- Research article
- Open Access
- Open Peer Review
Schistosoma haematobium infection status and its associated risk factors among pregnant women in Munyenge, South West Region, Cameroon following scale-up of communal piped water sources from 2014 to 2017: a cross-sectional study
BMC Public Healthvolume 19, Article number: 392 (2019)
In 2014, a study in Munyenge revealed a high prevalence of urogenital schistosomiasis (UGS) among pregnant women. This study investigated he prevalence and risk factors of UGS in pregnancy following scale-up of piped water sources from 2014 to 2017. Secondly, we compared stream usage, stream contact behaviour, infection rate and intensity with the findings of 2014.
Consenting pregnant women reporting for antenatal care (ANC) in the different health facilities were enrolled consecutively between November 2016 and January 2018. Information on age, gravidity status, residence, marital status, educational level, occupation, household water source, frequency of contact with water and stream activities were obtained using a semi-structured questionnaire. Urine samples were examined for the presence of microhaematuria and S. haematobium ova using test strip and filtration/microscopy methods respectively. Data were analysed using univariate and multivariate regression analyses and relative risk reductions calculated.
Of the 368 women enrolled, 22.3% (82) were diagnosed with UGS. Marital status (single) (aOR = 2.24, 95% CI: 1.04–4.79), primary - level of education (aOR = 2.0; 95% CI: 1.04–3.85) and domestic activity and bathing in the stream (aOR = 3.3; 95% CI: 1.83–6.01) increased risk of S. haematobium infection. Meanwhile, fewer visits (< 3 visits/week) to stream (aOR = 0.35, 95% CI = 0.17–0.74) reduced exposure to infection. Piped water usage was associated with reduced stream usage and eliminated the risk of infection among women who used safe water only. Compared with the findings of 2014, stream usage (RRR = 23 95% CI: 19–28), frequency (≥ 3 visits) (RRR = 69 95% CI: 59–77) and intensity of contact with water (RRR = 37 95% CI = 22–49) has reduced. Similarly, we observed a decrease in infection rate (RRR = 52, 95% CI = 40–62) and prevalence of heavy egg intensity (RRR = 71, 95% CI = 53–81).
Following increased piped water sources in Munyenge, S. haematobium infection has declined due to reduced stream contact. This has important implication in the control of UGS in pregnancy.
Schistosomiasis is a chronic parasitic disease caused by blood flukes of the genus Schistosoma and transmitted by snails found in fresh water bodies that have been contaminated by Schistosoma eggs. People become infected during dermal contact with water containing schistosome cercariae. In endemic areas, where there is lack of adequate water supply, poverty, ignorance and poor hygienic practices, children, women, fishermen and farmers are the high risk groups for schistosomiasis [1,2,3,4]. Women, in particular, are more likely to be exposed to infection during activities carried out in streams such as domestic activities including washing clothes, fetching water and bathing [5, 6]. It is estimated that approximately 40 million women of childbearing age are infected with schistosomiasis, with almost 10 million infected pregnant women in Africa [1, 7]. Increasingly, findings from several studies suggest that schistosomiasis in pregnancy is an area of major public health concern [6, 8,9,10,11,12,13].
Schistosoma haematobium is prevalent in Africa and Middle East, where the infection is causing significant morbidity and mortality when compared with S. mansoni. Schistosome eggs deposited in the wall of the urogenital bladder  release highly inflammatory antigens , triggering granuloma formation, a range of urothelial abnormalities and related signs such as haematuria, dysuria and lesions of the bladder, kidney failure and bladder cancer . Several studies have reported associations between UGS and HIV [17,18,19] and increasing evidence supports that it is a plausible risk factor for HIV acquisition . In pregnancy, UGS has been associated with severe anaemia  particularly in co-infection with P. falciparum , maternal mortality [8, 21], premature birth and low birth weight [13, 22]. Drug-based control of morbidity related to infection has been the primary WHO strategy for schistosomiasis control, with treatment given mainly through community and school-based mass treatment with praziquantel . Older age groups, including pregnant women are often left untreated. Despite recent evidence of the safety of praziquantel in human pregnancy, barriers to adopting polices for such treatment still remain . Consequently, affected pregnant women can serve as reservoirs for infection bringing the distribution of the disease to pre-control level over time. More so, morbidity that builds in untreated pregnant women may result in poor pregnancy outcomes . To achieve sustainable control (elimination or eradication of schistosomiasis), improvements of water, sanitation, hygiene infrastructure and modification of risk behaviour are necessary to prevent transmission of the schistosome parasite [26,27,28]. The provision of safe water supply is one important approach to reduce the need for contact with contaminated water bodies and diminish the risk of schistosomiasis transmission .
