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Necator americanus in the DSN hamster: density-dependent expulsion of adult worms during primary infection

Published online by Cambridge University Press:  06 April 2009

R. A. Rose  and
J. M. Behnke
R. A. Rose
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
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Summary

Neonatal hamsters were exposed to varying doses of Necator americanus larvae and changes in the stability of the resulting worm burdens were monitored over a period of 25 weeks. No change in worm burdens was evident for the first 5 weeks of infection, irrespective of the infection intensity, but the more heavily infected groups subsequently lost worms in a density-dependent manner. Male and female hamsters lost comparable proportions of their established parasite burdens indicating that there was no host sex-linked difference in this respect. By week 15 infections had stabilized and the residual worm burdens, usually a maximum of 30 worms survived for a considerably longer period of time. Initially the percentage of male worms varied from 45% to 50% but as infection progressed male worms comprised a significantly increasing proportion of the total worm burden. By week 25 the percentage of male worms was usually in excess of 60%. The growth of infected animals was not severely affected by N. americanus, even when heavy worm burdens established initially, but a significant effect was detected particularly in week 5, prior to worm loss, when the adult worms would have been feeding on intestinal tissues and causing blood loss for a period of about 2 weeks. The most severe depression in the packed cell volume was also recorded in week 5, indicating that anaemia had been initiated in infected hamsters. Whilst, the regulation of parasite burdens in weeks 5–10 post-infection may have resulted from host immunity, the persistence of the residual worm burdens, the marked density-dependent anaemia and the subtle effect on host weight, all reflected well-documented aspects of chronic human necatoriasis.

Keywords

Necator americanushookwormsnematodehamsterworm lossanaemiaweight lossdensity-dependent expulsion
Type
Research Article
Information
Parasitology , Volume 100 , Issue 3 , June 1990 , pp. 469 - 478
Copyright
Copyright © Cambridge University Press 1990

