Knowledge, perceptions and practices regarding schistosomiasis among women living in a highly endemic rural district in Zimbabwe: implications on infections among preschool-aged children

Background Schistosomiasis primarily affects poor and neglected communities due to their lack of safe water and sanitation facilities. In an effort to improve intervention strategies, the present study investigated the association of socio-demographic characteristics of women with their existing knowledge, perceptions and practices (KPP) in five urogenital schistosomiasis endemic rural communities in Zimbabwe. Methods In February 2016, a cross sectional study was conducted in which 426 women in rural Madziwa area, Shamva District were interviewed using a pretested structured questionnaire seeking their KPP and socio-demographic characteristics. Logistic regression analysis was performed to identify socio-demographic factors associated with the KPP variables. Results Among the 426 participants, 93.7% knew about schistosomiasis, while 97.7 and 87.5% understood the disease transmission and methods for prevention, respectively. A significantly higher percentage of women aged ≥ 30 years compared to those < 30 years indicated that infertility is a complication of untreated chronic schistosomiasis (OR: 1.7, 95% CI: 0.9–3.0). Compared to women who had no history of infection, those who had been infected before were more likely to think that they were currently infected (OR: 3.7, 95% CI: 2.4–6.0). Bathing in unsafe water sources was more common in non-apostolic compared to apostolic followers (OR: 2.1, 95% CI: 1.2–3.7). Sole use of unsafe water for domestic purposes was significantly higher in uneducated women compared to the educated (OR: 1.8, 95% CI: 1.0–3.1). Compared to women of the Chakondora community, those in Chihuri, Nduna and Kaziro were more likely to know that dysuria is a symptom of schistosomiasis while those in Chihuri were also likely to allow young children to perform water contact activities (OR: 2.9, 95% CI: 1.5–5.5). Conclusions Despite the high level of schistosomiasis awareness, some women had inadequate knowledge about the mode of transmission and preventive measures for schistosomiasis. Socio-demographic characteristics were associated with the KPP of women. Thus, disease control efforts should consider socio-demographic factors, which may influence the knowledge, perceptions and practices of occupants in a given setting.


Background
Schistosomiasis is a neglected tropical parasitic disease [1], particularly found among people living in communities that are generally poor with inadequate or no safe water and sanitary facilities [2,3]. Approximately 90% of global schistosomiasis cases occur in the sub-Saharan Africa [2], where 224 million people are affected [4]. In Zimbabwe, schistosomiasis occurs in 91% of all the districts with an overall mean prevalence of 22.7% [5].
Recognising the public health impact of schistosomiasis [6][7][8][9], the 54th World Health Assembly (WHA) encouraged all endemic states to scale up mass drug administration (MDA) earmarking school-aged children (SAC) as the prime target group [10]. The recent 65th WHA schistosomiasis elimination resolution has resulted in a shift of focus from MDA, not only in SAC but also to include all high-risk groups [11]. Besides recognizing other high-risk groups such as preschool-aged children (PSAC) and women [12][13][14][15][16][17][18], a number of obstacles are limiting the scaling up of schistosomiasis control activities in a number of endemic countries. Efforts to treat all high-risk age groups are hindered by limited provision of praziquantel and lack of an appropriate paediatric formulation for young children [19]. Other challenges include lack of political commitment and health education to improve the understanding of the public health importance of schistosomiasis in addition to improving awareness of disease control and elimination interventions [9]. A compelling rationale for health education in any setting takes into account knowledge, perceptions and practices (KPP) of the target population. Lack of knowledge and wrong perceptions may result in people unknowingly contaminating water bodies or using unprotected water sources [20]. Despite the fact that women also perform most of the water contact activities within the family, putting them at high risk of infection, previous studies in Zimbabwe seeking knowledge and water contact behaviour have focused on SAC who are considered to be the most high risk group for infection [21,22]. Furthermore, as caregivers of PSAC, women play a major role in influencing the water contact exposure and activities of young children [12,[23][24][25][26][27][28]. We recently reported the relationship between KPP of women caregivers and schistosomiasis infection in PSAC [29]. However, some studies have shown that the KPP of individuals regarding schistosomiasis are influenced by socio-demographic characteristics such as age, sex, occupation, level of education and religion [30][31][32][33]. In addition, low socioeconomic status results in the lack of access to safe water and improved sanitation coupled with poor hygiene practices. These localised factors lead to small-scale spatial heterogeneity of schistosomiasis. In Zimbabwe, there is a dearth of information on the association of KPP and socio-demographic characteristics of women in endemic communities. Such data are important for identifying, designing, and implementing effective community-based control interventions. Within this context, this study evaluated the schistosomiasis KPP of women and their association with the women's socio-demographic factors in an endemic rural area in Shamva District, Zimbabwe. It is hoped that the findings from this investigation will provide preliminary insights into female related KPP and socio-demographic characteristics in Zimbabwe.

