Ayse Ercumen

Coliform Bacteria as Indicators of Diarrheal Risk in Household Drinking Water: Systematic Review and Meta-Analysis

Background Current guidelines recommend the use of Escherichia coli (EC) or thermotolerant (“fecal”) coliforms (FC) as indicators of fecal contamination in drinking water. Despite their broad use as measures of water quality, there remains limited evidence for an association between EC or FC and diarrheal illness: a previous review found no evidence for a link between diarrhea and these indicators in household drinking water. Objectives We conducted a systematic review and meta-analysis to update the results of the previous review with newly available evidence, to explore differences between EC and FC indicators, and to assess the quality of available evidence. Methods We searched major databases using broad terms for household water quality and diarrhea. We extracted study characteristics and relative risks (RR) from relevant studies. We pooled RRs using random effects models with inverse variance weighting, and used standard methods to evaluate heterogeneity and publication bias. Results We identified 20 relevant studies; 14 studies provided extractable results for meta-analysis. When combining all studies, we found no association between EC or FC and diarrhea (RR 1.26 [95% CI: 0.98, 1.63]). When analyzing EC and FC separately, we found evidence for an association between diarrhea and EC (RR: 1.54 [95% CI: 1.37, 1.74]) but not FC (RR: 1.07 [95% CI: 0.79, 1.45]). Across all studies, we identified several elements of study design and reporting (e.g., timing of outcome and exposure measurement, accounting for correlated outcomes) that could be improved upon in future studies that evaluate the association between drinking water contamination and health. Conclusions Our findings, based on a review of the published literature, suggest that these two coliform groups have different associations with diarrhea in household drinking water. Our results support the use of EC as a fecal indicator in household drinking water.

Water distribution system deficiencies and gastrointestinal illness: A systematic review and meta-analysis

Background: Water distribution systems are vulnerable to performance deficiencies that can cause (re)contamination of treated water and plausibly lead to increased risk of gastrointestinal illness (GII) in consumers. Objectives: It is well established that large system disruptions in piped water networks can cause GII outbreaks. We hypothesized that routine network problems can also contribute to background levels of waterborne illness and conducted a systematic review and meta-analysis to assess the impact of distribution system deficiencies on endemic GII. Methods: We reviewed published studies that compared direct tap water consumption to consumption of tap water re-treated at the point of use (POU) and studies of specific system deficiencies such as breach of physical or hydraulic pipe integrity and lack of disinfectant residual. Results: In settings with network malfunction, consumers of tap water versus POU-treated water had increased GII [incidence density ratio (IDR) = 1.34; 95% CI: 1.00, 1.79]. The subset of nonblinded studies showed a significant association between GII and tap water versus POU-treated water consumption (IDR = 1.52; 95% CI: 1.05, 2.20), but there was no association based on studies that blinded participants to their POU water treatment status (IDR = 0.98; 95% CI: 0.90, 1.08). Among studies focusing on specific network deficiencies, GII was associated with temporary water outages (relative risk = 3.26; 95% CI: 1.48, 7.19) as well as chronic outages in intermittently operated distribution systems (odds ratio = 1.61; 95% CI: 1.26, 2.07). Conclusions: Tap water consumption is associated with GII in malfunctioning distribution networks. System deficiencies such as water outages also are associated with increased GII, suggesting a potential health risk for consumers served by piped water networks. Citation: Ercumen A, Gruber JS, Colford JM Jr. 2014. Water distribution system deficiencies and gastrointestinal illness: a systematic review and meta-analysis. Environ Health Perspect 122:651–660; http://dx.doi.org/10.1289/ehp.1306912

Upgrading a Piped Water Supply from Intermittent to Continuous Delivery and Association with Waterborne Illness: A Matched Cohort Study in Urban India

