Skip to main content
PMC home page
UKPMC Funders Author Manuscripts logoLink to UKPMC Funders Author Manuscripts
. Author manuscript; available in PMC: 2017 Oct 6.
Published in final edited form as: Trans R Soc Trop Med Hyg. 2002 Nov-Dec;96(6):577–579. doi: 10.1016/s0035-9203(02)90316-0

Schistosomiasis and soil-transmitted helminth infections: forging control efforts

Lorenzo Savioli 1, Sally Stansfield 2, Donald AP Bundy 3, Arlene Mitchell 4, Rita Bathia 5, Dirk Engels 1, Antonio Montresor 1, Maria Neira 1, Ali Mohammed Shein 6
PMCID: PMC5630087  EMSID: EMS74300  PMID: 12625126

“….. both school performance and worm burden are significantly related to the social and hygienic conditions of families”. (de Carneri et al. 1967)

Ten years ago in this journal we issued a challenge to expand the delivery of affordable and sustainable interventions for intestinal parasite control in a global effort commensurate with the scale of the problem (Savioli et al., 1992).

After gradual intensification of efforts over the ensuing ten years, WHO, its Member States and partners are implementing a combined strategy for the control of schistosomiasis and soil-transmitted helminths integrated into ongoing health and education initiatives (WHO, 2002a).

This strategy is summarized in the World Health Assembly resolution WHA 54.19 of May 2001. The resolution urges Member States to ensure access to essential drugs against schistosomiasis and soil-transmitted helminthiasis in all health services in endemic areas for the treatment of clinical cases and groups at high risk of morbidity such as women and children, with the goal of attaining a minimum target of regular administration of chemotherapy to at least 75% and up to 100% of all school-age children at risk of morbidity by 2010. This policy is based on the evidence that morbidity can be controlled by periodical treatment of high-risk groups with anthelminthics.

The burden of disease

The burden of disease due to schistosomiasis and soil-transmitted helminth infections remains enormous. About 2 billion people are affected worldwide, of whom 300 million suffer associated severe morbidity. In 1999, WHO estimated that these infections represented more than 40% of the disease burden due to all tropical diseases, excluding malaria.

Because of their hygiene and play habits, children are especially vulnerable to these infections. The over 400 million school-age children who are infected with schistosomes or soil-transmitted helminths (WHO, 2002a) are often physically and intellectually compromised by anaemia, attention deficits, learning disabilities, school absenteeism and higher dropout rates. The failure to treat school age children therefore hampers child development, yields a generation of adults disadvantaged by the irreversible sequelae of infection, and compromises the economic development of their communities and nations (Partnership for Child Development, 1997;WHO, 2002a).

Eighty five percent of the 200 million people with schistosomiasis live on the African continent (Chitsulo et al., 2000). The burden of disease due to schistosomiasis in Africa has recently been re-estimated (van der Werf et al., 2002). 70 Million individuals have haematuria associated with Schistosoma haematobium infection and 18 and 10 million respectively suffer major bladder wall pathology and hydronephrosis. S.haematobium related mortality due to non-functioning kidney and portal hypertension due to Schistosoma mansoni are estimated to be respectively 150 and 130 thousand per year (van der werf et al., 2002).

Chemotherapy based morbidity control

Accumulated experience from medium to large scale programmes and has clearly demonstrated that human suffering and the burden due to these infections can be significantly reduced through repeated/regular treatment with single dose anthelminthics delivered through school health programmes or other ongoing health or education programmes (Partnership for Child Development, 1998; Albonico et al., 1999). Several controlled trials demonstrated a positive effect on growth, even if differences were observed on the extent of benefit gained. (Dickson et al 2000, Michael 2000, Savioli et al 2000). The plummeting price of praziquantel has made this approach more feasible than it was ten years ago. Moreover, recent tests of praziquantel samples from 19 different manufacturers collected in the field reassured that many low cost generics are of satisfactory quality (Appleton and Mbaye, 2001).

