Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-25T18:44:46.621Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): dose-dependent expulsion of adult worms

Published online by Cambridge University Press:  06 April 2009

M. Robinson ,
F. Wahid ,
J. M. Behnke  and
F. S. Gilbert
M. Robinson
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD
F. Wahid
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD
J. M. Behnke*
Affiliation:
MRC Experimental Parasitology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD
F. S. Gilbert
Affiliation:
Behavioural Ecology Research Group, Department of Zoology, University of Nottingham, University Park, Nottingham NG7 2RD
*
Author to whom reprint requests should be addressed.
Get access Rights & Permissions [Opens in a new window]

Summary

The survival of Heligmosomoides polygyrus was monitored during primary infections in female C57Bl10, NIH and BALB/c mice at low and high intensities of infection. Survivorship curves were fitted for each data set and analysed. C57Bl10 mice, given either low or high intensities of infection, harboured parasites for 28–37 weeks, heavier infections surviving marginally but significantly longer. Essentially the survivorship curves of H. polygyrus in C57Bl10 mice could be accounted for by senility, the increased probability of worms with a longer life-span occurring at high infection intensities and, possibly, by a contribution from host-protective immune mechanisms in the terminal stages of infection. The pattern of survivorship was different in NIH and BALB/c mice. NIH mice showed weak but significant density-dependent suppression of parasite loss and infections in this strain did not exceed 27·5 weeks in duration. Primary infections in BALB/c mice were briefer still and showed marked dependence on parasite density. Thus low-level infections lasted 10–15 weeks whereas heavier infections survived for 21–34 weeks. The data suggested that both strains developed host-protective responses to adult H. polygyrus and that parasite survival was curtailed earlier than would be expected if senility alone was involved. The hybrid strains (C57Bl10 × NIH)F1 and (B10G × NIH)F1 both expelled H. polygyrus in a dose-dependent manner, worm loss commencing within 10 weeks of infection. In some experiments worm loss was clearly evident by weeks 4 and 6. These hybrid strains showed gene complementation in that adult worms were cleared considerably earlier than in parental strains.

Type
Research Article
Information
Parasitology , Volume 98 , Issue 1 , February 1989 , pp. 115 - 124
Copyright
Copyright © Cambridge University Press 1989

