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. Approximately, 240 million people worldwide (WHO, 2010; Stothard et al., 2009) are infected with schistosomiasis, with a disease burden of 3.3 million disability-adjusted life-years (Murray et al., 2012). In sub-Saharan Africa alone, an estimated 163 million people were infected in 2012 (Lai et al., 2015). Following the London declaration (Uniting to Combat Neglected Tropical Diseases, 2012), the World Health Organization (WHO) has set a goal of increasing mass drug administration coverage to 75% of at-risk children in endemic countries (WHO, 2013). Despite progress in many so-called ‘neglected tropical diseases’, the fourth progress report of the London Declaration records that schistosomiasis has the lowest coverage of all helminth diseases treatable by mass drug administration (Uniting to Combat Neglected Tropical Diseases, 2016).

For achieving sustained control, elimination, or eradication of schistosomiasis, improvements of water, sanitation, and hygiene infrastructure and modification of risk behaviour are necessary (Freeman et al., 2013; WHO, 2015; Steinmann et al., 2006; Echazú et al., 2015). One important approach is the provision of safe water supplies to reduce the need for contact with contaminated water bodies and diminish the risk of schistosomiasis transmission. However, quality evidence for the impact of provision of safe water on schistosomiasis infection is currently lacking. Recently, a systematic review concluded that previous studies on this topic were of poor quality and likely confounded by multiple socio-economic and other variables (Grimes et al., 2014). The authors conclude that new research is needed ‘on the relationships between water, sanitation, hygiene, human behaviour, and schistosome transmission'. In this regard, the previously used exposure measures of household or individual access to safe water (Grimes et al., 2014) will underestimate the true health impacts of the provision of safe water at a population level. This is because the introduction of safe water supplies into a community offers protection from schistosomiasis infection in two ways. Firstly, it offers direct protection to individuals with access to safe water by reducing their contact with infected water bodies through household domestic water collection activities. Secondly, the scale-up in 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’ (Fine et al., 2011). This form of protection is conferred 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. Thus, the greater the proportion of individuals in a community who are not actively contributing to the perpetuation of the schistosomiasis transmission cycle, the smaller the probability that those who interact with open water bodies will come into contact with free swimming cercariae released by infected snails.

Hence, to capture the true overall population-level impact of the introduction of piped water, it is necessary to move beyond a simple household/individual level exposure approach towards a sensitive community-level exposure estimate that quantifies the coverage of piped water in the surrounding local community over an extended period of time preceding the measurement of the disease outcome. To date, no studies have quantified the (likely non-linear) relationship between coverage of piped water (%) at the community level and corresponding reductions in risk of schistosomiasis infection. From an epidemic control and eradication perspective, quantification of such a relationship would provide the best indicator of the true overall impact of the scale-up in piped water and would reveal critical coverage targets for achieving meaningful reductions in risk of schistosomiasis infection.

To accomplish this goal, we nested a Schistosoma haematobium survey within one of Africa’s largest population-based cohorts in which all children and their families (N≈90,000) have been intensively followed up in an endemic area of rural KwaZulu-Natal, South Africa. We exploit the heterogeneity in the space-time scale-up of piped water over seven years and detailed longitudinal risk factor information to provide a rigorous quantification of the impact of the introduction of piped water on risk of urogenital schistosomiasis infection measured in children living in the study community. We then validate the veracity of our findings using an instrumental variable approach.

Of the 2105 participants tested in the parasitological survey, 353 were infected with Schistosoma haematobium. The overall prevalence was 16.8% (95% CI: 15.2–18.4) and the prevalence of heavy infection (≥50 eggs/10 ml of urine) was 9.5% (95% CI: 8.3–10.8). Prevalence was twice as high in boys compared to girls (22.6% versus 11.4%) and peaked at 30% in boys at age 14 years and 15% in girls at age 12 years (Figure 1). Prevalence of heavy infection was 13.5% in boys (and peaked at 21.4% at age 14 years) and 5.7% in girls (peaking at 8.7% at age 12 years). 57% of all infected participants had heavy infections with a geometric mean egg burden of 65 eggs/10 ml urine. Overall, 80% of the egg burden was borne by just 3.4% of all pupils tested (20.4% of all infected participants).