Background Intermittent delivery of piped water can lead to waterborne illness through contamination in the pipelines or during household storage, use of unsafe water sources during intermittencies, and limited water availability for hygiene. We assessed the association between continuous versus intermittent water supply and waterborne diseases, child mortality, and weight for age in Hubli-Dharwad, India. Methods and Findings We conducted a matched cohort study with multivariate matching to identify intermittent and continuous supply areas with comparable characteristics in Hubli-Dharwad. We followed 3,922 households in 16 neighborhoods with children <5 y old, with four longitudinal visits over 15 mo (Nov 2010–Feb 2012) to record caregiver-reported health outcomes (diarrhea, highly credible gastrointestinal illness, bloody diarrhea, typhoid fever, cholera, hepatitis, and deaths of children <2 y old) and, at the final visit, to measure weight for age for children <5 y old. We also collected caregiver-reported data on negative control outcomes (cough/cold and scrapes/bruises) to assess potential bias from residual confounding or differential measurement error. Continuous supply had no significant overall association with diarrhea (prevalence ratio [PR] = 0.93, 95% confidence interval [CI]: 0.83–1.04, p = 0.19), bloody diarrhea (PR = 0.78, 95% CI: 0.60–1.01, p = 0.06), or weight-for-age z-scores (Δz = 0.01, 95% CI: −0.07–0.09, p = 0.79) in children <5 y old. In prespecified subgroup analyses by socioeconomic status, children <5 y old in lower-income continuous supply households had 37% lower prevalence of bloody diarrhea (PR = 0.63, 95% CI: 0.46–0.87, p-value for interaction = 0.03) than lower-income intermittent supply households; in higher-income households, there was no significant association between continuous versus intermittent supply and child diarrheal illnesses. Continuous supply areas also had 42% fewer households with ≥1 reported case of typhoid fever (cumulative incidence ratio [CIR] = 0.58, 95% CI: 0.41–0.78, p = 0.001) than intermittent supply areas. There was no significant association with hepatitis, cholera, or mortality of children <2 y old; however, our results were indicative of lower mortality of children <2 y old (CIR = 0.51, 95% CI: 0.22–1.07, p = 0.10) in continuous supply areas. The major limitations of our study were the potential for unmeasured confounding given the observational design and measurement bias from differential reporting of health symptoms given the nonblinded treatment. However, there was no significant difference in the prevalence of the negative control outcomes between study groups that would suggest undetected confounding or measurement bias. Conclusions Continuous water supply had no significant overall association with diarrheal disease or ponderal growth in children <5 y old in Hubli-Dharwad; this might be due to point-of-use water contamination from continuing household storage and exposure to diarrheagenic pathogens through nonwaterborne routes. Continuous supply was associated with lower prevalence of dysentery in children in low-income households and lower typhoid fever incidence, suggesting that intermittently operated piped water systems are a significant transmission mechanism for Salmonella typhi and dysentery-causing pathogens in this urban population, despite centralized water treatment. Continuous supply was associated with reduced transmission, especially in the poorer higher-risk segments of the population.

Effects of source- versus household contamination of tubewell water on child diarrhea in rural Bangladesh: a randomized controlled trial.

Background Shallow tubewells are the primary drinking water source for most rural Bangladeshis. Fecal contamination has been detected in tubewells, at low concentrations at the source and at higher levels at the point of use. We conducted a randomized controlled trial to assess whether improving the microbiological quality of tubewell drinking water by household water treatment and safe storage would reduce diarrhea in children <2 years in rural Bangladesh. Methods We randomly assigned 1800 households with a child aged 6-18 months (index child) into one of three arms: chlorine plus safe storage, safe storage and control. We followed households with monthly visits for one year to promote the interventions, track their uptake, test participants’ source and stored water for fecal contamination, and record caregiver-reported child diarrhea prevalence (primary outcome). To assess reporting bias, we also collected data on health outcomes that are not expected to be impacted by our interventions. Findings Both interventions had high uptake. Safe storage, alone or combined with chlorination, reduced heavy contamination of stored water. Compared to controls, diarrhea in index children was reduced by 36% in the chlorine plus safe storage arm (prevalence ratio, PR = 0.64, 0.55-0.73) and 31% in the safe storage arm (PR = 0.69, 0.60-0.80), with no difference between the two intervention arms. One limitation of the study was the non-blinded design with self-reported outcomes. However, the prevalence of health outcomes not expected to be impacted by water interventions did not differ between study arms, suggesting minimal reporting bias. Conclusions Safe storage significantly improved drinking water quality at the point of use and reduced child diarrhea in rural Bangladesh. There was no added benefit from combining safe storage with chlorination. Efforts should be undertaken to implement and evaluate long-term efforts for safe water storage in Bangladesh. Trial Registration ClinicalTrials.gov NCT01350063

Brief Report: Negative Controls to Detect Selection Bias and Measurement Bias in Epidemiologic Studies

Supplemental Digital Content is available in the text.

Animal Feces Contribute to Domestic Fecal Contamination: Evidence from E. coli Measured in Water, Hands, Food, Flies, and Soil in Bangladesh

Fecal-oral pathogens are transmitted through complex, environmentally mediated pathways. Sanitation interventions that isolate human feces from the environment may reduce transmission but have shown limited impact on environmental contamination. We conducted a study in rural Bangladesh to (1) quantify domestic fecal contamination in settings with high on-site sanitation coverage; (2) determine how domestic animals affect fecal contamination; and (3) assess how each environmental pathway affects others. We collected water, hand rinse, food, soil, and fly samples from 608 households. We analyzed samples with IDEXX Quantitray for the most probable number (MPN) of E. coli. We detected E. coli in source water (25%), stored water (77%), child hands (43%), food (58%), flies (50%), ponds (97%), and soil (95%). Soil had >120 000 mean MPN E. coli per gram. In compounds with vs without animals, E. coli was higher by 0.54 log10 in soil, 0.40 log10 in stored water and 0.61 log10 in food (p < 0.05). E. coli in stored water and food increased with increasing E. coli in soil, ponds, source water and hands. We provide empirical evidence of fecal transmission in the domestic environment despite on-site sanitation. Animal feces contribute to fecal contamination, and fecal indicator bacteria do not strictly indicate human fecal contamination when animals are present.

