Effects of weather extremes on fecal contamination along pathogen transmission pathways in rural Bangladeshi households

BackgroundWeather extremes are predicted to influence pathogen exposure but their effects on specific fecal-oral transmission pathways are not well investigated. We evaluated effects of extreme rain and temperature during different antecedent periods (0-14 days) on E. coli along eight fecal-oral transmission pathways in rural Bangladeshi households. MethodsE. coli was enumerated in mother and child hand rinses, food, stored drinking water, tubewells, flies, ponds, and courtyard soil using IDEXX Quanti-Tray/2000 in nine rounds over 3{middle dot}5 years (n=26,659 samples) and spatiotemporally matched to daily weather data. We used generalized linear models with robust standard errors to estimate E. coli count ratios (ECRs) associated with extreme rain and temperature, defined as >90th percentile of daily values during the study period. FindingsControlling for temperature, extreme rain on the sampling day was associated with increased E. coli in food (ECR=3{middle dot}13 (1{middle dot}63, 5{middle dot}99), p=0{middle dot}001), stored drinking water (ECR=1{middle dot}98 (1{middle dot}36, 2{middle dot}88), p<0{middle dot}0005) and ponds (ECR=3{middle dot}46 (2{middle dot}34, 5{middle dot}11), p<0{middle dot}0005), and reduced E. coli in soil (ECR=0{middle dot}36 (0{middle dot}24, 0{middle dot}53), p<0{middle dot}0005). Extreme rain the day before sampling was associated with reduced E. coli in tubewells (ECR=0{middle dot}10 (0{middle dot}02, 0{middle dot}62), p=0{middle dot}014). Effects were similar for rainfall 1-7 days before sampling and slightly attenuated for rainfall 14 days before sampling. Controlling for rainfall, extreme temperature on the sampling day was associated increased E. coli in stored drinking water (ECR=1{middle dot}49 (1{middle dot}05, 2{middle dot}12), p=0{middle dot}025) and food (ECR=3{middle dot}01 (1{middle dot}51, 6{middle dot}01), p=0{middle dot}002). Rainfall/temperature was not consistently associated with E. coli on hands and flies. InterpretationIn rural Bangladesh, measures to control enteric infections following weather extremes should focus on reducing contamination of drinking water and food stored at home and reducing exposure to surface waters. FundingBill & Melinda Gates Foundation, National Institutes of Health, World Bank. Research in Context Evidence before this studyHigher temperatures and levels of rainfall are associated with increased waterborne and vector-borne disease incidence, including child diarrhea. However, the specific pathways that facilitate increased transmission of diarrheagenic pathogens under these weather conditions have not been well investigated. We searched Google Scholar for articles published since 2000 using the following search terms: ("climate change" OR weather OR temperature OR heatwave OR rainfall OR precipitation) AND (pathogen OR enteropathogen OR "Escherichia coli" OR "E. coli" OR "fecal indicator" OR "fecal contamination") AND (environment OR water OR hands OR food OR soil OR flies). A large body of literature has evaluated the effect of rainfall or temperature on water quality and generally found that higher temperatures and magnitudes of rainfall were associated with higher levels of fecal indicator bacteria, such as Escherichia coli (E. coli), in surface and groundwaters, public and private drinking water sources and drinking water stored at homes. However, studies on the impact of rainfall and temperature on fecal contamination along non-waterborne fecal-oral transmission pathways are limited. Contamination of food stored at home has been linked to storage temperature. We found only one study on hand contamination with respect to weather, which found lower E. coli counts on child hands when daily temperatures were higher but no effect from rain. No studies have simultaneously assessed the effects of weather events on a comprehensive set of fecal-oral transmission pathways, which are typically described with the F-diagram and can include drinking water (at the source or stored), surface waters, caregiver and child hands, food, soil and flies. Added value of this studyWe spatiotemporally matched historical meteorological data to over 26,000 E. coli measurements collected in nine rounds over 3{middle dot}5 years in a randomized controlled trial in rural Bangladesh. E. coli was measured across eight different pathogen transmission pathways in the domestic environment. To our knowledge, this study is the first to utilize a large longitudinal dataset of environmental measurements collected over multiple years to investigate how increased rainfall and temperature affect fecal contamination across the full span of pathways described by the F-diagram. Our findings can help identify fecal-oral transmission pathways that are the most susceptible to extreme weather events and should be prioritized for intervention in their wake, as well as offer guidance on the time windows when interventions should be implemented with respect to weather events to interrupt these pathways in the context of climate change. This study can inform the effective delivery of WASH interventions, supporting climate change adaptation to reduce the enteric disease burden associated with weather extremes. Implications of all the available evidenceExtreme rainfall within two weeks of sampling was associated with increased E. coli contamination in stored food, stored drinking water and ponds, and reduced contamination of tubewell water and courtyard soil. Extreme temperature during the same timeframe was associated with increased contamination of stored food and stored drinking water. These findings illuminate environmental mechanisms behind previously reported increases in diarrheal diseases associated with extreme rainfall and temperature. Our findings suggest that, as extreme weather events become more common with climate change, intervention efforts to control exposure to fecal contamination in rural Bangladesh should prioritize reducing contamination of stored food and drinking water as well as reducing exposure to contaminated surface waters.