Figure 1

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Overall, 67% of participants who were present at school on the day of testing had parental consent and assent and provided a urine specimen. Only 2.2% of linked participants reported receiving praziquantel in the last 12 months (Table 1). Participation in the parasitological survey did not differ significantly by piped water access or any of the environmental and socio-economic control variables used in the analysis. However, there were differences in levels of participation by school (p<0.05) and small differences by age and sex (p<0.1). After standardising for these differences according to age, sex and school, the prevalence remained virtually unchanged at 16.9%.

The geospatial analysis using the Gaussian kernel approach revealed substantial spatial variation in prevalence of urogenital schistosomiasis across the different communities within the surveillance area (Figure 2). The kernel-derived prevalence of urogenital schistosomiasis varied between 0% and 85% and revealed two clear regions of high transmission where prevalence was >50%. A formal micro-geographical clustering analysis using the Kulldorff spatial scan statistic revealed four significant foci of infection around open water collection sites (relative risk = 2.99–5.63, p<0.05; Figure 2, Table 2). Two clusters of infection were located along the Nsane River in the northeast of the surveillance area (clusters 2 and 3) and the other two located around water bodies towards the south of the study area.

Figure 2

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Between 2001 and 2007, the provision of piped water in the surveillance area nearly doubled from 42% to 80% (Figure 3). The community-based mean coverage of piped water between 2001 and 2007 was 61.7% (Figure 3, bottom right). There is a high degree of temporal and spatial consistency in the patterns of expansion of piped water access across the five respective surveys, providing assurance of the quality of the underlying population-based data.

Figure 3

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We identified a clear dose-response between the risk of urogenital schistosomiasis infection and piped water coverage in the surrounding local community (Figure 4a). Participants living in communities with a high coverage of piped water (median coverage = 95.5%) were eight times less likely to be infected (aOR = 0.12, 95% CI 0.06–0.26, p<0.001; Model 1 of Table 3) in comparison to those living in communities with lowest coverage (median coverage = 8.4%). This reduction was greater for girls than boys (aOR = 0.07 versus aOR = 0.17 in boys; Model 1 of Table 4) after controlling for key socio-economic and environmental predictors of infection.

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Using a continuous measure of community-level piped water coverage, we found that every 1% increase in the coverage of community piped water was independently associated with a 2.5% decrease in the odds of infection (aOR = 0.975, 95% CI 0.966–0.985, p<0.001; see Figure 4b). The relationship is a non-linear one because it is derived from the piped water coverage regression coefficient (–0.025) and then exponentiated to derive an odds ratio. The resulting relationship would imply that relatively modest levels of piped water coverage in a given community could have a large impact on reduction in the odds of infection. For example, a piped water coverage of 30% would correspond to a greater than 50% decrease in the odds of infection for individuals living in that community (Figure 4b). We also found that the result of our primary analysis (ie effect of community-level piped water coverage) was robust to the exact specification of the community (kernel) evaluating the piped water coverage around each member of the cohort. For example, when we increased the size of the kernel’s search radius from 2 km to 3 km then we found that both the continuous (aOR = 0.97, 95% CI: 0.96–0.98, p<0.001) and categorical effect-size estimates (quintile five versus quintile one aOR = 0.12, 95% CI: 0.06–0.24, p<0.001) remained virtually unchanged. Further, we report similar results for a parallel set of analyses (using a Poisson model) to derive risk ratios of infection (Figure 4—figure supplement 1, Supplementary file 2).

For a comparative exercise, we replaced the mean community-level piped water exposure (2001–2007) exposure variable with the piped water coverage only in the year of the parasitological survey (2007). As anticipated, we find in this model that the resulting risk-reduction is attenuated (by 44%) but nevertheless still significant (aOR = 0.986, 95% CI: 0.98–0.99, p=0.004), providing further empirical support for the analytical approach taken in the longitudinal measurement of mean piped water coverage in the years leading up to the parasitological survey.

As a secondary objective, we analysed the impact of household access to piped water on risk of urogenital schistosomiasis infection. We found that this exposure was independently associated with a significant reduction in the odds of infection (aOR = 0.54, 95% CI: 0.33–0.89, p=0.017; Model 2 of Table 3), which was considerably smaller than its community-level counterpart. Once again this reduction was driven mostly by the reduction in risk in girls (aOR = 0.38, 95% CI: 0.19–0.75, p=0.005; Model 2 of Table 4), which was substantially larger than the corresponding impact in boys (aOR = 0.76, 95% CI: 0.41–1.42, p=0.38; Model 2 of Table 4, see also Figure 5). When formally testing this as an interaction effect in the combined-sex model, the reduction in risk was significantly greater for girls (p=0.014).

