Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-28T13:05:47.818Z Has data issue: false hasContentIssue false
  • English
  • Français

Immuno-epidemiology of human geohelminthiasis: ecological and immunological determinants of worm burden

Published online by Cambridge University Press:  06 April 2009

D. A. P. Bundy  and
G. F. Medley
D. A. P. Bundy
Affiliation:
Welcome Trust Research Centre for Parasitic Infections, Imperial College, Prince Consort Road, London
G. F. Medley
Affiliation:
Welcome Trust Research Centre for Parasitic Infections, Imperial College, Prince Consort Road, London
Get access Rights & Permissions [Opens in a new window]

Summary

The morbidity and transmission dynamics of geohelminthiases are determined by the patterns of infection intensity in the community. Understanding the determinants of these patterns requires a combination of field, laboratory and theoretical study. Studies of age-specific reinfection, and of the phenomenon of predisposition, indicate that the major determinant of convex age-intensity profiles and of heterogeneity in infection intensity is the rate of establishment of infection, rather than the rate of adult worm mortality. The rate of establishment is, in turn, determined by exposure to, and protection from, infection. The evidence indicates that exposure, at least to the orally-transmitted geohelminths, varies with age and is highly heterogeneous between hosts. The immune response in geohelminthiasis is vigorous, parasite-specific, hetero geneous between hosts, and both age and infection dose dependent, but has yet to be convincingly shown to be protective. Since the immune response is itself a function of exposure, unravelling the interaction between ecology and immunology as determinants of geohelminth worm burden will require simultaneous assessment of both processes via immuno epidemiological study.

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. S105 - S119
Copyright
Copyright © Cambridge University Press 1992

