Urogenital schistosomiasis transmission hot-spot areas in Zanzibar have remained resilient to PC and additional control interventions for multiple years. We aimed to better characterise persistent hot-spot shehias in Unguja to inform and improve intervention planning for schistosomiasis elimination in Zanzibar.
No major difference in the treatment coverage was found between persistent hot-spot and low-prevalence shehias. The SCORE coverage survey revealed that while the observed coverage in all targeted schools in 2013 was above the 75 % mark, the overall observed coverage for CWT in persistent hot-spot and low-prevalence shehias was 70 % and 61 %, respectively. Hence, a substantial part of the population remained untreated and potentially infected individuals might have contributed to the perpetuation of transmission in areas where intermediate host snails were present. Recent modelling work has shown that interruption of schistosomiasis transmission in moderate intensity settings is possible, if at least 75 % of school-aged children are treated annually with praziquantel and if a moderate treatment coverage in adults is reached [37]. However, heterogeneity in terms of water contact type and the sort of aquatic habitat near each village had not been considered and would require individual based stochastic models, which incorporate spatial transmission [37, 38].
Indeed, we identified considerably more HWCSs containing B. globosus (average: ?=?8 vs n?=?2) and B. globosus infected with S. haematobium (average: ?=?2 vs n?=?0) in persistent hot-spot than in low-prevalence shehias. Bulinus globosus infected with S. haematobium were found exclusively at HWCSs located in hot-spot but not in low-prevalence shehias. The proportion of snails with a patent infection (2 %) found in the persistent hot-spot shehias in our study, is in line with the proportion of snails collected with patent infections reported from other studies conducted in Zanzibar and elsewhere in sub-Saharan Africa [35, 39–41]. While these infection levels seem rather low considering the S. haematobium prevalence in children in the persistent hot-spot shehias, previous work conducted in Zanzibar has shown that the cercariae shedding method misses many prepatent infections [35]. If more advanced, molecular techniques are used for screening snails instead, it is likely to detect a considerably higher number of infected snails [35, 40, 42–44]. Rapid detection of schistosome cercariae ribosomal DNA in environmental samples using new methods could also aid in uncovering transmission sites that may have previously been missed following classic snail ‘shedding’ methods [45].
Our study also revealed that the distance to HWCSs containing intermediate host snails was shorter from schools with high S. haematobium prevalence than from the low-prevalence schools where the S. haematobium prevalence was??5 %. Similarly, another study from Zanzibar had shown that the highest S. haematobium prevalence was found in village hamlets that were located in close proximity to HWCSs containing B. globosus and infected B. globosus [17]. Also in Mali, the vicinity of intermediate host snail breeding sites in six communities was one of the main risk factors for S. haematobium infection in residents [46].
The presence of B. globosus in our study areas was associated with certain behavioural activities observed at the HWCSs. Bathing and swimming/ playing significantly reduced the odds of finding B. globosus at HWCSs. This observation might be explained by the use of soap and the turbulent nature of these activities creating an environment less favourable for B. globosus [34]. In contrast, washing dishes and fishing significantly increased the odds of finding B. globosus at HWCS, perhaps indicating a nutrient rich environment caused by food remnants washed from dishes and indicated by the presence of fish, respectively. Interestingly, intermediate host snails infected with S. haematobium were significantly less likely to be present at HWCSs where water was collected for drinking and cooking. People not urinating and contaminating the water source that is used for potable water collection might be an explanation for this observation. Infected snails were also less present at HWCSs used for washing clothes. Soap might have an adverse effect on cercariae, as suggested elsewhere [17, 47].
In line with the baseline snail survey conducted at the onset of the SCORE operational research trial [14], but in contrast to studies previously conducted in Unguja [32, 35], water characteristics were not linked to the presence/ absence of B. globosus in the present study. Other, not presently measured factors and environmental dynamics, such as the permanence of the water body itself or flooding events that re-seed areas, might better predict the occurrence of intermediate host snails and merit future investigation.
We found that on average there were less taps in persistent hot-spot shehias than in low-prevalence shehias (?=?19 vs n?=?30). In addition, the taps located in persistent hot-spot shehias had significantly lower odds of providing a constantly available water supply. While wells constituted a frequent and relatively constant water source particularly in the persistent hot-spot shehias of our study, they are reasonably cumbersome to use for children, who might use nearby freshwater bodies as alternatives for bathing or washing. The lack of reliable taps from which water collection is easy might contribute to people using potentially infectious freshwater bodies as a simple alternative for conducting domestic chores [48]. Improving and increasing the access to safe water and additional water, sanitation and hygiene (WASH) measures should be part of a sustainable schistosomiasis elimination strategy in Zanzibar and elsewhere [49–53].
Interestingly, in the “hottest” persistent hot-spot shehia, Koani, the distance from the school to the nearest HWCS (152 m) and HWCS containing B. globosus (218 m) was much shorter than the distance to the nearest SWS (376 m), although it was the shehia with the highest number of reliably working SWSs. Moreover, the highest number of B. globosus (?=?503) was collected in Koani.
Our small study design clearly limits the ability to attribute a meaning to unexpected findings. However, already the inclusion of only a small number of shehias has provided evidence that characteristics such as a larger number of HWCSs containing intermediate host snails and B. globosus infected with S. haematobium, a shorter distance from the primary school to the nearest HWCS and the lack of easy to use and reliably functioning SWSs play an important role in defining persistent hot-spot areas. This information can help to define, tailor and target future multidisciplinary interventions that will effectively reduce urogenital schistosomiasis transmission hot-spots in Zanzibar.
Recent reviews and analyses of the existing literature have outlined snail control as the most effective way of reducing schistosomiasis prevalence in endemic areas [54, 55]. Indeed, to sustainably curtail schistosomiasis transmission in Zanzibar, large-scale mollusciciding in hot-spot areas and focussed to HWCSs will be essential. With regard to the movement of potentially infected individuals between the shehias and the potential for re-contamination of treated freshwater bodies, it will be important to identify all HWCSs and the intermediate host snail abundance in areas of high transmission and to rigorously treat HWCSs regularly when intermediate host snails are present. The molluscicide niclosamide is the only commercially available and approved chemical for control of freshwater snails. However, while it is effective, it does have an impact on other aquatic organisms such as fish and amphibia and should be used carefully.
In addition to PC and area-wide snail control, the reduction of human-water contact by improving access to easy to use and reliably working SWSs and the minimisation of water contamination by changing human behaviour in hot-spot areas will be crucial for reaching elimination of transmission. Partnering with organisations and ministries that have the infrastructure and expertise to support and enhance WASH and educational measures can strengthen future interventions for elimination of urogenital schistosomiasis transmission in Zanzibar and elsewhere.