Volume 98, Issue 4
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Case reports and pathology series suggest associations of female genital schistosomiasis () with infertility and ectopic pregnancy. Differential geographic distribution of infertility is not explained by analyses of known risk factors. In this cross-sectional multilevel semi-ecologic study, interpolated prevalence maps for and in East Africa were created using data from two open-access Neglected Tropical Diseases Databases. Prevalence was extracted to georeferenced survey sample points for Demographic and Health Surveys for Ethiopia, Kenya, Tanzania, and Uganda for 2000 and 2010. Exploratory spatial analyses showed that infertility was not spatially random and mapped the clustering of infertility and its co-location with schistosomiasis. Multilevel logistic regression analysis demonstrated that women living in high compared with absent locations had significantly higher odds of infertility (2000 odds ratio [OR] = 1.5 [confidence interval = 1.3, 1.8]; 2010 OR = 1.2 [1.1, 1.5]). Women in high compared with high locations had significantly higher odds of infertility (2000 OR 1.4 [1.1, 1.9]; 2010 OR 1.4 [1.1, 1.8]). Living in high compared with absent locations did not affect the odds of infertility. Infertility appears to be associated spatially with .


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  1. Friedman JF, Mital P, Kanzaria HK, Olds GR, Kurtis JD, , 2007. Schistosomiasis and pregnancy. Trends Parasitol 23: 159164.
  2. Salawu OT, Odaibo AB, , 2014. Maternal schistosomiasis: a growing concern in sub-Saharan Africa. Pathog Glob Health 108: 263270.
  3. Christinet V, Lazdins-Helds JK, Stothard JR, Reinhard-Rupp J, , 2016. Female genital schistosomiasis (FGS): from case reports to a call for concerted action against this neglected gynaecological disease. Int J Parasitol 46: 395404.
  4. Hotez PJ, Fenwick A, , 2009. Schistosomiasis in Africa: an emerging tragedy in our new global health decade. PLoS Negl Trop Dis 3: e485.
  5. Colley DG, Bustinduy AL, Secor WE, King CH, , 2014. Human schistosomiasis. Lancet 383: 22532264.
  6. Abdel-Malek E, , 1958. Factors conditioning the habitat of bilharziasis intermediate hosts of the family Planorbidae. Bull World Health Organ 18: 785818.
  7. van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, Habbema JD, Engels D, , 2003. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop 86: 125139.
  8. King CH, Dangerfield-Cha M, , 2008. The unacknowledged impact of chronic schistosomiasis. Chronic Illn 4: 6579.
  9. Poggensee G, Feldmeier H, , 2001. Female genital schistosomiasis: facts and hypotheses. Acta Trop 79: 193210.
  10. Leutscher P, Raharisolo C, Pecarrere JL, Ravaoalimalala VE, Serieye J, Rasendramino M, Vennervald B, Feldmeier H, Esterre P, , 1997. Schistosoma haematobium induced lesions in the female genital tract in a village in Madagascar. Acta Trop 66: 2733.
  11. Hegertun IE, Sulheim Gundersen KM, Kleppa E, Zulu SG, Gundersen SG, Taylor M, Kvalsvig JD, Kjetland EF, , 2013. S. haematobium as a common cause of genital morbidity in girls: a cross-sectional study of children in South Africa. PLoS Negl Trop Dis 7: e2104.
  12. Kjetland EF, Mduluza T, Ndhlovu PD, Gomo E, Gwanzura L, Midzi N, Mason PR, Friis H, Gundersen SG, , 2006. Genital schistosomiasis in women: a clinical 12-month in vivo study following treatment with praziquantel. Trans R Soc Trop Med Hyg 100: 740752.
  13. Cui W, , 2010. Mother or nothing: the agony of infertility. Bull World Health Organ 88: 881882.
  14. Rutstein SO, Shah IH, , 2004. Infecundity, Infertility, and Childlessness in Developing Countries. DHS Comparative Reports 9. Available at: http://www.who.int/reproductivehealth/topics/infertility/DHS-CR9.pdf.
