Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T06:57:46.808Z Has data issue: false hasContentIssue false

Epidemiology and immunology of Necator americanus infection in a community in Papua New Guinea: humoral responses to excretory-secretory and cuticular collagen antigens

Published online by Cambridge University Press:  06 April 2009

D. I. Pritchard
Affiliation:
Department of Zoology, University Park, Nottingham NG7 2RD
R. J. Quinnell
Affiliation:
Department of Zoology, University Park, Nottingham NG7 2RD
A. F. G. Slater
Affiliation:
Department of Zoology, University Park, Nottingham NG7 2RD
P. G. McKean
Affiliation:
Department of Zoology, University Park, Nottingham NG7 2RD
D. D. S. Dale
Affiliation:
Department of Zoology, University Park, Nottingham NG7 2RD
A. Raiko
Affiliation:
Department of Zoology, University Park, Nottingham NG7 2RD
A. E. Keymer
Affiliation:
Department of Zoology, University Park, Nottingham NG7 2RD

Summary

Baseline data from an immuno-epidemiological study of hookworm infection in a rural village in Madang Province, Papua New Guinea are reported. Necator americanus was found to be the commonest helminth infection, with a prevalence of near 100% and intensity of 40 worms per host in adults. Enterobius vermicularis, Ascaris lumbricoides and Trichuris trichiura were also present, at prevalences of 53, 10 and 3% respectively; Ancylostoma duodenale was absent. The frequency distribution of N. americanus was highly over-dispersed, and was well described by a negative binomial distribution with aggregation parameter, k, of 0·370. Intensity of infection was significantly related to host age, but did not differ between the sexes. Haemoglobin levels and haematocrit values were indicative of anaemia in the community, but were unrelated to hookworm infection. Levels of antibodies (IgG, IgA and 1gM combined) against adult Necator cuticular collagen and excretory-secretory (ES) products were determined.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1990

