https://orcid.org/0000-0002-6122-6359
Figures
Abstract
Schistosoma haematobium, the parasite that causes urogenital schistosomiasis, is widely prevalent in Tanzania. In addition to well-known effects on the urinary tract, S. haematobium also causes clinically- evident damage to the reproductive tract in approximately half of infected women, which is known as female genital schistosomiasis (FGS). FGS has major gynecologic and social consequences on women’s reproductive health, yet little information is available regarding FGS in Tanzania. To cover that gap, we conducted the present scoping review to examine the epidemiology of FGS in Tanzania (both in the mainland and Zanzibar island) and to make recommendations for future work in this area. The available evidence from community-based and hospital-based retrospective studies indicates that FGS is a significant health problem in the country. Very few community-based studies have been reported from mainland Tanzania, and Zanzibar. Our review highlights the scarcity of efforts to address FGS in Tanzania and the need for additional community-based studies. The studies will help us understand the true burden of the disease nationwide, to assess the impact of praziquantel on FGS lesions, and to address social and mental health in relation to FGS. This review emphasizes integration of delivery of FGS related services in primary health care systems through the reproductive health clinics which covers sexually transmitted infections, HIV and cervical cancer screening. These actions are essential if this neglected gynecological disease is to be addressed in Tanzania.
Author summary
Female genital schistosomiasis (FGS) caused by Schistosoma haematobium affects mostly the reproductive tract of girls and women in rural and marginalized communities. This disease has been largely neglected by the schistosomiasis endemic communities and public health professionals. The present review aimed at assessing the evidence/epidemiology of FGS among women/girls in Tanzania.
Furthermore, the review assessed the availability of information, published literature on FGS including comorbidities that address FGS in Tanzania mainland and Zanzibar islands. The evidence generated was important to inform the need to address FGS key gaps among researchers, healthcare workers and communities. Overall, the findings indicated that the knowledge of FGS was lacking among the endemic communities and healthcare workers. Findings from this review have shown the available gaps in literature on FGS in Tanzania, from very few community-and-hospitals based studies reported from mainland Tanzania, and Zanzibar. To address this gap, further research is essential to understanding the true burden of disease-associated morbidity, to assessing the impact of single dose praziquantel in FGS lesions, to understanding mental health in relation to FGS, and to integrating delivery of FGS related services in primary health care systems.
Citation: Mbwanji G, Mazigo HD, Maganga JK, Downs JA (2024) Female genital schistosomiasis is a neglected public health problem in Tanzania: Evidence from a scoping review. PLoS Negl Trop Dis 18(3): e0011954. https://doi.org/10.1371/journal.pntd.0011954
Editor: Uwem Friday Ekpo, Federal University of Agriculture Abeokuta, NIGERIA
Received: July 27, 2023; Accepted: January 31, 2024; Published: March 11, 2024
Copyright: © 2024 Mbwanji et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All data are in the manuscript and/or supporting information files.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Schistosomiasis is prevalent in tropical and subtropical areas, especially in poor communities with limited access to potable water or adequate sanitation [1]. The infection is common in rural and underdeveloped urban areas where communities rely on open surface water sources such as rivers, streams and lakes for work or daily chores [2]. It is estimated that >250 million people require preventive treatment for schistosomiasis worldwide and over 90% of these live in Africa [3,4]. In sub- Saharan Africa, two species of schistosomes are highly prevalent: Schistosoma mansoni that causes intestinal schistosomiasis and Schistosoma haematobium that causes urogenital schistosomiasis [1]. Approximately two-thirds of cases on the African continent are caused by S. haematobium [5]. Urogenital schistosomiasis can occur in both men and women [6]; however, the current review will focus on S. haematobium infections in women given the greater morbidity associated with female genital schistosomiasis (FGS), including associations with HIV infection and infertility [7]. At present, FGS is one of the most prevalent but also underrecognized gynecological conditions in Africa, affecting roughly 56 million girls and women [8,9].
For over 120 years, S. haematobium has been known to cause pathology of the urinary and genital tracts in women, with eggs of the parasites reported in vaginal tissues in Egypt in 1899 [10]. Diagnosis of FGS is challenging due to the lack of a simple test specific to the genital tract [11,12]. It is estimated that 33% to 75% of the women living in schistosomiasis endemic areas have FGS [7].
