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Schistosoma haematobium in the baboon (Papio anubis): assessment of protection levels against either a single mass challenge or repeated trickle challenges after vaccination with irradiated schistosomula

Published online by Cambridge University Press:  05 June 2009

G.D.F. Reid ,
R.F. Sturrock ,
R.A. Harrison  and
R.P. Tarara
G.D.F. Reid
Affiliation:
Department of Parasitology, Institute of Primate Research, National Museums of Kenya, PO Box 24481, Nairobi, Kenya
R.F. Sturrock*
Affiliation:
Department of Medical Parasitology, London School Hygiene and Tropical Medicine, Keppel Street, London, WC1E 7HT, England
R.A. Harrison
Affiliation:
Department of Medical Parasitology, London School Hygiene and Tropical Medicine, Keppel Street, London, WC1E 7HT, England
R.P. Tarara
Affiliation:
Department of Parasitology, Institute of Primate Research, National Museums of Kenya, PO Box 24481, Nairobi, Kenya
*
†Author for correspondence.
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Abstract

Baboons vaccinated intramuscularly with three times 9000 20 krad irradiated Schistosoma haematobium schistosomula at monthly intervals were exposed percutaneously to either a single mass challenge of 3000 (VMC) or ten, weekly trickle challenges of 300 (VTC) normal S. haematobium cercariae. Unvaccinated mass (MCC) or trickle (TCC) challenge controls were exposed simultaneously. Faecal and urine egg production was delayed in the vaccinated groups which also had reduced adult, particularly female, worm recoveries. Total faecal, urine and tissue eggs were lower in the vaccinated groups, as also were the size of granulomata and the gross pathology and severity of inflammatory responses in the bladder and ureters, except for an increased proportion of tissue eggs in the livers of vaccinated animals. Differences in pathology between groups were less marked in the other organs. Most indices were reduced in the trickle versus the mass challenge control groups. Some of these trends were statistically significant, mostly in the trickle vaccination group (VTC), but others were not. Compared with the appropriate unvaccinated controls, the percentage reduction for the trickle challenge (VTC) group (73%) was three times greater than that of the mass challenge (VMC) group (23%). Overall, the protective effect of vaccination was more clearly demonstrated in the trickle than in the mass challenge groups. This conclusion is based on a single experiment. Nevertheless, because trickle infections probably approximate more closely to what humans receive naturally, it is recommended that they should be used for future testing of all potential vaccines in baboons.

Type
Research Papers
Information
Journal of Helminthology , Volume 69 , Issue 2 , June 1995 , pp. 139 - 147
Copyright
Copyright © Cambridge University Press 1995

