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Protein content of CBA/Ca mouse diet: relationship with host antibody responses and the population dynamics of Trichuris muris (Nematoda) in repeated infection

Published online by Cambridge University Press:  06 April 2009

E. Michael  and
D. A. P. Bundy
E. Michael
Affiliation:
Parasite Epidemiology Research Group, Department of Biology, Imperial College, University of London, Prince Consort Road, London SW7 2BB
D. A. P. Bundy
Affiliation:
Parasite Epidemiology Research Group, Department of Biology, Imperial College, University of London, Prince Consort Road, London SW7 2BB
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Extract

The influence of host dietary protein on acquired immunity and intestinal helminth population dynamics during repeated infection was studied using the mouse–Trichuris muris experimental model. CBA/Ca mice fed a 2% (by mass) protein diet ad libitum maintained body weight during the experiment, but when fed diets containing either 4% or 16% (by mass) protein gained weight steadily. Infection with T. muris did not affect the growth of the latter mice but significantly reduced the growth of animals fed on the 2% protein diet. When repeatedly infected with either 5 or 50 eggs every 10 days, the mice fed the 2% or 4% protein diet accumulated adults in proportion to infection dose. The results show that this is due to both the establishment of larvae at each repeated infection and the survival of established adults. In contrast, very few worms were recovered from animals fed the 16% protein diet, principally as a result of the development of strong acquired immunity to reinfection. T. muris egg output/mouse increased with infection dose in animals fed the low protein diets, but no parasite eggs were detected in the faeces of hosts fed the 16% protein diet. Mouse antibody reponses to adult worm excretory/secretory antigen were time- and infection dose-dependent in all 3 dietary groups. The major finding was that the specific antibody response was more intense, both quantitatively (serum OD levels) and qualitatively (antigen recognition by IgG1), in mice fed the low protein diets, even though they remained susceptible to infection. This study shows that host dietary protein deficiency, even at levels irrelevant to normal growth, can markedly potentiate the transmission of T. muris via alterations in host resistance. The high levels of antibody in susceptible animals suggest that this defect in resistance is unlikely to be due to nutrient deficiency-associated defects in humoral immunity.

