Abstract
Background
Chronic infection with Schistosoma haematobium causes female genital schistosomiasis (FGS), which leads to diverse lesions in the female genital tract and several complications, including infertility and a higher risk for HIV transmission. This study aims to understand the knowledge, attitudes, and practices (KAP) toward FGS and associated factors among women and health professionals in the schistosomiasis endemic focus of Kimpese, western Democratic Republic of Congo (DRC).
Methods
In January 2022, two semi-quantitative questionnaires were administered to 201 randomly selected community women in Kifua II village, and to purposely selected health professionals (20 nurses and 41 doctors) from Kimpese Health Zone. KAP statements were coded using Likert scale, summarized as frequencies and percentages, and assessed for internal reliability using Cronbach’s alpha. Associations between the socio-demographic characteristics of respondents and the KAP variables were assessed using Pearson chi-square (χ2) test, Cramer’s V (φ) and gamma (γ) coefficients.
Results
Overall, respondents had high knowledge of schistosomiasis in general but low FGS-specific knowledge (91% versus 45%). Misconceptions concerned the disease transmission, with 30.3% of women and 25% of the nurses believing that FGS is transmitted by drinking untreated water, while 26.8% of the doctors mentioned sexual contact as a mode of FGS transmission. Negative attitudes included considering FGS not a very serious disease (34.8%), feeling uncomfortable during gynaecological examination (35.3%), difficulties avoiding risky water contact (72.1%) and open defecation/urination (41.3%), not intending to share FGS status with their husbands (38.3%) and loved ones (63.6%), and believing that husbands would leave them if they were infertile (31.8%). Regarding practices, 77.6% of women engaged daily in activities involving contact with water. Practices of health professionals were hampered by the lack of equipment and specialized knowledge for FGS diagnosis with only 57% of healthcare workers having a microscope in their facilities. Women’s KAPs varied by age, education, marital status, occupation and monthly income.
Conclusion
This study highlights insufficient knowledge, existing negative attitudes, at risk practices towards FGS by women, and limitations of FGS management by health professionals. These findings can help for tailored health education and WASH strategies, and call for health professional’s capacities reinforcement.
Author summary
Schistosomiasis is a disease caused by parasitic worms and it is contracted through contact with contaminated water. FGS is a long-term consequence of urogenital schistosomiasis, a form of the disease that affects the female reproductive organs and can lead to infertility, but also stigma and discrimination. This study used a quantitative research approach to explore community women and healthcare workers’ knowledge, attitudes and practices on and health-seeking behaviour of the women regarding FGS in Kongo Central, DRC. While both groups had high knowledge of schistosomiasis, they had a limited understanding of FGS specifically. Misconceptions about its cause and prevention were common, particularly among medical doctors. Many community members engaged in risky water contact and hygiene practices. Healthcare workers reported limited diagnostic tools and expressed interest in specialised training on FGS diagnosis, treatment, and prevention. Consequent to limited knowledge and ill-equipped laboratories, health workers are most likely underreporting the disease in the region. The study highlights the need to integrate FGS into public health education programs for both community members and healthcare workers in Kongo Central and underscores the importance of addressing misconceptions about the disease and the prevention measures.
1. Introduction
Human schistosomiasis (generally known as bilharzia or snail fever) is a neglected tropical parasitic infection [1], endemic to communities living in areas that have no access to adequate safe water and sanitation amenities [2]. There are over 240 million schistosomiasis infections globally, with 95% of these prevailing in Africa [2–5]. Schistosomiasis ranks second to malaria in terms of prevalence, constantly raising public health and socio-economic apprehension in Africa [6]. Three main species affect humans on the African continent: Schistosoma haematobium causes urogenital schistosomiasis, while Schistosoma mansoni and Schistosoma intercalatum cause intestinal schistosomiasis. The respective parasite species are transmitted through freshwater snails that belong to different genera, namely Biomphalaria (S. mansoni) and Bulinus (S. intercalatum and S. haematobium). When a person comes into contact with infested water, the parasite larvae (cercariae) penetrate the skin [7, 8]. Both forms of schistosomiasis (intestinal and urogenital) cause anaemia, stunted growth, and reduced learning ability in children. The eggs of S. mansoni and S. intercalatum are lodged in the mesenteric veins of the intestines, while those of S. haematobium are lodged in the veins surrounding the urogenital system [9–11]. The parasite eggs trigger an inflammatory immune response that causes acute or chronic illness. The disease is often not fatal, but in its chronic form, S. mansoni and S. intercalatum mainly lead to abdominal pain, bloody diarrhoea, severe fever, hepatomegaly and hepatic fibrosis, while chronic S. haematobium infection can lead to haematuria, irritation in the bladder, bladder cancer, painful and frequent urination [1].
Chronic infection with S. haematobium also causes female genital schistosomiasis (FGS), characterised by schistosome eggs and /or a distinctive pathology in the female reproductive system [12–14]. Eggs that are trapped in the urogenital tissues will provoke an inflammatory reaction with diverse lesions in the genital tract of women and girls [12–14]. Other symptoms include postcoital haemorrhage, itchiness, unusual discharge, dyspareunia and incontinence [9, 15]. Additionally, non-specific symptoms, for example, vaginal discharge and itchiness, are often mistaken for sexually transmitted illnesses. This leaves many girls and women misdiagnosed, leading to the affected females, especially young girls, being accused of sexual promiscuity, which in turn causes stigma and discrimination [16]. Other ripple effects associated with FGS include marital conflicts and emotional distress [16]. Besides these adverse reproductive, emotional and social consequences, FGS is also known to be a co-factor in acquiring human immunodeficiency virus type 1 (HIV-1), human papillomavirus (HPV) and cervical cancer [14, 17–19].
Genital manifestations of schistosomiasis have received less attention than urinary and intestinal manifestations in terms of the number of publications [19]. In addition, the risk posed by FGS to sexual reproductive health is insufficiently addressed in public health policies [9, 10]. FGS is often linked to problematic detection, as diagnosis requires specialised equipment (colposcope) and training, which leads to underreporting in most endemic areas, hence, a lack of reliable data on prevalence. However, based on the prevalence of S. haematobium, an estimated 56 million women and girls in most communities of Africa are at risk of FGS infection [16]. Moreover, apart from the communities lacking knowledge of FGS, many healthcare professionals are unaware of the disease, diagnosis, risks, and treatment [16]. Therefore, increasing awareness among the communities and healthcare professionals is important to enable early detection of FGS and focus on preventive measures. Studies show that community mobilisation and participation (bottom-up approach) are key to sustainable and compelling communication to inform the affected communities on symptoms, prevention and control of FGS [20, 21]. However, for bottom-up approaches to be successful, the existing knowledge, attitudes and practices (KAP) toward the disease need to be assessed [22]. The KAP information gathered could inform the development of effective control strategies. This study, therefore, sought to fill this gap by assessing the KAP toward FGS and sociodemographic characteristics associated with the KAP among community women and health professionals in a highly endemic region in Kongo Central province, DRC.
2. Methodology
2.1 Ethics statement
The study was approved by the Ethical Committee of the University of Kinshasa, DRC (n°191/CNES/BN/PMMF/2020). Before the start of the interviews, the community members were invited on the 7th of January 2022 for a sensitisation meeting at Kifua II local health centre, where the village chief and the nurses of Kifua II local health centre were present. Permission to interview the medical doctors and the nurses was sought from the Chief Medical Officer at Kimpese Health Zone. The community surveys were conducted at the women’s households in a comfortable private setting of their choice. The doctors were visited at their respective working facilities in Kimpese city, while nurses were invited at the Kimpese Health Zone office. Facemasks were provided before the start of the interviews, given the COVID-19 pandemic context. The interviewer explained the aims of the study and the guaranteed confidentiality of the data collected to the participants. In addition, they were informed about the right to stop their participation at any time without any consequence and were encouraged to ask questions about the research. Additionally, an oral inform consent was sought from each participant over 18 years of age. For this, it was set in the questionnaire that when a participant did not agree to proceed with the interview after the introduction of the study, the questionnaire ended automatically. For participants under 18 years old, an assent was obtained from the participant, followed by an oral consent from the participant’s parent. When one of them did not agree to proceed with the interview, the questionnaire ended automatically.
2.2 Study area and setting
This study was conducted in January 2022 in two areas of Kongo Central province of DRC: (i) community women were interviewed in Kifua II village located in the Health Zone (HZ) of Kwilu Ngongo and (ii) the medical doctors and nurses in the city of Kimpese HZ (Fig 1). Kifua II lies 20 Km from the city of Kimpese on the national road n°1 and borders the Ngongo River, which supplies water to many households in the community. The city of Kimpese includes the central office of the rural HZ of Kimpese and the general referral hospital of this zone. The region is known to be endemic for urogenital schistosomiasis [23, 24] and Kifua II was selected based on its high prevalence (68%) of schistosomiasis infections and the recent study on co-infection of schistosomiasis with salmonella [24]. The transmission of schistosomiasis is favoured by climatic conditions (temperature and rainfall) that are conducive to the survival of the snails that transmit schistosomiasis, poor hygiene with no latrines or access to latrines, risky activities involving contact with water and the absence of a mass treatment programme in this village before 2016. Kimpese HZ is characterised by poor hygiene, with previous studies reporting 41% not having a toilet in the household, while 48% opting for open defecation and urination [25]. Furthermore, the communities are primarily engaged in farming and small-scale animal husbandry, which are mostly done on hillsides and riverbanks, increasing the likelihood of contact with water containing infected snails. Finally, there is no prior record of mass drug administration (MDA) for schistosomiasis control in Kifua II village since the village was misclassified as low endemic [23, 24]. However, treatment was provided to the infected people after the schistosomiasis prevalence study in 2015 [24] and the village is now part of the MDA program.
