Volume 89, Issue 5
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



We conducted a cluster-randomized trial to assess the impact of a school-based water treatment, hygiene, and sanitation program on reducing infection with soil-transmitted helminths (STHs) after school-based deworming. We assessed infection with STHs at baseline and then at two follow-up rounds 8 and 10 months after deworming. Forty government primary schools in Nyanza Province, Kenya were randomly selected and assigned to intervention or control arms. The intervention reduced reinfection prevalence (odds ratio [OR] 0.56, 95% confidence interval [CI] 0.31–1.00) and egg count (rate ratio [RR] 0.34, CI 0.15–0.75) of . We found no evidence of significant intervention effects on the overall prevalence and intensity of , hookworm, or reinfection. Provision of school-based sanitation, water quality, and hygiene improvements may reduce reinfection of STHs after school-based deworming, but the magnitude of the effects may be sex- and helminth species-specific.


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  1. Crompton DW, , 1999. How much human helminthiasis is there in the world? J Parasitol 85: 397403.[Crossref] [Google Scholar]
  2. Hotez PJ, Bundy DAP, Beegle K, Brooker S, Drake L, de Silva N, Montresor A, Engels D, Jukes M, Chitsulo L, Chow J, Laxminarayan R, Michaud CM, Bethony J, Correa–Oliveira R, Xiao SH, Fenwick A, Savioli L, , 2006. Helminth Infections: Soil-Transmitted Helminth Infections and Schistosomiasis. Disease Control Priorities in Developing Countries. New York: Oxford University Press, 467482. [Google Scholar]
  3. Dickson R, Awasthi S, Williamson P, Demellweek C, Garner P, , 2000. Effects of treatment for intestinal helminth infection on growth and cognitive performance in children: systematic review of randomized trials. BMJ 320: 16971701.[Crossref] [Google Scholar]
  4. Sur D, Saha DR, Manna B, Rajendran K, Bhattacharya SK, , 2005. Periodic deworming with albendazole and its impact on growth status and diarrhoeal incidence among children in an urban slum of India. Trans R Soc Trop Med Hyg 99: 261267.[Crossref] [Google Scholar]
  5. Taylor-Robinson DC, Jones AP, Garner P, , 2007. Deworming drugs for treating soil-transmitted intestinal worms in children: effects on growth and school performance. Cochrane Database Syst Rev (4): CD000371. [Google Scholar]
  6. Gulani A, Nagpal J, Osmond C, Sachdev HP, , 2007. Effect of administration of intestinal anthelmintic drugs on hemoglobin: systematic review of randomized controlled trials. BMJ 334: 1095.[Crossref] [Google Scholar]
  7. Smith JL, Brooker S, , 2010. Impact of hookworm infection and deworming on anemia in non-pregnant populations: a systematic review. Trop Med Int Health 15: 776795.[Crossref] [Google Scholar]
  8. Keiser J, Utzinger J, , 2008. Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. JAMA 299: 19371948.[Crossref] [Google Scholar]
  9. Miguel E, Kremer M, , 2004. Worms: identifying impacts on education and health in the presence of treatment externalities. Econometrica 72: 159217.[Crossref] [Google Scholar]
  10. Bundy DAP, Wong MS, Lewis LL, Horton J, , 1990. Control of geohelminths by delivery of targeted chemotherapy through schools. Trans R Soc Trop Med Hyg 84: 115120.[Crossref] [Google Scholar]
  11. Jia T-W, Melville S, Utzinger J, King CH, Zhou X-N, , 2012. Soil-transmitted helminth reinfection after drug treatment: a systematic review and meta-analysis. PLoS Negl Trop Dis 6: e1621.[Crossref] [Google Scholar]
  12. Yap P, Du Z-W, Wu F-W, Jiang J-Y, Chen R, Zhou X-N, Hattendorf J, Utzinger J, Steinmann P, , 2013. Rapid re-infection with soil-transmitted helminths after triple-dose albendazole treatment of school-aged children in Yunnan, People's Republic of China. Am J Trop Med Hyg 89: 2331.[Crossref] [Google Scholar]
  13. Asaolu SO, Ofoezie IE, , 2003. The role of health education and sanitation in the control of helminth infections. Acta Trop 86: 283294.[Crossref] [Google Scholar]
  14. Henry FJ, , 1988. Reinfection with Ascaris lumbricoides after chemotherapy: a comparative study in three villages with varying sanitation. Trans R Soc Trop Med Hyg 82: 460464.[Crossref] [Google Scholar]