Women actively excreting S. haematobium eggs in the urine also have the parasite eggs in their uterine cervix, vagina or vulva [13,14]. At the same time, even in the absence of urinary ova excretion in women, 23%–41% of those with S. haematobium infection are found to have genital schistosomiasis [7]. Further complicating the diagnosis of FGS, women with S. haematobium infection do not excrete as many eggs for a given worm burden as do men with S. haematobium [10].
FGS has been implicated as a major cofactor in the poor reproductive health of many women in Africa. It can cause infertility, menstrual and pregnancy complications, genital lesions, pain and bleeding from intercourse, anaemia, genital itching, and genital discharge [15]. On a macroscopic level, FGS has been associated with genital mucosal changes, such as sandy patches and pathological blood vessels [16,17] as well as with genital immunological changes [17,18] that may increase women’s susceptibility to infections such as HIV.
After Nigeria, Tanzania ranks second-highest in schistosome infections in Africa, with a national prevalence ranging between 12–87% [19]. S. haematobium, which comprises two-thirds of Tanzanian cases, is endemic throughout the country but its transmission is focalized and heterogeneous in nature [5,20–22]. A high prevalence has been repeatedly documented among school aged children using detection of eggs in urine [21]. The parasite has been studied less frequently among women of reproductive age, and studies of FGS in Tanzania are limited. Even less programmatic data is not available to guide local and regional policy. As a result, control program managers and policy makers do not have data to inform them where the FGS burden is greatest, which populations are most affected, and where and how to implement the highest-yield interventions. To address this gap, the present work reviews the available published articles on FGS throughout Tanzania and provides summaries of the key findings and geographical areas where the study was conducted. Studies that address the overlap of FGS with other reproductive health issues are included.
Methods
1. Study design and research question
We conducted a review of literature to address two key research questions: Is there evidence of female genital schistosomiasis in Tanzania, and what is known about FGS from studies conducted in Tanzania?
A scoping review was conducted in order to systematically map the research done in the country, as well as to identify any existing gaps in knowledge. We sought to consider these research questions from a public health perspective in order to guide policy makers in Tanzania.
2. Search strategy
To identify potentially relevant papers a full systematic electronic search of literature on PubMed and Google Scholar were used to compile a list of English language papers. It was carried out using predefined search terms for subject headings and text words. In addition, Boolean operators, Medical Subject Heading (MeSH) and non- MeSH terms were also used under the following themes: Epidemiology, AND female genital schistosomiasis, AND comorbidities AND neglected tropical diseases AND Tanzania or Zanzibar. Search terms for subject headings and for text words were developed for four (4) search elements: FGS, comorbidities, epidemiology, and Tanzania. The search terms used for PubMed and Google scholar to identify FGS in Tanzania are provided in S1 Table.
These searches were limited to peer reviewed articles published between 1981 and June 2022 and to studies conducted in human participants only. This systematic approach was done to minimize bias and random errors. Masters and PhD theses available from institutional websites and libraries were not included in this search. All data searches were performed by 4 independent authors (GCM, HDM, JKM, JD). Duplicate citations from the multiple databases were removed.
3. Eligibility screening
After the searches were carried out, peer reviewed papers meeting the eligibility criteria were applied by two reviewers (GCM, JKM). Search results were screened using pre-defined criteria, conforming to the Population/Participants, Interventions/exposures, Comparison, Outcome, Setting/Study design (PICOS) framework [23]. Title and abstracts of all search results were screened for eligibility by the reviewers based on prespecified eligibility criteria (S2 Table). Articles that did not meet inclusion criteria were excluded. Studies published in non-English languages were excluded. Quantitative, and qualitative studies were included in order to consider different aspects of measuring female genital schistosomiasis burden.
4. Data extraction method
Data were extracted by two authors (GCM, JD) using a standardized extraction form. Extracted data included: publication details, study setting, study design, study population, evaluated outcomes, results and findings, and authors’ conclusions (S3 Table). Tabulated results data were independently extracted by the two reviewers (GCM, HDM), discussed the results and continued charting the results in the data charting form.
