Abstract
Many communities in low- and middle-income countries globally lack sustainable, cost-effective and mutually beneficial solutions for infectious disease, food, water and poverty challenges, despite their inherent interdependence1,2,3,4,5,6,7. Here we provide support for the hypothesis that agricultural development and fertilizer use in West Africa increase the burden of the parasitic disease schistosomiasis by fuelling the growth of submerged aquatic vegetation that chokes out water access points and serves as habitat for freshwater snails that transmit Schistosoma parasites to more than 200 million people globally8,9,10. In a cluster randomized controlled trial (ClinicalTrials.gov: NCT03187366) in which we removed invasive submerged vegetation from water points at 8 of 16 villages (that is, clusters), control sites had 1.46 times higher intestinal Schistosoma infection rates in schoolchildren and lower open water access than removal sites. Vegetation removal did not have any detectable long-term adverse effects on local water quality or freshwater biodiversity. In feeding trials, the removed vegetation was as effective as traditional livestock feed but 41 to 179 times cheaper and converting the vegetation to compost provided private crop production and total (public health plus crop production benefits) benefit-to-cost ratios as high as 4.0 and 8.8, respectively. Thus, the approach yielded an economic incentive—with important public health co-benefits—to maintain cleared waterways and return nutrients captured in aquatic plants back to agriculture with promise of breaking poverty–disease traps. To facilitate targeting and scaling of the intervention, we lay the foundation for using remote sensing technology to detect snail habitats. By offering a rare, profitable, win–win approach to addressing food and water access, poverty alleviation, infectious disease control and environmental sustainability, we hope to inspire the interdisciplinary search for planetary health solutions11 to the many and formidable, co-dependent global grand challenges of the twenty-first century.
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Data availability
All the data generated or used for this Article are deposited in Zenodo: https://doi.org/10.5281/zenodo.7765059.
Code availability
All the code used for this Article are deposited in Zenodo: https://doi.org/10.5281/zenodo.7765059.
References
Hotez, P. J. et al. Control of neglected tropical diseases. New Engl. J. Med. 357, 1018–1027 (2007).
Hotez, P. J. Neglected infections of poverty in the United States of America. PLoS Negl.Trop. Dis. 2, e256 (2008).
Ngonghala, C. N. et al. Poverty, disease, and the ecology of complex systems. PLoS Biol. 12, e1001827 (2014).
Barrett, C. B., Carter, M. R. & Chavas, J. The Economics of Poverty Traps (Univ. Chicago Press, 2019).
Lozano, R. et al. Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380, 2095–2128 (2013).
Rohr, J. R. et al. Emerging human infectious diseases and the links to global food production. Nat. Sustain. 2, 445 (2019).
Halstead, N. T. et al. Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts. Nat. Commun. 9, 837 (2018).
Steinmann, P., Keiser, J., Bos, R., Tanner, M. & Utzinger, J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 6, 411–425 (2006).
Gryseels, B., Polman, K., Clerinx, J. & Kestens, L. Human schistosomiasis. Lancet 368, 1106–1118 (2006).
King, C. H. Parasites and poverty: the case of schistosomiasis. Acta Trop. 113, 95–104 (2010).
Whitmee, S. et al. Safeguarding human health in the Anthropocene epoch: report of The Rockefeller Foundation–Lancet Commission on Planetary Health. Lancet 386, 1973–2028 (2015).
FAO, IFAD, UNICEF, WFP & WHO. The State of Food Security and Nutrition in the World: Transforming Food Systems for Food Security, Improved Nutrition and Affordable Healthy Diets for All https://doi.org/10.4060/cb4474en (FAO, 2021).
Collecting and Carrying Water, Burdensome Reality for Women https://www.unwomen.org/en/news/stories/2014/3/collecting-and-carrying-water-burdensome-reality-for-women (UN Women, 2014).
Hoover, C. M. et al. Modelled effects of prawn aquaculture on poverty alleviation and schistosomiasis control. Nat. Sustain. 2, 611–620 (2019).
Haggerty, C. J. et al. Aquatic macrophytes and macroinvertebrate predators affect densities of snail hosts and local production of schistosome cercariae that cause human schistosomiasis. PLoS Negl.Trop. Dis. 14, e0008417 (2020).
Wood, C. L. et al. Precision mapping of snail habitat provides a powerful indicator of human schistosomiasis transmission. Proc. Natl Acad. Sci. USA 116, 23182–23191 (2019).
Underwood, G. J. C., Thomas, J. D. & Baker, J. H. An experimental investigation of interactions in snail–macrophyte–epiphyte systems. Oecologia 91, 587–595 (1992).
