BRIEF RESEARCH REPORT published: 09 March 2022 doi: 10.3389/fpubh.2022.778110 Schistosomiasis Among Female Migrants in Non-endemic Countries: Neglected Among the Neglected? A Pilot Study Sílvia Roure 1,2*, Olga Pérez-Quílez 1 , Xavier Vallès 1,3 , Lluís Valerio 1 , Israel López-Muñoz 1 , Laura Soldevila 1,2 , Ariadna Torrella 1 , Gema Fernández-Rivas 4 , Anna Chamorro 5,6,7 and Bonaventura Clotet 5,6,7 1 North Metropolitan International Health Unit Programa de Salud Internacional del Institut Català de la Salut (PROSICS), Badalona, Spain, 2 Infectious Diseases Department, Germans Trias i Pujol University Hospital, Universitat Autònoma de Barcelona, Badalona, Spain, 3 Fundació Institut per la Recerca en Ciències de la Salut Germans Trias i Pujol, Badalona, Spain, 4 Microbiology Department, Germans Trias i Pujol University Hospital, Badalona, Spain, 5 AIDS Research Institute-IrsiCaixa Foundation, Badalona, Spain, 6 Germans Trias i Pujol University Hospital, Universitat Autònoma de Barcelona, Badalona, Spain, 7 Fundació Lluita contra la Sida i les Malaties Infeccioses, Germans Trias i Pujol University Hospital, Badalona, Spain Background: Schistosomiasis among migrant populations in Europe is an Edited by: Judith Kuoh Anchang-Kimbi, underdiagnosed infection, yet delayed treatment may have serious long-term University of Buea, Cameroon consequences. In this study we aimed to characterize the clinical manifestations Reviewed by: of Schistosoma infection among migrant women, and the degree of underdiagnosis. Emily Webb, University of London, United Kingdom Methods: We carried out a prospective cross-sectional study among a migrant Martin Nelwan, population living in the North Metropolitan Barcelona area and coming from Nelwan Institution for Human Resource Development, Indonesia schistosomiasis-endemic countries. We obtained clinical, laboratory and socio- *Correspondence: demographic data from electronic clinical records, as well as information about years Sílvia Roure of residence and previous attendance at health services. Blood sample was obtained sroura.mn.ics@gencat.cat and schistosomiasis exposure was assessed using a specific ELISA serological test. Specialty section: Results: Four hundred and five patients from schistosomiasis-endemic regions were This article was submitted to screened, of whom 51 (12.6%) were female. Seropositivity prevalence was 54.8%, but Infectious Diseases - Surveillance, Prevention and Treatment, considering women alone we found a prevalence of 58.8% (30 out of 51). The median a section of the journal age of the 51 women was 41.0 years [IQR (35–48)] and the median period of residence Frontiers in Public Health in the European Union was 13 years [IQR (10–16)]. Schistosoma-positive women (N = Received: 16 September 2021 Accepted: 11 February 2022 30) showed a higher prevalence of gynecological signs and symptoms compared to Published: 09 March 2022 the seronegative women (96.4 vs. 66.6%, p = 0.005). Among seropositive women, the Citation: median number of visits to Sexual and Reproductive Health unit prior to diagnosis of Roure S, Pérez-Quílez O, Vallès X, schistosomiasis was 41 [IQR (18–65)]. Valerio L, López-Muñoz I, Soldevila L, Torrella A, Fernández-Rivas G, Conclusion: The high prevalence of signs and symptoms among seropositive women Chamorro A and Clotet B (2022) and number of previous visits suggest a high rate of underdiagnosis and/or delayed Schistosomiasis Among Female Migrants in Non-endemic Countries: diagnosis of Schistosoma infection, particularly female genital schistosomiasis, among Neglected Among the Neglected? A migrant females. Pilot Study. Front. Public Health 10:778110. Keywords: female genital schistosomiasis, imported schistosomiasis, migrants females, neglected, migrants doi: 10.3389/fpubh.2022.778110 population in Europe, schistosomiasis in non-endemic countries Frontiers in Public Health | www.frontiersin.org 1 March 2022 | Volume 10 | Article 778110 Roure et al. Schistosomiasis Neglected Among Female Migrants INTRODUCTION June 2021. The inclusion criteria entailed showing signs and symptoms of Schistosoma infection and/or having a background Schistosomiasis is a parasitic infection which is included in the that suggested likely past exposure to the Schistosoma parasite, World Health Organization’s list of neglected tropical diseases. including having been born in an endemic country. Patients with In recent decades, migration to Europe from regions where previous diagnosis or treatment for Schistosoma infection