Study area
The study was conducted in the rural area of Madziwa, Shamva District, Mashonaland Central Province, Zimbabwe. Shamva District was selected based on its recorded high prevalence of schistosomiasis in SAC (62%) [5]. The area has been previously described [34] and is located approximately 55 km from Bindura, the nearest town with a provincial hospital. One big river (Mupfure) and three small rivers (Nyamaruru, Nyarukunda and Kamoyo) and a stream (Zvisokwe) drain the area serving as water sources for most household and farming activities. A significant number of families depend on vegetable and tobacco farming as a source of income.

Study design and population
The study was cross-sectional in design and was conducted within a major study investigating host-schistosome interactions: Disease burden in children aged five years and below, mothers and compliance during a one year schistosomiasis control programme in a district described as highly endemic in Zimbabwe. The questionnaire was administered to women who had brought their children to the urine collection point, and included in the study as described by Mutsaka-Makuvaza et al. [29].

Sample size
In estimating the sample size of the study population, the previously reported prevalence of 62% in Shamva District was used [5]. Also considered was the assumption that the prevalence of schistosomiasis in school-aged children (SAC) is a proxy of the surrounding population age groups [8]. The required sample size of 363 women was calculated using Dobson's formula as follows: where Z is the Z-value for the 95% confidence interval, that is alpha = 5% (z = 1.96), p is the proportion/ prevalence of the outcome to be investigated (p = 0.62), q = 1 − p = 0.38, d is the precision for the given confidence interval expected expressed as a decimal (d = 0.05) and n = 363.
Due to the overwhelming response from the women, 426 participated in the questionnaire survey.

Interview using questionnaire
The questionnaire was developed and administered as described by Mutsaka-Makuvaza et al. [29]. The validated Shona survey questionnaire sourcing for socio-demographic characteristics, and KPP related to schistosomiasis infection was used to collect data from all women attending the survey. Variables such as age of the participant, religion, employment status, education status, perceptions regarding high risk groups, sanitary practices and water contact behaviour were captured. Additional information on the knowledge of current and past occurrences, transmission of urogenital schistosomiasis, symptoms, and prevention methods of infection were captured from the women as previously described [29].

Data analysis
The collected data were double entered into excel and analysed using STATA v.15.2 (Stata Corp, College Station, TX, USA). The data were summarised using descriptive statistics, including percentages and frequency values. We also performed logistic regression analysis to identify socio-demographic characteristics associated with the KPP variables among the participants. Association between KPP variables and all communities was assessed using the Chi-square test. Odds ratios (OR) and 95% confidence intervals (95% CI) were generated for all variables. Univariate and multivariate logistic regression analysis were performed with bathing in unsafe water as the dependent variable while women's community of residence, age, education status, employment status, religion and history of infection as the independent variables. For the inclusion of variables in the multivariate logistic regression, we set a liberal P-value at 0.1. Statistical significance was set at 5% in all analyses.

