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Intestinal nematode infections in children: the pathophysiological price paid

Published online by Cambridge University Press:  06 April 2009

E. S. Cooper ,
C. A. M. Whyte-Alleng ,
J. S. Finzi-Smith  and
T. T. MacDonald
E. S. Cooper
Affiliation:
Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica Parasite Epidemiology Research Group, Department of Biology, Imperial College, London SW7 2AZ, UK
C. A. M. Whyte-Alleng
Affiliation:
Department of Zoology, University of the West Indies (Jamaica)
J. S. Finzi-Smith
Affiliation:
Tropical Metabolism Research Unit, University of the West Indies, Mona, Kingston 7, Jamaica
T. T. MacDonald
Affiliation:
Department of Paediatric Gastroenterology, St Bartholomew's Hospital Medical College, London ECIA 7BE, UK
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Summary

The mechanism by which small animals such as rodents resist or eliminate nematode parasites requires mucosal in flammation as the final effector of the immune response. The resulting freedom from chronic infection may be worth the price of short-term illness. Putative vaccines which attempt to enhance the natural effect will have to take into account the inflammatory cost to the host. Human helminthiases involve a more stable equilibrium between host and parasite. The medical literature on hookworm disease and clinical ascariasis describes, for the former, some chronic inflammatory effects correlated with worm burden, but for the latter a less quantified or predictable set of detrimental effects. We describe a current, systematic study of the inflammatory response to whipworm infection, in which anaemia, growth retardation and intestinal leakiness are viewed as predictable consequences related to infection intensity. There is evidence for the absence of cell-mediated immunopathology. However, a specific, IgE-mediated local anaphylaxis may, at least partly, mediate the deleterious effects. Increased numbers of mucosal macrophages may also contribute to the chronic, systemic effects through their output of cytokines. Similar attempts to show the mechanisms of pathogenesis and quantify the effects of hookworm disease should be undertaken.

Keywords

mucosal inflammationlocal anaphylaxishelminthiaseshuman growth.
Type
Geohelminthiasis
Information
Parasitology , Volume 104 , Issue S1: Symposia of the British Society for Parasitology Volume 29:Human parasitic disease: the complementory roles of field and laboratory studies , June 1992 , pp. S91 - S103
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Areekul, S., Devakul, K., Chantachum, Y., Boonanyanta, C., Ecoromaiphol, S. & Viravan, C. (1971). Gastrointestinal protein loss in patients with hookworm infection. Journal of the Medical Association of Thailand 34, 28–32.Google Scholar
Beaver, P. C. & Danaraj, T. J. (1958). Pulmonary ascariasis resembling eosinophilic lung. American Journal of Tropical Medicine and Hygiene 7, 100–11.CrossRefGoogle ScholarPubMed
Beer, R. J., Sansom, S. F. & Taylor, R. J. (1974). Erythrocyte losses from pigs with experimental Trichuris suis infections measured with a whole-body counter. Journal of Comparative Pathology 84, 331–46.Google Scholar
Behrens, R. H., Lunn, P. G., Northrop, C. A., Hanlon, P. W. & Neale, G. (1987). Factors affecting the integrity of the intestinal mucosa of Gambian children. American Journal of Clinical Nutrition 45, 1433–41.Google Scholar
Blackman, V., Marsen, P., Banwell, J. G. & Craggs, M. H. (1965). Albumin metabolism in hookworm anaemia. Transactions of the Royal Society of Tropical Medicine and Hygiene 59, 472–82.Google Scholar
Blom, M., Prag, J. B. & Norredam, K. (1979). α1-glycoprotein, α1 and ceruloplasmin in human intestinal helminthiasis. American Journal of Tropical Medicine and Hygiene 28, 76–83.Google Scholar
Braegger, C. P., Corrigan, C. J. & MacDonald, T. T. (1990). Finger clubbing and tumour necrosis factor α. Lancet 336, 759–60.Google Scholar
Bremner, O. A., O'hara, M. D., Angel, P., Chojkier, M. & Karin, M. (1989). Prolonged activation of jun and collagenase genes by tumour necrosis factor-α. Nature, London 337, 661–3.Google Scholar
