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Prevalence of urinary schistosomiasis in women: a systematic review and meta-analysis of recently published literature (2016–2020)

Prevalence of urinary schistosomiasis in women: a systematic review and meta-analysis of recently... Background: Urinary schistosomiasis is a serious threat in endemic territories of Africa and the Middle East. The sta- tus of female urinary schistosomiasis (FUS) in published literature between 2016 and 2020 was investigated. Methods: A systematic search in PubMed, Scopus, Google Scholar, and Web of Science, based on the ‘Preferred Reporting Items for Systematic Reviews and Meta-analyses’ checklist, and a meta-analysis using random-effects model to calculate the weighted estimates and 95% confidence intervals (95% CIs) were done. Results: Totally, 113 datasets reported data on 40,531 women from 21 African countries, showing a pooled preva- lence of 17.5% (95% CI: 14.8–20.5%). Most studies (73) were performed in Nigeria, while highest prevalence was detected in Mozambique 58% (95% CI: 56.9–59.1%) (one study). By sample type and symptoms, vaginal lavage [25.0% (95% CI: 11.4–46.1%)] and hematuria 19.4% (95% CI: 12.2–29.4%) showed higher FUS frequency. Studies using direct microscopy diagnosed a 17.1% (95% CI: 14.5–20.1%) prevalence rate, higher than PCR-based studies 15.3% (95% CI: 6.1–33.2%). Except for sample type, all other variables had significant association with the overall prevalence of FUS. Conclusions: More studies are needed to evaluate the true epidemiology of FUS throughout endemic regions. Keywords: Epidemiology, Urinary schistosomiasis, Women, Meta-analysis Background subtropical territories and renders approximately 70 Schistosomiasis, due to trematodes of the genus Schis- million disability-adjusted life years [1–3]. In endemic tosoma (blood flukes), is a snail-transmitted hel - areas such as sub-Saharan Africa morbidity is higher minthiasis and the third most degenerative tropical among school-aged children (60–80%) than adults disease with substantial morbidity/mortality rates, (20–40%), with a mortality rate of 280,000 people [4]. particularly in low- and middle-income countries [1]. Six species out of 24 recognized schistosomes result in With about 800 million at-risk individuals, schistoso- disease in humans, comprising Schistosoma haemato- miasis afflicts over 250 million people in tropical and bium (S. haematobium) the causative agent of urogeni- tal schistosomiasis (UGS), S. japonicum, S. mansoni, S. intercalatum, S. mekongi and S. guineensis as agents of hepato-intestinal disease [5]. In a public health per- *Correspondence: asghari3@yahoo.com Department of Medical Parasitology and Mycology, School of Medicine, spective, Africa and the Mideast (S. mansoni and S. Shiraz University of Medical Sciences, Shiraz, Iran haematobium), Southeast Asia (S. japonicum) and Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Shams et al. Tropical Medicine and Health (2022) 50:12 Page 2 of 18 Latin America (S. mansoni) are considered as the most Methods distinguished geographical hotspots for schistosomiasis The present systematic review and meta-analysis was [6]. Adult paired worms would stay alive in host’s blood accomplished on the basis of Preferred Reporting Items stream for about 3–10  years and produce numerous for Systematic Reviews and Meta-analyses (PRISMA) spiny eggs, rendering chronicity and pathologic out- statement [24] (Additional file 1). comes of the infection [7–9]. The putative signs and symptoms of UGS were ini - Information sources and systematic searching tially ascribed about 1900 Before the Common Era Major English databases including Scopus, PubMed, (BCE), when hematuria was a common finding in Egyp - Web of Science and Google Scholar were systematically tian males, referred to as “menstruation” [10]. Infected searched for articles evaluating the prevalence of FUS planorbid snails, Bulinus spp., are intermediate hosts worldwide and published during a 5-year time period, releasing motile furcocercous cercariae in surround- from January 2016 until the end of 2020. This proce - ing water supplies. Following skin cercarial invasion and dure was conducted using the following keywords alone migration thorough lungs and liver, S. haematobium or in combination, using advanced search option in worms would finally lodge in the genitourinary venous most databases and Medical Subject Heading (MeSH) complex, in particular bladder veins, where they mature option in PubMed databases: “Urinary Schistosomiasis” and copulate therein [11]. Although harsh disease out- AND “Prevalence” OR “Epidemiology” AND “Female” comes primarily arise from the T-cell mediated, granu- OR “Women” Or “Girl”, where “AND” and/or “OR” are lomatous immune responses against tissue-deposited Boolean operators. Hand-searching of the bibliographic spiny eggs of schistosomes. Such lesions would represent list of related papers was an additional task to more manifestations comprising hematuria, dysuria, itching, cover those papers not found via database exploration. pelvic pain, as well as the life-threatening squamous cell Briefly, title and abstract of the literature were accurately carcinoma of the urinary bladder [12, 13]. Additionally, reviewed (H.M. and M.F.), relevant papers were included, S. haematobium is responsible of egg-induced patho- and upon duplicate removal, full-texts of eligible papers logical lesions and associated symptoms in both men and were retrieved (T.N.). Any disagreements were obviated women [14, 15]. by discussion and consensus with the leading researchers An active UGS could be detected through observation (M.SH and A.A.). of eggs in urine sediments and/or tissue biopsies [16]. For the aim of determining hotspots and control strategies, Inclusion/exclusion criteria and data collection World Health Organization (WHO) has recommended Specific inclusion criteria were determined in order to microscopic-based poly-carbonate filter examination for thoroughly gather relevant peer-reviewed cross-sec- urinary eggs as well as dipstick assays for urinary heme tional studies and conference reports limited to women detection [17, 18]. Serodiagnostic assays identifying anti- population in a 5-year time period (2016–2020). Only bodies against worm antigens may demonstrate valuable those papers with specified sample size and number of credibility in symptomatic travelers, whereas they usually FUS-positive women, diagnosed either by microscopic, fail to differentiate active or previous infections, unless filtration, sedimentation and/or molecular techniques those employing circulating antigens [19, 20]. An encour- were included in current systematic review. Other study aging degree of sensitivity and specificity have been types (case reports, letters, reviews), studies evaluating gained in utilization of molecular assays such as poly- animals or other Schistosomal infections, investigations merase chain reaction (PCR) for schistosome detection without sample size/prevalence rates or lacking full-texts in human serum and urine samples [21]. This method is, were all excluded from the present systematic review and also, beneficial for vaginal lavage analysis, revealing the meta-analysis. Finally, a pre-designed Microsoft Excel likely traits of the genital schistosomiasis [22]. Spreadsheet was used to extract the required informa- A very large number of female urinary schistosomiasis tion (E.J. and S.B.), as follows: first author’s last name, (FUS) studies were performed during the last two dec- publication year, start and end years of studies, study ades [23]. The emphasis of the present systematic review type, country, province, city, sample type, diagnostic and meta-analysis was on the published literature during method, sample size, positive number of infected cases the last 5 years (2016–2020), in order to define the latest and clinical symptoms (hematuria and proteinuria). status of FUS and its prevalence based on examined sub- groups. The novel findings of the present study may alert Quality assessment clinicians to the prevalence of this important helminthia- In the present systematic review, the Newcastle–Ottawa sis and its associated consequences on the genitourinary scale was employed to assess the quality of included stud- system of infected female individuals. ies. Those papers with the scores of < 3.5, 3.6–5.25, and Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 3 of 18 5.26–7 were categorized as low-, moderate-, and high- All analytical functions were applied by Comprehensive quality papers, respectively [25]. Meta-analysis (CMA) version 2.2. (Biostat Inc., USA). Results Data synthesis and meta‑analysis The flow diagram of the systematic search process and Meta-analytical approach was done according to pre- inclusion of relevant papers is shown in Fig.  1. Initially, vious studies (S.B. and D.A.) using a random-effects 3537 datasets were identified through comprehensive model [26–28]. For all included studies, point estimates database exploration. After removing duplicates (1821) and their respective 95% confidence intervals (CIs) of and those with irrelevant title and abstract (1571), 145 weighted prevalence were calculated. Heterogeneity datasets were finally assessed for eligibility. Among these, among these studies or variation in study outcomes was 35 datasets were excluded with reasons (review papers, visualized by drawing forest plots, calculated by