Leading Article Intestinal
public health problem
Lorenzo Savioli’, Don Bundy’ and Andrew Ton&ins3
’ Programme on Intestinal Parasitic Infections, Division of Communicable Diseases, World Health Organization, 1211 Geneva 27, Switzerland; ‘WHO Collaborating Centre on the Epidemiolop of Intestinal Parasites, Department of Biology, Imperial College of Science, Technology and Medicine, London, UK; Centre for International Child Health, Institute of Child Health, University of London, UK Intestinal parasitic helminth and protozoa1 infections are among the most common infections of humans worldwide. They occur throughout the developing world and are most common in the poorest communities. This ubiquity has led to a tendency to view the infections as a fact of life, or as a problem which is too large to be tackled by public health services. The public health impact of intestinal helminthic infections has been consistently and considerably underestimated. The mortality rate directly related to Ascaris lumbricoides is low; eien so, the absolute number of deaths is fairly high becauseof the high prevalence of infection in develooine countries (WHO. 1987). If the mortality rate werk oily 2 per 100‘000 people iniected, it would constitute thousands of deaths when multiplied by the hundreds of millions of people who are infected. In Cape Town, South Africa, surgical ascariasisconstituted about lO-15% of all acute abdominal emergencies (Louw, 1974). Iron deficiencv anaemia, ranging from mild to lifethreatening, is aninevitableresufi oFhookworm infection (WHO. 1990). It is oossible. and obviouslv desirable. to ;educe’hook&orm loads in ;he population through chemotherapy, thus keeping the prevalence and severity of hookworm-induced iron deficiency anaemia under control and significantly reducing morbidity and mortality (PAwLOWSKI et al., 1991). Trichuris trichiura, associated with undernutrition, growth stunting and iron deficiency anaemia in intense infections (COOPERet al., 1990), has more recently been found to have an adverse effect on cognitive function even when infections are only moderately intense (NOAKES et al., 1992). Furthermore, not only the major signs of infection but also the adverse effect of T. trichiura on school performance may be reversed by chemotherapy. The adverse effect of infection on cognition suggests that helminths may have even greater developmental consequences than- was previously thought, since the most intense infections with T. trichiura and A. lumbricoidesoccur at an age when children are receiving what may be the only education they will ever receive. Further studies are urgently required to determine whether the effect of infection has longer term implications for school achievement. Over the last decade, severalhealth programmesaimed at improving child survival have resulted in a significant increase in the number of children of school age. However, these measureshave had little or no impact on the improvement of the quality of life of this agegroup. The older child has tended to be a forgotten member of the community and yet improving the health and education of schoolchildren is a crucial investment in the human capital that will determine a nation’s future development. Efforts to develop an efficient and low cost system to improve the health of school-age children have been given new impetus through the formation of a Partnership for Child Development, with core support for biomedical studies from the United Nations Development Programme, the Rockefeller Foundation and the Edna McConnell Clark Foundation, and from the James S. McDonnell Foundation for studies of cognition and edu
cation. This partnership, in collaboration with the World Health Organization, is now working with endemic country partners to develop an efficient, sustainable and low cost strategy of delivering anthehnintics (BERKLEY & JAMISON, 1991; BUNDY& HALL, 1992). Chemotherapy directed against A. lumbricoides, the hookworms and T. trichiura and targeted at school-age children is a feasible and effective approach to worm control. Single oral dose treatment with mebendazole (500 mg) or albendazole (400 mg) is very effective, safe and inexpensive. In Bangladesh an approach using repeated mass treatment has been proposed as a feasible approach to control intensity of A. lumbricoides rather than the selective treatment of heavily infected individuals (HALL et al., 1992). Mebendazole may be purchased at less than 10 US cents for each single 500 mg dose. The claim that therapy is irrelevant to the control of helminth disease, because children become reinfected, cannot be sustained in the face of the remarkable improvement in health achieved after treatment (WHO, 1990). In Kenya treatment for hookworm, T. trichiura and A. lumbricoides in undernourished schoolboys improved physical fitness only 7 weeks after treatment, despite continual exposure to