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

Anderson, R. M. (1980). The dynamics and control of direct life cycle helminth parasites. Lecture Notes in Biomathematics 39, 278322.CrossRefGoogle Scholar
Anderson, R. M. (1986). The population dynamics and epidemiology of intestinal nematode infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 686–96.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1985). Herd immunity to helminth infection and implications for parasite control. Nature, London 315, 493–6.CrossRefGoogle ScholarPubMed
Anderson, R. M. & Medley, G. F. (1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology 90, 629–60.CrossRefGoogle Scholar
Anderson, R. M. & Schad, G. A. (1985). Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 812–25.CrossRefGoogle ScholarPubMed
Ball, P. A. J. & Bartlett, A. (1969). Serological reactions to infection with Necator americanus. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 362–9.CrossRefGoogle ScholarPubMed
Ball, P. A. J., Voller, A. & Taffs, L. F. (1971). Hypersensitivity to some nematode antigens. British Medical Journal 23 01. 1971, 210–11.CrossRefGoogle ScholarPubMed
Behnke, J. M. (1987). Do hookworms elicit protective immunity in man? Parasitology Today 3, 200–6.CrossRefGoogle ScholarPubMed
Butterworth, A. E. (1984). Cell-mediated damage to helminths. Advances in Parasitology 23, 143235.CrossRefGoogle ScholarPubMed
Carr, A. & Pritchard, D. I. (1986). Identification of hookworm (Necator americanus) antigens and their translation in vitro.Molecular and Biochemical Parasitology 19, 251–8.CrossRefGoogle ScholarPubMed
Carr, A. & Pritchard, D.I. (1987). Antigen expression during development of the human hookworm Necator americanus (Nematoda). Parasite Immunology 9, 219–34.CrossRefGoogle ScholarPubMed
Grove, D. I., Burston, T. O. & Forbes, I. J. (1974). Immunoglobulin E and eosinophil levels in atopic and non-atopic populations infested with hookworm. Clinical Allergy 4, 295300.CrossRefGoogle ScholarPubMed
Hagan, P. (1987). Human immune response. In The Biology of Schistosomes (ed. Rollinson, D. & Simpson, A. J. G.), pp. 295320. London: Academic Press.Google Scholar
Hall, A. (1981). Quantitative variability of nematode egg counts in faeces: a study among rural Kenyans. Transactions of the Royal Society of Tropical Medicine and Hygiene 75, 682–7.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 anthelminthic treatment in the South Indian fishing community of Vairavankuppam. Parasitology 96, 565–77.CrossRefGoogle ScholarPubMed
Hornabrook, R. W., Kelly, A. & Mcmillan, B. (1975). Parasitic infection of man on Kar Kar Island, New Guinea. American Journal of Tropical Medicine and Hygiene 24, 590–5.CrossRefGoogle Scholar
Jelliffe, D. B. (1966). The Assessment of the Nutritional Status of the Community. Geneva: World Health Organization Monograph Series, 53.Google ScholarPubMed
Jones, H. I. (1976). A study of human helminthiasis on Karkar Island, Madang Province. Papua New Guinea Medical Journal 19, 165–72.Google Scholar
Kelly, A. (1974). Alimentary Parasites of Man in Papua New Guinea. Papua New Guinea: Institute of Medical Research.Google Scholar
Marsh, K., Otoo, L., Hayes, R. J., Carson, D. C. & Greenwood, B. M. (1989). Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 293303.CrossRefGoogle ScholarPubMed
Maxwell, C., Hussain, R., Nutman, T. B., Poindexter, R. W., Little, M. D., Schad, G. A. & Ottesen, E. A. (1987). The clinical and immunological responses of normal human volunteers to low dose hookworm (Necator americanus) infection. American Journal of Tropical Medicine and Hygiene 37, 126–34.CrossRefGoogle ScholarPubMed
Mckean, P. G. (1989). Analysis of the antigens of the human hookworm Necator americanus. Unpublished Ph.D. thesis, University of Nottingham.Google Scholar
Neppert, J. & Warns, C-M. (1974). Mit Ascaris, Hakenwurm und Onchocerca — Antigenen kreuzreaginerende Seren aus Liberia, Westafrika. Tropenmedizin und Parasitologie 25, 492–7.Google Scholar
Ogilvie, B. M., Bartlett, A., Godfrey, F. 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, 6671.CrossRefGoogle ScholarPubMed
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
Pritchard, D. I., Mckean, P. G. & Rogan, M. T. (1988a). Cuticular collagens–a concealed target for immune attack in hookworms. Parasitology Today 4, 239–41.CrossRefGoogle Scholar
Pritchard, D. I., Mckean, P. G. & Rogan, M. T. (1988b). Cuticle preparations from Necator americanus and their immunogenicity in the infected host. Molecular and Biochemical Parasitology 28, 275–84.CrossRefGoogle ScholarPubMed
Pritchard, D. I., Mckean, P. G., Leggett, K. V., Quinnell, R. J., Slater, A. F. C. & Keymer, A. E. (1990). The molecular basis of antigenic cross-reactivity between Necator americanus and Ascaris lumbricoides. Parasite Immunology (in the Press).Google Scholar
Roche, M. & Layrisse, M. (1966). The nature and causes of ‘hookworm anaemia’. American Journal of Tropical Medicine and Hygiene 15, 1031–102.CrossRefGoogle Scholar
Schad, G. A. & Anderson, R. M. (1985). Predisposition to hookworm infection in humans. Science 228, 1537–40.CrossRefGoogle ScholarPubMed
Shield, J., Anian, G., Ostwald, R. & Rainer, A. (1984). Reinfection with intestinal helminths after treatment with mebendazole. Papua New Guinea Medical Journal 27, 41–4.Google ScholarPubMed
Taylor, M. M. & Turton, J. A. (1976). Antigen-induced lymphocyte blastogenesis in a hookworm (Necator americanus) infection in man. Tropenmedizin und Parasitologie 27, 8992.Google Scholar
Turner, K. J., Fisher, E. H. & Mcwilliam, A. S. (1980). Homology between roundworm (Ascaris) and hookworm (Necator americanus) antigens detected by human IgE antibodies. Australian Journal of Experimental Biology and Medicine 58, 249–57.CrossRefGoogle ScholarPubMed
Vines, A. P. (1970). The Epidemiological Sample Survey of the Highlands, Mainland and Island Regions of Papua New Guinea. Department of Public Health, Port Moresby, 621 pp.Google Scholar
Warren, K. S. (1988). Hookworm control. Lancet, 15, 10 1988, 897.CrossRefGoogle Scholar
Waterlow, J. C. (1976). Classification and definition of protein energy nutrition. In Nutrition in Preventive Medicine (ed. Beaton, G. H. & Bengoa, J. M.). Geneva: WHO.Google Scholar
White, C. J., Maxwell, C. J. & Gallin, J. I. (1986). Changes in the structural and functional properties of human eosinophils during experimental infection. Journal of Infectious Diseases 154, 7883.CrossRefGoogle Scholar
World Health Organization (1975). Control of nutritional anaemia with special reference to iron deficiency. Geneva: WHO Technical Report Series, No. 580.Google Scholar