A study carried out in 2014 in Munyenge, an endemic foci located in the mount Cameroon area, revealed that S. haematobium infection is common among pregnant women and regular contact with stream and long duration in contaminated water sources increased risk of infection. We suggested that provision of piped water and health education will decrease disease incidence and intensity . More so, a recent study by Ebai et al.  in some neighbouring villages to Munyenge showed that access to piped water protected individuals living in these communities from UGS. Thus, following scale up of piped water supply from 2014 to 2017 in Munyenge, this study investigated the prevalence and risk factors of UGS in pregnancy for an epidemiological update. Secondly, to assess the impact of increase piped water supply, we compared stream usage, stream contact behaviour and S. haematobium infection rate and intensity with the findings of 2014.
The study was carried out in Munyenge, a village located in the Bafia health area about 27 km from Muyuka town, South West Region, Cameroon. Bafia Health Area is an endemic focus for UGS, which is found in the Mount Cameroon Area. This health area is made up of three rural communities: Ikata, Bafia, and Munyenge. Munyenge has a heterogenous population of about 13,127 inhabitants (Delegation of Public Health, South West Region, 2017) with farming as the principal occupation. The characteristics of the study area has been described elsewhere [6, 31]. This community has four health centres, of which three provide antenatal care and delivery services for the local population. In Munyenge, piped water sources have increased from three to seven between 2014 and 2017 (Figs. 1 and 2). Nonetheless, access to safe water is still poor due to long distances to improved water source and water user fees that influence water use patterns and health benefits offered by improved water sources (personal observation). Consequently, the local population still makes frequent use of the streams for their daily needs.
This was a cross sectional study that involved pregnant women, who were enrolled consecutively between November 2016 and January 2018.
Pregnant women in their third trimester, who reported for antenatal care (ANC) at any of the three health centres (Government Integrated Health centre (HC), Banga Annex HC, Trans African HC) were enrolled in the study. Prior to enrolment, each participant provided an informed consent.
Population sample size determination
The minimum sample size was computed using the formula by Bryan  based on the S. haematobium infection prevalence of 46.8% in pregnancy reported from an epidemiological baseline study in Munyenge by Anchang-Kimbi et al. .
n = minimum sample size required
z = 1.96 is confidence level test statistic at the desired level of significance
p = 0.468 is the proportion of UGS in pregnancy
q = 1-p = is the proportion negative for UGS
d = the acceptable error willing to be committed
A sample size of at least 382 was determined to be adequate to detect a 5% change in the prevalence of UGS. However, due to logistics, we had a sample size of 368 pregnant women which is well above 95% of the expected sample size calculated.
Administration of questionnaire
The study participants were interviewed by a field researcher using a validated questionnaire to record socio-emographic information (age, residence), socio-economic indicators (marital status, educational level and occupation), gynaecologic/obstetric history (gravidity, gestational age) and questions related to schistosomiasis; household water source (stream or piped water), frequency of contact with water source, stream activities (domestic chores and bathing (measures of intensity of contact with water)). In addition, the questionnaire included questions related to knowledge about schistosomiasis etiology, transmission, clinical manifestation, prevention and control. Knowledge on UGS was scored on 4 points as described by Folefac et al. . Briefly, one point was allocated for a correct response and no point for a “I don’t know” or wrong answer. A knowledge score of < 2, 2–3 and > 3 was considered as poor, average and good respectively.
Sample collection and processing
About 20 ml of terminally voided urine sample was collected from consented participants into sterile, dry, leak-proof transparent, pre-labelled urine bottles. Women were instructed to collect urine between 10 am and 2 pm. Urine samples were immediately processed and analysed at the laboratory unit of the health facility. Haematuria was determined by visual observation of urine samples and urinalysis reagent strips (Mission® Expert-USA). Schistosoma. haematobium eggs were obtained and identified using the filtration technique and microscopy respectively as reported elsewhere . A pregnant woman was diagnosed with UGS when she was positive by microscopic examination of urine filtrate and/or urine reagent strip. The infection intensity was classified as light (< 50 eggs/10 ml of urine) or heavy (≥50 eggs/10 ml of urine) as defined by the World Health Organization .