Treatment of a child with praziquantel currently costs approximately 20 cents. A single-dose treatment for soil-transmitted helminth infections with any of the 4 anthelminthics on the WHO list of essential drugs (albendazole, levamisole, mebendazole and pyrantel) costs less than 3 US cents. WHO has calculated that the cost of intervention, including delivery, where schistosomiasis and soil-transmitted helminth infections are both endemic is typically less than one US$ and can be as low as 30 US cents per child per year, while treatment of soil-transmitted helminth infections alone costs as little as 10 US cents per child per year (Montresor et al, 2002a)

Progress in least-developed, low-income and lower-middle-income countries

Encouraging health effects have been reported from programmes implementing these control measures. In mainland Tanzania a single treatment with praziquantel delivered to school age children infected with S. haematobium eliminated 88% of the urinary tract pathology after the first six months, with more complete resolution of lesions in the younger age group. In this intense transmission area regular treatment as infrequently as every 18-24 months, starting in primary school, was indicated as an effective means to control morbidity and prevent the development and persistence of severe urinary tract pathology and genital lesions (Hatz et al., 1998).

Again in Tanzania, the Zanzibar Helminth Control Programme prevented 1260 cases of moderate to severe anaemia and 276 cases of severe anaemia per year in a population of 30,000 school-children by administering 500 mg of mebendazole twice a year (Stoltzfus et al., 1998). In addition to reaching 98% of the enrolled school children, a further 60% of non-enrolled school age children were reached by simply inviting their siblings and friends to the deworming school day (Montresor et al., 2001a).

In these two African high transmission settings, in spite of continuous re-infection, morbidity is controlled and irreversible sequelae in adulthood prevented by regular and inexpensive treatment of schoolchildren.

With the cooperative action of the Ministry of Health, the Ministry of Education, WFP and WHO, schools in Nepal provide anthelminthic treatment to each child every six months, an enriched hot meal on school days, and food for girls to take home as an incentive for good attendance. The programme also sustains the supply of drugs and strengthens the local economy by developing the capacity of a local pharmaceutical company to produce the required medication at low cost. The periodical control of the drug guaranteed its quality throughout the programme (Khanal &Walgate 2002).

School-based deworming programmes have been cost-effective in boosting school participation. In Kenya, such a programme reduced school absenteeism by one quarter, with the largest gains among the youngest children (Miguel & Kremer 2001). Perhaps even more importantly, this study showed that even those children who had not themselves been treated were able to benefit from the generally lowered transmission rate in the schools.

Unlike the other common helminthic infections, the prevalence and intensity of hookworm infections slowly increase with age (WHO 1996a). Hookworm infection is the leading cause of pathological blood loss in tropical and subtropical regions (Torlesse & Hodges, 2000). Some 44 million pregnancies are currently complicated by maternal hookworm infection (Bundy et al., 1995), placing both the mother and her child at higher risk of death during pregnancy and delivery. In Sierra Leone an additive effect was shown when anthelminthic treatment was combined with iron and folate supplements to control maternal anaemia during pregnancy (Torlesse & Hodges, 2000). In Sri Lanka the same combined intervention improved the health of the mothers with a beneficial effect on their birth outcome without any increase risk of malformations (de Silva et al., 1999, Bradley & Horton, 2001).

However this progress is impeded by the poor access to praziquantel in peripheral health services recently documented in Ghana and Cambodia (van der Werf, 2002, personal communication, URBANI , 2002, personal communication). Experience shows that effective morbidity control requires regular treatment of high-risk groups, especially school-age children, and access to treatment in the peripheral health care structures of endemic areas.

Strategy, tools, targets and drug monitoring

Technical problems associated with large-scale chemotherapy campaigns have been addressed and solved. For example, teachers and other non-health personnel are able with minimal training effectively to distribute anthelminthic drugs to school age children (Bundy & de Silva, 1998; WHO, 2002a). Treatment with praziquantel at the peripheral health and school level may be simplified by the use of a “dose pole” – a measurement of the child’s height that determines the correct dosage (Hall et al, 1999; Montresor et al., 2001b, Montresor et al., 2002c). To improve health and prevent sexually transmitted diseases due to the genital lesions caused by schistosomiasis, praziquantel should be made available to all school-age and adolescent girls and women of reproductive age in areas where schistosomiasis is endemic. A recent expert meeting concluded that praziquantel treatment should also be offered to pregnant women with schistosomiasis, as the benefits of such treatment greatly outweighed any reported adverse effects (WHO, 2002b). Mebendazole, albendazole and other anthelminthics have also recently been approved for use in children over 12 months of age (WHO, 2002b), so that there is no further justification for excluding these children from treatment to prevent severe complications due to soil-transmitted helminths (Montresor et al., 2002).

