Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-29T06:29:14.117Z Has data issue: false hasContentIssue false
  • English
  • Français

Multiple helminth infections in children: impact and control

Published online by Cambridge University Press:  08 June 2007

L. J. DRAKE  and
D. A. P. BUNDY
L. J. DRAKE
Affiliation:
Scientific Coordinating Centre for the Partnership for Child Development, Wellcome Trust Centre for the Epidemiology of Infectious Disease, University of Oxford, South Parks Road, Oxford OXI 3PS
D. A. P. BUNDY
Affiliation:
The Human Development Network, The World Bank, 1818 H Street, Washington DC 20433, USA
Get access Rights & Permissions [Opens in a new window]

Abstract

Parasitic worm infections are amongst the most widespread of all chronic human infections. It is estimated that there are more than 3 billion infections in the world today. In many low income countries it is often more common to be infected than not to be. Indeed, a child growing up in an endemic community can expect be infected soon after weaning, and to be infected and constantly reinfected for the rest of her or his life. Infection is most common amongst the poorest and most disadvantaged communities, and is typically most intense in children of school going age. As the risk of morbidity is directly related to intensity of infection, it follows that children are the most at risk from the morbid effects of disease. Multiparasite infections are also common in such communities and there is evidence that individuals harbouring such infections may suffer exacerbated morbidity, making children even more vulnerable. Thus, these infections pose a serious threat to the health and development of children in low income countries. For many years, the need to control these infections has lain uncontested, and with the advent of broad-spectrum anthelminthic drugs that are cheap, safe and simple to deliver, control has at last become a viable option for many communities. Furthermore, there is now increased emphasis being placed on a multispecies approach as a cost-effective mechanism to control the morbidity of virtually all the major helminthic infections of humans.

Keywords

helminthmultiple infectionsschool-age child
Type
Research Article
Information
Parasitology , Volume 122 , Supplement S1 , March 2001 , pp. S73 - S81
Copyright
© 2002 Cambridge University Press

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

AGARWAL, D. K., UPADHYAY, S. K., TRIPATHI, A. M. & AGARWAL, K. N. (1987). Nutritional status, physical work capacity and mental function in school children. Nutrition Foundation of India Scientific Report No. 6, New Delhi. Nutrition Foundation of India.Google Scholar
ANDERSON, R. M. & MEDLEY, G. F. (1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology 90, 629–660.CrossRefGoogle Scholar
ASHFORD, R. W., CRAIG, P. S. & OPPENHEIMER, S. J. (1992). Polyparasitism on the Kenya coast. 1. Prevalence, and association between parasitic infections. Annals of Tropical Medicine and Parasitology 86, 671–679.Google Scholar
BEASLEY, N. M. R., TOMPKINS, A. M. & HALL, A.. (1999). The impact of population level deworming on haemoglobin levels in Tanga, Tanzania. Tropical Medicine and International Health 4, 744–750.CrossRefGoogle Scholar
BEHNKE, J. M., PRITCHARD, D. I., WAKELIN, D., PARK, J. R., MCNICHOLAS, A. M. & GILBERT, F. S. (1994). Effect of ivermectin on infection with gastro-intestinal nematodes in Sierra Leone. Journal of Helminthology 68, 187–195.CrossRefGoogle Scholar