Fig 1. Study area showing locations of the study groups in Kongo Central, DRC.
(Base map: Database of Global Administrative Areas: https://geodata.ucdavis.edu/gadm/gadm4.1/shp/gadm41_COD_shp.zip).
2.3 Study design
A cross-sectional study design was employed with two semi-structured questionnaires for three weeks in January 2022: 1) for the community women and 2) another for the healthcare professionals; with both open-ended and closed-ended questions adapted from Anyolitho et al. and Masong et al. [26, 27]. The questionnaires were translated from English to French before feeding them into the open-source data collection application “KoBoToolbox”. The application enables researchers to collect data offline in remote settings and later upload the gathered information to a server once connected online [28]. The translated versions were administered by 8 trained field researchers who were competent in both French and the local language (Kikongo); Six of these were female (two from Kifua II and four from Kimpese) and two were male (one of them was a medical doctor from Kimpese). The two target study groups comprised the community women in Kifua II (only interviewed by the female researchers) and healthcare professionals (nurses and doctors) in Kimpese (all the doctors were interviewed by the medical doctor interviewer).
The questionnaire (Texts A and B in S1 File) was subdivided into four sections: (i) demographic information; (ii) knowledge indicators or familiarity with the signs and symptoms, modes of transmission, control methods and risk factors; (iii) attitudes toward the disease and perceptions toward the infected individuals (state of stigmatisation) (statements for the community women were different from those of the healthcare professionals); (iv) socio-cultural and management practices related to the spread of FGS and the health-seeking behaviour of the community women. Information guides were provided to the community women and the healthcare professionals after the interviews, with relevant information about FGS. The information guides were made based on available FGS literature and educational resources, such as from the Female genital schistosomiasis: A pocket atlas for clinical health-care professionals (who.int), and then translated into French and Kikongo.
2.4 Sample size determination and participants selection
Sample size determination for the women was based on similar studies conducted in Cameroon and Zimbabwe [27, 29]. The population size (N = 431) of women in the target reproductive age was derived based on United Nations World Population Prospects Report guidelines, using the total population of Kifua II village, estimated to be 1,400 [24]. The report suggests that 49.6% of the world’s population is female and 62% of them are between the ages of 15–59 years. Hence, N = 1400×0.496×0.62. The sample size (n = 203) was then estimated following Cochran’s formula n = [(z2pq)/e2]/[1+(z2pq/e2N)]; where, ‘n’ is the sample size, ‘Z’ is the critical value at 95% confidence level (1.96), ‘e’ is the margin of error (5%), ‘p’ is the sample proportion (50%), ‘q’ is 1-p and ‘N’ is the population size (431). The community women were selected through simple random sampling, while the selection of the healthcare professionals was purpose-driven. Head nurses from all the 20 local health posts in Kimpese Health Zone were chosen, while 41 of the available 44 medical doctors in Kimpese HZ participated in the survey.
2.6 Data processing and statistical analysis
The independent variables were the socio-demographic characteristics (age, level of education, monthly income, marital status and type of occupation). The variable age was assessed for suitability to differentiate between teenagers and young adults by grouping participants aged 15–25 into distinct age categories (15–19 and 20–25), to test for potential differences in their KAP towards FGS. For the dependent variables, we used Likert scales for knowledge, attitude and practices. The knowledge score was obtained by combining all the correct answers (coded one) given by the respondents. Total scores (maximum of 25 correct answers) were a combination of the knowledge of symptoms, complications and modes of transmission, with low knowledge (coded zero) ranging from 0 to 8, moderate knowledge (coded one) ranging from 9 to 16 and high knowledge (coded two) ranging from 17 to 25. Statements to measure attitude were collected using a 5-point Likert scale ranging from 1 (strongly disagree) to 5 (strongly agree). Scores were computed by averaging 13 statements, with the high scores indicating positive attitudes towards the disease. Cronbach’s alpha (α) coefficient was used to assess the internal reliability and consistency of the Likert scales. The coefficient ranges from 0 to 1, with “_> .9—Excellent, _> .8—Good, _> .7—Acceptable, _> .6—Questionable, _> .5—Poor, _< .5—Unacceptable” [30]. For the practice section, the responses indicating good practice (not involved in activities that could lead to the spread or transmission of FGS; seeking medical attention when experiencing FGS-like symptoms) were coded one and zero for otherwise (responses that reflect bad practice). Data were analysed using IBM SPSS software version 19. Summarised descriptive statistics (frequency values and percentages) were obtained for the KAP variables and the respondents’ sociodemographic profile. Contingency tables were computed and Pearson chi-square (χ2) (for the nominal variables), Cramer’s V (φ) and gamma (γ) coefficients (for the ordinal variables) were recorded to ascertain the sociodemographic characteristics that are associated with the knowledge, attitudes, and practice variables among the respondents. For the interpretation of the results, the level of statistical significance was set at a p-value of 0.05, while the strength of the associations (using φ and γ coefficients) were as follows: >0.5 high association; 0.3 to 0.5 moderate; 0.1 to 0.3 low association; 0.0 to 0.1 little if any association [28].
3. Results
3.1 Sociodemographic characteristics of the participants
A total of 262 participants were included (201 community women, 20 nurses and 41 doctors). The age of community women ranged between 15–59 years, with more than half (56.2%) aged 36 and below, while only 20.9% were older than 48 years. Most (65.6%) of them were married and over a third (39.8%) of the respondents never obtained primary education. The majority (59.7%) were farmers, while slightly over one-fifth (20.9%) were unemployed. Nearly two-thirds (60.2%) had monthly earnings of less than 100,000 Congolese Dollar Franc (CDF) (equivalent to USD 50). Almost two-thirds (62.3%) of the healthcare professionals were between 29 and 45 years old, with 85.2% of them being male. The majority (91.8%) have been practising for less than 20 years (Text C in S1 File).
3.2 Knowledge of FGS
3.2.1 Community women’s knowledge
The frequency of the level of knowledge by demographic characteristics of community women is given in Table 1. Overall, more than half (55.7%) of women had a low level of knowledge regarding FGS. This trend was the same for all categories except among women with monthly income of 100,000–199,000CDF where 66.7% had a moderate level of knowledge.
Table 1. Knowledge, attitude and practices towards female genital schistosomiasis by socio-demographic characteristics of community women in Kifua II village.