  15. WHO, UNICEF, 2010. Progress on Sanitation and Drinking-Water: 2010 Update. WHO/UNICEF Joint Monitoring Program for Water Supply and Sanitation. Geneva: WHO. [Google Scholar]
  16. UNICEF, 2009. Water, Sanitation and Hygiene Annual Report. New York: UNICEF. [Google Scholar]
  17. Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, Utzinger J, , 2012. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med 9: e1001162.[Crossref] [Google Scholar]
  18. Freeman MC, Greene LE, Dreibelbis R, Saboori S, Muga R, Brumback B, Rheingans R, , 2012. Assessing the impact of a school-based water treatment, hygiene, and sanitation program on pupil absence in Nyanza Province, Kenya: a cluster-randomized trial. Trop Med Int Health 17: 380391. [Google Scholar]
  19. Republic of Kenya Ministry of Education, 2008. National School Water, Sanitation and Hygiene Promotion Strategy 2008–2015. Nairobi. [Google Scholar]
  20. Tukahebwa EM, Vennervald BJ, Nuwaha F, Kabatereine NB, Magnussen P, , 2013. Comparative efficacy of one versus two doses of praziquantel on cure rate of Schistosoma mansoni infection and re-infection in Mayuge District, Uganda. Trans R Soc Trop Med Hyg 107: 397404.[Crossref] [Google Scholar]
  21. Moraes LR, Cancio JA, Cairncross S, , 2004. Impact of drainage and sewerage on intestinal nematode infections in poor urban areas in Salvador, Brazil. Trans R Soc Trop Med Hyg 98: 197204.[Crossref] [Google Scholar]
  22. Katz N, Chavez A, Pellegrino J, , 1972. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo 14: 397400. [Google Scholar]
  23. WHO, 1991. Basic Laboratory Methods in Medical Parasitology. Geneva: World Health Organization. [Google Scholar]
  24. Stothard JR, Imison E, French MD, Sousa-Figueiredo JC, Khamis IS, Rollinson D, , 2008. Soil-transmitted helminthiasis among mothers and their pre-school children on Unguja Island, Zanzibar with emphasis upon ascariasis. Parasitology 135: 14471455.[Crossref] [Google Scholar]
  25. Luoba AI, Wenzel Geissler P, Estambale B, Ouma JH, Alusala D, Ayah R, Mwaniki D, Magnussen P, Friis H, , 2005. Earth-eating and reinfection with intestinal helminths among pregnant and lactating women in western Kenya. Trop Med Int Health 10: 220227.[Crossref] [Google Scholar]
  26. Alemu A, Atnafu A, Addis Z, Shiferaw Y, Teklu T, Mathewos B, Birhan W, Gebretsadik S, Gelaw B, , 2011. Soil transmitted helminths and Schistosoma mansoni infections among school children in Zarima town, northwest Ethiopia. BMC Infect Dis 11: 189.[Crossref] [Google Scholar]
  27. Vyas S, Kumaranayake L, , 2006. Constructing socio-economic status indices: how to use principal components analysis. Health Policy Plan 21: 459468.[Crossref] [Google Scholar]
  28. Gwatkin DR, Rustein S, Johnson K, Suliman E, Wagstaff A, Amouzou A, , 2007. Socio-economic differences in health, nutrition, and population: Kenya. Country Reports on HPN and Poverty. Washington, DC: The World Bank. [Google Scholar]
  29. Anderson RM, Schad GA, , 1985. Hookworm burdens and fecal egg counts: an analysis of the biological basis of variation. Trans R Soc Trop Med Hyg 79: 812825.[Crossref] [Google Scholar]
  30. Anderson RM, May RM, , 1991. Infectious Diseases of Humans. Oxford: Oxford University Press. [Google Scholar]
  31. Brooker S, Bundy DA, Cook GC, Zumla AI, , 2008. Soil-transmitted helminths (geohelminths). , eds. Manson's Tropical Diseases. London: Elsevier, 15151548. [Google Scholar]
  32. Humphries D, Mosites E, Otchere J, Twum WA, Woo L, Jones-Sanpei H, Harrison LM, Bungiro RD, Benham-Pyle B, Bimi L, Edoh D, Bosompem K, Wilson M, Cappello M, , 2011. Epidemiology of hookworm infection in Kintampo North Municipality, Ghana: patterns of malaria coinfection, anemia, and albendazole treatment failure. Am J Trop Med Hyg 84: 792800.[Crossref] [Google Scholar]
  33. Hayes R, Moulton LH, Morgan BTJ, , 2009. Cluster randomized controlled trials. New York: Chapman and Hall/CRC Press.[Crossref] [Google Scholar]
  34. Brooker S, Bethony J, Hotez PJ, , 2004. Human hookworm infection in the 21st century. Adv Parasitol 58: 197288.[Crossref] [Google Scholar]