Data management and statistical analysis
Questionnaires were checked for the correct use of codes and completeness. Data were coded, validated and analysed using SPSS version 22.0 (SPSS, Inc., Chicago, IL, USA). The statistical tests performed included the Pearson’s chi-square for comparison of proportions. Bivariate analysis was performed to identify the factors associated with S. haematobium infection to be included in the multivariate logistic regression for analysis of risk factors for UGS. Variables that had a p- value < 0.20 in bivariate analysis or biological plausiblility were included in the multivariate logistic regression model. In order to assess the impact of increase piped water sources on infection rate and intensity, relative risk reduction was calculated using a Microsoft Excel confidence interval calculator as described by the Newcombe-Wilson method [34, 35]. A p - value < 0.05 was considered significant.
Characteristics of the study population
A total of 368 pregnant women were enrolled into the study. The mean age of the study participants was 25 ± 5.8 years (Range: 15–42 years). The characteristics of the study participants are shown in Table 1. The majority of the women were older (> 25 years), married and had attained at least a secondary level of education. Single women were predominantly younger (≤ 25 years) (72.5%; 71/98) while, more married women were older (> 25 years) (53.3%; 144/270). The difference was statistically significant (χ2 = 24.17; P < 0.001). A greater proportion of the women were housewives. The women obtained their water from the stream and piped water sources for personal and domestic purposes. However, stream usage was predominant (76.1%). Among the 368 women, 16.2% (54) reported piped water as their only source of water, 53.3% (178) had stream as their only source of water and 30.5% (102) used both piped and stream water. No association was found between socio-demographic factors and water source type but, women who used piped water (36.4%: 102/280) were less likely (aOR = 0.34, 95% CI: 0.21–0.57, p < 0.001) to use the stream when compared with those who reported no access to piped water (63.6%; 178/280). Generally, women made fewer contact (< 3 times/week) with stream. Although not statistically significant (χ2 = 2.94; P = 0.086), those who reported stream as the only source of water made more contacts (≥ 3 times/weeks) (75%; 33/44) than those who used both sources (25%; 11/44). Among the women who reported stream as a source of water, a majority of them visited the stream for domestic purposes and one- third of the women equally reported bathing (Table 1). With regard to knowledge on UGS, a greater percentage of the women had poor perception of the disease symptoms and its association with water contact.
The prevalence and risk factors of S. haematobium infection
Eighty-two (22.3%; 95% CI: 15.8–22.0) of the 368 pregnant women enrolled were positive for UGS. Excretion of ova in urine was recorded for 72 (19.6%; 95% CI: 18.3–26.8) women among whom 23 (32%) had heavy (≥50 eggs/10 ml of urine) infection, while 49 (68%) had light (< 50 eggs/10 ml of urine) infection. The prevalence of microhaematuria was 14.7% (54/368) of which, 2.7% (10) of the women were positive for microhaematuria only. Using microscopic urine examination as gold standard, the specificity and sensitivity of microhaematuria in the diagnosis of S. haematobium infection were 96.6% (95% CI: 93.9–98.2) and 61.1% (95% CI: 49.6–71.5), respectively.
In bivariate analysis, there was an association between the prevalence of infection and marital status (P < 0.001), water source type (P < 0.001), stream activity (P < 0.001) and frequency of contact with stream (P < 0.001). All women who had piped water as the only source of water were negative for UGS (Table 2). On the other hand, no association was seen between maternal age, gravidity status, educational level, occupation and infection (Table 2). All four factors associated with UGS were retained by multiple regression model analysis (Table 2). Maternal age and educational level were included in the final model based on the biological plausibility of these factors.
Single status increased risk for infection by 2.2 times (95% CI: 1.04–4.79) when compared with the married status. Equally, women with a primary - level education were at higher risk (aOR = 2.0; 95% CI: 1.04–3.85) of having UGS than those with at least secondary-level education. Furthermore, higher odds (aOR = 3.3; 95% CI: 1.83–6.01) of having UGS were identified among women who carried out both domestic activity and bathing in the stream. On the other hand, less frequency of contact with water (< 3 times per week) (aOR = 0.35, 95% CI = 0.17–0.74) was associated with decreased risk of infection.