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

Alizadeh, H. & Wakelin, D. (1982). Genetic factors controlling the intestinal mast cell response in mice infected with Trichinella spiralis. Clinical and Experimental Immunology 49, 331–7.Google ScholarPubMed
Anderson, R. M. (1986 a). Genetic variability in resistance to parasitic invasion: population implications for invertebrate host species. In Immune Mechanisms in Invertebrate Vectors. Symposia of the Zoological Society of London 56, 239–74, (ed. Lackie, A. M.). Oxford: Clarendon Press.Google Scholar
Anderson, R. M. (1986 b). The population dynamics and control of intestinal nematode infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 686–96.CrossRefGoogle ScholarPubMed
Behnke, J. M. (1987). Evasion of immunity by nematode parasites causing chronic infections. Advances in Parasitology 26, 1–71.CrossRefGoogle ScholarPubMed
Behnke, J. M. & Robinson, M. (1985). Genetic control of immunity to Nematospiroides dubius: a 9 day anthelmintic abbreviated immunising regime which separates weak and strong responder strains of mice. Parasite Immunology 7, 235–53.CrossRefGoogle ScholarPubMed
Behnke, J. M. & Wakelin, D. (1977). Nematospiroides dubius: stimulation of acquired immunity in inbred strains of mice. Journal of Helminthology 51, 167–76.CrossRefGoogle ScholarPubMed
Behnke, J. M., Williams, D. J. L., Hannah, J. & Pritchard, D. I. (1987). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): the capacity of adult worms to survive following transplantation to recipient mice. Parasitology 95, 569–81.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Blazkovec, A. A., Orsini, M. W. & Maginn, P. C. (1973). Sexual dimorphism in the primary immune response of the Syrian hamster. International Archives of Allergy 44, 274–93.CrossRefGoogle ScholarPubMed
Bundy, D. A. P., Cooper, E. S., Thompson, D. E., Didier, J. M., Anderson, R. M. & Simmons, I. (1987). Predisposition to Trichuris trichiura infection in humans. Epidemiology and Infection 98, 65–71.CrossRefGoogle ScholarPubMed
Cypess, R. H., Lucia, H. L., Zidian, J. L. & Rivera-Ortiz, C. I. (1977). Heligmosomoides polygyrus: temporal, spatial and morphological population characteristics in LAF1/J mice. Experimental Parasitology 42, 34–43.CrossRefGoogle ScholarPubMed
Cypess, R. H. & Zidian, J. L. (1975). Heligmosomoides polygyrus (Nematospiroides dubius): the development of self-cure and/or protection in several strains of mice. Journal of Parasitology 61, 819–24.CrossRefGoogle ScholarPubMed
Day, K. P., Howard, R. J., Prowse, S. J., Chapman, C. B. & Mitchell, G. F. (1979). Studies on chronic versus transient intestinal nematode infections in mice. I. A comparison of responses to excretory/secretory (ES) products of Nippostrongylus brasiliensis and Nematospiroides dubius worms. Parasite Immunology 1, 217–39.CrossRefGoogle Scholar
Dehlawi, M. S. & Wakelin, D. (1988). Suppression of mucosal mastocytosis by Nematospiroides dubius results from an adult worm-mediated effect upon host lymphocytes. Parasite Immunology 10, 85–95.CrossRefGoogle ScholarPubMed
Dehlawi, M. S., Wakelin, D. & Behnke, J. M. (1987). Suppression of mucosal mastocytosis by infection with the intestinal nematode Nematospiroides dubius. Parasite Immunology 9, 187–94.CrossRefGoogle ScholarPubMed
Dobson, C. (1961). Certain aspects of the host-parasite relationship of Nematospiroides dubius. I. Resistance of male and female mice to experimental infection. Parasitology 51, 173–9.CrossRefGoogle Scholar
Dobson, C. (1982). Passive transfer of immunity with serum in mice infected with Nematospiroides dubius: influence of quality and quantity of immune serum. Parasitology 12, 207–13.Google ScholarPubMed
Dobson, C. & Cayzer, C. J. R. (1982). Immunosuppressive activity in serum from mice infected with Nematospiroides dubius following passive serum transfer. International Journal for Parasitology 12, 561–6.CrossRefGoogle Scholar
Dobson, D., 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.CrossRefGoogle ScholarPubMed
Ehrenford, F. A. (1954). The life cycle of Nematospiroides dubius Baylis (Nematoda: Heligmosomidae). Journal of Parasitology 40, 480–1.CrossRefGoogle 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
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, 47–67.Google ScholarPubMed
Liu, S. K. (1966). Genetic influence on resistance of mice to Nematospiroides dubius. Experimental Parasitology 18, 311–19.CrossRefGoogle Scholar
Miller, H. R. P. (1984). The protective mucosal response against gastrointestinal nematodes in ruminants and laboratory animals. Veterinary Immunology and Immunopathology 6, 167–259.CrossRefGoogle ScholarPubMed
Mitchell, G. F. & Munoz, J. J. (1983). Vaccination of genetically susceptible mice against chronic infection with Nematospiroides dubius using pertussigen as adjuvant. Australian Journal of Experimental Biology and Medical Science 61, 425–34.CrossRefGoogle ScholarPubMed
Prowse, S. J., Mitchell, G. F., Ey, P. L. & Jenkins, C. R. (1979). The development of resistance in different inbred strains of mice to infection with Nematospiroides dubius. Parasite Immunology 1, 277–88.CrossRefGoogle ScholarPubMed
Ross, G. J. S. (1980). MLP: Maximum Likelihood Program. Rothhampsted Experimental Station.Google Scholar
Schad, G. A. & Anderson, R. M. (1985). Predisposition to hookworm infection in Man. Science 228, 1537–40.CrossRefGoogle Scholar
Sokal, R. R. & Rohlf, F. J. (1969). Biometry. San Francisco: Freeman.Google Scholar
Solomon, G. B. (1969). Host hormones in parasitic infections. International Review of Tropical Medicine 3, 101–58.Google Scholar
Wakelin, D. (1980). Genetic control of immunity to parasites. Infection with Trichinella spiralis in inbred and congenic mice showing rapid and slow responses to infection. Parasite Immunology 2, 85–98.CrossRefGoogle Scholar
Wakelin, D. & Blackwell, J. M. (1988). Genetics of Resistance to Bacterial and Parasitic Infection. London: Taylor & Francis (in the Press).Google Scholar
Wakelin, D. (1985). Genetic control of immunity to helminth infections. Parasitology Today 1, 17–23.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
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 ScholarPubMed
Williams, D. W. & Behnke, J. M. (1983). Host protective antibodies and serum immunoglobulin isotypes in mice chronically infected or repeatedly immunized with the nematode parasite Nematospiroides dubius. Immunology 48, 37–47.Google ScholarPubMed