The World Health Assembly resolution set the global target of regularly treating 75% of school-age children at risk by 2010. This represents approximately 398 million children today and approximately 415 million in 2010, taking into account projected global growth rates (WHO 2002a). The challenge is to establish start-up activities in all endemic countries on all continents, and to expand them to a national level in the next 8 years.

Ongoing small-scale initiatives so far cover some 4 million school-age children in Africa, corresponding to only 4% of the target for this continent. Last year, however, in cooperation with the World Food Programme (WFP) and the World Bank, WHO trained representatives of the ministries of health and education of 21 countries. Start-up funding of up to $50,000 per country was provided by the Canadian International Development Agency and deworming and school-feeding programs have already begun in 19 of the 41 African endemic countries.

In April 2000, at the Dakar World Education Forum, a partnership was launched by UNESCO, UNICEF, WHO, Education International and the World Bank to assist countries in Focusing Resources on Effective School Health, including support for the distribution of anthelminthics through schools (FRESH, 2000). This “FRESH” partnership aims to improve the health and nutrition of school children as a contribution to the global Education for All efforts to ensure universal access to basic education. To date, more than 20 projects targeting 45 million school-age children have been supported in Africa, and projects being developed should significantly increase the number of beneficiaries

On other continents, the strategy must be adapted to the epidemiological setting. For example, in South-east Asia activities are also targeting food-borne trematodes and cestodes

Expanding treatment programmes will increase the drug pressure on parasite populations. The danger of drug resistance is probably more real for soil-transmitted helminths than for schistosomes (Geerts & Gryseels, 2001). To prevent or delay the emergence of resistance chemotherapy should be targeted only to high-risk groups, such as schoolchildren, with possible alternation among different drug classes. Frequency of re-treatment should be sufficient to control morbidity but also reduced to a minimum to avoid drug pressure on parasite populations. Monitoring and surveillance of drug efficacy must be built into operational programmes (WHO, 1996b).

Moving ahead

Scaling up interventions will require a concerted effort at both the global and country levels. A key step in achieving this has been the request from the 54th WHA to WHO to combat schistosomiasis and soil-transmitted helminthiasis by advocating new partnerships with organizations of the United Nations system, bilateral agencies, non-governmental organizations and the private sector, and by continuing to provide international direction and co-ordination.

WHO has proposed a broad partnership that promotes the incorporation of deworming into regular, current activities in the field, for both the education and health sectors. In June 2001 and April 2002 two meetings of the Partnership for Parasite Control (PPC) took place in Geneva and Rome, hosted respectively by WHO and WFP. The PPC mobilizes increased resources and permits new synergy among public and private efforts for the control of soil-transmitted helminths and schistosomiasis at the global and national levels.

In 1992 we expressed concern that the public health impact of helminthic infections was consistently and considerably underestimated (Savioli et al., 1992). Today the burden of disease has been reassessed, practical field tools have been further refined, the price of anthelminthics has dropped, a public health policy has been developed, the education sector has recognized its role in parasite control and political commitment by endemic countries and international organizations is building. The possibility of significantly reducing the morbidity caused by schistosomiasis and soil-transmitted helminths, and having a real and lasting impact on one group of the neglected diseases of the poorest of the poor, is no longer a dream.

Acknowledgements

We wish to thank, among many others, Dr D. Cioli, Dr D. Colley, Dr J. A. Cook, Professor D.W.T. Crompton, Dr S. Chandiwana, Dr A. Davis, Professor B. Gryseels, Professor P. Hagan, Professor M. Ishmael, Dr P. Jordan, Dr A. Kochi, Dr J. Mahjour, Dr M.G. Mokbel, Professor P.G. Smith, Professor G. Schad, Professor L. Stephenson, Professor T. Takeuchi, Professor M.G. Taylor, Dr G. Torrigiani. They have been advocating and supporting worm control when few believed in it. A particular note of thanks to all those involved at country level in helminth control. Without their contribution in finding solutions with limited resources, schistosomiasis and soil-transmitted helminths control would never be possible.

