Hostname: page-component-76fb5796d-45l2p Total loading time: 0 Render date: 2024-04-26T12:10:45.470Z Has data issue: false hasContentIssue false
  • English
  • Français

Density-dependent regulation of the growth of the hookworms Necator americanus and Ancylostoma ceylanicum

Published online by Cambridge University Press:  06 April 2009

S. M. B. Norozian-Amiri  and
J. M. Behnke
S. M. B. Norozian-Amiri
Affiliation:
MRC Experimental Parasitology Research Group, Department of Life Science, University of Nottingham, University Park, Nottingham NG7 2RD
J. M. Behnke
Affiliation:
MRC Experimental Parasitology Research Group, Department of Life Science, University of Nottingham, University Park, Nottingham NG7 2RD
Get access Rights & Permissions [Opens in a new window]

Summary

Laboratory bred DSN hamsters were exposed to varying doses of infective larvae of Ancylostoma ceylanicum (orally) or Necator americanus (percutaneously) and were autopsied at times which corresponded to a period immediately before cessation of growth of worms or soon afterwards. A total of 829 (404 male and 425 female) A. ceylanicum and 1582 (781 male and 801 female) N. americanus were measured. At worm burdens of fewer than 100, the length of A. ceylanicum appeared to increase with infection intensity and no evidence was found that growth was retarded under crowded conditions. In an experiment comparing directly low (mean worm burden = 22) and heavy infections (mean worm burden = 180) significant negative associations between both weight and width, and worm burden were detected, but length again increased with worm burden. In contrast, 5 experiments with N. americanus indicated negative relationships between measures of worm size (length, width, wet and dry weight) and worm burden. It was concluded that N. americanus is subject to regulation by density-dependent processes within the host while A. ceylanicum is not sensitive to the same degree.

Keywords

NematodaNecator americanusAncylostoma ceylanicumhookwormscrowdinggrowth
Type
Research Article
Information
Parasitology , Volume 109 , Issue 1 , July 1994 , pp. 119 - 128
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

