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Zotero
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Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, Gwanzura L, Mason PR, Sandvik L, Friis H, Gundersen SG, 2006. Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS 20: 593–600.
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Dhana A, Luchters S, Moore L, Lafort Y, Roy A, Scorgie F, Chersich M, 2014. Systematic review of facility-based sexual and reproductive health services for female sex workers in Africa. Glob Health 10: 46.
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Urogenital Schistosomiasis and Sexually Transmitted Coinfections among Pregnant Women in a Schistosome-Endemic Region of the Democratic Republic of Congo
Adva Gadoth
Adva Gadoth
Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California;
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Gisèle Mvumbi
Gisèle Mvumbi
Kinshasa School of Public Health, Kinshasa, Democratic Republic of the Congo;
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Nicole A. Hoff
Nicole A. Hoff
Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California;
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Kamy Musene
Kamy Musene
Kinshasa School of Public Health, Kinshasa, Democratic Republic of the Congo;
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Patrick Mukadi
Patrick Mukadi
National Institute for Biomedical Research, Kinshasa, Democratic Republic of the Congo;
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Hayley R. Ashbaugh
Hayley R. Ashbaugh
Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California;
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Reena H. Doshi
Reena H. Doshi
Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California;
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Marjan Javanbakht
Marjan Javanbakht
Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California;
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Pamina Gorbach
Pamina Gorbach
Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California;
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Emile Okitolonda-Wemakoy
Emile Okitolonda-Wemakoy
Kinshasa School of Public Health, Kinshasa, Democratic Republic of the Congo;
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Jeffrey D. Klausner
Jeffrey D. Klausner
Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California;
Department of Medicine, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California
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Anne W. Rimoin
Anne W. Rimoin
Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, California;
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Schistosomiasis afflicts an estimated 10 million pregnant women in Africa annually. With mounting evidence of adverse impacts to reproductive health resulting from urogenital schistosomiasis, including increased transmission of HIV, further research on prenatal disease epidemiology is warranted, with implications for maternal and fetal health. Between October 2016 and March 2017, we conducted a cross-sectional study examining the prevalence of urogenital schistosomiasis and its association with sexually transmitted infections (STIs) other than HIV among pregnant women visiting antenatal clinics in Kisantu health zone, Democratic Republic of Congo. An extensive sociodemographic and clinical survey was administered to consenting participants, with urine samples and vaginal swabs collected to deduce active schistosomiasis and STIs, respectively. In total, 17.4% of expectant mothers were infected with Schistosoma haematobium, 3.1% with Chlamydia trachomatis (CT), 1.4% with Neisseria gonorrhoeae (NG), and 14.6% with Trichomonas vaginalis (TV). Women infected with urogenital schistosomiasis were at significantly increased odds of harboring a CT, NG, or TV infection (adjusted odds ratio = 3.0, 95% CI: 1.5, 6.0), but reports of clinical symptoms were low, ranging from 17.2% of schistosomiasis to 30.8% of TV cases. Laboratory confirmation of schistosomiasis and STIs provided objective evidence of disease in a cohort with low symptomology where syndromic management may not suffice. Shedding light on local risk factors and associated coinfections of urogenital schistosomiasis can identify unique intervention opportunities for prenatal care in trematode-endemic regions and aid in reducing adverse pregnancy outcomes.
Author Notes
Financial support: This study was funded by a seed grant from the UCLA Center for AIDS Research (ref. 5P30 AI028697), a grant from the National Center for Advancing Translational Sciences at the National Institutes of Health (NIH-NCATS; ref. UL1TR000124), and the Faucett Catalyst Fund.
Authors’ addresses: Adva Gadoth, Nicole A. Hoff, Hayley R. Ashbaugh, Reena H. Doshi, Marjan Javanbakht, Pamina Gorbach, and Anne W. Rimoin, Department of Epidemiology, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, CA, E-mails: advag@ucla.edu, nhoff84@ucla.edu, hashbaugh@ucla.edu, reenahdoshi@gmail.com, javan@g.ucla.edu, pgorbach@ucla.edu, and arimoin@ucla.edu. Gisèle Mvumbi and Kamy Musene, Kinshasa School of Public Health, Kinshasa, Democratic Republic of the Congo, E-mails: mvumbig@gmail.com and kamymusene@yahoo.fr. Patrick Mukadi, National Institute for Biomedical Research, Kinshasa, Democratic Republic of the Congo, E-mail: patrickmukadi@gmail.com. Emile Okitolonda-Wemakoy, Center for HIV/AIDS Strategic Information, University of Kinshasa, Kinshasa, Democratic Republic of the Congo, E-mail: okitow@yahoo.fr. Jeffrey D. Klausner, Department of Medicine, Jonathan and Karin Fielding School of Public Health, University of California Los Angeles, Los Angeles, CA, E-mail: jdklausner@mednet.ucla.edu.
