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The relationship between Trichuris trichiura transmission intensity and the age-profiles of parasite-specific antibody isotypes in two endemic communities

Published online by Cambridge University Press:  06 April 2009

C. S. Needham ,
D. A. P. Bundy ,
J. E. Lillywhite ,
J. M. Didier ,
I. Simmons  and
A. E. Bianco
C. S. Needham
Affiliation:
Wellcome Trust Research Centre for Parasitic Infections, Department of Biology, Imperial College, Prince Consort Road, London SW7 2BB, U.K.
D. A. P. Bundy
Affiliation:
Wellcome Trust Research Centre for Parasitic Infections, Department of Biology, Imperial College, Prince Consort Road, London SW7 2BB, U.K.
J. E. Lillywhite
Affiliation:
Wellcome Trust Research Centre for Parasitic Infections, Department of Biology, Imperial College, Prince Consort Road, London SW7 2BB, U.K.
J. M. Didier
Affiliation:
Parasite Epidemiology Project, University Centre, PO Box 306, Castries, St Lucia, West Indies
I. Simmons
Affiliation:
Ministry of Health, Castries, St Lucia, West Indies
A. E. Bianco
Affiliation:
Wellcome Trust Research Centre for Parasitic Infections, Department of Biology, Imperial College, Prince Consort Road, London SW7 2BB, U.K.
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Summary

The present study compares parasite-specific antibody responses in two Caribbean communities with high and low levels of Trichuris trichiura transmission. The age-dependency of antibody levels suggest that IgG1 and IgG2 levels relate to the current intensity of infection (as assessed by density of eggs in stool (e.p.g.) and reflect the age–intensity profile at the population level. IgG4, IgE and IgA levels persist into early adulthood and the subsequent decline is gradual. In the low transmission area, lower infection levels are reflected in lower parasite-specific antibody levels (of all isotypes) in the community as a whole. Despite a significantly greater past experience of infection in the high transmission area, antibody levels are not maintained at significantly higher levels throughout adulthood. The production of IgA appears to require a threshold for triggering, and a vigorous IgA response is maintained into early adulthood only in the high transmission village where peak intensity is greatest and the age-convexity of intensity is most marked. Experimental and theoretical studies focusing on the dynamic nature of host–helminth interactions in hosts exposed to high and low infection levels, and the putative role of acquired immunity, are discussed in relation to the data presented.

Keywords

Trichuris trichiuratransmission intensityantibody responseage-dependency
Type
Research Article
Information
Parasitology , Volume 105 , Issue 2 , October 1992 , pp. 273 - 283
Copyright
Copyright © Cambridge University Press 1992

