• 1.

    WHO, 2012. Schistosomiasis: population requiring preventive chemotherapy and number of people treated in 2010. Wkly Epidemiol Rec 87: 3744.

    • Search Google Scholar
    • Export Citation
  • 2.

    Steinmann P, Keiser J, Bos R, Tanner M, Utzinger J, 2006. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6: 411425.

    • Search Google Scholar
    • Export Citation
  • 3.

    King CH, 2010. Parasites and poverty: the case of schistosomiasis. Acta Trop 113: 95104.

  • 4.

    WHO, 2008. The Global Burden of Disease: 2004 Update. Geneva: World Health Organization.

  • 5.

    Verani JR, Abudho B, Montgomery SP, Mwinzi PN, Shane HL, Butler SE, Karanja DM, Secor WE, 2011. Schistosomiasis among young children in Usoma, Kenya. Am J Trop Med Hyg 84: 787791.

    • Search Google Scholar
    • Export Citation
  • 6.

    Odogwu SE, Ramamurthy NK, Kabatereine NB, Kazibwe F, Tukahebwa E, Webster JP, Fenwick A, Stothard JR, 2006. Schistosoma mansoni in infants (aged < 3 years) along the Ugandan shoreline of Lake Victoria. Ann Trop Med Parasitol 100: 315326.

    • Search Google Scholar
    • Export Citation
  • 7.

    Stothard JR, Kabatereine NB, Tukahebwa EM, Kazibwe F, Mathieson W, Webster JP, Fenwick A, 2005. Field evaluation of the Meade Readiview handheld microscope for diagnosis of intestinal schistosomiasis in Ugandan school children. Am J Trop Med Hyg 73: 949955.

    • Search Google Scholar
    • Export Citation
  • 8.

    Satayathum SA, Muchiri EM, Ouma JH, Whalen CC, King CH, 2006. Factors affecting infection or reinfection with Schistosoma haematobium in coastal Kenya: survival analysis during a nine-year, school-based treatment program. Am J Trop Med Hyg 75: 8392.

    • Search Google Scholar
    • Export Citation
  • 9.

    Smith JH, Christie JD, 1986. The pathobiology of Schistosoma haematobium infection in humans. Hum Pathol 17: 333345.

  • 10.

    Warren KS, 1978. The pathology, pathobiology and pathogenesis of schistosomiasis. Nature 273: 609612.

  • 11.

    King CH, Dickman K, Tisch DJ, 2005. Reassessment of the cost of chronic helmintic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 365: 15611569.

    • Search Google Scholar
    • Export Citation
  • 12.

    Jukes MC, Nokes CA, Alcock KJ, Lambo JK, Kihamia C, Ngorosho N, Mbise A, Lorri W, Yona E, Mwanri L, Baddeley AD, Hall A, Bundy DA; Partnership for Child Development, 2002. Heavy schistosomiasis associated with poor short-term memory and slower reaction times in Tanzanian schoolchildren. Trop Med Int Health 7: 104117.

    • Search Google Scholar
    • Export Citation
  • 13.

    Ndamba J, Makaza N, Munjoma M, Gomo E, Kaondera KC, 1993. The physical fitness and work performance of agricultural workers infected with Schistosoma mansoni in Zimbabwe. Ann Trop Med Parasitol 87: 553561.

    • Search Google Scholar
    • Export Citation
  • 14.

    Collins KJ, Brotherhood RJ, Davies CT, Dore C, Hackett AJ, Imms FJ, Musgrove J, Weiner JS, Amin MA, El Karim M, Ismail HM, Omer AH, Sukkar MY, 1976. Physiological performance and work capacity of Sudanese cane cutters with Schistosoma mansoni infection. Am J Trop Med Hyg 25: 410421.

    • Search Google Scholar
    • Export Citation
  • 15.

    Fenwick A, Figenschou BH, 1972. The effect of Schistosoma mansoni infection of the productivity of cane cutters on a sugar estate in Tanzania. Bull World Health Organ 47: 567572.

    • Search Google Scholar
    • Export Citation
  • 16.

    King CH, Sturrock RF, Kariuki HC, Hamburger J, 2006. Transmission control for schistosomiasis - why it matters now. Trends Parasitol 22: 575582.

    • Search Google Scholar
    • Export Citation
  • 17.

