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The saga of schistosome migration and attrition

  • R. A. WILSON (a1)

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.’

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N. O. Christensen (1977). A method for the in vivo labelling of Schistosoma mansoni and S. intercalatum cercariae with radioselenium. Zeitschrift für Parasitenkunde 54, 275288.

J. E. Crabtree and R. A. Wilson (1986 a). The role of pulmonary cellular reactions in the resistance of vaccinated mice to Schistosoma mansoni. Parasite Immunology 8, 265285.

G. P. Dillon , T. Feltwell , J. Skelton , P. S. Coulson , R. A. Wilson and A. C. Ivens (2008). Altered patterns of gene expression underlying the enhanced immunogenicity of radiation-attenuated schistosomes. PLoS Neglected Tropical Diseases 2, e240.

M. Eberl , J. A. Langermans , P. A. Frost , R. A. Vervenne , G. J. Van Dam , A. M. Deelder , A. W. Thomas , P. S. Coulson and R. A. Wilson (2001). Cellular and humoral immune responses and protection against schistosomes induced by a radiation-attenuated vaccine in chimpanzees. Infection and Immunity 69, 53525362.

J. R. Georgi , D. A. Dean and S. K. Chandiwanna (1982). Quantification of Schistosoma mansoni in mouse lungs by radioassay and autoradiography of 75Se-labeled schistosomula. Journal of Parasitology 68, 10921095.

R. Harrop and R. A. Wilson (1993). Irradiation of Schistosoma mansoni cercariae impairs neuromuscular function in developing schistosomula. Journal of Parasitology 79, 286289.

T. M. Kariuki , I. O. Farah , D. S. Yole , J. M. Mwenda , G. J. Van Dam , A. M. Deelder , R. A. Wilson and P. S. Coulson (2004). Parameters of the attenuated schistosome vaccine evaluated in the olive baboon. Infection and Immunity 72, 55265529.

M. J. Laxer and C. U. Tuazon (1992). Migration of 75Se-methionine-labeled Schistosoma japonicum in normal and immunized mice. Journal of Infectious Diseases 166, 11331138.

F. A. Lewis and D. G. Colley (1977). Modification of the lung recovery assay for schistosomula and correlations with worm burdens in mice infected with Schistosoma mansoni. Journal of Parasitology 63, 413417.

R. E. Madden , A. Paparo and M. Schwartz (1968). Limiting vascular diameters in various organs: as determined by microspheres. Archives of Surgery 96, 130137.

S. R. Smithers and R. J. Terry (1969 b). The immunology of schistosomiasis. Advances in Parasitology 7, 4193.

O. D. Standen (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, 292298.

M. A. Stirewalt (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, 400413.

R. A. Wilson , P. S. Coulson and S. M. McHugh (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.

R. A. Wilson , P. S. Coulson , R. F. Sturrock and G. D. Reid (1990). Schistosome migration in primates: a study in the olive baboon (Papio anubis). Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 8083.

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