Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-17T22:05:50.168Z Has data issue: false hasContentIssue false

Pathologically induced alterations in the dimensions of the hepatic portal vasculature of mice infected with Schistosoma mansoni

Published online by Cambridge University Press:  06 April 2009

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

Summary

Alterations in the hepatic portal vasculature of NMRI mice infected with Schistosoma mansoni were assessed using a microsphere injection technique. The accumulation of eggs in the livers of infected mice and the development of portal hypertension were closely related to the worm pair burden during the first 15 weeks of infection. Individual variation between mice harbouring identical patent worm pair burdens was partially explained by the reduced fecundity of females from sexually biased infections. As eggs accumulated in the liver and portal hypertension increased, the number of injected microspheres escaping from the hepatic portal system rose in rank order of diameter from 9 μm through 15 μm and 25 μm to 50 μm. There was a strong correlation between the numbers of parasite eggs in the lungs and injected microspheres recovered from the lungs. The pattern of detection of microspheres in the lungs indicated a progressive increase in diameter of intra-hepatic porta-systemic connexions, followed by development of large-bore extra-hepatic collateral vessels. An accurate temporal profile of the pathological state of the host and the extent of collateral vessel formation was obtained. Injection of 141Ce-labelled microspheres demonstrated that the arterial supply to all organs of the body was affected by alterations in the micro-vasculature of the liver and lungs.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1987

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

Andrade, Z. A. & Brito, P. A. (1981). Evolution of schistosomal hepatic vascular lesions after specific chemotherapy. American Journal of Tropical Medicine and Hygiene 30, 1223–7.CrossRefGoogle ScholarPubMed
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 for Tropical Medicine and Hygiene 73, 3741.CrossRefGoogle ScholarPubMed
Bickle, Q. D., Ford, M. J. & Andrews, B. J. (1983). Studies on the development of an ti-schistosomula surface antibodies by mice exposed to irradiated cercariae, adults and/or eggs of Schistosoma mansoni. Parasite Immunology 5, 499511.CrossRefGoogle ScholarPubMed
Bloch, E. H. (1979). Inflammation in schistosomiasis. In Microcirculation in Inflammation. Bibliotheca anatomica, vol. 17, pp. 105–14. Basel: Karger.Google Scholar
Bloch, E. H., Wahab, M. F. A. & Warren, K. S. (1972). In vivo microscopic observations of the pathophysiology of hepatosplenic schistosomiasis in the mouse liver. American Journal of Tropical Medicine and Hygiene 21, 546–57.CrossRefGoogle ScholarPubMed
Campbell, R. C. (1974). Statistics for Biologists. Cambridge: Cambridge University Press.Google Scholar
Cheever, A. W. (1965). A comparative study of Schistosoma mansoni infections in mice, gerbils, multimammate rats and hamsters. I. The relation of portal hypertension to size of hepatic granulomas. American Journal of Tropical Medicine and Hygiene 14, 211–26.CrossRefGoogle ScholarPubMed
Cheever, A. W. (1968). Conditions affecting the accuracy of the potassium hydroxide digestion technique for counting Schistosoma mansoni eggs in the tissues of mice. Bulletin of the World Health Organization 39, 328–31.Google Scholar
Cheever, A. W. & Warren, K. S. (1963). Portal vein ligation of mice: portal hypertension, collateral circulation and blood flow. Journal of Applied Physiology 18, 405–7.CrossRefGoogle ScholarPubMed
Cheever, A. W. & Warren, K. S. (1964). Hepatic portal blood flow in mice with acute hepatosplenic Schistosomiasis mansoni. Transactions of the Royal Society for Tropical Medicine and Hygiene 58, 406–12.CrossRefGoogle 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.CrossRefGoogle 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. C57Bl/KsJ, SWR/J, SJL/J, Balb/CAnN, DBA/2N, A/J, BIO.A(3R), and B10.A(5R) mice. American Journal of Tropical Medicine and Hygiene 32, 543–9.CrossRefGoogle Scholar
Crombie, J. A. & Anderson, R. M. (1985). Population dynamics of Schistosoma mansoni in mice repeatedly exposed to infection Nature, London 316, 491–3.CrossRefGoogle Scholar
Dean, D. A. (1983). Schistosoma and related genera: acquired resistance in mice. Experimental Parasitology 55, 1104.CrossRefGoogle ScholarPubMed
Dean, D. A., Bukowski, M. A. & Cheever, A. W. (1981). 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.CrossRefGoogle ScholarPubMed
Dean, D. A., Minard, P., Murrell, K. D. & Vannier, W. E. (1978 a). 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
Dean, D. A., Minard, P., Stirewalt, M. A., Vannier, W. E. & Murrell, K. D. (1978 b). Resistance of mice to secondary infection with Schistosoma mansoni. I. Comparison of bisexual and unisexual infections. American Journal of Tropical Medicine and Hygiene 27, 937–56.Google Scholar
DeWitt, W. B. & Warren, K. S. (1959). Hepatosplenic schistosomiasis in mice. American Journal of Tropical Medicine and Hygiene 8, 440–6.CrossRefGoogle ScholarPubMed
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, 93110.CrossRefGoogle Scholar
Madden, R. E., Paparo, M. S. & Schwartz, M. (1968). Limiting vascular dimensions in various organs. Archives of Surgery 96, 130–7.CrossRefGoogle Scholar
Mangold, B. L. & Dean, D. A. (1983). Autoradiographic analysis of Schistosoma mansoni migration from the skin to the lungs in naive mice. Evidence that most attrition occurs after the skin phase. American Journal of Tropical Medicine and Hygiene 32, 785–9.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
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
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
Rappaport, A. M. (1980). Hepatic blood flow: morphologic aspects and physiological regulation. In Liver and Biliary Tract Physiology, vol. 1 (ed. Javitt, N. B. and Gayton, K. C.). International Reviews in Physiology 21, 163.Google Scholar
Smithers, S. R. & Terry, R. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of adult worms. Parasitology 55, 695770.CrossRefGoogle ScholarPubMed
Warren, K. S. (1980). The immunopathology of schistosomiasis. In The Host Invader Interplay (ed. H., van den Bossche), pp. 371–80. Amsterdam: Elsevier/North-Holland Biomedical Press.Google Scholar
Warren, K. S. (1982). Mechanisms of immunopathology in parasitic infections. In Immunology of Parasitic Infections. 2nd ed. (ed. Cohen, S. and K.S., Warren), pp. 116–37. Oxford: Blackwell Scientific Publications.Google Scholar
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, 595601.CrossRefGoogle Scholar