reinfection and some incomplete cures (STEPHENSONet al., 1990). In the Republic of Korea, where a national control programme targeted at schoolchildren has reduced infection prevalence from 60% to 1% since 1969, the incidence of surgical complications has decreased proportionally to the national figures ofA. lumbricoides prevalence (CHAI et al., 1991). The direct benefit of chemotherapy is that the worm burden is removed, which immediately alleviates morbidity and may reduce the rate of transmission. Repeated treatment ensures that even if reinfection occurs the worm burdens are maintained below the level associated with morbidity. Thus the aim of repeated chemotherapy is not to eradicate or prevent infection, but to ensure that levels of infection are below those associatedwith morbidity. This approach is likely to make a major contribution to, for example, the prevention of protein energy malnutrition and iron deficiency anaemia, estimated to affect globally 500 million children and 800-900 million adults (WHO, 1990). Chemotherapy may also have indirect benefits. Ascariasis, and such protozoan infections as giardiasis (see below), may cause malabsorption of vitamin A (MAHALANABIS et al., 1979). This argues that nutritional supplementation programmes need to be supported by anthelmintic chemotherapy (TOMKINS& WATSON,1989). Control of worm infections through chemotherapy in school-agechildren may also have broader influences by generating a beneficial collaboration between Ministries of Health and Ministries of Education in endemic countries. The personnel of the peripheral health care system and the schoolteachers may successfully collaborate to deliver health care, in partnership with parents. The uotential imoact on multiole diseasecontrol is illustrateh by the expkrience of Zaizibar, where treatment against schistosomiasis has been successfully administered on a regular basis since November 1988 by schoolteachers(SAVIOLI et al.. 19891.Control of morbiditv due to intestinal helminths ‘has now been added to this pro-
354 gramme as a natural process of progressively integrating the control of other communicable diseases(ZANZIBAR, 1991). Health improvement and cost-effectiveness of chemotherapy against helminths can be monitored in schoolage children (SAVIOLI et al., 1989; BUNDYet al., 1992). From the evaluation of these types of programmes, models may be developed to help in predicting resource requirements for control. The school-based approach is only one of a range of strategies for control. Hehninth control at the community level can be easily integrated into the existing health care systems or into current health programmes such asmaternal and child health, family planning, water supply and sanitation, and health education. In Sri Lanka an integrated project has used intestinal parasite control as an entry point for promoting nutrition and family planning (PEREIRA, 1985). Alternatively, worm control may become a prime mover towards an integrated approach for the control of other diseases.Planning, management and programme operation will vary in each country but few health administrations exist without the infrastructure capable of introducing and sustaining the very simple technology involved (WHO, 1990). Programmes to control intestinal protozoa1 infections are at an earlier stageof development. The problems are also rather different. Entamoeba histolytka, Giardia duodenalis (=G. intestinalis) and Crwtosaoridium parvum are found both in industrialized anAddeveloping countries. However, the epidemiology of these infections differs in these settings as do the resources available for treatment and control. Deprived communities in the developed world may experience problems causedby intestinal protozoa in a similar manner and intensity to developing countries (WHO, 1992). E. histoZytica is one of the 10 most common infections in the world today. In 1984it was estimated that at least 40 000-100 000 deaths every year were causedby this infection (WALSH, 1988). Compelling evidence now indicates that what is currently identified as E. histolytica actually comprises 2 morphologically identical species, differing genetically and in their capacity to causedisease (WHO, 1992). The proportion of infections which produces diseasemay then-simply reflect the proportion of infections with ‘invasive’ E. histolvtica or (more likelv) the relationship may be more complex. New approaches to both epidemiological research and control strategies will clearly be necessary. In some developing countries studies have shown that virtually all children have been infected with G. duodenalis by 3 years of age. On the other hand, in the United States of America. G. duodenalis is the leadins cause of diarrhoeal disease outbreaks associated with- drinking water and is responsible for an estimated minimum of 4000 hospital admissions per year (WHO, 1992). Infection can causeweight loss, malabsorption and vitamin A deficiency, and is an important causeof growth faltering in children in industrialized countries. The effect on the nutritional status and growth of children in developing countries is difficult to evaluate becauseof the presence of multiple pathogens that could also explain differences in growth (TOMKINS & WATSON, 1989). The impact of G.