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References

REFERENCES

Alexander, J. & Stimson, W. H. (1988). Sex hormones and the course parasitic infection. Parasitology Today 4, 189–93.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1985). Helminth infections of humans: mathematical models, population dynamics and control. Advances in Parasitology 24, 1–101.CrossRefGoogle ScholarPubMed
Banwell, J. G. & Schad, G. A. (1978). Hookworms. In Clinics in Gastroenterology 7, 129–56.CrossRefGoogle Scholar
Beaver, P. C., Yoshida, Y. & Ash, L. R. (1964). Mating of Ancylostoma caninum in relation to blood loss in the host. Journal of Parasitology 50, 286–93.CrossRefGoogle ScholarPubMed
Behnke, J. M. (1987). Do hookworms elicit protective immunity in man? Parasitology Today 3, 200–6.CrossRefGoogle ScholarPubMed
Behnke, J. M. (1990). Laboratory animal models. In Hookworm Disease: Current Status and New Directions. (ed. Schad, G. A. & Warren, K. S.) London: Taylor & Francis. (In the Press).Google Scholar
Behnke, J. M., Paul, V. & Rajasekariah, G. R. (1986 a). The growth and migration of Necator americanus following infection of neonatal hamsters. Transactions of the Royal Society for Tropical Medicine and Hygiene 80, 146–9.CrossRefGoogle ScholarPubMed
Behnke, J. M. & Pritchard, D. I. (1987). Necator americanus in neonatally hamsters. The time-course of infection and antibody response to the surface antigens of L4 and adult worms. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 967–72.CrossRefGoogle Scholar
Behnke, J. M., Wells, C. & Brown, J. (1986 b). An improved technique for experimental infections with skin penetrating nematode larvae (Necator americanus). International Journal for Parasitology 16, 461–4.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. (1988). Gender-dependent patterns of infection and disease. Parasitology Today 4, 186–9.CrossRefGoogle Scholar
Carr, A. & Pritchard, D. I. (1986). Identification of hookworm (Necator americanus) antigens and their translationin vitro. Molecular and Biochemical Parasitology 19, 251–8.CrossRefGoogle Scholar
Carroll, S. M. & Grove, D. I. (1984). Parasitological, hematologic, and immunologic responses in acute and chronic infections of dogs with Ancylostoma ceylanicum: a model of human hookworm infection. Journal of Infectious Diseases 150, 284–94.CrossRefGoogle Scholar
Crompton, D. W. T. (1989). Hookworm disease: current status and new directions, Parasitology Today 5, 1–2.CrossRefGoogle Scholar
Garside, P. & Behnke, J. M. (1989). Ancylostoma ceylanicum in the hamster: observations on the host–parasite relationship during primary infection. Parasitology 98, 283–9.CrossRefGoogle ScholarPubMed
Goble, F. C. & Konopka, E. A. (1973). Sex as a factor in infectious diseases. Transactions of the New York Academy of Sciences 35, 325–46.CrossRefGoogle Scholar
Haley, A. J. (1962). Biology of the rat nematode, Nippostrongylus brasiliensis (Travassos, 1914). II. Preparasitic stages and development in the laboratory rat. Journal of Parasitology 48, 13–23.CrossRefGoogle Scholar
Holland, C. (1987). Hookworm infection. In Impact of Helminth Infections on Human Nutrition (Stephenson, L. S.), pp. 128–60. London: Taylor & Francis.Google Scholar
Holmes, J. C. (1973). Site selection by parasitic helminths: interspecific interactions, site segregation and their importance to the development of the helminth communities. Canadian Journal of Parasitology 51, 574–8.Google Scholar
Jarrett, E. E. E., Jarrett, W. F. H. & Urquhart, G. M. (1968 a). Immunological unresponsiveness to helminth parasites: 1. The pattern of Nippostrongylus brasiliensis infection in young rats. Experimental Parasitology 23, 151–60.CrossRefGoogle Scholar
Jarrett, E. E. E., Jarrett, W. F. W. & Urquhart, G. M. (1968 b). Quantitative studies on the kinetics of establishment and expulsion of intestinal nematode populations in susceptible and immune hosts. Nippostrongylus brasiliensis in the rat. Parasitology 58, 625–39.CrossRefGoogle ScholarPubMed
Keymer, A. E. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573–87.CrossRefGoogle ScholarPubMed
Keymer, A. E. & Bundy, D. A. P. (1989). Seventy-five years of solicitude. Nature, London 337, 114.CrossRefGoogle ScholarPubMed
Knight, R. & Merrett, T. G. (1981). Hookworm infection in rural Gambia. Seasonal changes, morbidity and total IgE levels. Annals of Tropical Medicine and Parasitology 75, 299–314.CrossRefGoogle ScholarPubMed
