Prevalence and distribution of schistosomiasis in human, livestock, and snail populations in northern Senegal: a One Health epidemiological study of a multi-host system
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Date
2020-08
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Elsevier
Abstract
Background Schistosomiasis is a neglected tropical disease of global medical and veterinary importance. As efforts to
eliminate schistosomiasis as a public health problem and interrupt transmission gather momentum, the potential
zoonotic risk posed by livestock Schistosoma species via viable hybridisation in sub-Saharan Africa have been largely
overlooked. We aimed to investigate the prevalence, distribution, and multi-host, multiparasite transmission cycle of
Haematobium group schistosomiasis in Senegal, West Africa.
Methods In this epidemiological study, we carried out systematic surveys in definitive hosts (humans, cattle, sheep,
and goats) and snail intermediate hosts, in 2016–18, in two areas of Northern Senegal: Richard Toll and Lac de Guiers,
where transmission is perennial; and Barkedji and Linguère, where transmission is seasonal. The occurrence and
distribution of Schistosoma species and hybrids were assessed by molecular analyses of parasitological specimens
obtained from the different hosts. Children in the study villages aged 5–17 years and enrolled in school were selected
from school registers. Adults (aged 18–78 years) were self-selecting volunteers. Livestock from the study villages
in both areas were also randomly sampled, as were post-mortem samples from local abattoirs. Additionally,
five malacological surveys of snail intermediate hosts were carried out at each site in open water sources used by the
communities and their animals.
Findings In May to August, 2016, we surveyed 375 children and 20 adults from Richard Toll and Lac de Guiers, and
201 children and 107 adults from Barkedji and Linguère; in October, 2017, to January, 2018, we surveyed 386 children
and 88 adults from Richard Toll and Lac de Guiers, and 323 children and 85 adults from Barkedji and Linguère. In
Richard Toll and Lac de Guiers the prevalence of urogenital schistosomiasis in children was estimated to be 87%
(95% CI 80–95) in 2016 and 88% (82–95) in 2017–18. An estimated 63% (in 2016) and 72% (in 2017–18) of infected
children were shedding Schistosoma haematobium–Schistosoma bovis hybrids. In adults in Richard Toll and Lac de
Guiers, the prevalence of urogenital schistosomiasis was estimated to be 79% (52–97) in 2016 and 41% (30–54)
in 2017–18, with 88% of infected samples containing S haematobium–S bovis hybrids. In Barkedji and Linguère the
prevalence of urogenital schistosomiasis in children was estimated to be 30% (23–38) in 2016 and 42% (35–49)
in 2017–18, with the proportion of infected children found to be shedding S haematobium–S bovis hybrid miracidia
much lower than in Richard Toll and Lac de Guiers (11% in 2016 and 9% in 2017–18). In adults in Barkedji and
Linguère, the prevalence of urogenital schistosomiasis was estimated to be 26% (17–36) in 2016 and 47% (34–60)
in 2017–18, with 10% of infected samples containing S haematobium–S bovis hybrids. The prevalence of S bovis in the
sympatric cattle population of Richard Toll and the Lac de Guiers was 92% (80–99), with S bovis also found in sheep
(estimated prevalence 14% [5–31]) and goats (15% [5–33]). In Barkedji and Linguère the main schistosome species in
livestock was Schistosoma curassoni, with an estimated prevalence of 73% (48–93) in sheep, 84% (61–98) in goats and
8% (2–24) in cattle. S haematobium–S bovis hybrids were not found in livestock. In Richard Toll and Lac de Guiers
35% of infected Bulinus spp snail intermediate hosts were found to be shedding S haematobium–S bovis hybrids
(68% shedding S haematobium; 17% shedding S bovis); however, no snails were found to be shedding S haematobium
hybrids in Barkedji and Linguère (29% shedding S haematobium; 71% shedding S curassoni).
Interpretation Our findings suggest that hybrids originate in humans via zoonotic spillover from livestock populations,
where schistosomiasis is co-endemic. Introgressive hybridisation, evolving host ranges, and wider ecosystem contexts
could affect the transmission dynamics of schistosomiasis and other pathogens, demonstrating the need to consider
control measures within a One Health framework.
Funding Zoonoses and Emerging Livestock Systems programme (UK Biotechnology and Biological Sciences Research
Council, UK Department for International Development, UK Economic and Social Research Council, UK Medical
Research Council, UK Natural Environment Research Council, and UK Defence Science and Technology Laboratory).
Description
The Lancet Planetary Health, 4(8), e330-e342.
Keywords
CEA-AGIR, Université Cheikh Anta Diop, Sénégal, Nicolas D Diouf, Samba D Diop, Lucy Yasenev, Stefano Catalano, Cheikh T Thiam, Alassane Ndiaye, Aidan Emery, Alice Morrell, Muriel Rabone, Momar Ndao, Prof Babacar, David Rollinson, James W Rudge, Mariama Sène, Joanne P Webster
Citation
Léger, E., Borlase, A., Fall, C. B., Diouf, N. D., Diop, S. D., Yasenev, L., ... & Webster, J. P. (2020). Prevalence and distribution of schistosomiasis in human, livestock, and snail populations in northern Senegal: a One Health epidemiological study of a multi-host system. The Lancet Planetary Health, 4(8), e330-e342.