frenkel, 1974; Frenkel and Dubey, 1975a, b). The fact that T. gondii can cause serious disease in animals and man, • including both fatal congenital and post-natally acquired infections, is well-known.
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