Lee, D. L. & Martin, J. (1976). Changes in Nematodirus battus associated with the development of immunity to this nematode in lambs. In Biochemistry of Parasites and Host–Parasite Relationships (ed. van den Bossche, H.). Amsterdam: Elsevier.Google Scholar
Michael, E. & Bundy, D. A. P. (1989). 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.CrossRefGoogle ScholarPubMed
Miller, T. A. (1979). Hookworm infection in man. Advances in Parasitology 17, 315–84.CrossRefGoogle ScholarPubMed
Moss, G. D. (1971). The nature of the immune response of the mouse to the bile duct cestode, Hymenolepis microstoma. Parasitology 62, 285–94.CrossRefGoogle Scholar
Murrell, K. D. (1985). Trichinella spiralis: acquired immunity in swine. Experimental Parasitology 59, 347–54.CrossRefGoogle ScholarPubMed
Nawalinski, T., Schad, G. A. & Chowdhury, A. B. (1978 a). Population biology of hookworms in children in rural West Bengal. 1. General parasitological observations. American Journal of Tropical Medicine and Hygiene 27, 1152–61.CrossRefGoogle ScholarPubMed
Nawalinski, T., Schad, G. A. & Chowdhury, A. B. (1978 b). Population biology of hookworms in West Bengal. 2. Acquisition and loss of hookworms. American Journal of Tropical Medicine and Hygiene 27, 1162–73.CrossRefGoogle ScholarPubMed
Palmer, E. D. (1955). Course of egg output over a 15 year period in a case of experimentally induced necatoriasis americanus, in the absence of hyperinfection. American Journal of Tropical Medicine and Hygiene 4, 756–7.CrossRefGoogle Scholar
Porter, D. A. (1935). A comparative study of Nippostrongylus muris in rats and mice. American Journal of Hygiene 22, 444–66.Google Scholar
Pritchard, D. I., Behnke, J. M., Carr, A. & Wells, C. (1986). The recognition of antigens on the surface of adult and L4 Necator americanus by human and hamster post-infection sera. Parasite Immunology 8, 359 –67.CrossRefGoogle ScholarPubMed
Rajasekariah, G. R., Deb, B. N., Dhage, K. R. & Bose, S. (1985). Site of resistance to Necator americanus. Acta Tropica 42, 333–40.Google ScholarPubMed
Read, C. P. (1951). The ‘crowding effect’ in tapeworm infections. Journal of Parasitology 37, 174–8.CrossRefGoogle ScholarPubMed
Rep, B. H. (1964). A new system for the diagnosis of Ancylostomidae, especially the human hookworm species. Tropical and Geographical Medicine 16, 354–69.Google ScholarPubMed
Rep, B. H. (1966). The pathogenicity of Ancylostoma braziliense. III. Distribution and migration of a hookworm population in its host. Tropical and Geographical Medicine 18, 227–41.Google Scholar
Rep, B. H. (1975). The topographic distribution of Necator americanus and Ancylostoma duodenale in the human intestine. Tropical and Geographical Medicine 27, 169–76.Google ScholarPubMed
Roberts, L. S. (1961). The influence of population density of patterns and physiology of growth in Hymenolepis diminuta (Cestoda: Cyclophyllidea) in the definitive host. Experimental Parasitology 11, 332–71.CrossRefGoogle ScholarPubMed
Roche, M. & Layrisse, M. (1966). The nature and causes of ‘hookworm’ anemia. American Journal of Tropical Medicine and Hygiene 15, 1031–40.CrossRefGoogle ScholarPubMed
Roche, M. & Patrzek, D. (1966). The female to male ratio (FMR) in hookworm. Journal of Parasitology 52, 117–21.CrossRefGoogle ScholarPubMed
Sen, H. G. (1972). Necator americanus: behaviour in hamsters. Experimental Parasitology 32, 26–32.CrossRefGoogle ScholarPubMed
Sen, H. G. & Seth, D. (1967). Complete development of the human hookworm, Necator americanus, in golden hamsters, Mesocricetus auratus. Nature, London 214, 609–10.CrossRefGoogle Scholar
Sokal, R. R. & Rohlf, F. J. (1969). Biometry. San Francisco: Freeman.Google Scholar
Stiles, C. W. & Altman, W. L. (1913). Hookworm disease: proportion of males to females in the American hookworm (Necator americanus) based on 13,080 worms from 102 cases. US Public Health Reports, Washington 28, 7–20.Google Scholar
Upatham, E. S., Viyanant, V., Brockelman, W. Y., Kurathong, S., Lee, P. & Chindaphol, U. (1989). Prevalence, incidence, intensity and associated morbidity of intestinal helminths in South Thailand. International Journal for Parasitology 19, 217–28.CrossRefGoogle ScholarPubMed
Wakelin, D. & Donachie, A. M. (1983). Genetic control of immunity to Trichinella spiralis: influence of H-2 linked genes on immunity to the intestinal phase of infection. Immunology 48, 343–50.Google Scholar