    WHO, 2006. Preventive Chemotherapy in Human Helminthiasis. Coordinated use of anthelmintic drugs in control interventions: guidelines for health professionals and programme managers. Geneva: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 18.

    Vennervald BJ, Booth M, Butterworth AE, Kariuki HC, Kadzo H, Ireri E, Amaganga C, Kimani G, Kenty L, Mwatha J, Ouma JH, Dunne DW, 2005. Regression of hepatosplenomegaly in Kenyan school-aged children after praziquantel treatment and three years of greatly reduced exposure to Schistosoma mansoni. Trans R Soc Trop Med Hyg 99: 150160.

    • Search Google Scholar
    • Export Citation
  • 19.

    Kabatereine NB, Brooker S, Koukounari A, Kazibwe F, Tukahebwa EM, Fleming FM, Zhang Y, Webster JP, Stothard JR, Fenwick A, 2007. Impact of a national helminth control programme on infection and morbidity in Ugandan schoolchildren. Bull World Health Organ 85: 9199.

    • Search Google Scholar
    • Export Citation
  • 20.

    Koukounari A, Gabrielli AF, Toure S, Bosque-Oliva E, Zhang Y, Sellin B, Donnelly CA, Fenwick A, Webster JP, 2007. Schistosoma haematobium infection and morbidity before and after large-scale administration of praziquantel in Burkina Faso. J Infect Dis 196: 659669.

    • Search Google Scholar
    • Export Citation
  • 21.

    Abdel-Rahman TA, Collins KJ, Dore C, 1990. Oxylog studies of energy expenditure and schistosomiasis in the Sudan. J Trop Med Hyg 93: 365371.

    • Search Google Scholar
    • Export Citation
  • 22.

    Richter J, 2003. The impact of chemotherapy on morbidity due to schistosomiasis. Acta Trop 86: 161183.

  • 23.

    Handzel T, Karanja DM, Addiss DG, Hightower AW, Rosen DH, Colley DG, Andove J, Slutsker L, Secor WE, 2003. Geographic distribution of schistosomiasis and soil-transmitted helminths in western Kenya: implications for anthelmintic mass treatment. Am J Trop Med Hyg 69: 318323.

    • Search Google Scholar
    • Export Citation
  • 24.

    Committee WHOE, 2002. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ Tech Rep Ser 912: ivi, 1–57 back cover.

    • Search Google Scholar
    • Export Citation
  • 25.

    Kimathi NAMJ, Murithi, 2002. Clinical Guidelines for Diagnosis and Treatment of Common Conditions in Kenya. GoK MoH, ed. Nairobi: The Regal Press Kenya Lett, 190202.

    • Search Google Scholar
    • Export Citation
  • 26.

    WHO, 2012. Child Growth Standards. Available at: http://www.who.int/childgrowth/software/en/. Accessed September 12, 2011.

  • 27.

    Leger LA, Mercier D, Gadoury C, Lambert J, 1988. The multistage 20 metre shuttle run test for aerobic fitness. J Sports Sci 6: 93101.

  • 28.

    Richter J, Domingues AL, Barata CH, Prata AR, Lambertucci JR, 2001. Report of the second satellite symposium on ultrasound in schistosomiasis. Mem Inst Oswaldo Cruz 96 (Suppl): 151156.

    • Search Google Scholar
    • Export Citation
  • 29.

    Binder DA, 1983. On the variances of asymptotically normal estimators from complex surveys. Int Stat Rev 51: 279292.

  • 30.

    Harrell FE, 2001. Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis. New York: Springer.

    • Search Google Scholar
    • Export Citation
  • 31.

    Groenwold RH, Donders AR, Roes KC, Harrell FE Jr, Moons KG, 2012. Dealing with missing outcome data in randomized trials and observational studies. Am J Epidemiol 175: 210217.

    • Search Google Scholar
    • Export Citation
  • 32.

    Hamel MJ, Adazu K, Obor D, Sewe M, Vulule J, Williamson JM, Slutsker L, Feikin DR, Laserson KF, 2011. A reversal in reductions of child mortality in western Kenya, 2003–2009. Am J Trop Med Hyg 85: 597605.

    • Search Google Scholar
    • Export Citation
  • 33.

    Sokhna C, Le Hesran JY, Mbaye PA, Akiana J, Camara P, Diop M, Ly A, Druilhe P, 2004. Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal. Malar J 3: 43.

