Stephen Luby, Postdoctoral Faculty Sponsor
- Age-related changes to environmental exposure: variation in the frequency that young children place hands and objects in their mouths JOURNAL OF EXPOSURE SCIENCE AND ENVIRONMENTAL EPIDEMIOLOGY 2020; 30 (1): 205–16
Effect of Sanitation Improvements on Pathogens and Microbial Source Tracking Markers in the Rural Bangladeshi Household Environment.
Environmental science & technology
Diarrheal illnesses from enteric pathogens are a leading cause of death in children under five in low- and middle-income countries (LMICs). Sanitation is one way to reduce the spread of enteric pathogens in the environment; however, few studies have investigated the effectiveness of sanitation in rural LMICs in reducing pathogens in the environment. In this study, we measured the impact of a sanitation intervention (dual-pit latrines, sani-scoops, child potties delivered as part of a randomized control trial, WASH Benefits) in rural Bangladeshi household compounds by assessing prevalence ratios, differences, and changes in the concentration of pathogen genes and host-specific fecal markers. We found no difference in the prevalence of pathogenic Escherichia coli, norovirus, or Giardia genes in the domestic environment in the sanitation and control arms. The prevalence of the human fecal marker was lower on child hands and the concentration of animal fecal marker was lower on mother hands in the sanitation arm in adjusted models, but these associations were not significant after correcting for multiple comparisons. In the subset of households with ≥10 individuals per compound, the prevalence of enterotoxigenic E. coli genes on child hands was lower in the sanitation arm. Incomplete removal of child and animal feces or the compound (versus community-wide) scale of intervention could explain the limited impacts of improved sanitation.
View details for DOI 10.1021/acs.est.9b04835
View details for PubMedID 32167305
Soil ingestion among young children in rural Bangladesh.
Journal of exposure science & environmental epidemiology
Ingestion of soil and dust is a pathway of children's exposure to several environmental contaminants, including lead, pesticides, and fecal contamination. Empirically based estimates of central tendency for soil consumption by children in high-income countries range from 9 to 135 dry mg/day. Using a Monte Carlo simulation, we modeled the mass of soildirectly and indirectly ingested per day by rural Bangladeshi children and identified the parameters that influence the mass ingested. We combined data from observations of direct and indirect ingestion among children with measurements of soil mass on the children's hands, mother's hands, and objects to quantify soil ingestion/day. Estimated geometric mean soil ingestion was 162 dry mg/day for children 3-5 months, 224 dry mg/day for children 6-11 months, 234 dry mg/day for children 12-23 months, 168 dry mg/day for children 24-35 months, and 178 dry mg/day for children 36-47 months old. Across all age groups, children placing their hands in their mouths accounted for 46-78% of total ingestion and mouthing objects contributed 8-12%. Direct ingestion of soil accounted for nearly 40% of soil ingested among children 6-23 months old. Sensitivity analyses identified that the parameters most affecting the estimates were the load of soil on the child's hand, the frequency of hand-to-mouth contacts while not eating, and, for children 6-23 months old, the frequency of direct soil ingestion. In a rural, low-income setting, children's soil consumption was substantially more than the estimates for children in high-income countries. Further characterizing soil ingestion of children in low-income contexts would improve assessments of the risks they face from soil-associated contaminants.
View details for DOI 10.1038/s41370-019-0177-7
View details for PubMedID 31673039
Age-related changes to environmental exposure: variation in the frequency that young children place hands and objects in their mouths.
Journal of exposure science & environmental epidemiology
Children are exposed to environmental contaminants through direct ingestion of water, food, soil, and feces, and through indirect ingestion due to mouthing hands and objects. We quantified ingestion among 30 rural Bangladeshi children<4 years old, recording every item touched or mouthed during 6-h video observations that occurred annually for 3 years. We calculated the frequency and duration of mouthing and the prevalence of mouth contacts with soil and feces. We compared the mouthing frequency distributions to those from US children to evaluate the appropriateness of applying the US data to the Bangladeshi context. Median hand mouthing frequency was 97-160times/h and object mouthing 23-50times/h among the five age groups assessed. For more than half of the children, >75% of all hand mouthing was associated with eating. The frequency of hand mouthing not related to eating was similar to the frequency of all hand-mouthing among childrenin the US. Object-mouthing frequency was higher among Bangladeshi children compared to US children. There was low intra-child correlation of mouthing frequencies over our longitudinal visits. Our results suggest that children's hand- and object-mouthing vary by geography and culture and that future exposure assessments can be cross-sectional if the goal is to estimate population-level distributions of mouthing frequencies. Of all observations, a child consumed soil in 23% and feces in 1%.
View details for PubMedID 30728484
MODIFYING TOILETS TO MAKE THEM CHILD FRIENDLY IN RURAL BANGLADESH
AMER SOC TROP MED & HYGIENE. 2019: 195
View details for Web of Science ID 000507364502636
Microbiological contamination of young children's hands in rural Bangladesh: Associations with child age and observed hand cleanliness as proxy.
