Introduction
Female genital schistosomiasis (FGS) is usually caused by Schistosoma haematobium infection, which results from the entrapment of Schistosoma eggs in the female genital tract (Christine et al., Reference Christine, Lazdins-Held, Stothard and Reinhard-Rupp2016; Bustinduy et al., Reference Bustinduy, Randriansolo, Sturt, Kayuni, Leustcher, Webster, Van Lieshout, Stothard, Feldmeier and Gyapong2022; Buonfrate et al., Reference Buonfrate, Ferrari, Adegnika, Russell Stothard and Gobbi2025), a phenomenon seen as early as 1899 (Madden, Reference Madden1899). Autopsy series have found the presence of eggs and inflammatory reaction in all genital organs, including the cervix, uteri, fallopian tubes and ovaries (Gelfand et al., Reference Gelfand, Ross, Blair and Weber1971). As a result, FGS is responsible for menstrual disorders, infertility, ectopic pregnancy and abortion, polypus and papillomatous tumours, and cervical dysplasia; it also increases the susceptibility to HIV infection (Christine et al., Reference Christine, Lazdins-Held, Stothard and Reinhard-Rupp2016; Patel et al., Reference Patel, Rose, Kjetlan, Downs, Mbabaz, Sabin, Chege, Watts and Secor2021; Bustinduy et al., Reference Bustinduy, Randriansolo, Sturt, Kayuni, Leustcher, Webster, Van Lieshout, Stothard, Feldmeier and Gyapong2022; Orish et al., Reference Orish, Morhe, Azanu, Alhassan and Gyapong2022). FGS can affect up to 75% of women with S. haematobium infection in endemic countries (Christine et al., Reference Christine, Lazdins-Held, Stothard and Reinhard-Rupp2016; Bustinduy et al., Reference Bustinduy, Randriansolo, Sturt, Kayuni, Leustcher, Webster, Van Lieshout, Stothard, Feldmeier and Gyapong2022). Therefore, it is estimated that around 56 million women worldwide in endemic countries have FGS, most of them in sub-Saharan Africa (World Health Organization, 2018).
However, adult worms can survive for decades in the human body (Warren et al., Reference Warren, Mahmoud, Cummings, Murphy and Houser1974; Chabasse et al., Reference Chabasse, Bertrand, Leroux, Gauthey and Hocquet1985; Colley et al., Reference Colley, Bustinduy, Secor and King2014; Potters et al., Reference Potters, Van Duffel, Broeckx and Bottieau2019; Carbonell et al., Reference Carbonell, Rodríguez-Alonso, López-Bernús, Almeida, Galindo-Pérez, Velasco-Tirado, Marcos, Pardo-Lledías and Belhassen-García2021; Buonfrate et al., Reference Buonfrate, Ferrari, Adegnika, Russell Stothard and Gobbi2025), and the granulomatous process may evolve to chronic schistosomiasis. Consequently, migrant women from sub-Saharan countries can have FGS with a wide array of long-term unspecific clinical signs and symptoms of the genitourinary tract, often presented in an aggregated form (Roure et al., Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, España, Hegazy, Fernández-Rivas, Gorriz, Herena, Oliveira, Miralles, Conde, Montero-Alia, Fernández-Pedregal, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024a, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, Gorriz, Herena, Pedregal, España, Serra, Cera, Rodríguez, Serrano, Falguera, Hegazy, Fernández-Rivas, Miralles, Conde, Montero-Alia, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024b). Nevertheless, there is still an important gap of knowledge regarding the clinical history, the associated morbidity and the therapeutic response, particularly in regard to long-term or chronic FGS.
