Immunodepressed Animals as Models for Intestinal Protozoan Infections

  • M. Elaine Rose


In studies of parasitic infections the chief value of immunodepressed animals, particularly those with specific immunodeficiencies, is as an aid in the unravelling of the immune mechanisms which, in normal animals, are responsible for the maintenance of an equable host-parasite relationship. Such studies on intestinal protozoa are comparatively sparse, but this chapter attempts to consider the available literature, mainly with respect to infections with the intracellular Eimeria and surface-epithelium-dwelling Giardia, the causative agents, respectively, of coccidiosis in domestic animals and giardiasis in man.


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  1. Abioye, A. A. (1973). Fatal amoebic colitis in pregnancy and Puerperium: a new clinico-pathological entity. J. trop. Med. Hyg., 76, 97–100Google Scholar
  2. Agarwal, A., Sharma, G. L., Bhatia, A., Naik, S. R., Chakravarti, R. N. and Vinayak, V. K. (1980). Effect of corticosteroid and irradiation on experimental Giardia lamblia infection in mice. Ann. trop. Med. Parasit., 74, 369–71Google Scholar
  3. Ament, M. E., Ochs, H. D. and Davis, S. D. (1973). Structure and function of the gastrointestinal tract in primary immunodeficiency syndromes. A study of 39 patients. Medicine, 52, 227–47CrossRefGoogle Scholar
  4. Ament, M. E. and Rubin, C. E. (1972). Relation of giardiasis to abnormal intestinal structure and function in gastrointestinal immunodeficiency syndromes. Gastroenterology, 62, 216–26Google Scholar
  5. Anderson, R. E. and Warner, N. L. (1976). Ionising radiation and the immune response. Adv. Immun., 24, 216–335Google Scholar
  6. Bird, R. G. and Smith, M. D. (1980). Cryptosporidiosis in man: parasite life cycle and fine structural pathology. J. Path., 132, 217–33CrossRefGoogle Scholar
  7. Boorman, G. A., Lina, P. H. C., Zurcher, C. and Nieuwerkerk, H. T. M. (1973). Hexamita and Giardia as a cause of mortality in congenitally thymus-less (nude) mice. Clin. exp. Immun., 15, 623–7Google Scholar
  8. Bray, R. S. and Harris, W. G. (1977). Cellular immune responses to amoebic liver abscess in the guinea pig. Clin. exp. Immun., 29, 147–51Google Scholar
  9. Chessum, B. S. (1972). Reactivation of Toxoplasma oocyst production in the cat by infection with Isospora felis. Br. vet. J., 128, 33–6Google Scholar
  10. Connan, R. M. (1970). The effect of host lactation on the ‘self-cure’ of Nippostrongylus brasiliensis in rats. Parasitology, 61, 27–33CrossRefGoogle Scholar
  11. Connan, R. M. (1972). The effect of host lactation on a second infection of Nippostrongylus brasiliensis in the rat. Parasitology, 64, 229–33CrossRefGoogle Scholar
  12. Desai, A. C. and Bhide, M. B. (1977). Effect of depressed cell mediated immunity on hepatic amoebiasis in hamsters. Bull. Haffkine Inst., 5, 35–7Google Scholar
  13. Dineen, J. K. and Kelly, J. D. (1972). The suppression of rejection of Nippostrongylus brasiliensis in lactating rats: the nature of the immunological defect. Immunology, 22, 1–12Google Scholar
  14. Doe, W. F. (1979). An overview of intestinal immunity and malabsorption. Am. J. Med., 67, 1077–83CrossRefGoogle Scholar
  15. Dubey, J. P. (1975). Immunity to Hammondia hammondi infection in cats. J. Am. vet. med. Ass., 167, 373–7Google Scholar
  16. Dubey, J. P. (1976). Reshedding of Toxoplasma gondii oocysts by chronically infected cats. Nature, Lond., 262, 213–4CrossRefGoogle Scholar
  17. Dubey, J. P. (1978a). Life cycle of Isospora ohioensis in dogs. Parasitology, 77, 1–11CrossRefGoogle Scholar