I and theses, conference papers and studies with confus- Cochrane’s Q tests [29, 30]. The subgroup analysis was ing data) and 3 additional datasets were added through performed based on year, country, sample type, symp- manual searching. Therefore, 106 articles containing toms and diagnostic methods. The presence of publica - 113 datasets were finally included in our meta-analysis tion bias was estimated by using Egger’s regression test (Table 1) [33–139]. [31]. This kind of bias, if present, skews the results and Finally, 113 datasets evaluating 40,531 individuals were published reports are not a representative sample of the included in the present review. Among these, 11,308 available evidence anymore. The trim-and-fill method individuals were shown to be affected by FUS and based was, also, used to “estimate the number of missing stud- on the random-effects model meta-analysis, the pooled ies that might exist in a meta-analysis and the effect that prevalence of FUS was 17.5% (95% CI: 14.8–20.5%). The these studies might have had on its outcome” [32]. P-val- included studies demonstrated a strong heterogene- ues less than 0.05 were considered statistically significant. ity (I = 98.12%, P < 0.01) (Additional file  2). Publication Fig. 1 PRISMA flow diagram describing included/excluded studies on FUS prevalence (2016–2020) Shams et al. Tropical Medicine and Health (2022) 50:12 Page 4 of 18 Table 1 Detailed characteristics of the included studies in the present systematic review and meta-analysis (2016–2020) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 1 Awosolu, 2020 Nigeria Osun and 2012 Urine Filtrations and 258 122 5 [56] Kwara microscopic examination 2 Olayinka, 2020 Nigeria Ogun 2015–2017 Urine Microscopic 280 42 6 [112] examination 3 Awosolu, 2019 Nigeria Ikota 2015 Urine Microscopic 74 20 7 [55] examination 4 Otuneme, 2019 Nigeria Ogun 2017 Urine Microscopic 47 39 5 [118] examination 5 Muhammad, Nigeria Sokoto NR Urine Microscopic 107 47 5 2019 [101] examination 6 Sule, 2019 [129] Nigeria Kano NR Urine Microscopic 56 0 6 examination 7 Idris, 2019 [87] Nigeria New-Bussa NR Urine Microscopic 24 2 7 examination 8 Geraji, 2019 [81] Nigeria Jalingo 2019 Urine Microscopic 86 13 7 examination 9 Adamu, 2019 Nigeria Kaduna 2017 Urine Microscopic 136 4 7 [36] examination 10 Ngwamah, 2019 Nigeria Adamawa NR Urine Microscopic 679 141 7 [105] examination 11 Aribodor, 2019 Nigeria Enugu 2016 Urine Microscopic 121 17 7 [51] examination 12 Sobande, 2019 Nigeria Ogun NR Urine Microscopic 84 40 6 [128] examination 13 Obisike, 2019 Nigeria Benue 2017 Urine Membrane 84 20 5 [110] filtration and (sedimentation) microscopic examination 14 Ahmed, 2019 Nigeria Katsina NR Urine (sedimentation) 68 15 6 [40] Microscopic examination 15 Aderibigbe, Nigeria Kwara NR Urine Microscopic 883 293 7 2019 [37] examination 16 Noriode, 2018 Nigeria Edo NR Urine Microscopic 109 75 5 [106] examination 17 Bishop, 2016 Nigeria Kaduna NR Urine Microscopic 92 5 6 [164] examination 18 Mohammed, Nigeria Sokoto 2016 Urine Microscopic 51 18 5 2018 [95] examination 19 Akinneye, 2018 Nigeria Ondo NR Urine Microscopic 202 22 5 [43] examination 20 Alabi, 2018 [46] Nigeria Ogun NR Urine Microscopic 73 36 6 examination 21 Damen, 2018 Nigeria Plateau NR Urine Microscopic 7 1 6 [68] examination 22 Yauba, 2018 Nigeria Maiduguri 2014–2015 Urine Microscopic 180 113 7 [138] examination 23 Abdulkareem, Nigeria Kwara NR Urine Microscopic 309 131 7 2018 [34] examination 24 Oladeinde, 2018 Nigeria Edo 2014 Urine Microscopic 98 8 6 [111] examination 25 Ebong, 2018 Nigeria Akwa Ibom NR Urine Microscopic 199 5 7 [70] examination Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 5 of 18 Table 1 (continued) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 26 Akeju Adebayo, Nigeria Ondo NR Urine Microscopic 1022 441 5 2018 [42] examination 27 Oluwole, 2018 Nigeria Ogun 2013 Urine Microscopic 1034 43 6 [114] examination 28 Adewale, 2018 Nigeria Ondo NR Urine Microscopic 190 44 6 [38] examination 29 Nwachukwu, Nigeria Imo 2014–2016 Urine Test strip and 1125 57 7 2018 [107] filtration 30 Nwachukwu, Nigeria Ebonyi 2016–2017 Urine Microscopic 254 8 7 2018 [108] examination 31 Duwa, 2018 [69] Nigeria Kano 2018 Urine Microscopic 105 8 5 examination 32 Babagana, 2018 Nigeria Borno NR Urine Microscopic 180 31 7 [57] examination 33 Mohammed, Nigeria Kebbi 2016 Urine (Filtration) 81 16 5 2018 [94] Microscopic examination 34 Oluwole, 2018 Nigeria Ogun NR Urine and vainal Microscopic 317 149 6 [114] lavage and gyneco- logic examina- tion 35 Kenneth, 2017 Nigeria Edo NR Urine Microscopic 76 6 7 [92] examination 36 Birma, 2017 [61] Nigeria Adamawa NR Urine Microscopic 90 42 5 examination 37 Amoo, 2017 [47] Nigeria Ogun NR Urine Microscopic 160 61 6 examination 38 Paul, 2017 [119] Nigeria Cross River NR Urine Microscopic 140 24 5 examination 39 Orpin, 2017 Nigeria Katsina NR Urine Microscopic 145 12 5 [116] examination 40 Ekanem, 2017 Nigeria South-South 2011 Urine Microscopic 177 27 6 [71] examination 41 Akpan, 2017 Nigeria Cross River NR Urine Microscopic 208 34 7 [45] examination 42 Elom, 2017 [73] Nigeria Ebonyi NR Urine Microscopic 147 33 7 examination 43 Akpan, 2017 Nigeria Cross River NR Urine Microscopic 122 1 7 [44] examination 44 Abubakar, 2017 Nigeria Jigawa 2015 Urine Microscopic 65 46 7 [35] examination 45 Dalhat, 2017 Nigeria Sokoto NR Urine Microscopic 140 41 7 [67] examination 46 Emmanuel, Nigeria Benue 2014 Urine Microscopic 207 77 6 2017 [75] examination 47 Wokem, 2017 Nigeria Abia NR Urine Microscopic 570 215 7 [135] examination 48 Anorue, 2017 Nigeria Ebonyi 2002–2003 Urine Microscopic 1367 640 6 [49] examination 49 Orpin, 2016 Nigeria Benue NR Urine Microscopic 104 8 7 [117] examination 50 Onile, 2016 Nigeria Eggua 2012–2013 Urine Microscopic 178 45 7 [115] examination 51 Houmsou, 2016 Nigeria Taraba NR Urine Microscopic 529 231 5 [86] examination Shams et al. Tropical Medicine and Health (2022) 50:12 Page 6 of 18 Table 1 (continued) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 52 Goodhead, Nigeria River NR Urine Microscopic 76 17 7 2016 [83] examination 53 Usman, 2016 Nigeria Bauchi NR Urine Microscopic 300 58 7 [133] examination 54 Dahesh, 2016 Nigeria Giza 2016 Urine Microscopic 582 12 7 [66] examination 55 Igbeneghu, Nigeria Osun 2016 Urine Microscopic 154 60 7 2016 [88] examination 56 Nafiu, 2016 Nigeria Niger 2016 Urine Microscopic 97 9 6 [104] examination 57 Abah, 2016 [33] Nigeria River 2016 Urine Microscopic 184 23 5 examination 58 Umar, 2016 Nigeria Kano NR Urine Microscopic 20 9 5 [132] examination 59 Atalabi, 2016 Nigeria Katsina NR Urine Microscopic 240 14 6 [52] examination 60 Houmsou, 2016 Nigeria Taraba NR Urine Microscopic 510 3 7 [86] examination 61 Nwibari, 2016 Nigeria Plateau NR Urine Microscopic 134 6 5 [165] examination 62 Omoruyi, 2016 Nigeria Edo NR Urine Microscopic 77 4 6 [166] examination 63 Morenikeji, Nigeria Ogun NR Urine Microscopic 79 60 6 2016 [99] examination 64 Bashir, 2016 [60] Nigeria Jigawa NR Urine Microscopic 31 2 7 examination 65 Ganau, 2016 Nigeria Sokoto NR Urine Microscopic 58 24 5 [79] examination 66 Musa, 2016 Nigeria Kaduna NR Urine Microscopic 131 13 6 [102] examination 67 Ajakaye, 2016 Nigeria Ondo NR Urine Microscopic 404 50 7 [41] examination 68 Mong, 2016 [98] Nigeria Abia NR Urine Microscopic 129 13 7 examination 69 Atalabi, 2016 Nigeria Katsina 2015 Urine Microscopic 317 23 6 [53] examination 70 Oluwatoyin, Nigeria Ibadan NR Urine Microscopic 507 1 7 2016 [113]* examination 71 Oluwatoyin, Nigeria Ibadan NR Urine Microscopic 507 28 6 2016 [113] examination 72 Bishop, 2016 Nigeria Kaduna NR Urine Microscopic 251 39 5 [63] examination 73 Maki, 2020 [93] Sudan Darfur 2018 Urine Microscopic 55 39 6 examination 74 Qutoof, 2019 Sudan Khartoum NR Urine Microscopic 589 2 5 [122] examination 75 Elsiddig, 2019 Sudan White Nile 2011 Urine Microscopic 162 67 6 [74] examination 76 Hajissa, 2018 Sudan Khartoum 2017–2018 Urine Microscopic 95 11 6 [85] examination 77 Mohammed, Sudan White Nile NR Urine Microscopic 175 97 7 2018 [96] examination 78 Talab, 2018 Sudan White Nile 2014 Urine (Filtration) 174 97 5 [167] Microscopic examination Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 7 of 18 Table 1 (continued) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 79 Sulieman, 2017 Sudan River Nile 2016 Urine (Sedimentation) 191 1 6 [130] Microscopic examination 80 Sabah Alzain Sudan El khiar 2016 Urine Microscopic 76 7 5 Mohamed, 2017 examination [124] 81 Afifi, 2016 [39] Sudan Kassala 2013 Urine Microscopic 1238 172 6 examination 82 Elhusein, 2016 Sudan Gezira 2016 Urine Microscopic 29 0 7 [72] examination 83 Shukla, 2019 South Africa KwaZulu-Natal 2011–2013 Urine and Microscopic 933 256 5 [126] cervico-vaginal examination lavage 84 Galappaththi- South Africa KwaZulu-Natal NR Urine Microscopic 1123 292 5 Arachchige, examination 2018 [78] 85 Kabuyaya, 2017 South Africa uMkhanyakude 2015 Urine Microscopic 199 73 7 [89] examination 86 Galappaththi- south Africa KwaZulu-Natal NR Urine Microscopic 883 270 6 Arachchige, examination 2016[168] 87 Pillay, 2016 South Africa KwaZulu-Natal 2010–2012 vaginal lavages PCR 394 38 7 [169] and Urine 88 South Africa KwaZulu-Natal 2010–2012 Urine PCR 394 91 7 89 South Africa KwaZulu-Natal 2010–2012 Urine Microscopic 394 78 7 examination 90 Fokuo, 2020 [76] Ghana Asutsuare 2014 Urine Microscopic 59 8 6 examination 91 Arhin-Wiredu, Ghana Akyemansa 2014 Urine Microscopic 161 10 6 2019 [50] examination 92 Nyarko, 2018 