  15. Mascarenhas MN, Flaxman SR, Boerma T, Vanderpoel S, Stevens GA, , 2012. National, regional, and global trends in infertility prevalence since 1990: a systematic analysis of 277 health surveys. PLoS Med 9: e1001356.
  16. Cates W, Farley TM, Rowe PJ, , 1985. Worldwide patterns of infertility: is Africa different? Lancet 2: 596598.
  17. Mayaud P, , 2001. The role of reproductive tract infections. Boerma J, Mgalla Z, eds. Women and Infertility in Sub-Saharan Africa: A Multidisciplinary Perspective. Amsterdam, The Netherlands: Royal Tropical Institute, 71–107.
  18. Larsen U, , 2000. Primary and secondary infertility in sub-Saharan Africa. Int J Epidemiol 29: 285291.
  19. Ericksen K, Brunette T, , 1996. Patterns and predictors of infertility among African women: a cross-national survey of twenty-seven nations. Soc Sci Med 42: 209220.
  20. Tesfaghiorghis H, , 1991. Infecundity and subfertility among the rural population of Ethiopia. J Biosoc Sci 23: 461475.
  21. Romaniuk A, , 1968. Infertility in tropical Africa. Caldwell JC, Okonjo C, eds. The Population of Tropical Africa. New York, NY: Columbia University Press, 214–224.
  22. Olack B, Cosmas L, Mogeni D, Montgomery J, , 2014. Causes of mortality in women of reproductive age living in an urban slum (Kibera) in Nairobi American Society of Tropical Medicine and Hygiene Annual Meeting. Abstract #1869.
  23. Amoko DH, Buga GA, , 1995. Clinical presentation of ectopic pregnancy in Transkei, South Africa. East Afr Med J 72: 770773.
  24. Lindow SW, Moore PJ, , 1988. Ectopic pregnancy: analysis of 100 cases. Int J Gynaecol Obstet 27: 371375.
  25. Kjetland EF, Kurewa EN, Mduluza T, Midzi N, Gomo E, Friis H, Gundersen SG, Ndhlovu PD, , 2010. The first community-based report on the effect of genital Schistosoma haematobium infection on female fertility. Fertil Steril 94: 15511553.
  26. Miller-Fellows SC, Howard L, Kramer R, Hildebrand V, Furin J, Mutuku FM, Mukoko D, Ivy JA, King CH, . Cross-sectional interview study of fertility, pregnancy, and urogenital schistosomiasis in coastal Kenya: documented treatment in childhood is associated with reduced odds of subfertility among adult women. PLoS Negl Trop Dis 11: e0006101.
  27. Hurlimann E, 2011. Toward an open-access global database for mapping, control, and surveillance of neglected tropical diseases. PLoS Negl Trop Dis 5: e1404.
  28. Brooker S, Hotez PJ, Bundy DAP, , 2010. The global atlas of helminth infection: mapping the way forward in neglected tropical disease control. PLoS Negl Trop Dis 4: e779.
  29. Flueckiger RM, 2015. Integrating data and resources on neglected tropical diseases for better planning: the NTD mapping tool ( NTDmap.org ). PLoS Negl Trop Dis 9: e0003400.
  30. Doumenge J, Mott K, Cheung C, Villenave D, Chapuis O, , eds., 1987. Atlas of the Global Distribution of Schistosomiasis. Geneva, Switzerland: World Health Organization. Available at: http://www.who.int/schistosomiasis/epidemiology/Global_atlas_toc.pdf?ua=1.
  31. Brooker S, , 2007. Spatial epidemiology of human schistosomiasis in Africa: risk models, transmission dynamics and control. Trans R Soc Trop Med Hyg 101: 18.
  32. Simoonga C, Utzinger J, Brooker S, Vounatsou P, Appleton CC, Stensgaard AS, Olsen A, Kristensen TK, , 2009. Remote sensing, geographical information system and spatial analysis for schistosomiasis epidemiology and ecology in Africa. Parasitology 136: 16831693.