  35. Gunawardena GS, Karunaweera ND, Ismail MM, , 2005. Effects of climatic, socio-economic and behavioral factors on the transmission of hookworm (Necator americanus) on two low-country plantations in Sri Lanka. Ann Trop Med Parasitol 99: 601609.[Crossref] [Google Scholar]
  36. Traub RJ, Robertson ID, Irwin P, Mencke N, Andrew Thompson RC, , 2004. The prevalence, intensities and risk factors associated with geohelminth infection in tea-growing communities of Assam, India. Trop Med Int Health 9: 688701.[Crossref] [Google Scholar]
  37. Knopp S, Mohammed KA, Stothard JR, Khamis IS, Rollinson D, Marti H, Utzinger J, , 2010. Patterns and risk factors of helminthiasis and anemia in a rural and a peri-urban community in Zanzibar, in the context of helminth control programs. PLoS Negl Trop Dis 4: e681.[Crossref] [Google Scholar]
  38. Gungoren B, Latipov R, Regallet G, Musabaev E, , 2007. Effect of hygiene promotion on the risk of reinfection rate of intestinal parasites in children in rural Uzbekistan. Trans R Soc Trop Med Hyg 101: 564569.[Crossref] [Google Scholar]
  39. Kanoa B, George E, Abed Y, Al-Hindi A, , 2006. Evaluation of the relationship between intestinal parasitic infection and health education among school children in Gaza City, Beit-Lahia Village and Jabalia Refugee Camp, Gaza Strip, Palestine. The Islamic University Journal 14: 3949 (Series of Natural Studies and Engineering). [Google Scholar]
  40. Moraes LR, Cancio JA, Cairncross S, Huttly S, , 2003. Impact of drainage and sewerage on diarrhoea in poor urban areas in Salvador, Brazil. Trans R Soc Trop Med Hyg 97: 153158.[Crossref] [Google Scholar]
  41. Olsen A, Namwanje H, Nejsum P, Roepstorff A, Thamsborg SM, , 2009. Albendazole and mebendazole have low efficacy against Trichuris trichiura in school-age children in Kabale District, Uganda. Trans R Soc Trop Med Hyg 103: 443446.[Crossref] [Google Scholar]
  42. Hlaing T, Saw T, Lwin M, , 1987. Reinfection of people with Ascaris lumbricoides following single, 6-month and 12-month interval mass chemotherapy in Okpo village, rural Burma. Trans R Soc Trop Med Hyg 81: 140146.[Crossref] [Google Scholar]
  43. Hall A, Anwar KS, Tomkins AM, , 1992. Intensity of reinfection with Ascaris lumbricoides and its implications for parasite control. Lancet 339: 12531257.[Crossref] [Google Scholar]
  44. Elkins DB, Haswell-Elkins M, Anderson RM, , 1988. The importance of host age and sex to patterns of reinfection with Ascaris lumbricoides following mass anthelmintic treatment in a South Indian fishing community. Parasitology 96: 171184.[Crossref] [Google Scholar]
  45. Quinnell RJ, , 2003. Genetics of susceptibility to human helminth infection. Int J Parasitol 33: 12191231.[Crossref] [Google Scholar]
  46. Pullan RL, Kabatereine NB, Quinnell RJ, Brooker S, , 2010. Spatial and genetic epidemiology of hookworm in a rural community in Uganda. PLoS Negl Trop Dis 4: e713.[Crossref] [Google Scholar]
  47. Brooker S, Kabatereine NB, Smith JL, Mupfasoni D, Mwanje MT, Ndayishimiye O, Lwambo NJ, Mbotha D, Karanja P, Mwandawiro C, Muchiri E, Clements AC, Bundy DA, Snow RW, , 2009. An updated atlas of human helminth infections: the example of East Africa. Int J Health Geogr 8: 42.[Crossref] [Google Scholar]
  48. Habtamu K, Degarege A, Ye-Ebiyo Y, Erko B, , 2011. Comparison of the Kato-Katz and FLOTAC techniques for the diagnosis of soil-transmitted helminth infections. Parasitol Int 60: 398402.[Crossref] [Google Scholar]
  49. Tarafder M, Carabin H, Joseph L, Balolong E, Jr Olveda R, McGarvey S, , 2010. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a ‘gold standard’. Int J Parasitol 40: 399404.[Crossref] [Google Scholar]
  50. WHO, 2012. Accelerating Work to Overcome the Global Impact of Neglected Tropical Disease: A Roadmap for Implementation. Geneva: World Health Organization. [Google Scholar]
  51. Cairncross S, Blumenthal U, Kolsky P, Moraes L, Tayeh A, , 1996. The public and domestic domains in the transmission of disease. Trop Med Int Health 1: 2734.[Crossref] [Google Scholar]

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  • Received : 02 May 2013
  • Accepted : 13 Jul 2013
  • Published online : 06 Nov 2013

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