5. Quality assessment
The in-depth demonstration of the burden of FGS in Tanzania is lacking. To reduce the risk of bias in the eligible studies, a quality assessment was carried out using a risk of bias tool for observational data and classifying each domain into low, high or unclear risk of bias. Five domains were considered: Selection bias, missing data, misclassification of outcome, misclassification of exposures, confounding and statistical analysis approach (S4 Table).
Results
Of 6,140 records identified from the PubMed and google scholar databases (S1 Table), only 20 papers met the eligibility criteria and were therefore included in this review as shown in Fig 1. Of the 20 papers included in the review we grouped articles as community based epidemiologic studies, hospital based histopathologic studies, case reports, FGS diagnostic studies and qualitative studies as shown in Table 1 below.
Community based studies
Community-based studies conducted in northern Tanzania [13,14,31,35,36,39] have revealed that FGS is a public health problem among women living in these areas. In a community-based study in northern Tanzania in 1998, 40% of 543 women of child-bearing age were diagnosed with urinary schistosomiasis, and among 263 women who agreed to cervical biopsy, 85 (32%) of them had S. haematobium eggs seen in wet crushed biopsies [14]. Co-existence of urinary schistosomiasis and FGS was observed in 62% of the women, while 23% of them had eggs in their cervical tissue without detectable eggs in urine samples [14]. In the same setting, in 2000, the overall prevalence of urinary schistosomiasis was 36% among 657 women screened at community level and that of FGS was 37% (134/359) [13]. Cervical lesions occurred in 75% of the FGS cases, with the majority presenting with swollen and disrupted epithelium [13]. One additional report in northern Tanzania revealed that not only S. haematobium but also S. mansoni contributed to FGS [28,35] In that report, ~5% of the cervical tissues examined had S. mansoni eggs and these women complained of irregular menses (41%), intermenstrual bleeding (26%), infertility (37%) and spontaneous abortion (56%) [28]. Of note, this entire body of work in northern Tanzania was conducted over 20 years ago and no further data has been reported from this part of the country.
In north-western Tanzania, the prevalence of S. haematobium infection was 5% among women screened at the community level, with marked variation from one village to another (from 0%-11% based on urine and cervical microscopy [33]. In this setting, S. haematobium infection was noted to be associated with HIV infection, with a four- fold increased odds of HIV infection among women diagnosed with FGS. Similarly, FGS was associated with younger age ≤ 35 years [33]. In a community-based intervention study, single dose praziquantel treatment resulted in declining schistosome eggs in urine and schistosome Polymerase Chain Reaction (PCR) values in urine and cervical lavages six months post-treatment, but cervical abnormalities did not improve significantly [34]. A recent population-based study in another district in northwest Tanzania reported that overall prevalence of urogenital schistosomiasis was 4.5% based on detectable eggs in urine samples, with a mean egg intensity of 19.5eggs/10mL [37]. Notably, this study did not include gynaecologic examinations.
Studies in northwest Tanzania have further characterized the co-occurrence of FGS and other diseases of the female reproductive tract, which is complicated given that gynecological symptoms such as abdominal-pelvic pain, menorrhagia, genital itching, dysmenorrhea, dyspareunia and foul-smelling discharge were commonly noted and can be symptoms of FGS or of sexually-transmitted infections [33]. Other community-based studies in the region have investigated immunologic and microbial associations with FGS and documented altered cytokine profiles in cervical lavages of women with S. haematobium infection and altered cervicovaginal bacterial populations in women with S. mansoni infection and women with persistent S. haematobium infection following treatment [28,34]. Other studies have demonstrated that mass treatment for gynaecological schistosomiasis should be done in collaboration with the school system as a joint venture [31]. Does treatment with praziquantel in infected women lead to restoration of cytokine levels and bacterial populations? The answer is still unclear.
