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Ecotoxicology and Human Environmental Health
Fecal indicator bacteria along multiple environmental transmission pathways (water, hands, food, soil, flies) and subsequent child diarrhea in rural Bangladesh Amy J Pickering, Ayse Ercumen, Benjamin F. Arnold, Laura H. Kwong, Sarker Masud Parvez, Mahfuja Alam, Debashis Sen, Sharmin Islam, Craig Kullmann, Claire Chase, Rokeya Ahmed, Leanne Unicomb, John M. Colford, and Stephen P. Luby Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b00928 • Publication Date (Web): 14 Jun 2018 Downloaded from http://pubs.acs.org on June 18, 2018
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Fecal indicator bacteria along multiple environmental transmission pathways
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(water, hands, food, soil, flies) and subsequent child diarrhea in rural
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Bangladesh
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Amy J. Pickering*1,2, Ayse Ercumen*3,4, Benjamin F. Arnold3, Laura H. Kwong4, Sarker
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Masud Parvez5, Mahfuja Alam5, Debashis Sen5, Sharmin Islam5, Craig Kullmann6,
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Claire Chase6, Rokeya Ahmed7, Leanne Unicomb5, John M. Colford Jr.3, Stephen P.
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Luby1
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*Co-primary author with equal contribution
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1. Woods Institute for the Environment, Stanford University, Stanford, CA, USA
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2. Civil and Environmental Engineering, Tufts University, Medford, MA, USA
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3. Division of Epidemiology and Biostatistics, School of Public Health,
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University of California, Berkeley, CA, USA 4. Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC, USA
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5. Civil and Environmental Engineering, Stanford University, Stanford, CA, USA
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6. Infectious Disease Division, icddr,b, Bangladesh
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7. Water Global Practice, World Bank, Washington DC, USA
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8. Water Global Practice, World Bank, Dhaka, Bangladesh
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Corresponding author: Amy J. Pickering, Science and Engineering Complex, 200
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College Ave, Tufts University, Medford, MA, 02155, email:
[email protected],
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phone: 617-627-5163
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Running title: Fecal transmission pathways and child diarrhea
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Acknowledgements: This study was financially supported by the World Bank and by
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grant OPPGD759 from the Bill and Melinda Gates Foundation to the University of
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California at Berkeley. icddr,b is grateful to the Governments of Bangladesh, Canada,
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Sweden and the UK for providing core or unrestricted support. We thank the study
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participants and excellent field staff that made this study possible.
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Abstract
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Enteric pathogens can be transmitted through multiple environmental pathways,
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yet little is known about the relative contribution of each pathway to diarrhea risk
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among children. We aimed to identify fecal transmission pathways in the household
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environment associated with prospectively measured child diarrhea in rural
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Bangladesh. We measured the presence and levels of E. coli in tubewells, stored
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drinking water, pond water, child hand rinses, courtyard soil, flies, and food in 1843
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households. Gastrointestinal symptoms among children ages 0-60 months were
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recorded concurrently at the time of environmental sample collection and again a
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median of 6 days later. Incident diarrhea (3 or more loose stools in a 24-hr period)
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was positively associated with the concentration of E. coli on child hands measured
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on the first visit (incidence rate ratio [IRR]=1.23, 95% CI 1.06, 1.43 for a log10
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increase), while other pathways were not associated. In cross-sectional analysis,
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there were no associations between concurrently measured environmental
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contamination and diarrhea. Our findings suggest higher levels of E. coli on child
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hands are strongly associated with subsequent diarrheal illness rates among
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children in rural Bangladesh.
