African schistosomes in small mammal communities: Perspectives from a spatio-temporal survey in the vicinity of Lake Guiers, Senegal
Résumé
Abstract:
Schistosomiasis is a neglected tropical disease of public health significance. In view of its elimination as a public health problem by 2030, adopting a One Health approach is necessary, considering its multidimensional nature. Animal reservoirs, in particular, pose a significant threat to schistosomiasis control in Africa and beyond. In this study, we conducted a spatio-temporal survey of Schistosoma infections in small mammal communities and intermediate snail hosts in the vicinity of Lake Guiers in northern Senegal. Sampling campaigns were undertaken four times between April 2021 and August 2022 around eight villages. A total of 534 small mammals of four species, primarily Hubert's multimammate mice Mastomys huberti, were captured. Out of 498 individuals examined, only 18 rodents (17 M. huberti and 1 Arvicanthis niloticus) were infected with schistosomes. The infection rates in M. huberti varied over time (prevalence range: 2.4% to 9.3%, intensity range: 4 to 132), and space (prevalence range: 3.1% to 40%, intensity range: 2 to 110) and were higher in adult hosts captured during or just after the rainy season, a time when older individuals dominate in rodent populations. Using a multi-locus molecular approach (cox1 and ITS) on Schistosoma larvae (cercariae and miracidia) and adult worms, we identified Schistosoma mansoni as the most widespread species. We also detected Schistosoma bovis and Schistosoma haematobium in M. huberti from one locality (Temeye). Although no Schistosoma hybrids were found, the discovery of a male S. mansoni and a female S. bovis pair raises concerns about potential hybridization patterns that could occur in rodents. Finally, three snail species were found infected (25 Biomphalaria pfeifferi, 3 Bulinus truncatus and 1 Bulinus senegalensis) including with S. mansoni, S. bovis, S. haematobium and S. haematobium x S. bovis hybrids. Our findings highlight the spatial-temporal variations of Schistosoma infections in rodents and emphasize the need for fine-scale monitoring over time and space for effective One Health measures and ensuring the sustainability of schistosomiasis control efforts.
Author summary:
Schistosomiasis is a neglected tropical disease of major human and veterinary health concern. To ensure its sustainable control, the role of animal reservoirs that could maintain and spread the disease needs a better understanding. We investigated the spatio-temporal variations of Schistosoma infections in small mammal communities around Lake Guiers, northern Senegal. Small mammal species diversity was relatively low at transmission sites. Most infected rodents were found during or just after the rainy season, a time when older individuals dominate in rodent populations. From a spatial perspective, transmission was highly focalized and infection parameters (prevalence, intensity) highly variable, making it challenging to establish clear patterns. Schistosoma mansoni, responsible for human intestinal schistosomiasis, was the most widespread species found. However, sporadic infections with species of human (S. haematobium) and animal significance (S. bovis), including a case of mixed infections (S. mansoni x S. bovis) in rodents raises concerns about hybridization events that may occur in these hosts. Our findings confirm the role of rodents as reservoir or spill-over hosts for Schistosoma in northern Senegal and suggest that fine scale monitoring of animals at transmission sites could help to ensure the sustainability of schistosomiasis control.
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