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References

REFERENCES

Anderson, R. M. (1985). Mathematical models in the study of the epidemiology and control of ascariasis in man. In Ascariasis and its Public Health Significance, (ed. Crompton, D. W. T., Nesheim, M. C. & Pawlowski, Z. S.) pp. 39–67. London: Taylor & Francis.Google 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.Google Scholar
Anderson, R. M. (1987). Determinants of infection in human schistosomiasis. Baillières Clinical and Tropical Medicine and Communicable Diseases 2, 279–300.Google Scholar
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. & May, R. M. (1991). Infectious Diseases of Humans. Dynamics and Control. Oxford: Oxford University Press.CrossRefGoogle Scholar
Auriault, C., Grass-Masse, H., Pierce, R. J., Butterworth, A. E., Wolowczuk, I., Capron, M., Ouma, J. H., Balloul, J. M., Khalife, J., Neyrinck, J. L., Tartar, A., Koech, D. F. & Capron, A. (1990). Antibody response to Schistosoma mansoni-infected human subjects to the recombinant P28 Glutathione-S-Transferase and to synthetic peptides. Journal of Clinical Microbiology 28, 1918–24.CrossRefGoogle Scholar
Barger, I. A., Le Jambre, L. F., Georgi, J. R. & Davies, H. I. (1985). Regulation of Haemonchus contortus populations in sheep exposed to continuous infection. International Journal for Parasitology 15, 529–35.CrossRefGoogle ScholarPubMed
Befus, D. (1986). Immunity in intestinal helminth infections: present concepts, future direction. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 735–41.CrossRefGoogle Scholar
Berding, C., Keymer, A. E., Murray, J. D. & Slater, A. F. G. (1986). The population dynamics of acquired immunity to helminth infection. Journal of Theoretical Biology 122, 459–71.Google Scholar
Berding, C., Keymer, A. E., Murray, J. D. & Slater, A. F. G. (1987). The population dynamics of acquired immunity to helminth infection: experimental and natural transmission. Journal of Theoretical Biology 126, 167–82.Google Scholar
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248–54.CrossRefGoogle ScholarPubMed
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, 706–18.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. (1988). Population ecology of intestinal helminth infections in human communities. Philosophical Transactions of the Royal Society of London, B321, 405–20.Google ScholarPubMed
Bundy, D. A. P. & Cooper, E. S. (1989). Trichuris and trichuriasis in humans. Advances in Parasitology 28, 107–73.Google Scholar
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 infection in a St Lucian community. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 85–94.CrossRefGoogle Scholar
Bundy, D. A. P., Lillywhite, J. E., Didier, J. M., Simmons, I. & Bianco, A. E. (1991). Age-dependency of infection status and serum antibody levels in human whipworm (Trichuris trichiura) infection. Parasite Immunology 13, 629–38.Google Scholar
Bundy, D. A. P. & Steel, J. H. (1984). Parasitic zoonoses in the Caribbean region. International Journal of Zoonoses 11, 1–38.Google ScholarPubMed
Bundy, D. A. P., Thompson, D. E., Cooper, E. S. & Blanchard, J. (1985). Rate of expulsion of Trichuris trichiura with multiple and single dose regimens of Albendazole. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 641–4.CrossRefGoogle ScholarPubMed
Butterworth, A. E., Capron, M., Cordingley, J. S., Dalton, P. R., Dunne, D. W., Kariuki, H. C., Kimani, G., Koech, D., Mugambi, M., Ouma, J. H., Prentice, M. A., Richardson, B. A., Arap-Siongok, T. K., Sturrock, R. F. & Taylor, D. W. (1985). Immunity after treatment of human Schistosomiasis mansoni. II. Identification of resistant individuals and analysis of their immune response. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 393–408.CrossRefGoogle Scholar
Butterworth, A. E., Fulford, A. J. C., Dunne, D. W., Ouma, J. H. & Sturrock, R. F. (1988). Longitudinal studies on human schistosomiasis. Philosophical Transactions of the Royal Society of London, B321, 495–511.Google ScholarPubMed
Butterworth, A. E. & Hagan, P. (1987). Immunity in human Schistosomiasis. Parasitology Today 3, 11–15.Google Scholar
Chandiwana, S. K., Woolhouse, M. E. J. & Bradley, M. (1991). Factors affecting the intensity of reinfection with Schistosoma haematobium following treatment with praziquantel. Parasitology 102, 73–83.Google Scholar