The pooled estimates of Schistosoma seroprevalence among sub-Saharan population in Europe is up to 24% (Asundi et al., Reference Asundi, Beliavsky, Liu, Akaberi, Schwarzer, Bisoffi, Requena-Méndez, Shrier and Greenaway2019). The total population of migrants from sub-Saharan countries living in Europe account for 11 million of inhabitants (IOM, 2024), from which less than half are women. Therefore, imported schistosomiasis and FGS may represent an important burden of diseases which has been systematically neglected in terms of knowledge, clinical suspicion, treatment and lack of appropriate guidelines (Roure et al., Reference Roure, Pérez-Quílez, Vallès, Valerio, López-Muñoz, Soldevila, Torrella, Fernández-Rivas, Chamorro and Clotet2022; Marchese et al., Reference Marchese, Remkes, Kislaya, Rausche, Brito, Hey, Rasamoelina, Rakotoarivelo, May and Fusco2025; Rafferty et al., Reference Rafferty, Warrell, Polley, Bodhani, Nabarro, Godbole, Bustinduy, Kjetland, Hsieh and Chiodini2025). This is a consequence of the overlapping symptoms with other common conditions, lack of awareness by clinicians in non-endemic countries, lack of a gold standard diagnostic test and stigma surrounding Sexual and Reproductive Health; acknowledging the barriers migrant populations face in accessing healthcare services.
Grounded in previous research (Roure et al., Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, España, Hegazy, Fernández-Rivas, Gorriz, Herena, Oliveira, Miralles, Conde, Montero-Alia, Fernández-Pedregal, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024a, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, Gorriz, Herena, Pedregal, España, Serra, Cera, Rodríguez, Serrano, Falguera, Hegazy, Fernández-Rivas, Miralles, Conde, Montero-Alia, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024b, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Valerio, Soldevila, Chamorro, Abad, Hegazy, Fernández-Rivas, Gorriz, Herena, Fernández-Pedregal, España-Cueto, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2025), we have developed a screening protocol of FGS on long-term migrant women from sub-Saharan Africa. This protocol has been implemented at the Sexual and Reproductive Health Unit (SRHU) of the Northern Metropolitan Area from Barcelona after formal training of health professionals. We present and discuss the early results of this protocol implementation, which include a deeper gynaecological examination [colposcopy, cytology, human papillomavirus (HPV) determination, biopsy and response to specific treatment with praziquantel (PZQ) (Figure 1)]. The objective of this analysis is to contribute to the development of a research agenda and Public Health interventions towards imported FGS in countries with substantial pockets of exposed migrant female population.
Figure 1. Proposed algorithm for screening, treatment and follow-up of imported FGS. *Epidemiological risk has been defined as having been born in a high endemic country or region; **Suspicion of FGS has considered in any screened women with a serology-positive test (ICT or ELISA) with the presence of at least 1 compatible gynaecological clinical sign or symptom without alternative diagnostic (Vulvar itching, vulvovaginal discharge, leucorrhoea, dysmenorrhea, hypermenorrhea, vaginal pain, vaginal bleeding, pelvic pain, metrorrhagia, amenorrhea, dyspareunia); ***Microbiological samples include urine for microscopic examination and cervical swaps/cervical lavages for PCR if PCR is available. Previous colposcopy examination was abnormal.
Material and methods
Study sample and population
The study was performed in the Barcelona North Metropolitan Health Region, Catalonia, Spain. Around 20,000 migrants from Western sub-Saharan Africa are currently living in the study area, from which around 30% are women (IDESCAT, 2021). In the initial community-based screening we included non-pregnant adult women (≥18 years), who had not been previously diagnosed and/or treated for schistosomiasis. Participants underwent a detailed revision of clinical history, health records and a questionnaire to determine the presence of genitourinary and gynaecological signs and symptoms defined according to the International Classification of Diseases [Table S1 (ICD, 2019)]. We performed a Schistosoma-specific Enzyme-Linked Immunosorbent Assay (ELISA) and immunochromatography (ICT) blood test, and parasitological examination of urine. Results of the screening study have been previously published in full (Roure et al., Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, España, Hegazy, Fernández-Rivas, Gorriz, Herena, Oliveira, Miralles, Conde, Montero-Alia, Fernández-Pedregal, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024a, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, Gorriz, Herena, Pedregal, España, Serra, Cera, Rodríguez, Serrano, Falguera, Hegazy, Fernández-Rivas, Miralles, Conde, Montero-Alia, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024b, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Valerio, Soldevila, Chamorro, Abad, Hegazy, Fernández-Rivas, Gorriz, Herena, Fernández-Pedregal, José, España-Cueto, Paredes, Miranda-Sánchez, Miralles, Conde, Montero, Núñez-Andrés, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024c).