Beaver, P. C. (1988). Light, long-lasting Necator infection in a volunteer. American Journal of Tropical Medicine and Hygiene 39, 369–72.CrossRefGoogle Scholar
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.), pp. 105–28. London: Taylor and Francis.Google Scholar
Behnke, J. M. (1991). Immunology. In Human Parasitic Diseases, Vol. 4, Hookworm Infections (ed. Gilles, H. M. & Ball, P. A. J.), pp. 93–155. Amsterdam: Elsevier.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 of Tropical Medicine and Hygiene 80, 146–9.CrossRefGoogle ScholarPubMed
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
Behnke, J. M. & Pritchard, D. I. (1987). Necator americanus in neonatally infected 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
Bonne, C. (1942). Invasion of the wall of the human intestine by ancylostomes. American Journal of Medicine 22, 507–9.Google Scholar
Bradley, M., Chandiwana, S. K., Bundy, D. A. P. & Medley, G. F. (1992). The epidemiology and population biology of Necator americanus infection in a rural community in Zimbabwe. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 73–6.CrossRefGoogle Scholar
Bundy, D. A. P. (1990). Is the hookworm just another geohelminth? In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.), pp. 147–64. London: Taylor and Francis.Google 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
Garside, P. & Behnke, J. M. (1989). Ancylostoma ceylanicum: observations on host-parasite relationship during primary infection. Parasitology 98, 283–9.CrossRefGoogle ScholarPubMed
Haswell-Elkins, M. R., Elkins, D. B., Manjula, K., Michael, E. & Anderson, R. M. (1988). An investigation of hookworm infection and reinfection following mass anthelmintic treatment in the South Indian fishing community of Vairavankuppam. Parasitology 96, 565–77.CrossRefGoogle ScholarPubMed
Kendrick, J. R. (1934). The length of life and rate of loss of hookworms, Ancylostoma duodenale and Necator americanus. American Journal of Tropical Medicine and Hygiene 14, 363–79.CrossRefGoogle Scholar
Keymer, A. (1982). Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 84, 573–87.CrossRefGoogle ScholarPubMed
Komiya, Y. & Yasuraoka, K. (1966). The biology of hookworms. In Progress of Parasitology in Japan, Vol. 3, pp. 1–114. Tokyo: Meguro Parasitological Museum.Google Scholar
Krupp, I. M. (1961). The effects of crowding and super-infection on habitat selection and egg production of Ancylostoma caninum. Journal of Parasitology 47, 957–61.CrossRefGoogle Scholar
McCoy, O. R. (1931). Immunity reactions of the dog against hookworm (Ancylostoma caninum) under conditions of repeated infection. American Journal of Hygiene 14, 268–303.Google Scholar
Meddis, R. (1984). Statistics Using Ranks. A Unified Approach. New York: Basil Blackwell Publishers Ltd.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. (1971). Vaccination against the canine hookworm diseases. Advances in Parasitology 9, 153–83.CrossRefGoogle ScholarPubMed
Moss, G. E. (1971). The nature of the immune response of the mouse to the bile duct cestode Hymenolepis microstoma. Parasitology 62, 285–94.CrossRefGoogle Scholar
Nagayoshi, K. & Mudaguchi, T. (1956). Studies on bionomics of hookworms. 1. Effect of crowding on the length of worms. Tokyo Iji Shinshi 73, 367–8.Google Scholar
Ogilvie, B. M., Bartlett, A., Godfrey, R. C., Turton, J. A., Worms, M. J. & Yeates, R. A. (1978). Antibody responses in self-infections with Necator americanus. Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 66–71.CrossRefGoogle ScholarPubMed
Pritchard, D. I., Quinnell, R. J., Slater, A. F. G., McKean, P. G., Dale, D. D. S., Raiko, A. & Keymer, A. E. (1990). The epidemiological significance of acquired immunity to Necator americanus: humoral responses to parasite collagen and excretory–secretory antigens. Parasitology 100, 317–26.CrossRefGoogle Scholar
Pritchard, D. I., Walsh, E. A., Quinnell, R. J., Raiko, A., Edmonds, P. & Keymer, A. E. (1992). Isotypic variation in antibody responses in a community in Papua New Guinea to larval and adult antigens during infection, and following reinfection, with the hookworm. Necator americanus. Parasite Immunology 14, 617–31.CrossRefGoogle Scholar
Quinnell, R. J., Slater, A. F. G., Tighe, P., Walsh, E. A., Keymer, A. E. & Pritchard, D. I. (1993). Reinfection with hookworm after chemotherapy in Papua New Guinea. Parasitology 106, 379–85.CrossRefGoogle ScholarPubMed
Rajasekariah, G. R., Deb, B. N., Dhage, K. R. & Bose, S. (1985). Site of resistance to Necator americanus in hamsters. 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
Roche, M. & Layrisse, M. (1966). The nature and causes of hookworm anemia. American Journal of Tropical Medicine and Hygiene 15, 1031–100.CrossRefGoogle ScholarPubMed
Rose, R. A. & Behnke, J. M. (1990). Necator americanus in the DSN hamster: density dependent expulsion of adult worms during primary infection. Parasitology 100, 469–78.CrossRefGoogle ScholarPubMed
Sarles, M. P. (1929 a). The length of life and rate of loss of the dog hookworm, Ancylostoma caninum. American Journal of Hygiene 10, 667–82.Google Scholar
Sarles, M. P. (1929 b). The effect of age and size of infestation on the egg production of the dog hookworm, Ancylostoma caninum. American Journal of Hygiene 10, 658–66.Google Scholar
Sen, H. G. (1972). Necator americanus: behaviour in hamsters. Experimental Parasitology 32, 26–32.CrossRefGoogle ScholarPubMed
Yazima, F. & Machida, K. (1958). On the ecological relations of parasite state of Ancylostoma caninum, especially on the density effect of population. Kiseichugaku Zasshi 7, 631–40.Google Scholar