Figure 5

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Our risk-reduction estimate for access to piped water at the household level (aOR = 0.54) is close to the Schistosoma haematobium specific aOR of 0.57 generated as part of Grimes et al. systematic review (Grimes et al., 2014) comprising 17 previous studies (Abou-Zeid et al., 2012; Al-Waleedi et al., 2013; Awoke et al., 2013; Dame et al., 2006; Dawet, 2012; Farooq et al., 1966; Howarth et al., 1988; Knopp et al., 2013; Nworie et al., 2012; Reuben et al., 2013; Sady et al., 2013) (Figure 6). The revised overall risk-reduction estimate changes marginally after inclusion of our results and rerunning the meta-analysis, to 0.56 (95% CI: 0.45–0.70). The fact that our effect-size estimate for this secondary analysis is close to that obtained from the systematic review and meta-analysis (based on 17 data-points), lends further credence to our findings - including the risk-reduction result reported from our primary analysis (described above).

Figure 6

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Finally, our IV analysis to address any potential residual confounding confirms all of our main results. Our instrumental variable met the relevance condition of instrumental variable estimation, as shown by the size of the F-test for instrument strength (F-statistic = 55). In the IV analysis using a linear model, a 1% increase in the coverage of piped water in the surrounding community was independently associated with a 0.48% decrease in the risk of urogenital schistosomiasis infection (Coef= –0.0048, p<0.001; Model 2 of Supplementary file 2). This effect-size estimate is larger than the risk reduction observed without the IV, which was 0.30% (Coef = –0.003, p<0.001; Model 1 of Supplementary file 2). Household access to piped water was associated with a 15.6% reduction in the risk of infection (Coef = –0.156, p=0.035; Model 4 of Supplementary file 2). This effect-size is higher than the estimate in the analysis without the IV, which was 9.2% (Coef = –0.092; p=0.013; Model 3 of Supplementary file 2). These findings demonstrate that the reductions in urogenital schistosomiasis risk are not overestimated as a result of other unmeasured variables or residual confounding.

We have linked longitudinal population-based exposures to schistosomiasis outcomes in a large cohort of children to provide a rigorous quantification of the relationship between piped water coverage and the risk of urogenital schistosomiasis infection in a typical rural sub-Saharan African population. This approach provides a strong indicator of the overall impact of the introduction of piped water because it captures both the direct and indirect protection conferred by the scale-up. Our results reveal a large impact of piped water scale-up on urogenital schistosomiasis infection. This impact is substantially greater than previous results had suggested (Grimes et al., 2014), based on measurement of access to safe water supplies at the household or individual level. In our study, 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. Every 1% increase in the coverage of piped water in the surrounding local community was associated with a corresponding 2.5% decrease in the odds of infection. As a secondary objective, we also provide a robust household-level piped water risk-reduction estimate (aOR = 0.54) after controlling for key socio-economic and environmental predictors of infection. This result is also important, because the relationship between piped water and schistosomiasis infection at the household or individual level would be confounded in different ways by multiple socio-economic and environmental factors, as the recent systematic review of the existing literature points out (Grimes et al., 2014). Importantly, we validate the veracity of all of the above findings using an instrumental variable approach to control for the influence of residual unobserved confounding that could have biased our effect-size estimates.

Our results show that nearly 1 in 5 primary school children (median age = 11 years) were infected with urogenital schistosomiasis and nearly 1 in 10 were heavily infected. These levels of urogenital schistosomiasis infection are markedly lower than the overall prevalence of 60–70% recorded in the general area thirty years earlier (Gear et al., 1980) and 69% prevalence recorded in a more recent survey undertaken in a neighbouring district at similar altitude (<300 metres above sea level) but with limited access to piped water (Saathoff et al., 2004). Importantly, our geographical analyses revealed remarkable spatial heterogeneity in urogenital schistosomiasis prevalence across the relatively small surveillance area. For example, the prevalence of infection was >80% in some communities where the roll-out of piped water had not taken place. At a micro-geographical level, we identified clear spatial clustering of infections around four specific open water collection sites. This heterogeneity in schistosomiasis transmission is consistent with the results of a 2004 study conducted 200 km north of the surveillance area (Saathoff et al., 2004).