References

  1. Albonico M, Crompton DWT, Savioli L. Control strategies for human intestinal nematode infections. Advances in Parasitology. 1999;42:277–341. doi: 10.1016/s0065-308x(08)60151-7. [DOI] [PubMed] [Google Scholar]
  2. Appleton CC, Mbaye A. Praziquantel - quality, dosages and markers of resistance. Trends in Parasitology. 2001;17:356–357. doi: 10.1016/s1471-4922(01)02028-1. [DOI] [PubMed] [Google Scholar]
  3. Bradley M, Horton J. Assessing the risk of benzimidazole therapy during pregnancy. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2001;95:72–73. doi: 10.1016/s0035-9203(01)90338-4. [DOI] [PubMed] [Google Scholar]
  4. Bundy DAP, Chan MS, Savioli L. Hookworm infection in pregnancy. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1995;89:521–522. doi: 10.1016/0035-9203(95)90093-4. [DOI] [PubMed] [Google Scholar]
  5. Bundy DAP, De Silva NR. Can we deworm this wormy world? British Medical Bulletin. 1998;54(2):421–432. doi: 10.1093/oxfordjournals.bmb.a011698. [DOI] [PubMed] [Google Scholar]
  6. Chitsulo L, Engels D, Montresor A, Savioli L. The global status of schistosomiasis and its control. Acta Tropica. 2000;77:41–51. doi: 10.1016/s0001-706x(00)00122-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. De Carneri I, Garofano M, Grassi L. On the role of trichocephalosis in infantile physical and mental retardation as determined on the basis of a quantitative survey carried out in an endemic area of Northern Italy. Rivista di Parassitologia. 1967;XXVIII:103–122. [PubMed] [Google Scholar]
  8. de Silva NR, Sirisena JL, Gunasekera DP, Ismail MM, de Silva HJ. Effect of mebendazole therapy during pregnancy on birth outcome. Lancet. 1999;353:1145–1149. doi: 10.1016/s0140-6736(98)06308-9. [DOI] [PubMed] [Google Scholar]
  9. Dickson R, Awasthi S, Williamson P, Demellweek C, Garner P. Effects of treatment for intestinal helminth infection on growth and cognitive performance in children: systematic review of randomised trials. BMJ. 2000;320:1697–701. doi: 10.1136/bmj.320.7251.1697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. FRESH. Focusing Resources on Effective School Health: ensuring the quality and equity of basic education. Jointly published by UNESCO, UNICEF, WHO and the World Bank; Washington, DC, USA: 2000. [Google Scholar]
  11. Geerts S, Gryseels B. Anthelmintic resistance in human helminths: a review. Tropical Medicine and International Health. 2001;6:915–921. doi: 10.1046/j.1365-3156.2001.00774.x. [DOI] [PubMed] [Google Scholar]
  12. Hall A, Nokes C, Wen S-T, Adjei S, Kihamia C, Mwanre L, Bobrow E, DeGraft-Johnson, Bundy DAP. Alternatives to body weight for estimating the dose of praziquantel needed to treat schistosomiasis. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1999;93:653–658. doi: 10.1016/s0035-9203(99)90087-1. [DOI] [PubMed] [Google Scholar]
  13. Hatz CF, Vennervald BJ, Nkulila T, Vounatsou P, Kombe Y, Mayombana C, Mshinda H, Tanner M. Evolution of Schistosoma haematobium-related pathology over 24 months after treatment with praziquantel among school children in southeastern Tanzania. American Journal of Tropical Medicine and Hygiene. 1998;59:775–781. doi: 10.4269/ajtmh.1998.59.775. [DOI] [PubMed] [Google Scholar]
  14. Khanal P, Walgate R. Nepal deworming programme ready to go worldwide. Bulletin of the World Health Organization. 2002;80:423–424. [PMC free article] [PubMed] [Google Scholar]
  15. Michael E. Treatment for intestinal helminth infection. Contrary to authors' comments, meta-analysis supports global helminth control initiatives. BMJ. 2000;321:1224–5. [PMC free article] [PubMed] [Google Scholar]
  16. Miguel E, Kremer M. Worms: education and health externalities in Kenya. 2001 NBER Working Paper No.w8481 ( http://www.nber.org/papers/W8481)
  17. Montresor A, Ramsan M, Chwaya HM, Ameir H, Foum A, Albonico M, Gyorkos TW, Savioli L. Extending anthelminthic coverage to non-enrolled school-age children using a simple and low-cost method. Tropical Medicine and International Health. 2001a;6:535–537. doi: 10.1046/j.1365-3156.2001.00750.x. [DOI] [PubMed] [Google Scholar]