Hospital based studies
Histopathological studies conducted in national and referral hospitals in Tanzania have revealed a significant burden of FGS in women who underwent biopsies or surgery [24,29,30]. At the Muhimbili National hospital in Dar es Salaam, a retrospective study from 1975–1980 analysed a total of 170 specimens involving schistosomiasis of the female genital tract [24]. The commonest clinical manifestations observed were warts, nodules, papillomata, swelling and cervical bleeding [24]. FGS most frequently affected the cervix, followed by the vulva, vagina, and Fallopian tubes [24]. Another retrospective review of histopathological tissues revealed the co-occurrence of the human papillomaviruses (HPVs) and urogenital schistosomiasis in 31 cervical cancer patients and concluded that there was no evidence that the parasite is associated with cervical cancer because all women with S. haematobium infection also had HPV type 16 or 18 [26]. In southern Tanzania, women who reported a history of urogenital schistosomiasis more frequently had infection with a high-risk HPV type, although the numbers included in this study were small and only 6 women had confirmed S. haematobium infection [29]. At a consultant hospital in northern Tanzania from 1994–2005, a total of 423 organ specimens were found to contain schistosome ova, 125 (41%) of which were from female genital organs [30]. Predominant symptoms associated with FGS included bleeding disorders, ulcers, tumors, lower abdominal pain, and infertility [30]. Out of 53 cases of suspected cervical cancer, 40 (75%) had severe cervical schistosomiasis and only 13 (25%) had confirmed malignancy [30].
Case report
In the past four decades, only a single case of FGS involving a 9-year-old girl from Pemba island was published [25]. This girl presented with two polypoid nodular growths of the left labium major and hypertrophy of the left labium minor. Schistosoma haematobium eggs were detected both in her urine sample and in a scraping of the genital tissue. Six months after a single dose of praziquantel, she had experienced full resolution of her symptoms.
Diagnostic studies
Several diagnostic studies focused on improving the detection of genital schistosomiasis at the community level or within hospital settings [27,32,38]. A study from 2001 compared three methods: cytological inspection of a cervical smear, histopathological examination of a preserved biopsy, and parasitological examination of a wet crushed cervical biopsy [27]. Among 228 women, 3% had positive cervical smears, 18% had eggs detected histopathologically, and 49% had schistosome eggs detected in the cervix using the quantitative compressed biopsy technique. It is worthwhile to note that performing a cervical biopsy, except when necessary to rule out cervical cancer, is no longer recommended in areas with endemic HIV infection due to concerns of transiently increasing the risk of HIV acquisition while the cervical mucosa heals.
Urine reagent strip to detect haematuria is a simple indirect tool that has been studied for rapid screening of S. haematobium infection in endemic areas [27], although false positives can be obtained in cases of urinary tract infections or during menses. In women, reagent urine strips identified haematuria in 65% of those with S. haematobium eggs in urine [27].
In a three-country study that included 933 women, of whom nearly half were from the Mwanza region of Tanzania, cervicovaginal lavage PCR for Schistosoma DNA was significantly associated with detection of Schistosoma DNA in urine, demonstrating the utility of real-time PCR to diagnose FGS in endemic areas. Of note, cervicovaginal PCR positivity was not associated with urine egg microscopy, nor with cytologic examination for eggs in genital specimens [27].
Qualitative studies
A qualitative study was conducted in 2021 on FGS. It focused on gaps in healthcare workers’ knowledge about FGS in Tanzania. Findings from the community-based study demonstrated that most communities living in known S. haematobium endemic areas of Tanzania had a relatively good knowledge of urogenital schistosomiasis but lacked knowledge of FGS [40].
Misconceptions on the aetiology and modes of transmission of urogenital schistosomiasis and FGS were common. Community members recognized the need for being educated about these diseases. The data emphasized the urgent need for public health interventions to focus on improving community awareness of FGS, which in turn will reduce stigma and improve women and girls’ health seeking behavior when they have genital related lesions.
The findings among health care workers demonstrated the high need for offering education about FGS to fill knowledge gaps. The data suggested that in-service training should cover such topics as identification of women and adolescent girls at risk; symptoms, etiology, modes of transmission, and ways of preventing FGS; management of FGS (including the management of other STIs as part of the differential diagnosis); and mitigating stigma faced by women and girls suffering from FGS both at the healthcare facility settings and in the communities.