Another important finding to emerge from the work is that the greater burden of urogenital schistosomiasis infection is borne by boys who had more than twice the prevalence of infection in comparison to girls. In addition, there were clear sex differentials in the pathways of infection and the impact of piped water at a household and community level. Whilst environmental variables (distance to water-body, altitude and landcover class) were highly predictive of infection in both sexes, higher socio-economic status was independently associated with a decrease in the odds of infection for girls but not for boys. At the community level, piped water coverage was associated with significantly greater reductions in the infection risk for girls. Similarly, household access to piped water was associated with a significant reduction in risk in girls but not in boys. These sex differences at both the community and household level could reflect the cultural context in which girls are responsible for the majority of the domestic water collection and/or a situation where boys swim more often in infected water bodies (Ngorima et al., 2008; Thomassen Morgas et al., 2010).

The differential in the community/household risk-reduction result for boys suggests that the scale-up of piped water has conferred substantial indirect protection to boys through the lowering of the overall parasite reservoir in a particular community. Had we only analysed access to piped water as a single household-level exposure, we would have failed to demonstrate that the scale-up this intervention offered any significant protection to boys. Boys are exposed in the community to free swimming cercariae released by snails infected not just by themselves but also by their family members and neighbours. Therefore, in order to fully capture the impact of piped water in reducing schistosomiasis transmission risk, it is crucial to look beyond the household and consider the piped water coverage level in the surrounding local community. This view is also expressed by other authors (Esrey and Habicht, 1986). The greater than four-fold ratio in the community-level (aOR = 0.12) versus household-level (aOR = 0.54) risk-reduction estimate provides empirical support for this viewpoint. Whilst no such community-level analyses have previously been conducted for Schistosoma haematobium, a study in China found Schistosoma japonicum infection rates to be significantly lower in communities where more than 50% of people used ‘hygienic lavatories’ (Yang et al., 2009).

Our study design has several strengths that overcome many of the limitations typically associated with school-based surveys in which the exposures and disease outcomes are measured at the same point in time. By nesting the parasitological survey within a population cohort followed over seven years preceding the measurement of the disease, we utilise longitudinal data collected both on the participants of the parasitological survey, as well as the entire population to provide a rigorous quantification of the impact of the introduction of piped water on risk of urogenital schistosomiasis infection. A key strength of the work is that rather than treating access to piped water as a household/individual level exposure as in previous work (Abou-Zeid et al., 2012; Al-Waleedi et al., 2013; Awoke et al., 2013; Dame et al., 2006; Dawet, 2012; Farooq et al., 1966; Howarth et al., 1988; Knopp et al., 2013; Nworie et al., 2012; Reuben et al., 2013; Sady et al., 2013), we were able to quantify the clear dose-response in the relationship between community coverage of piped water and risk of infection. In addition, we used a novel spatial methodology to perform a micro-geographical clustering analysis, based on the exact location of the participants’ households, to pinpoint clear transmission foci around four open water collection points. Crucially, through the use of high resolution satellite imagery, ancillary environmental data and variables collated as part of the ongoing population cohort, we controlled for the key individual, social, environmental and community determinants of schistosomiasis infection which are vital to quantifying the independent impact of piped water. Notwithstanding the above, we wanted to completely exclude the possibility of residual confounding (on the basis of unmeasured social and environmental factors) leading to an over-estimate of the impact of the introduction of piped water on risk of infection. To address this possibility, we performed an instrumental variables (IV) analysis using the year that piped water was first introduced into the community as the instrument. Our results remained robust in this analysis: all effect-size estimates remained significant and increased to some extent in comparison to the main results. These findings demonstrate that the reductions in risk reported in this paper are robust and may be regarded as being marginally conservative.

However, the study has some limitations. The results are based on a single urine sample and as a result we would likely have missed some light infections (Kosinski et al., 2011). The true prevalence of infection is therefore probably higher than 16.8% reported in this study. A further limitation is that, while South Africa is a country with near-universal primary school attendance (Lund, 2011), we could be missing some children who did not attend school on the day of testing because they have schistosomiasis-related morbidity. This would lead to an under-estimate of the prevalence of urogenital schistosomiasis. In addition, the high mobility of this population (Dobra et al., 2017) means that children would be moving between communities, resulting in an ascertainment error leading ultimately to a reduction in the true effect-size, which would bias the result towards the null hypothesis of no piped water impact. In addition, infrequent, ad-hoc schistosomiasis ‘test and treat’ activities conducted in schools in the highest-risk areas (where piped water coverage was lowest), could theoretically bias the effect-size towards the null hypothesis of no piped water impact. However, introduction of such a bias by these activities is unlikely given the large piped water effect-sizes that we report and the fact that only 2% of participants in our survey reported receiving praziquantel in the previous 12 months (which we use as a control variable in the statistical model). In any event, any related ‘residual confounding’ effect if it did exist, would be controlled for in the IV approach which confirmed all of our main findings.

