Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T12:12:29.709Z Has data issue: false hasContentIssue false

Heligmosomoides polygyrus and Trypanosoma congolense infections in mice: a laboratory model for concurrent gastrointestinal nematode and trypanosome infections

Published online by Cambridge University Press:  06 April 2009

B. B. Fakae
Affiliation:
Centre for Tropical Veterinary Medicine, Easter Bush, Roslin, Midlothian EH25 9RG, UK
L. J. S. Harrison
Affiliation:
Centre for Tropical Veterinary Medicine, Easter Bush, Roslin, Midlothian EH25 9RG, UK
C. A. Ross
Affiliation:
Centre for Tropical Veterinary Medicine, Easter Bush, Roslin, Midlothian EH25 9RG, UK
M. M. H. Sewell
Affiliation:
Centre for Tropical Veterinary Medicine, Easter Bush, Roslin, Midlothian EH25 9RG, UK

Summary

A murine model using Heligmosomoides polygyrus and Trypanosoma congolense has been developed for studying the effects of concurrent chronic gastrointestinal nematode and trypanosome infections. Female outbred mice were infected either with 500 infective larvae (L3) of H. polygyrus or with 104 bloodstream forms of T congolense or both. In concurrent infections, animals were dosed with both parasites simultaneously or the trypanosomes were injected 5 or 10 days after the mice were infected with the nematode. The course of infection was monitored by routine parasitological and immunological techniques for 30 days after the H. polygyrus infection. Concurrently infected mice were severely compromised, except when T. congolense was superimposed on a 10-day-old (adult) H. polygyrus infection. In H. polygyrus-infected mice, simultaneous or subsequent infection with trypanosomes did not markedly influence worm establishment or fecundity, but the female worms were slightly stunted. Surviving mice displayed a markedly reduced antibody response to H. polygyrus antigens and a slightly reduced antibody response to T. congolense antigens.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1994

