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Background: Schistosomiasis is an emerging disease associated with changes to the environment that have increased human contact rates with disease-causing parasites, flatworms that are released from freshwater snails. For example, schistosomiasis remains a major public health problem in Northern Senegal, where prevalence in schoolchildren often reaches 90%. Aim: This study focuses on the impact of seasonality on the risk of human exposure (RHE) to Schistosoma mansoni, defined as the total number of cercariae (the free-living life stage that infects humans) shed from all Biomphalaria pfeifferi snails collected at a site using standardized methods. We focus on RHE because it is rarely quantified and a recent study demonstrated that snails stop shedding cercariae when snail densities increase and thus per capita snail resources become limited [2], suggesting that densities of snails might not be directly proportional to RHE to schistosomes. Method: We sampled four water access points in three villages every other week during the early (Dry1) and later dry seasons (Dry2) and the rainy season, quantifying the abundance of infected and non-infected snail intermediate hosts, cercariae released per infected snail, and water chemistry. We used simple and multiple linear regressions to assess how seasonality and environmental parameters affect non-infected and infected snail abundance and RHE. Results: Although RHE was found across all seasons, the abundance of infected and non-infected snail intermediate hosts and cercariae, as well as prevalence (23.71%), were all highest in the rainy season. In the rainy season, RHE was positively associated with the density of snail hosts and their periphyton food resource. Conclusion: Although previous studies have examined the influence of seasonality on snail densities, few studies have explored the effects of seasonality on cercarial densities, which is the primary source of infection to humans. Our study demonstrates that cercarial densities are greater in the rainy season than in the early or late dry seasons. Given that cercarial densities directly pose risk of infection to humans, unlike non-infected or infected snails, these finding should help to inform decision making and schistosomiasis control efforts in West Africa.
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Transmission potential of human schistosomes can be driven by resource competition among snail intermediate hosts
Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.
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- PAR ID:
- 10326479
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 119
- Issue:
- 6
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2116512119