Ghana different munic- 2016 Urine Microscopic 173 7 6 [109] ipal-ities examination 93 Boye, 2016 [65] Ghana Apewosika and 2013 Urine Microscopic 114 16 5 Putubiw examination 94 Wilkinson, 2018 Malawi Lilongwe 2013 Urine Microscopic 96 2 6 [134] examination 95 Kayuni, 2017 Malawi Mangochi 2012 Urine Microscopic 226 29 6 [91] examination 96 Moyo, 2016 Malawi Nkhotakota NR Urine Microscopic 51 6 6 [100] examination 97 Yameny, 2018 Egypt El-Fayoum NR Urine Microscopic 487 33 7 [137] examination 98 Ghieth, 2017 Egypt Beni Suef NR Urine Microscopic 220 0 5 [82] examination 99 Kaiglova, 2020 Kenya Kwale 2018 Urine Microscopic 323 47 5 [90] examination 100 Mutsaka- Zimbabwe Mashonaland 2010 Urine Microscopic 569 96 6 Makuvaza, 2019 examination [103] 101 Woldegerima, Ethiopia Sanja 2017–2018 Urine Microscopic 189 53 7 2019 [136] examination 102 Phillips, 2018 Mozambique Cabo Delgado 2011 Urine Microscopic 7538 4372 7 [120] examination 103 Gbalegba, 2017 Mauritania Kaedi 2014–2015 Urine Microscopic 1064 54 6 [80] examination Shams et al. Tropical Medicine and Health (2022) 50:12 Page 8 of 18 Table 1 (continued) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 104 Simoonga, 2017 Zambia Lusaka NR Urine Microscopic 954 83 7 [127] examination 105 Balahbib, 2017 Morocco Tata 2015 Urine Microscopic 13 0 6 [58] examination 106 Anchang-Kimbi, Cameroon Mount Cam- 2014 Urine Microscopic 250 117 7 2017 [48] eroon examination 107 Mombo- Gabon Lambarene 2009–2013 Urine Microscopic 1115 103 7 Ngoma, 2017 examination [97] 108 Greter, 2016 [84] Chad Chad NR Urine (Filtration) 96 1 7 Microscopic examination 109 Botelho, 2016 Guinea-Bissau Guinea-Bissau NR Urine Microscopic 43 8 6 [64] examination 111 Senghor, 2016 Senegal Niakhar 2011–2014 Urine Microscopic 320 149 5 [125] examination 111 Rasomanami- Madagascar Madagascar 2015 Urine Microscopic 1043 325 5 haja, 2016 [123] examination 112 Bangura, 2016 Sierra Leon Korwama and 2015 Urine Microscopic 86 32 7 [59] Lewabu examination 113 Zida, 2016 [139] Burkina Faso Bazega 2013 Urine Microscopic 151 7 7 examination *In this dataset, S. mansoni was found in urine instead of S. haematobium bias was checked by Egger’s regression test, showed that women, with vaginal lavage demonstrating a higher it may have a substantial impact on total prevalence frequency of FUS [25.0% (95% CI: 11.4–46.1%)] than estimate (Egger’s bias: 7.5, P < 0.01) (Fig.  2). Since the urine specimen [17.2% (95% CI: 14.5–20.3%)]. Report- heterogeneity of included studies was very high, meta- edly, hematuria and proteinuria as the most promi- regression of subgroups such as year, country, type of nent symptoms of FUS were estimated in some studies, sample, type of symptoms, and diagnostic method were showing 19.4% (95% CI: 12.2–29.4%) and 13.6% (95% CI: used to overcome heterogeneity (Table  2). According 6.69–24.8%) prevalence rates, correspondingly. Direct to subgroup analysis of included data, the prevalence of microscopy was the most frequently utilized diagnostic FUS demonstrated a relatively but worrying increasing test, yielding a relatively higher prevalence 17.1% (95% trend from 14.6% (95% CI: 11.3–18.6%) in 2016 to 28.6% CI: 14.5–20.1%) than PCR method 15.3% (95% CI: 6.1– (95% CI: 13.1–51.6%) in 2020, respectively. In total, stud- 33.2%); however, only two studies employed molecular ies were conducted in 21 countries, including Nigeria (73 method. Additional microscopy-based procedures were datasets), Sudan (10 datasets), South Africa (7 datasets), filtration and sedimentation, which in detail yielded a Ghana (4 datasets), Malawi (3 datasets), Egypt (2 data- prevalence rate of 18.2% (95% CI: 5.9–43.9%) and 11.4% sets), as well as Kenya, Zimbabwe, Ethiopia, Mozam- (95% CI: 3.6–30.9%), respectively. Altogether, subgroup bique, Mauritania, Zambia, Morocco, Cameroon, Gabon, analysis revealed that there were statistically significant Chad, Guinea-Bissau, Senegal, Madagascar, Sierra Leone differences between the overall prevalence of FUS and and Burkina Faso (one dataset per country). The highest year. Of note, the quality score of the included papers is prevalence rates were estimated for women in Mozam- provided in Additional file 3. bique with 58% (95% CI: 56.9–59.1%) (one study), while female individuals in Chad had the lowest prevalence rate Discussion 1.0% (95% CI: 0.1–7.0%). Year-based prevalence for the Helminth-induced diseases are ancient catastrophic phe- six most studied countries, showed no determined pat- nomena in humans, some dating back to pre-biblical era, tern for frequency of FUS, however, a relatively decreas- with huge but chronic and snaky damages in nature [140]. ing pattern of prevalence was recorded for Malawi (three Schistosomiasis or bilharziasis is one of the most impor- studies) (Figs.  3, 4, 5, 6, 7, 8). Regarding sample type, tant water-borne helminthic diseases, which have always urine and vaginal lavage were gathered from examined been interconnected with archaic civilizations over the Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 9 of 18 Fig. 2 A bias assessment plot from Egger for the FUS prevalence (2016–2020) millennia, and it is still a global public health concern due last 5  years were from African countries. This continent to its astonishing, complex life cycle [141, 142]. Among is probably known as the “cradle of schistosomes”, since schistosome species infecting humans, S. haematobium African great lakes provide a favorable milieu for the worms are the causative agents of UGS which localize optimum evolution of both parasites and their respec- within draining venous complex of the pelvic organs such tive intermediate hosts [144]. Schistosomiasis may have as uterus, cervix and the bladder [143]. These worms spread to Africa, particularly Egypt, in virtue of mon- are highly prolific, releasing about 3000 eggs/day, half key importation and slave trades during fifth dynasty of of which are excreted through urine, while the rest are pharaohs [145]. Based on our results obtained from lim- lodged within vasculature of urogenital organs. Immune- ited number of heterogeneous investigations included in mediated pathologic processes elicited against tissue- the present meta-analysis, a large number of studies (73) embedded ova result in granulomatous inflammation, on FUS were done in a western African nation, Nigeria, tissue destruction and the so-called “sandy patches” as whereas the highest prevalence rate was estimated for fibrotic nodules [16]. With respect to the significance of women in Mozambique with 58% (95% CI: 56.9–59.1%) UGS and large number of affected individuals, the pre - (one study), a country in the southeast coast of Africa. sent systematic review and meta-analysis was contrived Nigerian researchers have shown a substantial effort in in order to reveal the latest status of urinary schistosomi- search of urinary schistosomiasis during last 5  years by asis in women population based on published literature conducting 73 datasets, which could be a favorable layout in the last 5 years and provide a premise for future clini- for other African countries [143]. Nevertheless, the true cal directions on women health. picture of FUS prevalence throughout African territories The required information was assembled from availa - in a 5-year time period was not accurately captured, since ble full-texts published between 2016 and 2020 and their out of 21 countries examining female individuals, only 6 overall estimates were assessed through a meticulous countries had sufficient studies to perform meta-analyt - meta-analytical method. During last 5  years, 11,308 out ical approach and most of the remaining had only one of 40,531 women were suffering from urinary schistoso - investigation per country. Moreover, a statistically sig- miasis, contributing to the global weighted prevalence of nificant gradual increase was observed in FUS prevalence 17.5% (95% CI: 14.8–20.5%). Interestingly, all cases in the based on publication year of the included literature, from Shams et al. Tropical Medicine and Health (2022) 50:12 Page 10 of 18 Table 2 Subgroup analysis of FUS prevalence according to year, country, type of sample, type of symptoms and diagnostic methods Subgroup variable Prevalence % (95% CI) I (%) Heterogeneity (Q) P‑ value Interaction P‑ value test (X ) Year 2016 14.6 (11.3–18.6) 96.3% 1034.7 < 0.01 375.3 < 0.01 2017 17.5 (12–24.9) 97.8% 1055.2 < 0.01 2018 19.0 (13.1–26.7) 98.8% 2179.6 < 0.01 2019 21.7 (16.8–27.5) 93.4% 274.7 < 0.01 2020 28.6 (13.1–51.6) 97.1% 138.2 < 0.01 Country Ghana 9.1 (6.8–12.2) 73.46% 11.31 < 0.01 Malawi 11.4 (0.8–15.4) 70.62% 6.81 < 0.01 Nigeria 21.1 (17.6–25.0) 96.9% 2337.91 < 0.01 South Africa 27.4 (25.6–29.2) 92.53% 80.36 < 0.01 Sudan 55.8 (43.9–67.1) 97.59% 374.17 < 0.01 430.6 < 0.01 Egypt 1.7 (0.1–32.8) 83.57 5.90 < 0.01 Type of sample Urine 17.2 (14.5–20.3) 98.11% 5949.4 < 0.01 1285.2 > 0.05 Vaginal lavage 25.0 (11.4–46.1) 98.2% 110.40 < 0.01 Type of symptoms Hematuria 19.4 (12.2–29.4) 92.33% 52.19 < 0.01 82.4 < 0.01 Proteinuria 13.6 (6.69–24.8) – 0.00 = 1.00 Diagnostic method Direct microscopy 17.1 (14.5–20.1) 98.1% 6013 < 0.01 350.6 < 0.01 Filtration and microscopy 18.2 (5.9–43.9) 99.1% 563.1 < 0.01 PCR 15.3 (6.1–33.2) 95.9% 24.64 < 0.01 Sedimentation and microscopy 11.4 (3.6–30.9) 96.6% 59.5 < 0.01 2016 until the end of 2020, ranging from 14.6% (95% CI: enzymes of egg origin that barricade tissue necrosis 11.3–18.6%) to 28.6% (95% CI: 13.1–51.6%), respectively. [149]. In accordance