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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Schistosome infection in Senegal is associated with different spatial extents of risk and ecological drivers for Schistosoma haematobium and S. mansoni
Schistosome parasites infect more than 200 million people annually, mostly in sub-Saharan Africa, where people may be co-infected with more than one species of the parasite. Infection risk for any single species is determined, in part, by the distribution of its obligate intermediate host snail. As the World Health Organization reprioritizes snail control to reduce the global burden of schistosomiasis, there is renewed importance in knowing when and where to target those efforts, which could vary by schistosome species. This study estimates factors associated with schistosomiasis risk in 16 villages located in the Senegal River Basin, a region hyperendemic for Schistosoma haematobium and S . mansoni . We first analyzed the spatial distributions of the two schistosomes’ intermediate host snails ( Bulinus spp. and Biomphalaria pfeifferi , respectively) at village water access sites. Then, we separately evaluated the relationships between human S . haematobium and S . mansoni infections and (i) the area of remotely-sensed snail habitat across spatial extents ranging from 1 to 120 m from shorelines, and (ii) water access site size and shape characteristics. We compared the influence of snail habitat across spatial extents because, while snail sampling is traditionally done near shorelines, we hypothesized that snails further from shore also contribute to infection risk. We found that, controlling for demographic variables, human risk for S . haematobium infection was positively correlated with snail habitat when snail habitat was measured over a much greater radius from shore (45 m to 120 m) than usual. S . haematobium risk was also associated with large, open water access sites. However, S . mansoni infection risk was associated with small, sheltered water access sites, and was not positively correlated with snail habitat at any spatial sampling radius. Our findings highlight the need to consider different ecological and environmental factors driving the transmission of each schistosome species in co-endemic landscapes.
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- NSF-PAR ID:
- 10326477
- Editor(s):
- Secor, W. Evan
- Date Published:
- Journal Name:
- PLOS Neglected Tropical Diseases
- Volume:
- 15
- Issue:
- 9
- ISSN:
- 1935-2735
- Page Range / eLocation ID:
- e0009712
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Schistosomiasis is a debilitating parasitic disease of poverty that affects more than 200 million people worldwide, mostly in sub-Saharan Africa, and is clearly associated with the construction of dams and water resource management infrastructure in tropical and subtropical areas. Changes to hydrology and salinity linked to water infrastructure development may create conditions favorable to the aquatic vegetation that is suitable habitat for the intermediate snail hosts of schistosome parasites. With thousands of small and large water reservoirs, irrigation canals, and dams developed or under construction in Africa, it is crucial to accurately assess the spatial distribution of high-risk environments that are habitat for freshwater snail intermediate hosts of schistosomiasis in rapidly changing ecosystems. Yet, standard techniques for monitoring snails are labor-intensive, time-consuming, and provide information limited to the small areas that can be manually sampled. Consequently, in low-income countries where schistosomiasis control is most needed, there are formidable challenges to identifying potential transmission hotspots for targeted medical and environmental interventions. In this study, we developed a new framework to map the spatial distribution of suitable snail habitat across large spatial scales in the Senegal River Basin by integrating satellite data, high-definition, low-cost drone imagery, and an artificial intelligence (AI)-powered computer vision technique called semantic segmentation. A deep learning model (U-Net) was built to automatically analyze high-resolution satellite imagery to produce segmentation maps of aquatic vegetation, with a fast and robust generalized prediction that proved more accurate than a more commonly used random forest approach. Accurate and up-to-date knowledge of areas at highest risk for disease transmission can increase the effectiveness of control interventions by targeting habitat of disease-carrying snails. With the deployment of this new framework, local governments or health actors might better target environmental interventions to where and when they are most needed in an integrated effort to reach the goal of schistosomiasis elimination.more » « less
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Cwiklinski, Krystyna (Ed.)The neglected tropical disease schistosomiasis impacts over 700 million people globally. Schistosoma mansoni , the trematode parasite that causes the most common type of schistosomiasis, requires planorbid pond snails of the genus Biomphalaria to support its larval development and transformation to the cercarial form that can infect humans. A greater understanding of neural signaling systems that are specific to the Biomphalaria intermediate host could lead to novel strategies for parasite or snail control. This study examined a Biomphalaria glabrata neural channel that is gated by the neuropeptide FMRF-NH 2 . The Biomphalaria glabrata FMRF-NH 2 gated sodium channel ( Bgl- FaNaC) amino acid sequence was highly conserved with FaNaCs found in related gastropods, especially the planorbid Planorbella trivolvis (91% sequence identity). In common with the P . trivolvis FaNaC, the B . glabrata channel exhibited a low affinity (EC 50 : 3 x 10 −4 M) and high specificity for the FMRF-NH 2 agonist. Its expression in the central nervous system, detected with immunohistochemistry and in situ hybridization, was widespread, with the protein localized mainly to neuronal fibers and the mRNA confined to cell bodies. Colocalization of the Bgl- FaNaC message with its FMRF-NH 2 agonist precursor occurred in some neurons associated with male mating behavior. At the mRNA level, Bgl- FaNaC expression was decreased at 20 and 35 days post infection (dpi) by S . mansoni . Increased expression of the transcript encoding the FMRF-NH 2 agonist at 35 dpi was proposed to reflect a compensatory response to decreased receptor levels. Altered FMRF-NH 2 signaling could be vital for parasite proliferation in its intermediate host and may therefore present innovative opportunities for snail control.more » « less
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Abstract Agricultural expansion is predicted to increase agrochemical use two to fivefold by 2050 to meet food demand. Experimental evidence suggests that agrochemical pollution could increase snails that transmit schistosomiasis, a disease impacting 250 million people, yet most agrochemicals remain unexamined.
Here we experimentally created >100 natural wetland communities to quantify the relative effects of fertilizer, six insecticides (chlorpyrifos, terbufos, malathion, λ‐cyhalothrin, permethrin and esfenvalerate), and six herbicides (acetochlor, alachlor, metolachlor, atrazine, propazine and simazine) on two snail genera responsible for 90% of global schistosomiasis cases.
We identified four of six insecticides (terbufos, permethrin, chlorpyrifos and esfenvalerate) as high risk for increasing snail biomass by reducing snail predators. Hence, malathion and λ‐cyhalothrin might be useful for improving food production without increasing schistosomiasis. This top‐down effect of insecticides on predators was so strong that the effects of herbicides on schistosomiasis risk were masked in the presence of predators because there were so few snails. In the absence of snail predators, herbicide effects on snails were generally negative by reducing submerged vegetation
Hydrilla verticillata . The exception was that atrazine and acetochlor significantly increased the biomass of infected snails and total snails respectively.Like insecticides, fertilizer had strong positive effects on snail populations. Fertilizer increased both snail habitat (submerged vegetation) and snail food (periphyton), but of these two pathways, the increases in snail habitat resulted in greater snail population growth. Total snail biomass was positively associated with both infected snail biomass and parasite production and thus human infection risk.
Synthesis and applications . Our findings suggest that fertilizers and insecticides generally have consistently higher chances of increasing human schistosomiasis than herbicides in natural communities. Furthermore, our results highlight the need to identify other low risk insecticides, which might help reduce crop pests without increasing snails and thus risk of schistosomiasis.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pntd.0009712