BERLINGEUR, G., DEL TRONO, L. & ORECCHIA, P. (1964). Eliminitasi intestinali, accrescimento scolastico (1964). Indagine sugli alumni della scuola D. Chiesa di Roma [Intestinal helminthiases, growth, and school achievement: A study among students of the D. Chiesa School in Rome]. Rivista di Parassitologia 25, 77–92.Google Scholar
BOIVIN, M. J., GIORDANI, B., NDANGA, K., MAKY, M. M., MANZEKI, K. M., NGUNU, N. & MUAMBA, K. (1993). Effects of treatment for intestinal parasites and malaria on cognitive abilities of school children in Zaire. Health Psychology 12, 220–226.CrossRefGoogle Scholar
BOOTH, M. & BUNDY, D. A. P. (1995). Estimating the numbers of multiple-species geohelminth infections in human communities. Parasitology 111, 645–653.CrossRefGoogle Scholar
BOOTH, M., BUNDY, D. A. P., ALBANICO, M., CHWAYA, H. M., ALAWI, K. S. & SAVIOLI, L. (1998). Associations among multiple geohelminth infections in schoolchildren from Pemba Island. Parasitology 116, 85–93.CrossRefGoogle Scholar
BOOTH, M., MAYOMBANA, C. & KILIMA, P. (1998). The population biology and epidemiology of schistosome infections among schoolchildren in Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 491–495.CrossRefGoogle 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, 826–828.CrossRefGoogle Scholar
BROOKER, S., BOOTH, M. & GUYATT, H. L. (1999). Comparison of schistosome and geohelminth infection prevalences in school-aged children from selected areas of Africa: implications for rapid assessment and combined control. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 125–126.CrossRefGoogle Scholar
BROOKER, S., MIGUEL, E. & MOULIN, S. (2000). Epidemiology of single and multiple species of helminth infections among schoolchildren in Busia District, Kenya. East African Medical Journal 77, 157–161.Google Scholar
BROOKER, S., PESHU, N., WARN, P. A., MOSOBO, M., GUYATT, H. L., MARSH, K. & SNOW, R. W. (1999). The epidemiology of hookworm infection and its contribution to anaemia among pre-school children on the Kenyan Coast. Transactions of the Royal Society of Tropical Medicine and Hygiene 93, 240–246.CrossRefGoogle Scholar
BUNDY, D. A. P. (1997). This wormy world – Then and now. Parasitology Today 13, 407–408.CrossRefGoogle Scholar
BUNDY, D. A. P., CHANDIWANA, S., HOMEIDA, M. M., YOON, S. & MOTT, K. E. (1991). The epidemiological implications of a multiple species approach to the control of human helminth infections. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 274–276.CrossRefGoogle Scholar
BUNDY, D. A. P. & COOPER, E. S. (1988). The evidence for predisposition to trichuriasis in humans: comparison of institutional and community studies. Annals of Tropical Medicine and Parasitology 82, 251–256.CrossRefGoogle Scholar
BUNDY, D. A. P. & COOPER, E. S. (1989). Trichuris and trichuriasis in humans. Advances in Parasitology 28, 107–173.CrossRefGoogle Scholar
BUNDY, D. A. P., COOPER, E. S., THOMPSON, D. E., DIDIER, J. M., ANDERSON, R. M. & SIMMONS, I. (1987). Predisposition to Trichuris trichiura infections in humans. Epidemiology and Infection 98, 65–71.CrossRefGoogle Scholar
CALLENDER, J. E., GRANTHAM-MCGREGOR, S. M., WALKER, S. P. & COOPER, E. S. (1994). Treatment effects in Trichuris dysentery syndrome. Acta Paediatrica 83, 1182–1187.CrossRefGoogle Scholar
CHAN, L., BUNDY, D. A. P. & KAN, S. P. (1994). Aggregation and predisposition to Ascaris lumbricoides and Trichuris trichiura at the familial level. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 46–8.CrossRefGoogle Scholar
