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Characterization of Natural and Affected Environments
Do sanitation improvements reduce fecal contamination of water, hands, food, soil and flies? Evidence from a cluster-randomized controlled trial in rural Bangladesh Ayse Ercumen, Amy Pickering, Laura H. Kwong, Andrew Mertens, Benjamin F. Arnold, Jade BenjaminChung, Alan E. Hubbard, Mahfuja Alam, Debashis Sen, Sharmin Islam, Md. Masudur Rahman Khalil, Craig Kullmann, Claire Chase, Rokeya Ahmed, Sarker Masud Parvez, Leanne Unicomb, Mahbubur Rahman, Pavani Ram, Thomas F. Clasen, Stephen P. Luby, and John M. Colford Environ. Sci. Technol., Just Accepted Manuscript • DOI: 10.1021/acs.est.8b02988 • Publication Date (Web): 26 Sep 2018 Downloaded from http://pubs.acs.org on September 27, 2018
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Do sanitation improvements reduce fecal contamination of water, hands, food, soil and flies? Evidence from a cluster-randomized controlled trial in rural Bangladesh Ayse Ercumen1,2*, Amy J. Pickering3, Laura H. Kwong4, Andrew Mertens2, Benjamin F. Arnold2, Jade Benjamin-Chung2, Alan E. Hubbard2, Mahfuja Alam5, Debashis Sen5, Sharmin Islam5, Md. Zahidur Rahman5, Craig Kullmann6, Claire Chase6, Rokeya Ahmed7, Sarker Masud Parvez5, Leanne Unicomb5, Mahbubur Rahman5, Pavani K. Ram8, Thomas Clasen9, Stephen P. Luby10, John M. Colford Jr.2 1. Department of Forestry and Environmental Resources, North Carolina State University, Raleigh, NC, 27695 2. School of Public Health, University of California, Berkeley, CA, 94720 3. Civil and Environmental Engineering, Tufts University, Medford, MA, 02153 4. Civil and Environmental Engineering, Stanford University, Stanford, CA, 94305 5. Infectious Disease Division, International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, 1212, Bangladesh 6. Water Global Practice, World Bank, Washington, DC, 20433 7. Water Global Practice, World Bank, Dhaka, 1207, Bangladesh 8. University at Buffalo, Buffalo, NY, 14214, USA 9. Rollins School of Public Health, Emory University, Atlanta, GA 30322 10. Infectious Diseases & Geographic Medicine, Stanford University, Stanford, CA, 94305 * Corresponding author: Ayse Ercumen Jordan Hall, 2800 Faucette Drive, Raleigh, NC 27695
[email protected] Word count Abstract: 189 (limit 200) Text: 4542 Tables: 1 x 300 = 300 Figures: 300 + 300 + 600 = 1200 Total including tables and figures: 6042 (limit 7000)
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Abstract
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Sanitation improvements have had limited effectiveness in reducing the spread of fecal
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pathogens into the environment. We conducted environmental measurements within a
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randomized controlled trial in Bangladesh that implemented individual and combined
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water treatment, sanitation, handwashing (WSH) and nutrition interventions (WASH
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Benefits, NCT01590095). Following approximately 4 months of intervention, we enrolled
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households in the trial’s control, sanitation and combined WSH arms to assess whether
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sanitation improvements, alone and coupled with water treatment and handwashing,
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reduce fecal contamination in the domestic environment. We quantified fecal indicator
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bacteria in samples of drinking and ambient waters, child hands, food given to young
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children, courtyard soil and flies. In the WSH arm, E. coli prevalence in stored drinking
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water was reduced by 62% (prevalence ratio=0.38 (0.32, 0.44)) and E. coli concentration
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by 1-log (∆log10 = -0.88 (-1.01, -0.75)). The interventions did not reduce E. coli along other
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sampled pathways. Ambient contamination remained high among intervention households.
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Potential reasons include non-community-level sanitation coverage, child open defecation,
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animal fecal sources or naturalized E. coli in the environment. Future studies should
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explore potential threshold effects of different levels of community sanitation coverage on
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environmental contamination.