  18. Montresor A, Engels D, Chitsulo L, Bundy DAP, Brooker S, Savioli L. Development and validation of a ‘tablet pole’ for the administration of praziquantel in sub-Saharan Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2001b;95:542–544. doi: 10.1016/s0035-9203(01)90034-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Montresor A, Crompton DWT, Gyorkos TW, Savioli L. Helminth control in school-age children. A guide for managers of control programmes. Geneva: World Health Organization; 2002a. (in press) [Google Scholar]
  20. Montresor A, Stoltzfus RJ, Albonico M, Tielsch JM, Rice A, Chwaya HM, Savioli L. Is the exclusion of children under 24 months from anthelminthic treatment justifiable? Transactions of the Royal Society of Tropical Medicine and Hygiene. 2002b;96:197–199. doi: 10.1016/s0035-9203(02)90303-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Montresor A, Ramsan M, Engels D, Foum A, Savioli L. Field test of the ‘dose pole’ for praziquantel in Zanzibar. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2002c doi: 10.1016/s0035-9203(02)90111-2. (in press) [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Partnership for Child Development. Health and nutritional status of schoolchildren in Africa: evidence from school based health programmes in Ghana and Tanzania. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1998;92:254–261. doi: 10.1016/s0035-9203(98)90999-3. [DOI] [PubMed] [Google Scholar]
  23. The Partnership for Child Development. Better health, nutrition and education for the school aged child. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1997;91:1–2. doi: 10.1016/s0035-9203(97)90370-9. [DOI] [PubMed] [Google Scholar]
  24. Savioli L, Bundy D, Tomkins A. Intestinal parasitic infections: a soluble public health problem. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1992;86:353–354. doi: 10.1016/0035-9203(92)90215-x. [DOI] [PubMed] [Google Scholar]
  25. Savioli L, Neira M, Albonico M, Beach MJ, Chwaya HM, Crompton DW, Dunne J, Ehrenberg JP, Gyorkos T, Kvalsvig J, Taylor MG, et al. Treatment for intestinal helminth infection. Review needed to take account of all relevant evidence, not only effects on growth and cognitive performance. BMJ. 2000;321:1226–7. [PubMed] [Google Scholar]
  26. Stoltzfus RJ, Albonico M, Chwaya HM, Tielsch JM, Schulze KJ, Savioli L. Effects of the Zanzibar school-based deworming program on iron status of children. The American Journal of Clinical Nutrition. 1998;68:179–186. doi: 10.1093/ajcn/68.1.179. [DOI] [PubMed] [Google Scholar]
  27. Torlesse H, Hodges M. Anthelminthic treatment and haemoglobin concentrations during pregnancy. Lancet. 2000;356:1083. doi: 10.1016/S0140-6736(00)02738-0. [DOI] [PubMed] [Google Scholar]
  28. van der Werf MJ, de Vlas SJ, Brooker S, Looman CWN, Nagelkerke NJD, Habbema JDF, Engels D. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Tropica. 2002 doi: 10.1016/s0001-706x(03)00029-9. (in press) [DOI] [PubMed] [Google Scholar]
  29. WHO. Report of the WHO informal consultation on hookworm infection and anaemia in girls and women. Geneva: World Health Organization; 1996a. WHO/CTD/SIP/96.1. [Google Scholar]
  30. WHO. Report of the WHO informal consultation on monitoring of drug efficacy in the control of schistosomiasis and intestinal nematodes. Geneva: World Health Organization; 1996b. WHO/CDS/CPC/SIP/99.1. [Google Scholar]
  31. WHO. Prevention and control of schistosomiasis and soil-transmitted helminthiasis Report of the joint WHO Expert Committees. Geneva: World Health Organization; 2002a. Technical Report Series, no. (in preparation) [PubMed] [Google Scholar]
  32. WHO. Report of the WHO informal consultation on the use of praziquantel during pregnancy and lactation and albendazole/mebendazole in children under 24 months. Geneva: World Health Organization; 2002b. WHO/CDS/CPE/PVC/2002.4 (in preparation) [Google Scholar]

RESOURCES