| Socio-demographic characteristics | n | Knowledge (levels) | Attitudes (means) | Practices | |||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| Low | Moderate | High | 1 | 2 | 3 | 4 | 5 | Bad | Good | ||
| All | 201 | 112 (55.7) | 80 (39.8) | 9 (4.5) | 70 (34.8) | 11 (5.5) | 3 (1.5) | 98 (48.8) | 19 (9.4) | 5 (2.5) | 196 (97.5) |
| Age (years) | |||||||||||
| 15–25 | 61 | 38 (62.3) | 22 (36.1) | 1 (1.6) | 22 (36.0) | 7 (11.5) | 2 (3.3) | 27 (44.3) | 3 (4.9) | 1 (1.6) | 60 (98.4) |
| 26–36 | 52 | 29 (55.8) | 21 (40.4) | 2 (3.8) | 27 (51.9) | 3 (5.8) | 0 (0.0) | 17 (32.7) | 5 (9.6) | 2 (3.8) | 50 (96.2) |
| 37–47 | 46 | 23 (50.0) | 21 (45.7) | 2 (4.4) | 9 (19.6) | 0 (0.0) | 0 (0.0) | 32 (69.6) | 5 (10.9) | 1 (2.2) | 45 (97.8) |
| 48–59 | 42 | 22 (52.4) | 16 (38.1) | 4 (9.5) | 12 (28.6) | 1 (2.4) | 1 (2.4) | 22 (52.4) | 6 (14.3) | 1 (2.4) | 41 (97.6) |
| Education Level | |||||||||||
| Without education | 80 | 43 (53.8) | 33 (41.3) | 4 (5.0) | 24 (30.0) | 4 (5.0) | 0 (0.0) | 45 (56.2) | 7 (8.8) | 2 (2.5) | 78 (97.5) |
| Primary Education | 108 | 61 (56.5) | 43 (39.8) | 4 (3.7) | 39 (36.1) | 7 (6.5) | 3 (2.8) | 49 (45.4) | 10 (9.2) | 3 (2.8) | 105 (97.2) |
| Secondary & high Education | 13 | 8 (61.5) | 4 (30.8) | 1(7.7) | 5 (45.4) | 0 (0.0) | 0 (0.0) | 4 (36.4) | 2 (18.2) | 0 (0.0) | 13 (100.0) |
| Marital Status | |||||||||||
| Not married | 69 | 35 (50.7) | 32 (46.4) | 2 (2.9) | 29 (42.0) | 1 (1.4) | 1 (1.4) | 32 (46.4) | 6 (8.7) | 2 (2.9) | 67 (97.1) |
| Married | 132 | 77 (58.3) | 48 (36.4) | 7 (5.3) | 41 (31.0) | 10 (7.6) | 2 (1.5) | 66 (50.0) | 13 (9.8) | 3 (2.3) | 129 (97.7) |
| Employment Status | |||||||||||
| Unemployed | 100 | 58 (58.0) | 40 (40.0) | 2 (2.0) | 43 (43.0) | 4 (4.0) | 3 (3.0) | 38 (38.0) | 12 (12.0) | 4 (4.0) | 96 (96.0) |
| Employed | 101 | 54 (53.5) | 40 (39.6) | 7 (6.9) | 27 (26.7) | 7 (6.9) | 0 (0.0) | 60 (59.4) | 7 (6.9) | 1 (1.0) | 100 (99.0) |
| Monthly Income (CDF) | |||||||||||
| No response | 49 | 30 (61.2) | 16 (32.7) | 3 (6.1) | 29 (59.2) | 1 (2.0) | 1 (2.0) | 16 (32.6) | 2 (4.1) | 3 (6.1) | 46 (93.9) |
| Less than 100,000 | 120 | 71 (59.2) | 43 (35.8) | 6 (5.0) | 38 (31.7) | 8 (6.7) | 0 (0) | 63 (52.5) | 11 (9.2) | 1 (0.8) | 119 (99.2) |
| 100,000–199,000 | 24 | 8 (33.3) | 16 (66.7) | 0 (0.0) | 2 (8.3) | 2 (8.3) | 2 (8.3) | 14 (58.3) | 4 (16.7) | 1 (4.2) | 23 (95.8) |
| 200,000–299,000 | 5 | 3 (60.0) | 2 (40.0) | 0 (0.0) | 1 (20.0) | 0 (0.0) | 0 (0.0) | 2 (40.0) | 2 (40.0) | 0 (0.0) | 5 (100.0) |
| 300,000–399,000 | 1 | 0 (0.0) | 1 (100.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 1 (100.0) | 0 (0.0) | 0 (0.0) | 1 (100.0) |
| More than 400,000 | 2 | 0 (0.0) | 2 (100.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 0 (0.0) | 2 (100.0) | 0 (0.0) | 0 (0.0) | 2 (100.0) |
*In () are the percentages
Fig 2 shows detailed frequencies of answers to questions regarding knowledge of FGS. While schistosomiasis was known by 91% of the respondents, only 45% had heard about FGS. More than half of the respondents recognised lower abdominal pain as the sign and symptom of FGS (70.6%), reduced fertility (75.1%) and miscarriage (56.2%) as the common complications of FGS, contact with contaminated water as increasing the risk of FGS infection (57.7%) and PZQ as the drug that treats symptoms related to FGS (50.2%). Similarly, 86.1% of the respondents mentioned that FGS can be spread through defecating and urinating in water by an infected person and treating all the infected persons (72.5%) as a way of preventing FGS. For other questions, correct answers were found by less than 50% of community women.
Fig 2. Community women’s, community nurses’ and medical doctors’ knowledge of female genital schistosomiasis in Kifua II and Kimpese, DRC.
Table 2 shows the association between community women’s knowledge of FGS and their sociodemographic characteristics. Age was significantly associated with knowledge of FGS transmission (φ = 0.556, p = 0.000), the group at risk of FGS (φ = 0.521, p = 0.04), and FGS disease prevention (0.518, p = 0.000). Marital status was significantly associated with knowledge of signs and symptoms (φ = 0.796, p = 0.001), transmission mode (φ = 0.595, p = 0.001), and who is at risk of getting FGS (φ = 0.298, p = 0.016). Monthly income was significantly associated with knowledge of signs and symptoms (φ = 0.866, p = 0.000), FGS complications (φ = 0.84, p = 0.000), who is at risk of getting infected (0.322, p = 0.002), and FGS prevention (φ = 0.056, p = 0.000). Type of occupation was significantly associated with knowledge of transmission mode (φ = 0.669, p = 0.000), who is at risk of getting infected (φ = 0.344, p = 0.000), FGS treatment (φ = 0.313, p = 0.000), and FGS prevention (φ = 0.546, p = 0.019). Level of education was significantly associated with knowledge of treatment (φ = 0.224, p = 0.02).
Table 2. Association between community women’s knowledge of female genital schistosomiasis and their sociodemographic background.
| Statement | Age | Marital status | Education level | Occupation type | Monthly income | |||||
|---|---|---|---|---|---|---|---|---|---|---|
| φ | p-value | φ | p-value | φ | p-value | φ | p-value | φ | p-value | |
| Signs and symptoms | 0.737 | 0.283 | 0.796 | 0.001 * | 0.730 | 0.546 | 0.757 | 0.160 | 0.866 | 0.000 * |
| Complications | 0.658 | 0.487 | 0.661 | 0.439 | 0.644 | 0.742 | 0.677 | 0.214 | 0.840 | 0.000 * |
| Transmission | 0.556 | 0.000 * | 0.595 | 0.001 * | 0.517 | 0.687 | 0.699 | 0.000 * | 0.512 | 0.752 |
| Who is at risk of infection | 0.521 | 0.004 * | 0.298 | 0.016 * | 0.228 | 0.895 | 0.344 | 0.000 * | 0.322 | 0.002 * |
| How infected persons spread FGS | 0.502 | 0.221 | 0.232 | 0.009 * | 0.165 | 0.592 | 0.125 | 0.708 | 0.206 | 0.026 * |
| Treatment | 0.461 | 0.811 | 0.199 | 0.130 | 0.224 | 0.020 * | 0.313 | 0.000 * | 0.194 | 0.064 |
| Prevention | 0.518 | 0.000 * | 0.559 | 0.001 * | 0.491 | 0.549 | 0.546 | 0.019 * | 0.656 | 0.000 * |
*Cramer’s V coefficient (φ) test of association was significant at p<0.05
3.2.2 Healthcare professionals’ knowledge
Lower abdominal pain, contact bleeding and genital itching or burning sensation were the most (97.6%, 90.2% and 87.7% respectively) mentioned signs and symptoms of FGS by the doctors. Similarly, the nurses mentioned lower abdominal pain (90.0%) and genital itching or burning sensation (80.0%) as the common symptoms of FGS. Almost two-thirds (65.0%) of the nurses stated irregular menstruation as a sign of FGS, while only 17.1% of the doctors mentioned it (Fig 2A). Most (92.7%) of the doctors mentioned miscarriage as a complication of FGS, while reduced fertility was mentioned as the common complication by most (80.0%) of the nurses. Urinary incontinence (involuntary urination) was mentioned by 40.0% of the nurses and only 7.3% of the doctors (Fig 2B). The majority (85.4%) of the doctors believe that women or girls who are sexually active are at risk of acquiring FGS (Fig 2C). All the doctors and 80.0% of the nurses mentioned that FGS is treated by PZQ (biltricide) (Fig 2D). The doctors and the nurses had high knowledge of FGS transmission modes; however, a few misconceptions were mentioned. These include drinking untreated water (doctors: 26.8% and nurses: 5.0%), sexual contact (doctors: 26.8% and nurses: 5.0%) and eating unwashed fruits and vegetables (nurses: 25.0% and doctors: 4.9%) (Fig 2E). Almost a third (29.3%) of the doctors did not mention defecating and urinating in water as how an infected person contributes to the spread of FGS (Fig 2F). For FGS prevention, health education was mentioned by almost all the doctors (97.5%) and by only 45% of the nurses. Avoiding open defecation/urination was said by 95.2% of the doctors and 80.0% of the nurses, while treating all the infected persons by 90.2% of the doctors and 85.0% of the nurses. Lastly, some misconceptions exist on ways to prevent FGS; including avoiding eating uncooked meat and unwashed fruits and vegetables (mentioned by 30.0% of the nurses and 14.7% of the doctors), washing hands after going to the toilet (mentioned by 40.0% of the nurses and 9.8% doctors), and avoiding walking barefoot and playing in the soil (mentioned by 7.4% of the doctors and 5.0% of the nurses) (Fig 2G).
3.2 Attitudes toward FGS
3.2.1 Community women’s attitude
The Cronbach’s α coefficient was 0.934, indicating that the Likert scales were reliable and internally consistent. The means of the scores of attitude by sociodemographic characteristics of community women are shown in Table 1. Overall, more than half of them had a positive attitude, with 48.8% reaching a mean of 4 and 9.4% a mean of 5 (the most positive attitude). Almost one-third of women (34.8%) had a negative attitude towards FGS (mean = 1). Positive attitude (mean = 4) was the most frequent among all categories of sociodemographic characteristics, except among women aged 26–36 years, those with secondary and higher education, and those unemployed, with respectively 51.9%, 45.5%, 43% scoring a mean of 1.
