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Article

Female Genital Schistosomiasis (FGS) Prevalence and Burden Across Endemic Countries, Timelines, and Age Groups: A Retrospective Study

1
Department of Biomedical Sciences, College of Health Sciences, Marquette University, Milwaukee, WI 53233, USA
2
Department of Medical Laboratory Science, Marquette University, Milwaukee, WI 53233, USA
3
Directorate of Research and Postgraduate Studies, Lusaka Apex Medical University, Lusaka 10101, Zambia
4
Institute of Basic and Biomedical Sciences, Levy Mwanawasa Medical University, Lusaka 10101, Zambia
*
Author to whom correspondence should be addressed.
Parasitologia 2024, 4(4), 382-389; https://doi.org/10.3390/parasitologia4040034
Submission received: 10 October 2024 / Revised: 18 November 2024 / Accepted: 25 November 2024 / Published: 28 November 2024

Abstract

Female Genital Schistosomiasis (FGS) is caused by Schistosoma haematobium, which causes chronic gynecological conditions that lead to substantial morbidity and infertility. This study’s objective is to determine the prevalence and burden of FGS based on the presence of S. haematobium-specific DNA in females across age groups using our previously field-acquired filtered human urine samples from Zambia, Tanzania, and Ghana, collected over multiple years. For Ghana (2013), 39 out of 90 samples were from females, of which 31 (79.5%) were positive and 8 (20.5%) were negative. In Zambia (2016), 80 out of 133 samples were from females, of which 46 (57.5%) tested positive and 34 (42.5%) were negative. For Zambia (2017), 60 out of 110 samples were from females, of which 45 (75%) tested positive and 15 (25%) tested negative. In Tanzania (2018), 70 out of 104 samples were from females, of which 43 (61.4%) tested positive and 27 (38.6%) tested negative. FGS prevalence ranged from 57.5% (Zambia in 2016) to 79.5% (Ghana in 2013) and was found predominantly among the 11–20 years age group. The analytical outcome highlights that FGS is predominant among females in different endemic countries and in the age range of pre-teen to young adult.

1. Introduction

Schistosomiasis is the second deadliest parasitic disease in the world after malaria, affecting approximately 220 million people and accounting for approximately 200,000 human deaths [1,2]. It is a major source of morbidity and mortality in sub-Saharan Africa, caused by a trematode parasite of the genus Schistosoma and three common species that infect humans: Schistosoma haematobium, S. japonicum, and S. mansoni.
Female genital schistosomiasis (FGS) is caused by S. haematobium and is predominant in young girls between 12 and 15 years old. The disease is caused by the release of terminal-spine parasite eggs from female S. haematobium. FGS is a serious and chronic gynecological condition causing substantial morbidity among affected women [3,4]. When the eggs are deposited in the tissues of the cervix and lower female genital tract, the combination of the presence of the eggs with host inflammation and increased vascularity in the cervicovaginal mucosa produces typical intravaginal lesions that result in genital itching, pain, bleeding, and dyspareunia [5,6,7]. In addition, eggs deposited in the uterus and fallopian tubes can result in infertility [8]. It causes vaginal discharge, blood in urine, and abdominal and pelvic pain. It is a chronic gynecological condition that, if left untreated, can lead to a range of complications for women living with FGS, including infertility [8], abortion, genital ulcers, modified immunological responses to HPV and HIV [9], and increased risks of contracting HPV [10] and HIV [11,12].
According to the World Health Organization (WHO), many young women in sub-Saharan Africa are at risk of acquiring FGS, HIV infection, and cervical cancer [13]. Furthermore, FGS remains largely overlooked within the national health systems and Neglected Tropical Disease (NTD) programs, and its prevalence is underestimated [14]. In some lower- and middle-income countries (LMICs) like Zambia, where schistosomiasis is endemic, knowledge and understanding of FGS among community members and healthcare workers (HCWs) within affected communities is often incomplete and confused with other Sexually Transmitted Diseases (STDs). In addition, there is a paucity of scholarly work exploring the knowledge, perceptions, and practices of women of reproductive age and in HCWs’ knowledge about FGS. To sustainably control and prevent FGS, an understanding of community and HCWs’ perceptions and attitudes towards people with FGS and their knowledge and practices may play an important role. In addition, a lack of knowledge may exacerbate levels of misconceptions [15] that may, in turn, create stigma among women misdiagnosed with STDs instead of FGS.
The absence of definitive policies for FGS may, in turn, have caused the following: (i) a lack of treatment and diagnostic guidelines, (ii) limited investment, (iii) a lack of awareness among multiple stakeholders, and (iv) poor FGS surveillance among women of reproductive age. When treatment and diagnostic guidelines are lacking, there is an increased risk of misdiagnosis, inappropriate treatment, and missed opportunities for developing innovative solutions to control FGS in endemic communities. Hence, having the right knowledge, attitude, and improved perception of FGS is essential in reducing cases of stigma and modifying risk behaviors to reduce the odds of re-infection at both the individual and community levels.
This proposed pilot study will provide substantial evidence of the presence, prevalence (infection intensity), geographic distribution, age group, and gender-specific infection prevalence for FGS in females from a database of extracted DNA from field-collected urine samples from Ghana, Zambia, and Tanzania, over multiple years. The project will determine and explore the burden of FGS to develop strategies to improve the control of FGS among endemic communities in sub-Saharan Africa.

