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Studies on heterologous resistance between Schistosoma mansoni and Fasciola hepatica in inbred rats

Published online by Cambridge University Press:  06 April 2009

M. J. Ford
Affiliation:
London School of Hygiene and Tropical Medicine, Winches Farm Field Station, 395 Hatfield Road, St Albans, Herts AL4 0XQ
M. G. Taylor
Affiliation:
London School of Hygiene and Tropical Medicine, Winches Farm Field Station, 395 Hatfield Road, St Albans, Herts AL4 0XQ
S. M. McHugh
Affiliation:
Department of Biology, University of York, Heslington, York YO1 5DD
R. A. Wilson
Affiliation:
Department of Biology, University of York, Heslington, York YO1 5DD
D. L. Hughes
Affiliation:
AFRC Institute for Research on Animal Diseases, Compton, Newbury, Berks.

Summary

Fischer rats infected with Fasciola hepatica showed significant resistance to Schistosoma mansoni challenge, and vice versa, whereas immunization with 20 Krad-irradiated S. mansoni cercariae failed to protect against F. hepatica challenge, but did protect against homologous challenge. When groups of rats received intraperitoneal implants of newly excysted juvenile flukes, 20- to 22-day-old juveniles, or 8- to 10-week-old flukes, none was significantly protected against S. mansoni challenge, whereas juvenile implants did protect against homologous F. hepatica challenge. In passive transfer experiments in rats, serum from F. hepatica-infected rats or rabbits protected recipients against homologous, but not heterologous challenge, and serum from rats vaccinated with 20 Krad-irradiated S. mansoni cercariae protected recipients against homologous, but not heterologous challenge. These experiments provide evidence that the mechanisms involved in homologous and heterologous resistance are different, the latter lacking immunological specificity. Microsphere injections in F. hepatica-infected rats demonstrated ‘shunting’ from the portal system to the systemic circulation. If migrating schistosomula are also ‘shunted’ in Fasciola-infected rats, this, rather than immunologically specific effector mechanisms, might explain their failure to establish in the portal system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1987

