Hostname: page-component-cd4964975-pf4mj Total loading time: 0 Render date: 2023-03-31T15:30:23.170Z Has data issue: true Feature Flags: { "useRatesEcommerce": false } hasContentIssue true

Studies on the immunity of sheep to Oesophagostomum columbianum: effects of low-protein diet on resistance to infection and cellular reactions in the gut

Published online by Cambridge University Press:  06 April 2009

Colin Dobson
Department of Parasitology, University of Queensland, St Lucia, Brisbane, Queensland, 4067, Australia
Richard J. Bawden
Department of Agricultural Biology, Faculty of Rural Science, University of New England, Armidale, N.S.W., 2351, Australia


Adult Oesophagostomum columbianum populations were larger in sheep fed low-protein diets than in adequately fed animals. Diet did not influence the numbers of larva which became established in sheep. Sheep fed high-protein diets eliminated more worms and were more immunologically competent than poorly fed animals. More encapsulated larvae, showing arrested development, were found in adequately fed sheep than in those fed low-protein diets. Adult O. columbianum produced eggs at an earlier time after infection in poorly fed sheep than worms in well fed sheep. More eggs/female worm were produced in sheep on a low-protein diet compared with the number of eggs produced in well fed hosts over the last week of the infection. The effects of immunity on the behaviour of the worm in both host diet groups is discussed.

There was a greater cellular proliferation in the intestines of infected adequately fed sheep than in infected animals on low-protein diets. These changes were most pronounced in the large intestine where the adult parasites were found. The macrophage-lymphocyte series of cells underwent hyperplasia in well fed animals but these changes were reduced, particularly among the plasma cells, in sheep fed low-protein diets. Increased mucin and mast cell counts were observed in sheep on high-protein, but not in hosts on low-protein diets: the intestinal populations of eosinophil and globule leucocytes were also reduced in poorly fed sheep.

The relationship of these various cellular reactions and their effect on the protective immunity of sheep to O. columbianum is discussed. It was concluded that the increased susceptibility of protein deprived sheep to O. columbianum infections was associated with malfunctions of the innate immunity of the gut, involving decreased peristalsis and failure of the mucin cell response, and with reduction of the adaptive immune response which was reflected by impoverished lymphocyte and plasma cell reactions, and possibly with poor cooperation between sensitized lymphocytes, antibodies and the mast cell-granulocyte effector mechanisms in protective immunity.

Research Article
Copyright © Cambridge University Press 1974

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.)