Protocol implementation
We offered a novel diagnostic and follow-up protocol to all women screened with criteria of imported FGS (serology-positive test and clinical signs and symptoms compatible with FGS) (Figure 1). These women were addressed to the SRHU to perform a full gynaecological examination including colposcopy, cervical cytology and biopsy, ultrasonography and HPV test. Colposcopy examination was based on the World Health Organization (WHO) guidelines, which describe the pathognomonic characteristic findings of FGS: yellow sandy patches (either single, in clustered grains or appearing as homogenous lesions), abnormal vessels and rubbery papules (WHO, 2015). Antiparasitic treatment was offered to all suspected FGS cases at a community level (60 mg/kg oral PZQ twice within 15 days). Follow-ups were made at the 12th month, where they were addressed at the SRHU for a final gynaecological checking according to the protocol (Figure 1).
Statistical methods
Continuous variables were described with mean and standard deviation or median and interquartile ranges (IQRs) and categorical variables with proportions and 95% confidence intervals. Bivariate analysis used the Chi-square test or McNemar test for paired data, or Student’s t-test for categorical or continuous variables or signed-rank test for paired data (pre–post treatment assessment), respectively, or their nonparametric counterparts when necessary (Fisher test and Wilcoxon test). Data were analysed using Stata v14.0 and R v3.1.4.
Ethical issues
The study was approved by the ethics committee the Jordi Gol Foundation, with certification number 22/063-P. A participant consent form was obtained prior to enrolment and personal identifiers were encrypted prior the analysis. The study was performed according to the Helsinki declaration principles and recommendations. Standard of care was offered to all participants with diagnosis performed during the roll out of the study.
Results
General description and findings at baseline
A total of 136 women were enrolled during the community-based screening. Among them, 39 (28.7%) had a positive schistosomiasis serology and only 1 (0.7%) woman had visible urine S. haematobium eggs observed during microscopic examination. Baseline characteristics are shown in the study flow chart (Figure 2). Median age was of 42.7 years (IQR 35–45), median time living in the EU was of 14 years (IQR 10–19) and all of them were coming from a West African country, mainly Senegal (17 out of 39; 43.6%) and Gambia (13 out of 39; 33.3%). All these women had at least 1 gynaecological clinical sign or symptom [median 5 (IQR 2–6)] and fitted the definition of suspected FGS. According to previous analysis in this sample (Roure et al., Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, España, Hegazy, Fernández-Rivas, Gorriz, Herena, Oliveira, Miralles, Conde, Montero-Alia, Fernández-Pedregal, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024a, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, Gorriz, Herena, Pedregal, España, Serra, Cera, Rodríguez, Serrano, Falguera, Hegazy, Fernández-Rivas, Miralles, Conde, Montero-Alia, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024b), several genitourinary and gynaecological signs and symptoms were statistically associated (p < 0.05) with serology-positive test (vaginal discharge/leucorrhoea, vulvar itching, dysmenorrhea and amenorrhea), and most of them were associated with other general clinical findings (i.e. chronic abdominal pain or dysuria). The most prevalent were pelvic pain (64.1%), vaginal discharge (64,1%) and dysmenorrhea (71,8%). One participant tested positive for HIV-1 (0.7%). Figure 3A shows the distribution of different signs and symptoms at baseline.