Socio-demographic characteristics of the study participants
All 426 women were interviewed. The age profiles for the respondents are described in Table 1. There were more educated women (58.2%) than uneducated ones (41.8%). African apostolic sect followers (85.2%) dominated in the area (Table 1). While the overall number of women who used toilets was 362 (85.0%), 343 had toilets at home but 4 (1.2%) of them did not use the toilets. Amongst the 362 women who used toilets, 23 (6.4%), participants used their neighbours' toilets. Of the 61 women who had S. haematobium infections, 11 (18.0%) had no toilet.  29.8% thought that they were currently infected. Of the 97.7% respondents who knew at least one method of schistosomiasis transmission, 92.7% knew that schistosomiasis transmission occurs through contact with contaminated water. Among the 399 participants who knew about schistosomiasis, 92.0% knew at least one symptom of schistosomiasis infection, 73.4% indicated haematuria as a symptom of schistosomiasis, while 3.8% indicated that they did not know the symptoms for infection. The participants showed a relatively low level of knowledge of the complications associated with chronic schistosomiasis (57.1%). While 98.3% of the participants were aware of the annual national mass drug administration (MDA) programme (mass praziquantel treatment), only 25.8% thought that anti-schistosomal treatment was a prevention and control method. Of the respondents, 44.4% believed that avoiding unsafe water bodies prevents and controls schistosomiasis transmission.

Perceptions and practices of women to schistosomiasis
Results on perceptions and practices of the participants towards schistosomiasis are described in Table 3. The majority of women reported that SAC were the most at risk group (76.9%) and regarded MDA as an important programme (99.8%) that they were willing to be part of (99.0%). Amongst the respondents, 66.7% reported that they exposed their children aged 5 and below to unsafe water sources, 43.4% allowed the children to play in shallow water and 14.1% placed the children in water-filled basins at all times during other water activities, particularly laundry. Meanwhile, 162 (38.0%) of the participants indicated that they used unprotected water sources (rivers and dams) for bathing. Among the participants, 77.5% had vegetable gardens, while 93.0% and 32.4% of these used unsafe river water and allowed their PSAC to assist with watering the garden, respectively. Table 4 shows that women aged ≥ 30 were more likely to know that infertility is a complication of untreated chronic schistosomiasis (OR: 1.6, 95% CI: 1.1-2.4) and were also more likely to discuss schistosomiasis with their children at home (OR: 4.5, 95% CI: 1.7-12.2) than women aged less than 30 years. The apostolic followers were less likely to know that avoiding unprotected water bodies is a schistosomiasis prevention method compared to non-apostolic followers (OR: 0.6, 95% CI: 0.3-1.0). However, they were more likely to use safe water for bathing (OR: 2.1, 95% CI: 1.2-3.7) but less likely to have and to use a toilet at their homes compared to the nonapostolic followers (OR: 0.4, 95% CI: 0.2-0.9 and OR: 0.2, 95% CI: 0.1-0.8, respectively). Notes: The table describes the age of the women, community of origin, education level, employment status, religious beliefs, their domestic water source, presence and use of toilet a All women who went to school only up to primary level or below were considered as not educated. Participants were considered to be educated if they attained secondary level of education b All women who had some form of income generating activity were considered employed. This included the teachers, hairdressers, village health workers, youth officers, small-scale farmers, domestic workers and tailors.    Association of women's knowledge, perceptions and practices about schistosomiasis with community of residence Table 6 and Additional file 1: Table S1 show that there were significant associations of knowledge, perceptions, and practices of the women regarding schistosomiasis with their community of residence. Compared to women residing in Chakondora community, the odds of knowing that dysuria is a symptom of schistosomiasis was significantly higher in Chihuri  Table 7 describes the association of knowledge, perceptions and practices of the women regarding schistosomiasis with their history of infection. Compared to women with no history of infection, women who had schistosomiasis before were more likely to think they were currently infected (OR: 3.7, 95% CI: 2.4-6.0). Meanwhile, those who had been infected before were less likely to depend solely on unsafe water for bathing and laundry compared to those who had had no infection before. However, they were also more likely to allow their children to assist in watering the garden compared to those who had no infection before (OR: 1.9, 95% CI: 1.2-3.0). Table 8 describes the univariate and multivariate logistic regression analysis for the location of bathing of women in relation to their socio-demographic characteristics. Univariate analysis showed that bathing in unsafe water sources was associated with the community of residence, history of infection and religion of the participant. Multivariate analysis revealed that the odds of bathing in unsafe water sources were higher in Chihuri (AOR: 0.5, 95% CI: 03-1.0), while those who had a history of infection were less likely to bath in unsafe water sources (AOR: 0.6, 95% CI: 0.4-1.0).