CHAN, M. S., MEDLEY, G. F., JAMISON, D. & BUNDY, D. A. P. (1994). The evaluation of potential global morbidity due to intestinal nematode infections. Parasitology 109, 373–387.CrossRefGoogle Scholar
CHUN, F. (1971). Nutrition and education – a study. Journal of Singapore Pediatric Society 13, 91–96.Google Scholar
COOPER, E. S. & BUNDY, D. A. P. (1988). Trichuris is not trivial. Parasitology Today 4, 301–306.CrossRefGoogle Scholar
COOPER, E. S., DUFF, E. M. W., HOWELL, S. & BUNDY, D. A. P. (1995). ‘‘Catch up’’ growth velocities after treatment for Trichuris dysentery syndrome. Transactions of the Royal Society of Tropical Medicine and Hygiene 89, 653.CrossRefGoogle Scholar
CROMPTON, D. W. T. & TULLEY, J. J. (1987). How much ascariasis is there in Africa? Parasitology Today 3, 123–127.Google Scholar
CROMPTON, D. W. T. & WHITEHEAD, R. (1993). Hookworm infections and human iron metabolism. Parasitology 107, S137–S145.CrossRefGoogle Scholar
DE CARNERI, I., GAROFANO, M. & GRASSI., L. (1968). Il ruolo della tricocepalosi nel ritardo dello sviluppo frisco e mentale infantile in base ad un'inchiesta quantitative nel Basso Lodigiano [The role of trichuriasis in the physical and mental retardation of children based on a quantitative study in Basso Lodigiano]. Rivista de Parassitologia 28, 103–122.Google Scholar
DICKSON, R., AWSATHI, S. & WILLIAMSON, P. (2000). Effects of treatment for intestinal helminth infection on growth and cognitive performance in children: systematic review of randomised trials. British Medical Journal 320, 1697–1701.CrossRefGoogle Scholar
DRAKE, L. J., JUKES, M. & STERNBERG, R. (2000). Geohelminthiases (ascariasis, trichuriasis and hookworm): cognitive and developmental impact. Journal of Paediatric Infectious Disease (in press).Google Scholar
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, 774–792.Google Scholar
FORRESTER, J. E., SCOTT, M. E., BUNDY, D. A. P. & GOLDEN, M. H. (1988). Clustering of Ascaris lumbricoides and Trichuris trichuria infections within households. Transactions of the Royal Society of Tropical Medicine and Hygiene 82, 282–288.CrossRefGoogle Scholar
FORRESTER, J. E., SCOTT, M. E., BUNDY, D. A. P. & GOLDEN, M. H. (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, 272–276.CrossRefGoogle Scholar
FERNALD, L. C. & GRANTHAM-MCGREGOR, S. M. (1998). Stress response in school-age children who have been growth retarded since early childhood. American Journal of Clinical Nutrition 68, 691–698.CrossRefGoogle Scholar
FLORENCIO, C. (1988). Nutrition, Health and Other Determinants of Academic Achievement and School-related Behaviour of Grades One to Six Pupils. Quezan City, Philippines. University of the Philippines.Google Scholar
GRANTHAM-MCGREGOR, S. M. (1987). Field studies in early nutrition and later achievement. In Early Nutrition and Later Achievement (ed. Dobbing, J.), pp. 128–174. London: Academic Press.
GRANTHAM-MCGREGOR, S. M., POWELL, C. & FLETCHER, P. (1989). Stunting, severe malnutrition and mental development in young children. European Journal of Clinical Nutrition 43, 403–409.Google Scholar
GRANTHAM-MCGREGOR, S. M., WALKER, S. P. & CHANG, S. (2000). Nutritional deficiencies and later behavioural development. Proceedings of the Nutritional Society 59, 1–8.CrossRefGoogle Scholar
HAILU, M., JEMANEH, L. & KEBEDE, D. (1995). The use of questionnaires for the identification of communities at risk for intestinal schistosomiasis in western Gojam. Ethiopian Medical Journal 33, 103–113.Google Scholar
HASWELL-ELKINS, M. R., ELKINS, D. B. & ANDERSON, R. M. (1987). Evidence for predisposition in humans to infections with Ascaris, hookworm, Enterobius and Trichuris in a South Indian fishing community. Parasitology 95, 323–327.CrossRefGoogle Scholar