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

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. & Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–98.Google Scholar
Anderson, R. M. & May, R. M. (1985 a). Helminth infections of humans: mathematical models, population dynamics and control. Advances in Parasitology 24, 1–101.Google Scholar
Anderson, R. M. & May, R. M. (1985b). Herd immunity to helminth infections: 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
Anderson, R. M. & Medley, G. F. (1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology 90, 629–60.Google Scholar
Anderson, R. M. & Schad, G. A. (1986). 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 Scholar
Bailey, N. T. J. (1964). The Elements of Stochastic Procedures. London: John Wiley & Sons.Google Scholar
Beaver, P. C. (1975). Biology of soil-transmitted helminths: the massive infection. Health Laboratory Science 2, 116–25.Google Scholar
Behnke, J. M. (1987). Do hookworms elicit protective immunity in man? Parasitology Today 3, 200–6.Google Scholar
Behnke, J. M., Ali, N. M. H. & Jenkins, S. N. (1984). Survival to patency of low-level infections with Trichuris muris in mice concurrently infected with Nematospiroides dubius. Annals of Tropical Medicine and Parasitology 78, 509–17.Google Scholar
Behnke, J. M., Hannah, J. & Pritchard, D. I. (1983). Nematospiroides dubius in the mouse: evidence that adult worms depress the expression of homologous immunity. Parasite Immunology 5, 397–408.CrossRefGoogle ScholarPubMed
Beisel, W. R. (1982). Single nutrients and immunity. American Journal of Clinical Nutrition 35, 417–68.Google 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.CrossRefGoogle ScholarPubMed
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
Bradley, D. J. & McCullough, F. S. (1974). Egg output stability and epidemiology of Schistosoma haematobium. II. An analysis of the epidemiology of endemic S. haematobium. Transactions of the Royal Society of Tropical Medicine and hygiene 80, 706–18.Google Scholar
Bradley, M. (1990). Rate of expulsion of Necator americanus and the false hookworm Ternidens derminutus Railliet and Henry 1909 (Nematoda) from humans following albendazole treatment. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 720.Google Scholar
Bradley, M. & Chandiwana, S. K. (1990). Age-dependency in predisposition to hookworm infection in the Burma valley area of Zimbabwe. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 826–8.Google Scholar
Bradley, M., Chandiwana, S. K., Medley, G. F. & Bundy, D. A. P. (1992). The epidemiology and population biology of Necator americanus in a rural community in Zimbabwe. Transactions of the Royal Society of Tropical Medicine and Hygiene (in the Press).CrossRefGoogle 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, 706–18.Google Scholar
Bundy, D. A. P. (1988). Population ecology of intestinal helminth infections in human communities. Philosophical Transactions of the Royal Society of London, B 321, 405–20.Google 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
Bundy, D. A. P. & Blumenthal, U. (1990). Human behaviour and epidemiology of helminth infection. In Parasitism and Host Behaviour (ed. Barnard, C. & Behnke, J. M.), pp. 264–89. London: Taylor and Francis.Google Scholar
Bundy, O. A. P. & Cooper, B.. (1988 a). Human Trichuris and trichuriasis. Advances in Parasitology 28, 107–73.CrossRefGoogle Scholar
Bundy, D. A. P. & Cooper, E. S. (1988 b). The evidence for predisposition to trichuriasis in humans: comparison of institutional and community studies. Annals of Tropical Medicine and Parasitology 82, 251–6.Google Scholar
Bundy, D. A. P., Cooper, E. S., Thompson, D. E., Didier, J. M. & Simmons, I. (1988). Effect of age and initial infection status on the rate of reinfection with Trichuris trichiura after treatment. Parasitology 97, 469–76.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. & Golden, M. H. N. (1987). The impact of host nutrition on gastro-intestinal helminth populations. Parasitology 95, 623–35.Google 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.CrossRefGoogle ScholarPubMed
Bundy, D. A. P., Thompson, D. E., Golden, M. H. N., Cooper, E. S., Anderson, R. M. & Harland, P. S. E. (1985). Population distribution of Trichuris trichiura in a community of Jamaican children. Transactions of the Royal Society of Tropical Medicine and Hygiene 79, 232–7.CrossRefGoogle Scholar
Bundy, D. A. P., Cooper, E. S., Thompson, D. E., Anderson, R. M. & Didier, J. M. (1987 a). Age-related prevalence and intensity of Trichuris trichiura infection in a St. Lucian community. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 85–94.CrossRefGoogle Scholar
Bundy, D. A. P., Cooper, E. S., Thompson, D. B., Didier, J. M., Anderson, R. M. & Simmons, L. (1987 b). Predisposition to Trichuris trichiura infections in humans. Epidemiology and Infection 98, 65–71.Google Scholar
