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The saga of schistosome migration and attrition

Published online by Cambridge University Press:  06 March 2009

R. A. WILSON
R. A. WILSON*
Affiliation:
Department of Biology, University of York, PO Box 373, York YO10 5YW
*
*Tel: 44 (0)1904 328600. Fax: 44 (0)1904 328505. E-mail: raw3@york.ac.uk
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Summary

Schistosomes infect the mammalian host by direct penetration of the skin and must then undergo a protracted migration to the site of parasitization, for Schistosoma mansoni the hepatic portal vasculature. This article reviews the work published roughly between 1976 and 1986 that clarified our understanding of the process in the laboratory mouse. A combination of histopathology, larval injection experiments and autoradiographic tracking revealed that migration involved one to several circuits of the pulmonary-systemic vasculature before chance delivery in cardiac output to splanchnic arteries that lead indirectly to the portal tract. The kinetics of migration through different capillary beds was established, with the lungs of naïve mice not the skin proving the greatest obstacle; a proportion of schistosomula entered the alveoli from where they did not recover. The ‘immunity’ displayed by mice with a chronic infection was shown to be an artefact of a ‘leaky’ hepatic portal system, generated as a result of egg-induced hepatic pathology. The blockade of pulmonary migration was exacerbated in mice vaccinated with irradiated cercariae by immune-mediated inflammatory foci that developed around lung schistosomula thus decreasing the proportion that matured, but parasite elimination was a prolonged process, not an acute cytolytic ‘hit.’

Keywords

Schistosoma mansoniautoradiographic trackingirradiated vaccinechronic infectionMus musculus
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 12: Special Centenary Issue – Parasitology 1908–2008 , October 2009 , pp. 1581 - 1592
Copyright
Copyright © 2009 Cambridge University Press