Changes in stream usage and contact behaviour, S. haematobium infection rate and intensity after scale-up of piped water sources between 2014 and 2017
About 42 % (42.4%; 156/368) of the study participants reported use of safe water after more communal piped water installations. In comparison with reports of 2014, changes in stream usage (stream contact) and frequency of contact with stream, stream activity, prevalence and intensity of UGS were observed (Fig. 3 and Additional file 1). Two hundred and eighty women (76.1%) reported stream water contact during the period of study (Table 1) while, in 2014, 99.2% of pregnant women used the stream as main source of water. Stream usage reduced by 23% (RRR = 0.23, 95% CI = 0.19–0.28). Equally, there was a decrease in the frequency of contact with water. Compared with 2014, frequent visits (≥ 3 visits/week) to the stream reduced by 69% (RRR = 0.69, 95% CI = 0.59–0.77) in 2017. Similarly, bathing activity (a measure of intense contact with water) in streams decreased by 37% (RRR = 0.37, 95% CI = 0.22–0.49). A decline in the prevalence and intensity of S. haematobium infection was observed among pregnant women. Infection rate decreased from 46.8% in 2014 to 22.3% in 2017 (RRR = 52, 95%, CI = 40–62%) With regards to infection intensity, cases with heavy infection decreased by 71% (RRR = 0.71, 95% CI = 0.53–0.81; P < 0.001) as well as the prevalence of light infection (RRR = 0.37, 95% CI = 0.14–0.54) (Additional file 1).
Munyenge village is an established endemic focus for UGS. [6, 30, 36]. The establishment of safe water is an essential prerequisite for schistosomiasis control in endemic areas since, the prevention of schistosmiasis is achieved by reducing contact with schistosoma-infested water . The present study is a follow-up survey which reports on the prevalence and risk factors of S. haematobium infection among pregnant women living in Munyenge, following the scale-up of communal piped water sources between 2014 and 2017. The impact of increased piped water sources was evaluated by assessing changes in stream contact patterns, prevalence and intensity of infection.
This study carried out in Munyenge, in 2017, revealed a reduced prevalence of S. haematobium infection among pregnant women by 52%. In addition, we recorded a decreased in the number of cases of heavy infection. Interestingly, our study revealed that the use of piped water eliminated the risk of infection among pregnant women who completely stopped using stream water but very little effect on those who reported partial use of safe water. Similarly, the protective role of access to piped water has been reported by Ebai et al.,  in a survey carried out in Ikata-Likoko area which, are neighbouring communities to Munyenge in the Bafia health area. Equally, studies in other endemic areas have shown that safe water supplies were associated with significantly lower odds of schistosomiasis [29, 37,38,39,40,41,42]. In Brazil, a communal water supply was shown to reduce the prevalence of the disease . In Egypt, even the partial use of safe water markedly lowered the prevalence of S. mansoni and S. haematobium . A recent study by Tanser et al.  reported a UGS prevalence of 16.8% following scale-up of piped water in rural South Africa which was markedly lower than the overall prevalence of 60–70% recorded in the same area thirty years earlier. Also, a cohort study carried out in the same area showed that children living in communities with a high coverage of piped water were eight times less likely to be infected relative to those living in areas with little or no access to piped water . Introduction of safe water supplies into a community offers protection from schistosomiasis infection either directly or indirectly. It offers direct protection to individuals with access to safe water by reducing their contact with infested water bodies through household domestic water collection activities. Secondly, the scale-up access to safe water will confer indirect protection to members of a community in a manner that is analogous to the concept of ‘herd immunity’. Herd immunity confers protection through a reduction in the number of contacts that infected individuals have with open water bodies leading to a decrease in the overall levels of intensity of infection in the surrounding community .
A water supply system that is either communal or household lowers the degree of contact with infested water in a community and people change their behaviour after safe water becomes available [38, 41, 42, 44]. With increased piped water sources in Munyenge, stream usage, frequent contact with stream and prolonged duration of water contact (bathing and domestic activities in the stream) decreased significantly by 23, 69 and 37% respectively. However, in the present study, piped water usage was associated with reduced stream usage and not changes in stream contact behaviour. The change in stream contact behaviour observed may be attributed to some level of awareness on UGS in the community which, may have influenced change in attitudes of some pregnant women from bathing and washing in water bodies to stream banks or at their homes. Despite the presence of more piped water sources, a majority of the pregnant women (76%) continue to use the streams for domestic purposes. Distance from home to the taps, limited number of communal piped water sources for a dispersed population and requirement for immediate payment of piped water may account for the reliance on the stream [41, 42, 45]. It will be interesting to assess the relationship between these factors and the distribution S. haematobium infection in the study area.