Keywords

Trichuris murisprotein malnutritionhumoral immunitypopulation biologyintestinal helminthiasis.
Type
Research Article
Information
Parasitology , Volume 105 , Issue 1 , August 1992 , pp. 139 - 150
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Anderson, R. M. & May, R. M. (1991). Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Abbott, E. M., Parkins, J. J. & Holmes, P. H. (1986). The effect of dietary protein on the pathogenesis of acute ovine haemonchosis. Veterinary Parasitology 4, 275–89.Google Scholar
Behnke, J. M. & Wakelin, D. (1973). The survival of Trichuris muris in wild populations of Its natural hosts. Parasitology 67, 157–64.CrossRefGoogle ScholarPubMed
Beisel, W. R. (1982). Synergism and antagonism of parasitic disease and malnutrition. Reviews of Infectious Diseases 4, 746–50.Google Scholar
Berding, C., Keymer, A. E., Murray, J. D. & Slater, A. F. G. (1986). The population dynamics of acquired immunity to helminth infection. Journal of Theoretical Biology 122, 459–71.Google Scholar
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–54.CrossRefGoogle ScholarPubMed
Brailsford, T. J. & Mapes, C. J. (1987). Comparisons of Heligmosomoides polygyrus primary infection in protein-deficient and well-nourished mice. Parasitology 95, 311–21.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. & Golden, M. H. N. (1987). The impact of host nutrition on gastrointestinal helminth populations. Parasitology 95, 623–35.Google Scholar
Chandra, R. K. & Newberne, P. M. (1977). Nutrition, Immunity and Infection. Mechanisms of Interactions. New York: Plenum Press.CrossRefGoogle Scholar
Crombie, J. A. & Anderson, R. M. (1985). Population dynamics of Schistosoma mansoni in mice repeatedly exposed to infection. Nature, London 315, 491–3.CrossRefGoogle ScholarPubMed
Crompton, D. W. T., Walters, D. E. & Arnold, S. (1981). Changes in the food intake and body weight of protein-malnourished rats infected with Nippostrongylus brasiliensis (Nematoda). Parasitology 82, 23–8.Google Scholar
Cummins, A. G., Duncombe, V. M., Bolin, T. D., Davis, A. E. & Yong, J. (1987). The response of the small intestine of the protein-deficient rat to infection with Nippostrongylus brasiliensis. International Journal for Parasitology 17, 1445–50.Google Scholar
Donaldson, A. W. & Otto, G. F. (1946). Effects of protein-deficient diets on immunity to a nematode. (Nippostrongylus muris) infection. American Journal of Hygiene 44, 384–99.Google Scholar
Duncombe, V. M., Bolin, T. D., Davis, A. E. & Kelly, J. D. (1981). Delayed rejection of the nematode Nippostrongylus brasiliensis from rats on a low protein diet: role of a bone marrow component. American Journal of Clinical Nutrition 34, 400–3.Google Scholar
Else, K. & Wakelin, D. (1989). Genetic variation in the humoral immune responses of mice to the nematode Trichuris muris. Parasite Immunology 11, 77–90.Google Scholar
Forsum, E., Nesheim, M. C. & Crompton, D. W. T. (1981). Nutritional aspects of Ascaris infection in young protein deficient pigs. Parasitology 83, 497–512.Google Scholar
Foster, A. O. & Cort, W. W. (1932). The relation of diet to the susceptibility of dogs to Ancylostoma caninum. American Journal of Hygiene 16, 216–65.Google Scholar
Gershwin, M. E., Richard, B. S. & Hurley, L. S. (1985). Nutrition and Immunology. New York: Academic Press.Google Scholar
Grenfell, B. T., Smith, G. & Anderson, R. M. (1987). The regulation of Ostertagia ostertagi populations in calves: the effect of past and current experience of infection on proportional establishment and parasite survival. Parasitology 95, 363–72.Google Scholar
Jose, D. G. & Welch, J. S. (1970). Growth retardation, anemia and infection, with malabsorption and infestation of the bowel. The syndrome of protein-calorie malnutrition in Australian Aboriginal children. Medical Journal of Australia 1, 349–52.Google Scholar
Keymer, A. E., Crompton, D. W. T. & Walters, D. E. (1983). Nippostrongylus (Nematoda) in protein-malnourished rats: host mortality, morbidity and rehabilitation. Parasitology 86, 461–75.CrossRefGoogle ScholarPubMed
Laine, K. & Hennttonen, H. (1983). The role of plant production in microtine cycles in northern Fennoscandia. Oikos 40, 407–18.Google Scholar
McMurray, D. N., Loomis, S. A., Casazza, L. J., Rey, H. & Miranda, R. (1981). Development of impaired cell-mediated immunity in mild and moderate malnutrition. American Journal of Clinical Nutrition 34, 68–77.Google Scholar
Michael, E. & Bundy, D. A. P. (1988). Density dependence in establishment, growth and worm fecundity in intestinal helminthiasis: the population biology of Trichuris muris (Nematoda) infection in CBA/Ca mice. Parasitology 98, 451–8.Google Scholar
Michael, E. & Bundy, D. A. P. (1991). The effect of the protein content of CBA/Ca mouse diet on the population dynamics of Trichuris muris (Nematoda) in primary infection. Parasitology 103, 403–11.Google Scholar
Michael, E. & Bundy, D. A. P. (1992). Nutrition, immunity and helminth infection: effect of dietary protein on the dynamics of the primary antibody response to Trichuris muris (Nematoda) in CBA/Ca mice. Parasite Immunology 14, 169–83.Google Scholar
Slater, A. F. G. (1988). The influence of dietary protein on the experimental epidemiology of Heligmosomoides polygurus (Nematoda) in the laboratory mouse. Proceedings of the Royal Society of London, B 234, 239–54.Google Scholar
Slater, A. F. G. & Keymer, A. E. (1986). Heligmosomoides polygyrus (Nematoda): the influence of dietary protein on the dynamics of repeated infection. Proceedings of the Royal Society of London, B 229, 69–83.Google Scholar
Slater, A. F. G. & Keymer, A. E. (1988). The influence of protein deficiency on immunity to Heligmosomoides polygyrus (Nematoda) in mice. Parasite Immunology 10, 507–22.Google Scholar
Stephenson, L. S. (1987). The Impact of Helminth Infections on Human Nutrition. London: Taylor and Francis.Google Scholar
Sykes, A. R. (1982). Nutritional and physiological aspects of helminthiasis in sheep. In Biology and Control of Endoparasites (ed. Symonds, L. E. A., Donald, A. D. & Dineen, J. K.), pp. 217–234. Sydney: Academic Press.Google Scholar
Tomkins, A. (1986). Intestinal parasites. Part 1. Nutritional importance. In Diarrhoea and Malnutrition in Childhood, (ed. Walker-Smith, J. A. & McNeish, A. S.), pp. 60–67. London: Butterworth.Google Scholar
Tomkins, A. & Watson, F. (1989). Malnutrition and Infection. A Review. ACC/SCN State-of-the-Art Series. Nutrition Policy Discussion Paper, No. 5. Geneva: United Nations.Google Scholar
Towbin, H., Staehelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 4350–54.CrossRefGoogle ScholarPubMed
Wakelin, D. (1967). Acquired immunity to Trichuris muris in the albino laboratory mouse. Parasitology 57, 515–24.Google Scholar
Wakelin, D. (1973). The stimulation of immunity to Trichuris muris in mice exposed to low-level infections. Parasitology 66, 181–9.Google Scholar
Wakelin, D. (1975). Immune expulsion of Trichuris muris from mice during a primary infection: analysis of the components involved. Parasitology 70, 397–405.Google Scholar
Wakelin, D. & Lee, T. D. G. (1987). Immunobiology of Trichuris and Capillaria infections. In Immune Responses in Parasitic Infections: Immunology, Immunopathology and Immunoprophylaxis, vol. 1 (ed. Soulsby, E. J. L.), pp. 61–88. Boca Raton: CRC Press.Google Scholar
Wakelin, D. & Selby, G. R. (1976). Immune expulsion of Trichuris muris from resistant mice: suppression by irradiation and restoration by transfer of lymphoid cells. Parasitology 72, 41–50.Google Scholar