Global Invasive Species Database, http://www.iucngisd.org/gisd/species.php?sc=281 (accessed November 2022).
Best, E. P. Effects of nitrogen on the growth and nitrogenous compounds of Ceratophyllum demersum. Aquat. Bot. 8, 197–206 (1980).
Pietro, K. C., Chimney, M. J. & Steinman, A. D. Phosphorus removal by the Ceratophyllum/periphyton complex in a south Florida (USA) freshwater marsh. Ecol. Eng. 27, 290–300 (2006).
Quilliam, R. S. et al. Can macrophyte harvesting from eutrophic water close the loop on nutrient loss from agricultural land? J. Environ. Manage. 152, 210–217 (2015).
Lo, N. C. et al. Impact and cost-effectiveness of snail control to achieve disease control targets for schistosomiasis. Proc. Natl Acad. Sci. USA 115, E584 (2018).
WHO. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. World Health Organ. Tech. Rep. Ser. 912, 57 (2002).
Chu, K. Trials of ecological and chemical measures for the control of Schistosoma haematobium transmission in a Volta Lake village. Bull. World Health Organ. 56, 313 (1978).
Deol, A. K. et al. Schistosomiasis—assessing progress toward the 2020 and 2025 global goals. New Engl. J. Med. 381, 2519–2528 (2019).
Klumpp, R. & Chu, K. Importance of the aquatic weed Ceratophyllum to transmission of Schistosoma haematobium in the Volta Lake, Ghana. Bull. World Health Organ. 58, 791 (1980).
Boelee, E. & Laamrani, H. Environmental control of schistosomiasis through community participation in a Moroccan oasis. Trop. Med. Int. Health 9, 997–1004 (2004).
Garchitorena, A. et al. Disease ecology, health and the environment: a framework to account for ecological and socio-economic drivers in the control of neglected tropical diseases. Phil. Trans. R Soc. B 372, 20160128 (2017).
Liu, Z. Y.-C. et al. Deep learning segmentation of satellite imagery identifies aquatic vegetation associated with snail intermediate hosts of schistosomiasis in Senegal, Africa. Remote Sens. 14, 1345 (2022).
Jones, I. J. et al. Schistosome infection in Senegal is associated with different spatial extents of risk and ecological drivers for Schistosoma haematobium and S. mansoni. PLOS Neglect. Trop. Dis. 15, e0009712 (2021).
Sustainable Development Goals https://sdgs.un.org/goals (United Nations, 2021).
Hopkins, S. R. et al. Evidence gaps and diversity among potential win–win solutions for conservation and human infectious disease control. Lancet Planet. Health 6, e694–e705 (2022).
Leonardi, U. Senegal Land Cover Mapping, Technical Report. http://www.fao.org/fileadmin/user_upload/geospatial/docs/Land_Cover/Senegal_LC/Senegal_LC_Report_1208.pdf (FAO, 2008).
Moher, D. et al. CONSORT 2010 explanation and elaboration: updated guidelines for reporting parallel group randomised trials. Int. J. Surg, 10, 28–55 (2012).
Plouvier, S., Leroy, J. C. & Colette, J. A propos d’une technique simple de filtration des urines dans le diagnostic de la bilharziose urinaire en enquête de masse. Med. Trop. 35, 229–230 (1975).
Katz, N., Chaves, A. & Pellegrino, J. A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni. Rev. Inst. Med. Trop. Sao Paulo 14, 397–400 (1972).
Council for International Organizations of Medical Sciences. International ethical guidelines for biomedical research involving human subjects. Bull. Med. Ethics 182, 17–23 (2002).
Venables, W. N. & Ripley, B. D. Modern Applied Statistics with S 4th edn (Springer, 2002).
Lefcheck, J. S. piecewiseSEM: piecewise structural equation modeling in R for ecology, evolution, and systematics. Methods Ecol. Evol. 7, 6 (2016).
Wickham, H. The split-apply-combine strategy for data analysis. J. Stat. Softw. 40, 1–29 (2011).
Brooks, M. E. et al. glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).
Fox, J. & Weisberg, S. An R Companion to Applied Regression (Sage Publications, 2018).
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2016).
Lenth, R. V. Least-squares means: the R package lsmeans. J. Stat. Softw. 69, 1–33 (2016).
Huang, F. L. Alternatives to logistic regression models in experimental studies. J. Exp. Educ. 90, 213–228 (2022).
Anderson, M. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods (Primer-E, 2008).
Bartoń, K. MuMIn: Multi-modal inference. Model selection and model averaging based on information criteria (AICc and alike). (2019).
Lenth, R. Emmeans: Estimated marginal means, aka least-squares means. R package version 1.4.7. (2020).