were schistosomiasis is endemic has increased the risk of imported excluded. For each patient included in the study, her clinical infections, which may remain largely underdiagnosed. A recent history (including laboratory and ultrasound explorations), review study estimates the prevalence of infection in sub- records of all previous contacts with the health system’s Sexual Saharan immigrants living in non-endemic countries at 24% (1). and Reproductive Health (SRH) units were obtained from the Applying this figure to the estimated number of immigrants electronic data kept by the health services provider. Additional coming from schistosomiasis-endemic countries now living in basic sociodemographic information including country of our region (Catalonia), there could be as many as 17,000 infected origin and years of residence in the EU was obtained by means individuals, most of them undiagnosed. More specifically, in the of a questionnaire, which included a checklist of the most catchment area of our public health unit (North Metropolitan commonly recognized signs and symptoms of Schistosoma Barcelona), which serves ∼1,300,000 inhabitants (of whom infection and FGS (8–11). Exposure to schistosomiasis was roughly 15% are immigrants from non-EU countries), there confirmed using the standard ELISA SCHISTO-96 serological could be over 5,000 infected individuals (1, 2). Estimation of test (SciMedx Corporation, Denville, NJ, USA) on a blood the real burden of schistosomiasis is hampered by the lack of an serum extracted from participants. Cross-check examination adequate gold standard for diagnosis. Detection of parasite eggs of urine and stool samples was not performed since it did not in urine or stool samples has very low sensitivity and serological add substantial benefit to the screening strategy due to the very testing is considered the most cost-effective diagnostic tool in low yield (3, 4). Proportions were calculated considering as a non-endemic countries (3–5). denominator participants with corresponding data available and Schistosomiasis infection may lead to long-term and chronic stratified by serology results, as shown in Table 1. To detect complications related to the respective organ-specific targets significant differences between groups, we used the Chi-square of the two Schistosoma species most common in Africa, S. or Fisher’s exact test for categorical variables and the Student haematobium (urogenital tract) and S. mansoni (gastrointestinal t-test or Mann–Whitney U-test for continuous variables, where system). The most characteristic chronic complications include appropriate. Logistic regression was used for multivariate chronic renal insufficiency and bladder cancer, as well as a analysis when necessary. Statistical significance was set at p ≤ large number of specific and unspecific morbidities (6). More 0.05. Statistical Package Stata 14.0 was used for all statistical particularly, infection may produce pathological alterations in analyses. The study was approved by the Ethics Committee the genitalia of women, defined as female genital schistosomiasis of the Germans Trias i Pujol University Hospital, the referral (FGS). FGS is mostly caused by S. haematobium. However, S. hospital for the study area. Consent was obtained from all study japonicum and S. mansoni also occasionally affect the genital participants. All women with Schistosoma diagnosis received tract (6). Currently, FGS is considered a common but neglected appropriate treatment with praziquantel, as well as treatment infection, with estimations of global prevalence ranging from 33 for other concomitant conditions (i.e., sexually transmitted to 75% among infected women. FGS thus potentially affects up infections, STIs). to 28 to 64 million among the estimated 85 million of women infected by S. haematobium worldwide (7). FGS prevention and treatment is an important component of the sexual and RESULTS reproductive health care of exposed women. This is particularly concerning since Schistosoma infection is easily treatable with an Between 2016 and 2021 a total of 405 patients originating from effective, safe and low-cost drug (praziquantel). schistosomiasis-endemic countries passed through the screening This pilot study has two main goals: first, to characterize program, of whom 51 (12.6%) were females, a proportion that the clinical manifestations of presumptive Schistosoma infection contrasts with the total proportion of women among sub- among migrant women, and second, to test the hypothesis that