Skip to main content
×
Home
    • Aa
    • Aa

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

  • D. A. P. Bundy (a1) and G. F. Medley (a1)
Summary
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.

Copyright
References
Hide All
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.
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.
Anderson R. M. & May R. M. (1985 a). Helminth infections of humans: mathematical models, population dynamics and control. Advances in Parasitology 24, 1101.
Anderson R. M. & May R. M. (1985b). Herd immunity to helminth infections: implications for parasite control. Nature, London 315, 493–6.
Anderson R. M. & MAY R. M. (1991). Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press.
Anderson R. M. & Medley G. F. (1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology 90, 629–60.
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.
Bailey N. T. J. (1964). The Elements of Stochastic Procedures. London: John Wiley & Sons.
Beaver P. C. (1975). Biology of soil-transmitted helminths: the massive infection. Health Laboratory Science 2, 116–25.
Behnke J. M. (1987). Do hookworms elicit protective immunity in man? Parasitology Today 3, 200–6.
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.
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, 397408.
Beisel W. R. (1982). Single nutrients and immunity. American Journal of Clinical Nutrition 35, 417–68.
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.
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.
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.
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.
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.
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).
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.
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.
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.
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.
Bundy O. A. P. & Cooper B.. (1988 a). Human Trichuris and trichuriasis. Advances in Parasitology 28, 107–73.
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.
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.
Bundy D. A. P. & Golden M. H. N. (1987). The impact of host nutrition on gastro-intestinal helminth populations. Parasitology 95, 623–35.
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.
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.
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, 8594.
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, 6571.
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.
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.
Chan L. L. (1991). The Epidemiology of Intestinal Nematode Infection in Urban Malaysia. Ph.D. thesis, Faculty of Science, University of London.
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).
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.
Crombie J. A. & Anderson R. M. (1985). Population dynamics of Schistosoma mansoni in mice repeatedly exposed to infection. Nature, London 315, 491–3.
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.
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.
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.
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.
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.
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.
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).
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.
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.
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.
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.
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.
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.
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.
Hsieh H. C. (1970). Studies on endemic hookworm. I. Survey and longitudinal observation in Taiwan. Japanese Journal of Parasitology 19, 508–22.
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.
Kennedy M. W. (1989). Genetic control of the immune repertoire in nematode infections. Parasitology Today 5, 316–24.
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, 2030.
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. 177210. London: Taylor and Francis.
Keymer A. E. & Slater A. F. G. (1987). Helminth fecundity: density dependence or statistical illusion? Parasitology Today 3, 56–8.
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, 491507.
McCallum H. I. (1990). Covariance in parasite burdens: the effect of predisposition to infection. Parasitology 100, 153–9.
Maizels R. M. & Lawrence R. A. (1991). Immunological tolerance: the key feature in human filariasis. Parasitology Today 7, 271–6.
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.
Nakada K., Kohakura M., Komoda H. & Hinuma Y. (1984). High incidence of HTLV antibody in carriers of Strongyloides stercoralis. Lancet i, 633.
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, 6671.
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.
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, 191201.
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.
Schad G. A. & Anderson R. M. (1985). Predisposition to hookworm infection in humans. Science 228, 1537–40.
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. 187223. New York: Academic Press.
Schweitzer N. & Anderson R. M. (1991). Helminths, immunology and equations. Immunology Today 12, A76A81.
Stephenson L. S. (1987). The Impact of Helminth Infections on Human Nutrition. London: Taylor and Francis.
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. 140155. Vienna: Hans Huber Publishers.
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.
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.
Wakelin D. M. & Blackwell J. M. (1988). Genetics of Resistance to Bacterial and Parasitic Infection. London: Taylor and Francis.
Warren K.. (1973). Regulation of the prevalence and intensity of schistosomiasis in man: immunology or ecology? Journal of Infectious Diseases 127, 595609.
Wassom D. L., Krco C. J. & David C. S. (1987). I-E expression and susceptibility to parasite infection. Immunology Today 8, 3943.
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.
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.
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.
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, 8991.
Woolhouse M. E. J., Taylor P., Matanhire D. & Chandiwana S. K. (1991). Acquired immunity and epidemiology of Schistosoma haematobium. Nature, London 351, 757–9.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 13 *
Loading metrics...

Abstract views

Total abstract views: 177 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th October 2017. This data will be updated every 24 hours.