2. Materials and Methods

2.1. Data Source

The data used for this study were preexisting. All the collected data came from analyzing the field-acquired filtered urine samples from previous studies, which were acquired from three different geographical locations over four years. The existing data sources were from previously individually published and unpublished studies conducted in Ghana in 2013, Zambia in 2016 and 2017, and Tanzania in 2018. The existing data were extensively analyzed (Figure 1) to determine the FGS presence, prevalence, distribution, and burden across age groups.

2.2. Model of Data Analysis

2.2.1. Overall FGS Prevalence

The total FGS-positive samples for each year were determined based on the polymerase chain reaction (PCR) testing. All the duplicates and missing samples were discarded before analysis. The total number of positive and negative results for S. haematobium among females was determined based on three countries (Ghana, Zambia, and Tanzania). The disease prevalence was calculated based on the proportion of positive infections from each test out of the total number of samples evaluated. For S. mansoni, PCR was carried out by amplifying a highly repeated 121 bp Sm1-7 fragment (GenBank: M61098.1) [16]. For S. haematobium, 121 bp Dra, one repeat fragment (GenBank: DQ157698.1) was amplified [17,18]. For both schistosome species, the repeat fragments that makeup 12–16% of each parasite genome (~600,000 copies per cell) are species-specific and occur in different regions of the genomes of these two schistosome parasites, so there is no chance of cross-amplification.

2.2.2. FGS Prevalence Based on Parasite DNA Concentration in Urine

The overall infection prevalence was assessed for each year across three countries: Ghana (2013), Zambia (2016 and 2017), and Tanzania (2018). The infection prevalence was defined as the number of positive samples out of the total number of samples evaluated each year. The extracted DNA from filtered urine samples (used to assess FGS prevalence) for each year was categorized into three groups, as follows: high DNA load (>10 ng/μL), medium DNA load (4–10 ng/μL), and low DNA load (0.5–3 ng/μL). The categories corresponded to the infection levels present among the participants in the three countries. All the duplicates and missing samples were discarded. The prevalence of FGS was also determined by comparing the different diagnostic tests, such as hematuria, urine filtration, and PCR, for each year for the three countries.

2.2.3. Geographical and Gender-Based Distribution of FGS

The country-wise distribution of FGS was determined based on the S. haematobium infection of the collected urine samples from three countries over four years. The same approach was taken with males to evaluate the S. haematobium infection that causes Male Genital Schistosomiasis (MGS). The distribution of FGS was compared against S. mansoni infection only in girls and women and the overall S. mansoni infection over four years in three countries. For Ghana, samples were collected from Tomefa, a community in the Weija Lake area of the GA South district of the Greater Accra region. For Zambia, samples were collected from the Chongwe district in Lusaka Province and the Siavonga district along the shores of Lake Kariba, which is endemic for both Schistosome species. For Tanzania, samples were collected from the Kayenze villages where schistosomiasis infection was prevalent. In Africa, two major human-infecting species, S. mansoni and S. haematobium, are often sympatric; concurrent infection is debilitating [19]. Because the former is intestinal, and the latter is a urogenital parasite, their pathophysiological outcome is completely different. So, identifying both species from co-infected individuals is important for surveillance, pathology, and monitoring.

2.2.4. FGS Age Distribution

Data for each year were categorized into four age groups: Group A (1–10 years, children and juveniles), Group B (11–20 years, pre-teens to young adults), Group C (21–30 years, young adults to mature adults), and Group D (>31 years, mid-ages). The FGS infection prevalence for all four age groups was determined, along with the highest infection for the age group across years and countries. Also, we evaluated the infection variability amongst different age groups across years and geography and compared this against similar age groups in males.