with our finding, hematuria is con - However, no such an increasing trend was observed in sidered as a defining symptom in S. haematobium infec - year-based analysis of each country; even the prevalence tion, mostly being accompanied by suprapubic ailment, relatively decreased in Malawi, though only three studies burning micturition as well as frequent urination [150]. were involved in this country. Such findings derived from Poor immunoregulatory mechanisms in response to eggs limited number of included studies in current review provoke a lasting fibrotic reaction in the urinary tract may be interpreted as a spread of the endemic situation of infected individuals [151]. The resulting obstructive of FUS, or as a result of the increased understanding uropathy elicit subsequent dreadful consequences such about FUS among health care professionals in each coun- as the hydroureter and hydronephrosis [152]. The latter try. Nevertheless, more in-depth studies are required to is the milestone in ascending bacterial superinfections, further elucidate this issue. renal dysfunctions and the ensuing proteinuria [153]. The The characteristic symptoms of UGS were prominently consequences are more horrific in affected women, since reported among examined women, so that a higher prev- the proximity of vesical and genital venous plexuses facil- alence rate was recorded for hematuria with 19.4% (95% itates easy migration of parasites and/or eggs, leading to CI: 12.2–29.4%), in comparison to 13.6% (95% CI: 6.69– harsh outcomes regarding women’s reproductive health 24.8%) frequency of proteinuria. As previously men- [154–156]. The subsequent lesions in genital organs, tioned, disease morbidity largely results from entrapped from ovaries to vagina, may be associated with pain and eggs, which strongly induce a granulomatous immune stress, allowing human immunodeficiency virus-1 (HIV- response [146], characterized by Th2-type lymphocytes, 1) to simply access sub-epithelial target cells [157]. In a alternatively activated macrophages and eosinophils [147, recently published meta-analysis, the chance of acquir- 148]. Thereby, the eggs are immunologically confined ing HIV among people suffering from schistosomiasis within the so-called “granulomas”, containing proteolytic was 2.3-fold (95% CI: 1.2–4.3%) higher than non-infected Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 11 of 18 Fig. 3 Forest plot of year-based prevalence in Nigeria (2016–2020) Fig. 4 Forest plot of year-based prevalence in Sudan (2016–2020) Shams et al. Tropical Medicine and Health (2022) 50:12 Page 12 of 18 Fig. 5 Forest plot of year-based prevalence in South Africa (2016–2020) Fig. 6 Forest plot of year-based prevalence in Ghana (2016–2020) Fig. 7 Forest plot of year-based prevalence in Malawi (2016–2020) Fig. 8 Forest plot of year-based prevalence in Egypt (2016–2020) Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 13 of 18 patients [158]. Finally, the affected women might experi - and any definite inference must accompany with caution. ence painful intercourse (dyspareunia), fibrotic ovaries Inevitably, implementation of large-scale or nation-wide and/or granuloma-induced tubal blockage, all of which prevalence studies on FUS throughout African nations, lead to the female infertility. Hence, FUS may lead to particularly in neglected regions of the continent, using harsh reproductive outcomes that ultimately endangers microscopy of urine specimen (gold standard method) the fecundity, fertility and pregnancy of women [159]. coupled with unprecedented molecular approaches will The result of the present meta-analysis highlighted that more elucidate the true epidemiological picture of uri- a higher prevalence of FUS was demonstrated by vaginal nary schistosomiasis among women population. Conse- lavage [25.0% (95% CI: 11.4–46.1%)] than urine speci- quently, such information benefits the clinicians for the mens [17.2% (95% CI: 14.5–20.3%)]. Although there was prevention of the horrible sequelae of chronic FUS. not statistically significant difference between the total prevalence of FUS and sample type (P > 0.05). Moreover, the results of current review demonstrated that micros- Conclusion copy 17.1% (95% CI: 14.5–20.1%) contributed more In conclusion, information provided in the present sys- to reveal the FUS prevalence than PCR method 15.3% tematic review and meta-analysis showed that women (95% CI: 6.1–33.2%); nevertheless, only two studies uti- in endemic territories in Africa are moderately at risk lized molecular method for diagnosis, and any deduc- of acquiring FUS and its harsh consequences, including tions should accompany with caution. Notably, urine renal dysfunction, urinary bladder carcinoma as well as filtration (about 10  mL) that is routinely performed for reproductive disorders such as dyspareunia and gran- egg detection was more efficient in detecting parasite uloma-induced infertility. Consequently, health assess- eggs than sedimentation method, with 18.2% (95% CI: ment of FUS should be considered as a routine necessity 5.9–43.9%) versus 11.4% (95% CI: 3.6–30.9%), respec- for women in susceptible age groups such as those in tively. Urine microscopy is the gold standard in detec- active reproductive status and/or child-bearing age. tion of S. haematobium eggs in areas of endemicity [160]. Relying only on low-sensitivity microscopic results can- However, it is not sensitive sufficiently for monitoring not rule out the presence of schistosomes in blood ves- praziquantel therapeutic efficiency in mass drug admin - sels. Hence, clinical assessment must be performed using istration (MDA) campaigns, particularly in low-trans- gold standard methods, i.e., microscopic examination of mission intensity areas, because weeks after adult worm urine samples, combined with highly sensitive and spe- elimination eggs are still observable in urine or some cific molecular approaches. Altogether, our goal on bet - worms may have temporarily stopped shedding eggs ter control and prevention of urinary schistosomiasis [161]. Also, it lacks adequate sensitivity, due to the fact may not be achievable, unless by a global collaboration that eggs are only detectable in urine samples 2  months to accurately reveal the parasite epidemiology in endemic after infection onwards [162]. Therefore, it is highly rec - territories. ommended to carry out at least two follow-up visits and microscopic examination for more accurate diagnosis Abbreviations [163]. Additionally, in order to enhance the sensitivity UGS: Urogenital schistosomiasis; BCE: Before common era; WHO: World Health and specificity and deter underestimation of the true dis - Organization; PCR: Polymerase chain reaction; FUS: Female urinary schis- tosomiasis; PRISMA: Preferred Reporting Items for Systematic Reviews and ease burden, performing highly sensitive methods such Meta-analyses; MeSH: Medical subject heading; CI: Confidence interval; CMA: as molecular techniques are inevitable [21]. As men- Comprehensive meta-analysis; HIV-1: Human immunodeficiency virus-1; MDA: tioned earlier, only two studies in the last 5  years used Mass drug administration. PCR method, which exhibited a remarkable prevalence rate for FUS, implicating the importance of such modali- Supplementary Information ties in accurate detection of urinary schistosomiasis. The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s41182- 022- 00402-x. The present systematic review and meta-analysis met some limitations, including: (1) lack of adequate preva- Additional file 1. PRISMA checklist employed for the present systematic lence studies in countries other than Nigeria; (2) diag- review. nosis of the infection mostly based on microscopic Additional file 2. Forest plot of the FUS prevalence obtained from pub - examination of urine samples; (3) inadequate number lished literature during 2016–2020. of molecular-based studies in the last 5  years, and (4) Additional file 3. Quality assessment analysis of the included papers due to the nature of the systematic review and meta- using Newcastle–Ottawa scale. analysis studies, which exclude some papers relied on a designed inclusion criteria, the provided results are only Acknowledgements based on the information extracted from 113 datasets Not applicable. Shams et al. Tropical Medicine and Health (2022) 50:12 Page 14 of 18 Authors’ contributions 8. 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Prevalence of urinary schistosomiasis in women: a systematic review and meta-analysis of recently published literature (2016–2020)

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Abstract