Although the burden of UGS has declined in Munyenge over the indicated three-year period, the prevalence of infection still remains high (22.3%) among pregnant women. Coupled with the high rate of stream usage, other factors predisposed these women to the risk of S. haematobium infection. Marital status influenced infection outcome where single women were twice more likely to be infected with S. haematobium than their married counterparts irrespective of their age and gravidity status. The role of marital status in the risk of malaria parasite infection in pregnancy has also been reported . Studies have shown that marriage has advantages on the health outcomes of individuals . A spouse may improve economic well-being  as well as play an important role in monitoring and encouraging healthy behaviours . Partner support may be important in limiting or preventing contact with infested water by the pregnant woman. Furthermore, infection was more common among individuals with low level of education. This is in conformity with findings of Lima E Costa et al.  and Bethony et al.  in Brazil, Khalid et al.  in Sudan and Salawu and Odiabo,  in Nigeria. Ugbomoiko et al.  suggested that education affects attitudes and behaviour. Individuals with low educational status are more likely to enter the stream barefoot and spend longer hours in water (exposing themselves to cercarial penetration) than their more educated counterparts. On the other hand, the self-awareness of the disease may account for the reduced prevalence level observed among women with at least a secondary level of education. Consistent with our previous findings in Munyenge, bathing and domestic activities in infested waters predisposed pregnant women to infection. Both activities increase intensity of water contact with infested water [6, 44, 52]. These findings strongly suggest that the extension of more piped water sources in this endemic area will reduce the incidence of infection by reducing the need for intense or frequent contact with infested water. However, a productive and sustainable intervention cannot be achieved without adequate education [52, 53]. We suggest that educating women during antenatal clinic visits on the harmful effects of UGS and the local risk factors of infection will help reduce frequency of water contact and thus infection risk in this endemic areas.
This study had a few limitations. This study examined the short-term effect of piped water supply on water contact patterns and transmission of S. haematobium infection in Munyenge. Studies have demonstrated that over long-term period, water supply facilities had little impact on the overall prevalence and intensity of infection [39, 42]. Secondly, piped water usage and stream contact behaviour were based on self- reports and not by direct observation. Analysis of spatial pattern of infection, observations of human contact at the stream and a questionnaire on water use gives a better assessment of the impact of piped supply on human water contact [39, 41, 42].
Following the scale-up of communal pipe water sources in Munyenge from 2014 to 2017, the prevalence of UGS among pregnant women has decreased significantly by 52%. Equally, a reduction in stream usage, frequency and intensity of contact with stream was observed. The use of piped water reduced stream usage by pregnant women and eliminated the risk of UGS among those who completely avoided the stream. Single status, low level of education and activities that the prolong duration in water predisposed the women to S. haematobium infection. Despite the increase safe water sources, the majority of these women still depend on the natural source of water for their daily activities. It is obvious that expansion of piped water sources is important in interrupting stream contact but this intervention is productive and sustainable, if health education activities directed towards avoiding water contacts are achieved.
Antenatal care clinic
Human Immunodeficiency Virus
Relative risk reduction
Friedman JF, Mital P, Kanzaria HK, Olds GR, Kurtis JD. Schistosomiasis and pregnancy. Trends Parasitol. 2007;23(4):159–64.
Gryseels B. Schistosomiasis. Infectious Disease Clinical of North America. 2012;26:383–97.
Stothard JR, Sousa-Figueiredo JC, Betson M, Bustinduy A, Reinhard-Rupp J. Schistosomiasis in African infants and preschool children: let them now be treated. Trends Parasitol. 2013;29:197–205.
Knopp S, Person B, Ame SM, Mohammed KA, Ali SM, Khamis IS, Rabone M, Allan F, Gouvras A, Blair L, et al. Elimination of schistosomiasis transmission in Zanzibar: baseline findings before the onset of a randomized intervention trial. PLoS Negllected Tropical Disease. 2013;7(10):e2474.
Ntonifor HN, Ajayi JA. Water contact and Schistosoma haematobium infection. A case study of some communities in Toro local government council area (TLGCA) of Bauchi state. Nigeria Journal of Natural and Applied Sciences. 2005;1(1):54–9.