Discussion
To our knowledge, this study is the first attempt to demonstrate the association of women's knowledge, perceptions and practices with their socio-demographic factors in relation to schistosomiasis awareness and transmission, in an endemic rural setting in Zimbabwe. The results show that the majority of the women were educated, but unemployed, knew about schistosomiasis and a significant number of them undertook their water contact activities in unsafe water sources.  The present study was implemented in an endemic area where previous schistosomiasis control programmes where conducted [16,17] and annual MDA targeted at SAC is also ongoing. This may explain why 93.7% of the participants were aware of the disease. Almost half of the participants declared a history of infection, substantiating the endemicity of the disease in the area.
The high level of schistosomiasis awareness among women in this study is corroborated by findings from a previous study conducted in Malawi [35] in the same age group. In contrast, another study in the same country [28] reported poor knowledge of the disease among women. This calls for more studies in women from different settings to improve the benefits of targeted schistosomiasis control interventions, particularly education and increased awareness. The present study revealed inadequate knowledge on dysuria as a symptom of urogenital schistosomiasis infection and the complications of chronic untreated schistosomiasis infection among the women. This is despite the fact that previous studies carried out in the same area focused on female genital schistosomiasis (FGS) and its complications [36][37][38]. Moreover, the present study was implemented in an endemic area currently undergoing MDA in SAC, which most of the respondents indicated as important and their willingness to participate if the programme was to be extended to the whole community. As such, it would be expected that most of the female community would have knowledge of the signs and symptoms of the disease. However, a considerable number of women showed confusion surrounding schistosomiasis transmission with some stating that the disease is transmitted by a combination of contact with contaminated water and also drinking dirty water. Mazigo et al. [39] also observed the same findings but from SAC. Such Table 6 Association of knowledge, perceptions and practices of women regarding schistosomiasis with their community of residence Note: Chakondora community was considered as the reference group a Multiple responses were considered b Those who rely solely on unsafe water for the indicated water contact activities * Significant association of P < 0.05; ** Borderline significance P = 0.05 Abbreviations: OR, odds ratio; 95% CI, 95% confidence interval; PSAC, preschool-aged children; WASH, water, sanitation and hygiene What are the signs and symptoms of bilharzia infection? a incorrect beliefs are due to lack of health education regarding schistosomiasis, whose provision could precede routine national MDA campaigns. However, the current MDA embedded health education campaigns carried out by the community nurses and village health workers only encourage parents to allow children to be treated. In addition, text messages are sent to individuals and posters are distributed to community health centres by the ministry. The short text messages informing the public on the dates of the MDA and indicating that treatment prevents the spread of schistosomiasis do not elaborate on the transmission, symptoms, prevention and control methods of the disease. The study shows that there is poor knowledge about treatment for schistosomiasis and also health education as a schistosomiasis prevention and control measure. Knowledge of diseases without proper understanding of its mode of transmission, signs and symptoms, complications, prevention, and control methods is not only insufficient [20] but also less useful in control and elimination of the disease. On the other hand, while the literacy rate and the number of people with mobile phones in the area has not been established, the sending of mobile phone messages hinders the dissemination of information to those who are illiterate or individuals who do not have mobile phones. Effectiveness of the dissemination of information via posters is also dependent on the literacy of the targeted population. Some studies have already shown that the use of posters in dissemination of information is not effective [39,40]. Thus, there is a need to plan comprehensive health education strategies if the 2025 schistosomiasis elimination goal is to be achieved by endemic member states [11].