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References

REFERENCES

Bickle, Q. D., Taylor, M. G., Doenhoff, M. J. and Nelson, G. S. (1979). Immunization of mice with gamma-irradiated intramuscularly injected schistosomula of Schistosoma mansoni. Parasitology 79, 209–222.CrossRefGoogle ScholarPubMed
Christensen, N. O. (1977). A method for the in vivo labelling of Schistosoma mansoni and S. intercalatum cercariae with radioselenium. Zeitschrift für Parasitenkunde 54, 275–288.CrossRefGoogle ScholarPubMed
Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–147.CrossRefGoogle ScholarPubMed
Clegg, J. A. and Smithers, S. R. (1968). Death of schistosome cercariae during penetration of the skin. II. Penetration of mammalian skin by Schistosoma mansoni. Parasitology 58, 111–128.CrossRefGoogle ScholarPubMed
Coulson, P. S. and Wilson, R. A. (1989). Portal shunting and resistance to Schistosoma mansoni in 129 strain mice. Parasitology 99, 383–389.CrossRefGoogle ScholarPubMed
Crabtree, J. E. and Wilson, R. A. (1980). Schistosoma mansoni: a scanning electron microscope study of the developing schistosomulum. Parasitology 81, 553–564.CrossRefGoogle ScholarPubMed
Crabtree, J. E. and Wilson, R. A. (1985). Schistosoma mansoni: an ultrastructural examination of skin migration in the hamster cheek pouch. Parasitology 91, 111–120.CrossRefGoogle ScholarPubMed
Crabtree, J. E. and Wilson, R. A. (1986 a). The role of pulmonary cellular reactions in the resistance of vaccinated mice to Schistosoma mansoni. Parasite Immunology 8, 265–285.CrossRefGoogle ScholarPubMed
Crabtree, J. E. and Wilson, R. A. (1986 b). Schistosoma mansoni: an ultrastructural examination of pulmonary migration. Parasitology 92, 343–354.CrossRefGoogle ScholarPubMed
Dean, D. A., Bukowski, M. A. and Clark, S. S. (1981). Attempts to transfer the resistance of Schistosoma mansoni-infected and irradiated cercaria-immunized mice by means of parabiosis. American Journal of Tropical Medicine and Hygiene 30, 113–120.CrossRefGoogle ScholarPubMed
Dean, D. A., Minard, P., Murrell, K. D. and 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, 957–965.CrossRefGoogle Scholar
Dean, D. A., Minard, P., Stirewalt, M. A., Vannier, W. E. and Murrell, K. D. (1978 b). Resistance of mice to secondary infection with Schistosoma mansoni. I. Comparison of bisexual and unisexual initial infections. American Journal of Tropical Medicine and Hygiene 27, 951–956.CrossRefGoogle ScholarPubMed
Dessein, A., Samuelson, J. C., Butterworth, A. E., Hogan, M., Sherry, B. A., Vadas, M. A. and David, J. R. (1981). Immune evasion by Schistosoma mansoni: loss of susceptibility to antibody or complement-dependent eosinophil attack by schistosomula cultured in medium free of macromolecules. Parasitology 82, 357–374.CrossRefGoogle ScholarPubMed
Dillon, G. P., Feltwell, T., Skelton, J., Coulson, P. S., Wilson, R. A. and Ivens, A. C. (2008). Altered patterns of gene expression underlying the enhanced immunogenicity of radiation-attenuated schistosomes. PLoS Neglected Tropical Diseases 2, e240.CrossRefGoogle ScholarPubMed
Eberl, M., Langermans, J. A., Frost, P. A., Vervenne, R. A., Van Dam, G. J., Deelder, A. M., Thomas, A. W., Coulson, P. S. and Wilson, R. A. (2001). Cellular and humoral immune responses and protection against schistosomes induced by a radiation-attenuated vaccine in chimpanzees. Infection and Immunity 69, 5352–5362.CrossRefGoogle ScholarPubMed
Georgi, J. R. (1982). Schistosoma mansoni: quantification of skin penetration and early migration by differential external radioassay and autoradiography. Parasitology 84, 263–281.CrossRefGoogle ScholarPubMed
Georgi, J. R., Dean, D. A. and Chandiwanna, S. K. (1982). Quantification of Schistosoma mansoni in mouse lungs by radioassay and autoradiography of 75Se-labeled schistosomula. Journal of Parasitology 68, 1092–1095.CrossRefGoogle ScholarPubMed
Georgi, J. R., Dean, D. A. and Mangold, B. L. (1983). Schistosoma mansoni: temporal distribution of radioselenium-labelled schistosomula in lungs of mice during the first two weeks of infection. Parasitology 86, 31–36.CrossRefGoogle ScholarPubMed
Georgi, J. R., Wade, S. E. and Dean, D. A. (1986). Attrition and temporal distribution of Schistosoma mansoni and S. haematobium schistosomula in laboratory mice. Parasitology 93, 55–70.CrossRefGoogle ScholarPubMed
