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Strongyloides ratti: studies of cutaneous reactions elicited in naive and sensitized rats and of changes in surface antigenicity of skin-penetrating larvae

Published online by Cambridge University Press:  06 April 2009

T.D. McHugh
Affiliation:
School of Biological Sciences, Portsmouth Polytechnic, Portsmouth PO1 2DY
T. Jenkins
Affiliation:
School of Biological Sciences, Portsmouth Polytechnic, Portsmouth PO1 2DY
Diane J. McLaren
Affiliation:
Division of Parasitology, National Institute for Medical Research, Mill Hill, London NW7 1AA

Summary

This study provides the first quantitative assessment of the cutaneous reaction elicited in naive and sensitized rats by invading larvae of Strongyloides ratti. Parasites were identified in skin samples harvested from both naive and sensitized rats between 0·5 and 8 h following percutaneous infection, but were no longer visible at the site of invasion at 24 h. Mast cells, neutrophils, eosinophils and mononuclear cells recruited into the dermis in response to invading larvae were recorded and quantified. Cellular infiltrates were observed as early as 1 h post-invasion in naive/challenged skin, where total cell numbers were up to 3 times greater than in naive control tissue. Peak numbers of all cell types were recorded from 3 to 8 h in both naive/challenged and sensitized/challenged hosts. Interestingly, the reaction in sensitized/challenged rats was neither enhanced nor accelerated, a feature perhaps attributable to lack of recognition of parasite antigens by the host. This possibility was investigated by immunofluorescent labelling, which clearly demonstrated changes in the surface antigen profile of the parasite following penetration of the host skin both in vitro and in vivo. It is proposed that these changes in surface antigenicity constitute an evasive stratagem used by the parasite to deter the host from mounting a potentially lethal inflammatory response.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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References

Bancroft, J. D. & Stevens, A. (1982). Theory and Practice of Histological Techniques. Edinburgh: Churchill Livingstone.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, 7998.CrossRefGoogle ScholarPubMed
Dawkins, H. J. S., Muir, G. M. & Grove, D. I. (1981). Histopathological appearances in primary and secondary infections with Strongyloides ratti in mice. International Journal for Parasitology 11, 97103.CrossRefGoogle ScholarPubMed
Genta, R. M. & Ward, P. A. (1980). The histopathology of experimental strongyloidiasis. American Journal of Pathology 99, 207–20.Google ScholarPubMed
Grove, D. I., Warwick, A. & Lovegrove, F. T. (1984). Loss of surface coat by Strongyloides ratti infective larvae during skin penetration: Evidence using larvae radiolabelled with 67gallium. Journal of Parasitology 70, 689–93.CrossRefGoogle ScholarPubMed
Grove, D. I., Warton, A., Northern, c. & Papadimitriou, J. M. (1987). Electron microscopical studies of Strongyloides ratti infective larvae: loss of surface coat during skin penetration. Journal of Parasitology 73, 1030–4.CrossRefGoogle ScholarPubMed
Incani, R. N. & Mclaren, D. J. (1984). Histopathological and ultrastructural studies of cutaneous reactions elicited in naive and chronically infected mice by invading schistosomula of Schistosoma mansoni. International Journal for Parasitology 14, 259–76.CrossRefGoogle ScholarPubMed
Lee, D. L. (1972). Penetration of mammalian skin by infective larvae of Nippostrongylus brasiliensis. Parasitology 65, 99105.CrossRefGoogle ScholarPubMed
Lee, D. L. (1976). Ultrastructural changes in the infective larvae of Nippostrongylus brasiliensis in the skin of immune mice. Rice University Studies 62, 175–82.Google Scholar
Lichtenberg, F. Von, Sher, A., Gibbons, N. & Doughty, B. L. (1976). Eosinophil-enriched inflammatory response to schistosomula in the skin of mice immune to Schistosoma mansoni. American Journal of Pathology 84, 479500.Google ScholarPubMed
Mackenzie, C. D., Preston, P. M. & Ogilvie, B. M. (1978). Immunological properties of the surface of parasitic nematodes. Nature, London 276, 826–8.CrossRefGoogle ScholarPubMed
Mackenzie, C. D. (1980). Eosinophil leucocytes in filarial infections. Transactions of the Royal Society for Tropical Medicine and Hygiene 74, (Suppl.), 51–8.CrossRefGoogle Scholar
Mclaren, D. J. (1985). Parasite defence mechanisms. In Inflammation. Basic Mechanisms, Tissue Injuring Principles, and Clinical Models (ed. Venge, P. and Lindbom, A.), pp. 219–54. Stockholm: Almquist & Wiksell International.Google Scholar
Matthews, B. E. (1975). Mechanism of skin penetration of Ancylostoma tubaeforme larvae. Parasitology 70, 2538.CrossRefGoogle ScholarPubMed
Matthews, B. E. (1977). The passage of larval helminths through tissue barriers. In Parasite Invasion. Symposia of the British Society for Parasitology, vol. 15 (ed. Taylor, A. E. R. and Muller, R.), pp. 2937. Oxford: Blackwell.Google Scholar
Moqbel, R. (1980). Histopathological changes following primary, secondary and repeated infections of rats with Strongyloides ratti, with special reference to tissue eosinophils. Parasite Immunology 2, 1127.CrossRefGoogle Scholar
Murrell, K. D. & Graham, C. E. (1983). Shedding of antibody complexes by Strongyloides ratti (Nematoda) larvae. Journal of Parasitology 69, 70–3.CrossRefGoogle ScholarPubMed
Pearce, E. J. & McLaren, D. J. (1986). Schistosoma mansoni: the cutaneous response to cercarial challenge in naive guinea pigs and guinea pigs vaccinated with highly irradiated cercariae. International Journal for Parasitology 16, 491510.CrossRefGoogle ScholarPubMed
Smithers, S. R. & Terry, R. J. (1965). Infection of laboratory hosts with cercariae of Schistosoma mansoni and recovery of adult worms. Parasitology 55, 695700.CrossRefGoogle ScholarPubMed
Taliaferro, W. H. & Sarles, M. P. (1939). The cellular reactions in the skin, lungs and intestine of normal and immune rats after infection with Nippostrongylus muris. Journal of Infectious Diseases 64, 157–92.CrossRefGoogle Scholar
Ward, R. E. M. & McLaren, D. J. (1988). Schistosoma mansoni: evidence that eosinpohils and/or macrophages contribute to skin phase challenge attrition in the vaccinated CBA/Ca mouse. Parasitology 96, 63–4.CrossRefGoogle ScholarPubMed
Wilson, P. A. G. & Simpson, N. E. (1981). Dynamics of infection in rats given low doses of homogonic and heterogonic Strongyloides ratti. Parasitology 83, 459–75.CrossRefGoogle Scholar