Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-24T17:41:24.008Z Has data issue: false hasContentIssue false

Population dynamics in echinococcosis and cysticercosis: regulation of Taenia hydatigena and T. ovis in lambs through passively transferred immunity

Published online by Cambridge University Press:  06 April 2009

M. A. Gemmell
Affiliation:
Hydatid Research Unit, University of Otago Medical School, P.O. Box 913, Dunedin, New Zealand
J. R. Lawson
Affiliation:
Hydatid Research Unit, University of Otago Medical School, P.O. Box 913, Dunedin, New Zealand
M. G. Roberts
Affiliation:
Wallaceville Animal Research Centre, MAFTech, Ministry of Agriculture and Fisheries, P.O. Box 40063, Upper Hutt, New Zealand
J. F. T. Griffin
Affiliation:
Department of Microbiology, University of Otago Medical School, P.O. Box 913, Dunedin, New Zealand

Summary

A comparison has been made of the interactions between passively transferred and actively acquired immunity in regulating populations of Taenia hydatigena and T. ovis. When ewes were grazed prior to parturition under a high infection pressure, immunity was transferred to their offspring for up to 8 weeks. A qualititative difference between the species was the destruction of larval T. ovis prior to their establishment (‘pre-encystment immunity’) and that of T. hydatigena after they had become established (‘post-encystment immunity’) in the challenged lambs. The major difference in terms of population regulation between the two parasites was that infection occurred with T. hydatigena but not with T. ovis in those lambs reared from birth for 16 weeks under high infection pressure. Passive, like active immunity, is a density-dependent constraint. It plays an important role in the population regulation of T. ovis, but not of T. hydatigena. This is discussed in terms of transmission in the natural environment, an hypothesis on humoral protection and the need to elucidate pathways of protection when immunization schedules are being evaluated for controlling the taeniid zoonoses.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, R. M. (1982). Transmission dynamics and control of infectious diseases. In Population Biology of Infectious Diseases (ed. Anderson, R. M. & May, R. M.), pp. 149–76. Berlin, Heidelberg and New York: Springer-Verlag.Google Scholar
Beh, K. J. & Lascelles, A. K. (1981). The effect of route of administration of antigen on the antibody containing cell response in lymph of sheep. Immunology 42, 577–82.Google Scholar
Butler, J. E. (1981). A concept of humoral immunity among ruminants and an approach to its investigation. In The Ruminant Immune System (ed. Butler, J. E., Nielson, K. & Duncan, J. R.), pp. 355. New York: Plenum Press.Google Scholar
Chang, C. C., Winter, A. J. & Norcross, N. L. (1981). Immune response in the bovine mammary gland of the intestine, local and systemic immunization. Infection Immunity 31, 650–9.Google Scholar
Gemmell, M. A. (1970). Hydatidosis and cysticercosis. 2. Distribution of Cysticercus ovis in sheep. Australian Veterinary Journal 46, 22–4.CrossRefGoogle ScholarPubMed
Gemmell, M. A. (1972). Hydatidosis and cysticercosis. 5. Some problems of inducing resistance to Taenia hydatigena under conditions of a high infection pressure. Australian Veterinary Journal 48, 2931.Google Scholar
Gemmell, M. A. (1976 a). Factors regulating tapeworm populations: the changing opportunities of lambs for ingesting eggs of Taenia hydatigena. Research in Veterinary Science 21, 223–6.Google Scholar
Gemmell, M. A. (1976 b). Immunology and regulation of the cestode zoonoses. In Immunology of Parasitic Infections (ed. Cohen, S. & Sadun, E.) pp. 333–58. Oxford: Blackwell Scientific Publications.Google Scholar