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Background
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Diarrheal disease, intestinal parasites, and subclinical enteric infections are transmitted
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through environmentally mediated pathways 1,2, which can be interrupted by water,
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sanitation and hygiene interventions. Sanitation as a “primary barrier” isolates fecal matter
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from the environment to prevent the spread of fecal pathogens and reduce fly breeding
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sites. Water treatment and handwashing as “secondary barriers” reduce the transmission
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of pathogens from the environment to new hosts while handwashing also reduces person-
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to-person transmission 3. Water treatment and handwashing have been shown to lower
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fecal contamination of drinking water and hands, respectively, and reduce reported
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diarrhea 4–7. In contrast, sanitation interventions have shown mixed health impact and
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generally no effect on domestic environmental contamination 8–11 . Larger impact can
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potentially be achieved by augmenting sanitation improvements with water treatment and
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handwashing to synergistically interrupt multiple disease transmission pathways.
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Few studies have assessed how water, sanitation and hygiene interventions affect disease
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transmission through pathways other than the conventionally studied routes of drinking
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water and hands 11. In low-income countries, fecal contamination is pervasive on surfaces
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and objects in the domestic environment 12 and ambient waters used for bathing and
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washing dishes 13. Flies carry fecal pathogens 14,15 and can transmit these to stored food 16;
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fly control programs have successfully reduced diarrheal diseases 17,18. Soil is increasingly
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recognized as a reservoir for fecal organisms and has been linked to fecal contamination of
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drinking water, hands and food 19; ingestion of soil by children has been associated with
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environmental enteric dysfunction and stunting 20. Identifying which of these transmission
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pathways are blocked by different interventions elucidates the mechanisms through which
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water, sanitation and hygiene programs improve health and allows broader understanding
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of how findings might generalize to other settings. Without measuring fecal contamination
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in different environmental matrices as a causal intermediate, trials are limited to a “black
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box” understanding, where underlying mechanisms of interventions are unknown and
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investigators can only speculate about reasons for intervention success or failure.
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We collected environmental measurements within a randomized controlled trial in rural
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Bangladesh (WASH Benefits, ClinicalTrials.gov NCT01590095) to assess how sanitation
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improvements, alone and combined with water and handwashing interventions, affect fecal
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contamination along a comprehensive set of environmentally mediated pathways.
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Methods
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Study design
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The WASH Benefits trial was conducted in four districts (Gazipur, Kishoreganj,
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Mymensingh, Tangail) in central rural Bangladesh. Groundwater in parts of Bangladesh
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contains high levels of naturally occurring arsenic and iron 21. Study districts were chosen
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to have low concentrations of these groundwater chemicals because the trial’s chlorine-
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based microbiological water quality intervention was not designed to remove arsenic and
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also because the chlorine demand exerted by iron limits the effectiveness of chlorination 22.
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The areas were also chosen to not have any major water, sanitation and hygiene programs
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that would interfere with study activities.
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The parent WASH Benefits trial enrolled pregnant women with the objective of following
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their birth cohort (referred to as “index children” hereinafter). Field staff screened the
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study area for eligible women and recorded their global positioning system (GPS)
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coordinates. Neighboring groups of eight eligible women were grouped into clusters based
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on their coordinates. Cluster dimensions were chosen such that one field worker could visit
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all cluster participants in one day. A minimum 1-km buffer was enforced between clusters
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to minimize spillovers of intervention effects and/or intervention messages between study
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arms. Every eight adjacent clusters formed a geographic block. An off-site investigator
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(BFA) block-randomized clusters into study arms using a random number generator,
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providing geographically pair-matched randomization. The trial arms included individual
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and combined water, sanitation, handwashing and nutrition interventions and a control
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arm which received no intervention. Details of the trial design have been reported 23. The
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primary outcomes of WASH Benefits were child diarrhea and growth, and additional trial
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outcomes included protozoa and soil-transmitted helminth infections; these have been
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reported separately 24–26. Measures of environmental contamination were pre-specified
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intermediate outcomes 23.
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We conducted an environmental assessment among the control, sanitation and combined
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water, sanitation and handwashing (WSH) arms of the trial (see SI Text S1 and Figure S1
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for details of all environmental assessments nested within WASH Benefits). The sanitation
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intervention included upgrades to concrete-lined double-pit latrines, and provision of child
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potties and scoops for the disposal of human and animal feces. Households in Bangladesh
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are clustered in multi-family compounds. All households in the compound where the
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enrolled women and their newborns lived received latrine upgrades, potties and scoops in
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order to reduce fecal contamination in the shared compound environment. Enrolled
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compounds made up