Bundy, D. A. P., Wong, M. S., Lewis, L. & Horton, J. (1990). Control of gastrointestinal helminths by agetargeted chemotherapy delivered through schools. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 115–20.CrossRefGoogle Scholar
Cabrera, B. D. (1981). Reinfection and infection rate studies of soil-transmitted helminthiasis in Juban, Sorsogon. In Collected Papers on the Control of Soil-Transmitted Helminthiases, vol. 1, pp. 181–91. Tokyo, Japan: Asian Parasitic Control Organisation.Google Scholar
Chan, L. L. (1991). The Epidemiology of Intestinal Nematode Infection in Urban Malaysia. Ph.D. thesis, Faculty of Science, University of London.Google Scholar
Chan, L. L., Kan, S. P. & Bundy, D. A. P. (1992). The effect of repeated chemotherapy on age-related predisposition to Ascaris lumbricoides and Trichuris trichiura. Parasitology (in the Press).Google Scholar
Cooper, E. S. & Bundy, D. A. P. (1988). Trichuriaisis. In Intestinal Helminthic Infections (ed. Pawlowski, Z. S.), Baillière's Clinical Tropical Medicine and Communicable Disease vol. 2, pp. 629–43. London: Baillière Tindall.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.Google Scholar
Elkins, O. 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
Else, K. & Wakelin, D. (1988). The effects of H-2 and non-H-2 genes on the expulsion of the nematode Trichuris muris from inbred congenic mice. Parasitology 96, 543–50.Google Scholar
Forrester, J. E., Scott, M. E., Bundy, D. A. P. & Golden, M. H. N. (1988). Clustering of Ascaris lumbricoides and Trichuris trichiura infections within households. Transactions of Royal Society of Tropical Medicine and Hygiene 82, 282–8.Google Scholar
Forrester, J. E., Scott, M. E., Bundy, D. A. P. & Golden, M. H. N. (1990). Predisposition of individuals and families in Mexico to heavy infection with Ascaris lumbricoides and Trichuris trichiura. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 272–6.Google Scholar
Compels, M. M., Todd, J., Peters, B. S., Main, J. & Pinching, A. J. (1991). Disseminated strongyloides in AIDS: uncommon but important. AIDS 5, 329–32.Google Scholar
Greenwood, M. & Yule, G. U. (1920). An enquiry into the nature of frequency distributions representative of multiple happenings with particular reference to the occurrence of multiple attacks of disease or of repeated accidents. Journal of the Royal Statistical Society 83, 255–79.CrossRefGoogle Scholar
Guyatt, H. L. & Bundy, D. A. P. (1991). Estimating prevalence of community morbidity due to intestinal helminths: prevalence of infection as an indicator of the prevalence of disease. Transactions of the Royal Society of Tropical Medicine and Hygiene (in the Press).Google Scholar
Guyatt, H. L., Bundy, D. A. P., Medley, G. F. & Grenfell, B. T. (1990). The relationship between the frequency distribution of Ascaris lumbricoides and the prevalence and intensity of infection in human communities. Parasitology 101, 139–43.Google Scholar
Hagen, P., Blumenthal, U. J., Dunn, D., Simpson, A. J. G. & Wilkins, A. (1991). Human IgE, IgG4 and resistance to reinfection with Schistosoma haematobium. Nature, London 349, 243–5.Google Scholar
Haswell-Elkins, M. R., Elkins, D. B. & Anderson, R. M. (1987). Evidence for predisposition in humans to infection with Ascaris, hookworm, Enterobius and Trichuris in a South Indian fishing community. Parasitology 95, 323–37.Google Scholar
Haswell-Elkins, M. R., Kennedy, M. W., Maizels, R. M., Elkins, D. B. & Anderson, R. M. (1989). The antibody recognition profiles of humans naturally infected with Ascaris lumbricoides. Parasite Immunology 11, 615–27.Google Scholar
Hirayama, K., Matsushita, S., Kikuchi, I., Iuchi, M., Ohta, N. & Sasazuki, T. (1987). HLA-DQ is epistatic to HLA-DR in controlling the immune response to Schistosoma antigen in humans. Nature, London 327, 426–30.Google Scholar
Holland, C. V., Asaolu, S. O., Crompton, D. W. T., Stoddart, R. C., MacDonald, R. & Torimiro, S. E. A. (1989). The epidemiology of Ascaris lumbricoides and other soil-transmitted helminths in primary school children from Ile-Ife, Nigeria. Parasitology 99, 275–85.Google Scholar
Hominick, W. M., Dean, C. G. & Schad, G. A. (1987). Population biology of hookworms in West Bengal: analysis of numbers of infective larvae recovered from damp pads applied to the soil surface at defaecation sites. Transactions of the Royal Society for Tropical Medicine and Hygiene 81, 978–86.Google Scholar
Hsieh, H. C. (1970). Studies on endemic hookworm. I. Survey and longitudinal observation in Taiwan. Japanese Journal of Parasitology 19, 508–22.Google Scholar
Hussain, R. & Ottesen, E. A. (1986). IgE responses in human filariasis. IV. Parallel antigen recognition by IgG and IgG4 subclass antibodies. Journal of Immunology 136, 1859.Google Scholar
Kennedy, M. W. (1989). Genetic control of the immune repertoire in nematode infections. Parasitology Today 5, 316–24.CrossRefGoogle ScholarPubMed