Anchang-Kimbi J, Mansoh DE, Sotoing GT, Achidi EA. Coinfection with Schistosoma haematobium and Plasmodium falciparum and Anaemia severity among pregnant women in Munyenge, Mount Cameroon area: a cross-sectional study. Journal of Parasitology Research. 2017. https://doi.org/10.1155/2017/6173465.
WHO. Report of the WHO Informal Consultation on the use of praziquantel during pregnancy/Lactation and Albendazole/Mebendazole in Children under 24 months. WHO/CDS/CPE/PVC/2002.4; 2002.
Ajanga A, Lwambo NJ, Blair I, Nyandindi U, Fenwick A, Brooker S. Schistosoma mansoni in pregnancy and associatiation with anaemia in Northwest Tanzania. Transactions of Royal Soceity for Tropical Medicine and Hygiene. 2012;100(1):59–63.
Khalid A, Abdelgadir MA, Ashmaig A, Ibrahim AM, Ahmed AA, Adam I. Schistosoma mansoni infection among prenatal attendees at a secondary-care hospital in Central Sudan. Int J Gynaecol Obstet. 2012;116(1):10–2.
Salawu OT, Odaibo AB. Schistosomiasis among pregnant women in rural communities in Nigeria. Int J Gynaecol Obstet. 2013;122(1):1–4.
Basra A, Mombo-Ngoma G, Melser MC, Diop DA, Wurbel H, Mackanga JR, et al. Efficacy of mefloquine intermittent preventive treatment in pregnancy against Schistosoma haematobium infection in Gabon: a nested randomized controlled assessor-blinded clinical trial. Clinical Infectious Disease. 2013;56:68–75.
Salawu OT, Odaibo AB. Schistosomiasis transmission; socio-demographic, knowledge and practices as transmission risk factors in pregnant women. Journal of Parasitology and Disease. 2014. https://doi.org/10.1007/s12639-014-0454-2.
Mombo-Ngoma G, Honkpehedji J, Basra A, Mackanga JR, Zoleko RM, Zinsou J, Agobe JCD, Lell B, Matsiegui PB, Gonzales R, Agnandji ST, Yazdanbakhsh M, Menendez C, Kremsner PG, Adegnika AA, Ramharter M. Urogenital schistosomiasis during pregnancy is associated with low birth delivery: analysis of a prospective cohort of pregnant women and their offspring in Gabon. Int J Parasitol. 2016;47(2017):69–74.
Kohno M, Kuwatsuru R, Suzuki K, Nishii N, Hayano T, Mituhashi N, Tanabe K. Imaging findings from a case bilharziasis in a patient with gross haematuria of several years’ duration. Radiat Med. 2008;26(9):553–6.
Botelho MC, Veiga I, Oliveira PA, Lopes C, Teixeira M, Correia da Costa JM, Machado JC. Carcinogenic ability of Schistosoma haematobium possibly through oncogenic mutation of KRAS gene. Adv Cancer Res Treat. 2013:876585.
Fenwick A, Savioli L, Engels D, Bergquist NR, Todd MH. Drugs for the control of parasitic diseases: current status and development in schistosomiasis. Trends Parasitol. 2003;19:509–15.
Kjetland EF, Ndhlovu PD, Gomo E, Mduluza T, Midzi N, Gwanzura L, Mason PR, Sandvik L, Friis H, Gundersen SG. Association between genital schistosomiasis and HIV in rural Zimbabwean women. AIDS. 2006;20:593–600.
Ndhlovu PD, Mduluza T, Kjetland EF, Midzi N, Nyanga L, et al. Prevalence of urinary schistosomiasis and HIV in females living in a rural community of Zimbabwe: does age matter? Transactions of Royal Soceity of Tropical Medicine and Hygiene. 2007;101:433–8.
Downs JA, Mguta C, Kaatano GM, Mitchell KB, Bang H, Simplice H, Kalluvya SE, Changalucha JM, Johnson WD Jr, Fitzgerald DW. Urogenital schistosomiasis in women of reproductive age in Tanzania’s Lake Victoria region. Am J Trop Med Hyg. 2011;84:364–9.
Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA. Examining the Relationship between Urogenital Schistosomiasis and HIV Infection. PLoS Neglected Tropical Diseases. 2011;5(12). https://doi.org/10.1371/journal.pntd.0001396.
