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Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): the capacity of adult worms to survive following transplantation to recipient mice

Published online by Cambridge University Press:  06 April 2009

J. M. Behnke
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD
Diane J. Williams
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD
J. Hannah
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD
D. I. Pritchard
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD

Summary

Chronic primary infections with Heligmosomoides polygyrus (Nematospiroides dubius) are still relatively poorly documented, particularly in relation to the role of host resistance in limiting worm survival. In the present work the duration of infection with H. polygyrus was studied in CFLP mice given doses of infective larvae ranging from 50 to 500 L3. The least heavily infected (50 L3) group ceased egg production earliest (week 36) whereas eggs were still detected in the faeces of mice given 500 larvae in week 42. At autopsy (week 42) mice given 50 larvae had virtually lost their entire worm burden with 5 out of 11 mice still harbouring a single worm each. However, all the mice in the group given 500 larvae were still infected, the highest worm burden being 93. The concentration of serum IgGl and specific antibody was highest in mice given 500 larvae, but sera taken from mice with declining worm burdens 19–38 weeks post-infection did not contain detectable host-protective antibody. During the course of infection in CFLP mice, H, polygyrus sustained irreversible changes in its capacity for subsequent survival. Thus, adult worms transferred to naive mice 2, 7, 14, 30 or 36 weeks post-infection did not live longer than worms of a comparable age in the respective donor group. In contrast, primary infection worms taken from jirds in which expulsion is usually completed by 6 weeks post-infection, re-established in mice and survived considerably longer than in the group of donor jirds. These results were discussed in relation to the possible interactions between parasite senility and immunomodulation, and host resistance in limiting primary infections with H. polygyrus in mice and jirds.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1987