  18. Dubey, J. P. (1978b). Effect of immunisation of cats with Isospora felis and BCG on immunity to re-excretion of Toxoplasma gondii oocysts. J. Protozool., 25, 380–2CrossRefGoogle Scholar
  19. Dubey, J. P. (1979). Life cycle of Isospora rivolta (Grassi, 1879) in cats and mice. J. Protozool., 26, 433–41CrossRefGoogle Scholar
  20. Dubey, J. P. and Frenkel, J. K. (1972a). Extra intestinal stages of Isospora felis and I. rivolta (Protozoa: Eimeriidae) in cats. J. Protozool., 19, 89–92CrossRefGoogle Scholar
  21. Dubey, J. P. and Frenkel, J. K. (1972b). Cyst induced toxoplasmosis in cats. J. Protozool., 19, 155–77CrossRefGoogle Scholar
  22. Dubey, J. P. and Frenkel, J. K. (1974). Immunity to feline toxoplasmosis: modification by administration of corticosteroids. Vet. Path., 11, 350–79Google Scholar
  23. Duncombe, V. M., Bolin, T. D., Davis, M., Fagan, M. R. and Davis, A. E. (1980). The effect of iron deficiency, protein deficiency and dexamethasone on infection, reinfection and treatment of Giardia muris in the mouse. Aust. J. exp. Biol. med. Sci., 58, 19–26CrossRefGoogle Scholar
  24. Ferguson, A., Gillon, J. and Al Thamery, D. (1980). Intestinal abnormalities in murine giardiasis. Trans. R. Soc. trop. Med. Hyg., 74, 445–8CrossRefGoogle Scholar
  25. Ferguson, A. and MacDonald, T. T. (1977). Effects of local delayed hypersensitivity on the small intestine. In Immunology of the Gut, Ciba Foundation Symposium No. 46 (new series), Elsevier, Amsterdam, pp. 305–27Google Scholar
  26. Ferguson, A., Paul, G. and MacDonald, T. T. (1977). Quoted in Immunology of the Gut, Ciba Foundation Symposium No. 46 (new series), Elsevier, Amsterdam, p. 258Google Scholar
  27. Gabrielsen, A. E. and Good, R. A. (1967). Chemical suppression of adaptive immunity. Adv. Immun., 6, 92–229Google Scholar
  28. Gold, D. and Kagan, I. G. (1978). Susceptibility of various strains of mice to Entameba histolytica. J. Parasit., 64, 937–8CrossRefGoogle Scholar
  29. Helle, O. (1973). Differentiation of Eimeria species infecting sheep during the grazing season on permanent and new pastures under Norwegian conditions. Acta vet. scand., 14, 57–68Google Scholar
  30. Horwitz, M. A., Hughes, J. M. and Craun, G. F. (1976). Outbreaks of waterborne disease in the United States. J. infect. Dis., 133, 588–93CrossRefGoogle Scholar
  31. Hoskins, L. C., Winawer, S. J., Broitman, S. A. and Gottlieb, L. S. (1967). Clinical giardiasis and intestinal malabsorption. Gastroenterology, 53, 265–79Google Scholar
  32. Jeffers, T. K. (1978). Genetics of coccidia and the host response. In Avian Coccidiosis (P. L. Long, K. N. Boorman and B. M. Freeman, eds), British Poultry Science Ltd, Edinburgh, pp. 51–125Google Scholar
  33. Jeffers, T. K. and Shirley, M. W. (1982). Genetics, specific and intraspecific variation. In The Biology of the Coccidia (P.L. Long, ed.), University Park Press, Baltimore, pp. 63–100Google Scholar
  34. Jones, E. G. and Brown, W. R. (1974). Serum and intestinal fluid immunoglobulins in patients with giardiasis. Am. J. dig. Dis., 19, 791–6CrossRefGoogle Scholar
  35. Juniper, K. (1978). Amoebiasis. Clinics Gastroent., 7, 3–29Google Scholar
  36. Kasliwal, R. M. and Mathur, M. S. (1958). Adrenal cortical hypofunction in amoebiasis. J. Indian med. Ass., 31, 477–9Google Scholar
  37. Kass, E. H. and Finland, M. (1953). Adrenocortical hormones in infection and immunity. Ann. Rev. Microbiol., 7, 361–87CrossRefGoogle Scholar
  38. Katz, A. J. and Rosen, F. S. (1977). Gastrointestinal complications of immunodeficiency syndromes. In Immunology of the Gut, Ciba Foundation Symposium No. 46 (new series), Elsevier, Amsterdam, pp. 243–61Google Scholar