Discussion
The current review indicates that, for the past four decades, there have been sporadic hospital-based retrospective studies, community-based studies, case reports, immunological, and diagnostic studies addressing FGS in Tanzania. However, there is a marked paucity of community-based studies focusing on FGS in many areas of Tanzania, in both Tanzania’s mainland and Tanzania’s islands Pemba and Unguja (Zanzibar). Overall, the current scoping review reveals that FGS occurs in Tanzanian women living in areas of the country with different transmission intensities of S. haematobium [13,14,33]. Retrospective hospital- based studies at national and zonal consultant hospitals confirm that S. haematobium eggs have been commonly identified in women’s reproductive tract tissues submitted for pathological examination at histopathology departments for decades. Furthermore, community-based studies conducted in the northern and the north-western part of the country have concluded that FGS is common, though heterogeneously dispersed, in these areas [24,29,30]. We found a severe lack of information on FGS from Unguja and Pemba. Only one case report of FGS involving a young girl was retrieved [25]. This is particularly striking because the two islands are known to be highly endemic for S. haematobium, with high prevalence of infection in both sexes and a range of age groups [41]. Indeed, multiple studies have worked towards elimination of S. haematobium from the islands [41,42], but there has been no focus on FGS.
Overall, considering the high prevalence of S. haematobium infection in Tanzania [21], FGS has been neglected in the country. These findings suggest that routine, repeated MDA or other interventions may be needed to improve the cervical tissue abnormalities caused by FGS in women living in highly endemic areas. However, to date, there is paucity of information on the effects of praziquantel on the gynaecological lesions resulting from S. haematobium infections. Public health efforts are hindered by lack of reliable up-to-date epidemiological information on prevalence, incidence and geographical distribution of FGS in the country. Community-based studies included in the current review were conducted in only two geographical areas in the country, with that from northern part reported from only a single district of Mwanga and conducted over 20 years ag [13,14]. Given efforts for mass administration of praziquantel in Tanzania and the effects of climate change which highly impacts snail survival [42], up-to-date epidemiological information is urgently needed. We anticipate that current data from across the country will elevate FGS to the Tanzanian national agenda. This will allow FGS not only to be considered for interventions by policy makers, but also to be integrated in improving women’s overall health—reproductive, maternal, and mental health—in Tanzania. One approach to increase the availability of data is to integrate FGS screening, diagnosis, and treatment into women’s reproductive health services in endemic health facilities, as recently recommended in the Bulletin of the World Health Organization [43]. This approach will help to generate current epidemiological data from clinical facilities as well as to view women’s health holistically, as experienced by the women themselves. Importantly, this approach will require trained and knowledgeable health workers and availability of appropriate diagnostic equipment. Our team is working to improve knowledge and provide training to local health workers as part of all of our currently ongoing studies of FGS in Tanzania, and further capacity building should be prioritized.
Limitation
It should be noted that this review was not conducted without limitation. This review only included papers available in google scholar and PubMed. To add to this some articles contained proprietary information which are not publicly available. Furthermore, this scoping review only included studies to June 2022.
Conclusion
Female Genital Schistosomiasis is a significant problem in Tanzanian women living in S. haematobium transmission zones; however, up-to-date epidemiological data to guide interventions is severely lacking. The island part of the country has limited data related to FGS available in the public domain. Current efforts to administer single-dose mass praziquantel treatment for schistosomiasis are intensified among school children in Tanzania but not among adolescent girls and women of reproductive age, many of whom are no longer in school. Further complicating this challenge, women with FGS may require multiple doses of praziquantel or other intervention to achieve complete resolution of FGS. Epidemiological and treatment studies are urgently needed. Moreover, further research is essential to understanding the true burden of disease-associated morbidity, to assessing the impact of single dose praziquantel in FGS lesions, to understanding mental health in relation to FGS, and to integrating delivery of FGS related services in primary health care systems. We urge that this most neglected aspect of schistosomiasis, which is itself already a neglected tropical disease, receives the attention that women suffering with FGS deserve.
Supporting information
S1 Table. Search terms and limits used by database.
https://doi.org/10.1371/journal.pntd.0011954.s001
(DOCX)
S2 Table. Study eligibility criteria, conforming to PICOS format as per PRISMA recommendations.
https://doi.org/10.1371/journal.pntd.0011954.s002
(DOCX)
S3 Table. Data extracted from included publications.
https://doi.org/10.1371/journal.pntd.0011954.s003
(DOCX)
S4 Table. Narrative synthesis of quality assessment.
https://doi.org/10.1371/journal.pntd.0011954.s004
(DOC)
References
- 1.