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

Adams, D. B. & Beh, K. J. (1981). Immunity acquired by sheep from an experimental infection with Haemonchus contortus. International Journal for Parasitology 11, 381–6.CrossRefGoogle ScholarPubMed
Ali, N. M. H. & Behnke, J. M. (1983). Nematospiroides dubius: factors affecting the primary response to sheep red blood cell in infected mice. Journal of Helminthology 57, 343–53.CrossRefGoogle ScholarPubMed
Allonby, E. W. & Urquhart, G. M. (1973). Self-Cure of Haemonchus contortus infections under field conditions. Parasitology 66, 4353.CrossRefGoogle ScholarPubMed
Askonas, B. A., Corsini, A. C., Clayton, C. E. & Ogilvie, B. M. (1979). Functional depletion of T- and B- memory cells and other lymphoid cell subpopulations during trypanosomiasis. Immunology 36, 313–21.Google Scholar
Bancroft, G. J. & Askonas, B. A. (1985). Immunobiology of African trypanosomiases in laboratory rodents. In Immunology and Pathogenesis of Trypanosomiasis (ed. Tizard, I.), pp. 75101. Boca Raton, FL: CRC Press.Google Scholar
Bartlett, A. & Ball, P. A. J. (1972). Nematospiroides dubius in the mouse as a possible model of endemic human hookworm infection. Annals of Tropical Medicine and Parasitology 66, 129–34.CrossRefGoogle ScholarPubMed
Behnke, J. M., Hannah, J. & Pritchard, D. I. (1983). Nematospiroides dubius in the mouse: evidence that adult worms depress the expression of homologous immunity. Parasite Immunology 5, 397408.CrossRefGoogle ScholarPubMed
Behnke, J. M., Keymer, A. E. & Lewis, J. W. (1991). Heligmosomoides polygyrus or Nematospiroides dubius? Parasitology Today 7, 177–9.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
Bell, R. G., Adams, L. S. & Ogden, R. W. (1984 a). Trypanosoma musculi with Trichinella spiralis or Heligmosomoides polygyrus: concomitant infections in the mouse. Experimental Parasitology 58, 818.CrossRefGoogle ScholarPubMed
Bell, R. G., Adams, L. S. & Ogden, R. N. (1984 b). Trypanosoma musculi and Trichinella spiralis: concomitant infections and selection for resistance genotypes in mice. Experimental Parasitology 58, 1926.CrossRefGoogle ScholarPubMed
Borowy, N. K., Sternberg, J. M., Schreiber, D., Nonnengasser, C. & Overath, P. (1990). Suppressive macrophages occurring in murine Trypanosoma brucei infection inhibit T-cell responses in vivo and in vitro. Parasite Immunology 12, 233–46.CrossRefGoogle ScholarPubMed
Chiejina, S. N. (1987). Some parasitic diseases of intensively managed West African Dwarf sheep and goats in Nsukka, eastern Nigeria. British Veterinary Journal 143, 246–72.CrossRefGoogle ScholarPubMed
Chiejina, S. N., Fakae, B. B. & Eze, B. O. (1988). Arrested development of gastrointestinal trichostrongylids in goats in Nigeria. Veterinary Parasitology 28, 103–13.CrossRefGoogle ScholarPubMed
Chowaniec, W., Westcott, R. B. & Congdon, L. L. (1972). Interaction of Nematospiroides dubius and influenza virus in mice. Experimental Parasitology 32, 3344.CrossRefGoogle ScholarPubMed
Christensen, N., Furu, P., Kurtzhals, J. & Odaibo, A. (1988). Heterologous synergistic interactions in concurrent experimental infection in the mouse with Schistosoma mansoni, Echinostoma revolutum, Plasmodium yoelii, Babesia microti and Trypanosoma brucei. Parasitology Research 74, 544–51.CrossRefGoogle ScholarPubMed
Christensen, N., Nansen, P., Fagbemi, B. O. & Monrad, J. (1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental infection of mammalian hosts. Parasitology Research 73, 387410.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.CrossRefGoogle ScholarPubMed
Durette-Desset, M. C., Kinsella, J. M. & Forrester, D. J. (1972). Arguments en faveur de la double origine de nématodes néavetiques du genre Heligmosmoides Hall, 1916. Annales de Parasitologic Humaine et Comparée 47, 365–82.CrossRefGoogle Scholar
Fagbemi, B. O., Christensen, N. & Nansen, P. (1985 a). Suppression of Babesia microti infection in mice concurrently infected with Fasciola hepatica. Veterinary Parasitology 17, 101–10.CrossRefGoogle ScholarPubMed
Fagbemi, B. O., Christensen, N. & Nansen, P. (1985 b). Suppression of Babesia microti infection in mice concurrently infected with Schistosoma mansoni. Acta Veterinaria Scandinavica 26, 121204.CrossRefGoogle ScholarPubMed
Fakae, B. B. (1990). Epidemiology of helminthosis of small ruminants under the traditional husbandry system in eastern Nigeria. Veterinary Research Communications 14, 381–91.CrossRefGoogle ScholarPubMed
Fakae, B. B. (1993). Conjoint Heligmosmoides polygyrus and Trypanosoma congolense infection in mice. Ph.D. thesis, University of Edinburgh, xiii + 219 pp.Google Scholar
Fakae, B. B. & Chiejina, S. N. (1993). The prevalence of concurrent trypanosome and gastrointestinal nematode infections in West African dwarf sheep and goats in Nsukka area of Eastern Nigeria. Veterinary Parasitology 44, 49.Google Scholar
Fowler, J. & Cohen, L. (1990). Practical Statistics for Field Biology. Milton Keynes: Open University Press.Google Scholar
Frame, I. A., Ross, C. A. & Luckins, A. G. (1990). Characterization of Trypanosoma congolense serodemes in stocks isolated from Chipata District, Zambia. Parasitology 101, 235–41.CrossRefGoogle Scholar