  39. Kelly, J. D. and Dineen, J. K. (1973). The suppression of rejection of Nippostrongylus brasiliensis in Lewis strain rats treated with ovine prolactin. The site of the immunological defect. Immunology, 24, 551–8Google Scholar
  40. Kelly, J. D. and Ogilvie, B. M. (1972). Intestinal mast cell and eosinophil numbers during worm expulsion in nulliparous and lactating rats infected with Nippostrongylus brasiliensis. Int. Archs Allergy appl. Immun., 43, 497–509CrossRefGoogle Scholar
  41. Klesius, P. M. and Hinds, S. E. (1979). Strain-dependent differences in murine susceptibility to coccidia. Infect. Immun., 26, 1111–5Google Scholar
  42. Knight, R. (1978). Giardiasis, isosporiasis and balantidiasis. Clinics Gastroent., 7, 3147Google Scholar
  43. Kocan, R. M. (1971). The effect of dexamethasone on immune pigeons infected with various strains of Trichomonas gallinae. J. Protozool., 18 (Suppl.), 30Google Scholar
  44. Kraft, S. C. (1979). The intestinal immune response in giardiasis [Editorial]. Gastroenterology, 76, 877–9Google Scholar
  45. Kunstyr, I., Ammerpohl, E. and Meyer, B. (1977). Experimental spironucleosis (hexamitiasis) in the nude mouse as a model for immunologic and pharmacologic studies. Lab. Anim. Sci., 27, 782–8Google Scholar
  46. Lewis, E. A. and Antia, A. U. (1969). Amoebic colitis: review of 295 cases. Trans. R. Soc. trop. Med. Hyg., 63, 633–8CrossRefGoogle Scholar
  47. Long, P. L. (1970). Development (schizogony) of Eimeria tenella in the liver of chickens treated with corticosteroid. Nature, Lond., 225, 290–1CrossRefGoogle Scholar
  48. Long, P. L. and Millard, B. J. (1976). The detection of occult coccidial infections by inoculating chickens with corticosteroid drugs. Z. ParasitKde., 48, 287–90CrossRefGoogle Scholar
  49. Long, P. L. and Rose, M. E. (1970). Extended schizogony of Eimeria mivati in betamethasone-treated chickens. Parasitology, 60, 147–65CrossRefGoogle Scholar
  50. Love, R. J. and Ogilvie, B. M. (1975). Nippostrongylus brasiliensis in young rats. Lymphocytes expel larval infections but not adult worms. Clin. exp. Immun., 21, 153–62Google Scholar
  51. Love, R. J., Ogilvie, B. M. and McLaren, D. J. (1976). The immune mechanism which expels the intestinal stage of Trichinella spiralis from rats. Immunology, 30, 7–15Google Scholar
  52. MacDonald, T. T. and Ferguson, A. (1978). Small intestinal epithelial cell kinetics and protozoal infection in mice. Gastroenterology, 74, 496–500Google Scholar
  53. McLoughlin, D. K. (1969). The influence of dexamethasone on attempts to transmit Eimeria meleagrimitis to chickens and E. tenella to turkeys. J. Protozool., 16, 145–8CrossRefGoogle Scholar
  54. Mattern, C. F. T. and Keister, D. B. (1977a). Experimental amebiasis. I. Pathogenicity of axenically cultured Entameba histolytica in the brain of the newborn mouse. Am. J. trop. Med. Hyg., 26, 393–401Google Scholar
  55. Mattern, C. F. T. and Keister, D. B. (1977b). Experimental amebiasis. II. Hepatic amebiasis in the newborn hamster. Am. J. trop. Med. Hyg., 26, 402–11Google Scholar
  56. Mesfin, G. M. and Bellamy, J. E. C. (1979). Thymic dependence of immunity to Eimeria falciformis var. pragensis in mice. Infect. Immun., 23, 460–4Google Scholar
  57. Meyer, E. A. and Radulescu, S. (1979). Giardia and giardiasis. In Adv. Parasit., 1–47Google Scholar
  58. Mitchell, G. (1978). Metazoan and protozoan parasitic infections in nude mice. Contemp. Topics Immunobiol., 8, 55–67CrossRefGoogle Scholar
  59. Mitchell, G. F. (1979). Responses to infection with metazoan and protozoan parasites in mice. Adv. Immun., 28, 451–511CrossRefGoogle Scholar
  60. Mitchell, G. F. (1980). T cell dependent effects in parasitic infection and disease. In Immunology 80. Progress in Immunology IV (M. Fougereau and J. Dausset, eds), Academic Press, London, New York, pp. 794–808Google Scholar