Background: Urinary schistosomiasis is a serious threat in endemic territories of Africa and the Middle East. The sta- tus of female urinary schistosomiasis (FUS) in published literature between 2016 and 2020 was investigated. Methods: A systematic search in PubMed, Scopus, Google Scholar, and Web of Science, based on the ‘Preferred Reporting Items for Systematic Reviews and Meta-analyses’ checklist, and a meta-analysis using random-effects model to calculate the weighted estimates and 95% confidence intervals (95% CIs) were done. Results: Totally, 113 datasets reported data on 40,531 women from 21 African countries, showing a pooled preva- lence of 17.5% (95% CI: 14.8–20.5%). Most studies (73) were performed in Nigeria, while highest prevalence was detected in Mozambique 58% (95% CI: 56.9–59.1%) (one study). By sample type and symptoms, vaginal lavage [25.0% (95% CI: 11.4–46.1%)] and hematuria 19.4% (95% CI: 12.2–29.4%) showed higher FUS frequency. Studies using direct microscopy diagnosed a 17.1% (95% CI: 14.5–20.1%) prevalence rate, higher than PCR-based studies 15.3% (95% CI: 6.1–33.2%). Except for sample type, all other variables had significant association with the overall prevalence of FUS. Conclusions: More studies are needed to evaluate the true epidemiology of FUS throughout endemic regions. Keywords: Epidemiology, Urinary schistosomiasis, Women, Meta-analysis Background subtropical territories and renders approximately 70 Schistosomiasis, due to trematodes of the genus Schis- million disability-adjusted life years [1–3]. In endemic tosoma (blood flukes), is a snail-transmitted hel - areas such as sub-Saharan Africa morbidity is higher minthiasis and the third most degenerative tropical among school-aged children (60–80%) than adults disease with substantial morbidity/mortality rates, (20–40%), with a mortality rate of 280,000 people [4]. particularly in low- and middle-income countries [1]. Six species out of 24 recognized schistosomes result in With about 800 million at-risk individuals, schistoso- disease in humans, comprising Schistosoma haemato- miasis afflicts over 250 million people in tropical and bium (S. haematobium) the causative agent of urogeni- tal schistosomiasis (UGS), S. japonicum, S. mansoni, S. intercalatum, S. mekongi and S. guineensis as agents of hepato-intestinal disease [5]. In a public health per- *Correspondence: asghari3@yahoo.com Department of Medical Parasitology and Mycology, School of Medicine, spective, Africa and the Mideast (S. mansoni and S. Shiraz University of Medical Sciences, Shiraz, Iran haematobium), Southeast Asia (S. japonicum) and Full list of author information is available at the end of the article © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Shams et al. Tropical Medicine and Health (2022) 50:12 Page 2 of 18 Latin America (S. mansoni) are considered as the most Methods distinguished geographical hotspots for schistosomiasis The present systematic review and meta-analysis was [6]. Adult paired worms would stay alive in host’s blood accomplished on the basis of Preferred Reporting Items stream for about 3–10  years and produce numerous for Systematic Reviews and Meta-analyses (PRISMA) spiny eggs, rendering chronicity and pathologic out- statement [24] (Additional file 1). comes of the infection [7–9]. The putative signs and symptoms of UGS were ini - Information sources and systematic searching tially ascribed about 1900 Before the Common Era Major English databases including Scopus, PubMed, (BCE), when hematuria was a common finding in Egyp - Web of Science and Google Scholar were systematically tian males, referred to as “menstruation” [10]. Infected searched for articles evaluating the prevalence of FUS planorbid snails, Bulinus spp., are intermediate hosts worldwide and published during a 5-year time period, releasing motile furcocercous cercariae in surround- from January 2016 until the end of 2020. This proce - ing water supplies. Following skin cercarial invasion and dure was conducted using the following keywords alone migration thorough lungs and liver, S. haematobium or in combination, using advanced search option in worms would finally lodge in the genitourinary venous most databases and Medical Subject Heading (MeSH) complex, in particular bladder veins, where they mature option in PubMed databases: “Urinary Schistosomiasis” and copulate therein [11]. Although harsh disease out- AND “Prevalence” OR “Epidemiology” AND “Female” comes primarily arise from the T-cell mediated, granu- OR “Women” Or “Girl”, where “AND” and/or “OR” are lomatous immune responses against tissue-deposited Boolean operators. Hand-searching of the bibliographic spiny eggs of schistosomes. Such lesions would represent list of related papers was an additional task to more manifestations comprising hematuria, dysuria, itching, cover those papers not found via database exploration. pelvic pain, as well as the life-threatening squamous cell Briefly, title and abstract of the literature were accurately carcinoma of the urinary bladder [12, 13]. Additionally, reviewed (H.M. and M.F.), relevant papers were included, S. haematobium is responsible of egg-induced patho- and upon duplicate removal, full-texts of eligible papers logical lesions and associated symptoms in both men and were retrieved (T.N.). Any disagreements were obviated women [14, 15]. by discussion and consensus with the leading researchers An active UGS could be detected through observation (M.SH and A.A.). of eggs in urine sediments and/or tissue biopsies [16]. For the aim of determining hotspots and control strategies, Inclusion/exclusion criteria and data collection World Health Organization (WHO) has recommended Specific inclusion criteria were determined in order to microscopic-based poly-carbonate filter examination for thoroughly gather relevant peer-reviewed cross-sec- urinary eggs as well as dipstick assays for urinary heme tional studies and conference reports limited to women detection [17, 18]. Serodiagnostic assays identifying anti- population in a 5-year time period (2016–2020). Only bodies against worm antigens may demonstrate valuable those papers with specified sample size and number of credibility in symptomatic travelers, whereas they usually FUS-positive women, diagnosed either by microscopic, fail to differentiate active or previous infections, unless filtration, sedimentation and/or molecular techniques those employing circulating antigens [19, 20]. An encour- were included in current systematic review. Other study aging degree of sensitivity and specificity have been types (case reports, letters, reviews), studies evaluating gained in utilization of molecular assays such as poly- animals or other Schistosomal infections, investigations merase chain reaction (PCR) for schistosome detection without sample size/prevalence rates or lacking full-texts in human serum and urine samples [21]. This method is, were all excluded from the present systematic review and also, beneficial for vaginal lavage analysis, revealing the meta-analysis. Finally, a pre-designed Microsoft Excel likely traits of the genital schistosomiasis [22]. Spreadsheet was used to extract the required informa- A very large number of female urinary schistosomiasis tion (E.J. and S.B.), as follows: first author’s last name, (FUS) studies were performed during the last two dec- publication year, start and end years of studies, study ades [23]. The emphasis of the present systematic review type, country, province, city, sample type, diagnostic and meta-analysis was on the published literature during method, sample size, positive number of infected cases the last 5 years (2016–2020), in order to define the latest and clinical symptoms (hematuria and proteinuria). status of FUS and its prevalence based on examined sub- groups. The novel findings of the present study may alert Quality assessment clinicians to the prevalence of this important helminthia- In the present systematic review, the Newcastle–Ottawa sis and its associated consequences on the genitourinary scale was employed to assess the quality of included stud- system of infected female individuals. ies. Those papers with the scores of < 3.5, 3.6–5.25, and Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 3 of 18 5.26–7 were categorized as low-, moderate-, and high- All analytical functions were applied by Comprehensive quality papers, respectively [25]. Meta-analysis (CMA) version 2.2. (Biostat Inc., USA). Results Data synthesis and meta‑analysis The flow diagram of the systematic search process and Meta-analytical approach was done according to pre- inclusion of relevant papers is shown in Fig.  1. Initially, vious studies (S.B. and D.A.) using a random-effects 3537 datasets were identified through comprehensive model [26–28]. For all included studies, point estimates database exploration. After removing duplicates (1821) and their respective 95% confidence intervals (CIs) of and those with irrelevant title and abstract (1571), 145 weighted prevalence were calculated. Heterogeneity datasets were finally assessed for eligibility. Among these, among these studies or variation in study outcomes was 35 datasets were excluded with reasons (review papers, visualized by drawing forest plots, calculated by I and theses, conference papers and studies with confus- Cochrane’s Q tests [29, 30]. The subgroup analysis was ing data) and 3 additional datasets were added through performed based on year, country, sample type, symp- manual searching. Therefore, 106 articles containing toms and diagnostic methods. The presence of publica - 113 datasets were finally included in our meta-analysis tion bias was estimated by using Egger’s regression test (Table 1) [33–139]. [31]. This kind of bias, if present, skews the results and Finally, 113 datasets evaluating 40,531 individuals were published reports are not a representative sample of the included in the present review. Among these, 11,308 available evidence anymore. The trim-and-fill method individuals were shown to be affected by FUS and based was, also, used to “estimate the number of missing stud- on the random-effects model meta-analysis, the pooled ies that might exist in a meta-analysis and the effect that prevalence of FUS was 17.5% (95% CI: 14.8–20.5%). The these studies might have had on its outcome” [32]. P-val- included