Gemmell, M. A. (1987). A critical approach to the concept of control and eradication of echinococcosis/hydatidosis and taeniasis/cysticercosis. International Journal for Parasitology 17, 465–72.CrossRefGoogle Scholar
Gemmell, M. A., Blundell, S. K. & MacNamara, F. N. (1969). Immunological responses of the mammalian host against tapeworm infections. IX. The transfer via colostrum of immunity to Taenia hydatigena. Experimental Parasitology 26, 52–7.CrossRefGoogle ScholarPubMed
Gemmell, M. A. & Johnstone, P. D. (1977). Experimental epidemiology of hydatidosis and cysticercosis. Advances in Parasitology 15, 311–69.Google Scholar
Gemmell, M. A. & Johnstone, P. D. (1981). Factors regulating tapeworm populations: estimations of the duration of acquired immunity by sheep to Taenia hydatigena. Research in Veterinary Science 30, 53–6.CrossRefGoogle ScholarPubMed
Gemmell, M. A., Johnstone, P. D. & Boswell, C. C. (1978). Factors regulating tapeworm populations: dispersion patterns of Taenia hydatigena eggs on pasture. Research in Veterinary Science 24, 334–8.CrossRefGoogle ScholarPubMed
Gemmell, M. A., Lawson, J. R. & Roberts, M. G. (1986 a). Population dynamics in echinococcosis and cysticercosis: biological parameters of Echinococcus granulosus in dogs and sheep. Parasitology 92, 599620.CrossRefGoogle ScholarPubMed
Gemmell, M. A., Lawson, J. R. & Roberts, M. G. (1986 c). Present status of world–wide progress in the control of echinococcosis/hydatidosis. Bulletin of the World Health Organization 64, 333–9.Google Scholar
Gemmell, M. A., Lawson, J. R. & Roberts, M. G. (1987 a). Population dynamics in echinococcosis and cysticercosis: evaluation of biological parameters of Taenia hydatigena and T. ovis and comparisons with those of Echinococcus granulosus. Parasitology 94, 161–80.Google Scholar
Gemmell, M. A., Lawson, J. R. & Roberts, M. G. (1987 b). Towards global control of cystic and alveolar hydatid diseases. Parasitology Today 3, 144–51.CrossRefGoogle ScholarPubMed
Gemmell, M. A., Lawson, J. R., Roberts, M. G., Kerin, B. R. & Mason, C. J. (1986 b). Population dynamics in echinococcosis and cysticercosis: comparison of the response of Echinococcus granulosus, Taenia hydatigena and T. ovis to control. Parasitology 93, 357–69.Google Scholar
Gemmell, M. A. & MacNamara, F. M. (1972). Immune responses to tissue parasites. 11. Cestodes. In Immunity to Animal Parasites (ed. Soulsby, E. J. L.), pp. 235–72. New York and London: Academic Press.Google Scholar
Gemmell, M. A. & Soulsby, E. J. L. (1968). The development of acquired immunity to tapeworms and progress towards active immunization with special reference to Echinococcus spp. Bulletin of the World Health Organization 39, 4555.Google Scholar
Heath, D. D., Osborn, P. J., Parmeter, S. N. & Lawrence, S. B. (1979 a). The immunising potential of various stages of Taenia ovis injected subcutaneously into neonatal or sixteen-week-old lambs. Veterinary Parasitology 5, 51–5.Google Scholar
Heath, D. D., Yong, W. K., Osborn, P. J., Parmeter, S. N., Lawrence, S. B. & Twaalfhoven, H. (1979 b). The duration of passive protection against Taenia ovis larvae in lambs. Parasitology 79, 177–82.CrossRefGoogle ScholarPubMed
Johnson, K. S., Harrison, G. B. L., Lightowlers, M. W., O'hoy, K. L., Cougle, W. G., Dempster, R. P., Lawrence, S. B., Vinton, J. G., Heath, D. D. & Rickard, M. D. (1989). Vaccination against ovine cysticercosis using a defined recombinant antigen. Nature, London 338, 585–7.CrossRefGoogle ScholarPubMed