2.3. Statistical Analysis

We performed a quantitative assessment to evaluate FGS presence, prevalence, distribution, and burden across age groups for four years from three countries. The above-mentioned statistical analysis was carried out by comparing positive and negative infections detected by PCR for S. haematobium. The disease prevalence was determined based on the number of positive cases found by each diagnostic test against the total number of samples evaluated. The data and analysis were processed through Microsoft Excel and JMP 12 (JMP® v12, SAS Institute Inc., Cary, NC, USA) and converted to numerical values (1 = positive and 0 = negative) for statistical analysis. Excel and JMP analyses were performed blindly and then compared for accuracy.

3. Results

3.1. Overall FGS Prevalence

For Ghana in 2013, the prevalence of FGS was 79.5% (31 out of 39 females were positive). For Zambia in 2016 and 2017, the figures were 57.5% (46 out of 80 females were positive) and 75% (45 out of 60 females were positive), whereas, in Tanzania in 2018, the prevalence was 61.4% (43 out of 70 females were positive, Table 1).
Out of the total samples, all the duplicates and missing samples were discarded. Positive samples are based on PCR testing.

3.2. FGS Prevalence Based on Parasite DNA Concentration

Data for each year were categorized as follows based on the concentration of extracted DNA collected from filtered urine samples of PCR-positive individuals to assess FGS prevalence: high DNA load (>10 ng/μL), medium DNA load (4–10 ng/μL), and low DNA load (0.5–3 ng/μL). The highest positivity rate was found in the low DNA load over three years, as follows: in Zambia (2016), 42 (91.30%) females were positive; in Zambia (2017), 40 (88.89%) females were positive; and in Tanzania (2018), 41 (95.35%) females were positive. Based on a medium DNA load, the positivity rate ranged between 0 and 16 (0–51.61%). For a high DNA load, the positivity rate ranged between 2 and 6 (4.44–19.35%, Table 2).

3.3. FGS Geographical Distribution Based on Diagnostic Testing

The FGS prevalence based on PCR detection ranged from 57.5% (Zambia in 2016) upwards to 79.5% (Ghana in 2013) and others in between (Table 3). PCR consistently detected S. haematobium-specific DNA (4–15 times) in extracted DNA from urine samples collected from different endemic countries compared to traditional diagnostic tests, such as hematuria and urine filtration.

3.4. FGS Distribution Comparison Based on Gender

S. haematobium (the causative agent of FGS) infections were comparatively higher among females than in males in Zambia (2016: 35% vs. 24.4%, and 2017: 41% vs. 33.6%) and Tanzania (2018: 41.4% vs. 23.1%) (Table 4). Similarly, females had higher S. mansoni infections over three years (Zambia 2016 and 2017, and Tanzania 2018) than males with S. mansoni infections. Co-occurrence (S. haematobium and S. mansoni) among females and males remained somewhat similar throughout the years in the three countries (Table 4).

3.5. FGS Distribution Based on Age Group

The FGS infection level had been consistently higher among pre-teens to young adults (11–20 years) for three years (2013, 2016, and 2017) in two countries (Ghana and Zambia) (Table 5). The infection level was higher for mid-ages (>31 years) for only Tanzania in 2018 (Table 5). The second highest infection level was found among children and juveniles (1–10 years) (Table 5).

