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The relationship between pathology and resistance to reinfection with Schistosoma mansoni in mice: a causal mechanism of resistance in chronic infections

Published online by Cambridge University Press:  06 April 2009

S. M. McHugh ,
Patricia S. Coulson  and
R. A. Wilson
S. M. McHugh
Affiliation:
Department of Biology, University of York, Heslington, York YO1 5DD
Patricia S. Coulson
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
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Summary

The development of resistance in mice to reinfection with Schistosoma mansoni was recorded during an early chronic infection, and compared with hepatic portal pathological and vascular changes. The latter were assessed using a microsphere injection technique. The degree of acquired resistance was directly dependent on the patent worm burden and the time post-infection. Strong correlations were noted between the development of resistance and the appearance of parasite eggs in the lungs and spleens of infected hosts. Weaker associations were present between resistance and other aspects of the disease pathology, such as portal hypertension and organ weights. The appearance of injected microspheres in the lungs and spleens correlated well with the appearance of eggs in those organs and with the development of resistance. The levels of resistance had risen and microspheres were detected in the lungs, before the development of major extra-hepatic, porta-systemic collateral vessels. It is concluded that intra-hepatic vascular alterations may be a causal factor in the development of resistance, preventing the sequestration of migrating schistosomula in the liver. It is estimated that as much as 70–75% of the recorded resistance can be attributed to this immunologically non-specific mechanism.

Type
Research Article
Information
Parasitology , Volume 94 , Issue 1 , February 1987 , pp. 81 - 91
Copyright
Copyright © Cambridge University Press 1987