Although almost half of the women included in this study had a history of schistosomiasis infection, they were more likely to use unsafe water sources, probably due to lack of adequate safe water or had lack of knowledge regarding the transmission of the disease and its prevention and control methods. Although there are available boreholes providing safe water, they are few and widely scattered such that some of the residents have to travel long distances to access them. Therefore, most residents have no choice but to use any source of water available in their vicinity regardless of their knowledge of the risks associated. Thus, schistosomiasis control efforts should include health education and provision of adequate accessible safe water sources.
Overall, the study participants perceived that the most at risk group are SAC followed by PSAC. This observation is corroborated by studies conducted elsewhere [41]. Among the few participants who perceived women to be a high-risk group were caregivers of infected PSAC [29]. Their perception may have resulted in them not expecting their PSAC to be at risk of infection when they are playing at water contact sites, thus predisposing PSAC to schistosomiasis infection. This substantiates the need of comprehensive health education for different risk groups for infection.
Educated women had a significantly higher knowledge that haematuria is a symptom of schistosomiasis. They were also more likely to rely solely on safe water for domestic purposes compared to uneducated respondents. This strongly indicates that education is important for the community to acquire knowledge of the disease and change their behaviour to reduce the risk of acquiring infection [42,43].
Some of the women in the ≥ 30 years age group confirmed that they were part of the previous FGS studies [17,18], indicating that they later fell pregnant after successful treatment that resolved granulomatous lesions associated with FGS, which they thought were a cause of infertility. Their involvement in the previous studies might have resulted in them having a significantly higher knowledge of the complications of chronic schistosomiasis, compared to those < 30 years of age. The presence and use of toilets was significantly lower in African apostolic than non-apostolic followers indicating that religion can have an impact on individual practices. Interestingly they were more likely to use safe bathing water than the non-apostolic followers. African apostolic followers are reserved, such that they shun bathing in the open area at rivers or other unprotected water bodies. Our study showed that of the 61 women who were S. haematobium-positive, 43 (70.5%) had toilets at home. This means that they are still being infected due to water contact, but they may not be contaminating water sources with excreta and thus infecting snails. Nevertheless, these results show that the provision of toilets alone is not adequate for elimination of indiscriminate disposal of excreta; health education emphasizing the importance and proper use of toilets for schistosomiasis control is of essence [44].
The use of unsafe water for water contact activities puts individuals directly at risk of being infected [21,28]. We previously reported that women who allowed their child to assist in watering their garden had a significantly higher number of infected PSAC under their care while women with schistosomiasis infections and caregivers of infected PSAC were less likely to use safe bathing water [29].
Multivariate analysis has shown that the odds of using unsafe bathing water were different among the communities. The practice of using unprotected water sources was also associated with having been infected before. This shows that unsafe water sources predispose individuals to schistosomiasis infection. However, the difference in water use among the geographically close communities contributes to small-scale spatial heterogeneity in schistosomiasis transmission [45]. Previously, we reported a significant difference in schistosomiasis infection among these communities [34].
Although the study results have given an insight into the KPP of rural women in Zimbabwe, the country has diverse cultural beliefs and socio-demographic characteristics due to the existence of different tribes. Thus, KPP regarding schistosomiasis might differ by tribe or geographical area. The endemicity of schistosomiasis also varies across the country [5]. This calls for more studies in other tribes in different geographical settings with different levels of endemicity to inform targeted schistosomiasis control strategies.