Cooper, E. S. & Bundy, D. A. P. (1987). Trichuriasis. Baillières Clinical and Tropical Medicine and Communicable Diseases 2, 629–43.Google Scholar
Cooper, E. S., Spencer, J., Whyte-Alleng, C. A. M., Cromwell, O., Whitney, P., Venugopal, S., Bundy, D. A. P., Haynes, B. & MacDonald, T. T. (1991). Immediate hypersensitivity in colon of children with chronic Trichuris trichiura dysentery. The Lancet 388, 1104–7.Google Scholar
Crombie, J. A. & Anderson, R. M. (1985). Population dynamics of Schistosoma mansoni in mice repeatedly exposed to infection. Nature, London 315, 491–3.CrossRefGoogle ScholarPubMed
Elkins, D. B., Haswell-Elkins, M. & Anderson, R. M. (1986). The epidemiology and control of intestinal helminths in the Pulicat Lake region of Southern India. I. Study design and pre- and post-treatment observations on Ascaris lumbricoides infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 774–92.Google Scholar
Gray, B. M. (1979). Methodology for polysaccharide antigens: protein coupling of polysaccharides for absorption to plastic tubes. Journal of Immunological Methods 28, 187–9.CrossRefGoogle Scholar
Hagan, P. (1992). Reinfection, exposure and immunity in human schistosomiasis. Parasitology Today 8, 12–16.CrossRefGoogle ScholarPubMed
Hagan, P., Blumenthal, U. J., Dunn, D., Simpson, A. J. G. & Wilkins, H. A. (1991). Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature, London 349, 243–5.CrossRefGoogle ScholarPubMed
Hammarstrom, L. & Smith, C. I. (1986). IgG subclass changes in response to vaccination. Monographs in Allergy 19, 241–52.Google ScholarPubMed
Haswell-Elkins, M., Kennedy, M. W., Maizels, R. M., Elkins, D. B. & Anderson, R. M. (1989). The antibody recognition profile of naturally infected humans against Ascaris lumbricoides larval ES antigen. Parasite Immunology 11, 615–27.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 131, 491–507.CrossRefGoogle Scholar
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 caecum in children with the Trichuris dysentery syndrome. Journal of Clinical Pathology 44, 194–9.Google Scholar
Michael, E. & Bundy, D. A. P. (1992 a). Nutrition, immunity and helminth infection: effect of dietary protein on the dynamics of the primary antibody response to Trichuris muris (Nematoda) in CBA/Ca mice. Parasite Immunology (in the Press).Google Scholar
Michael, E. & Bundy, D. A. P. (1992 b). Protein content of CBA/Ca mouse diet: relationship with host antibody responses and the population dynamics of Trichuris muris (Nematoda) in repeated infection. Parasitology 105, 139–50.CrossRefGoogle ScholarPubMed
Nash, T. E., Lunde, M. N. & Cheever, A. W. (1981). Analysis and antigenic activity of a carbohydrate fraction derived from adult Schistosoma mansoni. Journal of Immunology 126, 805–10.Google Scholar
Pritchard, D. I., Quinnell, R. J., Slater, A. F. G., McKean, P. G., Dale, D. D. S., Raiko, A. & Keymer, A. E. (1990). Epidemiology and immunity of Necator americanus infection in a community in Papua New Guinea: humoral responses to excretory–secretory and cuticular collagen antigens. Parasitology 100, 317–26.Google Scholar
Roach, T. I. A., Else, K. J., Wakelin, D., McLaren, D. J., Grencis, R. K. (1991). Trichuris muris: antigen recognition and transfer of immunity in mice by IgA monoclonal antibodies. Parasite Immunology 13, 1–12.Google Scholar
Slater, A. F. G. & Keymer, A. E. (1986). Heligmosomoides polygyrus (Nematoda): the influence of dietary protein on the dynamics of repeated infection. Proceedings of the Royal Society London, B 229, 69–83.Google Scholar
Warren, K. S. (1973). Regulation of the prevalence and intensity of schistosomiasis in man; Immunology or ecology? Journal of Infectious Diseases 127, 595–609.Google Scholar
Wilkins, H. A., Goll, P. H., Marshall, T. F. & Moore, P. T. (1984). Dynamics of Schistosoma haematobium infection in a Gambian community. I. The pattern of human infection in the study area. Transactions of the Royal Society of Tropical Medicine and Hygiene 7, 216–21.Google Scholar
Wilkins, H. A., Blumenthal, U. J., Hagan, P., Hayes, R. J. & Tulloch, S. (1987). Resistance to reinfection after treatment of urinary schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 29–35.Google Scholar
Woolhouse, M. E. J., Taylor, P., Matanhire, D. & Chandiwana, S. K. (1991). Acquired immunity and epidemiology of Schistosoma haematobium. Nature, London 351, 757–9.CrossRefGoogle ScholarPubMed
Zar, J. H. (1984). Biostatistical Analysis, 2nd Edn.Prentice Hall, New Jersey.Google Scholar