Figure 2. Study flow chart and basic socio-demographic information of women with suspicion of FGS (n = 39).
Figure 3. Pretreatment presence of clinical signs and symptoms assessed at baseline and serology results at baseline (A) and at the 12th month of follow-up (B)*. *Partial resolution of symptoms have been considered as a decrease in intensity and/or number of episodes of the assessed clinical sign/symptom during the prior 6 months.
All 39 cases were addressed to the SRHU according to the protocol, but only 11 underwent baseline gynaecological examination. These 11 women were similar in age and duration of residence in the EU to the overall sample of women suspected of having FGS (p > 0.05). Among them the most prevalent clinical sign and symptom was pelvic pain, vaginal discharge, dysmenorrhea and hypermenorrhoea (9 out of 11) followed by abdominal pain and vulvar itching (8 out of 11 both). All of them had at least 1 menstrual disorder. Five of them referred a history of infertility, 5 had spontaneous abortion history and 2 had history of ectopic pregnancies with secondary salpingectomy. Colposcopy examination was abnormal in 7 out of 11 women examined, all of them with at least 1 macroscopic feature characteristic of FGS (22): 6 with sandy patches, 5 with abnormal vessels and 3 with rubbery papules. Four patients showed Naboth cysts at colposcopy examination. Six of them had low-grade dysplasia at cytology examination [3 Atypical Glandular/Squamous Cells of Undetermined Significance (ASCUS/ASGUS), 2 Low-grade Squamous Intraepithelial Lesion (LSIL) and 1 with squamous metaplasia]. One woman had a history of High-grade Squamous Intraepithelial Lesion (HSIL) with a negative HPV test and underwent a conization. All tested women had a negative result for HPV. Clinical findings, colposcopy results, biopsy, cytology and echography findings are summarized in Table 1.
Table 1. Description of clinical signs and symptoms and results of 11 women who underwent full gynaecological examination at baseline
a Women that underwent colposcopy examination at month 12 (n = 3).
HSIL, high grade of squamous intraepithelial lesion; ASCUS, atypical squamous cells of unknown significance; LSIL, low-grade squamous intraepithelial lesion; ASGUS, atypical squamous glandular cells of unknown significance.
Follow-up results
Overall, 28 out of 39 participants were clinically assessed at month 12 (28.2% lost to follow-up, see flow chart in Figure 2). A significant decrease of prevalence was observed in all clinical items (p < 0.05) except for dysuria (p = 0.1) and post-coital bleeding (p = 0.08) (Table 2). The total number of assessed clinical signs and symptoms significantly decreased from baseline assessment at screening to month 12 [5 (IQR 2–6) vs 0 (IQR 0–2) p < 0.001). All women experienced the resolution of at least 1 or several signs and symptoms and 35.7% of them (10 out of 28) a total resolution. Furthermore, we observed a decreased trend on positive serology prevalence throughout the 12-month of follow-up, both in terms of ICT positivity (rate clearance of 30.8%, from 74.3% to 47.4%; p = 0.04) or ELISA positivity (rate clearance of 64.3%; from 64.1% to 26.3%; p = 0.003); and a decrease in optical density of ELISA in the overall sample, including those who remained positive [median 0.48 (IQR 0.29–1.0) vs 0.34 (IQR 0.2–0.6); p < 0.001]. In Figure 3A, B, we show the comparative evolution of the prevalence pre- and post-treatment for the set of clinical items assessed and serology results. All 3 women who had abnormal colposcopy at the beginning and underwent colposcopy examination at month 12, showed total resolution of lesions. Table 1 displays the detailed description pre and post treatment assessment of the 11 women who underwent full gynaecological examination at baseline.
Table 2. Pre–post prevalence of different genitourinary signs and symptoms assessed at baseline and at month 12
a Number of individuals with complete data for the specific clinical item at baseline and month 12 (general denominator).
b Number of individuals with the specific symptom at baseline.
c Number of individuals with the specific symptom at month 12.
d Cure rate has been calculated considering as the proportion of women with the assessed symptom at baseline which have not had a clinical episode during the last 6 months.