studies demonstrated a strong heterogene- ues less than 0.05 were considered statistically significant. ity (I = 98.12%, P < 0.01) (Additional file  2). Publication Fig. 1 PRISMA flow diagram describing included/excluded studies on FUS prevalence (2016–2020) Shams et al. Tropical Medicine and Health (2022) 50:12 Page 4 of 18 Table 1 Detailed characteristics of the included studies in the present systematic review and meta-analysis (2016–2020) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 1 Awosolu, 2020 Nigeria Osun and 2012 Urine Filtrations and 258 122 5 [56] Kwara microscopic examination 2 Olayinka, 2020 Nigeria Ogun 2015–2017 Urine Microscopic 280 42 6 [112] examination 3 Awosolu, 2019 Nigeria Ikota 2015 Urine Microscopic 74 20 7 [55] examination 4 Otuneme, 2019 Nigeria Ogun 2017 Urine Microscopic 47 39 5 [118] examination 5 Muhammad, Nigeria Sokoto NR Urine Microscopic 107 47 5 2019 [101] examination 6 Sule, 2019 [129] Nigeria Kano NR Urine Microscopic 56 0 6 examination 7 Idris, 2019 [87] Nigeria New-Bussa NR Urine Microscopic 24 2 7 examination 8 Geraji, 2019 [81] Nigeria Jalingo 2019 Urine Microscopic 86 13 7 examination 9 Adamu, 2019 Nigeria Kaduna 2017 Urine Microscopic 136 4 7 [36] examination 10 Ngwamah, 2019 Nigeria Adamawa NR Urine Microscopic 679 141 7 [105] examination 11 Aribodor, 2019 Nigeria Enugu 2016 Urine Microscopic 121 17 7 [51] examination 12 Sobande, 2019 Nigeria Ogun NR Urine Microscopic 84 40 6 [128] examination 13 Obisike, 2019 Nigeria Benue 2017 Urine Membrane 84 20 5 [110] filtration and (sedimentation) microscopic examination 14 Ahmed, 2019 Nigeria Katsina NR Urine (sedimentation) 68 15 6 [40] Microscopic examination 15 Aderibigbe, Nigeria Kwara NR Urine Microscopic 883 293 7 2019 [37] examination 16 Noriode, 2018 Nigeria Edo NR Urine Microscopic 109 75 5 [106] examination 17 Bishop, 2016 Nigeria Kaduna NR Urine Microscopic 92 5 6 [164] examination 18 Mohammed, Nigeria Sokoto 2016 Urine Microscopic 51 18 5 2018 [95] examination 19 Akinneye, 2018 Nigeria Ondo NR Urine Microscopic 202 22 5 [43] examination 20 Alabi, 2018 [46] Nigeria Ogun NR Urine Microscopic 73 36 6 examination 21 Damen, 2018 Nigeria Plateau NR Urine Microscopic 7 1 6 [68] examination 22 Yauba, 2018 Nigeria Maiduguri 2014–2015 Urine Microscopic 180 113 7 [138] examination 23 Abdulkareem, Nigeria Kwara NR Urine Microscopic 309 131 7 2018 [34] examination 24 Oladeinde, 2018 Nigeria Edo 2014 Urine Microscopic 98 8 6 [111] examination 25 Ebong, 2018 Nigeria Akwa Ibom NR Urine Microscopic 199 5 7 [70] examination Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 5 of 18 Table 1 (continued) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 26 Akeju Adebayo, Nigeria Ondo NR Urine Microscopic 1022 441 5 2018 [42] examination 27 Oluwole, 2018 Nigeria Ogun 2013 Urine Microscopic 1034 43 6 [114] examination 28 Adewale, 2018 Nigeria Ondo NR Urine Microscopic 190 44 6 [38] examination 29 Nwachukwu, Nigeria Imo 2014–2016 Urine Test strip and 1125 57 7 2018 [107] filtration 30 Nwachukwu, Nigeria Ebonyi 2016–2017 Urine Microscopic 254 8 7 2018 [108] examination 31 Duwa, 2018 [69] Nigeria Kano 2018 Urine Microscopic 105 8 5 examination 32 Babagana, 2018 Nigeria Borno NR Urine Microscopic 180 31 7 [57] examination 33 Mohammed, Nigeria Kebbi 2016 Urine (Filtration) 81 16 5 2018 [94] Microscopic examination 34 Oluwole, 2018 Nigeria Ogun NR Urine and vainal Microscopic 317 149 6 [114] lavage and gyneco- logic examina- tion 35 Kenneth, 2017 Nigeria Edo NR Urine Microscopic 76 6 7 [92] examination 36 Birma, 2017 [61] Nigeria Adamawa NR Urine Microscopic 90 42 5 examination 37 Amoo, 2017 [47] Nigeria Ogun NR Urine Microscopic 160 61 6 examination 38 Paul, 2017 [119] Nigeria Cross River NR Urine Microscopic 140 24 5 examination 39 Orpin, 2017 Nigeria Katsina NR Urine Microscopic 145 12 5 [116] examination 40 Ekanem, 2017 Nigeria South-South 2011 Urine Microscopic 177 27 6 [71] examination 41 Akpan, 2017 Nigeria Cross River NR Urine Microscopic 208 34 7 [45] examination 42 Elom, 2017 [73] Nigeria Ebonyi NR Urine Microscopic 147 33 7 examination 43 Akpan, 2017 Nigeria Cross River NR Urine Microscopic 122 1 7 [44] examination 44 Abubakar, 2017 Nigeria Jigawa 2015 Urine Microscopic 65 46 7 [35] examination 45 Dalhat, 2017 Nigeria Sokoto NR Urine Microscopic 140 41 7 [67] examination 46 Emmanuel, Nigeria Benue 2014 Urine Microscopic 207 77 6 2017 [75] examination 47 Wokem, 2017 Nigeria Abia NR Urine Microscopic 570 215 7 [135] examination 48 Anorue, 2017 Nigeria Ebonyi 2002–2003 Urine Microscopic 1367 640 6 [49] examination 49 Orpin, 2016 Nigeria Benue NR Urine Microscopic 104 8 7 [117] examination 50 Onile, 2016 Nigeria Eggua 2012–2013 Urine Microscopic 178 45 7 [115] examination 51 Houmsou, 2016 Nigeria Taraba NR Urine Microscopic 529 231 5 [86] examination Shams et al. Tropical Medicine and Health (2022) 50:12 Page 6 of 18 Table 1 (continued) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 52 Goodhead, Nigeria River NR Urine Microscopic 76 17 7 2016 [83] examination 53 Usman, 2016 Nigeria Bauchi NR Urine Microscopic 300 58 7 [133] examination 54 Dahesh, 2016 Nigeria Giza 2016 Urine Microscopic 582 12 7 [66] examination 55 Igbeneghu, Nigeria Osun 2016 Urine Microscopic 154 60 7 2016 [88] examination 56 Nafiu, 2016 Nigeria Niger 2016 Urine Microscopic 97 9 6 [104] examination 57 Abah, 2016 [33] Nigeria River 2016 Urine Microscopic 184 23 5 examination 58 Umar, 2016 Nigeria Kano NR Urine Microscopic 20 9 5 [132] examination 59 Atalabi, 2016 Nigeria Katsina NR Urine Microscopic 240 14 6 [52] examination 60 Houmsou, 2016 Nigeria Taraba NR Urine Microscopic 510 3 7 [86] examination 61 Nwibari, 2016 Nigeria Plateau NR Urine Microscopic 134 6 5 [165] examination 62 Omoruyi, 2016 Nigeria Edo NR Urine Microscopic 77 4 6 [166] examination 63 Morenikeji, Nigeria Ogun NR Urine Microscopic 79 60 6 2016 [99] examination 64 Bashir, 2016 [60] Nigeria Jigawa NR Urine Microscopic 31 2 7 examination 65 Ganau, 2016 Nigeria Sokoto NR Urine Microscopic 58 24 5 [79] examination 66 Musa, 2016 Nigeria Kaduna NR Urine Microscopic 131 13 6 [102] examination 67 Ajakaye, 2016 Nigeria Ondo NR Urine Microscopic 404 50 7 [41] examination 68 Mong, 2016 [98] Nigeria Abia NR Urine Microscopic 129 13 7 examination 69 Atalabi, 2016 Nigeria Katsina 2015 Urine Microscopic 317 23 6 [53] examination 70 Oluwatoyin, Nigeria Ibadan NR Urine Microscopic 507 1 7 2016 [113]* examination 71 Oluwatoyin, Nigeria Ibadan NR Urine Microscopic 507 28 6 2016 [113] examination 72 Bishop, 2016 Nigeria Kaduna NR Urine Microscopic 251 39 5 [63] examination 73 Maki, 2020 [93] Sudan Darfur 2018 Urine Microscopic 55 39 6 examination 74 Qutoof, 2019 Sudan Khartoum NR Urine Microscopic 589 2 5 [122] examination 75 Elsiddig, 2019 Sudan White Nile 2011 Urine Microscopic 162 67 6 [74] examination 76 Hajissa, 2018 Sudan Khartoum 2017–2018 Urine Microscopic 95 11 6 [85] examination 77 Mohammed, Sudan White Nile NR Urine Microscopic 175 97 7 2018 [96] examination 78 Talab, 2018 Sudan White Nile 2014 Urine (Filtration) 174 97 5 [167] Microscopic examination Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 7 of 18 Table 1 (continued) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 79 Sulieman, 2017 Sudan River Nile 2016 Urine (Sedimentation) 191 1 6 [130] Microscopic examination 80 Sabah Alzain Sudan El khiar 2016 Urine Microscopic 76 7 5 Mohamed, 2017 examination [124] 81 Afifi, 2016 [39] Sudan Kassala 2013 Urine Microscopic 1238 172 6 examination 82 Elhusein, 2016 Sudan Gezira 2016 Urine Microscopic 29 0 7 [72] examination 83 Shukla, 2019 South Africa KwaZulu-Natal 2011–2013 Urine and Microscopic 933 256 5 [126] cervico-vaginal examination lavage 84 Galappaththi- South Africa KwaZulu-Natal NR Urine Microscopic 1123 292 5 Arachchige, examination 2018 [78] 85 Kabuyaya, 2017 South Africa uMkhanyakude 2015 Urine Microscopic 199 73 7 [89] examination 86 Galappaththi- south Africa KwaZulu-Natal NR Urine Microscopic 883 270 6 Arachchige, examination 2016[168] 87 Pillay, 2016 South Africa KwaZulu-Natal 2010–2012 vaginal lavages PCR 394 38 7 [169] and Urine 88 South Africa KwaZulu-Natal 2010–2012 Urine PCR 394 91 7 89 South Africa KwaZulu-Natal 2010–2012 Urine Microscopic 394 78 7 examination 90 Fokuo, 2020 [76] Ghana Asutsuare 2014 Urine Microscopic 59 8 6 examination 91 Arhin-Wiredu, Ghana Akyemansa 2014 Urine Microscopic 161 10 6 2019 [50] examination 92 Nyarko, 2018 Ghana different munic- 2016 Urine Microscopic 173 7 6 [109] ipal-ities examination 93 Boye, 2016 [65] Ghana Apewosika and 2013 Urine Microscopic 114 16 5 Putubiw examination 94 Wilkinson, 2018 Malawi Lilongwe 2013 Urine Microscopic 96 2 6 [134] examination 95 Kayuni, 2017 Malawi Mangochi 2012 Urine Microscopic 226 29 6 [91] examination 96 Moyo, 2016 Malawi Nkhotakota NR Urine Microscopic 51 6 6 [100] examination 97 Yameny, 2018 Egypt El-Fayoum NR Urine Microscopic 487 33 7 [137] examination 98 Ghieth, 2017 Egypt Beni Suef NR Urine Microscopic 220 0 5 [82] examination 99 Kaiglova, 2020 Kenya Kwale 2018 Urine Microscopic 323 47 5 [90] examination 100 Mutsaka- Zimbabwe Mashonaland 2010 Urine Microscopic 569 96 6 Makuvaza, 2019 examination [103] 101 Woldegerima, Ethiopia Sanja 2017–2018 Urine Microscopic 189 53 7 2019 [136] examination 102 Phillips, 2018 Mozambique Cabo Delgado 2011 Urine Microscopic 7538 4372 7 [120] examination 103 Gbalegba, 2017 Mauritania Kaedi 2014–2015 Urine Microscopic 1064 54 6 [80] examination Shams et al. Tropical Medicine and Health (2022) 50:12 