Epidemiology of schistosomiasis in The Gambia: from human infections to intermediate snail host distribution and genetic diversity

Background Urogenital schistosomiasis is endemic in the eastern regions (Central River and Upper River Regions) of The Gambia, with occasional reports of intestinal schistosomiasis. Following the London Declaration for schistosomiasis control/elimination in 2012, The Gambia initiated a national schistosomiasis control programme. However, a lack of comprehensive and current information on the epidemiology of schistosomiasis in the country presents a major challenge for the implementation of the control programme. This study investigated the epidemiology of schistosomiasis in The Gambia, from human infections to intermediate snail host distribution and genetic diversity, to generate novel information required for the control of schistosomiasis in the country. Methods/Principal findings To assess prevalence and risk factors of schistosomiasis, we used data from a previous study involving 40 primary schools from 4 regions of The Gambia: North Bank Region (NBR), Lower River Region (LRR), Central River Region (CRR) and Upper River Region (URR). We extracted unpublished data generated by this previous study and utilised it in this PhD research for epidemiological analysis of schistosomiasis in The Gambia. Urogenital schistosomiasis had an overall prevalence of 10.2% while intestinal schistosomiasis had a prevalence of 0.3% among the sampled school children. Prevalence of urogenital schistosomiasis was highest in CRR (27.6%), followed by URR (12.0%), then LRR (0.6%), and NBR (0.0%). Intestinal schistosomiasis was observed in only CRR and URR. Blood in urine (haematuria) was significantly associated with presence of S. haematobium eggs in urine. Boys had higher infection rate for S. haematobium compared to girls and being a male was a risk factor of S. haematobium infection. Malacological surveys were conducted in all 5 regions of The Gambia: Western Region (WR), North Bank Region (NBR), Lower River Region (LRR), Central River Region (CRR) and Upper River Region (URR). Field collected snails were identified morphologically and screened for schistosome infections using molecular techniques. While three species of Bulinus were collected, no Biomphalaria snails were found in any of the sites sampled. Bulinus senegalensis was the most common species, found mostly in seasonal pools while Bulinus forskalii and Bulinus truncatus were observed to thrive in permanent habitats. CRR had the highest abundance of Bulinus snails, followed by URR among the regions. Bulinus senegalensis was found infected with both S. haematobium and S. bovis, while B. forskalii and B. truncatus had only S. bovis infection. While the human parasite S. haematobium was restricted to just four sites, the livestock parasite S. bovis had a much more widespread geographical distribution across both CRR and URR. We characterise the genetic structure of field-collected Bulinus species in relation to schistosome infection using the mitochondrial cytochrome oxidase subunit 1 (cox1) and the nuclear internal transcribed spacer 2 (ITS-2) genes. B. senegalensis had a relatively low genetic diversity. There was a pattern in the distribution of B. senegalensis haplotypes with some shared haplotypes restricted to only certain parts and regions of the country while some were found broadly across multiple regions of the country. High genetic variation with a clear haplotype structuring was observed in B. forskalii. More haplotype sharing and homogeneity was observed in B. forskalii from URR compared to B. forskalii from CRR. B. truncatus had a relatively low genetic diversity with less haplotype sharing between populations. No association was observed between genetic diversity and schistosome infection for any of the three Bulinus species. We however found a significant association between two B. senegalensis genotypes (haplotypes) and S. bovis infection. Conclusions This new information on the epidemiology of schistosomiasis in humans and the distribution of intermediate snail hosts in The Gambia will be vital in establishing and guiding an integrated control approach for schistosomiasis in the country. B. senegalensis genotypes associated with S. bovis infection might pose an increased risk of transmission in areas they occur. Future studies should genetically characterise schistosome parasites from humans and snails, and investigate S. haematobium hybrids in The Gambia