Detailed responses to statements related to community women’s attitudes toward FGS are summarized in Fig 3. More than a third of women (34.8%) considered FGS not a very serious disease. Regarding disease diagnosis, 34.8% would not go to the hospital if infected and 35.3% would feel uncomfortable during gynaecological examination. As for treatment and prevention, 34.8% of women did not perceive taking FGS medication to be important for their health, 72.1% found it difficult to avoid risky water contact and 41.3% didn’t think that defecating and urinating in the toilet was important for their health. Regarding the need for social support, 38.3% didn’t intend to share their FGS status with their husband or their loved ones (63.6%), and 31.8% believed that their husbands would leave them if they were infertile.
Fig 3. Community women’s attitudes toward female genital schistosomiasis in Kifua II, DRC (SD—Strongly Disagree; D—Disagree; NS—Not Sure; A—Agree; SA—Strongly Agree).
Associations between community women’s attitudes toward FGS and their socio-demographic characteristics are summarized in Table 3. Age and monthly income were found to have a positive association with how serious FGS is considered (γ = 0.218, p = 0.016; γ = 0.244, p = 0.025), openness to undergo gynaecological examination (γ = 0.182, p = 0.042; γ = 0.342, p = 0.001) and taking medication (γ = 0.192, p = 0.007; γ = 0.24, p = 0.017). This implies that younger women and those with lower monthly income do not believe that FGS is a serious disease, are uncomfortable to find out if they have FGS and do not agree that taking medication is important. Avoiding risky water contact had a significant and positive association with age (γ = 0.312, p = 0.001). Health importance of defecating and urinating in the toilet had a positive association with the level of income (γ = 0.304, p = 0.003) and occupation (γ = 0.15.327, p = 0.002). This implies that women with lower income do not consider avoiding open defecation or urination unhygienic or important for their health. Visiting a traditional healer was found to have a positive and significant association with age (γ = 0.386, p = 0.003), monthly income (γ = 0.375, p = 0.006) and type of occupation (γ = 23.33 p = 0.000). This suggests that older women with more income would not visit a traditional healer if they found out they have FGS. Talking to their husbands or loved ones regarding FGS symptoms was positively associated with monthly income (γ = 0.214, p = 0.034; γ = 0.26, p = 0.012) and occupation (γ = 9.354, p = 0.025; γ = 17.818, p = 0.000). These infer that community women with lower income are less willing to open up and talk about their symptoms to other people.
Table 3. Association between community women’s attitudes toward FGS and their socio-demographic background.
| Statement | Age | Education | Monthly income | Marital status | Occupation type | |||||
|---|---|---|---|---|---|---|---|---|---|---|
| γ | p-value | γ | p-value | γ | p-value | χ2 | p-value | χ2 | p-value | |
| FGS is a very serious disease | 0.218 | 0.016 * | -0.226 | 0.047 * | 0.244 | 0.025 * | 2.044 | 0.563 | 7.237 | 0.065 |
| I would take action if I found that I had FGS by going to the hospital | 0.159 | 0.064 | -0.157 | 0.16 | 0.145 | 0.17 | 4.241 | 0.237 | 17.326 | 0.001 * |
| I feel comfortable during a gynaecological examination | 0.182 | 0.042 * | -0.179 | 0.126 | 0.342 | 0.001 * | 1.871 | 0.6 | 9.197 | 0.027 * |
| It is important to avoid contact with contaminated water | 0.312 | 0.001 * | -0.17 | 0.16 | 0.016 | 0.89 | 5.952 | 0.114 | 6.313 | 0.097 |
| Defecating and urinating in the toilet is important for my health | 0.132 | 0.073 | 0.143 | 0.192 | 0.304 | 0.003 * | 4.927 | 0.177 | 15.327 | 0.002 * |
| Taking FGS medication is important for my health | 0.192 | 0.007 * | -0.155 | 0.15 | 0.24 | 0.017 * | 1.889 | 0.596 | 15.998 | 0.001 * |
| If I find out I have FGS, I need to see a traditional healer | 0.386 | 0.003 * | -0.252 | 0.102 | 0.375 | 0.006 * | 6.704 | 0.082 | 23.33 | 0.000 * |
| If I find out I have FGS, I need to see a religious leader | 0.112 | 0.418 | -0.154 | 0.351 | 0.255 | 0.087 | 1.233 | 0.745 | 26.839 | 0.000 * |
| My husband’s family and community will not respect me if I am infertile or have FGS | 0.232 | 0.067 | -0.015 | 0.921 | 0.254 | 0.064 | 0.101 | 0.992 | 20.748 | 0.000 * |
| I can talk/I talk to my husband about the symptoms of FGS | 0.127 | 0.144 | -0.176 | 0.112 | 0.218 | 0.034 * | 4.984 | 0.173 | 9.354 | 0.025 * |
| I talk about FGS with my loved ones | 0.108 | 0.23 | -0.094 | 0.415 | 0.26 | 0.012 * | 3.525 | 0.317 | 17.818 | 0.000 * |
*Gamma coefficient (γ) test of association was significant at p<0.05
3.2.2 Healthcare professionals’ attitude
Detailed responses to statements related to healthcare professionals’ attitudes toward FGS are shown in Fig 4. Most (81.9%) of healthcare professionals regard FGS as a very serious disease and 95.7% believe that it is necessary to advocate for its prevention measures. Similarly, 96.7% consider diagnosing FGS their responsibility and very important for them. When asked if the medication for FGS is expensive, 62.3% were not sure, while 18.0% disagreed and 11.5% agreed that FGS medication is expensive. Most (91.8%) of the respondents agreed to talk about FGS to their colleagues, while only 6.6% were not sure if they could.
Fig 4. Healthcare professionals’ attitudes and perceptions toward female genital schistosomiasis.
3.3 Practices
3.3.1 Community women’s practices
a) Water, sanitation, and hygiene practices
As shown in Table 4, the main source of water for household use was protected wells (42.3%) or rivers/streams (40.3%). More than three-quarters (77.6%) of the respondents come into contact with the river/stream daily through fetching water, followed by agriculture (48.3%) cassava retting (43.3%), washing dishes and laundry (38.3%) and bathing (31.1%). Almost two-thirds (63.2%) visit the river/stream twice a day, and about 50% spend more than 15 minutes in the water. At least 31.3% of the respondents do not own a latrine, while a large majority (70.6%) defecate or urinate outside the toilet, mostly in the bush (59.7%), because they do not have access to a toilet (46.8%). This happens daily for 46.8% of the respondents.
Table 4. Summary of community women’s practices, water, sanitation, and hygiene regarding FGS.
| Variable | Response | Frequency | Percentage |
|---|---|---|---|
| Main source of water for the households | Protected/covered water well | 85 | 42.3 |
| River /stream | 81 | 40.3 | |
| Piped water | 33 | 16.4 | |
| Unprotected/uncovered water well | 2 | 1.0 | |
| Activities leading to water contact | Fetch water | 156 | 77.6 |
| Agriculture | 97 | 48.3 | |
| Cassava retting | 87 | 43.3 | |
| Laundry and washing dishes | 77 | 38.3 | |
| Bathing | 63 | 31.3 | |
| Fishing | 28 | 13.9 | |
| Baptism | 10 | 5.0 | |
| Swimming | 8 | 4.0 | |
| Time taken for activities in contact with water | More than15 minutes | 101 | 50.2 |
| Less than 5 minutes | 56 | 27.9 | |
| 5 to10 minutes | 25 | 12.4 | |
| 10 to 15 minutes | 19 | 9.5 | |
| Number of times for daily contact with water | Twice | 127 | 63.2 |
| Once | 46 | 22.9 | |
| More than 3 times | 17 | 8.5 | |
| Thrice | 11 | 5.5 | |
| Type of toilet for the household | Pit latrine | 89 | 44.3 |
| No toilet | 63 | 31.3 | |
| Communal latrine | 39 | 19.4 | |
| Flush toilet | 10 | 5.0 | |
| If defecate/urinate outside the toilet | Yes | 142 | 70.6 |
| No | 59 | 29.4 | |
| Where defecated/urinated outside the toilet | In the bush | 120 | 59.7 |
| In an open space | 65 | 32.3 | |
| In the water | 22 | 10.9 | |
| In a tin bucket | 5 | 2.5 | |
| I don’t remember. | 2 | 1.0 | |
| Why did not use the toilet | No access to the toilet | 94 | 46.8 |
| The Call of Nature | 37 | 18.4 | |
| The toilet was busy/cluttered | 18 | 9.0 | |
| The toilet is there but poorly maintained | 14 | 7.0 | |
| When in the field | 9 | 4.5 | |
| I don’t like using the toilet | 5 | 2.5 | |
| Lack of water to supply the toilet | 1 | 0.5 | |
| The toilet is far from the house | 1 | 0.5 | |
| How many times of defecation/urination outside the toilet | Every day and when nature calls | 87 | 43.3 |
| I do not remember | 42 | 20.9 | |
| It was only once | 10 | 5.0 | |
| Occasionally and when in the field | 3 | 1.5 |
Associations between socio-cultural factors and WASH practices of the community women and their socio-demographic characteristics are shown in Table 5. Age (φ = 0.664, p = 0.000), marital status (φ = 0.7, p = 0.000), and monthly income (φ = 0.682, p = 0.007) were found to have a statistically significant association with activities done in water. Level of education (φ = 0.239, p = 0.012) was associated with the type of toilet used in the household. Defecating or urinating outside the toilet was found to be associated with age, marital status, level of education and occupation. Lastly, type of occupation (φ = 0.348, p = 0.051), had a statistically significant relationship with the action taken when symptoms are experienced (visiting a health facility or not).