World Health Organization. Schistosomiasis. 2023; Available from: https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections.
- 2.
World Health Organization Expert Committee. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Vol. 912, World Health Organization technical report series. Switzerland; 2002.
- 3. World Health Organization. Schistosomiasis: number of people receiving preventive chemotherapy in 2012 = Schistosomiase: nombre de personnes ayant bénéficié d’une chimioprévention en 2012. Wkly Epidemiol Rec = Relev épidémiologique Hebd. 2014;89(02):21–8.
- 4.
World Health Organization. Schistosomiasis.fact sheet. Schistosomiasis [Internet]. https://www.who.int/news-room/fact-sheets/detail/schistosomiasis. 2023 [cited 2023 Jun 9]. Available from: https://www.who.int/news-room/fact-sheets/detail/schistosomiasis.
- 5. Lwambo NJS, Siza JE, Brooker S, Bundy DAP, Guyatt H. Patterns of concurrent hookworm infection and schistosomiasis in schoolchildren in Tanzania. Trans R Soc Trop Med Hyg [Internet]. 1999 [cited 2023 May 17];93(5):497–502. Available from: https://pubmed.ncbi.nlm.nih.gov/10696404/ pmid:10696404
- 6. Mazigo H, Zinga M, Heukelbach J, Rambau P. Case series of adenocarcinoma of the prostate associated with Schistosoma haematobium infection in Tanzania. J Glob Infect Dis. 2010;2(3):307. pmid:20927294
- 7. Kjetland EF, Kurewa EN, Ndhlovu PD, Midzi N, Gwanzura L, Mason PR, et al. 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 Heal. 2008;13(12):1509–17.
- 8.
WHO. Female genital schistosomiasis: simultaneous screening of diseases can improve reproductive health [Internet]. World Health Organization. 2018 [cited 2023 Oct 10]. p. 1. Available from: https://www.who.int/news/item/20-07-2018-female-genital-schistosomiasis-simultaneous-screening-of-diseases-can-improve-reproductive-health.
- 9. UNAIDS, UNAIDS. No more neglect female genital schistosomiasis and HIV. Integr Sex Reprod Heal Interv Improv women’s lives. 2019;(UNAIDS/JC2979):1–44.
- 10. Madden FC. A CASE OF BILHARZIA OF THE VAGINA. Lancet [Internet]. 1899 Jun 24 [cited 2023 May 19];153(3956):1716. Available from: http://www.thelancet.com/article/S0140673601513859/fulltext.
- 11. Bustinduy AL, Randriansolo B, Sturt AS, Kayuni SA, Leutscher PDC, Webster BL, Van Lieshout L, Stothard JR, Feldmeier H, Gyapong M. An update on female and male genital schistosomiasis and a call to integrate efforts to escalate diagnosis, treatment and awareness in endemic and non-endemic settings: The time is now, [Internet]. 2022. p. 1–44. Available from: pmid:35249661
- 12. Sturt AS, Webb EL, Phiri CR, Mweene T, Chola N, van Dam GJ, et al. Genital self-sampling compared with cervicovaginal lavage for the diagnosis of female genital schistosomiasis in zambian women: The BILHIV study. PLoS Negl Trop Dis [Internet]. 2020;14(7):1–18. Available from: pmid:32663222
- 13. Poggensee G, Kiwelu I, Weger V, Göppner D, Diedrich T, Krantz I, et al. Female genital schistosomiasis of the lower genital tract: Prevalence and disease-associated morbidity in Northern Tanzania. J Infect Dis. 2000;181(3):1210–3. pmid:10720558
- 14. Poggensee G, Kiwelu I, Saria M, Richter J, Krantz I, Feldmeier H. Schistosomiasis of the lower reproductive tract without egg excretion in urine. Am J Trop Med Hyg [Internet]. 1998 Nov 1 [cited 2023 May 19];59(5):782–3. Available from: https://www.ajtmh.org/view/journals/tpmd/59/5/article-p782.xml. pmid:9840597