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References

Bickle, Q. D., Bain, J., McGregor, A. & Doenhoff, M. (1979). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. III. The failure of primary infections with cercariae of one sex to induce resistance to reinfection. Transactions of the Royal Society of Tropical Medicine and Hygiene 73, 37–41.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Ford, M. J. & Andrews, B. J. (1983). Studies on the development of anti-schisto somula surface antibodies by mice exposed to irradiated cercariae, adults and/or eggs of Schistosoma mansoni. Parasite Immunology 5, 499–511.Google Scholar
Bickle, Q. D., Long, E. G., James, E. R., Doenhoff, M. J. & Festing, M. (1980). Schistosoma mansoni: Influence of the host's sex, age and strain on resistance to reinfection. Experimental Parasitology 50, 222–32.CrossRefGoogle ScholarPubMed
Bradley, D. J. & McCullough, F. S. (1973). Egg output and the epidemiology of endemic Schistosoma haematobium. II. An analysis of the epidemiology of endemic S. haematobium. Trans actions of the Royal Society of Tropical Medicine and Hygiene 67, 491–500.Google Scholar
Colley, D. G. & Freeman, G. L. (1980). Differences in adult Schistosoma mansoni worm burden requirements for the establishment of resistance to reinfection in inbred mice. I. CBA/J and C57B1/6 mice. American Journal of Tropical Medicine and Hygiene 29, 1279–85.Google Scholar
Colley, D. G. & Freeman, G. L. (1983). Differences in adult Schistosoma mansoni worm burden requirements for the establishment of resistance to reinfection in mice. II. C57BI/KsJ, SWR/J, SJL/J, Balb/CAnN, DBA/2N, A/J, B10. A(3R), and B10. A(5R) mice. American Journal of Tropical Medicine and Hygiene 32, 543–9.Google Scholar
Dean, D. A. (1983). Schistosoma and related genera: Acquired resistance in mice. Experimental Parasitology 55, 1–104.CrossRefGoogle ScholarPubMed
Dean, D. A., Bukowski, M. A. & Cheever, A. W. (1981 a). Relationship between acquired resistance, portal hypertension and lung granulomas in ten strains of mice infected with Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 30, 806–14.Google Scholar
Dean, D. A., Bukowski, M. A. & Clarke, S. S. (1981 b). Attempts to transfer the resistance of Schistosoma mansoni– infected and irradiated cercariae immunised mice by means of parabiosis. American Journal of Tropical Medicine and Hygiene 30, 113–20.Google Scholar
Dean, D. A., Minard, P., Murrell, K. D. & Vannier, W. E. (1978). Resistance of mice to secondary infection with Schistosoma mansoni. II. Evidence for a correlation between egg deposition and worm elimination. American Journal of Tropical Medicine and Hygiene 27, 957–65.CrossRefGoogle Scholar
Doenhoff, M. J., Bickle, Q. D., Bain, J., Webbe, G. & Nelson, G. (1980). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. V. Reduction in the degree of resistance to reinfection after chemotherapeutic elimination of recently patent primary infections. Journal of Helminthology 54, 7–16.CrossRefGoogle ScholarPubMed
Doenhoff, M. J. & Long, E.G. (1979). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. IV. The inability of T-cell deprived mice to resist reinfection, and other in vivo studies on the mechanisms of resistance. Parasitology 78, 171–83.Google Scholar
Doenhoff, M. J., Musallam, R., Bain, J. & McGregor, A. (1979). Schistosoma mansoni infections in T-cell deprived mice, and the ameliorating effect of administering chronic infection serum. I. Pathogenesis. American Journal of Tropical Medicine and Hygiene 28, 260–73.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Pearson, S., Dunne, D. W., Bickle, Q. D., Lucas, S., Bain, J., Musallam, R. & Hassounah, O. (1981). Immunological control of hepatotoxicity and parasite egg excretions in Schistosoma mansoni infections: Stage specificity of the reactivity of immune sera in T-cell deprived mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 41–53.Google Scholar
Domingo, E. O. & Warren, K. S. (1968). Endogenous desensitisation: changing host granulomatous response to schistosome eggs at different stages of infection with Schistosoma mansoni. American Journal of Pathology 52, 369–77.Google Scholar
Harn, D. A., Mitsuyama, M. & David, J. R. (1984). Schistosoma mansoni: Anti-egg monoclonal antibodies protect against cercarial challenge in vivo. Journal of Experimental Medicine 159, 1371–87.Google Scholar
Harrison, R. A., Bickle, Q. D. & Doenhoff, M. J. (1982). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. IX. Evidence that the mechanisms which mediate resistance during early patent infections may lack immunological specificity. Parasitology 84, 93–110.Google Scholar
James, S. L. & Cheever, A. W. (1985). Comparison of immune responses between high and low responder mice in the concomitant immunity and vaccine models of resistance to Schistosoma mansoni. Parasitology 91, 301–15.CrossRefGoogle ScholarPubMed
James, S. L., Leonard, E. J. & Meltzer, M. S. (1982). Macrophages as effector cells in murine schistosomiasis. IV. Coincident induction of macrophage activation for extracellular killing of schistosomula and tumor cells. Cellular Immunology 74, 86–96.CrossRefGoogle ScholarPubMed
James, S. L., Skamene, E. & Meltzer, M. S. (1983). Macrophages as effector cells of protective immunity in murine schistosomiasis. Journal of Immunology 131, 948–54.Google Scholar
Long, E., Harrison, R., Bickle, Q., Bain, J., Nelson, G. & Doenhoff, M. (1980). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. The effect of varying the route and number of primary infections, and the correlation between the size of the primary infection and the degree of resistance acquired. Parasitology 81, 355–71.Google Scholar
Mahmoud, A. A. F., Warren, K. S. & Peters, P. A. (1975). A role for the eosinophil in acquired resistance to Schistosoma mansoni infection as determined by anti-eosinophil serum. Journal of Experimental Medicine 142, 805–13.CrossRefGoogle Scholar
McHugh, S. M. (1984). The relationship between egg-induced pathology and the development of resistance to reinfection in NMRI mice infected with Schistosoma mansoni. D. Phil. thesis, University of York.Google Scholar
McHugh, S. M., Coulson, P. S. & Wilson, R. A. (1987). Pathologically induced alterations in the dimensions of the hepatic portal vasculature in mice infected with Schistosoma mansoni. Parasitology 94, 69–80.CrossRefGoogle ScholarPubMed
Moloney, N. A. & Webbe, G. (1984). Factors affecting the acquisition of resistance against Schistosoma japonicum in the mouse. II. Evidence that resistance to reinfection is not mediated by specific effector mechanisms. Parasitology 89, 361–8.CrossRefGoogle Scholar
Moloney, N. A., Webbe, G. & Luty, A. (1984). Factors affecting the acquisition of resistance against Schistosoma japonicum in the mouse. I. The correlation between egg deposition and worm elimination. Parasitology 89, 345–60.CrossRefGoogle ScholarPubMed
Ramalho-Pinto, F. J., McLaren, D. J. & Smithers, S. R. (1978). Complement mediated killing of schistosomula of Schistosoma mansoni by rat eosinophils in vitro. Journal of Experimental Medicine 147, 147–56.Google Scholar
Ramalho-Pinto, F. J., de Rossi, R. & Smithers, S. R. (1979). Murine Schistosomiasis mansoni; Anti-schistosomula antibodies and the IgG subclasses involved in the complement and eosinophil mediated killing of schistosomula in vitro. Parasite Immunology 1, 295.Google Scholar
Smithebs, S. R. & Gammage, K. (1980). The recovery of Schistosoma mansoni from the skin, lungs and hepatic portal system of naive mice and mice previously exposed to S. mansoni. Evidence for two phases of parasite attrition in immune mice. Parasitology 80, 269–300.Google Scholar
Warren, K. S., Domingo, E. O. & Cowan, R. B. T. (1967). Granuloma formation around eggs as a manifestation of delayed hypersensitivity. American Journal of Pathology 51, 735–56.Google ScholarPubMed
Wilson, R. A. (1980). Is immunity to Schistosoma mansoni in the chronically infected laboratory mouse an artefact of pathology? proceedings of the Third European Multicolloquium of Parasitology, p. 37.Google Scholar
Wilson, R. A., Coulson, P. S. & McHugh, S. M. (1983). A significant part of the concomitant immunity of mice to Schistosoma mansoni is the consequence of a leaky hepatic portal system, not immune killing. Parasite Immunology 5, 595–601.Google Scholar