Table 5. Association between socio-cultural factors and WASH practices of the community women and their socio-demographic characteristics.
| Statement | Age | Marital status | Education | Occupation type | Monthly income | |||||
|---|---|---|---|---|---|---|---|---|---|---|
| φ | p-value | Φ | p-value | Φ | p-value | φ | p-value | φ | p-value | |
| Activities with water contact | 0.664 | 0.000* | 0.700 | 0.000* | 0.587 | 0.974 | 0.658 | 0.101 | 0.682 | 0.007* |
| Type of toilet | 0.509 | 0.178 | 0.224 | 0.034* | 0.239 | 0.012* | 0.293 | 0.000* | 0.201 | 0.060 |
| Defecating/urinating outside the toilet | 0.570 | 0.041* | 0.310 | 0.004* | 0.325 | 0.002 | 0.410 | 0.000* | 0.173 | 0.305 |
| Action after experiencing the symptoms | 0.491 | 0.250 | 0.333 | 0.098 | 0.272 | 0.959 | 0.348 | 0.051* | 0.253 | 0.994 |
b) Community women’s health-seeking behaviour
Nearly three-quarters (73.1%) of the respondents stated that they would / visit the health facility when they experienced / will experience any of the symptoms related to FGS. Some (15.0%) stated that they would do nothing. Urine and stool tests were mentioned by 52.2% and 34.3% of the respondents respectively, as the tests were done when FGS-related symptoms were experienced. More than half (57.7%) of the respondents reported having received PZQ/biltricide via a treatment campaign, while a few (8.0%) did not because they did not know while family and friends advised against the treatment for 5.0%. Nearly all the respondents (95.0%) stated that they would accept a vaccine if available (Table 6).
Table 6. Summary of community women’s health-seeking behaviour in Kifua II.
| Variable | Response | Frequency | Percentage |
|---|---|---|---|
| What is done after experiencing any FGS-like symptoms | Visited a health facility | 147 | 73 |
| Visited a pharmacist/drug vendor | 35 | 17 | |
| I did nothing | 31 | 15 | |
| Visited a village health worker/midwife | 29 | 14 | |
| I treated myself | 15 | 7.5 | |
| Visited a religious leader | 1 | 0.5 | |
| I washed bathed with hot water | 1 | 0.5 | |
| The reason for not seeking any help | No reason | 21 | 11 |
| I didn’t know who to consult | 5 | 2.5 | |
| Too expensive to obtain treatment | 2 | 1 | |
| I feel ashamed | 2 | 1 | |
| Too difficult to get to a health facility | 1 | 0.5 | |
| Unfriendly healthcare workers | 1 | 0.5 | |
| The tests that were done | Urine test | 105 | 52 |
| Stool test | 69 | 34 | |
| None | 36 | 18 | |
| Vaginal/Cervical screening | 16 | 8 | |
| Sexual Transmitted Infections test | 6 | 3 | |
| If ever received PZQ (Biltricide) through a treatment campaign | Yes | 116 | 58 |
| No | 83 | 41 | |
| I don’t know | 2 | 1 | |
| The last time PZQ was received | Cannot remember | 59 | 29 |
| Within the last 6 months | 39 | 19 | |
| Within the last 2 years | 18 | 9 | |
| Reason for not receiving PZQ | I wasn’t offered the drug/the drugs were not available | 36 | 18 |
| I was not ill | 19 | 9.5 | |
| Did not know about the campaign | 16 | 8 | |
| Family member/ neighbour/friend advised against | 10 | 5 | |
| No reason | 7 | 3.5 | |
| I was not eligible | 3 | 1.5 | |
| Drugs don’t work | 1 | 0.5 | |
| Whether would accept FGS vaccine if available | Yes | 191 | 95 |
| No | 10 | 5 | |
| Why would not receive FGS vaccine | No reason | 3 | 1.5 |
| I don’t like vaccines | 2 | 1 | |
| Poor perception of vaccines in the community | 2 | 1 | |
| I have never suffered from bilharzia | 1 | 0.5 | |
| I am already old | 1 | 0.5 | |
| I fear vaccines | 1 | 0.5 |
3.3.2 Healthcare professionals’ practices and management of FGS
More than three-quarters (77%) of the respondents consider FGS prevalent in Kimpese and 65.6% of them mentioned having had patients with FGS. Some respondents (9.8%) stated to have seen between 5–25 cases and 8.2% saw between 25–35 cases. Of those who had patients with FGS, when asked how they diagnosed the patients, 21% mentioned by clinical examination of urine sediments and stool, while 4% mentioned symptomology. Another misconception concerning FGS diagnosis mentioned was a vaginal smear to reveal the Schistosoma species eggs. For the FGS diagnostic test (referring to a microscope), 57.4% of the respondents mentioned they were available in their working stations and only 49.2% had sometimes access to PZQ (Text D in S1 File).
4. Discussion
This study assessed, for the first time, the KAP toward FGS among community women and health professionals in a well-known endemic area of the Kongo Central province of DRC [23, 25]. Such knowledge is needed to design tailored control strategies. While 91% of women claimed to know about schistosomiasis, more than half (55%) had a low level of knowledge about FGS. This is in line with other studies conducted in endemic sub-Saharan African settings, which reported a higher level of knowledge about urinary schistosomiasis compared to the knowledge of FGS [31–33]. Higher knowledge of urinary schistosomiasis can be explained by the fact that urinary schistosomiasis is generally well recognised by the presence of blood in urine, which is a sensitive and specific symptom. In addition, high knowledge might also result from long-standing endemicity, contact with research teams and/or the organisation of schistosomiasis control campaigns, through mass treatment or health education. In our study area, schistosomiasis is well known since Lengeler at al. (2000) successfully assessed the use of questionnaires on urinary schistosomiasis to map both intestinal and urinary schistosomiasis [34]. Recent sensitisation activities were also conducted in our study area in the framework of research studies and MDA campaigns [23, 24, 35].
The association between high income and high knowledge of FGS symptoms in this study could partly be explained by the fact that people with high income are more likely to access information from sources such as written material or radio and television. A similar observation was made in endemic communities surrounding Lake Albert in Uganda [27].
As expected, medical doctors and nurses had a higher knowledge of FGS symptoms than the community women. As reported previously by Linsuke et al. [35], healthcare staff in this region are aware of schistosomiasis symptoms, including haematuria as an indication of S. haematobium. This is probably linked to regular exposure to cases and the region’s long history of high schistosomiasis prevalence [25, 35].
Our study recorded some misconceptions, mainly linked to FGS transmission, with one in four (27%) medical doctors linking FGS transmission to sexual contact, and 85% claiming that only women and girls who are sexually active are at risk of FGS infection. The same responses were given by 5% and 21% of the nurses and community women, respectively. A similar misconception of sexual transmission of FGS has been reported in studies conducted among local health workers in Zanzibar and Ghana [36, 37]. These misconceptions could be linked to confusion, as reported in Ghana, Tanzania and Zanzibar, where the respondents could not clearly distinguish the transmission modes from those of other water-borne diseases and sexually transmitted infections (STI) [31, 32, 37]. Moreover, only half of the health professionals linked FGS with an increased risk of infection with HIV and HPV. These results point to the need for updating the knowledge of health professionals regarding FGS. In this context, the dissemination of WHO FGS training guides and atlas for primary healthcare workers to manage FGS in limited-resource settings in endemic regions is recommended. Other misconceptions included one in four health professionals and one in three of the community women who mentioned drinking untreated water and eating unwashed fruits and vegetables as transmission modes for FGS. Also, only a third of the community women linked transmission of FGS with swimming in the rivers, ponds, and streams. This was similar to what was found in the local community of Mwea in Kenya (33%) [22], but much lower than the proportion reported in the communities living around Lake Albert, Uganda (81%) [27].