&ode&s infection and diseaseon nutritional status and growth in children in developing countries needs further study and evaluation. There is now overwhelming evidence that the disease causedby intestinal helminth and protozoan infections is a oervasive nublic health uroblem. There is also good evidence from pilot studies, for helminthiases at least, that the problem is amenable to solution. Current efforts are needed to improve sanitation and water supplies, but are not sufficient. The challenge is to develop affordable
and sustainable solutions which are appropriate to the scaleof the problem. References Berkley,S. St Jamison, D. (1991). A Conference on the Health of School-age Children. Summary Report. New York: Rockefeller Foundation(mimeographed document). Bundy, D. A. P. & Hall, A. (1992).Partnership for child development. an international mooramme to imProvethe health and education of children through school based services.New York:
United Nations DevelopmentProgramme,Division of Glo-
bal and Inter-Regional-Prograr&es(mimeographeddocument). Bundy, D. A. P., Hall, A., Medley, G. F. & Savioli, L. (1992). Evaluating measuresto control intestinal parasitic infections. World Health Statistics Quarterly, in press. Chai, J. Y., Seung, Y. C., Soon, H. L. & Byong, S. S. (1991). Reduction in mevalence of biliarv and other surgical comalications of ascariasisaccording to-the decreaseo‘i its national ;iIg-q:qvalence in Korea. KoreanJournal of Parasitology, 29, _“_
Cooper, E. S., Bundy, D. A. P., Macdonald, T. T. & Golden, M. H. N (1990). Growth suppression in the Trichuris dysentery syndrome. European Journal of Clinical Nutrition, 44, 138-147. Hall, A., Anwar, K. S. & Ton&ins, A. M. (1992). Intensity of reinfection with Ascaris lumbricoides and its implications for parasite control. Lancet, 339, 1253-1257. Louw, J. H. (1974). Biliary ascariasisin childhood. South AfticanJournal ofsurgey, 12,219-225. Mahalanabis, D., Simpson, T. W., Chakraborty, M. L., Gangull, C., Bhatta Charjee, A. & Mukherjee, K. L. (1979). Malabsorption of water miscible vitamin A in children with giardiasis and ascariasis.American Journal of Clinical Nutrition, 32,313-318. Nokes, C., Grantham-McGregor, S. M., Sawyer, A. W., Cooper, E. S., Robinson, B. A. & Bundy, D. A. P. (1992). Moderate to heavy infections of Trichuris trichiura affect congnitive function in Jamaican school children. Parasitology, in press. Pawlowski, Z. S., Schad, G. A. & Stott, G. J. (1991). Hookworm Infection and Hookworm Anaemia. Approaches to prevention and control. Geneva: World Health Organization. Pereira, D. (1985). Helping the People to Hap Themselves. The Experience of the Integrated Project in Sri Lanka 1980-1984.
Tokyo: Japanese Organization for International Co-operation in Family Planning, Documentary Series no. 16, Japan. Savioli, L., Dixon, H., Kisumku, U. M. & Mott, K. E. (1989). Control of morbidity due to Schistosuma haematobium on Pemba island: selective population chemotherapy of schoolchildren with haematuria to identifv high risk areas. Transactions of the Royal Society of Tropical Medicine and Hygiene,
83.805-810. Stephenson, L. S., Latham, M. C., Kinoti, S. N., Kurz, K. M. & Brigham, H. (1990). Improvements in physical fitness of Kenyan schoolboys infected with hookworm, Trichuris trichiura and Ascaris lumbricoides following a single dose of albendazole. Transactions of the Royal Socie& of Tropical Medicine and Hygiene, 84,277-282. Tomkins, A. & Watson, F. (1989). Malnutrition and Infection: a Review. New York: United Nations Administrative Committee on Coordination/Subcommittee on Nutrition, State of the Art Series, Nutrition Policy Discussion Paper no. 5. Walsh, J. A. (1988). Prevalence of Entamoeba histolytica infection. In: Amoebiasis:Human Infection by Entamoeba histolytica, Ravdin, J. I. (editor). New York: Wiley. WHO (1987). Prevention and Control of Intestinal Parasitic Infections. Report of a WHO Expert Committee. Geneva: World Health Organization, Technical Report Series, no. 749. WHO (1990). Informal consultationon intestinal parasitic infections. Geneva 9-12July 1990. Geneva: World Health Organization, mimeographed document no. WHO/CDS/IPII90.1. WHO (1992). WHOII’AHO informal consultation on intestinal protozoa1 infections. Mexico, 21-23 October 1991. Geneva: World Health Organization, mimeographed document no. WHOICDSIIPII92.2. Zanzibar (1991). Revolutionary Governmentof Zanzibar, Priority Plan for Health Services 199112-199516. Zanzibar: Al-Khayria PressLtd (P.O. Box 3421, Zanzibar).