  61. Mody, V. R. (1959). Corticosteroid in latent amoebiasis. Br. med. J., ii, 1399CrossRefGoogle Scholar
  62. Naik, S. R., Kumar, L., Naik, S., Sehgal, S., Rau, N. R. and Vinayak, V. K. (1979a). Immunological studies in giardiasis. Ann. trop. Med. Parasit., 73, 291–2Google Scholar
  63. Naik, S. R., Sehgal, S., Krishnan, S., Broor, S. L. and Vinayak, V. K. (1979b). Immunoglobulins in serum and duodenal juice and peripheral blood lymphocyte subpopulations in patients with giardiasis. Trop. geograph. Med., 31, 493–8Google Scholar
  64. Neal, R. A. (1951). The duration and epidemiological significance of Entamoeba histolytica infections in rats. Trans. R. Soc. trop. Med. Hyg., 45, 363CrossRefGoogle Scholar
  65. Neal, R. A. and Harris, W. G. (1977). Attempts to infect inbred strains of rats and mice with Entamoeba histolytica. Protozoology, 3, 197–9Google Scholar
  66. Niilo, L. (1970). The effect of dexamethasone on bovine coccidiosis. Can. J. comp. Med. vet. Sci., 34, 325–8Google Scholar
  67. Ogilvie, B. M. and Jones, V. E. (1973). Immunity in the parasitic relationship between helminths and hosts. Int. Archs Allergy appl. Immun., 17, 93–144Google Scholar
  68. Ogilvie, B. M. and Love, R. J. (1974). Cooperation between antibodies and cells in immunity to a nematode parasite. Transplantation Rev., 19, 147–68Google Scholar
  69. Ogilvie, B. M. and Rose, M. E. (1977). The response of the host to some parasites of the small intestine: coccidia and nematodes. Colloques Inst. natn. Santé Rech. méd., INSERM 72, 237–48Google Scholar
  70. O’Neill, P. A. and Parfitt, J. W. (1976). Observations on Isospora suis infection in a minimal disease pig herd. Vet. Rec., 98, 321–3CrossRefGoogle Scholar
  71. Overdulve, J. P. (1978). Excretion of Toxoplasma gondii by non-immunised and immunised cats: its role in the epidemiology of Toxoplasmosis. Proc. K. ned. Akad. Wet., Series C, 81, 1–18Google Scholar
  72. Popović, O., Pendić, B., Paljm, A., Andrejević, M. and Trpković, D. (1974). Giardiasis, local immune defense and responses. Eur. J. clin. Invest., 4, 380Google Scholar
  73. Roberts-Thompson, I. C. and Mitchell, G. F. (1978). Giardiasis in mice. I. Prolonged infections in certain mouse strains and hypothymic (nude) mice. Gastroenterology, 75, 42–6Google Scholar
  74. Roberts-Thompson, I. C. and Mitchell, G. F. (1979). Protection of mice against Giardia muris infection. Infect. Immun., 24, 71–3Google Scholar
  75. Roberts-Thompson, I. C., Mitchell, G. F., Andere, R. F., Tait, B. D., Kerlin, P., Kerr-Grant, A. and Cavanagh, P. (1980). Genetic studies in human and murine giardiasis. Gut, 21, 397–401CrossRefGoogle Scholar
  76. Roberts-Thompson, I. C., Stevens, D. P., Mahmoud, A. A. F. and Warren, K. S. (1976). Giardiasis in the mouse: an animal model. Gastroenterology, 71, 57–61Google Scholar
  77. Rose, M. E. (1970). Immunity to coccidiosis: effect of betamethasone treatment of fowls on Eimeria mivati infections. Parasitology, 60, 137–46CrossRefGoogle Scholar
  78. Rose, M.E. (1973). Immunity. In The Coccidia (D.M. Hammond with P. L. Long, eds), Butterworths, London, pp. 295–341Google Scholar
  79. Rose, M. E. and Hesketh, P. (1979). Immunity to coccidiosis: T-lymphocyte or B-lymphocyte-deficient animals. Infect. Immun., 26, 630–7Google Scholar
  80. Rose, M. E. and Long, P. L. (1970). Resistance to Eimeria infections in the chicken: the effects of thymectomy, bursectomy, whole body irradiation and cortisone treatment. Parasitology, 60, 291–9CrossRefGoogle Scholar