The negative attitude that open defecation/urination is not unhygienic (41%) might be attributed to not owning a latrine as only 49% have a latrine in their household (see below). An alternative hypothesis is that open defecation and urination have been normalised as it has been going on for a long time [38]. Furthermore, some of the women do not consider FGS a serious disease; thus, knowing whether they have FGS or taking medication was not so important to them. This is an important local risk factor contributing to disease persistence in the region. Many women (72%), especially the younger ones, do not consider avoiding contact with contaminated water sources important. This sentiment is possibly linked to the fact that the Kifua II community depends directly on the water bodies for their livelihood and water needs. Also, other studies have shown that younger women and girls are the ones who tend to conduct most household chores, such as collecting water, and washing utensils or clothes, which inevitably makes it difficult to avoid water contact [27, 39]. On the other hand, talking about FGS-like symptoms is considered a taboo, as women do not speak freely. Thirty-eight percent of the women would not share their experiences and symptoms with their husbands, and 64% not even with their loved ones. This is also related to the belief that they would be left by their husbands or that their husbands would find a second wife if they failed to bear children (31.8%). Moreover, the cultural burden that tags a woman’s value on how many children she bears worsens this [40].
Although healthcare professionals in this study recognise that FGS is a serious disease and that diagnosis of FGS is their responsibility, user-friendly diagnostic technologies are limited (only 57.4% of the healthcare workers had a microscope in their facility) and this is worsened by the few skilled personnel. This is in line with the survey by Linsuke et al. [35] who reported that only 42% of the hospitals in Kongo Central perform urine sedimentation to diagnose S. haematobium, while none of the hospitals performs urine filtration. Therefore, most low-resource health facilities in DRC depend on syndromic approaches for diagnosis [35, 41]. A cross-sectional study conducted in a nearby Health Zone (Kisantu) reported the presence of urinary schistosomiasis among pregnant women (17.4%), ranging from asymptomatic to low symptomology [41]. Furthermore, their findings confirmed coinfections of urinary schistosomiasis and STIs (Chlamydia trachomatis, Neisseria gonorrhoeae and Trichomonas vaginalis) [41]. Therefore, relying on syndromic management alone cannot suffice, as medication for the different conditions differs despite the shared symptoms. For instance, FGS is treated by anthelminthic drugs, while STIs are treated by antibacterial or antiviral drugs. Moreover, the lack of equipment leads to underdiagnosis [9, 37]. Apart from microscopes, clinicians need specialised equipment like colposcopy, and specialised training to gain competence in FGS diagnosis.
While the village has few boreholes, obtaining water from them is not free of charge and this is costly for households with low income (more than half earn < USD 50 monthly). Consequently, a significant number of women (77.6%) undertake risky water practices daily, despite being aware of the risk of infection. Some households only purchase water for cooking and drinking, while the rivers and streams provide water for other domestic activities such as washing clothes and dishes (38.3%), bathing (31.3%) and cassava retting (43.3%). In 2010, Onyeneho [42] made similar observations in Nigeria, where community members opted for water from contaminated sources because they were nearby and the boreholes were quite distant. The lack of latrines in a third of the respondent households could explain the rampant open defecation /urination. In the last health survey report released for 2013–2014, more than 20% of rural households in DRC did not have access to any sanitation facility [43]. In our study area (Kifua II), 31.3% of the households did not have a toilet/latrine, and 70.6% of the respondents urinated/defecated outside the toilet. This huge sanitation problem contributes greatly to disease transmission. In addition, working in agricultural fields for many hours without latrines contributes to this. These fields are usually also located close to the water bodies (observed during the fieldwork), and thus the excreta are washed down into the water bodies when it rains. Their negative attitude that it is not unhygienic to defecate and/or urinate outside the toilet is also likely to contribute to this behaviour. Anyolitho and colleagues [27] reported that people in Ugandan communities surrounding Lake Albert believe that not defecating in the lake compromises their fish yield. In a study conducted among female heads of households in Mushandike Resettlement Irrigation Scheme, Zimbabwe, they reported 100% use of the constructed field toilets whilst working in the fields [44]. The toilets were built in a layout scheme that ensured people were always nearer to them than to a bush, hence promoting their usage. There is a need to consider building field latrines in Kifua II so that people working in the fields are always closer to the latrines [45]. Moreover, providing a piped water supply at a central point at a reduced cost or adding the number of boreholes and washing slabs could also be considered to reduce the use of natural water bodies. Increasing the use of toilets and boreholes could considerably reduce schistosomiasis (hence, FGS) in the communities.
Studies have reported cases where women and girls experiencing FGS-like signs and symptoms face stigmatisation, thereby negatively impacting their health-seeking behaviour [28, 32, 46]. However, stigma is generally low in Kifua II, probably because the community has a considerably high knowledge of schistosomiasis. It should be noted that this village has participated in many schistosomiasis-related studies before the start of this survey as mentioned above. This is probably the reason why our findings differ from other FGS KAP surveys conducted in several parts of Africa, reporting that infected and affected women or girls suffer both socially and mentally [27, 37]. In some communities, young girls and women were labelled as "prostitutes" for presenting with FGS or STIs symptoms [32, 37]. These stereotypes may hinder them from seeking medical attention for fear of being regarded as promiscuous. Additionally, Anyolitho et al. [26] reported that people who suffer from chronic effects of schistosomiasis such as swollen bellies and emaciation suffer from high stigma. However, to thoroughly evaluate self and external stigma among community women and girls in Kifua II, further surveys that include in-depth qualitative interviews and multiple focus group discussions need to be carried out. This is because a KAP survey by interviews only, records individual opinions based on the statement given. There might be considerable gaps in what is said and what is done [47], especially around sensitive cultural issues normally not spoken in public.
It is encouraging that the acceptability of the treatment is high in Kifua II, and most of the women (95%) mentioned they would accept a schistosomiasis vaccine if made available. Similar reports of high treatment acceptability were obtained in a survey in Mozambique [48], while this is not the case in the north-east and south-west of Uganda, where there is a persistent fear of taking treatment because of conspiracy theories and rumours behind the ‘real’ objective of the MDA campaigns and subjective side effects of the drugs [26, 48, 49]. In Morogoro, Tanzania, MDA for schistosomiasis were rejected through community riots, due to the failure of communication between the campaign programs’ leaders and the local people [49]. Rumours spread that these campaigns were part of the government’s covert birth control campaigns, while others claimed that the pills’ side effects were fatal [49, 50].
The study results may inform general schistosomiasis control strategies, as well as those focused on female reproductive health. The schistosomiasis control strategy in the DRC primarily relies on mass treatment of school-aged children. Our findings suggest that this approach should be complemented with health education and WASH that explicitly mention FGS as a clinical form of urinary schistosomiasis. It is also important to emphasize the need to seek medical advice if symptoms are detected. However, also adult women and health professionals should be targeted in awareness campaigns, since this study highlighted some important misconceptions about FGS transmission, while 34.8% of community women think FGS is not a serious disease. Our study also pointed to challenges in implementing the WASH recommendations daily, highlighting the need to strengthen WASH activities at the village level and to adapt these to the local context. For example, there is a need to find a sustainable approach to financing the maintenance of wells and the treatment of borehole water. Also, wells should be drilled in locations that promote equitable geographic access among different neighbourhoods within the village.
The demographic profile of health professionals, with approximately two-thirds between the ages of 29 and 45, 85.2% male, and the majority practicing for less than 20 years, may have some potential implications for the management of FGS, especially given that 35.3% of women reported feeling uncomfortable during gynaecological examinations. Although not explicitly tested in our study, it is known that women prefer to see a female health professional for gynaecological problems. Therefore, in addition to preventive activities (WASH and health education), fighting against FGS calls for better training and empowerment of healthcare professionals and the availability of more comfortable gynaecological consultations that take into account the gender balance within healthcare teams.
Although epidemiological data on FGS are lacking in the DRC, our study suggests that women are experiencing the symptoms of this disease. The innovation of our study is that it identifies the lack of knowledge and misperceptions about the disease, as well as the women’s fear of losing social support from their immediate family should they suffer from it. Moreover, it highlights the lack of specialized equipment and expertise for FGS diagnosis, with healthcare professionals specifically asking for training in FGS diagnosis and treatment. However, this study has some limitations that we acknowledge. Firstly, it was conducted in a setting where previous epidemiological studies on intestinal schistosomiasis have taken place, which may have contributed to raising awareness of schistosomiasis in general. Second, the quantitative method we used could not enable us to understand the factors underlying insufficient knowledge, negative attitudes and risky practices. Further qualitative studies could complement the results presented here. Finally, it should be noted that the Cramer’s coefficients calculated in this study only measure the strength of association, not causation.
Conclusion
Community women and the health professionals of the Kimpese region are well aware of schistosomiasis, but FGS-specific knowledge is low and misconceptions about disease transmission are evident. Besides, most women still undertake risky water contact practices and do not use latrines, thus predisposing themselves and the community to FGS. Health professionals also lack the necessary equipment for the diagnosis of FGS and need specialised knowledge in the diagnosis and management of FGS cases. Extensive qualitative research is needed to better understand factors underlying the variability of KAP among community women, and why the community engages in risky behaviour and fail to adhere to preventive measures despite being aware. This will help to optimise or adapt the WASH interventions and health communication. Clear and concise information about FGS, its symptoms and the importance of seeking medical attention if symptoms occur should be included in the health education program. WASH strategies should be tailored to the local context by ensuring the sustainability of the intervention and equitable access to potable water. Managing FGS patients should also consider the need for gender-balanced care teams. It is also crucial for healthcare professionals to acquire the right competencies regarding FGS as they are at the front line to offer primary health care and counselling on FGS to the communities. We concur with other researchers in recommending the integration of FGS with other routine women’s reproductive health services as part of long-term control and preventive measures.