Christensen, R. H. B. ordinal: Regression models for ordinal data. R package version 2019.12-10 (2019).
Best, P. Nutrient content of the aquatic macrophytes Elodea canadensis and Ceratophyllum in the course of the year. Hydrobiol. Bull. 10, 15–16 (1976).
Acknowledgements
The authors thank the people of Senegal who invited us into their communities to co-develop the research in this Article. This research was supported by a National Institutes of Health grant (R01GM109499) to J.R.R., J.V.R., S.H.S., G.A.D.L., N.J. and G.R. Additionally, this research was supported by grants from the National Science Foundation (EF-1241889, DEB-2109293, DEB-2017785, DEB-2011179 and ICER-2024383), National Institutes of Health (R01 TW010286), and the Indiana Clinical and Translational Sciences Institute to J.R.R.; the National Institutes of Health (K01AI091864) and the National Science Foundation (EAR-1646708 and EAR-1360330) to J.V.R., and the National Science Foundation (CNH grant no. 1414102), National Institutes of Health (R01 TW010286-01), Stanford GDP SEED (grant no. 1183573-100-GDPAO) and SNAP-NCEAS (working group ‘Ecological levers for health: Advancing a Priority Agenda for Disease Ecology and Planetary Health in the 21st Century’) to S.H.S. and G.A.D.L. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Contributions
J.R.R. conceptualized the experiments, directed the project and analyses, and wrote the majority of the manuscript. C.J.E.H. and A.S. contributed to figure development and statistical analyses, and helped to write sections of the manuscript. C.J.E.H., C.D., C.W., S.B. and R.A.N. performed field sampling, data collection and curation of field data. A.J.C. and I.J.J. provided the drone imagery and helped with some of the fieldwork. C.W. acquired the DigitalGlobe grant for the satellite imagery and conducted the remote sensing analyses. A.J.L. conducted the fertilizer use survey that was funded by D.L.-C. C.B.B. and M.J.D. performed economic analyses and contributed to writing those sections of the manuscript and to general editing. N.J., S.S. and G.R. directed the human sampling. A.T.L. collected human infection samples. A.-M.S. curated the human data. N.J. and M.S. oversaw the livestock feed trials. D.J.C. contributed to the original idea development. J.R.R., C.J.E.H., C.W., A.J.C. and I.J.J. collected the data to compare the quadrat and sweep net sampling protocols. J.R.R., G.A.D.L., N.J., J.V.R., G.R. and S.H.S. developed the grant that funded much of this research. G.A.D.L. and S.H.S. contributed to some of the conceptualization and methods development, site selection and baseline analyses. All co-authors contributed to manuscript editing.
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Extended data figures and tables
Extended Data Fig. 1 Google Earth Engine images of the St. Louis/Richard Toll region of Senegal before (1984–1986) and after (2014–2016) the opening of the Diama Dam.
on August 12, 1986, which was constructed to reduce saltwater intrusion and facilitate irrigation of the region. Note the profound increase in the amount of greenery in the landscape after the opening of the Dam. Image attribution: Esri, HERE, DeLorme, MapmyIndia, © OpenStreetMap contributors, and the GIS user community.
Extended Data Fig. 2 Log-transformed estimated quantity of vegetation removed (kg) for each removal round (1–10) during the study.
Each point represents an independent water access point, the dashed line is the median, and the gray rectangles represent a 95% confidence interval.
Extended Data Fig. 3 Amount and effect of onion rot across urea and compost treatments.
Per11m2 subplots, the (A) ln-transformed kg of onions unaffected by onion rot, (B) proportion of kg of onions with onion rot, and (C) ln-transformed kg of onions with onion rot all as a function of crossed compost and urea fertilizer treatments (shown are marginal means and 95% CI; C: compost, TC: tilled compost, NC: no compost, U: urea, NU: no urea; n = six plots for each of the six treatments, three plots at each of two villages).
Extended Data Fig. 4 Human baseline prevalence versus infection post-treatment.
Bi-variate scatterplots (with 95% confidence bands) of human baseline prevalence at 16 sites sampled in 2016 versus infection post-treatment in 2017 (A) and in 2018 (B).
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This file contains appendices 1–4, which include the Supplementary Methods and Discussion. It also contains Supplementary Tables 1–55 and Supplementary Figs. 1–12.
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Rohr, J.R., Sack, A., Bakhoum, S. et al. A planetary health innovation for disease, food and water challenges in Africa. Nature 619, 782–787 (2023). https://doi.org/10.1038/s41586-023-06313-z
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DOI: https://doi.org/10.1038/s41586-023-06313-z
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