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References

Behnke, J. M. (1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology, (in the Press).CrossRefGoogle ScholarPubMed
Behnke, J. M. & Hannah, J. (1984). Nematospiroides dubius in the jird, Meriones unguiculatus: stimulation and expression of acquired immunity. Journal of Helminthology 58, 221–9.CrossRefGoogle Scholar
Behnke, J. M., Hannah, J. & Pritchard, D. I. (1983). Evidence that adult Nematospiroides dubius impair the immune response to a challenge infection. Parasite Immunology 5, 397408.Google Scholar
Behnke, J. M. & Parish, H. A. (1979). Expulsion of Nematospiroides dubius from the intestine of mice treated with immune serum. Parasite Immunology 1, 1326.CrossRefGoogle ScholarPubMed
Behnke, J. M. & Parish, H. A. (1981). Transfer of immunity to Nematospiroides dubius: co-operation between lymphoid cells and antibodies in mediating worm expulsion. Parasite Immunology 3, 249–59.CrossRefGoogle ScholarPubMed
Behnke, J. M., Parish, H. A. & Hagan, P. (1980). The effect of gamma irradiation on Nematospiroid.es dubius. Factors affecting the survival of worms in a primary infection in mice. Journal of Helminthology 54, 173–82.CrossRefGoogle Scholar
Behnke, J. M. & Robinson, M. (1985). Genetic control of immunity to Nematospiroides dubius: a 9 day anthelmintic abbreviated immunizing regime which separates weak and strong responder strains of mice. Parasite Immunology 7, 235–53.Google Scholar
Bell, R. G., Adams, L. S. & Ogden, R. W. (1984). Trichinella spiralis: genetics of worm expulsion in inbred and F1 mice infected with different worm doses. Experimental Parasitology 58, 345–55.CrossRefGoogle ScholarPubMed
Bell, R. G., McGregor, D. D., Woan, M. C. & Adams, L. S. (1983). Trichinella spiralis: selective intestinal immune deviation in the rat. Experimental Parasitology 56, 129–42.Google Scholar
Dobson, C. & Cayzer, C. J. R. (1982). Passive transfer of immunity with serum in mice infected with Nematospiroides dubius: in vitro effect of immune serum on larval infectivity. International Journal for Parasitology 12, 413–21.CrossRefGoogle ScholarPubMed
Dobson, C., Sitepu, P. & Brindley, P. J. (1985). Influence of primary infection on the population dynamics of Nematospiroides dubius after challenge infections in mice. International Journal for Parasitology 15, 353–9.Google Scholar
Ehrenford, F. A. (1954). The life cycle of Nematospiroides dubius Baylis (Nematoda: Helig-mosomidae). Journal of Parasitology 40, 480–1.CrossRefGoogle Scholar
Hannah, J. (1983). Studies on the host-parasite relationships of Nematospiroides dubius in normal and abnormal hosts. Ph.D. thesis, University of Nottingham.Google Scholar
Hannah, J. & Behnke, J. M. (1982). Nematospiroides dubius in the jird, Meriones unguiculatus: factors affecting the course of a primary infection. Journal of Helminthology 56, 329–38.Google Scholar
Harness, E., Smith, K. & Bland, P. (1973). Structural changes in the bovine nematode Haemonchus placei, that may be associated with host immune response. Parasitology 66, 199205.Google Scholar
Jacobson, R. H., Brooks, B. O. & Cypess, R. H. (1982). Immunity to Nematospiroides dubius: parasite stages responsible for and subject to resistance in high responder (LAF1/J) mice. Journal of Parasitology 68, 1053–8.Google Scholar
Jenkins, D. C. (1977). Nematospiroides dubius: the course of primary and challenge infections in the Jird, Meriones unguiculatus. Experimental Parasitology 41, 335–40.CrossRefGoogle ScholarPubMed
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.Google Scholar
Jones, V. E. & Ogilvie, B. M. (1971). Protective immunity to Nippostrongylus brasiliensis: the sequence of events which expels worms from the rat intestine. Immunology 20, 549–61.Google Scholar
Kennedy, M. W. & Bruce, R. G. (1981). Reversibility of the effects of the host immune response on the intestinal phase of Trichinella spiralis in the mouse, following transplantation to a new host. Parasitology 82, 3948.CrossRefGoogle ScholarPubMed
Keymer, A. E. & Hiorns, R. W. (1986). Heligmosomoides polygyrus (Nematoda): the dynamics of primary and repeated infection in outbred mice. Proceedings of the Royal Society of London, B 229, 4767.Google Scholar
Lee, D. L. (1969). Changes in adult Nippostrongylus brasiliensis during the development of immunity to this nematode in rats. I. Changes in ultrastructure. Parasitology 59, 2930.Google Scholar
Love, R. J., Ogilvie, B. M. & McLaren, D. J. (1975). Nippostrongylus brasiliensis: further properties of antibody-damaged worms and induction of comparable damage by maintaining worms in vitro. Parasitology 71, 275–83.Google Scholar
Miller, H. R. P. (1984). The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Veterinary Immunology and Immunopathology 6, 167259.Google Scholar
Moqbel, R. & McLaren, D. J. (1980). Strongyloides ratti: structural and functional characteristics of normal and immune-damaged worms. Experimental Parasitology 49, 139–52.Google Scholar
Ogilvie, B. M. & Hockley, D. J. (1968). Effect of immunity on Nippostrongylus brasiliensis adult worms: reversible and irreversible changes in infectivity, reproduction and morphology. Journal of Parasitology 54, 1073–84.CrossRefGoogle ScholarPubMed
Pentilla, I. A., Ey, P. L., Lopez, A. F. & Jenkin, C. R. (1985). Suppression of early immunity to Nematospiroides dubius in mice by selective depletion of neutrophils with monoclonal antibody. Australian Journal of Experimental Biology and Medical Science 63, 531–43.Google Scholar
Pritchard, D. I., Williams, D. J. L., Behnke, J. M. & Lee, T. D. G. (1983). The role of IgG1 hypergammaglobulinaemia in immunity to the gastrointestinal nematode Nematospiroides dubius. The immunochemical purification, antigen-specificity and in vivo anti-parasite effect of IgG1 from immune serum. Immunology 49, 353–65.Google Scholar
Prowse, S. J., Mitchell, G. F., Ey, P. L. & Jenkin, C. R. (1979). The development of resistance in different inbred strains of mice to infection with Nemaiospiroides dubius. Parasite Immunology 1, 277–88.Google Scholar
Ruitenberg, E. J., Steerenberg, P. A., Brosi, B. J. M. & Buys, J. (1976). Reliability of the enzyme-linked immunosorbent assay (ELISA) for the serodiagnosis of Trichinella spiralis infections in conventionally raised pigs. Journal of Immunological Methods 10, 6783.Google Scholar
Sokal, R. R. & Rohlf, F. J. (1969). Biometry. San Francisco: Freeman.Google Scholar
Wakelin, D., Donachie, A. M. & Grencis, R. K. (1985). Genetic control of immunity to Trichinella spiralis in mice: capacity of cells from slow responder mice to transfer immunity in syngeneic and F1 hybrid recipients. Immunology 56, 203–11.Google Scholar
Wassom, D. L., Dougherty, A., Krco, C. J. & David, C. S. (1984). H-2 controlled, dose dependent suppression of the response that expels adult Trichinella spiralis from the small intestine of mice. Immunology 53, 811–18.Google Scholar
Williams, D. J. & Behnke, J. M. (1983). Host protective antibodies and serum immunoglobulin isotypes in mice chronically infected or repeatedly immunized with the nemotode parasite Nemaiospiroides dubius. Immunology 48, 3747.Google Scholar