Supporting information
Text A: FGS KAP Survey questionnaire for the community women in Kifua II. Text B: FGS KAP Survey questionnaire for the healthcare professionals in Kimpese Health Zone. Text C: Summary of the sociodemographic characteristics of community women and healthcare professionals. Text D: Summary of the healthcare professionals’ perception, practices, and management of female genital schistosomiasis in Kimpese Health Zone. Text E: Summary of FGS-like signs and symptoms experienced by the community women at Kifua II.
(DOCX)
Acknowledgments
We would like to thank the Kifua II community, the Kimpese healthcare professionals, the 8 field researchers (Edith Matota, Merveil Mafwana, Marceline Luntadila, Nana Nzuzi, Falone Nsimba, Gisele Nzuzi, Esther Miezi, and Benoir Nsimba) who aided in data collection, Germain Kapour, Théo Emboni and Chantal Mokoko for their support in the field. We also thank Dr. David De Coninck for his insights on data analysis. Gratitude goes to Stephen Ndung’u who assisted and guided the entry of the questionnaires into the KoboCollect toolbox and Pierre Sacré who assisted in translating the questionnaires from English to French and back to English.
Data Availability
All relevant data are within the manuscript and its Supporting Information files.
Funding Statement
This research is financed by the ATRAP project of the Belgian Development Cooperation program of the Royal Museum for Central Africa with support of the Directorate-General Development Cooperation and Humanitarian Aid. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
References
- 1.Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet. 2006;368: 1106–1118. doi: 10.1016/S0140-6736(06)69440-3 [DOI] [PubMed] [Google Scholar]
- 2.WHO. Ending the neglect to attain the Sustainable Development Goals. WHO (World Heal Organ. 2021; 2. Available: https://apps.who.int/iris/handle/10665/70809 [Google Scholar]
- 3.Poggensee G, Kiwelu I, Saria M, Richter J, Krantz I, Feldmeier H. Schistosomiasis of the lower reproductive tract without egg excretion in urine. Am J Trop Med Hyg. 1998;59: 782–783. doi: 10.4269/ajtmh.1998.59.782 [DOI] [PubMed] [Google Scholar]
- 4.Lai Y-S, Biedermann P, Ekpo UF, Garba A, Mathieu E, Midzi N, et al. Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analysis | Elsevier Enhanced Reader. Lancet Infect Dis. 2015;15: 927–940. Available: https://reader.elsevier.com/reader/sd/pii/S1473309915000663?token=693CE068678B84814B2F951E4386C1A923475E344BA3600933EE8556339C143E67D854124E2B2E53C880E35C658C9400&originRegion=eu-west-1&originCreation=20220102201621 [DOI] [PubMed] [Google Scholar]
- 5.Grimes JET, Croll D, Harrison WE, Utzinger J, Freeman MC, Templeton MR. The Relationship between Water, Sanitation and Schistosomiasis: A Systematic Review and Meta-analysis. PLoS Negl Trop Dis. 2014;8. doi: 10.1371/journal.pntd.0003296 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Musuva RM, Awiti A, Omedo M, Ogutu M, Secor WE, Montgomery SP, et al. Community knowledge, attitudes and practices on Schistosomiasis in Western Kenya-The SCORE Project. Am J Trop Med Hyg. 2014;90: 646–652. doi: 10.4269/ajtmh.13-0488 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Aula OP, McManus DP, Jones MK, Gordon CA. Schistosomiasis with a focus on Africa. Trop Med Infect Dis. 2021;6: 1–40. doi: 10.3390/tropicalmed6030109 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014;383: 2253–2264. doi: 10.1016/S0140-6736(13)61949-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Christinet V, Lazdins-Helds JK, Stothard JR, Reinhard-Rupp J. Female genital schistosomiasis (FGS): From case reports to a call for concerted action against this neglected gynaecological disease. Int J Parasitol. 2016;46: 395–404. doi: 10.1016/j.ijpara.2016.02.006 [DOI] [PubMed] [Google Scholar]
- 10.Kjetland EF, Leutscher PDC, Ndhlovu PD. A review of female genital schistosomiasis. Trends Parasitol. 2012;28: 58–65. doi: 10.1016/j.pt.2011.10.008 [DOI] [PubMed] [Google Scholar]
- 11.Kjetland EF, Kurewa EN, Ndhlovu PD, Midzi N, Gwanzura L, Mason PR, et al. Female genital schistosomiasis—A differential diagnosis to sexually transmitted disease: Genital itch and vaginal discharge as indicators of genital Schistosoma haematobium morbidity in a cross-sectional study in endemic rural Zimbabwe. Trop Med Int Heal. 2008;13: 1509–1517. doi: 10.1111/j.1365-3156.2008.02161.x [DOI] [PubMed] [Google Scholar]
- 12.Kjetland EF, Poggensee G, Helling-Giese G, Richter J, Sjaastad A, Chitsulo L, et al. Female genital schistosomiasis due to Schistosoma haematobium. Clinical and parasitological findings in women in rural Malawi. Acta Trop. 1996;62: 239–255. doi: 10.1016/s0001-706x(96)00026-5 [DOI] [PubMed] [Google Scholar]
- 13.Kjetland EF, Ndhlovu PD, Mduluza T, Gomo E, Gwanzura L, Mason PR, et al. Simple clinical manifestations of genital schistosoma Haematobium infection in rural Zimbabwean women. Am J Trop Med Hyg. 2005;72: 311–319. doi: 10.4269/ajtmh.2005.72.311 [DOI] [PubMed] [Google Scholar]
- 14.Sturt AS, Webb EL, Patterson C, Phiri CR, Mweene T, Kjetland EF, et al. Cervicovaginal Immune Activation in Zambian Women With Female Genital Schistosomiasis. Front Immunol. 2021;12. doi: 10.3389/fimmu.2021.620657 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Helling-Giese G, Sjaastad A, Poggensee G, Kjetland EF, Richter J, Chitsulo L, et al. Female genital schistosomiasis (FGS): Relationship between gynecological and histopathological findings. Acta Trop. 1996;62: 257–267. doi: 10.1016/s0001-706x(96)00027-7 [DOI] [PubMed] [Google Scholar]
- 16.Jacobson J, Pantelias A, Williamson M, Kjetland EF, Krentel A, Gyapong M, et al. Addressing a silent and neglected scourge in sexual and reproductive health in Sub-Saharan Africa by development of training competencies to improve prevention, diagnosis, and treatment of female genital schistosomiasis (FGS) for health workers. Reprod Health. 2022;19: 1–14. doi: 10.1186/s12978-021-01252-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Hotez PJ. Empowering women and improving female reproductive health through control of neglected tropical diseases. PLoS Negl Trop Dis. 2009;3. doi: 10.1371/journal.pntd.0000559 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Bullington BW, Lee MH, Mlingi J, Paul N, Aristide C, Fontana E, et al. Cervicovaginal bacterial communities in reproductive-aged Tanzanian women with Schistosoma mansoni, Schistosoma haematobium, or without schistosome infection. ISME J. 2021;15: 1539–1550. doi: 10.1038/s41396-020-00868-9 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA. Examining the relationship between urogenital schistosomiasis and hiv infection. PLoS Negl Trop Dis. 2011;5. doi: 10.1371/journal.pntd.0001396 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Amazigo U V., Leak SGA, Zoure HGM, Njepuome N, Lusamba-Dikassa PS. Community-driven interventions can revolutionise control of neglected tropical diseases. Trends in Parasitology. Elsevier Ltd; 2012. pp. 231–238. doi: 10.1016/j.pt.2012.03.002 [DOI] [PubMed] [Google Scholar]
- 21.Hotez PJ, Kamath A. Female genital schistosomiasis–a differential diagnosis to sexually transmitted disease: genital itch and vaginal discharge as indicators of genital Schistosoma haematobium morbidity in a cross-sectional study in endemic rural Zimbabwe. Trop Med Int. 2008;3. doi: 10.1111/j.1365-3156.2008.02161.x [DOI] [PubMed] [Google Scholar]
- 22.Okonjo E. Evaluation of the Knowledge and Activities of a Local Community in Mwea Endemic with Schistosomiasis Evaluation of the Knowledge and Activities of a Local Community in Mwea Endemic with Schistosomiasis. 2017;7: 95–104. [Google Scholar]
- 23.Atila DW, Luamba J, Nsembo L, Claude J, Tshijik K, Mutambel D. Identification des basommatophores hotes intermediaires des schistosomes humains a Kimpese en Republique Democratique du Congo [Identification of basommatophores intermediate hosts of human schistosomes in Kimpese in the Democratic Republic of Congo]. 2021;33: 158–168. [Google Scholar]