    • Search Google Scholar
    • Export Citation
  • 34.

    Wilson S, Vennervald BJ, Dunne DW, 2011. Chronic hepatosplenomegaly in African school children: a common but neglected morbidity associated with schistosomiasis and malaria. PLoS Negl Trop Dis 5: e1149.

    • Search Google Scholar
    • Export Citation
  • 35.

    Muok EM, Mwinzi PN, Black CL, Carter JM, Ng'ang'a ZW, Gicheru MM, Secor WE, Karanja DM, Colley DG, 2009. Short report: Childhood coinfections with Plasmodium falciparum and Schistosoma mansoni result in lower percentages of activated T cells and T regulatory memory cells than schistosomiasis only. Am J Trop Med Hyg 80: 475478.

    • Search Google Scholar
    • Export Citation
  • 36.

    Wilson S, Jones FM, Mwatha JK, Kimani G, Booth M, Kariuki HC, Vennervald BJ, Ouma JH, Muchiri E, Dunne DW, 2009. Hepatosplenomegaly associated with chronic malaria exposure: evidence for a pro-inflammatory mechanism exacerbated by schistosomiasis. Parasite Immunol 31: 6471.

    • Search Google Scholar
    • Export Citation
  • 37.

    Wilson S, Dunne DW, 2012. Advances in our understanding of the epidemiology of Plasmodium and schistosome infection: informing coinfection studies. Curr Opin HIV AIDS 7: 225230.

    • Search Google Scholar
    • Export Citation
  • 38.

    Ajanga A, Lwambo NJ, Blair L, Nyandindi U, Fenwick A, Brooker S, 2006. Schistosoma mansoni in pregnancy and associations with anaemia in northwest Tanzania. Trans R Soc Trop Med Hyg 100: 5963.

    • Search Google Scholar
    • Export Citation
  • 39.

    Brito LL, Barreto ML, Silva R de C, Assis AM, Reis MG, Parraga IM, Blanton RE, 2006. Moderate- and low-intensity co-infections by intestinal helminths and Schistosoma mansoni, dietary iron intake, and anemia in Brazilian children. Am J Trop Med Hyg 75: 939944.

    • Search Google Scholar
    • Export Citation
  • 40.

    Koukounari A, Fenwick A, Whawell S, Kabatereine NB, Kazibwe F, Tukahebwa EM, Stothard JR, Donnelly CA, Webster JP, 2006. Morbidity indicators of Schistosoma mansoni: relationship between infection and anemia in Ugandan schoolchildren before and after praziquantel and albendazole chemotherapy. Am J Trop Med Hyg 75: 278286.

    • Search Google Scholar
    • Export Citation
  • 41.

    Sowunmi A, 1996. Hepatomegaly in acute falciparum malaria in children. Trans R Soc Trop Med Hyg 90: 540542.

  • 42.

    Sowunmi A, Adedeji AA, Sowunmi CO, Falade CO, Falade AG, Ohaeri B, Happi TC, Oduola AM, 2001. Clinical characteristics and disposition kinetics of the hepatomegaly associated with acute, uncomplicated, Plasmodium falciparum malaria in children. Ann Trop Med Parasitol 95: 718.

    • Search Google Scholar
    • Export Citation
  • 43.

    Feikin DR, Laserson KF, Ojwando J, Nyambane G, Ssempijja V, Audi A, Nyakundi D, Oyieko J, Dallas MJ, Ciarlet M, Neuzil KM, Breiman RF, 2012. Efficacy of pentavalent rotavirus vaccine in a high HIV prevalence population in Kenya. Vaccine 30 (Suppl 1): A52A60.

    • Search Google Scholar
    • Export Citation
  • 44.

    Gong YY, Wilson S, Mwatha JK, Routledge MN, Castelino JM, Zhao B, Kimani G, Kariuki HC, Vennervald BJ, Dunne DW, Wild CP, 2012. Aflatoxin exposure may contribute to chronic hepatomegaly in Kenyan school children. Environ Health Perspect 120: 893896.

    • Search Google Scholar
    • Export Citation
  • 45.