Bundy, D. A. P. (1986). Epidemiological aspects of Trichuris and trichuriasis in Caribbean communities. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 702–18.CrossRefGoogle ScholarPubMed
Bundy, D. A. P., Cooper, E. S., Thompson, D. E., Anderson, R. M. & Didier, J. M. (1987). Age-related prevalence and intensity of Trichuris trichiura in a St Lucian community. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 85–94.Google Scholar
Burman, N. N., Sehgali, A. K., Chakravarti, R. N., Sodhi, J. G. & Chuttani, R. N. (1970). Morphological and absorption studies in hookworm infestation (ankylostomiasis). Indian Journal of Medical Research 58, 317–25.Google Scholar
Butcher, G. A., Garland, T., Ajdukiewlcz, A. B. & Clarke, I. A. (1990). Serum tumour necrosis factor associated with malaria in patients in the Solomon islands. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 658–61.CrossRefGoogle ScholarPubMed
Castro, G. A. (1989). Immunophysiology of enteric parasitism. Parasitology Today 5, 11–19.Google Scholar
Chanco, P. P. & Vidad, J. Y. (1978). A review of trichuriasis, its incidence, pathogenesis and treatment. Drugs (Suppl.) 15, 87–93.CrossRefGoogle Scholar
Clark, I. A., Chaudri, G. & Cowden, W. B. (1986). Roles of tumour necrosis factor in the illness and pathology of malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 658–61.Google Scholar
Cooper, E. S. & Bundy, D. A. P. (1986). Trichuriasis in St Lucia. In Diarrhoea and Malnutrition in Childhood (ed. McNeish, A. S. & Walker-Smith, J. A.), pp. 91–6. London: Butterworths.CrossRefGoogle Scholar
Cooper, E. S. & Bundy, D. A. P. (1987). Trichuriasis. Clinical Tropical Medicine and Communicable Diseases 2, 629–43.Google Scholar
Cooper, E., Spencer, J., Murch, S., Venugopal, S., Hanchard, B., Bundy, D. & MacDonald, T. T. (1990 a). Mucosal macrophages and plasma cachectin (TNF) in Trichuris colitis. Bulletin de la Socilté Française de Parasitologie (Suppl. 2), 347.Google Scholar
Cooper, E. S., Bundy, D. A. P., MacDonald, T. T. & Golden, M. H. N. (1990 b). Growth suppression in the Trichuris dysentery syndrome. European Journal of Clinical Nutrition 44, 285–91.Google Scholar
Cooper, E. S., Spencer, J. M., Whyte-Alleng, C. A. M., Cromwell, O., Whitney, P., Venugopal, S., Bundy, D. A. P. & MacDonald, T. T. (1991). Immediate hypersensitivity in the colon of children with chronic Trichuris trichiura dysentery. Lancet, 338, 1404–07.Google Scholar
Crompton, D. W. T., Walters, D. E. & Arnold, S. E. (1981). Changes in the food intake and body weight of protein-malnourished rats infected with Nippostrongylus brasiliensis (Nematoda). Parasitology 82, 23–38.Google Scholar
Cromwell, O. (1986). Provocation tests and measurements of mediators from mast cells and basophils in asthma and allergic rhinitis. In Handbook of Experimental Immunology (ed. Weir, D. M.), pp. 127.1–127.51. Oxford: Blackwell.Google Scholar
Ferguson, A. & Jarrett, E. E. E. (1975). Hypersensitivity reactions in the small intestine. 1. Thymus dependence of experimental ‘partial villous atrophy’. Gut 16, 114–17.Google Scholar
Forbes, D., Patrick, M., Perdue, M., Buret, A. & Gall, A. G. (1988). Intestinal anaphylaxis: in vivo and in vitro studies of the rat proximal colon. American Journal of Physiology 255, G201–205.Google ScholarPubMed
Gilman, R. H., Chong, Y. H., Davis, C., Greenberg, B., Virik, H. K. & Dixon, H. B. (1983). The adverse consequences of heavy Trichuris infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 77, 432–8.CrossRefGoogle ScholarPubMed
Golden, M. H. N. (1988). The role of individual nutrient deficiencies in growth retardation of children as exemplified by zinc and protein. In Linear Growth Retardation in Less Developed Countries (ed. Waterlow, J. C.), pp. 143–163. New York: Raven Press.Google Scholar
Greenberg, E. R. & Cline, B. L. (1979). Is trichuriasis associated with iron deficiency anaemia? American Journal of Tropical Medicine and Hygiene 28, 770–2.Google Scholar
Grimble, R. F. (1989). Cytokines: their relevance to nutrition. European Journal of Clinical Nutrition 43, 217–30.Google ScholarPubMed