Larralde, C., Flisser, A. & Perez-Montfort, R. (1981). Vaccination against cysticercosis: perspectives on the immunological prevention of human disease. In Cysticercosis: Present State of Knowledge and Perspectives (ed. Flisser, A., Willms, K., Laclette, J.-P., Larralde, C., Ridarau, C. & Beltran, F.) pp. 675–84. New York and London: Academic Press.Google Scholar
Lawson, J. R., Roberts, M. G., Gemmell, M. A. & Best, S. J. (1988). Population dynamics in echinococcosis and cysticercosis: economical assessment of control strategies for Echinococcus granulosus, Taenia ovis and T. hydatigena. Parasitology 97, 177–91.Google Scholar
Lloyd, S. & Soulsby, E. J. L. (1978). The role of IgA immunoglobulins in the passive transfer of protection to Taenia taeniaeformis in the mouse. Immunology 34, 939–45.Google ScholarPubMed
Lynch, R. G. (1987). Immunoglobulin-specific suppressor T cells. Advances in Immunology 40, 135–51.Google Scholar
Musoke, A. J., Williams, J. F., Leid, R. W. & Williams, C. F. S. (1975). The immunological response of the rat to infection with Taenia taeniaeformis. IV. Immunoglobulins involved in the passive transfer of resistance from mother to offspring. Immunology 34, 565–70.Google Scholar
Rickard, M. D. (1981). Immunization against infection with larval taeniid cestodes using oncospheral antigens. In Cysticercosis: Present State of Knowledge and Perspectives (ed. Flisser, A., Willms, K., Laclette, J.-P., Larralde, C., Ridarau, C. & Beltran, F.) pp. 633–46. New York and London: Academic Press.Google Scholar
Rickard, M. D. & Arundel, J. H. (1974). Passive protection of lambs against infection with Taenia ovis larvae via colostrum. Australian Veterinary Journal 50, 22–4.Google Scholar
Rickard, M. D. & Williams, J. F. (1982). Hydatidosis/cysticercosis: immune mechanisms and immunization against infection. Advances in Parasitology 21, 229–96.Google Scholar
Roberts, M. G., Lawson, J. R. & Gemmell, M. A. (1986). Population dynamics in echinococcosis and cysticercosis: mathematical model of the life-cycle of Echinococcus granulosus. Parasitology 92, 621–41.Google Scholar
Roberts, M. G., Lawson, J. R. & Gemmell, M. A. (1987). Population dynamics in echinococcosis and cysticercosis: mathematical model of the life-cycles of Taenia hydatigena and T. ovis. Parasitology 94, 181–97.Google Scholar
Soulsby, E. J. L. (1962). Antigen-antibody reactions in helminth infections. Advances in Immunology 2, 265308.Google Scholar
Soulsby, E. J. L. & Lloyd, s. (1982). Passive immunization in cysticercosis: characterization of antibodies concerned. In Cysticercosis: Present State of Knowledge and Perspectives (ed. Flisser, A., Willms, K., Laclette, J-P., Larralde, C., Ridarau, C. & Beltran, F.) pp. 539–48. New York and London: Academic Press.Google Scholar
Sutton, R. J. (1979). The passive transfer of immunity to Taenia ovis in lambs via colostrum. Research in Veterinary Science 27, 197–9.CrossRefGoogle ScholarPubMed
Urquhart, G. M. (1961). Epizootiological and experimental studies in bovine cysticercosis in East Africa. Journal of Parasitology 47, 857–69.CrossRefGoogle ScholarPubMed
Urquhart, G. M. (1980). Immunity to cestodes. In Vaccines Against Parasites (ed. Taylor, A. E. R. & Muller, R.), pp. 107–14. Oxford, London, Edinburgh, Boston and Melbourne: Blackwell Scientific Publications.Google Scholar
Urquhart, G. M. (1981). Modulation of the host response. In Cysticercosis: Present State of Knowledge and Perspectives (ed. Flisser, A., Willms, K., Laclette, J-P., Larralde, C., Ridarau, C. & Beltran, F.), pp. 585–92. New York and London: Academic Press.Google Scholar
Williams, J. F. (1982). Cestode infections. In Immunology of Parasitic Infections (ed. Cohen, S. & Warren, K. S.), pp. 676714. Oxford, London, Edinburgh, Boston and Melbourne: Blackwell Scientific Publications.Google Scholar