    Vennervald BJ, Kenty L, Butterworth AE, Kariuki CH, Kadzo H, Ireri E, Amaganga C, Kimani G, Mwatha J, Otedo A, Booth M, Ouma JH, Dunne DW, 2004. Detailed clinical and ultrasound examination of children and adolescents in a Schistosoma mansoni endemic area in Kenya: hepatosplenic disease in the absence of portal fibrosis. Trop Med Int Health 9: 461470.

    • Search Google Scholar
    • Export Citation
  • 46.

    Kariuki HC, Mbugua G, Magak P, Bailey JA, Muchiri EM, Thiongo FW, King CH, Butterworth AE, Ouma JH, Blanton RE, 2001. Prevalence and familial aggregation of schistosomal liver morbidity in Kenya: evaluation by new ultrasound criteria. J Infect Dis 183: 960966.

    • Search Google Scholar
    • Export Citation
  • 47.

    Malenganisho WL, Magnussen P, Friis H, Siza J, Kaatano G, Temu M, Vennervald BJ, 2008. Schistosoma mansoni morbidity among adults in two villages along Lake Victoria shores in Mwanza District, Tanzania. Trans R Soc Trop Med Hyg 102: 532541.

    • Search Google Scholar
    • Export Citation
  • 48.

    Silva CC, Domingues AL, Lopes EP, Morais CN, Santos RB, Luna CF, Nader HB, Martins JR, 2011. Schistosomiasis mansoni: ultrasound-evaluated hepatic fibrosis and serum concentrations of hyaluronic acid. Ann Trop Med Parasitol 105: 233239.

    • Search Google Scholar
    • Export Citation
  • 49.

    El Scheich T, Hofer L, Kaatano G, Foya J, Odhiambo D, Igogote J, Lwambo N, Ekamp H, Karst K, Haussinger D, Richter J, 2012. Hepatosplenic morbidity due to Schistosoma mansoni in schoolchildren on Ukerewe Island, Tanzania. Parasitol Res 110: 25152520.

    • Search Google Scholar
    • Export Citation
  • 50.

    Zhou H, Watanabe C, Ohtsuka R, 2007. Impacts of dietary intake and helminth infection on diversity in growth among schoolchildren in rural south China: a four-year longitudinal study. Am J Hum Biol 19: 96106.

    • Search Google Scholar
    • Export Citation
  • 51.

    Assis AM, Prado MS, Barreto ML, Reis MG, Conceicao Pinheiro SM, Parraga IM, Blanton RE, 2004. Childhood stunting in northeast Brazil: the role of Schistosoma mansoni infection and inadequate dietary intake. Eur J Clin Nutr 58: 10221029.

    • Search Google Scholar
    • Export Citation
  • 52.

    Olds GR, King C, Hewlett J, Olveda R, Wu G, Ouma J, Peters P, McGarvey S, Odhiambo O, Koech D, Liu CY, Aligui G, Gachihi G, Kombe Y, Parraga I, Ramirez B, Whalen C, Horton RJ, Reeve P, 1999. Double-blind placebo-controlled study of concurrent administration of albendazole and praziquantel in schoolchildren with schistosomiasis and geohelminths. J Infect Dis 179: 9961003.

    • Search Google Scholar
    • Export Citation
  • 53.

    Walker AR, Walker BF, Richardson BD, Smit PJ, 1972. Running performance in South African Bantu children with schistosomiasis. Trop Geogr Med 24: 347352.

    • Search Google Scholar
    • Export Citation
  • 54.

    Bustinduy AL, Thomas CL, Fiutem JJ, Parraga IM, Mungai PL, Muchiri EM, Mutuku F, Kitron U, King CH, 2011. Measuring fitness of Kenyan children with polyparasitic infections using the 20-meter shuttle run test as a morbidity metric. PLoS Negl Trop Dis 5: e1213.

    • Search Google Scholar
    • Export Citation
  • 55.

    Muller I, Coulibaly JT, Furst T, Knopp S, Hattendorf J, Krauth SJ, Stete K, Righetti AA, Glinz D, Yao AK, Puhse U, N'Goran EK, Utzinger J, 2011. Effect of schistosomiasis and soil-transmitted helminth infections on physical fitness of school children in Cote d'Ivoire. PLoS Negl Trop Dis 5: e1239.

    • Search Google Scholar
    • Export Citation
  • 56.