Kennedy, M. W., Qureshi, F., Haswell-Elkins, M. & Elkins, D. B. (1987). Homology and heterology between the secreted antigens of the parasitic larval stages of Ascaris lumbricoides and Ascaris suum. Clinical and Experimental Immunology 67, 20–30.Google Scholar
Keymer, A. & Pagel, M. (1990). Predisposition to hookworm infection. In Hookworm Infection: Current Status and New Directions (ed. Schad, C. A. & Warren, K. S.) pp. 177–210. London: Taylor and Francis.Google Scholar
Keymer, A. E. & Slater, A. F. G. (1987). Helminth fecundity: density dependence or statistical illusion? Parasitology Today 3, 56–8.Google Scholar
Lillywhite, J. E., Bundy, D. A. P., Didier, J. M., Cooper, E. S. & Bianco, A. E. (1991). Humoral responses Mw human infection with the whipworm Trichuris trichiura. Parasite Immunology 13, 491–507.Google Scholar
McCallum, H. I. (1990). Covariance in parasite burdens: the effect of predisposition to infection. Parasitology 100, 153–9.Google Scholar
Maizels, R. M. & Lawrence, R. A. (1991). Immunological tolerance: the key feature in human filariasis. Parasitology Today 7, 271–6.Google Scholar
Michael, E. & Bundy, D. A. P. (1988). 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.Google Scholar
Nakada, K., Kohakura, M., Komoda, H. & Hinuma, Y. (1984). High incidence of HTLV antibody in carriers of Strongyloides stercoralis. Lancet i, 633.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.Google Scholar
Pritchard, D. I., Quinnell, R. J., Slater, A. F. G., McKean, P. C., DALE, D. D. S., Raiko, A. & Keymer, A. E. (1990). Epidemiology and immunology 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
Quinnell, R. J., Medley, G. F. & Keymer, A. E. (1990). The regulation of gastrointestinal helminth populations. Philosophical Transactions of the Royal Society of London, B, 330, 191–201.Google Scholar
Sasazuki, T., Ohta, N., Kaneoka, R. & Kojima, s. (1980). Association between an HLA haplotype and low responsiveness to schistosomal worm antigen in man. Journal of Experimental Medicine 152, 314–18.Google Scholar
Schad, G. A. & Anderson, R. M. (1985). Predisposition to hookworm infection in humans. Science 228, 1537–40.Google Scholar
Schad, G. A., Nawalinski, T. A. & Kochar, V. K. (1983). Human ecology and distribution and abundance of hookworm populations. In Human Ecology and Infectious Disease (ed. Croll, N. A. & Cross, J.), pp. 187–223. New York: Academic Press.Google Scholar
Schweitzer, N. & Anderson, R. M. (1991). Helminths, immunology and equations. Immunology Today 12, A76–A81.CrossRefGoogle ScholarPubMed
Stephenson, L. S. (1987). The Impact of Helminth Infections on Human Nutrition. London: Taylor and Francis.Google Scholar
Suskind, R. M. (1980). Malnutrition and the immune response. In The Impact of Malnutrition on Immune Defence in Parasitic Infection, (ed. Isliker, H. & Schurch, B.) pp. 140–155. Vienna: Hans Huber Publishers.Google Scholar
Thein-Hlaing, , Than-Saw, & Myat-Lay-Kyin, (1991). The impact of three-monthly age-targetted chemotherapy on Ascaris lumbricoides infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 519–22.CrossRefGoogle ScholarPubMed
Thein-Hliang, , Than-Saw, & Myint-Lwin, . (1987). Reinfection of people with Ascaris lumbricoides following single, 6-month and 12-month interval mass chemotherapy in Okpo village, rural Burma. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 140–6.Google Scholar
Wakelin, D. M. & Blackwell, J. M. (1988). Genetics of Resistance to Bacterial and Parasitic Infection. London: Taylor and Francis.Google Scholar
Warren, K.. (1973). Regulation of the prevalence and intensity of schistosomiasis in man: immunology or ecology? Journal of Infectious Diseases 127, 595–609.Google Scholar
Wassom, D. L., Krco, C. J. & David, C. S. (1987). I-E expression and susceptibility to parasite infection. Immunology Today 8, 39–43.Google Scholar
Wassom, D. L., Wakelin, D., Brooks, B. O., Krco, C. J. & David, C. S. (1984). Genetic control of immunity to Trichinella spiralis infections of mice. Hypothesis to explain the role of H-2 genes in primary and challenge infections. Immunology 51, 625–31.Google ScholarPubMed
Wong, M. S. & Bundy, D. A. P.(1990). Quantitative assessment of contamination of soil by the eggs of Ascaris lumbricoides and Trichuris trichiura. Transactions of the Royal Society of Tropical Medicine and Hygiene 84, 567–70.Google Scholar
Wong, M. S., Bundy, D. A. P. & Golden, M. H. N. (1988). Quantitative assessment of geophagous behaviour as a potential source of exposure to geohelminth infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 621–5.Google Scholar
Wong, M. S., Bundy, D. A. P. & Golden, M. H. N. (1991). The rate of ingestion of Ascaris lumbricoides and Trichuris trichiura eggs in soil and its relationship to infection in two children's homes in Jamaica. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 89–91.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.Google Scholar