Saharan immigrants (28%) (2). Sociodemographic data and there is a significant degree of underdiagnosis among this subset laboratory and imaging results for these women are set out in of the population. It is also hoped that this research will pave Table 1. The most frequent country of origin was Gambia (N = the way for more robust studies that can quantify the rate of 13, 27.1%). Of the 51 women screened, 30 (58.8%) had a positive underdiagnosis and clarify the reasons for it. serology, which was comparable to the observed prevalence among men (53.9%, p = 0.4). The median age was similar between positive and negative groups of women (40.8 vs. 41, METHODS p = 0.9) and the median number of years in the European Union was 13 for both groups, without significant differences We carried out a cross-sectional study which included (p = 0.4). Compared to the seronegative women, those with a all consecutive female patients who attended one of the positive test had a higher prevalence of eosinophilia (62.1 vs. International Health Units of the North Metropolitan Barcelona 14.3% p = 0.001), anemia (82.8 vs. 38.0%, p = 0.001), chronic Health Region for pre-travel counseling between June 2016 and abdominal pain (93.1 vs. 19.1%, p < 0.001), recurring urinary Frontiers in Public Health | www.frontiersin.org 2 March 2022 | Volume 10 | Article 778110 Roure et al. Schistosomiasis Neglected Among Female Migrants TABLE 1 | Baseline sociodemographic information, symptoms of schistosomiasis, gynecological symptoms, laboratory findings and imaging results for 51 sub-Saharan femalesa . Variable Nb Overall Serology + (N = 30) Serology – (N = 21) p-value Socio-demographic data Age (median, IQR) 51 41.0 [35–48] 40.5 [35–48] 41 [36–48] 0.9 Years in the EU (median, IQR) 51 13 (10-16) 13 (11-18) 13 (9-15) 0.4 Country of origin 51 Senegal 11 (22.9) 5 (45.4) 6 (54.5) NA Mali 9 (18.5) 5 (55.5) 4 (44.5) Guinea 5 (10.4) 2 (40.0) 3 (60.0) Gambia 13 (27.1) 10 (76.9) 3 (23.1) Nigeria 3 (6.25) 3 (100) 0 (0) Other 10 (20.8) 6 (60.0) 4 (40.0) Laboratory findings Eosinophiliac 50 21 (42.0) 18 (62.1) 3 (14.3) 0.001 Anemia 50 32 (64.0) 24 (82.8) 8 (38.0) 0.001 Hypertransaminasemia of unknown origin 49 9 (18.4) 7 (24.1) 2 (10) 0.3 Clinical symptoms and findings Chronic abdominal pain 50 31 (62) 27 (93.1) 4 (19.1) <0.001 Recurring urinary tract infections 49 25 (51.0) 19 (67.9) 6 (28.6) 0.006 Dysuria 48 15 (31.3) 14 (51.9) 1 (4.8) <0.001 Haematuria 47 11 (23.4) 10 (38.5) 1 (4.8) 0.01 Gynecological symptoms (overall) 50 41 (83.7) 27 (96.4) 14 (66.7) 0.02 Vaginal discharge 48 31 (64.6) 22 (81.5) 9 (42.9) 0.006 Vaginal pain 40 11 (27.5) 11 (55.0) 0 (0.0) <0.001 Vulvovaginal infections 48 31 (64.6) 23 (85.2) 8 (31.8) 0.001 Pelvic discomfort 44 19 (43.2) 18 (78.3) 1 (4.8) <0.001 Recurrent Candida albicans infections 48 30 (62.5) 22 (81.5) 8 (31.8) 0.002 Genital itching 48 29 (60.4) 20 (74.1) 9 (42.9) 0.03 Menstrual pain/dysmenorrhea 44 5 (11.4) 5 (21.7) 0 (0.0) 0.05 Bleeding after sexual inter course 46 14 (21.7) 14 (53.9) 0 (0.0) <0.001 Amenorrhea 44 9 (20.5) 9 (39.1) 0 (0.0) 0.002 Hypermenorrhea 46 10 (21.7) 7 (28) 3 (14.3) 0.3 Spontaneous abortion 46 11 (23.9) 7 (28) 4 (19.1) 0.5 Infertility 47 11 (23.4) 8 (30.8) 3 (14.3) 0.3 Sandy patches in mucosa 48 2 (4.2) 2 (7.4) 0 (0.0) 0.5 Polyps 48 3 (6.3) 3 (11.1) 0 (0.0) 0.3 Cervical dysplasia 45 4 (8.5) 2 (7.69) 2 (9.5) 0.9 Inflammatory pelvic disease 47 3 (6.4) 3 (11.5) 0 (0.0) 0.2 Imaging results Abnormal ultrasound transvaginal exploration (overall) 45 15 (33.3) 12 (46.2) 3 (15.8) 0.05 Abnormal ultrasound finding (urogenital and/or hepatosplenic) 33 9 (27.3) 8 (34.8) 1 (10) 0.2 Uterine myoma 45 8 (17.1) 5 (20.8) 3 (14.3) 0.7 Ovarian cysts 44 9 (20.5) 9 (39.1) 0 (0.0) 0.002 Polycystic ovarian 44 6 (13.6) 6 (25) 0 (0.0) 0.03 Other findings Female genital mutilation 45 9 (20) 6 (23.1) 3 (15.8) 0.7 Asthma 42 5 (11.9) 5 (23.8) 0 (0.0) 0.05 Coinfections HBV 22 4 (18.2) 2 (16.6) 2 (20.0) 0.9 HPV 30 3 (10.0) 1 (5.0) 2 (20.0) 0.3 HIV 51 1 (2.0) 1 (3.2) 0 (0.0) 0.9 Strongyloides stercolaris 44 7 (15.9) 5 (20.8) 2 (10.0) 0.4 a Global prevalence of study variables are expressed in rows taking as denominator the total number of individuals with this data available, as well as the prevalence of country origin by serology result. All other results consider as denominator the respective number of seropositive and seronegative individuals (columns), excluding those with no data available. Of note, proportions of participants with missing data were similar between seropositive and