HOLLAND, C. V., ASAOLU, S. O., CROMPTON, D. W. T., STODDART, R. C., MACDONALD, R. & TORIMIRO, S. E. (1989). The epidemiology of Ascaris lumbricoides and other soil-transmitted helminths in primary school children from Ile-Ife, Nigeria. Parasitology 99, 275–285.CrossRefGoogle Scholar
HOWARD, S. C., DONNELLY, C. & CHAN, M. S. (2000). Methods for estimation of associations between multiple species parasite infections. Parasitology (in press).Google Scholar
IDJRADINATA, P. & POLLITT, E. (1993). Reversal of developmental delays among iron deficient anemic infants treated with iron. Lancet 341, 1–4.Google Scholar
JAMISON, D. (1986). Child malnutrition and school performance in China. Journal of Development Economics 20, 299–309.CrossRefGoogle Scholar
JOHNSTON, F., LOW, S. & DE BAESSA, Y. (1987). Interaction of nutrition and socio-economic status as determinants of cognitive development in disadvantaged urban Guatemalan children. American Journal of Physical Anthropology 73, 501–506.CrossRefGoogle Scholar
KVALSVIG, J. D., COOPPAN, R. M. & CONNOLLY, K. J. (1991). The effects of parasite infections on cognitive processes in children. Annals of Tropical Medicine and Parasitology 85, 551–568.CrossRefGoogle Scholar
LENGELER, C., SALA-DIAKANDA, D. & TANNER, M. (1992). Using questionnaires through an existing administrative system: a new approach to health interview surveys. International Journal of Epidemiology 20, 796–807.CrossRefGoogle Scholar
LEVAV, M, MIRSKY, A. F., SCHANTZ, P. M., CASTRO, S & CRUZ, M. E. (1995). Parasitic infection in malnourished school children. Parasitology 110, 103–111.CrossRefGoogle Scholar
LOZOFF, B. (1998). Exploratory mechanisms for poorer development in iron-deficient anemic infants. In Nutrition, Health and Child Development: Research Advances and Child Development (ed. GRANTHAM-MCGREGOR, S. M.), pp. 162–178. Washington, DC: PAHO.
LOZOFF, B., BRITTENHAM, G. M. & WOLF, A. W. (1987). Iron deficiency anemia and iron therapy effects on infant developmental test performance. Paediatrics 79, 981–995.Google Scholar
LOZOFF, B., JIMENEZ, E. & WOLF, A. W. (1991). Long-term developmental outcome of infants with iron deficiency. New England Journal of Medicine 325, 687–694.CrossRefGoogle Scholar
LOZOFF, B., KLEIN, N. K., NELSON, E. C., MCCLISH, D. K., MANUEL, M. & CHACON, M. E.. (1998). Behaviour of infants with iron deficiency anaemia. Child Development 1, 24–36.CrossRefGoogle Scholar
MARQUET, S., ABEL, L., HILLAIRE, D., DESSEIN, H., KALIL, J., FEINGOLD, J., WEISSENBACH, J & DESSEIN, A. J. (1996). Genetic localisation of a locus controlling the intensity of infection by Schistosoma mansoni on chromosome 5q31-q33. Nature Genetics 14, 181–184.CrossRefGoogle Scholar
MOOCK, P. & LESLIE, J. (1986). Childhood malnutrition and schooling in the Terai region of Nepal. Journal of Development Economics 20, 33–52.CrossRefGoogle Scholar
NEEDHAM, C. S., KIM, H. & CONG, L. (1998). Epidemiology of soil-transmitted nematodes in Ha Nam province, Viet Nam. Tropical Medicine and International Health 3, 904–912.CrossRefGoogle Scholar
NOKES, C. & BUNDY, D. A. P. (1994). Does helminth infection affect mental processing and educational achievement? Parasitology Today 10, 14–18.Google Scholar
NOKES, C., COOPER, E. S., ROBINSON, B. A. & BUNDY, D. A. P. (1991). Geohelminth infection and academic assessment in Jamaican children. Transactions of the Royal Society of Tropical Medicine and Hygiene 85, 272–273.CrossRefGoogle Scholar
