Systems epidemiology of snail-borne diseases : from methodological to social-ecological considerations in the fight towards elimination

Background: Snail-borne trematode infections, including schistosomiasis and fascioliasis, affect an estimated 250 million and 2.4 million people worldwide, respectively. Health implications range from asymptomatic infections to severe morbidity, developmental and cognitive impairment, thus affecting the current and later life of infected individuals. Nonetheless, snail-borne trematodiasis in general, and fascioliasis in particular, remain among the most neglected of the neglected tropical diseases. The occurrence of these parasitic liver- and blood-fluke infections depend on a myriad of interrelating factors comprising a complex system of disease and health. A key feature pertains to the availability of suitable aquatic snail intermediate hosts from the family of the Lymnaeidae (for schistosomiasis) and Planorbidae (for fascioliasis). The distribution of these intermediate host snails, in turn, depends on ecological and environmental factors of their habitats, whereas these habitats are shaped by humans. The construction of dams, for example, extends the suitable habitats for intermediate host snail species and has been implicated with the spread and intensification of schistosomiasis. Furthermore, socio-economic and cultural factors as well as behaviour largely determine the extent of risky water contact including direct and indirect consumption and thus govern the risk of becoming infected with Schistosoma and Fasciola. Prevailing habits and social believes as well as knowledge and education likewise influence water contact patterns and health seeking behaviour. Individual immunology plays a role in acquiring infections and subsequent development of the disease for individuals exposed to these fluke infections. The nature of the interrelations in snail-borne trematode infections are complex and widespread. In order to eliminate snail-borne trematodiasis, especially schistosomiasis, efforts in the domains from innovation to application need to be increased covering all aspects of the whole system.
Goal and specific objectives: The overarching goal of this PhD thesis was to obtain a systems overview of schistosomiasis and – to some extend – fascioliasis in the northern area of Côte d’Ivoire, placing particular emphasis of disease prevalence, social-ecological systems and methodological considerations. Specific objectives include: (i) to evaluate and improve currently existing tools for the assessment of infection within the communities ranging from household sampling to the validation of two rapid-diagnostic test within the setting; (ii) to elucidate prevailing water contact pattern and underlying reasons thereof alongside other factors leading to an increased risk of acquiring snail-borne trematodiasis for the local communities in northern Côte d’Ivoire; and (iii) to assess the distribution and ecological determinants of aquatic snail species serving as intermediate hosts for schistosomiasis and fascioliasis and relating it to the prevalence of infections within the human communities using these water sources.
Methods: A literature review was performed to identify suitable household sampling methods for situations where sampling frames are not available. Identified and newly proposed sampling methods were simulated over 250 iterations to identify features or the resulting samplings and assessing the amount of oversampling, systematic household exclusion as well as clustering.
For the studies involving fieldwork, a total of forty villages were randomly selected for participation. The study protocols received clearance from the ethics committees of Basel (EKBB, reference no. 64/13) and the national ethics committee in Côte d’Ivoire (reference no. 32-MSLS/CNERdkn). In Chad, research authorization including ethical approval was granted by the
District, regional and local authorities, village chiefs, study participants and parents/guardians of individuals aged below 18 years were informed about the purpose, procedures and potential risks and benefits of the study. Written informed consent was obtained from all participants and the parents/guardians of minors. Parasitological examinations as well as questionnaire surveys, focus group discussions and direct observations were performed within the villages, nearby Peulh settlements and surrounding water bodies. Parasitological examinations included reagent strip testing with Hemastix®, (Bayer Diagnostics; Basingstoke, United Kingdom), urine filtration of 10 ml of urine, double Kato-Katz of a single stool sample, Baerman filtration and the point-of-care circulating cathodic antigen test. Snails and water parameters were collected from water sites indicated by the communities as the ones most frequently accessed by the population.
Results: Our literature review revealed 21 methods for household sampling and/or the creation or update of sampling frames. Some methods describe variations of cluster sampling, some aiming at the creation/obtaining or improving of existing sampling frames and some pertaining to achieve sampling in the absence of a sampling frame. Three methods pertained to sampling with rather strict requirements in surveys. A preliminary computer simulation of several existing and newly proposed spatial methods for household sampling revealed that all sampling methods based on a spatial approach oversampled houses around the starting point. Additionally many also systematically excluded certain households. One newly proposed method which employs the simple to implement use of a pouch of numbered paper lots is an adaption of the method from the extended programme of immunization (EPI). Equally sized and shaped paper lots containing numbers ranging from 1 to 20 are put into the pouch. An additional 21st lot is included, indicating that a new walking direction will have to be chosen randomly by spinning a bottle. This method delivered the best sample in the simulations, whereas several methods developed to improve the original EPI methods actually had worse outcomes compared to the original EPI method. A decision frame for choosing an adequate household sampling method for researchers and other individuals conducting surveys is proposed in the respective chapter.
The prevalence of schistosomiasis in the Tchologo region of northern Côte d’Ivoire was very low; Infections with S. haematobium and S. mansoni infections were found in 2.2% and 1.0%, respectively. No human Fasciola infection was found. With a prevalence of 13%, microhaematuria, as assessed with reagent strips, far surpassed the prevalence of S. haematobium determined with urine filtration in the study region. Our literature review revealed that in many published surveys, microhaematuria-positive test results that were not linked to positive urine filtration results occurred irrespective of the underlying S. haematobium prevalence assessed by urine filtration. These findings indicate either the occurrence of alternative causes for blood in urine in endemic settings or the gross underestimation of the true prevalence of S. haematobium in various settings.
All individuals in our study villages had access to, and were using, safe water sources. Nevertheless, accessing and consuming unsafe water was very common and occurred in most instances during work on the fields or at the side of the road where it was unfeasible to transport needed quantities of drinking water and/or where water from the dams, rivers and small water collections was needed for the work. Additionally we could show that 38% of direct physical contact with unsafe water resulted from the fact that people who otherwise reported to only use safe water sources had to cross open water and thus increase the risk of acquiring schistosomiasis, albeit adequate water supply and sanitation facilities.
Intermediate host snail species were present in the study area, with fascioliasis intermediate host snails from the family of the Lymnaeidae occurring mostly in the northern part of the region, whereas Schistosoma mansoni transmitting Biomphalaria snails occurred mostly in the southern region, while Bulinus (intermediate host of S. haematobium) were ubiquitous. Human and animal presence at the water sites strongly correlated with snail occurrence.
Conclusions: The adoption of a systemic approach for the control and elimination of snail-borne trematodiases can be very helpful, as it allows inclusion and consideration of a myriad of factors, ranging from methodological to social-ecological issues. Furthermore, researchers and intervention programmes could benefit from an even greater collaboration between different scientific fields, including but not limited to epidemiology, parasitology, sociology, anthropology and social psychology. Indeed, understanding the factors which make humans act in a certain desired or undesired way can play a major role in the success of control or elimination efforts. Most notably, the largest potential benefit could arise from working together with social marketers and drawing upon their years of experience in adequately identifying and analysing target populations and designing ways to tailor implement and communicate public health programmes/messages in a way that maximises community interest and incentives to adopt and sustain the programmes.