4. Discussion

The outcome of this study highlights that FGS has been predominant in females in different endemic countries over the years, with a high overall prevalence in certain age groups and when compared to males. The findings are crucial as awareness and knowledge of FGS are largely absent in communities and healthcare workforces in endemic countries [2]. The analytical outcome highlights that FGS is predominant in females among the evaluated urine samples in Ghana (2013), Zambia (2016 and 2017), and Tanzania (2018), and the prevalence ranges from 57.5% to 79.5% (Table 1). This is a prelude to underestimating the true prevalence of FGS as it is currently based on a small number of studies [5,20].
Cell-free S. haematobium-specific DNA detection via Polymerase Chain Reaction (PCR) consistently detected more infections (4–15 times) than traditional diagnostic tests, such as hematuria and urine filtration for urine samples collected from different endemic countries over the years (Table 3). The presence of S. haematobium-specific DNA in urine is an indication of an active infection that clears within two weeks of Mass Drug Administration (MDA [21]). The level of DNA extracted from the urine of PCR-positive individuals is reflective of the infection level and mirrors the high (10 and above ng/µL), medium (4–10 ng/µL), and low infection (0.5–3 ng/µL) levels. PCR has shown its effectiveness as most of the positive infections detected occurred in low-level infections (Table 2). Sensitive and effective diagnostics are paramount for gaining a true sense of the prevalence and extent of FGS in endemic areas, as it is currently substantially under-reported [5,22,23].
Infections related to S. haematobium were relatively higher among females compared to males in three years for two different countries, except for Ghana (Table 4). Co-occurrence along with S. mansoni was higher only for Zambia across two years and lower for Ghana and Tanzania when compared to males (Table 4). FGS infection was consistently higher within the age group of pre-teens to young adults (11–20-yer-olds) in Ghana and Zambia for three years, except for Tanzania (Table 5). Interestingly, children (1–10-year-olds) had the second highest infection level for Ghana and Zambia (Table 5). Girls and women are susceptible to schistosomiasis from a young age in endemic areas, and it affects women of all age groups [5,24]. Recurrent infection occurs throughout the life of these women in endemic areas due to repeated exposure to infested water bodies [5]. In addition, 30–75% of girls and women with urinary schistosomiasis develop FGS [24,25]. So, it is important to detect FGS infection at an early stage of life, such as in children and young adults, as this is the age impacted most by S. haematobium infection [5]. Moreover, FGS infection leads to adverse reproductive health outcomes, organ dysfunction, and reproductive morbidity [20].
This study has its shortcomings. It was a retrospective study based on urine samples collected previously and evaluated via PCR for S. haematobium detection. The sample size per country could be a limiting factor, although the general findings were similar to previous findings [5,20]. Only urine samples were part of this study; vaginal swabs or colposcopy pictures of lesions were absent in the three countries, usually used to validate the pathological signs of FGS. However, cell-free repeat species-specific DNA detection for S. haematobium from urine has been successful in previous studies [26,27].
This study helped to explore the true burden of FGS for broader geographical areas, which will help to develop strategies to control FGS and improve current intervention measurements. FGS is largely neglected, overlooked, and not researched to determine the true prevalence, geographic distribution, and age group infection variation for S. haematobium endemic countries. Future priorities will be aimed at improving awareness and addressing the lack of knowledge by providing accurate data, using highly sensitive molecular diagnostics along with vaginal swabs, and developing an integrated control approach within broader Schistosomiasis control programs. These measures will be important for the detection, control, and elimination of FGS from endemic countries.

Author Contributions

Conceptualization: N.L.; data management, extraction, and analysis: N.L., J.M., M.M.M. and N.K.; original draft: N.L., L.Z. and L.B.; supervision and funding acquisition: N.L. and N.K.; revision of the manuscript: N.L., L.Z. and L.B. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the mini-grant provided by the Institute for Women’s Leadership at Marquette University.

Institutional Review Board Statement

This study was based on retrospective data analysis. All utilized data for this study were collected as part of other studies and data were generated as per the guidelines set by the Marquette University IRB during those studies. For the current study, we just utilized the existing data and conducted the new analysis. No new human samples were collected or evaluated as part of this study. Hence, approval from the Marquette University IRB was not required to perform the tasks of this study.

Informed Consent Statement

Not applicable.

Data Availability Statement

The raw data supporting the conclusions of this article will be made available by the authors upon request.

Conflicts of Interest

The authors declare that this research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