Discussion
The observed results and previous research (Christine et al., Reference Christine, Lazdins-Held, Stothard and Reinhard-Rupp2016; Bustinduy et al., Reference Bustinduy, Randriansolo, Sturt, Kayuni, Leustcher, Webster, Van Lieshout, Stothard, Feldmeier and Gyapong2022; Orish et al., Reference Orish, Morhe, Azanu, Alhassan and Gyapong2022; Roure et al., Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, España, Hegazy, Fernández-Rivas, Gorriz, Herena, Oliveira, Miralles, Conde, Montero-Alia, Fernández-Pedregal, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024a, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, Gorriz, Herena, Pedregal, España, Serra, Cera, Rodríguez, Serrano, Falguera, Hegazy, Fernández-Rivas, Miralles, Conde, Montero-Alia, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024b, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Valerio, Soldevila, Chamorro, Abad, Hegazy, Fernández-Rivas, Gorriz, Herena, Fernández-Pedregal, España-Cueto, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2025) support the development and implementation of a screening protocol for chronic FGS among long-term sub-Saharan women migrants. Such protocols are feasible and yield significant resolution rate of clinical and colposcopy findings compatible with this condition. We found a general improvement of clinical genitourinary and gynaecological signs and symptoms of women with probable imported FGS after specific treatment, including clearance of serology positivity. Furthermore, in a set of them (n = 7) we observed colposcopy examination findings considered compatible of FGS (sandy patches, rubbery papules and/or abnormal vessels), which were fully resolved in the 3 cases with gynaecological examination at the 12th month of follow-up. According to our own experience, women with compatible signs and symptoms tended to have had multiple visits without a clear definitive diagnosis and underwent disparate diagnostic procedures and treatments in the past (Roure et al., Reference Roure, Pérez-Quílez, Vallès, Valerio, López-Muñoz, Soldevila, Torrella, Fernández-Rivas, Chamorro and Clotet2022), which resulted in a waste of resources and drives to an increased morbidity. The early identification and treatment would result in substantial savings in terms of cost and quality of life.
However, the diagnosis of chronic FGS is still far from straightforward and needs the combination of clinical and gynaecological examination, laboratory tests to be diagnosed and the monitor of therapeutic outcome. With this regard, some gynaecological symptoms seem to respond better to the treatment (vulvar itching and vaginal discharge), whereas others (mainly menstrual disorders) seem to be more unresponsive. The first might be associated with the inflammation secondary to the presence of adult worm and more susceptible to PZQ, whereas the second could be secondary to an established fibrotic process. Particularly, as noted in our previous publication (Roure et al., Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, España, Hegazy, Fernández-Rivas, Gorriz, Herena, Oliveira, Miralles, Conde, Montero-Alia, Fernández-Pedregal, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024a, Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, Gorriz, Herena, Pedregal, España, Serra, Cera, Rodríguez, Serrano, Falguera, Hegazy, Fernández-Rivas, Miralles, Conde, Montero-Alia, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024b), amenorrhea might be a specific manifestation of long-term chronic schistosomiasis in the context of the Asherman Syndrome secondary to the chronic inflammatory process of the uterine mucosal (Krolikowsky et al., Reference Krolikowsky, Janowski and Larsen1995).
In any case, the realization of colposcopy and cytology in women with suspected FGS remains mandatory. Particularly, colposcopy results are the most specific way to diagnose FGS. All assessed women with abnormal colposcopy presented the characteristic findings of FGS (World Health Organization, 2015). The presence of Naboth cysts (4 out of 11 examined women) might be indicative of chronic cervicitis (Mikes et al., Reference Mikes and Puckett2025). The association with chronic FGS deserves further assessment with a larger sample.