Schistosomiasis and soil-transmitted helminthiasis affect more than 1.5 billion of the world's poorest people (Lai et al., 2015). Without a change in strategy to control these diseases, the population of sub-Saharan Africa will lose an estimated US$3.5 billion of economic productivity every year, which is comparable to recent acute epidemics, including the 2014 Ebola and 2015 Zika epidemics (Lo et al., 2017). Our analytical approach (quantifying the combined direct and indirect impact of the scale-up in piped water) has captured a large measurable association between the introduction of piped water and the reduction in risk of urogenital schistosomiasis in a rural African community. This reduction is substantially greater than had been suggested by previous work (Grimes et al., 2014), which focused on household or individual level access to safe water. The continued expansion of safe water supplies, decreasing prevalence and highly focal nature of disease transmission, suggest that the disease is retreating and could be vulnerable to eradication in similar African contexts. Recent modelling work indicates that the current WHO treatment goals (which aim to mass-treat 75% of at-risk children) should be successful in eradicating schistosomiasis transmission if continued for a decade in areas of low to moderate transmission (Anderson et al., 2015). However, once mass treatment is suspended, the prevalence of infection can rebound to pre-control levels over a period of 25–30 years (Gurarie et al., 2015), emphasising the need for a fully integrated approach that includes the provision of safe water supplies, community health education as well as the possibility of focal snail control (Knopp et al., 2013; King et al., 2015).

The overall moderate levels of infection (significantly lower than historical surveys (Gear et al., 1980) combined with the extreme inter-host and geographical heterogeneity as well as ever increasing access to safe water suggest that sustained mass treatment campaigns in such populations could drive schistosomiasis towards low levels of endemicity (Crompton and WHO, 2006). Our results emphasise the need to rapidly increase the provision of safe water supplies to schistosomiasis endemic areas, where the resulting impact will extend well beyond prevention of transmission of schistosomiasis to diarrhoeal diseases, for example (Esrey and Habicht, 1986); as well as having substantial related economic benefits (Lo et al., 2017). Scale-up in the provision of safe water and sanitation, along with the small cost of drugs combined with the renewed commitment to increase funding for neglected tropical diseases, including schistosomiasis, means that there is a real opportunity to push back the disease from areas where it has long been endemic.

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Author details

1. Frank Tanser

   1. Africa Health Research Institute, KwaZulu-Natal, South Africa
   2. School of Nursing and Public Health, University of KwaZulu-Natal, Durban, South Africa
   3. Centre for the AIDS Programme of Research in South Africa (CAPRISA), University of KwaZulu-Natal, Durban, South Africa
   4. Institute of Epidemiology and Health Care, University College London, London, United Kingdom

   Contribution

   Conceptualization, Data curation, Formal analysis, Supervision, Funding acquisition, Validation, Investigation, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   ftanser@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9797-0000

2. Daniel K Azongo

   Navrongo Health Research Centre, Ghana Health Service, Navrongo, Upper East Region, Ghana

   Contribution

   Investigation, Methodology, Writing—original draft, Project administration, Writing—review and editing

   Competing interests

   No competing interests declared

3. Alain Vandormael

   1. Africa Health Research Institute, KwaZulu-Natal, South Africa
   2. School of Nursing and Public Health, University of KwaZulu-Natal, Durban, South Africa
   3. KwaZulu-Natal Research Innovation and Sequencing Platform (KRISP), College of Health Sciences, University of KwaZulu-Natal, Durban, South Africa

   Contribution

   Formal analysis, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5742-0511

4. Till Bärnighausen

   1. Africa Health Research Institute, KwaZulu-Natal, South Africa
   2. Institute of Epidemiology and Health Care, University College London, London, United Kingdom
   3. Department of Global Health and Population, Harvard T.H. Chan School of Public Health, Boston, United States
   4. Institute for Public Health, University of Heidelberg, Heidelberg, Germany

   Contribution

   Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

5. Christopher Appleton

   School of Life Sciences, University of KwaZulu-Natal, Durban, South Africa

   Contribution

   Conceptualization, Funding acquisition, Investigation, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

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