seronegative women, excluding a recording bias. b N indicates the number of participants with data available. c We excluded a confounding effect of Strongyloides infection and eosinofilia through an adjusted analysis, which yielded an OR between eosinophilia and seropositivity of 9.17 (95%CI = 2.0–42.1; p = 0.004). Frontiers in Public Health | www.frontiersin.org 3 March 2022 | Volume 10 | Article 778110 Roure et al. Schistosomiasis Neglected Among Female Migrants tract infections (67.9 vs. 28.6%, p = 0.006), dysuria (51.9 vs. symptoms among Schistosoma seropositive women may denote 4.8%, p < 0.001), haematuria (38.5 vs. 4.8%, p = 0.01) and a disruption of their sexual and reproductive health wellbeing, gynecological symptoms, which were reported by 96.4% of the which probably also explains the very high number of visits positive women (vs. 66.6%, p = 0.005). The most prevalent made to SRH services. Symptoms of Schistosoma infection may gynecological symptoms among infected women were vaginal have been persistently misdiagnosed. This is in addition to the discharge (81.5 vs. 42.9%, p = 0.006), vulvovaginal infections unspecific chronic complications, such as renal insufficiency, (85.2 vs. 31.8%, p = 0.001) and vaginal pain (55.0 vs. 0.0%, p < that Schistosoma infections may cause and other unspecific 0.001). Transvaginal ultrasounds showed abnormalities in 12 of manifestations (non-FGS) due mainly to S. mansoni infection. the infected women but in only three of the seronegative women The long-term residence in Europe of most of the infected (46.2 vs. 15.8%, p = 0.05). The most frequent finding was ovarian women (median >13 years) supports the notion that migrant cysts (39.1 vs. 0.0%, p = 0.002) and polycystic ovarian disease females may experience a high rate of delayed schistosomiasis (25.0 vs. 0.0%, p = 0.03). Other findings include the presence of diagnosis. Delayed diagnosis and underdiagnosis rates have been female genital mutilation in 20% of the women studied (23.1 vs. estimated to be high among migrant populations in general 15.8%, p = 0.7) and bronchial asthma in 23.8% of the infected (17, 18). Therefore, migrant females exposed to schistosomiasis women (vs. 0.0%, p = 0.05). As regards severe complications could be fairly regarded as “neglected among the neglected”, that of schistosomiasis, one patient had liver cirrhosis and another is, a doubly neglected subset of the population in Europe. The severe chronic renal failure. Both women were seropositive. The underlying causes of this neglect may be primarily the lack of median number of previous visits to a SRH unit prior to diagnosis awareness among health professionals in the SRH and primary was 41 [IQR (18–65)] and 17 [IQR (11–44)] among seropositive care health services. The fact that such services are poorly tailored and seronegative women, respectively (p < 0.001). for migrant female populations may play a role as well, as has been shown to be the case for preventive and screening services among migrant populations elsewhere in Europe (17, 18). As DISCUSSION a result, our perception is that the prevalence of Schistosoma spp. infection among women may be heavily underestimated We ascertained a much higher prevalence of gynecological signs and underdiagnosed not only in endemic countries, but in non- and symptoms among women with Schistosoma seropositive endemic countries as well (19). The frequent diagnosis of STIs results compared to those with negative results. This finding may be due to an overlapping of signs and symptoms with FGS. supports the hypothesis that these women may have a chronic Therefore, we cannot exclude a certain confounding between the infection of Schistosoma. Furthermore, our data revealed some two conditions. In addition, the frequent diagnosis of asthma important details. Firstly, the strikingly low number of women observed among infected women (p = 0.05) may be due in that underwent Schistosoma screening (in both absolute and fact to a misdiagnosis of the signs and symptoms coming from relative terms) cannot be attributed to a gender imbalance in pulmonary involvement of Schistosoma infection, as described the migrant population, but is likely due to an accessibility bias elsewhere (20). on the part of exposed women to our health service and/or the This study has some limitations. Firstly, the serological test lack of clinical suspicion when they accessed other preventive or does not distinguish between present/active and past/resolved screening services. Records showed that