NOKES, C., GRANTHAM-MCGREGOR, S. M., SAWYER, A. W., COOPER, E. S., ROBINSON, B. A. & BUNDY, D. A. P. (1992). Moderate to high infections of Trichuris trichiura and cognitive function in Jamaican school children. Parasitology 104, 539–547.CrossRefGoogle Scholar
OLSEN, A., MAGNUSSEN, P., OUMA, J. H., ANDREASSEN, J. & FRIIS, H. (1998). The contribution of hookworm and other parasitic infections to haemoglobin and iron status among children and adults in Western Kenya. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 643–649.CrossRefGoogle Scholar
PARTNERSHIP FOR CHILD DEVELOPMENT (1997). Better health, nutrition and education for the school-age child. Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 1–2.Google Scholar
PARTNERSHIP FOR CHILD DEVELOPMENT (1998). The health and nutritional status of schoolchildren in Africa: evidence from school-based programmes in Ghana and Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 254–261.Google Scholar
PETNEY, T. N. & ANDREWS, R. H. (1998). Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. International Journal for Parasitology 28, 377–393.CrossRefGoogle Scholar
POLLITT, E., GORMAN, K. S., ENGLE, P. L., MARTORELL, R. & RIVERA, J. (1993). Early supplementary feeding and cognition: effects over two decades. Monographs of the Society for Child Development 58, 1–99.CrossRefGoogle Scholar
POLLITT, E., HATHIRAT, P. & KOTCHABHAKDI, N. (1989). Iron deficiency and educational achievement in Thailand. American Journal of Clinical Nutrition 50 (supplement 3), 687–697.CrossRefGoogle Scholar
POLLITT, E., PEREZ-ESCAMILLA, R. & WAYNE, W. (1991). Effects of infection with Trichuris trichiura, Ascaris lumbricoides and hookworm on information processing among Kenyan school children. FASEB Journal 5, A1081.Google Scholar
POWELL, C. & GRANTHAM-MCGREGOR, S. M. (1980). The associations between nutritional status, school achievement and school attendance in twelve-year-old children at a Jamaican school. West Indian Medical Journal 29, 247–253.Google Scholar
POWELL, C. & GRANTHAM-MCGREGOR, S. M. (1985). The ecology of nutritional status and development in young children in Kingston, Jamaica. American Journal of Clinical Nutrition 41, 1322–1331.CrossRefGoogle Scholar
ROBERTSON, L. J. (1992). Haemoglobin concentrations and concomitant infections with hookworm and Trichuris trichiura in Panamanian primary schoolchildren. Transactions of the Royal Society for Tropical Medicine and Hygiene 86, 654–656.CrossRefGoogle Scholar
ROCHE, M. & LAYRISSE, M. (1966). The nature and cause of hookworm anaemia. American Journal of Tropical Medicine and Hygiene 15, 1029–1102.Google Scholar
SAKTI, H., NOKES, C., HERTANTO, W. S., HENDRATNO, S., HALL, A., BUNDY, D. A. P. & SATOTO. (1999). Evidence for an association between hookworm infection and cognitive function in Indonesian school children. Tropical Medicine and International Health. 4, 322–334.CrossRefGoogle Scholar
SAVIOLI, L., BUNDY, D. & TOMKINS, A. (1992). Intestinal parasitic infections: a soluble public health problem. Transactions of the Royal Society of Tropical Medicine and Hygiene 86, 353–354.CrossRefGoogle Scholar
SCHAD, G. A. & ANDERSON, R. M. (1985). Predisposition to hookworm infection in humans. Science 228, 1537–1540.CrossRefGoogle Scholar
SESHADRI, S. & GOPALDAS, T. (1989). Impact of iron supplementation on cognitive function in pre-school and school-age children: the Indian experience. American Journal of Clinical Nutrition 50, 675–686.CrossRefGoogle Scholar
