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Immunologically mediated, non-specific interactions between the intestinal phases of Trichinella spiralis and Nippostrongylus brasiliensis in the mouse

Published online by Cambridge University Press:  06 April 2009

M. W. Kennedy
M. W. Kennedy
Affiliation:
Department of Zoology, University of Glasgow, Glasgow G12 8QQ
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Summary

Interactions between infections of Trichinella spiralis and Nippostrongylus brasiliensis were studied in the NIH strain of mouse which is known to react strongly to T. spiralis. The course of N. brasiliensis infection in this strain of mouse is described and expulsion is shown to be accelerated in immunized mice and inhibited in cortisone-treated mice. There was no evidence of inter-specific competition between the two species of worm in concurrent infections; the number and location of adults of both species were normal and T. spiralis was able to grow and reproduce normally. No evidence was found of direct immunological cross-reaction between N. brasiliensis and T. spiralis as assessed by the kinetics of adult worm numbers on heterologous challenge of immunized mice 90 days after the initiation of the last of 3 immunizing infections. Interaction was observed only when the timing of concurrent infections was such that one species was established in the intestine immediately before the beginning of expulsion of the second species. Interaction was manifested as a premature loss of worms and, in addition, as impairment of growth and fecundity of T. spiralis. These effects on T. spiralis were similar to those observed as a consequence of a specific immune response to T. spiralis. The rapidity of appearance of these effects and the lack of direct cross-immunity between the two species of worm suggest that the events involved in interaction were non-specific in action and possibly due to environmental changes in the gut caused by the immune response. These non-specific effects are therefore analogous, but not necessarily homologous, to the expulsion of these parasites in single species infections.

Type
Research Article
Information
Parasitology , Volume 80 , Issue 1 , February 1980 , pp. 61 - 72
Copyright
Copyright © Cambridge University Press 1980