  81. Rose, M. E., Ogilvie, B. M., Hesketh, P. and Festing, M. F. W. (1979). Failure of nude (athymic) rats to become resistant to reinfection with the intestinal coccidian parasite Eimeria nieschulzi or the nematode Nippostrongylus brasiliensis. Parasite Immun., 1, 125–32CrossRefGoogle Scholar
  82. Sehgal, A. K., Grewal, M. S., Chakravarti, R. N., Broor, S. L., Deka, N. C. and Chhuttani, P. N. (1976). Experimental giardiasis in albino rats. Indian J. med. Res., 64, 1015–8Google Scholar
  83. Snodgrass, D. R., Angus, K. W., Gray, E. W. and Keir, W. A. (1980). Cryptosporidia associated with rotavirus and an Escherichia coli in an outbreak of calf scour. Vet. Rec., 106, 458–9CrossRefGoogle Scholar
  84. Stevens, D. P. (1978). Giardiasis in the mouse: clues to host immune mechanisms. In Waterborne Transmission of Giardiasis (W. Jakubowski and J. C. Hoff, eds), pp. 82–9Google Scholar
  85. Stevens, D. P. and Frank, D. M. (1978). Local immunity in murine giardiasis:is milk protective at the expense of maternal gut? Trans. Ass. Am. Phys., 91, 268–72Google Scholar
  86. Stevens, D. P., Frank, D. M. and Mahmoud A. A. F. (1978). Thymus dependency of host resistance to Giardia muris infection: studies in nude mice. J. Immun., 120, 680–2Google Scholar
  87. Stevens, D. P. and Roberts-Thompson, I. C. (1978). Animal model of human disease. Giardiasis. Animal model: experimentally induced giardiasis. Am. J. Path., 90, 529–32Google Scholar
  88. Teodorovic, S., Ingalls, J. M. and Greenberg, L. (1963). Effect of corticosteroids on experimental amoebiasis. Nature, Lond., 197, 86–7CrossRefGoogle Scholar
  89. Thompson, R. G., Karadikar, D. S. and Leek, J. (1974). Giardiasis — an unusual course of epidemic diarrhoea. Lancet, i, 615–7CrossRefGoogle Scholar
  90. Tumka, A. F. (1972). Distribution of parasitic intestinal flagellates in mice exposed to X-irradiation. Parazitologia, 6, 222–8Google Scholar
  91. Villarejos, V. M. (1962). Corticosteroids and experimental amebiasis in the rat. J. Parasit., 48, 194CrossRefGoogle Scholar
  92. Vinayak, V. K., Chitkara, N. L. and Chhuttani, P. N. (1979b). Effect of corticosteroid and irradiation on caecal amoebic infection in rats. Trans. R. Soc. trop. Med. Hyg., 73, 266–8CrossRefGoogle Scholar
  93. Vinayak, V. K., Sharma, G. L. and Naik, S. R. (1979a). Experimental Giardia lamblia infection in Swiss mice — a preliminary report. Indian J. med. Res., 70, 195–8Google Scholar
  94. Wakelin, D. (1978). Genetic control of susceptibility and resistance to parasitic infection. Adv. Parasit., 16, 219–308CrossRefGoogle Scholar
  95. Walzer, P. D., Wolfe, M. S. and Schulz, M. G. (1971). Giardiasis in travelers. J. infect. Dis., 24, 235–7CrossRefGoogle Scholar
  96. Warner, N. L. (1967). The immunological role of the avian thymus and bursa of Fabricius. Folia biol., Praha, 13, 1–17Google Scholar
  97. Warner, N. L., Szenberg, A. and Burnet, F. M. (1962). The immunological role of different lymphoid organs in the chicken. I. Dissociation of immunological responsiveness. Aust. J. exp. Biol. med. Sci., 40, 373–88CrossRefGoogle Scholar
  98. Wijesundera, M. de S. (1980). Hepatic amoebiasis in immunodepressed mice. Trans. R. Soc. trop. Med. Hyg., 74, 216–20CrossRefGoogle Scholar
  99. Wright, S. G. (1979). Giardiasis and malabsorption. Anns Soc. belge Méd. trop., 59, 343–6Google Scholar
  100. Zinneman, H. H. and Kaplan, A. P. (1972). The association of giardiasis with reduced intestinal secretory immunoglobulin. Am. J. dig. Dis., 17, 793–7CrossRefGoogle Scholar

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© The contributors 1982

Authors and Affiliations

  • M. Elaine Rose
    • 1
  1. 1.Houghton Poultry Research StationHoughton, Huntingdon, Cambs.UK

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