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Introduction
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Diarrhea is a leading cause of global mortality, causing over 1 million deaths in the
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year 2016.1 The morbidity burden of diarrhea is also substantial: in 2010 there were
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an estimated 1.7 billion episodes of diarrhea.2 Diarrheal pathogens are transmitted
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along multiple environmental pathways, traditionally conceptualized as the “five-
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Fs”: fluids (water), fingers (hands), food, fields (soil), and flies.3,4 Fecal indicator
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bacteria and some enteric pathogens have been measured in source water,
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environmental waters, stored drinking water, on child and caregiver hands, in
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stored food, in soil, and on flies in low-income countries.5,6 However, there is limited
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evidence on which of these pathways are the most important for transmission of
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diarrhea among young children.4,7,8
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Additionally, most previous studies have used cross-sectional associations between
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levels of fecal contamination in the environment and concurrent diarrhea
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prevalence. For example, the association between fecal contamination levels in
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stored drinking water and concurrent diarrhea has been extensively studied, with
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equivocal results.9,10 One study in Tanzania found that levels of hand fecal
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contamination was a stronger predictor of concurrent diarrheal illness within a
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household than fecal contamination levels in stored drinking water.11 Another study
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in Tanzania found that pathogenic E. coli in stored drinking water was associated
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with a decrease in the odds of concurrent caregiver-reported diarrhea.12 Cross-
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sectional associations are difficult to interpret because the fecal contamination
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measured in an exposure pathway could have caused the diarrhea, or been caused
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by the diarrhea, or influenced by human behaviors elicited in response to the illness
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(e.g. treatment of water for sick individuals).
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The few studies that have prospectively examined fecal contamination along an
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exposure pathway in a low-income country and diarrhea have focused on drinking
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water. Luby et al. found that contaminated stored drinking water was associated
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with diarrhea measured 3-100 days later in rural Bangladesh.13 Also in rural
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Bangladesh, Ercumen et al. reported that prospective measurement yielded a
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stronger association between E. coli in stored drinking water and diarrhea than
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cross-sectional measurement.14 Neither study measured other fecal transmission
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pathways.
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Our objective for this study was to assess fecal contamination along multiple
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transmission pathways (including drinking water, ambient waters, hands, food, soil,
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and flies), to better understand their contribution to incident child diarrhea in rural
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Bangladesh. Diarrheal pathogen transmission pathways are likely heterogeneous
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across different settings; however, studying the relative risk of diarrhea from
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exposure to multiple fecal transmission pathways in this setting could provide
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useful insight into child diarrheal pathogen exposure in similar settings. We also
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examined how a prospective analysis with incident episodes measured after
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exposure compared with cross-sectional analysis of environmental fecal
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contamination and concurrently measured diarrhea prevalence.
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Methods
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Study design
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The data collection for this study was nested within the WASH Benefits trial in rural
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Bangladesh, a multi-year randomized controlled trial of water, sanitation, hygiene
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and nutrition interventions.15 Compounds (extended family groups of 1 or more
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households sharing a courtyard) were eligible for participation in the WASH
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Benefits trial if they had at least one pregnant woman in her first or second
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trimester who did not plan to move in the following 24 months. There were seven
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arms in the WASH Benefits trial; this substudy only included households from the
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control, sanitation, and combined water, sanitation, and hygiene (WSH) arms. These
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arms were selected to allow for analysis of the effect of the sanitation and combined
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WSH interventions on fecal contamination levels, which will be reported in a
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separate manuscript. The WASH Benefits trial targeted enrolling 720 households in
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each intervention arm. Study participants provided written informed consent.
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Human subjects approval was obtained from the International Centre for Diarrhoeal
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Diseases Research, Bangladesh (icddr,b) (PR-11063), University of California,
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Berkeley (2011-09-3652), and Stanford University (25863).
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Data collection for this substudy occurred during the first year of the trial after
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interventions were delivered and extended from July 2013 through March 2014,
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spanning both the rainy season (Jul-Oct) and dry season (Nov-Mar). We collected
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data through two successive visits to each study household. Samples from the
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household environment were collected during the first visit and analyzed for fecal
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indicator bacteria levels. Caregiver-reported gastrointestinal illness symptoms in
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children