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References

Andreassen, J., Hindsbo, O. & Ruitenberg, E. J. (1978). Hymenolepis diminuta infections in congenitally athymic (nude) mice: worm kinetics and intestinal histopathology. Immunology 34, 105–13.Google ScholarPubMed
Behnke, J. M., Bland, P. W. & Wakelin, D. (1977). Effect of the expulsion phase of Trichinella spiralis on Hymenolepis diminuta infection in mice. Parasitology 75, 79–88.CrossRefGoogle ScholarPubMed
Behnke, J. M., Wakelin, D. & Wilson, M. M. (1978). Trichinella spiralis: delayed rejection in mice concurrently infected with Nematospiroides dubius. Experimental Parasitology 46, 121–30.CrossRefGoogle ScholarPubMed
Brambell, M. R. (1965). The distribution of a primary infestation of Nippostrongylus brasiliensis in the small intestine of laboratory rats. Parasitology 55, 313–24.CrossRefGoogle ScholarPubMed
Bruce, R. G. & Wakelin, D. (1977). Immunological interactions between Trichinella spiralis and Trichuris muris in the intestine of the mouse. Parasitology 74, 163–73.CrossRefGoogle Scholar
Castro, G. A. (1976). Spatial and temporal integration of host responses to intestinal stages of Trichinella spiralis: retro- and prospective views. In Biochemistry of Parasites and Host-Parasite Relationships (ed. Van den Bossche, H.). Amsterdam: Elsevier/North Holland Biomedical Press.Google Scholar
Cox, H. W. (1952). The effect of concurrent infection with the dog hookworm, Ancylostoma caninum, on the natural and acquired resistance of mice to Trichinella spiralis. Journal of the Elisha Mitchell Scientific Society 68, 222–35.Google Scholar
Despommier, D. D., Sukhdeo, M. & Meerovitch, E. (1978). Trichinella spiralis: site selection by the larva during the enteral phase of infection in mice. Experimental Parasitology 44, 209–15.CrossRefGoogle ScholarPubMed
Fatunmbi, O. O. (1978). Studies on some aspects of the development of Trichinella spiralis in mice. M.Sc. Dissertation, University of Glasgow.Google Scholar
Faubert, G. M. (1976). Depression of the plaque-forming cells to sheep red blood cells by the new-born larvae of Trichinella spiralis. Immunology 30, 485–9.Google ScholarPubMed
Gardiner, C. H. (1976). Habitat and reproductive behavior of Trichinella spiralis. Journal of Parasitology 62, 865–70.CrossRefGoogle ScholarPubMed
Goulson, H. T. (1958). Studies on the influence of a prior infection with Ancylostoma caninum on the establishment and maintenance of Trichinella spiralis in mice. Journal of the Elisha Mitchell Scientific Society 74, 14–23.Google Scholar
Jenkins, D. C. (1975). The influence of Nematospiroides dubius on subsequent Nippostrongylus brasiliensis infections in mice. Parasitology 71, 349–55.CrossRefGoogle ScholarPubMed
Jenkins, S. N. (1977). Studies on the immune response of the mouse to the nematode Tri-churis muris. Ph.D. Dissertation, University of Glasgow.Google Scholar
Jenkins, S. N. & Behnke, J. M. (1977). Impairment of primary expulsion of Trichuris muris in mice concurrently infected with Nematospiroides dubius. Parasitology 75, 71–8.CrossRefGoogle ScholarPubMed
Jennings, F. W., Mulligan, W. & Urquhart, G. M. (1963). Variables in X-ray ‘inactiva-tion’ of Nippostrongylus brasiliensis larvae. Experimental Parasitology 13, 367–73.CrossRefGoogle ScholarPubMed
Kazacos, K. R. (1975). Increased resistance in the rat to Nippostrongylus brasiliensis following immunization against Trichinella spiralis. Veterinary Parasitology 1, 165–74.CrossRefGoogle Scholar
Kennedy, M. W. (1976). Kinetics of establishment and rejection of the enteral phase of a primary infection of Trichinella spiralis in the NIH strain mouse. Transactions of the Royal Society of Tropical Medicine and Hygiene 70, 285.Google Scholar
Kennedy, M. W., Wakelin, D. & Wilson, M. M. (1979). Transplantation of adult Trichinella spiralis between hosts: worm survival and immunological characteristics of the host-parasite relationship. Parasitology 78, 121–30.CrossRefGoogle ScholarPubMed
Larsh, J. E. Jr & Race, G. J. (1975). Allergic inflammation as a hypothesis for the expulsion of worms from tissues: a review. Experimental Parasitology 37, 251–66.CrossRefGoogle ScholarPubMed
Ljungström, I. & Huldt, G. (1977). Effect of experimental Trichinosis on unrelated humoral and cell-mediated immunity. Acta Pathologica Microbiologica Scandinavica, Section C 85, 131–41.CrossRefGoogle ScholarPubMed
Louch, C. D. (1962). Increased resistance to Trichinella spiralis in the laboratory rat following infection with Nippostrongylus muris. Journal of Parasitology 48, 24–6.CrossRefGoogle ScholarPubMed
Love, R. J. (1975). Nippostrongylus brasiliensis infections in mice: the immunological basis of worm expulsion. Parasitology 70, 11–18.CrossRefGoogle ScholarPubMed
Moqbel, R. & Wakelin, D. (1979). Trichinella spiralis and Strongyloides ratti: immune interaction in adult rats. Experimental Parasitology 47, 65–72.CrossRefGoogle ScholarPubMed
Ogilvie, B. M. (1971). Nippostrongylus brasiliensis in mice: an explanation for the failure to induce -worm expulsion from passively immunized animals. International Journal for Parasitology 1, 161–7.CrossRefGoogle ScholarPubMed
Ogilvie, B. M. & Jones, V. E. (1971). Nippostrongylus brasiliensis: a review of immunity and the host/parasite relationship in the rat. Experimental Parasitology 29, 138–77.CrossRefGoogle ScholarPubMed
Rogers, W. P. (1962). The Nature of Parasitism. New York and London: Academic Press.Google Scholar
Sinski, E. (1972). Preliminary studies on cross-resistance in Nippostrongylus brasiliensis and Trichinella spiralis infection of rats. Acta Parasitologica Polonica xx, 551–61.Google Scholar
Stahl, W. (1966). Experimental aspiculuriasis. II. Effects of concurrent helminth infection. Experimental Parasitology 18, 116–23.CrossRefGoogle ScholarPubMed
Symons, L. E. A. (1969). Pathology of gastrointestinal helminthiases. International Review of Tropical Medicine 3, 49–100.Google ScholarPubMed
Wakelin, D. & Lloyd, M. (1976 a). Immunity to primary and challenge infections of Trichinella spiralis in mice: a re-examination of conventional parameters. Parasitology 72, 173–82.CrossRefGoogle ScholarPubMed
Wakelin, D. & Lloyd, M. (1976 b). Accelerated expulsion of adult Trichinella spiralis in mice given lymphoid cells and serum from infected donors. Parasitology 72, 307–15.CrossRefGoogle ScholarPubMed
Weiner, L. M. & Neely, J. (1964). The nature of the antigenic relationship between Trichinella spiralis and Salmonella typhi. Journal of Immunology 92, 908–11.CrossRefGoogle ScholarPubMed
Weiner, L. M. & Price, S. (1956). A study of antigenic relationships between Trichinella spiralis and Salmonella typhi. Journal of Immunology 77, 111–14.CrossRefGoogle Scholar
Weinmann, C. J. (1964). Host resistance to Hymenolepis nana. II. Specificity of resistance to reinfection in the direct cycle. Experimental Parasitology 15. 514–26.CrossRefGoogle ScholarPubMed