Ackert, J. E. & Beach, T. D. (1933). Resistance of chickens to the nematode Ascaridia lineata, affected by dietary supplements. Transactions of the American Microscopical Society 52, 51–8.CrossRefGoogle Scholar
Ackert, J. E., Edgar, S. A. & Frick, L. P. (1939). Goblet cells and age resistance of animals to parasitism. Transactions of the American Microscopical Society 58, 81–9.CrossRefGoogle Scholar
Amman, A. J., Cain, W. A., Ishizaxa, K., Hong, R. & Good, R. A. (1969). Immunoglobulin E deficiency in ataxia-telangiectasia. New England Journal of Medicine 281, 469–72.CrossRefGoogle Scholar
Aref, G. H., Badr el Din, M. K., Hassan, A. I. & Araby, I. I. (1971). Immunoglobulins in kwashiorkor. The Journal of Tropical Medicine and Hygiene 73, 185–91.Google Scholar
Baird, D. M., Vegors, H. H., Sell, O. E. & Stewart, T. B. (1954). Performance and parasitism of beef calves as related to level of protein and pasture feeding. Journal of Animal Science 13, 1005.Google Scholar
Bawden, R. J. (1969). The establishment and survival of Oesophagostomum columbianum in male and female sheep given high and low protein diets. Australian Journal of Agricultural Research 20, 1151–9.CrossRefGoogle Scholar
Chandler, A. C. (1953). The relation of nutrition to parasitism. Journal of the Egyptian Medical Association 36, 533–52.Google ScholarPubMed
Curtain, C. C. & Anderson, N. (1971). Immunocytochemical localization of the ovine immunoglobulins IgA, IgG1, IgG1a, and Ig G2: Effect of gastro-intestinal parasitism in sheep. Clinical and Experimental Immunology 8, 151–62.Google Scholar
Dash, K. D. (1970). Biology of parasitic nematodes in relation to host immunity. Thesis: University of Queensland Library.Google Scholar
Dineen, J. K. & Adams, D. B. (1971). The role of the recirculating thymus-dependent lymphocyte in resistance to Trichostrongylus colubriformis in the guinea-pig. Immunology 20, 109–13.Google ScholarPubMed
Dobson, C. (1966 a). Studies on the immunity of sheep to Oesophagostomum columbianum: Proteins and haemagglutinating antibodies in mucous exudates and intestinal tissue extracts. Australian Journal of Agricultural Research 17, 779–96.CrossRefGoogle Scholar
Dobson, C. (1966 b). Distribution of Oesophagostomum columbianum larvae along the alimentary tract of the sheep. Australian Journal of Agricultural Research 17, 765–77.CrossRefGoogle Scholar
Dobson, C. (1966 c). Precipitating antibodies in extracts from the mucosa and tunica muscularis of the elimentary tract of sheep infected with Oesophagostomum columbianum. Journal of Parasitology 52, 1037–8.CrossRefGoogle ScholarPubMed
Dobson, C. (1967). Changes in the protein content of the serum and intestinal mucus of sheep with reference to the histology of the gut and immunological response to Oesophagostomum columbianum infections. Parasitology 57, 201–19.CrossRefGoogle ScholarPubMed
Dobson, C. (1972). Immune response to gastro-intestinal helminths. In Immunity to parasitic animals (ed. Soulsby, E. J. L.), pp. 191222. New York: Academic Press.Google Scholar
Dobson, C. (1974). Studies on the immunity of sheep to Oesophagostomum columbianum: effects of different and successive doses of larvae on worm burdens, worm growth and fecundity. Parasitology 68, 313–22.CrossRefGoogle ScholarPubMed
Frick, L. P. & Ackert, J. E. (1948). Further studies on duodenal mucus as a factor in age resistance of chickens to parasitism. Journal of Parasitology 34, 192201.CrossRefGoogle ScholarPubMed
Geefhuysen, J., Rosen, E. U., Katz, J., Ipp, T. & Metz, J. (1971). Impaired cellular immunity in kwashiorkor with improvement after therapy. British Medical Journal 4, 527–9.CrossRefGoogle ScholarPubMed
Geiman, Q. M. (1958). Nutritional effects of parasitic infections and disease. Vitamins and Hormones 16, 133.CrossRefGoogle ScholarPubMed
Gibson, T. E. (1963). The influence of nutrition on the relationships between gastro-intestinal parasites and their hosts. Proceedings of the Nutrition Society 22, 1520.CrossRefGoogle ScholarPubMed
Herd, R. P. (1969). Immunity to Chabertia ovina in the sheep. Australian Veterinary Journal 45, 595.Google ScholarPubMed
Hunter, G. C. (1953). Nutrition and host-helminth relationships. Nutrition Abstracts and Reviews 23, 705–14.Google ScholarPubMed
Jackson, G. M. (1925). The Effects of Inanition and Malnutrition upon Growth and Structure. Philadelphia: Blackiston.CrossRefGoogle Scholar
Kates, K. C. & Wilson, G. I. (1955). Effect of two rations, differing primarily in protein, carbohydrate and crude fiber content, on experimental Haemonchiasis in lambs. Journal of Parasitology 41, suppl. 43.Google Scholar
Kay, A. B. (1970). Studies on eosinophil leucocyte migration. 1. Eosinophil and neutrophil accumulation following antigen-antibody reactions in guinea-pig skin. Clinical and Experimental Immunology 6, 7586.Google Scholar
Keet, M. B. & Thom, H. (1969). Serum immunoglobulins in kwashiorkor. Archives of Disease in Childhood 44, 600–3.CrossRefGoogle ScholarPubMed
Keller, R. (1971). Nippostrongylus brasiliensis in the rat: Failure to relate intestinal histamine and mast cell levels with worm expulsion. Parasitology 63, 473–81.CrossRefGoogle ScholarPubMed
Loosli, C. G. (1936). Outlines of Histological Methods. Chicago: University of Chicago Press.Google Scholar
Magee, D. F. (1962). Gastro-intestinal Physiology. Springfield, Illinois: Charles C. Thomas.Google Scholar
Mathies, A. W. (1962). Certain aspects of the host-parasite relationship of Aspiculuris tetraptera, a mouse pin worm. III. Effect of cortisone. Journal of Parasitology 48, 244–8.CrossRefGoogle Scholar
Ogilvie, B. M. & Jones, V. E. (1971). Nippostrongylus brasiliensis: A review of immunity and the host/parasite relationship in the rat. Experimental Parasitology 29, 238–77.CrossRefGoogle Scholar
Parish, W. E. (1969). Investigations on eosinophilia. The influence of histamine on antigen-antibody complexes containing γ1 or γ2 globulins, foreign bodies (phagocytosis) and disrupted mast cells. British Journal of Dermatology 81, Supplement 3, 28.CrossRefGoogle Scholar
Peterson, R. D. A., Cooper, M. D. & Good, R. A. (1966). Lymphoid tissue abnormalities associated with ataxia-telangiectasia. American Journal of Medicine 4, 342–59.CrossRefGoogle Scholar
Roberts, F. H. S. & O'Sullivan, P. J. (1950). Methods for egg counts and larval cultures for strongyles infesting the gastro-intestinal tract of cattle. Australian Journal of Agricultural Research 1, 99102.CrossRefGoogle Scholar
Shelton, G. C. (1965). Host-parasite relationship studies of Oesophagostomum columbianum (Curtice, 1890) Stossich, 1899. Ph.D. thesis, University of Minnesota.Google Scholar
Taliaferro, W. H. & Sarles, M. P. (1939). The cellular reactions in the skin, lungs and intestine of normal and immune rats after infection with Nippostrongylus inuris. Journal of Infectious Disease 64, 157–92.CrossRefGoogle Scholar
Taliaferro, W. H., Woolridge, R. L. & Benditt, E. P. (1949). The effect of protein depletion on acquired immunity in trichinosis. Science 109, 443.Google Scholar
Taylor, E. L. & Michel, J. F. (1953). The parasitological and pathological significance of arrested development in nematodes. Journal of Helminthology 27, 199205.CrossRefGoogle Scholar
Vegors, H. H., Baird, D. M., Sell, O. E. & Stewart, T. B. (1956). Parasitism in beef yearlings as related to forage availability and levels of protein feed. Journal of Animal Sciences 15, 1199–206.Google Scholar
Watson, G. E. & Freesman, G. (1970). Immunoglobulins in protein-calorie malnutrition. Archives of Diseases in Childhood 45, 282–4.CrossRefGoogle ScholarPubMed
Wells, P. D. (1962). Mast cell, eosinophil and histamine levels in Nippostrongylus brasiliensis infected rats. Experimental Parasitology 12, 82101.CrossRefGoogle ScholarPubMed
Wells, P. D. (1963). Mucin-secreting cells in rats infected with Nippostrongylus brasiliensis. Experimental Parasitology 14, 1522.CrossRefGoogle ScholarPubMed