- 15. Poggensee G, Krantz I, Kiwelu I, Feldmeier H. Screening of Tanzanian women of childbearing age for urinary schistosomiasis: validity of urine reagent strip readings and self-reported symptoms. Bull World Health Organ. 2000;78(4):542–8. pmid:10885183
- 16. Norseth HM, Ndhlovu PD, Kleppa E, Randrianasolo BS, Jourdan PM, Roald B, et al. The Colposcopic Atlas of Schistosomiasis in the Lower Female Genital Tract Based on Studies in Malawi, Zimbabwe, Madagascar and South Africa. PLoS Negl Trop Dis. 2014;8(11):1–17. pmid:25412334
- 17. Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, Gwanzura L, et al. Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS. 2006 Feb;20(4):593–600. pmid:16470124
- 18. Kingery JR, Chalem A, Mukerebe C, Shigella PS, Miyaye D, Magawa RG, et al. Schistosoma mansoni Infection Is Associated With Increased Monocytes and Fewer Natural Killer T Cells in the Female Genital Tract. Open Forum Infect Dis [Internet]. 2022;9(12):1–5. Available from: pmid:36601557
- 19. Tanzania Ministry of Health. Strategic master plan for the neglected tropical diseases control program Tanzania Mainland. Minist Heal. 2021;(July).
- 20. WEBBE G. The transmission of Schistosoma haematobium in an area of Lake Province, Tanganyika. Bull World Health Organ. 1962;27:59–85. pmid:14005428
- 21. Mazigo HD, Nuwaha F, Kinung SM, Morona D, Moira AP De, Wilson S, et al. Epidemiology and control of human schistosomiasis in Tanzania. Parasit Vectors, 2012 5274. pmid:23192005
- 22. Lwambo NJ. Transmission of urinary schistosomiasis in Sukumaland, Tanzania. 1. Snail infection rates and incidence of infection in school children. J Helminthol. 1988 Sep;62(3):213–7. pmid:3192912
- 23. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, et al. The PRISMA statement for reporting systematic review. Ann Intern Med. 2009;151(4).
- 24. Van Raalte JA, Venkataramaiah NR, Shaba JK. Bilharziasis of the female genital tract in Tanzania. East Afr Med J [Internet]. 1981;58(7):543–7. Available from: http://europepmc.org/abstract/MED/7308113. pmid:7308113
- 25. Savioli L, Gabrielli A, Neve H. Vulvar Schistosoma haematobium lesion treated with praziquantel. Trop Doct. 1990 Jan;20(1):45–6. pmid:2106182
- 26. Moubayed P, Ziehe A, Peters J, Mwakyoma H, Schmidt D. Carcinoma of the uterine cervix associated with schistosomiasis and induced by human papillomaviruses. Int J Gynaecol Obstet Off organ Int Fed Gynaecol Obstet. 1995 May;49(2):175–9. pmid:7649324
- 27. Poggensee G, Sahebali S, Van Marck E, Swai B, Krantz I, Feldmeier H, et al. Diagnosis of genital cervical schistosomiasis: Comparison of cytological, histopathological and parasitological examination. Am J Trop Med Hyg [Internet]. 2001 [cited 2021 Aug 29];65(3):233–6. Available from: https://pubmed.ncbi.nlm.nih.gov/11561710/ pmid:11561710
- 28. Poggensee G, Krantz I, Kiwelu I, Diedrich T, Feldmeier H. Presence of Schistosoma mansoni eggs in the cervix uteri of women in Mwanga District, Tanzania. Trans R Soc Trop Med Hyg. 2001;95(3):299–300. pmid:11491002
- 29. Petry KU, Scholz U, Hollwitz B, Von Wasielewski R, Meijer CJLM. Human papillomavirus, coinfection with Schistosoma hematobium, and cervical neoplasia in rural Tanzania. Int J Gynecol cancer Off J Int Gynecol Cancer Soc. 2003;13(4):505–9. pmid:12911728
- 30. Swai B, Poggensee G, Mtweve S, Krantz I. Female genital schistosomiasis as an evidence of a neglected cause for reproductive ill-health: A retrospective histopathological study from Tanzania. BMC Infect Dis. 2006;6:1–8.