Kalkofen, U. P.(1974). Intestinal trauma resulting from feeding activities of Ancylostoma caninum. American Journal of Tropical Medicine and Hygiene 23, 1046–53.Google Scholar
Keller, A. E., Googe, H. B., Cotrell, H. B., Miller, D. G. & Harvey, R. H. (1935). Clinical study under controlled conditions of 1,083 children with hookworm. Journal of the American Medical Association 105, 1670–5.Google Scholar
Lillywhite, J. E., Bundy, D. A. P., Didier, J. M., Cooper, E. S. & Bianco, A. E. (1991). Humoral immune responses in human infection with the whipworm Trichuris trichiura. Parasite Immunology 13, 491–96.Google Scholar
Lobley, R. W., Burrows, P. C., Warwick, R., Dawson, D. J. & Holmes, R. (1990). Simultaneous assessment of intestinal permeability and lactose tolerance with orally administered raflinose, lactose and L-arabinose. Clinical Science 79, 173–83.Google Scholar
Love, R. J., Kelly, J. D. & Dineen, J. K. (1974). Nippostrongylus brasiliensis: effects of immunity on the pre-intestinal and intestinal larval stages of the parasite. International Journal for Parasitology 4, 183–91.Google Scholar
Lunn, P. C., Northrop, C. A., Behrens, R. H., Martin, J. & Wainwright, M. (1986). Protein losing enteropathy associated with Nippostrongylus brasiliensis infestation and its influence on albumin homeostasis in rats fed two levels of dietary protein. Clinical Science 70, 469–75.CrossRefGoogle Scholar
Lunn, P. G., Northrop-Clewes, C. A. & Downes, R. M. (1991). Recent developments in the nutritional management of diarrhoea. 2. Chronic diarrhoea and malnutrition in the Gambia: studies on intestinal permeability. Transactions of tile Royal Society of Tropical Medicine and Hygiene 85, 8–11.CrossRefGoogle ScholarPubMed
MacDonald, T. T., Choy, M.-Y., Spencer, J., Richman, P. I., Diss, T., Hanchard, B., VEnugopal, S., Bundy, D. A. P. & COOPER, E. S. (1991). Histopathology and immunohistochemistry of the caecum in children with the Trichuris dysentery syndrome. Journal of Clinical Pathology 44, 194–9.Google Scholar
MacDonald, T. T., Horton, M. A., Choy, M.-Y. & Richman, P. I. (1990). Increased expression of the laminin/collagen receptor (VLA-1) on epithelium of inflamed human intestine. Journal of Clinical Pathology 43, 313–15.CrossRefGoogle ScholarPubMed
MacDonald, T. T. & Spencer, J. M. (1988). Evidence that activated T cells play a role in the pathogenesis of enteropathy in human small intestine. Journal of Experimental Medicine 167, 1341–9.Google Scholar
Menzies, I. S., Pounder, R., Heyer, S., Laker, M. F., Bull, J., Wheeler, P. G. & Creamer, B. (1979). Abnormal intestinal permeability to sugars in villous atrophy. Lancet ii, 1107–9.Google Scholar
Miller, H. R. P., Huntley, J. F. & Wallace, G. R. (1981). Immune exclusion and mucus trapping during the rapid expulsion of Nippostrongylus brasiliensis from primed rats. Immunology 44, 419–29.Google Scholar
Miller, T. A. (1978). Industrial development and field use of the canine hookworm vaccine. Advances in Parasitology 16, 333–42.CrossRefGoogle ScholarPubMed
Miller, T. A. (1979). Hookworm infection in man. Advances in Parasitology 17, 315–83.Google Scholar
Moldawer, L. L., Anderson, C., Gelin, J., Lonroth, C. & Lundholm, K. (1988). Regulation of food intake and hepatic protein metabolism by recombinant-derived monokines. American Journal of Physiology 254, G450–456.Google Scholar
Moqbel, R. & MacDonald, A. J. (1990). Immunological and inflammatory responses in the small intestine associated with helminthic infections. In Parasites: Immunity and Pathology (ed. Behnke, J. M.), pp. 249–82. London: Taylor & Francis.Google Scholar
Mullin, J. M. & Snock, K. V. (1990). Effect of Tumour Necrosis Factor on epithelial tight junctions and transepithelial permeability. Cancer Research 50, 2172–6.Google Scholar
Murch, S. H., Lambikin, V. A., Savage, M. O., Walker-Smith, J. A. & MacDonald, T. T. (1991). Tumor necrosis factor/cachectin and growth suppression in children with inflammatory bowel disease. Gut, 32, 913–17.CrossRefGoogle Scholar
Otto, G. F. (1935). Blood studies on Trichuris-infested and worm-free children in Louisiana. American Journal of Tropical Medicine 15, 693–704.Google Scholar