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Figure 1. The model of FGS data analysis determines the prevalence and burden in different geographic locations over multiple years.
Figure 1. The model of FGS data analysis determines the prevalence and burden in different geographic locations over multiple years.
Parasitologia 04 00034 g001
Table 1. Prevalence of Female Genital Schistosomiasis (FGS) among the total samples collected in Ghana, Zambia, and Tanzania.
Table 1. Prevalence of Female Genital Schistosomiasis (FGS) among the total samples collected in Ghana, Zambia, and Tanzania.
Data SourceTotal SamplesTotal FemalesPositive Females
(S. haematobium Prevalence *)
Negative Females
(S. haematobium Prevalence *)
Ghana 20139039 (43%)31 (79.5%)8 (20.5%)
Zambia 201613380 (60%)46 (57.5%)34 (42.5%)
Zambia 201711060 (54.5%)45 (75%)15 (25%)
Tanzania 201810470 (67.3%)43 (61.4%)27 (38.6%)
* Disease prevalence = proportion of positive infections by each test out of a total number of samples evaluated.
Table 2. Prevalence of FGS based on the DNA concentrations of PCR-positive individuals in Ghana, Zambia, and Tanzania.
Table 2. Prevalence of FGS based on the DNA concentrations of PCR-positive individuals in Ghana, Zambia, and Tanzania.
DNA Concentration
(ng/μL)
DNA Concentration Total Females in Ghana 2013Total Females in Zambia 2016Total Females in Zambia 2017Total Females in Tanzania 2018
Gr. A (0.5–3)Low9 (29.04%)42 (91.30%)40 (88.89%)41 (95.35%)
Gr. B (4–10)Medium 16 (51.61%)4 (8.70%)3 (6.67%)0 (0%)
Gr. C (10–above)High6 (19.35%)0 (0%)2 (4.44%)2 (4.65%)
Duplicated/missing samples were discarded.
Table 3. Infection prevalence of FGS based on hematuria, urine filtration, and the PCR diagnostic test. -- = absence of positive or negative samples.
Table 3. Infection prevalence of FGS based on hematuria, urine filtration, and the PCR diagnostic test. -- = absence of positive or negative samples.
Data SourceHematuriaUrine FiltrationPCR
PositiveNegativePositiveNegativePositiveNegative
Ghana 20138 (18.6%)35 (81.4%)----31 (79.5%)8 (20.5%)
Zambia 20163 (3.7%)79 (96.3%)082 (100%)46 (57.5%)34 (42.5%)
Zambia 20177 (11.7%)53 (88.3%)3 (5%)57 (95%)45 (75%)15 (25%)
Tanzania 2018--------43 (61.4%)27 (38.6%)
Table 4. Comparison among females and males detected as positive for S. haematobium, S. mansoni, and dual infections. Male = M, Female = F.
Table 4. Comparison among females and males detected as positive for S. haematobium, S. mansoni, and dual infections. Male = M, Female = F.
LocationTotal Female Total MaleFemaleMale
S. haematobiumS. mansoniCo-OccurrenceS. haematobiumS. mansoniCo-Occurrence
Ghana 2013394731 (36%)33 (38%)27 (69%)39 (45%)41 (47.7%)35 (74.5%)
Zambia 2016805146 (35%)61 (46.6%)33 (41.3%)32 (24.4%)34 (26%)20(39%)
Zambia 2017605045 (41%)47 (42.8%)47 (78%)37 (33.6%)38 (34.6%)31 (62%)
Tanzania 2018703443 (41.4%)54 (52%)37 (52.9%)24 (23.1%)28 (27%)23 (67.7%)
It is found to be predominant among the age group of 11–20 years.
Table 5. Prevalence of Female Genital Schistosomiasis (FGS) among different female age groups. -- = absence of positive or negative samples.
Table 5. Prevalence of Female Genital Schistosomiasis (FGS) among different female age groups. -- = absence of positive or negative samples.
Location Total FemalesS. haematobium Positive
Gr. A (0–10 years) Gr. B (11–20 years)Gr. C (21–30 years)Gr. D (>31 years)
Ghana 2013399 (23.1%)22 (56.4%)----
Zambia 20168018 (22.5%)28 (35%)----
Zambia 20176013 (21.7%)32 (53.3%)----
Tanzania 201870--4 (5.7%)8 (11.4%)31 (44.3%)
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Kaur, N.; Buss, L.; Zorn, L.; Mwansa, J.; Mutengo, M.M.; Lodh, N. Female Genital Schistosomiasis (FGS) Prevalence and Burden Across Endemic Countries, Timelines, and Age Groups: A Retrospective Study. Parasitologia 2024, 4, 382-389. https://doi.org/10.3390/parasitologia4040034

AMA Style

Kaur N, Buss L, Zorn L, Mwansa J, Mutengo MM, Lodh N. Female Genital Schistosomiasis (FGS) Prevalence and Burden Across Endemic Countries, Timelines, and Age Groups: A Retrospective Study. Parasitologia. 2024; 4(4):382-389. https://doi.org/10.3390/parasitologia4040034

Chicago/Turabian Style

Kaur, Navneet, Lilianna Buss, Lauren Zorn, James Mwansa, Mable M. Mutengo, and Nilanjan Lodh. 2024. "Female Genital Schistosomiasis (FGS) Prevalence and Burden Across Endemic Countries, Timelines, and Age Groups: A Retrospective Study" Parasitologia 4, no. 4: 382-389. https://doi.org/10.3390/parasitologia4040034

APA Style

Kaur, N., Buss, L., Zorn, L., Mwansa, J., Mutengo, M. M., & Lodh, N. (2024). Female Genital Schistosomiasis (FGS) Prevalence and Burden Across Endemic Countries, Timelines, and Age Groups: A Retrospective Study. Parasitologia, 4(4), 382-389. https://doi.org/10.3390/parasitologia4040034

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