- 24.Mbuyi-Kalonji L, Barbé B, Nkoji G, Madinga J, Roucher C, Linsuke S, et al. Non-typhoidal Salmonella intestinal carriage in a Schistosoma mansoni endemic community in a rural area of the Democratic Republic of Congo. PLoS Negl Trop Dis. 2020;14: e0007875. doi: 10.1371/journal.pntd.0007875 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Madinga J, Linsuke S, Mpabanzi L, Meurs L, Kanobana K, Speybroeck N, et al. Schistosomiasis in the Democratic Republic of Congo: A literature review. Parasites and Vectors. 2015;8: 1–10. doi: 10.1186/s13071-015-1206-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Anyolitho MK, Poels K, Huyse T, Tumusiime J, Mugabi F, Tolo CU, et al. Knowledge, attitudes, and practices regarding schistosomiasis infection and prevention: A mixed-methods study among endemic communities of western Uganda. PLoS Negl Trop Dis. 2022;16: 1–21. doi: 10.1371/journal.pntd.0010190 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Masong MC, Wepnje GB, Marlene NT, Gamba V, Mengue M-T, Kouokam E, et al. Female Genital Schistosomiasis (FGS) in Cameroon: A formative epidemiological and socioeconomic investigation in eleven rural fishing communities. PLOS Glob Public Heal. 2021;1: e0000007. doi: 10.1371/journal.pgph.0000007 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.KoboToolbox. KoBoToolbox | Data Collection Tools for Challenging Environments. Available: https://www.kobotoolbox.org/
- 29.Mutsaka-Makuvaza MJ, Matsena-Zingoni Z, Tshuma C, Katsidzira A, Webster B, Zhou XN, et al. Knowledge, perceptions and practices regarding schistosomiasis among women living in a highly endemic rural district in Zimbabwe: Implications on infections among preschool-aged children. Parasites and Vectors. 2019;12: 1–15. doi: 10.1186/S13071-019-3668-4/TABLES/8 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.George D, Mallery P. IBM SPSS Statistics 26 Step by Step : A Simple Guide and Reference. IBM SPSS Stat 26 Step by Step. 2019. [cited 3 Nov 2022]. doi: 10.4324/9780429056765 [DOI] [Google Scholar]
- 31.Yirenya-Tawiah DR, Ackumey MM, Bosompem KM. Knowledge and awareness of genital involvement and reproductive health consequences of urogenital schistosomiasis in endemic communities in Ghana: a cross-sectional study. Reprod Health. 2016;13: 117. doi: 10.1186/s12978-016-0238-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Mazigo HD, Samson A, Lambert VJ, Kosia AL, Ngoma DD, Murphy R, et al. “We know about schistosomiasis but we know nothing about FGS”: A qualitative assessment of knowledge gaps about female genital schistosomiasis among communities living in Schistosoma haematobium endemic districts of Zanzibar and Northwestern Tanzania. PLoS Negl Trop Dis. 2021;15: e0009789. doi: 10.1371/journal.pntd.0009789 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Kukula VA, MacPherson EE, Tsey IH, Stothard JR, Theobald S, Gyapong M. A major hurdle in the elimination of urogenital schistosomiasis revealed: Identifying key gaps in knowledge and understanding of female genital schistosomiasis within communities and local health workers. Hsieh MH, editor. PLoS Negl Trop Dis. 2019;13: e0007207. doi: 10.1371/journal.pntd.0007207 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Lengeler C, Makwala J, Ngimbi D, Utzinger J. Simple school questionnaires can map both Schistosoma mansoni and Schistosoma haematobium in the Democratic Republic of Congo. Acta Trop. 2000;74: 77–87. doi: 10.1016/s0001-706x(99)00046-7 [DOI] [PubMed] [Google Scholar]
- 35.Linsuke S, Mpabanzi L, Nundu S, Mukunda F, Lutumba P, Polman K. The road towards sustainable control of schistosomiasis in the Democratic Republic of Congo: Pre-assessment of staff performance and material resources in endemic regions. Asian Pac J Trop Biomed. 2017;7: 275–279. doi: 10.1016/j.apjtb.2017.01.026 [DOI] [Google Scholar]
- 36.Mazigo HD, Samson A, Lambert VJ, Kosia AL, Ngoma DD, Murphy R, et al. Healthcare Workers’ Low Knowledge of Female Genital Schistosomiasis and Proposed Interventions to Prevent, Control, and Manage the Disease in Zanzibar. Int J Public Health. 2022;67. doi: 10.3389/ijph.2022.1604767 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Kukula VA, MacPherson EE, Tsey IH, Stothard JR, Theobald S, Gyapong M. A major hurdle in the elimination of urogenital schistosomiasis revealed: Identifying key gaps in knowledge and understanding of female genital schistosomiasis within communities and local health workers. PLoS Negl Trop Dis. 2019;13: e0007207. doi: 10.1371/journal.pntd.0007207 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.UNICEF. Putting an end to open defecation in the DRC | UNICEF. Available: https://www.unicef.org/drcongo/en/stories/putting-end-open-defecation-drc
- 39.Sanya RE, Tumwesige E, Elliott AM, Seeley J. Perceptions about interventions to control schistosomiasis among the Lake Victoria island communities of Koome, Uganda. PLoS Negl Trop Dis. 2017;11: e0005982. doi: 10.1371/journal.pntd.0005982 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Cosslett RL. Women are still being blamed for society’s problems with fertility. 2021. [cited 27 Jun 2023]. Available: https://www.theguardian.com/commentisfree/2021/oct/13/women-society-fertility-seminars-barriers-parenthood [Google Scholar]
- 41.Gadoth A, Mvumbi G, Hoff NA, Musene K, Mukadi P, Ashbaugh HR, et al. Urogenital schistosomiasis and sexually transmitted coinfections among pregnant women in a schistosome-endemic region of the Democratic Republic of Congo. Am J Trop Med Hyg. 2019;101: 828–836. doi: 10.4269/ajtmh.19-0024 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Onyeneho NG, Yinkore P, Egwuage J, Emukah E. Perceptions, attitudes and practices on schistosomiasis in delta state, Nigeria. Tanzan J Health Res. 2010;12. doi: 10.4314/thrb.v12i4.60123 [DOI] [PubMed] [Google Scholar]
- 43.MPSMRM MSP, ICF. Democratic Republic of Congo Demographic and Health Survey 2013–14: Key Findings. Demogr Heal Surv. 2014; 21. [Google Scholar]
- 44.Chimbari M, Ndlela B, Nyati Z, Thomson A, Chandiwana SK, Bolton P. Bilharzia in a small irrigation community: an assessment of water and toilet usage. Cent Afr J Med. 1992;38: 451–458. [PubMed] [Google Scholar]
- 45.Chimbari MJ. Enhancing schistosomiasis control strategy for Zimbabwe: Building on past experiences. Journal of Parasitology Research. 2012. doi: 10.1155/2012/353768 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Sturt AS, Webb EL, Francis SC, Hayes RJ, Bustinduy AL. Beyond the barrier: Female Genital Schistosomiasis as a potential risk factor for HIV-1 acquisition. Acta Trop. 2020;209: 105524. doi: 10.1016/j.actatropica.2020.105524 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 47.Leung F-H, Ratnapalan M, Med S, Bs MB, Frcpc M. Spotlight on focus groups. Can Fam Physician • Le Médecin Fam Can. 2009. Available: http://mc.manuscriptcentral.com/ [PMC free article] [PubMed] [Google Scholar]
- 48.Rassi C, Kajungu D, Martin S, Arroz J, Tallant J, Zegers de Beyl C, et al. Have You Heard of Schistosomiasis? Knowledge, Attitudes and Practices in Nampula Province, Mozambique. PLoS Negl Trop Dis. 2016;10: 1–19. doi: 10.1371/journal.pntd.0004504 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Hastings J., Rumours riots and the rejection of mass drug administration for the treatment of schistosomiasis in Morogoro, Tanzania. J Biosoc Sci. 2016;48: S16–S39. doi: 10.1017/S0021932016000018 [DOI] [PubMed] [Google Scholar]
- 50.Allen T. A new approach to eradicating ‘ neglected ‘ tropical diseases LSE Professor Tim Allen established that social factors crucially influence drug take-up in mass disease eradication programmes. 2015. [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Text A: FGS KAP Survey questionnaire for the community women in Kifua II. Text B: FGS KAP Survey questionnaire for the healthcare professionals in Kimpese Health Zone. Text C: Summary of the sociodemographic characteristics of community women and healthcare professionals. Text D: Summary of the healthcare professionals’ perception, practices, and management of female genital schistosomiasis in Kimpese Health Zone. Text E: Summary of FGS-like signs and symptoms experienced by the community women at Kifua II.
(DOCX)
Data Availability Statement
All relevant data are within the manuscript and its Supporting Information files.