Helling-Giese G, Kjetland F, Gundersenetal SG. Schistosomiasis in women: manifestations in the upper reproductive tract. Acta Trop. 1996;62(4):225–38.
Siegrist D, Siegrist-Obimpeh P. Schistosoma haematobium infection in pregnancy. Acta Trop. 1992;50:317–21.
WHO. The prevention and control of schistosomiasis and soil-transmitted helminthiasis. Report of a WHO Expert committee. World Health Organisation Tech Rep Ser. 2002;912:1–57.
Friedman JF, Olveda RM, Mirochnick MH, Bustinduy AL, Elliott AM. Praziquantel for the treatment of schistosomiasis during human pregnancy. In: Bulletin of the World Health Organization; 2017. ID: BLT.17.198879.
Friedman JK, Kanzaria HK, McGarvey ST. Human schistosomiasis and anemia: the relationship and potential mechanisms. Trends Parasitol. 2005;21:386–92.
Freeman MC, Ogden S, Jacobson J, Abbott D, Addiss DG, Amnie AG, Beckwith C, Cairncross S, Callejas R, Colford JM, Emerson PM, Fenwick A, Fishman R, Gallo K, Grimes J, Karapetyan G, Keene B, Lammie PJ, Macarthur C, Lochery P, et al. Integration of water, sanitation, and hygiene for the prevention and control of neglected tropical diseases: a rationale for inter-sectoral collaboration. PLoS Negl Trop Dis. 2013;7:e2439.
WHO. Water Sanitation and Hygiene for Accelerating and Sustaining Progress on Neglected Tropical Diseases a Global Strategy 2015–2020. Geneva: World Health Organisation; 2015.
Echazu A, Bonanno D, Juarez M, Cajal SP, Heredia V, Caropresi S, Cimino RO, Caro N, Vargas PA, Paredes G, Krolewiecki AJ. Effect of poor access to water and sanitation as risk factors for soil-transmitted helminth infection: selectiveness by the infective route. PLoS Negl Trop Dis. 2015;9. https://doi.org/10.1371/journal.pntd.0004111.
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 Neglected Tropical Disease. 2014;8:e3296.
Ebai CB, Kimbi HK, Sumbele IUN, Yunga JE, Lehman LG. Prevalence and risk factors of urinary schistosomiasis in the Ikata-Likoko area of Southwest Cameroon. International Journal of TROPICAL DISEASE & Health. 2016. https://doi.org/10.9734/IJTDH/2016/26669.
Ntonifor HN, Green AE, Bopda MOS, Tabot JT. Epidemiology of urogenital schistosomiasis and soil transmitted helminthiasis in a recently established focus behind Mount Cameroon. Int J Curr Microbiol App Sci. 2015;4(3):1056–66.
Bryan FJ. The design and analysis of research studies, University of Otago, Dunedin, New Zealand. Cambridge,UK: Cambridge University Press; 1992.
Folefac LN, Nde-Fon P, Verla VS, Nkemanjong TM, Njunda AL, Luma HN. Knowledge, attitudes and practices regarding urinary schistosomiasis among adults in the Ekombe Bonji Health Area, Cameroon. Pan African Medical Journal. 2018;29:161. https://doi.org/10.11604/pamj.2018.29.161.14980.
Armitage P, Berry G. Statistical methods in medical research. 3rd ed. London: Blackwell; 1994.
Newcombe RG. Interval estimation for the difference between independent proportions: comparison of eleven methods. Stat Med. 1998;17:873–90.
Ntonifor HN, Mbunkur GN, Ndaleh NW. Epidemiological survey of urinary schistosomiasis in some primary schools in a new focus behind Mount Cameroon (Munyenge), South West Region, Cameroon. East Afr Med J. 2012;89(3):82–8.
Barbosa FS, Pinto R, Souza OA. Control of schistosomiasis mansoni in a small north east Brazilian community. Trans R Soc Trop Med Hyg. 1971;65:206–13.
Farooq M, Nielsen J, Samaan SA, Mallah MB, Allam AA. The epidemiology of Schistosoma haematobium and S. mansoni infections in the Egypt-49 project area. Bull World Health Organ. 1966;35:319–30.
Tanser F, Azongo DK, Vandormael A, Barnighausen T, Appleton C. Impact of the scale-up of piped water on urogenital schistosomiasis infection in rural South Africa. eLife. 2018. https://doi.org/10.7554/eLife.33065.