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References

Bickle, Q.D., Dobinson, A.R. & James, E.R. (1979) The effects of gamma-irradiation on migration and survival of Schistosoma mansoni schistosomula in mice. Parasitology 79, 223–230.CrossRefGoogle ScholarPubMed
Boulanger, D., Reid, G., Sturrock, R.F., Wolowczuk, I., Baloul, J.M., Grezel, D., Pierce, R.J., Otieno, M.F., Guerret, F., Grimaud, J.A., Butterworth, A.E. & Capron, A. (1991) Immunization of mice and baboons with the recombinant Sm28GST affects both worm viability and fecundity after experimental infection with Schistosoma mansoni. Parasite Immunology 13, 473–490.CrossRefGoogle ScholarPubMed
Byram, J.E., Harrison, R.A., Von Lichtenberg, F., Webbe, G. & Sturrock, G. (1989) Pathology resulting from the administration of a live attenuated anti-Schistosoma haematobium vaccine in baboons. American Journal of Tropical Medicine and Hygiene 40, 55–65.CrossRefGoogle ScholarPubMed
Capron, A., Riveau, G., Gryzch, J.M., Boulanger, D., Capron, M. & Pierce, R. (1994) Development of a vaccine strategy against human and bovine schistosomiasis. Tropical and Geographic Medicine 46, 242–246.Google ScholarPubMed
Cheever, A.W. (1985) Schistosoma haematobium: the pathology of experimental infection. A review. Experimental Parasitology 59, 131–138.CrossRefGoogle Scholar
Cheever, A.W. & Powers, K.G. (1969) Schistosoma mansoni infections in rhesus monkeys: changes in egg production and egg distribution in prolonged infections in intact and splenectomized monkeys. Annals of Tropical Medicine and Parasitology 63, 83–93.CrossRefGoogle ScholarPubMed
Cheever, A.W. & Powers, K.G. (1971) Rate of destruction of Schistosoma mansoni eggs in the tissues of mice. American Journal of Tropical Medicine and Hygiene 23, 69–76.CrossRefGoogle Scholar
Cheever, A.W. & Powers, K.G. (1972) Schistosoma mansoni infections in rhesus monkeys: comparison of the course of heavy and light infections. Bulletin of the World Health Organization 46, 301–309.Google ScholarPubMed
Cheever, A.W., Kuntz, R.E., Myers, B.J., Moore, J.A. & Huang, T.C. (1974) Schistosomiasis haematobia inAfrican hamadryas and gelada baboons. American Journal of Tropical Medicine and Hygiene 27, 429–448.CrossRefGoogle Scholar
Colley, D.G. & Wikel, S.K. (1974) Schistosoma mansoni: simplified method for the production of schistosomules. Experimental Parasitology 35, 44–51.CrossRefGoogle ScholarPubMed
Damian, R.T., Greene, N.D. & Fitzgerald, K. (1974) Schistosomiasis mansoni in baboons. II. Acquisition of immunity to challenge infections after repeated small exposures to cercariae of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 23, 78–80.CrossRefGoogle ScholarPubMed
Damian, R.T. & Chapman, R.W. (1983) The fecundity of Schistosoma mansoni in baboons, with evidence for a sex ratio effect. Journal of Parasitology 69, 987–989CrossRefGoogle ScholarPubMed
Damian, R.T., Greene, N.D., Meyer, K.F., Cheever, A.W., Hubbard, W.J., Hawes, M.E. & Clark, J.D. (1976) Schistosoma mansoni in baboons. III. The course and characteristics of infection with additional observations on immunity. American Journal of Tropical Medicine and Hygiene 25, 299–306.CrossRefGoogle ScholarPubMed
Damian, R.T., Roberts, M.L., Powell, M.R., Clark, J.D., Stirewalt, M.A. & Lewis, EA. (1985) Schistosoma mansoni egg granuloma size reduction in challenged baboons after vaccination with irradiated, cryopreserved schistosomula. Proceedings of the National Academy of Sciences of the USA 81, 3352–3356.Google Scholar
Damian, R.T., Roberts, M.L., Powell, M.R., Clark, J.D., Lewis, F.A. & Stirewalt, M.A. (1985) Schistosoma mansoni: Parasitology and immunology of baboons vaccinated with irradiated, cryopreserved schistosomula. International Journal for Parasitology 5, 333–344.CrossRefGoogle Scholar
Farid, Z. (1993) Schistosomes with terminal-spined eggs: Pathological and clinical aspects. In: Jordan, P., Webbe, G. & Sturrock, R.F. (Eds) Human schistosomiasis. CAB International, Wallingford. pp. 159–193.Google Scholar
Foster, R. (1967) Schistosomiasis on an irrigated estate in Tanzania. II. Epidemiology. Journal of Tropical Medicine and Parasitology 65, 367–384.CrossRefGoogle Scholar
Harrison, R.A., Bickle, Q.D., Kiare, S., James, E.R., Andrews, B.J., Sturrock, R.F., Taylor, M.G. & Webbe, G. (1990) Immunization of baboons with attenuated schistosomula of Schistosoma haematobium: levels of protection induced by immunization with larvae irradiated with 20 and 60 krad. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 89–99.CrossRefGoogle ScholarPubMed
James, C., Webbe, G., Shaw, J.R. & Erasmus, D.A. (1976) Egg output suppression - a manifestation of schistosome immunity. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 18.Google Scholar
James, E.R., Otieno, M., Harrison, R., Dobinson, A.R., Monorei, J. & Else, J.G. (1986) Partial protection of baboons against Schistosoma mansoni using radiation-attenuated cryopreserved schistosomula. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 378–384.CrossRefGoogle ScholarPubMed