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BibTeX
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EndNote
-
1.
Hotez PJ, Kamath A, 2009. Neglected tropical diseases in sub-Saharan Africa: review of their prevalence, distribution, and disease burden. Plos Negl Trop Dis 3: e412.
-
2.
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-
3.
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-
4.
Gray DJ, Ross AG, Li YS, McManus DP, 2011. Diagnosis and management of schistosomiasis. BMJ 342: d2651.
-
5.
Hotez PJ, 2013. Female genital schistosomiasis (FGS): sub-Saharan Africa’s secret scourge of girls and women. PLoS Speaking of Medicine. Available at: https://blogs.plos.org/speakingofmedicine/2013/05/06/female-genital-schistosomiasis-fgs-sub-saharan-africas-secret-scourge-of-girls-and-women/. Accessed December 5, 2018.
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6.
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7.
Gallagher M, Malhotra I, Mungai PL, Wamachi AN, Kioko JM, Ouma JH, Muchiri E, King CL, 2005. The effects of maternal helminth and malaria infections on mother-to-child HIV transmission. AIDS 19: 1849–1855.
-
8.
Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, Gwanzura L, Mason PR, Sandvik L, Friis H, Gundersen SG, 2006. Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS 20: 593–600.
-
9.
Poggensee G, Kiwelu I, Weger V, Göppner D, Diedrich T, Krantz I, Feldmeier H, 2000. Female genital schistosomiasis of the lower genital tract: prevalence and disease-associated morbidity in northern Tanzania. J Infect Dis 181: 1210–1213.
-
10.
Salgame P, Yap GS, Gause WC, 2013. Effect of helminth-induced immunity on infections with microbial pathogens. Nat Immunol 14: 1118–1126.
-
11.
Ministère du Plan et Suivi de la Mise en œuvre de la Révolution de la Modernité–MPSMRM/Congo, Ministère de la Santé Publique–MSP/Congo, and ICF International, 2014. République Démocratique du Congo Enquête Démographique et de Santé (EDS-RDC) 2013–2014. Rockville, MD: MPSMRM, MSP, and ICF International.
-
12.
Leutscher PDC, Ramarokoto C-E, Hoffmann S, Jensen JS, Ramaniraka V, Randrianasolo B, Raharisolo C, Migliani R, Christensen N, 2008. Coexistence of urogenital schistosomiasis and sexually transmitted infection in women and men living in an area where Schistosoma haematobium is endemic. Clin Infect Dis 47: 775–782.
-
13.
Friedman JF, Mital P, Kanzaria HK, Olds GR, Kurtis JD, 2007. Schistosomiasis and pregnancy. Trends Parasitol 23: 159–164.
-
14.
el-Nahal HM, Kaddah MA, Hassan SI, Abdel Ghany A, Ibrahim AM, Ramzy RM, Mostafa EA, 1998. Effect of Schistosoma mansoni infection on offsprings born from infected mothers. J Egypt Soc Parasitol 28: 523–538.
-
15.
Amano T, Freeman GL Jr., Colley DG, 1990. Reduced reproductive efficiency in mice with schistosomiasis mansoni and in uninfected pregnant mice injected with antibodies against Schistosoma mansoni soluble egg antigens. Am J Trop Med Hyg 43: 180–185.
-
16.
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: 395–404.
-
17.
Randrianasolo BS et al. 2015. Gynecological manifestations, histopathological findings, and schistosoma-specific polymerase chain reaction results among women with Schistosoma haematobium infection: a cross-sectional study in Madagascar. J Infect Dis 212: 275–284.
-
18.
Nash TE, Cheever AW, Ottesen EA, Cook JA, 1982. Schistosome infections in humans: perspectives and recent findings. NIH conference. Ann Intern Med 97: 740–754.
-
19.
Malhotra I, Mungai P, Wamachi A, Kioko J, Ouma JH, Kazura JW, King CL, 1999. Helminth- and Bacillus Calmette-Guerin-induced immunity in children sensitized in utero to filariasis and schistosomiasis. J Immunol 162: 6843–6848.
-
20.
Ndibazza J et al. 2012. Impact of anthelminthic treatment in pregnancy and childhood on immunisations, infections and eczema in childhood: a randomised controlled trial. PLoS One 7: e50325.
-
21.
Sutton MY, Sternberg M, Nsuami M, Behets F, Nelson AM, St Louis ME, 1999. Trichomoniasis in pregnant human immunodeficiency virus-infected and human immunodeficiency virus-uninfected congolese women: prevalence, risk factors, and association with low birth weight. Am J Obstet Gynecol 181: 656–662.
-
22.
Mullick S, Watson-Jones D, Beksinska M, Mabey D, 2005. Sexually transmitted infections in pregnancy: prevalence, impact on pregnancy outcomes, and approach to treatment in developing countries. Sex Transm Infect 81: 294–302.