SIMEON, D. T., CALLENDER, J. & WONG, M. S. (1994). School performance, nutritional status and trichuriasis in Jamaican schoolchildren. Acta Paediatrica 83, 1188–1193.CrossRefGoogle Scholar
SIMEON, D. T. & GRANTHAM-MCGREGOR, S. M. (1990). Nutritional deficiency and children's behaviour and mental development. Nutritional Research Review 3, 1–24.CrossRefGoogle Scholar
SIMEON, D. T., GRANTHAM-MCGREGOR, S. M. & WONG, M. S. (1995). Trichuris trichiura infection and cognition in children: results of a randomised clinical trial. Parasitology 110, 457–464.CrossRefGoogle Scholar
SOEMANTRI, A. G. (1989). Preliminary findings on iron supplementation and learning achievement of rural Indonesian children. American Journal of Clinical Nutrition 50, 698–702.CrossRefGoogle Scholar
SOEWONDO, S., HUSAINI, M. & POLLITT, E. (1989). Effects of iron deficiency on attention and learning processes in preschool children: Bandung, Indonesia. American Journal of Clinical Nutrition 50, 667–674.CrossRefGoogle Scholar
STEPHENSON, L. S. (1987). Impact of Helminth Infections on Human Nutrition: Schistosomes and Soil Transmitted Helminths. London: Taylor & Francis.Google Scholar
STEPHENSON, L. S., LATHAM, M., ADAMS, E. J., KINOTI, S. N. & PERTET, A. (1993). Physical fitness, growth and appetite of Kenyan schoolboys with hookworm, Trichuris trichiura and Ascaris lumbricoides infections are improved four months after a single dose of albendazole. Journal of Nutrition 123, 1036–1046.Google Scholar
STERNBERG, R. J., POWELL, C. & MCGRANE, P. (1997). Effects of a parasitic infection on cognitive functioning. Journal of Experimental Psychology 3, 67–76.CrossRefGoogle Scholar
STOLTZFUS, R. J., ALBONICO, M., CHWAYA, H. M., TIELSCH, J. M., SCHULZE, K. J. & SAVIOLI, L. (1997). Epidemiology of iron deficiency anaemia in Zanzibari schoolchildren: the importance of hookworms. American Journal of Clinical Nutrition 65, 153–159.CrossRefGoogle Scholar
STOLTZFUS, R. J., ALBONICO, M., CHWAYA, H. M., TIELSCH, J. M., SCHULZE, K. J. & SAVIOLI, L. (1998). The effects of the Zanzibar school-based deworming programme on iron status of children. American Journal of Clinical Nutrition 68, 179–186.CrossRefGoogle Scholar
TATALA, S., SVANBERG, U. & MDUMA, B. (1998). Low dietary iron is a major cause of anaemia: a nutrition survey in the Lindi District of Tanzania. American Journal of Clinical Nutrition 68, 171–178.CrossRefGoogle Scholar
THEIN-HLAING (1993). Ascariasis and childhood nutrition. Parasitology 107, S125–S136.Google Scholar
WAITE, J. H. & NELSON, I. L. (1919). Study of the effects of hookworm infection upon the mental development of North Queensland schoolchildren. Medical Journal of Australia 1, 1–8.Google Scholar
WATKINS, W. E., CRUZ, J. R. & POLLITT, E. (1996a). The effects of deworming on indicators of school performance in Guatemala. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 156–162.Google Scholar
WATKINS, W. E., CRUZ, J. R. & POLLITT, E. (1999b). Whether deworming improves or impairs information processing depends on intensity of Ascaris infection. Yale-China Association, Shatin, New Territories, Hong Kong.Google Scholar
WARREN, K. S., BUNDY, D. A. P. & ANDERSON, R. M. (1993). Helminth Infection. In Disease Control Priorities in Developing Countries. (ed. Jamison, D. T.), pp. 131–16. Oxford: Oxford University Press.
WHO (1993). The control of schistosomiasis. Second report of the WHO Expert Committee. Technical Report Series 830, Geneva: WHO.Google Scholar
WORLD BANK (1993). World Development Report: Investing in Health. Oxford: Oxford University Press.Google Scholar