    Parker M, 1992. Re-assessing disability: the impact of schistosomal infection on daily activities among women in Gezira Province, Sudan. Soc Sci Med 35: 877890.

    • Search Google Scholar
    • Export Citation
  • 57.

    Bowden A, Fox-Rushby JA, 2003. A systematic and critical review of the process of translation and adaptation of generic health-related quality of life measures in Africa, Asia, Eastern Europe, the Middle East, South America. Soc Sci Med 57: 12891306.

    • Search Google Scholar
    • Export Citation
  • 58.

    Ukwandu NC, Nmorsi OP, 2004. The perception, beliefs and practices toward genitourinary schistosomiasis by inhabitants of selected endemic areas (Edo/Delta States) in south-eastern Nigeria. Rev Inst Med Trop Sao Paulo 46: 209216.

    • Search Google Scholar
    • Export Citation
  • 59.

    Wagatsuma Y, Aryeetey ME, Nkrumah FK, Sack DA, Kojima S, 2003. Highly symptom-aware children were heavily infected with urinary schistosomiasis in southern Ghana. Cent Afr J Med 49: 1619.

    • Search Google Scholar
    • Export Citation
  • 60.

    Amazigo UO, Anago-Amanze CI, Okeibunor JC, 1997. Urinary schistosomiasis among school children in Nigeria: consequences of indigenous beliefs and water contact activities. J Biosoc Sci 29: 918.

    • Search Google Scholar
    • Export Citation
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Schistosoma mansoni Morbidity among School-Aged Children: A SCORE Project in Kenya

Aaron M. SamuelsDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Elizabeth MateyDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Pauline N. M. MwinziDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Ryan E. WiegandDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Geoffrey MuchiriDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Edmund IreriDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Molly HydeDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Susan P. MontgomeryDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Diana M. S. KaranjaDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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W. Evan SecorDivision of Parasitic Diseases and Malaria, Centers for Disease Control and Prevention, Atlanta, Georgia; Center for Global Health Research, Kenya Medical Research Institute, Kisumu, Kenya

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Schistosomiasis control programs aim to reduce morbidity but are evaluated by infection prevalence and intensity reduction. We present baseline cross-sectional data from a nested cohort study comparing indicators of morbidity for measuring program impact. Eight hundred twenty-two schoolchildren 7–8 years of age from Nyanza Province, Kenya, contributed stool for diagnosis of Schistosoma mansoni and soil-transmitted helminths (STH) and blood smears for malaria, and were evaluated for anemia, quality of life, exercise tolerance, anthropometry, and ultrasound abnormalities. Schistosoma mansoni, STH, and malaria infection prevalence were 69%, 25%, and 8%, respectively. Only anemia and S. mansoni infection (adjusted odds ratio [aOR] = 1.70; confidence interval [CI] = 1.03–2.80), and hepatomegaly and heavy S. mansoni infection (aOR = 2.21; CI = 1.19–4.11) were associated. Though anemia and hepatomegaly appeared most useful at baseline, additional morbidity indicators may be sensitive longitudinal measures to evaluate schistosomiasis program health impact.

Author Notes

* Address correspondence to Aaron M. Samuels, Centers for Disease Control and Prevention, 1600 Clifton Rd NE, MS A06, Atlanta, GA 30329. E-mail: iyp2@cdc.gov

Financial support: This study received financial support from the University of Georgia Research Foundation, Inc., which is funded by the Bill and Melinda Gates Foundation for this SCORE project.

Disclosure: This work is published with the permission of the Director, Kenya Medical Research Institute. The findings and conclusions of this work are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Authors' addresses: Aaron M. Samuels, Ryan E. Wiegand, Molly Hyde, Susan P. Montgomery, and W. Evan Secor, Centers for Disease Control and Prevention, Atlanta, GA, E-mails: IYP2@cdc.gov, FWK2@cdc.gov, Molly1013@hotmail.com, ZQU6@cdc.gov, and WAS4@cdc.gov. Elizabeth Matey, Pauline N. M. Mwinzi, Geoffrey Muchiri, Edmund Ireri, and Diana M. S. Karanja, Kenya Medical Research Institute, Kisumu, Kenya, E-mails: Ematey@kemricdc.org, PMwinzi@kemricdc.org, Geoffmosh@yahoo.com, Eikareko@hotmail.com, and DKaranja@kemricdc.org.

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