Nonetheless, the absence of colposcopy lesions does not definitively exclude the presence of FGS; this is supported by the fact that the remaining 6 women examined showed no lesions despite having symptoms consistent with FGS. This is in addition to the limited sensitivity and specificity of serological tests against chronic schistosomiasis (Hinz et al., Reference Hinz, Schwarz, Hahn and Frickmann2017). The yield of microscopy examination is very poor in long-term exposed individuals. In addition, PCR and antigen-detection have not been validated as diagnostic tools of chronic schistosomiasis and FGS, and are not available in Primary Care Centres. Therefore, FGS should still be considered in an exposed women (migrant) presenting compatible clinical signs and symptoms without alternative diagnostic and the absence of typical colposcopy lesions.
Given the high tolerability and safety profile of PZQ, it is reasonable to provide treatment in such cases and monitor the therapeutic response according to the proposed protocol (Figure 1). This does not exclude the urgent need of PZQ validation for chronic imported FGS and, in general, for chronic schistosomiasis. Optimal PZQ dosage and factors associated with the therapeutic response need to be ascertained as well in the frame of a clinical trial. Late relapse or partial response of chronic FGS with current standard doses of PZQ cannot yet be ruled out.
It is important to point out that most of the previously published studies of FGS concern young women from endemic countries where reinfection is the norm. In contrast, our study sample are older long-term migrants, with remote past exposure and without or lower prevalence of other prevalent factors (coinfection with other parasitic infections, malnutrition, sexually transmitted infections, etc.). Therefore, our suspected cases of FGS may represent the chronic stage of the infection without the interference of other cofactors. Results in terms of clinical manifestation and response to treatment might not be fully comparable with FGS in endemic countries.
Furthermore, besides S. haematobium other Schistosoma species infection can involve the genitalia tract including Schistosoma mansoni in dual infection with S. haematobium (Bustinduy et al., Reference Bustinduy, Randriansolo, Sturt, Kayuni, Leustcher, Webster, Van Lieshout, Stothard, Feldmeier and Gyapong2022) or as hybrids (De Elías-Escribano et al., Reference De Elías-Escribano, Artigas, Salas-Coronas, Luzon-Garcia, Reguera-Gomez, Cabeza-Barrera, Vázquez-Villegas, Boissier, Mas-Coma and Bargues2025) or zoonotic species such Schistosoma mattheei (Stothard et al., Reference Stothard, Juhász and Musaya2025) and Schistosoma bovis hybridized with S. haematobium (Soentjens et al., Reference Soentjens, Cnops, Huyse, Yansouni, De Vos, Bottieau, Clerinx and Van Esbroeck2016; Bustinduy et al., Reference Bustinduy, Randriansolo, Sturt, Kayuni, Leustcher, Webster, Van Lieshout, Stothard, Feldmeier and Gyapong2022). Therefore, the risk of FGS in Schistosoma endemic countries might be higher than supposed.
Other findings deserve some additional comments. It is striking the high prevalence of abnormal cytology with HPV-negative results observed among women identified in the frame of the screening protocol (55%), even if there were low-grade lesions. Indeed, 1 of the women with colposcopy suggestive of FGS had a history of HSIL and conization in the previous 10 years. The interaction of FGS with cervical dysplasia and its role as co-factor for cervical cancer development is still a matter of debate, and lacks of enough research (Sturt et al., Reference Sturt, Omar, Hansingo, Kamfwa, Bustinduy and Kelly2025); nevertheless, the proven oncogenic capacity of Schistosoma has been well established with bladder cancer (Mantica et al., Reference Mantica, Terrone and Der Merwe2021). Therefore, the interaction of FGS and HPV infection should be considered an emerging issue in the era of HPV vaccination.