Gray, A. R., Ross, C. A., Taylor, A. M. & Luckins, A. G. (1984). In vitro cultivation of Trypanosoma congolense: the production of infective metacyclic trypanosomes in cultures initiated from cloned stocks. Acta Tropica 41, 343–53.Google ScholarPubMed
Griffin, L., Allonby, E. W. & Preston, J. M. (1981). The interaction of Trypanosoma congolense and Haemonchus contortus infection in two breeds of goat. I. Parasitology. Journal of Comparative Pathology 91, 8595.CrossRefGoogle Scholar
Griffin, L., Aucutt, M., Allonby, E. W., Preston, J. & Castelino, J. (1981). The interaction of Trypanosoma congolense and Haemonchus contortus infection in two breeds of goat. II. Haematology. Journal of Comparative Pathology 91, 97103.CrossRefGoogle Scholar
Hagan, P. & Wakelin, D. (1982). Nematospiroides dubius: effect of infection on lymphocyte responses to Trichinella spiralis in mice. Experimental Parasitology 54, 157–65.CrossRefGoogle ScholarPubMed
Herbert, W. J. & Lumsden, W. H. R. (1976). Trypanosoma brucei: a rapid ‘matching’ method for estimating the host's parasitaemia. Experimental Parasitology 40, 427–31.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
Kaufmann, J., Dwinger, R. H., Hallebeek, A., Van Dijk, B. & Pfister, K. (1992). The interaction of Trypanosoma congolense and Haemonchus contortus infections in trypanotolerant N'Dama cattle. Veterinary Parasitology 43, 157–70.CrossRefGoogle ScholarPubMed
Lanham, S. M. & Godfrey, D. G. (1970). Isolation of salivarian trypanosomes from man and other animals using DEAE-cellulose. Experimental Parasitology 28, 521–34.CrossRefGoogle ScholarPubMed
Liu, S. -K. (1965). Pathology of Nematospiroides dubius. I. Primary infections in C3 and Webster mice. Experimental Parasitology 17, 123–35.CrossRefGoogle Scholar
Losos, G. J. & Ikede, B. O. (1972). Review of pathology of diseases in domestic and laboratory animals caused by Trypanosoma congolense T. vivax, T. rhodesiense and T. gambiense. Veterinary Pathology 9 (Suppl.), 1–71.CrossRefGoogle Scholar
Maff, (1977). Manual of Veterinary Parasitological Laboratory Techniques, pp 3637. Technical Bulletin No. 18. London: HMSO.Google Scholar
Monroy, F. G. & Enriquez, F. J. (1992). Heligmosoides polygyrus: a model for chronic gastrointestinal helminthiasis. Parasitology Today 8, 4954.CrossRefGoogle Scholar
Morrison, W. I., Murray, M. & Akol, G. W. O. (1985). Immune responses of cattle to African trypanosomoses. In Immunology and Pathogenesis of Trypanosomiasis (ed. Tizard, I.), pp. 103131. Boca Raton, FL: CRC Press.Google Scholar
Murray, P. K., Jennings, F. W., Murray, M. & Urquhart, G. M. (1974 a). The nature of immunosuppression in Trypanosoma brucei infections in mice. I. The role of the macrophage. Immunology 27, 815–24.Google ScholarPubMed
Murray, P. K., Jennings, F. W., Murray, M. & Urquhart, G. M. (1974 b). The nature of immunosuppression in Trypanosoma brucei infections in mice. II. The role of the T and B lymphocytes. Immunology 27, 825–40.Google ScholarPubMed
Nichol, C. P. & Sewell, M. M. H. (1984). Immunosuppression by larval cestodes of Babesia microti infections. Annals of Tropical Medicine and Parasitology 78, 228–33.CrossRefGoogle ScholarPubMed
Phillips, R. S. & Wakelin, D. (1976). Trichuris muris: effect of concurrent infections with rodent piroplasms in immune expulsion from mice. Experimental Parasitology 39, 95100.CrossRefGoogle ScholarPubMed
Phillips, R. S., Selby, G. R. & Wakelin, D. (1974). The effect of Plasmodium berghei and Trypanosoma brucei infections on the immune expulsion of the nematode Trichuris muris from mice. International Journal for Parasitology 4, 409–15.CrossRefGoogle ScholarPubMed
Pritchard, D. I. & Behnke, J. M. (1985). The Suppression of homologous immunity by soluble antigens of Nematospiroides dubius. Journal of Helminthology 59, 251–6.CrossRefGoogle ScholarPubMed
Pritchard, D. I., Ali, N. M. H. & Behnke, J. M. (1984). Analysis of the mechanism of immunosuppression following heterologous antigenic stimulation during concurrent infection with Nematospiroides dubius. Immunology 51, 633–42.Google ScholarPubMed
Robinson, M., Wahid, F., Behnke, J. M. & Gilbert, F. S. (1989). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): dose-dependent expulsion of adult worms. Parasitology 98, 115–24.CrossRefGoogle ScholarPubMed
Shimp, R. G., Crandall, R. B. & Crandall, C. A. (1975). Heligomosomoides polygyrus (Nematospiroides dubius): suppression of antibody response to orally administered erythrocyte-infected mice. Experimental Parasitology 38, 257–69.CrossRefGoogle Scholar
Stephen, L. E. (1986). Trypanosomiasis: A Veterinary Perspective. Oxford: Pergamon Press.Google Scholar
Voller, A., Bidwell, D. E. & Bartlett, A. (1979). The Enzyme Linked Immunosorbent Assay (ELISA). A Guide with Abstracts of Microplate Applications, pp. 142. Dynatech Europe, Borough House, Guernsey, UK.Google Scholar
Wakelin, D. & Lloyd, M. (1976). Immunity to primary and challenge infections of Trichinella spiralis in mice: a re-examination of conventional parameters. Parasitology 72, 173–82.CrossRefGoogle ScholarPubMed
Warburgh, O. & Christian, W. (1941). Isolierung und Kristallisation des Garungsferments Enolase. Biochemische Zeitschrift 310, 384421.Google Scholar