Harrop, R. and Wilson, R. A. (1993). Irradiation of Schistosoma mansoni cercariae impairs neuromuscular function in developing schistosomula. Journal of Parasitology 79, 286–289.CrossRefGoogle ScholarPubMed
Kariuki, T. M., Farah, I. O., Yole, D. S., Mwenda, J. M., Van Dam, G. J., Deelder, A. M., Wilson, R. A. and Coulson, P. S. (2004). Parameters of the attenuated schistosome vaccine evaluated in the olive baboon. Infection and Immunity 72, 5526–5529.CrossRefGoogle ScholarPubMed
Knopf, P. M., Cioli, D., Mangold, B. L. and Dean, D. A. (1986). Migration of Schistosoma mansoni in normal and passively immunized laboratory rats. American Journal of Tropical Medicine and Hygiene 35, 1173–1184.CrossRefGoogle ScholarPubMed
Kruger, S. P., Heitman, L. P., Van Wyk, J. A. and McCully, R. M. (1969). The route of migration of Schistosoma mattheei from the lungs to the liver in sheep. Journal of the South African Veterinary Medical Association 40, 39–43.Google Scholar
Lawson, J. R. and Wilson, R. A. (1980). Metabolic changes associated with the migration of the schistosomulum of Schistosoma mansoni in the mammal host. Parasitology 81, 325–336.CrossRefGoogle ScholarPubMed
Laxer, M. J. and Tuazon, C. U. (1992). Migration of 75Se-methionine-labeled Schistosoma japonicum in normal and immunized mice. Journal of Infectious Diseases 166, 1133–1138.CrossRefGoogle ScholarPubMed
Lewis, F. A. and Colley, D. G. (1977). Modification of the lung recovery assay for schistosomula and correlations with worm burdens in mice infected with Schistosoma mansoni. Journal of Parasitology 63, 413–417.CrossRefGoogle ScholarPubMed
Long, E., Harrison, R., Bickle, Q., Bain, J., Nelson, G. and Doenhoff, M. (1980). Factors affecting the acquisition of resistance against Schistosoma mansoni in the mouse. The effect of varying the route and the number of primary infections, and the correlation between the size of the primary infection and the degree of resistance that is acquired. Parasitology 81, 355–371.CrossRefGoogle ScholarPubMed
Madden, R. E., Paparo, A. and Schwartz, M. (1968). Limiting vascular diameters in various organs: as determined by microspheres. Archives of Surgery 96, 130–137.CrossRefGoogle ScholarPubMed
Mangold, B. L. and Dean, D. A. (1983). Autoradiographic analysis of Schistosoma mansoni migration from skin to lungs in naive mice. Evidence that most attrition occurs after the skin phase. American Journal of Tropical Medicine and Hygiene 32, 785–789.CrossRefGoogle ScholarPubMed
Mangold, B. L. and Dean, D. A. (1984). The migration and survival of gamma-irradiated Schistosoma mansoni larvae and the duration of host-parasite contact in relation to the induction of resistance in mice. Parasitology 88, 249–265.CrossRefGoogle Scholar
Mangold, B. L., Dean, D. A., Coulson, P. S. and Wilson, R. A. (1986). Site requirements and kinetics of immune-dependent elimination of intravascularly administered lung stage schistosomula in mice immunized with highly irradiated cercariae of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 35, 332–344.CrossRefGoogle ScholarPubMed
Mastin, A., Bickle, Q. D. and Wilson, R. A. (1985). An ultrastructural examination of irradiated, immunizing schistosomula of Schistosoma mansoni during their extended stay in the lungs. Parasitology 91, 101–110.CrossRefGoogle ScholarPubMed
Mastin, A. J., Bickle, Q. D. and Wilson, R. A. (1983). Schistosoma mansoni: migration and attrition of irradiated and challenge schistosomula in the mouse. Parasitology 87, 87–102.CrossRefGoogle ScholarPubMed
McHugh, S. M., Coulson, P. S. and Wilson, R. A. (1987 a). Pathologically induced alterations in the dimensions of the hepatic portal vasculature of mice infected with Schistosoma mansoni. Parasitology 94, 69–80.CrossRefGoogle ScholarPubMed
McHugh, S. M., Coulson, P. S. and Wilson, R. A. (1987 b). The relationship between pathology and resistance to reinfection with Schistosoma mansoni in mice: a causal mechanism of resistance in chronic infections. Parasitology 94, 81–91.CrossRefGoogle ScholarPubMed
Miller, K. L. and Smithers, S. R. (1980). Schistosoma mansoni: the attrition of a challenge infection in mice immunized with highly irradiated live cercariae. Experimental Parasitology 50, 212–221.CrossRefGoogle ScholarPubMed