Current guidelines for cervical cancer screening in the scenario of high HPV vaccination coverage do not consider this possible co-factor among women exposed to schistosomiasis infection. Cervical-cancer screening guided on HPV test should not be sufficient among women with FGS. This interaction could be more relevant than currently contemplated among migrant women considering (i) the high prevalence of FGS; (ii) the increased exposure to sexually transmitted infection (which includes HPV) among migrant women compared to natives (Hernando-Rovirola et al., Reference Hernando Rovirola, Ortiz-Barreda, Galán Montemayor, Sabidó Espin and Casabona Barbarà2014); and (iii) the important prevalence of infection with oncogenic HPV genotypes (16 and 18) among African women (Seyoum et al., Reference Seyoum, Assefa, Gure, Seyoum, Mulu and Mihret2022). A re-evaluation of current cancer screening protocols might be necessary, but more data are still needed to ascertain this point. This potential interaction would be more relevant in terms of burden of disease in schistosomiasis high endemic countries.
As a final consideration, it seems clear that the morbidity burden of imported schistosomiasis infection is high among migrant women. The high rate of spontaneous abortions (26%), infertility (21%) and ectopic pregnancies (8%) in our study sample at baseline suggest an important morbidity associated with imported FGS. This is besides the frequent involvement of genitalia tract (male genital schistosomiasis) among their male counterparts (Roure et al., Reference Roure, Vallès, Pérez-Quílez, López-Muñoz, Chamorro, Abad, Valerio, Soldevila, España, Hegazy, Fernández-Rivas, Gorriz, Herena, Oliveira, Miralles, Conde, Montero-Alia, Fernández-Pedregal, Miranda-Sánchez, Llibre, Isnard, Bonet, Estrada, Prat and Clotet2024a).
Migrant population tend to suffer more disproportionally the barriers to access the health system in Europe (Graetz et al., Reference Graetz, Rechel, Groot, Norredam and Pavlova2017; Marques et al., Reference Marque, Nunes, Antunes, Heleno and Dias2020). Particularly, our study underscores the difficulty to access and retain health care for migrant women. Twelve out of 39 were lost-of follow-up and did not start the treatment with PZQ; only 11 were successfully addressed to the SHRU for gynaecological examination. It seems clear that a screening protocol should be complemented with an outreach strategy to ensure the continuum health care of these women. However, current guidelines from the European Centre for Disease Control only recommend parasitology-based screening among recently arrived migrants (less than 5 years), without specific mention to FGS (ECDC, 2018). Based on our findings and previous publications these guidelines need to be updated including FGS screening.
Conclusions
The implementation in long-lasting sub-Saharan migrant women of a screening protocol for chronic FGS in a community setting, including full clinical and gynaecological examination, follow-up, and empirical antiparasitic treatment was possible and rendered high rates of diagnosis and clinical improvement or complete resolution.
Apart from this public health intervention, there are many knowledge gaps that require research, including the evaluation of the optimal dose of PZQ in a clinical trial, the development of new diagnostic tools and interaction with other diseases (particularly HPV, HIV and cervical cancer).
Acknowledgements
We acknowledge participating women, migrants with chronic schistosomiasis and social entities for their support on this study. We thank Dr. Erica Pérez for the critical reading and formal corrections of the article.
Author contributions
Study design: SR, LSM, XV, ABR; Data collection: SR, LSM, RCG, CSS, MVM, OPQ, ILM, MCM, CC, LH and ABR; Analysis: SR, XV; Article writing: SR, XV, JML; Article revision: All co-authors; Administration and resources: SR, ABR; Supervision: SR, ABR.
Financial support
Foundation to Fight Against Infectious Diseases
Competing interests
None to declare.
Ethical standards
The study was approved by the ethics committee of the Jordi Gol Foundation, with certification number 22/063-P. A participant consent form was obtained prior to enrolment and personal identifiers were encrypted prior the analysis. The study was performed according to the Helsinki declaration principles and recommendations. Standard of care was offered to all participants with diagnosis performed during the roll out of the study.
Open access