all 51 women had made infections and between different Schistosoma species (S. at least one visit to a SRH unit prior to schistosomiasis screening, haematobium, S. mansoni, S. japonicum and others), and only and most of them had made more than 50 such visits. This denotes an exposure to Schistosoma. Furthermore, the test has suggests a lack of awareness of FGS among health professionals. limited specificity (84%) with a Negative Predictive Value of The low proportion of women that underwent Schistosoma 96%. However, the inclusion of compatible clinical symptoms screening in the study center (51 out of 405, 12.6%), is consistent and/or laboratory abnormalities would increase the Positive with previous series which report an underrepresentation of Predictive Value. The safety of treatment is clearly weighted women among the non-European migrant patients diagnosed with the risk of including false positives, and treatment is with schistosomiasis (28.5% of 748 individuals diagnosed also unspecific with regard to individual Schistosoma species. between 1997 and 2010) (12). Other case series in Europe, The second limitation is that this is a single-center study. mainly in Italy and southern Spain, show even lower rates for However, as a referral unit for imported diseases, the study schistosomiasis diagnosis among women, ranging from 3 to 20% center records most of the Schistosoma diagnoses in our of all cases diagnosed (13–16). These low rates of diagnosis area. Third, some data was collected retrospectively (i.e., among women may be due to poor access to screening programs, in past visits and through clinical histories), which may rather than a lower prevalence of the infection in women as hamper to some degree the quality of the data recorded. compared to men. Secondly, the high prevalence of gynecological Furthermore, the small sample size does not allow adjustments for potential confounders except for Strongyloides infection 1 https://www.who.int/data/gho/data/themes/topics/schistosomiasis and eosinophilia (see footnote of Table 1). Finally, because 2 https://www.who.int/news/item/20-07-2018-female-genital-schistosomiasis-simu of the cross-sectional study design, we cannot establish a ltaneous-screening-of-diseases-can-improve-reproductive-health (accessed October 2021). causative link between the gynecological signs and symptoms 3 https://www.who.int/health-topics/schistosomiasis#tab=tab_3 (accessed October and serology results, and therefore the diagnosis of FGS 2021). is presumptive. Frontiers in Public Health | www.frontiersin.org 4 March 2022 | Volume 10 | Article 778110 Roure et al. Schistosomiasis Neglected Among Female Migrants CONCLUSIONS DATA AVAILABILITY STATEMENT In spite of the above mentioned limitations, our findings The raw data supporting the conclusions of this article will be provide sufficient evidence to justify the implementation of made available by the authors, without undue reservation. more robust and prospective studies. These studies would help to determine the need for gender-orientated screening ETHICS STATEMENT programs among migrant populations in non-endemic countries. The study was approved by the Ethics Committee of the Germans Such strategies could involve, for instance, implementation of Trias Hospital, the reference hospital for the study area. adapted clinical questionnaires that include the set of FGS signs and symptoms, specific training for professionals devoted AUTHOR CONTRIBUTIONS to SRH so that they systematically screen at-risk females for Schistosoma infection, a reshaping of services to make them SR and OP-Q were responsible for collecting the data, more culturally-sensitive and gender-orientated in accordance investigation, writing the first draft, and editing the manuscript. with WHO evidence-based recommendations (21), and even XV was responsible for formal analysis and editing the community-based interventions (awareness campaigns through manuscript. 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Available online at: https://www.euro. this article, or claim that may be made by its manufacturer, is not guaranteed or who.int/en/publications/abstracts/report-on-the-health-of-refugees-and- endorsed by the publisher. migrants-in-the-who-european-region-no-public-health-without-refugee- and-migrant-health-2018 (accessed October 01, 2021). Copyright © 2022 Roure, Pérez-Quílez, Vallès, Valerio, López-Muñoz, Soldevila, Torrella, Fernández-Rivas, Chamorro and Clotet. 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