Hand- and Object-Mouthing of Rural Bangladeshi Children 3-18 Months Old.

Children are exposed to environmental contaminants by placing contaminated hands or objects in their mouths. We quantified hand- and object-mouthing frequencies of Bangladeshi children and determined if they differ from those of U.S. children to evaluate the appropriateness of applying U.S. exposure models in other socio-cultural contexts. We conducted a five-hour structured observation of the mouthing behaviors of 148 rural Bangladeshi children aged 3–18 months. We modeled mouthing frequencies using 2-parameter Weibull distributions to compare the modeled medians with those of U.S. children. In Bangladesh the median frequency of hand-mouthing was 37.3 contacts/h for children 3–6 months old, 34.4 contacts/h for children 6–12 months old, and 29.7 contacts/h for children 12–18 months old. The median frequency of object-mouthing was 23.1 contacts/h for children 3–6 months old, 29.6 contacts/h for children 6–12 months old, and 15.2 contacts/h for children 12–18 months old. At all ages both hand- and object-mouthing frequencies were higher than those of U.S. children. Mouthing frequencies were not associated with child location (indoor/outdoor). Using hand- and object-mouthing exposure models from U.S. and other high-income countries might not accurately estimate children’s exposure to environmental contaminants via mouthing in low- and middle-income countries.

Acute Illness Among Surfers After Exposure to Seawater in Dry- and Wet-Weather Conditions

Abstract Rainstorms increase levels of fecal indicator bacteria in urban coastal waters, but it is unknown whether exposure to seawater after rainstorms increases rates of acute illness. Our objective was to provide the first estimates of rates of acute illness after seawater exposure during both dry- and wet-weather periods and to determine the relationship between levels of indicator bacteria and illness among surfers, a population with a high potential for exposure after rain. We enrolled 654 surfers in San Diego, California, and followed them longitudinally during the 2013–2014 and 2014–2015 winters (33,377 days of observation, 10,081 surf sessions). We measured daily surf activities and illness symptoms (gastrointestinal illness, sinus infections, ear infections, infected wounds). Compared with no exposure, exposure to seawater during dry weather increased incidence rates of all outcomes (e.g., for earache or infection, adjusted incidence rate ratio (IRR) = 1.86, 95% confidence interval (CI): 1.27, 2.71; for infected wounds, IRR = 3.04, 95% CI: 1.54, 5.98); exposure during wet weather further increased rates (e.g., for earache or infection, IRR = 3.28, 95% CI: 1.95, 5.51; for infected wounds, IRR = 4.96, 95% CI: 2.18, 11.29). Fecal indicator bacteria measured in seawater (Enterococcus species, fecal coliforms, total coliforms) were strongly associated with incident illness only during wet weather. Urban coastal seawater exposure increases the incidence rates of many acute illnesses among surfers, with higher incidence rates after rainstorms.

Negative Control Outcomes: A Tool to Detect Bias in Randomized Trials

Investigators have several design, measurement, and analytic tools to detect and reduce bias in epidemiological studies. One such approach, “negative controls,” has been used on an ad hoc basis for decades. A formal approach has recently been suggested for its use to detect confounding, selection, and measurement bias in epidemiological studies.1,2 Negative controls in epidemiological studies are analogous to negative controls in laboratory experiments, in which investigators test for problems with the experimental method by leaving out an essential ingredient, inactivating the hypothesized active ingredient, or checking for an effect that would be impossible by the hypothesized mechanism.1 A placebo treatment group in a randomized trial is an example of a negative control exposure (leaving out an essential ingredient) that helps remove bias that can result from participant or practitioner knowledge of an individual’s treatment assignment—the placebo treatment is susceptible to the same bias structure as the actual treatment but is causally unrelated to the outcome of interest. Negative control outcomes are conceptually similar but are subtly different because, unlike exposures in a randomized trial, they are not under investigator control. The formal definition of a negative control outcome is one that shares the same potential sources of

Potential sources of bias in the use of Escherichia coli to measure waterborne diarrhoea risk in low-income settings

Escherichia coli is the standard water quality indicator for diarrhoea risk. Yet, the association between E. coli and diarrhoea is inconsistent across studies without a systematic assessment of methodological differences behind this variation. Most studies measure water quality cross‐sectionally with diarrhoea, risking exposure misclassification and reverse causation. Studies use different recall windows for self‐reported diarrhoea; longer periods increase potential outcome misclassification through misrecall. Control of confounding is inconsistent across studies. Additionally, diarrhoea measured in unblinded intervention trials can present courtesy bias. We utilised measurements from a randomised trial of water interventions in Bangladesh to assess how these factors affect the E. coli–diarrhoea association.