Gear J, Pitchford R, Van Eeden J. Atlas of bilharzia in South Africa. South African Institute for Medical Research: Johannesburg; 1980.
Noda S, Shimada M, Ngethe DM, Sato K, Francis BM, Simon MG, Wajyaki PG, Aoki Y. Effect of piped water supply on human water contact patterns in a Schistosoma haematobium-endemic area in coast province, Kenya. Am J Trop Med Hyg. 1997;56(2):118–26.
Abe M, Muhoho DN, Sunahara T, Moji K, Yamamoto T, Aoki Y. Effect of communal piped water supply on pattern of water use and transmission of schistosomiasis haematobia in an endemic area of Kenya. Tropical Medicine and Health. 2009;37(2):43–53.
Fine P, Eames K, Heymann DL. Herd immunity: a rough guide. Clin Infect Dis. 2011;52:911–6.
Lima E, Costa MFF, Magalhaes HA, Rocha S, Antunes MF, Katz N. Water-contact patterns and socioeconomic variables in the epidemiology of schistosomiasis mansoni in an endemic area in Brazil. Bull World Health Organ. 1987;65(1):57–66.
Shewakena F, Kloos H, Abebe F. The control of schistosomiasis in Jiga town, Ethiopia. III. Socioeconomic and water use factors. Riv Parasitol. 1993;10:399–411.
Anchang-Kimbi JK, Nkweti VN, Ntonifor HN, Apinjoh TO, Tata RB, Chi HF, Achidi EA. Plasmodium falciparum parasitaemia and malaria among pregnant women at first clinic visit in the Mount Cameroon area. BMC Infectious Disease. 2015;15:439. https://doi.org/10.1186/s12879-015-1211-6.
Wood RG, Goesling B, Avellar S. The effects of marriage on health: a synthesis of recent research evidence. Washington, DC: Mathematica Policy Research, Inc.; 2007.
Lerman R. Marriage and the economic well-being of families with children: a review of the literature. Washington, DC: The Urban Institute and American University; 2002.
Umberson D. Family status and health behaviors: social control as a dimension of social integration. J Health Social Beh. 1987;28(3):306–19.
Bethony J, Williams JT, Kloos H, Blangero J, Alves-Fraga L, Buck G, Michalek A, Williams-Blangero S, LoVerde PT, Correa-Oliveira R, Gazzinelli A. Exposure to Schistosoma mansoni infection in a rural area in Brazil. II: household risk factors. Trop Med Int Health. 2001;6(2):136–45.
Ugbomoiko US, Ofoezie IE, Okoye IC, Heukelbach J. Factors associated with urinary schistosomiasis in two peri-urban communities in South-Western Nigeria. Ann Trop Med Parasitol. 2010;104(5):409–19.
Da Silva AA, Cutrim RN, De Britto MT, Coimbra LC, Tonial SR, Borges DP. Water-contact patterns and risk factors for Schistosoma mansoni infection in a rural village of Northeast Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo. 1997;39:91–6.
Engels D, Ndoricimpa J, Gryseels B. Schistosomiasis mansoni in Burundi: progress in its control since 1985. Bull World Health Organ. 1993;71(2):207–14.
The authors are grateful to all the pregnant women who gave their consent to participate in the study. Our special thanks to the Chief of Centre, nurses and laboratory technicians of the Munyenge Integrated HC, Banga Annex HC and TransAfrican HC for their cooperation and contribution.
This work was supported by the staff development grant and special fund for research and modernization given to authors by the Government of Cameroon.
Availability of data and materials
All datasets generated and analysed during the study are presented in the paper and its supplementary file.
Ethics approval and consent to participate
Ethical clearance (No2017/0481/UB/FHS/IRB) was obtained from the University of Buea, Faculty of Health Sciences Institutional Review Board and administrative authorisation from the South West Regional Delegation of Public Health, Buea and District Medical Officer for Muyuka Subdivision. Written and verbal informed consent was obtained before enrolment into the study. Participation was voluntary and study participants were assured of confidentiality and anonymity of data.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Relative risk reduction in stream usage and contact behaviour, S. haematobium infection rate and intensity among pregnant women following scale-up of communal piped water sources from 2014 to 2017 in Munyenge. This file shows how much the risk of S. haematobium infection/intensity, stream usage and contact behaviour has reduced among pregnant women following scale-up of communal piped water sources from 2014 to 2017 in Munyenge. (DOCX 16 kb)