Page 8 of 18 Table 1 (continued) No. References Country Province/city Time Sample type Method Sample size Positive no Quality of data assessment collection score 104 Simoonga, 2017 Zambia Lusaka NR Urine Microscopic 954 83 7 [127] examination 105 Balahbib, 2017 Morocco Tata 2015 Urine Microscopic 13 0 6 [58] examination 106 Anchang-Kimbi, Cameroon Mount Cam- 2014 Urine Microscopic 250 117 7 2017 [48] eroon examination 107 Mombo- Gabon Lambarene 2009–2013 Urine Microscopic 1115 103 7 Ngoma, 2017 examination [97] 108 Greter, 2016 [84] Chad Chad NR Urine (Filtration) 96 1 7 Microscopic examination 109 Botelho, 2016 Guinea-Bissau Guinea-Bissau NR Urine Microscopic 43 8 6 [64] examination 111 Senghor, 2016 Senegal Niakhar 2011–2014 Urine Microscopic 320 149 5 [125] examination 111 Rasomanami- Madagascar Madagascar 2015 Urine Microscopic 1043 325 5 haja, 2016 [123] examination 112 Bangura, 2016 Sierra Leon Korwama and 2015 Urine Microscopic 86 32 7 [59] Lewabu examination 113 Zida, 2016 [139] Burkina Faso Bazega 2013 Urine Microscopic 151 7 7 examination *In this dataset, S. mansoni was found in urine instead of S. haematobium bias was checked by Egger’s regression test, showed that women, with vaginal lavage demonstrating a higher it may have a substantial impact on total prevalence frequency of FUS [25.0% (95% CI: 11.4–46.1%)] than estimate (Egger’s bias: 7.5, P < 0.01) (Fig.  2). Since the urine specimen [17.2% (95% CI: 14.5–20.3%)]. Report- heterogeneity of included studies was very high, meta- edly, hematuria and proteinuria as the most promi- regression of subgroups such as year, country, type of nent symptoms of FUS were estimated in some studies, sample, type of symptoms, and diagnostic method were showing 19.4% (95% CI: 12.2–29.4%) and 13.6% (95% CI: used to overcome heterogeneity (Table  2). According 6.69–24.8%) prevalence rates, correspondingly. Direct to subgroup analysis of included data, the prevalence of microscopy was the most frequently utilized diagnostic FUS demonstrated a relatively but worrying increasing test, yielding a relatively higher prevalence 17.1% (95% trend from 14.6% (95% CI: 11.3–18.6%) in 2016 to 28.6% CI: 14.5–20.1%) than PCR method 15.3% (95% CI: 6.1– (95% CI: 13.1–51.6%) in 2020, respectively. In total, stud- 33.2%); however, only two studies employed molecular ies were conducted in 21 countries, including Nigeria (73 method. Additional microscopy-based procedures were datasets), Sudan (10 datasets), South Africa (7 datasets), filtration and sedimentation, which in detail yielded a Ghana (4 datasets), Malawi (3 datasets), Egypt (2 data- prevalence rate of 18.2% (95% CI: 5.9–43.9%) and 11.4% sets), as well as Kenya, Zimbabwe, Ethiopia, Mozam- (95% CI: 3.6–30.9%), respectively. Altogether, subgroup bique, Mauritania, Zambia, Morocco, Cameroon, Gabon, analysis revealed that there were statistically significant Chad, Guinea-Bissau, Senegal, Madagascar, Sierra Leone differences between the overall prevalence of FUS and and Burkina Faso (one dataset per country). The highest year. Of note, the quality score of the included papers is prevalence rates were estimated for women in Mozam- provided in Additional file 3. bique with 58% (95% CI: 56.9–59.1%) (one study), while female individuals in Chad had the lowest prevalence rate Discussion 1.0% (95% CI: 0.1–7.0%). Year-based prevalence for the Helminth-induced diseases are ancient catastrophic phe- six most studied countries, showed no determined pat- nomena in humans, some dating back to pre-biblical era, tern for frequency of FUS, however, a relatively decreas- with huge but chronic and snaky damages in nature [140]. ing pattern of prevalence was recorded for Malawi (three Schistosomiasis or bilharziasis is one of the most impor- studies) (Figs.  3, 4, 5, 6, 7, 8). Regarding sample type, tant water-borne helminthic diseases, which have always urine and vaginal lavage were gathered from examined been interconnected with archaic civilizations over the Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 9 of 18 Fig. 2 A bias assessment plot from Egger for the FUS prevalence (2016–2020) millennia, and it is still a global public health concern due last 5  years were from African countries. This continent to its astonishing, complex life cycle [141, 142]. Among is probably known as the “cradle of schistosomes”, since schistosome species infecting humans, S. haematobium African great lakes provide a favorable milieu for the worms are the causative agents of UGS which localize optimum evolution of both parasites and their respec- within draining venous complex of the pelvic organs such tive intermediate hosts [144]. Schistosomiasis may have as uterus, cervix and the bladder [143]. These worms spread to Africa, particularly Egypt, in virtue of mon- are highly prolific, releasing about 3000 eggs/day, half key importation and slave trades during fifth dynasty of of which are excreted through urine, while the rest are pharaohs [145]. Based on our results obtained from lim- lodged within vasculature of urogenital organs. Immune- ited number of heterogeneous investigations included in mediated pathologic processes elicited against tissue- the present meta-analysis, a large number of studies (73) embedded ova result in granulomatous inflammation, on FUS were done in a western African nation, Nigeria, tissue destruction and the so-called “sandy patches” as whereas the highest prevalence rate was estimated for fibrotic nodules [16]. With respect to the significance of women in Mozambique with 58% (95% CI: 56.9–59.1%) UGS and large number of affected individuals, the pre - (one study), a country in the southeast coast of Africa. sent systematic review and meta-analysis was contrived Nigerian researchers have shown a substantial effort in in order to reveal the latest status of urinary schistosomi- search of urinary schistosomiasis during last 5  years by asis in women population based on published literature conducting 73 datasets, which could be a favorable layout in the last 5 years and provide a premise for future clini- for other African countries [143]. Nevertheless, the true cal directions on women health. picture of FUS prevalence throughout African territories The required information was assembled from availa - in a 5-year time period was not accurately captured, since ble full-texts published between 2016 and 2020 and their out of 21 countries examining female individuals, only 6 overall estimates were assessed through a meticulous countries had sufficient studies to perform meta-analyt - meta-analytical method. During last 5  years, 11,308 out ical approach and most of the remaining had only one of 40,531 women were suffering from urinary schistoso - investigation per country. Moreover, a statistically sig- miasis, contributing to the global weighted prevalence of nificant gradual increase was observed in FUS prevalence 17.5% (95% CI: 14.8–20.5%). Interestingly, all cases in the based on publication year of the included literature, from Shams et al. Tropical Medicine and Health (2022) 50:12 Page 10 of 18 Table 2 Subgroup analysis of FUS prevalence according to year, country, type of sample, type of symptoms and diagnostic methods Subgroup variable Prevalence % (95% CI) I (%) Heterogeneity (Q) P‑ value Interaction P‑ value test (X ) Year 2016 14.6 (11.3–18.6) 96.3% 1034.7 < 0.01 375.3 < 0.01 2017 17.5 (12–24.9) 97.8% 1055.2 < 0.01 2018 19.0 (13.1–26.7) 98.8% 2179.6 < 0.01 2019 21.7 (16.8–27.5) 93.4% 274.7 < 0.01 2020 28.6 (13.1–51.6) 97.1% 138.2 < 0.01 Country Ghana 9.1 (6.8–12.2) 73.46% 11.31 < 0.01 Malawi 11.4 (0.8–15.4) 70.62% 6.81 < 0.01 Nigeria 21.1 (17.6–25.0) 96.9% 2337.91 < 0.01 South Africa 27.4 (25.6–29.2) 92.53% 80.36 < 0.01 Sudan 55.8 (43.9–67.1) 97.59% 374.17 < 0.01 430.6 < 0.01 Egypt 1.7 (0.1–32.8) 83.57 5.90 < 0.01 Type of sample Urine 17.2 (14.5–20.3) 98.11% 5949.4 < 0.01 1285.2 > 0.05 Vaginal lavage 25.0 (11.4–46.1) 98.2% 110.40 < 0.01 Type of symptoms Hematuria 19.4 (12.2–29.4) 92.33% 52.19 < 0.01 82.4 < 0.01 Proteinuria 13.6 (6.69–24.8) – 0.00 = 1.00 Diagnostic method Direct microscopy 17.1 (14.5–20.1) 98.1% 6013 < 0.01 350.6 < 0.01 Filtration and microscopy 18.2 (5.9–43.9) 99.1% 563.1 < 0.01 PCR 15.3 (6.1–33.2) 95.9% 24.64 < 0.01 Sedimentation and microscopy 11.4 (3.6–30.9) 96.6% 59.5 < 0.01 2016 until the end of 2020, ranging from 14.6% (95% CI: enzymes of egg origin that barricade tissue necrosis 11.3–18.6%) to 28.6% (95% CI: 13.1–51.6%), respectively. [149]. In accordance with our finding, hematuria is con - However, no such an increasing trend was observed in sidered as a defining symptom in S. haematobium infec - year-based analysis of each country; even the prevalence tion, mostly being accompanied by suprapubic ailment, relatively decreased in Malawi, though only three studies burning micturition as well as frequent urination [150]. were involved in this country. Such findings derived from Poor immunoregulatory mechanisms in response to eggs limited number of included studies in current review provoke a lasting fibrotic reaction in the urinary tract may be interpreted as a spread of the endemic situation of infected individuals [151]. The resulting obstructive of FUS, or as a result of the increased understanding uropathy elicit subsequent dreadful consequences such about FUS among health care professionals in each coun- as the hydroureter and hydronephrosis [152]. The latter try. Nevertheless, more in-depth studies are required to is the milestone in ascending