Longitudinal malacological monitoring, with a parasitological survey, reveals new schistosomiasis transmission foci in deforested sites in Western Uganda

Abstract

Background In sub-Saharan Africa, the epidemiology of schistosomiasis, a waterborne parasitic disease, is often altered by environmental and land-use changes. In the upland area of Western Uganda, ongoing destruction of the Bugoma Forest is transforming many lotic freshwater habitats, potentially favouring intermediate hosts of schistosomes. We therefore undertook a longitudinal malacological monitoring study for Biomphalaria and Bulinus, keystone intermediate host snails, to describe actual or potential transmission of schistosomiasis. Methods Starting in June 2023, snail sampling was conducted regularly, every other month, at nine sites for eighteen months, until October 2024. To bolster this, an analysis of satellite imagery of vegetation and land-use change over the previous 20 years was undertaken. At each inspection site water temperature, conductivity and pH were noted, alongside on-site observations of human and animal activities. Snails were identified by morphology, with inspection for shedding Schistosoma cercariae, which were later identified by molecular analysis. Results Mean water temperature, conductivity and pH were 23.5 °C (± 1.8), 235.0µS (± 81.7) and 6.9 (± 0.3), respectively. A total of 2524 Biomphalaria snails at seven sites and 422 Bulinus snails at one site were examined. Abundance of Biomphalaria snails was greater (p < 0.01) in sites where the forest had been cleared, with human encroachment evident. Schistosoma cercariae were shed from 0.4% of Biomphalaria and 1.9% of Bulinus with monthly maxima of 3.1% and 3.7%, in December 2023 respectively. In August 2024, among local school-aged children (n = 41), the prevalence of intestinal schistosomiasis was 56.1% whereas urogenital schistosomiasis was absent. Further to the presence of Schistosoma mansoni cercariae, molecular analyses also revealed Schistosoma bovis and Schistosoma rodhaini. Satellite imagery showed land-use change with the Bugoma central Forest reduced by 18.0% and shrub land by 57.0% due to human agricultural activities, revealing an expanding zone of putative schistosomiasis transmission in upland areas. Conclusion This changing endemicity of human and animal schistosomiasis to new areas, some 15 Km away from Lake Albert, needs to be addressed by the Uganda Ministry of Health and National Forestry Authority. Further targeted malacological and schistosomiasis surveillance, at finer geographical resolutions, will pinpoint new foci and better guide local interventions.