Miller, P. and Wilson, R. A. (1978). Migration of the schistosomula of Schistosoma mansoni from skin to lungs. Parasitology 77, 281–302.CrossRefGoogle ScholarPubMed
Miller, P. and Wilson, R. A. (1980). Migration of the schistosomula of Schistosoma mansoni from the lungs to the hepatic portal system. Parasitology 80, 267–288.CrossRefGoogle Scholar
Minard, P., Dean, D. A., Jacobson, R. H., Vannier, W. E. and Murrell, K. D. (1978 a). Immunization of mice with cobalt-60 irradiated Schistosoma mansoni cercariae. American Journal of Tropical Medicine and Hygiene 27, 76–86.CrossRefGoogle ScholarPubMed
Minard, P., Dean, D. A., Vannier, W. E. and Murrell, K. D. (1978 b). Effect of immunization on migration of Schistosoma mansoni through lungs. American Journal of Tropical Medicine and Hygiene 27, 87–93.CrossRefGoogle ScholarPubMed
Sher, A., Mackenzie, P. and Smithers, S. R. (1974). Decreased recovery of invading parasites from the lungs as a parameter of acquired immunity to schistosomiasis in the mouse. Journal of Infectious Diseases 130, 626–633.CrossRefGoogle ScholarPubMed
Sher, A., Smithers, S. R. and Mackenzie, P. (1975). Passive transfer of acquired resistance to Schistosoma mansoni in laboratory mice. Parasitology 70, 347–357.CrossRefGoogle ScholarPubMed
Smithers, S. R. and Gammage, K. (1980). 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, 289–300.CrossRefGoogle Scholar
Smithers, S. R. and Terry, R. J. (1969 a). Immunity in schistosomiasis. Annals of the New York Academy of Sciences 160, 826–840.CrossRefGoogle ScholarPubMed
Smithers, S. R. and Terry, R. J. (1969 b). The immunology of schistosomiasis. Advances in Parasitology 7, 41–93.CrossRefGoogle ScholarPubMed
Standen, O. D. (1953). The penetration of the cercariae of Schistosoma mansoni into the skin and lymphatics of the mouse. Transactions of the Royal Society of Tropical Medicine and Hygiene 47, 292–298.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1959). Chronological analysis, pattern and rate of migration of cercariae of Schistosoma mansoni in body, ear and tail skin of mice. Annals of Tropical Medicine and Parasitology 53, 400–413.CrossRefGoogle ScholarPubMed
Von Lichtenberg, F., Correa-Oliveira, R. and Sher, A. (1985). The fate of challenge schistosomula in the murine anti-schistosome vaccine model. American Journal of Tropical Medicine and Hygiene 34, 96–106.CrossRefGoogle ScholarPubMed
Wheater, P. R. and Wilson, R. A. (1979). Schistosoma mansoni: a histological study of migration in the laboratory mouse. Parasitology 79, 49–62.CrossRefGoogle ScholarPubMed
Wilks, N. E. (1967). Lung-to-liver migration of schistosomes in the laboratory mouse. American Journal of Tropical Medicine and Hygiene 16, 599–605.CrossRefGoogle ScholarPubMed
Wilson, R. A. (1980). Is immunity to Schistosoma mansoni in the chronically infected laboratory mouse an artefact of pathology? In Proceedings of the Third Multicolloquium of Parasitology, p. 37. European Federation of Parasitologists.Google Scholar
Wilson, R. A., Coulson, P. S. and Dixon, B. (1986). Migration of the schistosomula of Schistosoma mansoni in mice vaccinated with radiation-attenuated cercariae, and normal mice: an attempt to identify the timing and site of parasite death. Parasitology 92, 101–116.CrossRefGoogle ScholarPubMed
Wilson, R. A., Coulson, P. S. and 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.CrossRefGoogle Scholar
Wilson, R. A., Coulson, P. S., Sturrock, R. F. and Reid, G. D. (1990). Schistosome migration in primates: a study in the olive baboon (Papio anubis). Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 80–83.CrossRefGoogle ScholarPubMed
Wilson, R. A., Draskau, T., Miller, P. and Lawson, J. R. (1978). Schistosoma mansoni: the activity and development of the schistosomulum during migration from the skin to the hepatic portal system. Parasitology 77, 57–73.CrossRefGoogle Scholar
Wilson, R. A. and Lawson, J. R. (1980). An examination of the skin phase of schistosome migration using a hamster cheek pouch preparation. Parasitology 80, 257–266.CrossRefGoogle ScholarPubMed
Yolles, T. K., Moore, D. V. and Meleney, H. E. (1949). Post-cercarial development of Schistosoma mansoni in the rabbit and hamster after intraperitoneal and percutaneous infection. Journal of Parasitology 35, 276–294.CrossRefGoogle ScholarPubMed