bacterial superinfections, further elucidate this issue. renal dysfunctions and the ensuing proteinuria [153]. The The characteristic symptoms of UGS were prominently consequences are more horrific in affected women, since reported among examined women, so that a higher prev- the proximity of vesical and genital venous plexuses facil- alence rate was recorded for hematuria with 19.4% (95% itates easy migration of parasites and/or eggs, leading to CI: 12.2–29.4%), in comparison to 13.6% (95% CI: 6.69– harsh outcomes regarding women’s reproductive health 24.8%) frequency of proteinuria. As previously men- [154–156]. The subsequent lesions in genital organs, tioned, disease morbidity largely results from entrapped from ovaries to vagina, may be associated with pain and eggs, which strongly induce a granulomatous immune stress, allowing human immunodeficiency virus-1 (HIV- response [146], characterized by Th2-type lymphocytes, 1) to simply access sub-epithelial target cells [157]. In a alternatively activated macrophages and eosinophils [147, recently published meta-analysis, the chance of acquir- 148]. Thereby, the eggs are immunologically confined ing HIV among people suffering from schistosomiasis within the so-called “granulomas”, containing proteolytic was 2.3-fold (95% CI: 1.2–4.3%) higher than non-infected Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 11 of 18 Fig. 3 Forest plot of year-based prevalence in Nigeria (2016–2020) Fig. 4 Forest plot of year-based prevalence in Sudan (2016–2020) Shams et al. Tropical Medicine and Health (2022) 50:12 Page 12 of 18 Fig. 5 Forest plot of year-based prevalence in South Africa (2016–2020) Fig. 6 Forest plot of year-based prevalence in Ghana (2016–2020) Fig. 7 Forest plot of year-based prevalence in Malawi (2016–2020) Fig. 8 Forest plot of year-based prevalence in Egypt (2016–2020) Shams  et al. Tropical Medicine and Health (2022) 50:12 Page 13 of 18 patients [158]. Finally, the affected women might experi - and any definite inference must accompany with caution. ence painful intercourse (dyspareunia), fibrotic ovaries Inevitably, implementation of large-scale or nation-wide and/or granuloma-induced tubal blockage, all of which prevalence studies on FUS throughout African nations, lead to the female infertility. Hence, FUS may lead to particularly in neglected regions of the continent, using harsh reproductive outcomes that ultimately endangers microscopy of urine specimen (gold standard method) the fecundity, fertility and pregnancy of women [159]. coupled with unprecedented molecular approaches will The result of the present meta-analysis highlighted that more elucidate the true epidemiological picture of uri- a higher prevalence of FUS was demonstrated by vaginal nary schistosomiasis among women population. Conse- lavage [25.0% (95% CI: 11.4–46.1%)] than urine speci- quently, such information benefits the clinicians for the mens [17.2% (95% CI: 14.5–20.3%)]. Although there was prevention of the horrible sequelae of chronic FUS. not statistically significant difference between the total prevalence of FUS and sample type (P > 0.05). Moreover, the results of current review demonstrated that micros- Conclusion copy 17.1% (95% CI: 14.5–20.1%) contributed more In conclusion, information provided in the present sys- to reveal the FUS prevalence than PCR method 15.3% tematic review and meta-analysis showed that women (95% CI: 6.1–33.2%); nevertheless, only two studies uti- in endemic territories in Africa are moderately at risk lized molecular method for diagnosis, and any deduc- of acquiring FUS and its harsh consequences, including tions should accompany with caution. Notably, urine renal dysfunction, urinary bladder carcinoma as well as filtration (about 10  mL) that is routinely performed for reproductive disorders such as dyspareunia and gran- egg detection was more efficient in detecting parasite uloma-induced infertility. Consequently, health assess- eggs than sedimentation method, with 18.2% (95% CI: ment of FUS should be considered as a routine necessity 5.9–43.9%) versus 11.4% (95% CI: 3.6–30.9%), respec- for women in susceptible age groups such as those in tively. Urine microscopy is the gold standard in detec- active reproductive status and/or child-bearing age. tion of S. haematobium eggs in areas of endemicity [160]. Relying only on low-sensitivity microscopic results can- However, it is not sensitive sufficiently for monitoring not rule out the presence of schistosomes in blood ves- praziquantel therapeutic efficiency in mass drug admin - sels. Hence, clinical assessment must be performed using istration (MDA) campaigns, particularly in low-trans- gold standard methods, i.e., microscopic examination of mission intensity areas, because weeks after adult worm urine samples, combined with highly sensitive and spe- elimination eggs are still observable in urine or some cific molecular approaches. Altogether, our goal on bet - worms may have temporarily stopped shedding eggs ter control and prevention of urinary schistosomiasis [161]. Also, it lacks adequate sensitivity, due to the fact may not be achievable, unless by a global collaboration that eggs are only detectable in urine samples 2  months to accurately reveal the parasite epidemiology in endemic after infection onwards [162]. Therefore, it is highly rec - territories. ommended to carry out at least two follow-up visits and microscopic examination for more accurate diagnosis Abbreviations [163]. Additionally, in order to enhance the sensitivity UGS: Urogenital schistosomiasis; BCE: Before common era; WHO: World Health and specificity and deter underestimation of the true dis - Organization; PCR: Polymerase chain reaction; FUS: Female urinary schis- tosomiasis; PRISMA: Preferred Reporting Items for Systematic Reviews and ease burden, performing highly sensitive methods such Meta-analyses; MeSH: Medical subject heading; CI: Confidence interval; CMA: as molecular techniques are inevitable [21]. As men- Comprehensive meta-analysis; HIV-1: Human immunodeficiency virus-1; MDA: tioned earlier, only two studies in the last 5  years used Mass drug administration. PCR method, which exhibited a remarkable prevalence rate for FUS, implicating the importance of such modali- Supplementary Information ties in accurate detection of urinary schistosomiasis. The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s41182- 022- 00402-x. The present systematic review and meta-analysis met some limitations, including: (1) lack of adequate preva- Additional file 1. PRISMA checklist employed for the present systematic lence studies in countries other than Nigeria; (2) diag- review. nosis of the infection mostly based on microscopic Additional file 2. Forest plot of the FUS prevalence obtained from pub - examination of urine samples; (3) inadequate number lished literature during 2016–2020. of molecular-based studies in the last 5  years, and (4) Additional file 3. Quality assessment analysis of the included papers due to the nature of the systematic review and meta- using Newcastle–Ottawa scale. analysis studies, which exclude some papers relied on a designed inclusion criteria, the provided results are only Acknowledgements based on the information extracted from 113 datasets Not applicable. Shams et al. Tropical Medicine and Health (2022) 50:12 Page 14 of 18 Authors’ contributions 8. Warren KS, Mahmoud AA, Cummings P, Murphy DJ, Houser HB. MS, SK and AA conceived the study protocol; SK, HM and SB performed the Schistosomiasis mansoni in Yemeni in California: duration of infection, systematic search; EJ and SB extracted the required information from included presence of disease, therapeutic management. Am J Trop Med Hyg. papers; SB, EJ and DA performed the meta-analytical approach; NN, MF, EG 1974;23(5):902–9. and TN wrote the manuscript draft; MS and AA critically revised the manu- 9. Anisuzzaman SF, Prodjinotho UF, Bhattacharjee S, Verschoor A, da Costa script. All authors have read and approved the manuscript. CP. Host-specific serum factors control the development and survival of Schistosoma mansoni. Front Immunol. 2021;12. Funding 10. Ansari N. Epidemiology and control of schistosomiasis (bilharziasis). The authors did not receive support from any organization for the submitted Switzerland: CABI; 1973. work. 11. Grevelding CG, Langner S, Dissous C. 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Pillay P, van Lieshout L, Taylor M, Sebitloane M, Zulu SG, Kleppa E, et al. Cervical cytology as a diagnostic tool for female genital schistosomiasis: correlation to cervical atypia and Schistosoma polymerase chain reac- tion. CytoJournal. 2016;13:10. Re Read ady y to to submit y submit your our re researc search h ? Choose BMC and benefit fr ? Choose BMC and benefit from om: : Publisher’s Note fast, convenient online submission Springer Nature remains neutral with regard to jurisdictional claims in pub- lished maps and institutional affiliations. thorough peer review by experienced researchers in your field rapid publication on acceptance support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations maximum visibility for your research: over 100M website views per year At BMC, research is always in progress. Learn more biomedcentral.com/submissions

Journal

Tropical Medicine and Health – Springer Journals

Published: Jan 29, 2022

Keywords: Epidemiology; Urinary schistosomiasis; Women; Meta-analysis

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