Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-02T18:54:52.792Z Has data issue: false hasContentIssue false
  • English
  • Français

Migration of the schistosomula of Schistosoma mansoni from skin to lungs

Published online by Cambridge University Press:  06 April 2009

Patricia Miller  and
R. A. Wilson
Patricia Miller
Affiliation:
Department of Biology, University of York, Heslington, York
R. A. Wilson
Affiliation:
Department of Biology, University of York, Heslington, York
Get access Rights & Permissions [Opens in a new window]

Summary

The number of schistosomula recovered from abdominal skin declined exponentially with time after infection. However, this decline was shown to be an untrue reflection of the numbers present because of changes in recoverability on days subsequent to infection. Digestion of skin by the enzymes collagenase and hyaluronidase produced a small increase in the number of schistosomula recovered. The number of schistosomula present in abdominal skin and capable of reaching maturity was estimated by exciting the area to which cercariae had been applied, from groups of hosts at daily intervals after exposure. The number of worms maturing in each group of hosts was then determined. The mean duration of stay of schistosomula in mouse, hamster and rat abdominal skin was estimated at 88, 64·5 and 70 h, respectively. The fluid content of abdominal skin to which cercariae had been applied, increased following infection but it was concluded that this alone was not the predominant factor controlling exit of worms. The stimulation of a delayed hypersensitivity response not directed against schistosomes (in mice previously sensitized with 1-chloro,2–4-dinitrobenzene (DNB)) 1 day after exposure to cercariae, produced a significant increase in the number of schistosomula leaving the skin and reaching maturity. Schistosomula can be recovered from the axial lymph nodes of mice, hamsters and rats. If the schistosomula from mice are injected into the tail vein of uninfected mouse hosts, they have the same chance of maturing as comparable skin schistosomula. They are therefore apparently unharmed by their passage through the nodes. Interference with lymphatic drainage by surgical removal of lymph nodes has no effect on the number of schistosomula recovered from the lungs, but the peak recovery is delayed by 24 h. The hamster cheek-pouch, a site with no afferent lymphatic drainage, was also used to investigate the importance of the lymphatic exit route. There was no reduction in the number of adult worms recovered following infection at this site compared with the normal abdominal skin site. The migration of schistosomula to deeper tissues and their entry into blood vessels was followed using the cheek-pouch preparation. It was concluded that the major route of exit from the skin is the blood vascular system.

Type
Research Article
Information
Parasitology , Volume 77 , Issue 3 , December 1978 , pp. 281 - 302
Copyright
Copyright © Cambridge University Press 1978

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

Billingham, R. E. & Silvers, W. K. (1962). Studies on pouch skin homografts in the Syrian hamster. In Ciba Symposium on Transplantation (ed. Wolstenholme, G. E. W. and Cameron, M. P.). Boston: Little Brown and Company.Google Scholar
Billingham, R. E., Ferrigan, L. W. & Silvers, W. K. (1960). Cheek pouch of the Syrian hamster and tissue transplantation immunity. Science 132, 1488.Google Scholar
Clegg, J. A. (1965). In vitro cultivation of Schistosoma mansoni. Experimental Parasitology 16, 133–47.CrossRefGoogle ScholarPubMed
Clegg, J. A. & Smithers, S. R. (1968). Death of schistosome cercariae during penetration of the skin. II. Penetration of mammalian skin by Schistosoma mansoni. Parasitology 58, 111–28.Google Scholar
Clegg, J. A. & Smithers, S. R. (1972). The effects of immune rhesus monkey serum on schistosomula of Schistosoma mansoni during cultivation in vitro. International Journal for Parasitology 2, 79–98.CrossRefGoogle ScholarPubMed
Cohen, S. N. (1961). Comparison of autologous, homologous and heterologous normal skin grafts in the hamster cheek pouch. Proceedings of the Society for Experimental Biology and Medicine 106, 677–80.CrossRefGoogle ScholarPubMed
Coles, G. C. (1972). The carbohydrate metabolism of larval Schistosoma mansoni. International Journal for Parasitology 2, 341–52.Google Scholar
Engeset, A. (1959). Intralymphatic injections in the rat. Cancer Research 19, 277–8.Google Scholar
Faust, E. C., Jones, C. A. & Hoffman, W. A. (1934). Studies on schistosomiasis mansoni in Puerto Rico. III. Biological studies. 2. The mammalian phase of the life cycle. Puerto Rico Journal of Public Health and Tropical Medicine 10, 133–96.Google Scholar
Faust, E. C. & Meleney, H. E. (1924). Studies on schistosomiasis japonica. American Journal of Hygiene, Monographic Series 3, 1–339.Google Scholar
Hockley, D. J. & McLaren, D. J. (1973). Schistosoma mansoni: changes in the outer membrane of the tegument during development from cercaria to adult worm. International Journal for Parasitology 3, 13–25.Google Scholar
Lewert, R. M. & Mandlowitz, S. (1963). Innate immunity to Schistosoma mansoni relative to the state of connective tissue. Annals of the New York Academy of Sciences 113, 54–62.Google Scholar
Miller, P. (1976). Migration of the human blood fluke Schistosoma mansoni, and its subsequent development in the mammalian host. D.Phil. thesis, University of York.Google Scholar
Miyagawa, Y. & Takemoto, S. (1921). The mode of infection of Schistosoma japonicum and the principal route of its journey from the skin, to the portal vein in the host. Journal of Pathology and Bacteriology 24, 168–74.Google Scholar
Nanson, N. (1962). A study of the powers of reanastomosis of the limb lymphatic vessels and nodes in the dog. Canadian Journal of Surgery 5, 329–32.Google Scholar
Pressman, J. J., Burtz, H. V. & Shafer, L. (1964). Further observations related to direct communications between lymph nodes and veins. Surgery, Gynecology and Obstetrics 119, 984–9.Google ScholarPubMed
Sher, A., Mackenzie, P. & 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, 626–33.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Terry, B. J. (1965). The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55, 695–700.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, 292–8.Google Scholar
Stirewalt, M. A. (1959). Chronological analysis, pattern, and rate of migration of Schistosoma mansoni in body, ear and tail skin of mice. Annals of Tropical Medicine and Parasitology 53, 400–13.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1963). Cercaria vs schistosomule (Schistosoma mansoni): absence of the pericercarial envelope in vivo and the early physiological and histological metamorphosis of the parasite. Experimental Parasitology 13, 395–406.Google Scholar
Stirewalt, M. A. (1974). Schistosoma mansoni: cercaria to schistosomule. Advances in Parasitology 12, 115–82.CrossRefGoogle ScholarPubMed
Tilney, N. L. & Gowans, J. L. (1971). The sensitization of rats by allografts transplanted to alymphatic pedicles of skin. Journal of Experimental Medicine 133, 951–62.Google Scholar
Webster, L. A. & Wilson, R. A. (1970). The chemical composition of protonephridial canal fluid from the cestode Hymenolepis diminuta. Comparative Biochemistry and Physiology 35, 201–9.CrossRefGoogle Scholar
Weiss, L. (1972). The Cells and Tissues of the Immune System. Engelwood Cliffs, N.J.: Prentice-Hall.Google 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, 57–73.Google Scholar
Yolles, T. K., Moore, D. V. & Meleney, H. E. (1949). Post-cercarial development of Schistosoma mansoni in the rabbit and hamster after intra-peritoneal and percutaneous infection. Journal of Parasitology 35, 276–94.Google Scholar