  33. Schur N, Hürlimann E, Stensgaard AS, Chimfwembe K, Mushinge G, Simoonga C, Kabatereine NB, Kristensen TK, Utzinger J, Vounatsou P, , 2013. Spatially explicit Schistosoma infection risk in eastern Africa using Bayesian geostatistical modelling. Acta Trop 128: 365377.
  34. Measure DHS, ed., 2012. Survey Organization Manual for Demographic and Health Surveys. Calverton, MD: ICF International. Available at: https://dhsprogram.com/pubs/pdf/DHSM10/DHS6_Survey_Org_Manual_7Dec2012_DHSM10.pdf.
  35. Measure DHS, ed., 2012. Demographic and Health Survey Sampling and Household Listing Manual. Calverton, MD: ICF International. Available at: https://dhsprogram.com/pubs/pdf/DHSM4/DHS6_Sampling_Manual_Sept2012_DHSM4.pdf.
  36. Perez-Heydrich C, Warren J, Burgert C, Emch M, , eds., 2013. Guidelines on the Use of DHS GPS Data. Spatial Analysis Reports No. 8. Calverton, MD: ICF International. Available at: https://dhsprogram.com/pubs/pdf/SAR8/SAR8.pdf.
  37. Larsen U, Menken J, , 1991. Individual-level sterility: a new method of estimation with application to sub-Saharan Africa. Demography 28: 229247.
  38. Mascarenhas MN, Cheung H, Mathers CD, Stevens GA, , 2012. Measuring infertility in populations: constructing a standard definition for use with demographic and reproductive health surveys. Popul Health Metr 10: 17.
  39. Anselin L, Syabri I, Kho Y, , 2006. GeoDa: an introduction to spatial data analysis. Geogr Anal 38: 5.
  40. Burgert CR, Bradley SEK, Arnold F, Eckert E, , 2014. Improving estimates of insecticide-treated mosquito net coverage from household surveys: using geographic coordinates to account for endemicity. Malar J 13: 254.
  41. Curtis S, Hossain M, , eds., 1998. West Africa Spatial Analysis Prototype Exploratory Analysis: The Effect of Aridity on Child Nutritional Status. DHS Spatial Analysis Reports No. 2. Calverton, MD: Macro International. Available at: https://dhsprogram.com/pubs/pdf/SAR2/GIS2.pdf.
  42. Burgert C, , ed., 2014. Spatial Interpolation with Demographic and Health Survey Data: Key Considerations. DHS Spatial Analysis Reports No. 9. Rockville, MD: ICF International. Available at: http://www.gbv.de/dms/zbw/821367854.pdf.
  43. Gething P, Tatem A, Bird T, Burgert-Brucker C, , eds., 2015. Creating Spatial Interpolation Surfaces with DHS Data. DHS Spatial Analysis Reports No. 11. Rockville, MD: ICF International. Available at: https://dhsprogram.com/pubs/pdf/SAR11/SAR11.pdf.
  44. Tchuem Tchuente L, Rollinson D, Stothard JR, Molyneux D, , 2017. Moving from control to elimination of schistosomiasis in sub-Saharan Africa: time to change and adapt strategies. Infect Dis Poverty 6: 42.
  45. Gurunath S, Pandian Z, Anderson RA, Bhattacharya S, , 2011. Defining infertility—a systematic review of prevalence studies. Hum Reprod Update 17: 575588.
  46. Menken J, Larsen U, , 1994. Estimating the incidence and prevalence and analyzing the correlates of infertility and sterility. Ann N Y Acad Sci 709: 249265.
  47. Haws RA, Mashasi I, Mrisho M, Schellenberg JA, Darmstadt GL, Winch PJ, , 2010. “These are not good things for other people to know”: how rural Tanzanian women’s experiences of pregnancy loss and early neonatal death may impact survey data quality. Soc Sci Med 71: 17641772.
  48. Feldmeier H, Leutscher P, Poggensee G, Harms G, , 1999. Male genital schistosomiasis and haemospermia. Trop Med Int Health 4: 791793.

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  • Received : 05 Apr 2017
  • Accepted : 20 Nov 2017

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