- 31. Lillerud LE, Stuestoel VM, Hoel RE, Rukeba Z, Kjetland EF. Exploring the feasibility and possible efficacy of mass treatment and education of young females as schistosomiasis influences the HIV epidemic. Arch Gynecol Obstet. 2010 Mar;281(3):455–60. pmid:19434416
- 32. Dirk Grothuesmann. Diagnosis of Female Genital Schistosomiaisis by Colposcopy: Feasibility and Options under Conditions of Sub-Saharan Africa. 2010;8(5):55.
- 33. Downs JA, Mguta C, Kaatano GM, Mitchell KB, Bang H, Simplice H, et al. Urogenital schistosomiasis in women of reproductive age in Tanzania’s Lake Victoria region. Am J Trop Med Hyg. 2011;84(3):364–9. pmid:21363971
- 34. Downs JA, Kabangila R, Verweij JJ, Jaka H E. Detectable Urogenital Schistosome DNA and Cervical Abnormalities Six Months after Single-Dose Praziquantel in Women with Schistosoma haematobium Infection. Natl Inst Heal [Internet]. 2013;18(9):1090–6. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3624763/pdf/nihms412728.pdf.
- 35. Woodall PA, Kramer MR. Schistosomiasis and infertility in East Africa. Am J Trop Med Hyg. 2018;98(4):1137–44. pmid:29313478
- 36. Dupnik KM, Lee MH, Mishra P, Reust MJ, Colombe S, Haider SR, et al. Altered Cervical Mucosal Gene Expression and Lower Interleukin 15 Levels in Women With Schistosoma haematobium Infection but Not in Women With Schistosoma mansoni Infection. 2019;10065:1777–85. pmid:30590736
- 37. Rite EE, Kapalata SN, Munisi DZ. Prevalence, Intensity, and Factors Associated with Urogenital Schistosomiasis among Women of Reproductive Age in Mbogwe District Council, Geita Region, Tanzania. López Sández CM, editor. Biomed Res Int [Internet]. 2020;5923025. Available from: pmid:33178830
- 38. Pillay P, Downs JA, Changalucha JM, Brienen EAT, Ramarokoto CE, Leutscher PDC, et al. Detection of Schistosoma DNA in genital specimens and urine: A comparison between five female African study populations originating from S. haematobium and/or S. mansoni endemic areas. Acta Trop [Internet]. 2020;204(January):105363. Available from: pmid:32035055
- 39. Bullington BW, Lee MH, Mlingi J, Paul N, Aristide C, Fontana E, et al. Cervicovaginal bacterial communities in reproductive-aged Tanzanian women with Schistosoma mansoni, Schistosoma haematobium, or without schistosome infection. ISME J. 2021 May;15(5):1539–50. pmid:33408370
- 40. Mazigo HD, Samson A, Lambert VJ, Kosia AL, Ngoma DD, Murphy R, et al. “We know about schistosomiasis but we know nothing about FGS”: A qualitative assessment of knowledge gaps about female genital schistosomiasis among communities living in schistosoma haematobium endemic districts of Zanzibar and Northwestern Tanzania. PLoS Negl Trop Dis [Internet]. 2021;15(9):1–25. Available from: pmid:34591872
- 41. Knopp S, Ame SM, Hattendorf J, Ali SM, Khamis IS, Bakar F, et al. Urogenital schistosomiasis elimination in Zanzibar: Accuracy of urine filtration and haematuria reagent strips for diagnosing light intensity Schistosoma haematobium infections. Parasites and Vectors. 2018;12(1):1–11. pmid:30352631
- 42. Trippler L, Ame SM, Hattendorf J, Juma S, Abubakar S, Ali SM, et al. Impact of seven years of mass drug administration and recrudescence of schistosoma haematobium infections after one year of treatment gap in zanzibar: Repeated cross-sectional studies. PLoS Negl Trop Dis [Internet]. 2021;15(2):1–21. Available from: pmid:33577601
- 43. Engels D, Hotez PJ, Ducker C, Gyapong M, Bustinduy AL, Secor WE, et al. Integration of prevention and control measures for female genital schistosomiasis, HIV and cervical cancer. Bull World Health Organ. 2020 Sep;98(9):615–24. pmid:33012861