James, S.L. & Sher, A. (1983) Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. III. Identification of a strain, P/N, that fails to respond to vaccination. Parasite Immunology 5, 567–575.CrossRefGoogle Scholar
James, S.L., Glaven, J., Goldenberg, S., Meltzer, M.S. & Pearce, E. (1990) Tumour necrosis factor (TNF) as a mediator of macrophage helminthotoxic activity. Parasite Immunology 12, 1–13.CrossRefGoogle ScholarPubMed
Knopf, P.M., Nutman, T.B. & Reasons, J.A. (1977) Schistosoma mansoni: resistance to reinfection in the rat. Experimental Parasitology 41, 74–82.CrossRefGoogle ScholarPubMed
McLaren, D.J. & Smithers, S.R. (1988) Serum from CRA/Ca mice vaccinated with irradiated cercariae of Schistosoma mansoni protects naive recipients through the recruitment of cutaneous effecter cells. Parasitology 97, 287–302.Google Scholar
Pearce, E.J., James, S.L., Hieny, S., Lanar, D.E. & Sher, A. (1988) Induction of protective immunity against Schistosoma mansoni by vaccination with paramyosin (Sm97), a nonsurface antigen. Proceedings of the National Academy of Sciences of the USA 85, 5768–5682.CrossRefGoogle ScholarPubMed
Smithers, S.R., Hackett, F., Omer Ali, P. & Simpson, A.J.C. (1989) Protective immunization of mice against Schistosoma mansoni with purified adult worm surface antigens. Parasite Immunology 11, 301–318.CrossRefGoogle Scholar
Snedecor, G.W. & Cochran, W.G. (1982) Statistical methods. The Iowa University Press, Ames, Iowa. pp. 194–237.Google Scholar
Soisson, L.A., Reid, G.D.F., Farah, I.O., Nayingo, M. & Strand, M. (1993) Protective immunity in baboons vaccinated witha recombinant antigen or radiation-attenuated cercariae of Schistosoma mansoni is antibody dependent. Journal of Immunology 151, 4782–789.CrossRefGoogle ScholarPubMed
Stek, M., Minard, P., Dean, D.A. & Hall, J.E. (1981) Immunization of baboons with Schistosoma mansoni cercariae attenuated by gamma irradiation. Science 212, 1518–1520.CrossRefGoogle Scholar
Sturrock, R.F. (1973) Field studies on the transmission of Schistosoma mansoni and on the bionomics of its intermediate host, Biomphalaria glabrata, on St Lucia, West Indies. International Journal for Parasitology 3, 175–194.CrossRefGoogle Scholar
Sturrock, R.F. (1986) A review of the use of primates in studying human schistosomiasis. Journal of Medical Primatology 15, 267–279.CrossRefGoogle ScholarPubMed
Sturrock, R.F., Butterworth, A.E. & Houba, V. (1976) Schistosoma mansoni in the baboon (Papio anubis): parasitological responses of Kenyan baboons to different exposures of a local parasite strain. Parasitology 73, 239–252.CrossRefGoogle ScholarPubMed
Sturrock, R.F., Butterworth, A.E., Houba, V., Karamsadkar, S.D. & Kimani, R. (1978) Schistosoma mansoni in the baboon (Papio anubis): the development and predictability of resistance to homologous challenge. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 251–261.CrossRefGoogle ScholarPubMed
Sturrock, R.F., James, C., James, E.R. & Webbe, G. (1980) Immunization of baboons (Papio anubis) against Schistosoma haematobium with irradiated cercariae or schistosomula. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 834–835.CrossRefGoogle ScholarPubMed
Sturrock, R.F., Kimani, R., Joseph, M., Butterworth, A.E., David, J.R., Capron, A. & Houba, V. (1981) Heat-labile and heat stable antibodies in Kenyan school children infected with Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 219–227.CrossRefGoogle Scholar
Sturrock, R.F., Cottrell, B.J. & Kimani, R. (1984) Observations on the ability of repeated, light exposures to Schistosoma mansoni cercariae to induce resistance to reinfection in Kenyan baboons (Papio anubis). Parasitology 88, 505–514.CrossRefGoogle ScholarPubMed
Sturrock, R.F., Cottrell, B.J., Mahmoud, A.A.F., Chedid, L. & Kimani, R. (1985) Attempts to induce resistance to Schistosoma haematobium and S. mansoni using non-specific immunostimulants. Journal of Helminthology 59, 175–186.CrossRefGoogle Scholar
Warren, K.S. (1973a) Regulation of the prevalence and intensity of schistosomiasis in man: immunology or ecology" Journal of Infectious Diseases 127, 595–609.CrossRefGoogle ScholarPubMed
Warren, K.S. (1973b) The pathology of schistosome infections. Helminthological Abstracts (series A) 42, 591–633.Google Scholar
Webbe, G. & James, C. (1973) Acquired resistance to Schistosoma haematobium in the baboon (Papio anubis). Transactions of the Royal Society of Tropical Medicine and Hygiene 67, 151–152.CrossRefGoogle ScholarPubMed
Webbe, G., James, C. & Nelson, G. (1974) Schistosoma haematobium in the baboon (Papio anubis). Annals of Tropical Medicine and Parasitology 68, 187–203.CrossRefGoogle ScholarPubMed
Webbe, G., James, C., Nelson, G., Smithers, S.R. & Terry, R.J. (1976) Acquired resistance toSchistosoma haematobium in the baboon (Papio anubis) after cercarial exposure and adult worm transplantation. Annals of Tropical Medicine and Parasitology 70, 411–424.CrossRefGoogle ScholarPubMed
Webbe, G., Sturrock, R.F., James, E.R. & James, C. (1982) Schistosoma haematobium in the baboon (Papio anubis): effect of vaccination with irradiated larvae on the subsequent infection with percutaneously applied cercariae. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 354–361.CrossRefGoogle ScholarPubMed