Prasad, A., Tanner, J. M. & Von Harnack, G. A. (1963). Catch-up growth following illness or starvation. Journal of Pediatrics 62, 646–59.Google Scholar
Prasad, A.. (1985). Clinical manifestations of zinc deficiency. Annual Reviews of Nutrition 5, 341–63.CrossRefGoogle ScholarPubMed
Roche, M. & Layrisse, M. (1966). The nature and causes of ‘hookworm anaemia’. American Journal of Tropical Medicine and Hygiene 15, Part 2.Google Scholar
Saklatvala, J. (1986). Tumour necrosis factor stimulates resorption and inhibits synthesis of proteoglycans in cartilage. Nature, London 322, 547–9.Google Scholar
Sanderson, I. R., Boulton, P., Menzies, I. & Walker-Smith, J. A. (1987). Improvement of abnormal lactulose/rhamnose permeability in active Crohn's disease of the small bowel by an elemental diet. Gut 28, 1073–6.Google Scholar
Selby, W. S., Janossy, G., Mason, D. Y. & Jewell, D. P. (1983). Expression of HLA-DR antigens by colonic epithelium in inflammatory bowel disease. Clinical and Experimental Immunology 53, 614–18.Google ScholarPubMed
Smillie, W. G. & Augustine, D. I.(1926). Hookworm infestation. The effect of varying intensities on the physical condition of schoolchildren. American Journal of Diseases of Children, 31, 151–68.CrossRefGoogle Scholar
Stadnyk, A. W. & Gauldie, J. (1991). The acute phase protein response during parasitic infection. In Immunoparasitology Today (ed. Ash, C. & Gallagher, R. B., pp. A7–A12. Cambridge: Elsevier.Google Scholar
Spencer, J., Isaacson, P. G., MacDonald, T. T., Thomas, A. J. & Walker-Smith, A. J. (1991). Gamma/delta T cells and the diagnosis of coeliac disease. Clinical and Experimental Immunology 85, 109–13.Google Scholar
Stephenson, L. S., Latham, M. C., Kurz, K. M., Kinoti, S. N. & Brigham, H. (1989). Treatment with a single dose of albendazole improves growth of Kenyan schoolchildren with hookworm, Trichuris trichiura, and Ascaris lumbricoides infections. American Journal of Tropical Medicine and Hygiene 41, 78–87.Google Scholar
Strobel, S., Miller, H. R. P. & Ferguson, A. (1981). Human intestinal mast cells: evaluation of fixing and staining techniques. Journal of Clinical Pathology 34, 851–8.Google Scholar
Symons, L. E. A. (1965). Kinetics of the epithelial cells and morphology of villi and crypts in the jejunum of the rat infected by the nematode Nippostrongylus brasiliensis. Gastroenterology 49, 158–68.Google Scholar
Tandon, B. N., Das, B. C., Saraya, A. K. & Geo, M. G. (1966). Functional and structural studies of the small bowel in ankylostomiasis. British Medical Journal 1, 714–16.Google Scholar
Tanner, J. M. & Whitehouse, R. H. (1976). Clinical longitudinal standards for height, weight, height velocity, weight velocity and stages of puberty. Archives of Disease in Childhood 56, 170–9.Google Scholar
Taren, D. L., Nesheim, M. C., Crompton, D. W. T. & Holland, C. (1987). Contribution of ascariasis to poor nutritional status in children from Chiriqui province, Republic of Panama. Parasitology 95, 615–22.Google Scholar
Tracey, K. J., Wei, H., Manogue, K. R., Fong, Y., Hesse, D. G., Hai, T. N., Kuo, G. C., Beutler, B., Cotran, R. S., Cerami, A. & Lowry, S. F. (1988). Cachectin/tumour necrosis factor induces cachexia, anemia and inflammation. Journal of Experimental Medicine 167, 1211–27.Google Scholar
Tripathy, K., Dugue, E., Bolanos, O., Lotero, H. & Mayoral, L. G. (1972). Malabsorption syndrome in trichuriasis. American Journal of Clinical Nutrition 25, 1276–87.Google Scholar
Walker, S. P., Powell, C. A. & Crantham-McCregor, S. I. (1990). Dietary intakes and activity levels of stunted and non-stunted children in Kingston, Jamaica. Part 1. Dietary intakes. European Journal of Clinical Nutrition 44, 527–34.Google Scholar
Walton, P. E. & Cronin, M. J. (1989). Tumour necrosis factor-α inhibits growth hormone secretion from cultured anterior pituitary cells. Endocrinology 125, 925–9.Google Scholar
Wilson, R. A. (1990). Pulmonary immune responses to parasites. In Parasites: Immunity and Pathology (ed. Behnke, J. M.), pp. 208–48. London: Taylor & Francis.Google Scholar
World Health Organization (1975). Control of nutritional anaemia with special reference to iron deficiency. Technical Report Series No. 580, Geneva: WHO.Google Scholar