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. 2019 Nov 12;116(46):23182-23191.
doi: 10.1073/pnas.1903698116. Epub 2019 Oct 28.

Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission

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Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission

Chelsea L Wood et al. Proc Natl Acad Sci U S A. .

Abstract

Recently, the World Health Organization recognized that efforts to interrupt schistosomiasis transmission through mass drug administration have been ineffective in some regions; one of their new recommended strategies for global schistosomiasis control emphasizes targeting the freshwater snails that transmit schistosome parasites. We sought to identify robust indicators that would enable precision targeting of these snails. At the site of the world's largest recorded schistosomiasis epidemic-the Lower Senegal River Basin in Senegal-intensive sampling revealed positive relationships between intermediate host snails (abundance, density, and prevalence) and human urogenital schistosomiasis reinfection (prevalence and intensity in schoolchildren after drug administration). However, we also found that snail distributions were so patchy in space and time that obtaining useful data required effort that exceeds what is feasible in standard monitoring and control campaigns. Instead, we identified several environmental proxies that were more effective than snail variables for predicting human infection: the area covered by suitable snail habitat (i.e., floating, nonemergent vegetation), the percent cover by suitable snail habitat, and size of the water contact area. Unlike snail surveys, which require hundreds of person-hours per site to conduct, habitat coverage and site area can be quickly estimated with drone or satellite imagery. This, in turn, makes possible large-scale, high-resolution estimation of human urogenital schistosomiasis risk to support targeting of both mass drug administration and snail control efforts.

Keywords: bilharzia; ecological levers for infectious disease control; snail control; spatial ecology; urogenital schistosomiasis.

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Conflict of interest statement

The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
(A–C) Conceptual diagram. (A) Snail density/abundance may not be correlated with human schistosomiasis cases if snails are ephemeral and patchy and therefore difficult to quantify without sampling that is intensive in space and time. (B) If the presence of suitable snail habitat is both stable in space and time and an effective predictor of the presence of snails, (C) it might provide a better indicator of human schistosomiasis cases than would direct counts of snails. Some environmental predictors of the presence of suitable snail habitat are easily observable by satellite or drones; for example, see (D) aerial images taken by drone for representative small-area (Merina Gewel 1) and large-area (Syer 1) sites.
Fig. 2.
Fig. 2.
Nonemergent vegetation is associated with human urogenital schistosomiasis risk at quadrat (A–C), water contact site (D), and village (E) scales. (A–C) Partial response of predicted snail count to 3 species of nonemergent vegetation: Ceratophyllum spp., Ludwigia spp., and Potamogeton spp. (SI Appendix, Table S6). The partial response of expected snail count (i.e., the product of encounter probability and expected nonzero count) was predicted across the range of each covariate while holding all other covariates at zero, instead of interpreting parameter estimates between model components (as recommended by ref. 65). Images of plant species courtesy of Danielle Claar (University of Washington, Seattle, WA). (D) The total number of B. truncatus/globosus snail clusters per site increased with area of nonemergent vegetation. The dotted line shows the best-fitting Poisson GLM (SI Appendix, Text S6). Points are jittered slightly to aid visualization. (E) Prediction plot for males in the top logistic GLMM by BIC. The likelihood of urogenital schistosomiasis infection increased with area of nonemergent vegetation at both river (open circle) and lake (closed circle) villages. Area of nonemergent vegetation per village was calculated as a weighted average among water contact sites within each village, and was natural log-transformed and scaled. Shown are values for villages in each of the 2 y of sampling (2016 to 2018).
Fig. 3.
Fig. 3.
Results of (A) logistic GLMM (prevalence) and (B) negative binomial GLMM (egg count) aiming to identify habitat-related, snail–habitat, and snail predictors of human urogenital schistosomiasis burden. All models within 10 ∆BIC of the top model are shown here. Models are numbered by their BIC rank and are described in detail in SI Appendix, Tables S11 and S12. An odds or incidence rate ratio >1 indicates the predictor is associated with increased risk or burden, and an odds or incidence rate ratio <1 indicates the predictor is associated with decreased risk or infection burden. Error bars indicate 95% confidence intervals.

References

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