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References

Anderson, J. C., Hughes, D. L. & Harness, E. (1975). The response of rats to subcutaneous implantation with Fasciola hepatica. British Veterinary Journal 131, 509–18.CrossRefGoogle ScholarPubMed
Armour, J. & Dargie, J. D. (1974). Immunity to Fasciola hepatica in the rat. Successful transfer of immunity by lymphoid cells and by serum. Experimental Parasitology 35, 381–8.CrossRefGoogle ScholarPubMed
Bickle, Q. D. & Ford, M. J. (1982). Studies on the surface antigenicity and susceptibility to antibody-dependent killing of developing schistosomular using sera from chronically infected mice and mice vaccinated with irradiated cercariae. Journal of Immunology 128, 2101–6.CrossRefGoogle Scholar
Boray, J. C. (1969). Experimental fascioliasis in Australia. Advances in Parasitology 7, 95210.CrossRefGoogle ScholarPubMed
Chapman, C. B. & Mitchell, G. F. (1982). Fasciola hepatica: comparative studies on fascioliasis in rats and mice. International Journal for Parasitology 12, 8191.CrossRefGoogle ScholarPubMed
Christensen, N. O., Monrad, J., Nansen, P & Fransden, F. (1980). Schistosoma mansoni and Fasciola hepatica: cross resistance in mice with single sex infections. Experimental Parasitology 49, 116–21.CrossRefGoogle Scholar
Christensen, N. O., Nansen, P., Fransden, F., Bjorneboe, A. & Monrad, J. (1978). Schistosoma mansoni and F. hepatica cross resistance in mice. Experimental Parasitology 46, 113–20.CrossRefGoogle Scholar
Doy, T. G. (1980). Examination of the immune response of rats to infection with Fasciola hepatica. Ph.D. thesis, Brunei University.Google Scholar
Eriksen, L. & Flagstead, T. (1974). Fasciola hepatica: influences of extra-hepatic adult flukes on infection and immunity in rats. Experimental Parasitology 35, 411–17.CrossRefGoogle Scholar
Ford, M. J. (1985). Studies on the mechanisms of induction and expression of acquired resistance to Schistosoma mansoni. Ph.D. thesis, University of London.Google Scholar
Ford, M. J., Bickle, Q. D. & Taylor, M. G. (1984 b). Immunization of rats against Schistosoma mansoni using irradiated cercariae, lung schistosomula and liver-stage worms. Parasitology 89, 327–34.CrossRefGoogle ScholarPubMed
Ford, M. J., Bickle, Q. D., Taylor, M. G. & Andrews, B. J. (1984 a). Passive transfer of resistance and the site of attrition of the challenge infection in rats vaccinated with highly irradiated cercariae of Schistosoma mansoni. Parasitology 89, 461–82.CrossRefGoogle ScholarPubMed
Harness, E., Doy, T. G. & Hughes, D. L. (1977). The early migratory behaviour of young Fasciola hepatica in sensitized mice. International Journal for Parasitology 7, 51–4.CrossRefGoogle ScholarPubMed
Haroun, E. M., Hammond, J. A. & Sewell, M. M. H. (1981). Passive transfer of humoral resistance to Fasciola hepatica in rats and rabbits. Research in Veterinary Science 30, 309–11.CrossRefGoogle ScholarPubMed
Harrison, R. A., Bickle, Q. D. & Doenhoff, M. J. (1982). Factors affecting acquisition of resistance against Schistosoma mansoni in the mouse. Evidence that the mechanisms which mediate resistance during early patent infections may lack immunological specificity. Parasitology 84, 93110.CrossRefGoogle ScholarPubMed
Hayes, T. J., Bailer, J. & Mitrovic, M. (1974 a). Serum transfer of immunity to Fasciola hepatica in rats. Journal of Parasitology 60, 722–3.CrossRefGoogle ScholarPubMed
Hayes, T. J., Bailer, J. & Mitrovic, M. (1974 b). Studies on serum transfer of immunity to Fasciola hepatica in rats. Journal of Parasitology 60, 930–4.CrossRefGoogle Scholar
Hillyer, G. V. (1981). Effects of Schistosoma mansoni on challenge infections with Fasciola hepatica in mice. Journal of Parasitology 48, 731–3.CrossRefGoogle Scholar
Hillyer, G. V., Garcia-Blanco, M. & Del Llano de Diaz, A. (1975). A new approach to the study of immunity to schistosomiasis. Boletin de la Asociacion Medica de Puerto Rico 67, 381–5.Google Scholar
Howell, M. J. (1979). Vaccination of rats against Fasciola hepatica. Journal of Parasitology 65, 817–19.CrossRefGoogle ScholarPubMed
Howell, M. J. & Sanderman, R. M. (1979). Fasciola hepatica: some properties of a precipitate which forms when metacercariae are cultured in immune rat serum. International Journal for Parasitology 9, 41–5.CrossRefGoogle ScholarPubMed
Howell, M. J., Sanderman, R. M. & Rajasekariah, G. R. (1977). In vivo and in vitro studies of the effects of immune rat serum on Fasciola hepatica. International Journal for Parasitology 7, 367–71.CrossRefGoogle ScholarPubMed
Hughes, D. L., Harness, E. & Doy, T. G. (1981). The different stages of Fasciola hepatica capable of inducing immunity and the susceptibility of various stages to immunological attack in the sensitized rat. Research in Veterinary Science 30, 93–8.CrossRefGoogle Scholar
Joky, A., Cornu, M., Louis, D. & Grimaud, J. A. (1978). Polyvinylchloride (PVC) particle implantation in the mouse liver. A technique for experimental study of schistosome egg-induced liver pathology. Experientia 34, 547–9.CrossRefGoogle Scholar
Kendall, S. B. & Parfitt, J. W. (1975). Chemotherapy of infection with Fasciola hepatica in cattle. Veterinary Record 97, 912.CrossRefGoogle ScholarPubMed
Lang, B. Z. (1974). Host-parasite relationships of Fasciola hepatica in the white mouse. V. Age of fluke responsible for the induction of acquired immunity. Journal of Parasitology 60, 90–2.CrossRefGoogle ScholarPubMed
Lang, B. Z. & Dronen, N. O. (1972). Host–parasite relationships of Fasciola hepatica in the white mouse. IV. Studies on worm transfer and the induction of acquired immunity by worms of different ages. Journal of Parasitology 58, 84–7.CrossRefGoogle ScholarPubMed
Lehner, R. P. & Sewell, M. M. H. (1979). Attempted immunization of laboratory animals with metabolic antigens of Fasciola hepatica. Veterinary Science Communications 2, 337–40.CrossRefGoogle Scholar
Mangold, B. L. & Knopf, P. M. (1981). Host protective humoral immune responses to Schistosoma mansoni infections in the rat. Kinetics of hyperimmune serum-dependent sensitivity and elimination of schistosomes in a passive transfer system. Parasitology 83, 559–74.CrossRefGoogle Scholar
Murray, M. & Rushton, B. (1975). The pathology of Fascioliasis, with particular reference to fibrosis. In Pathology of Parasitic Diseases, vol. 13 (ed. Taylor, A. E. R. and Muller, R.), pp. 2741. Oxford: Blackwell Scientific Publications.Google Scholar
Phillips, S. M., Reid, W. A., Bruce, J. I., Hedlund, K., Colvin, R. C., Campbell, R., Diggs, C. L. & Sadun, E. H. (1975). The cellular and humoral response to Schistosoma mansoni infection in the rat. I. Mechanisms during initial exposure. Cellular Immunology 19, 99116.CrossRefGoogle Scholar
Rajasekariah, G. R. & Howell, M. J. (1978). Fasciola hepatica: role of developmental stages in the rat's resistance to challenge. Experimental Parasitology 44, 233–8.CrossRefGoogle ScholarPubMed
Rajasekariah, G. R. & Howell, M. J. (1979). Fasciola hepatica in rats: transfer of immunity by serum and cells from infected to naive animals. Journal of Parasitology 65, 481–7.CrossRefGoogle ScholarPubMed
Rajasekariah, G. R., Mitchell, G. F., Chapman, C. B. & Montague, P. E. (1979). Fasciola hepatica: protection against infection in rats injected with ES products of immature worms. Parasitology 79, 393400.CrossRefGoogle Scholar
Sinclair, K. B. (1973). Resistance of sheep to Fasciola hepatica: studies on the development and pathogenicity of challenge infections. British Veterinary Journal 129, 236–50.CrossRefGoogle ScholarPubMed
Tielens, A. G. M., Van der Meer, P. & Van den Burgh, S. G. (1981). Fasciola hepatica: large scale, in vitro excystment of metacercariae and subsequent isolation of juvenile liver flukes. Experimental Parasitology 51, 812.CrossRefGoogle ScholarPubMed
Wilson, R. A., Coulson, P. S. & McHugh, S. M. (1983). A significant part of ‘concomitant immunity’ in mice to Schistosoma mansoni is the consequence of a leaky hepatic portal system, not of immune killing. Parasite Immunology 5, 595601.CrossRefGoogle Scholar
Wroblewski, F. & La Due, J. S. (1956). Serum glutamic pyruvic transaminase in cardiac and hepatic tissue. Proceedings of the Society of Experimental Biology and Medicine 91, 569–71.CrossRefGoogle Scholar