Hostname: page-component-78c5997874-s2hrs Total loading time: 0 Render date: 2024-11-06T07:10:40.318Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  06 April 2009

R. A Wilson
Affiliation:
Department of Biology, University of York, York YO1 5DD
Patricia S. Coulson
Affiliation:
Department of Biology, University of York, York YO1 5DD
B Dixon
Affiliation:
Department of Radiobiology, Gookridge Hospital, Leeds

Summary

The migration of the schistosomula of Schistosoma mansoni labelled with [75Se] has been followed from the skin to the hepatic portal system. Parasites were detected in all mouse tissues by compressed organ autoradiography. Two separate experiments were performed to track parasites in normal mice, and in mice previously vaccinated with irradiated cercariae. In normal mice, the profile of numbers of autoradiographic foci detected in the skin, lungs, systemic and splanchnic organs was described with time post-infection. The distribution of parasites to systemic organs, following exit from the lungs, paralleled the fractional distribution of cardiac output. Accumulation of schistosomula in the hepatic portal system was complete by day 21 post-infection. Only 2–3 passes of parasites around the vascular system would be required to produce the hepatic portal population. No significant decline in total foci was detected in the first 12 days post-infection. The majority of parasite elimination appeared to occur in the lungs as late as day 21, with lesser proportions in the systemic organs and skin infection site. The pattern of migration in vaccinated mice was similar to that in normal animals. One difference observed was the longer duration of stay in the skin; however, the majority of parasites eventually reached the lungs. The systemic phase of migration occurred on a reduced scale, as did accumulation of parasites in the hepatic portal system. The decline in total foci in vaccinated mice commenced approximately 7 days earlier than in normal mice and proceeded to a lower end-point. Again the majority of parasite elimination appeared to occur in the lungs with lesser proportions in the systemic organs and skin infection site. It is suggested that resistance to reinfection in vaccinated mice has two additive components which combine to retard the migration of schistosomula within the vasculature, preventing them from reaching the hepatic portal system.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1986

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

REFERENCES

Bickle, Q. D., Andrews, B. J., Doenhoff, M. J., Ford, M. J. & Taylor, M. G. (1985). Resistance against Schistosoma mansoni induced by highly irradiated infections: studies on species specificity of immunization and attempts to transfer resistance. Parasitology 90, 301–12.CrossRefGoogle ScholarPubMed
Dean, D. A., Bukowski, M. A. & Clark, S. S. (1981). Attempts to transfer the resistance of Schistosoma mansoni-infected and irradiated cercariae-immunized mice by means of parabiosis. American Journal of Tropical Medicine and Hygiene 30, 113–20.CrossRefGoogle Scholar
Dean, D. A., Mangold, B. L., Georgi, J. R. & Jacobsen, R. H. (1984). Comparison of Schistosoma mansoni migration patterns in normal and irradiated cercariae-immunized mice by means of autoradiographic analysis. Evidence that worm elimination occurs after the skin phase in immunized mice. American Journal of Tropical Medicine and Hygiene 33, 8996.CrossRefGoogle Scholar
Ford, M. J., Bickle, Q. D. & Taylor, M. G. (1984). Immunisation of rats against Schistosoma mansoni using irradiated cercariae, lung schistosomula and liver-stage worms. Parasitology 89, 327–44.CrossRefGoogle ScholarPubMed
Georgi, J. R. (1982). Schistosoma mansoni: quantification of skin penetration and early migration by differential external radioassay and autoradiography. Parasitology 84, 263–81.CrossRefGoogle ScholarPubMed
Georgi, J. R., Dean, D. A. & 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, 31–6.CrossRefGoogle ScholarPubMed
Mangold, B. L. & Dean, D. A. (1983). Autoradiographic analysis of Schistosonia 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, 785–9.CrossRefGoogle Scholar
Mangold, B. L. & Dean, D. A. (1984). The migration and survival of gamma-irradiated Schistosoma mansoni larvae and the duration of host contact in relation to the induction of resistance in mice. Parasitology 88, 249–66.CrossRefGoogle Scholar
Mastin, A. J., Bickle, Q. D. & Wilson, R. A. (1983). Schistosonia mansoni: migration and attrition of irradiated and challenge schistosomula in the mouse. Parasitology 87, 87102.CrossRefGoogle Scholar
Miller, K. L. & Smithers, S. R. (1980). Schistosoma mansoni: the attrition of a challenge infection in mice immunized with highly irradiated live cercariae. Experimental Parasitology 50, 212–2 1.CrossRefGoogle ScholarPubMed
Miller, K. L. & Smithers, S. R. (1982). Localized skin changes at the site of immunization with highly irradiated cercariae of Schistosoma mansoni are associated with enhanced resistance to a challenge infection. Parasitology 85, 305–14.CrossRefGoogle ScholarPubMed
Miller, P. & Wilson, R. A. (1978). Migration of the Schistosomula of Schistosoma mansoni from skin to lungs. Parasitology 77, 281302.CrossRefGoogle ScholarPubMed
Miller, P. & Wilson, R. A. (1980). Migration of the schistosomula of Schistosoma mansoni from the lungs to the hepatic portal system. Parasitology 80, 267–88.CrossRefGoogle Scholar
Minard, P., Dean, D. A., Vannier, W. E. & Murrell, K. D. (1978). Effect of immunization on migration of Schistosoma mansoni through lungs. American. Journal of Tropical Medicine and Hygiene 27, 8793.CrossRefGoogle Scholar
Olivier, L. & Stirewalt, M. A. (1952). An efficient method for exposure of mice to cercariae of Schistosoma mansoni. Journal of Parasitology 38, 1923.CrossRefGoogle ScholarPubMed
Sher, A., Hieny, S., James, S. L. & Asofsky, H. (1982). Mechanisms of protective immunity against Schistosoma mansoni infection in mice vaccinated with irradiated cercariae. ii. Analysis of immunity in hosts deficient in T lymphocytes, B lymphocytes or complement. Journal of Immunology 128, 1880–4.CrossRefGoogle ScholarPubMed
Smith, M. A.. & Clegg, J. A. (1984). Schistosoma mansoni: decay of resistance induced by gamma irradiated cercariae in the mouse. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 190–2.CrossRefGoogle ScholarPubMed
Smithers, S. R. & 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, 289300.CrossRefGoogle Scholar
Wilson, R. A. & Coulson, P. S. (1984). The effect of softwood sawdust bedding on the maturation of an infection of Schistosoma mansoni in mice exposed to cercariae via the tail or abdominal skin. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 411–12.CrossRefGoogle ScholarPubMed
Wilson, R. A. & Coulson, P. S. (1986). Schistosoma mansoni: dynamics of migration through the vascular system of the mouse. Parasitology 92, 83100.CrossRefGoogle ScholarPubMed
Wilson, R. A., Coulson, P. S. & McHugh, S. M. (1983). A significant part of the ‘oncomitant immunity’ of mice to Schistosoma mansoni is the consequence of a leaky hepatic portal system, not immune killing. Parasite Immunology 5, 595601.CrossRefGoogle Scholar
Wilson, R. A., Draskau, T., Miller, P. & 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, 57–7 3.CrossRefGoogle Scholar