-
23.
Dhana A, Luchters S, Moore L, Lafort Y, Roy A, Scorgie F, Chersich M, 2014. Systematic review of facility-based sexual and reproductive health services for female sex workers in Africa. Glob Health 10: 46.
-
24.
Mayaud P, Mabey D, 2004. Approaches to the control of sexually transmitted infections in developing countries: old problems and modern challenges. Sex Transm Infect 80: 174–182.
-
25.
Esri, 2009. World Imagery Map [Basemap]. Available at: http://www.arcgis.com/home/item.html?id=10df2279f9684e4a9f6a7f08febac2a9. Accessed April 6, 2018.
-
26.
World Resources Institute, 2013. Congo Basin Forest Atlases: DRC. Available at: http://www.wri.org/our-work/project/congo-basin-forests/democratic-republic-congo#project-tabs. Accessed April 6, 2018.
-
27.
American Red Cross, 2019. DRC Health Data. Available at: https://data.humdata.org/dataset/drc-health-data. Accessed January 30, 2019.
-
28.
Corcoran C, da Silva M, 2014. Diagnosing schistosomiasis: an update. PATHCHAT11. Available at: https://www.ampath.co.za/pdfs/ampathchats/pathchat-11-diagnosing-schistosomiasis-an-update.pdf. Accessed May 15, 2019.
-
29.
World Health Organization Coordinated, 2006. Use of Anthelminthic Drugs in Control Interventions-A Manual for Health Professionals and Programme Managers. Geneva, Switzerland: WHO.
-
30.
World Health Organization, 2016. WHO Guidelines for the Treatment of Chlamydia trachomatis. Geneva, Switzerland: WHO.
-
31.
World Health Organization, 2016. WHO Guidelines for the Treatment of Neisseria Gonorrhoeae. Geneva, Switzerland: WHO.
-
32.
Walker G, 2004. Interventions for Trichomoniasis in Pregnancy. Geneva, Switzerland: The WHO Reproductive Health Library.
-
33.
van Liere GAFSV, Dukers-Muijrers NHTM, Wolffs PFG, Hoebe CJPA, 2013. P3. 186. Substantial natural clearance of genital and extragenital Chlamydia trachomatis and Neisseria gonorrhoeae in STD clinic attendees. Sex Transm Infect 89: A206.
-
34.
Kjetland EF et al. 2008. Female genital schistosomiasis—a differential diagnosis to sexually transmitted disease: genital itch and vaginal discharge as indicators of genital Schistosoma haematobium morbidity in a cross-sectional study in endemic rural Zimbabwe. Trop Med Int Health 13: 1509–1517.
-
35.
Yirenya-Tawiah D, Annang TN, Apea-Kubi KA, Lomo G, Mensah D, Akyeh L, Bosompem KM, 2014. Chlamydia trachomatis and Neisseria Gonorrhoeae prevalence among women of reproductive age living in urogenital schistosomiasis endemic area in Ghana. BMC Res Notes 7: 349.
-
36.
World Health Organization, 2018. Fact Sheet: Schistosomiasis. Available from: https://www.who.int/news-room/fact-sheets/detail/schistosomiasis. Accessed December 20, 2018.
-
37.
Colley DG, Bustinduy AL, Secor WE, King CH, 2014. Human schistosomiasis. Lancet 383: 2253–2264.
-
38.
FAO, 2010. Crop Calendar: Democratic Republic of the Congo. Available from: http://www.fao.org/agriculture/seed/cropcalendar/searchbycountry.do. Accessed January 8, 2018.
-
39.
Behets FM, Matendo R, Vaz LM, Kilese N, Nanlele D, Kokolomami J, Okitolando EW, Van Rie A, 2006. Preventing vertical transmission of HIV in Kinshasa, Democratic Republic of the Congo: a baseline survey of 18 antenatal clinics. Bull World Health Organ 84: 969–975.
-
40.
World Health Organization, 2007. Global Strategy for the Prevention and Control of Sexually Transmitted Infections: 2006–2015. Geneva, Switzerland: WHO.
-
41.
Romoren M, Sundby J, Velauthapillai M, Rahman M, Klouman E, Hjortdahl P, 2007. Chlamydia and gonorrhoea in pregnant Batswana women: time to discard the syndromic approach? BMC Infect Dis 7: 27.
-
42.
Romoren M, Velauthapillai M, Rahman M, Sundby J, Klouman E, Hjortdahl P, 2007. Trichomoniasis and bacterial vaginosis in pregnancy: inadequately managed with the syndromic approach. Bull World Health Organ 85: 297–304.
-
43.
King CH, Bertsch D, 2013. Meta-analysis of urine heme dipstick diagnosis of Schistosoma haematobium infection, including low-prevalence and previously-treated populations. Plos Negl Trop Dis 7: e2431.
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