2019; 14 (9): e0222355
BACKGROUND: Hands are a route of transmission for fecal-oral pathogens. This analysis aimed to assess associations between hand E. coli contamination and child age and determine if observed hand cleanliness can serve as a proxy for E. coli contamination on young children's hands.METHODS: Trained field workers collected hand rinse samples from children aged 1-14 months in 584 households in rural Bangladesh and assessed the visual cleanliness of child hands (fingernails, finger pads and palms). Samples were analyzed using the IDEXX most probable number (MPN) methodto enumerate E. coli. We assessed if child age (immobile children aged 1-4 months vs. mobile children aged 5-14 months) is associated with log10 E. coli counts on hands using generalized estimating equations (GEE). We estimated the log10 difference in hand E. coli counts associated with the cleanliness of different hand parts using a multivariable GEE model.We calculated the sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) for dirty fingernails, fingerpads, palms and overall hands (the three observed parts combined) against binary E. coli presence on hands.RESULTS: E. coli was detected on 43% of child hands. Children in the mobile age range had 0.17 log10 MPN higher E. coli on hands than those in the immobile age range (Deltalog10 = 0.17, 95% CI = 0.02, 0.32, p = 0.03). Children with visible dirt particles on finger pads had 0.46 log10 MPN higher E. coli on hands than those with clean finger pads (Deltalog10 = 0.46, 95% CI = 0.05, 0.87, p = 0.03). Dirty fingernails indicated binary E. coli presence with 81% sensitivity and 26% specificity while dirty fingerpads and palms indicated E. coli presence with 29% sensitivity and 75-77% specificity. The PPV was 45-48% and NPV 59-65% for all three types of observations.CONCLUSION: Hand contamination with E. coli was prevalent among young children in rural Bangladesh, with higher levels of contamination among mobile children. Studies should assess if strategies to remove animal feces from the courtyard, provide designated hygienic play spaces for children and deliver targeted messaging to mothers to wipe or wash children's hands after contact with animals and animal feces reduce child hand contamination. Visible hand cleanliness was a poor predictor of E. coli presence on young children's hands so other low-cost field measurements are needed to accurately detect fecal contamination on hands.
View details for DOI 10.1371/journal.pone.0222355
View details for PubMedID 31504064
- Correction to: Age-related changes to environmental exposure: variation in the frequency that young children place hands and objects in their mouths. Journal of exposure science & environmental epidemiology 2019
Predictors of Enteric Pathogens in the Domestic Environment from Human and Animal Sources in Rural Bangladesh.
Environmental science & technology
Fecal indicator organisms are measured to indicate the presence of fecal pollution, yet the association between indicators and pathogens varies by context. The goal of this study was to empirically evaluate the relationships between indicator Escherichia coli, microbial source tracking markers, select enteric pathogen genes, and potential sources of enteric pathogens in 600 rural Bangladeshi households. We measured indicators and pathogen genes in stored drinking water, soil, and on mother and child hands. Additionally, survey and observational data on sanitation and domestic hygiene practices were collected. Log10 concentrations of indicator E. coli were positively associated with the prevalence of pathogenic E. coli genes in all sample types. Given the current need to rely on indicators to assess fecal contamination in the field, it is significant that in this study context indicator E. coli concentrations, measured by IDEXX Colilert-18, provided quantitative information on the presence of pathogenic E. coli in different sample types. There were no significant associations between the human fecal marker (HumM2) and human-specific pathogens in any environmental sample type. There was an increase in the prevalence of Giardia lamblia genes, any E. coli virulence gene, and the specific E. coli virulence genes stx1/2 with every log10 increase in the concentration of the animal fecal marker (BacCow) on mothers' hands. Thus, domestic animals were important contributors to enteric pathogens in these households.
View details for DOI 10.1021/acs.est.8b07192
View details for PubMedID 31356066
Do Sanitation Improvements Reduce Fecal Contamination of Water, Hands, Food, Soil, and Flies? Evidence from a Cluster-Randomized Controlled Trial in Rural Bangladesh
ENVIRONMENTAL SCIENCE & TECHNOLOGY
2018; 52 (21): 12089–97
Sanitation improvements have had limited effectiveness in reducing the spread of fecal pathogens into the environment. We conducted environmental measurements within a randomized controlled trial in Bangladesh that implemented individual and combined water treatment, sanitation, handwashing (WSH) and nutrition interventions (WASH Benefits, NCT01590095). Following approximately 4 months of intervention, we enrolled households in the trial's control, sanitation and combined WSH arms to assess whether sanitation improvements, alone and coupled with water treatment and handwashing, reduce fecal contamination in the domestic environment. We quantified fecal indicator bacteria in samples of drinking and ambient waters, child hands, food given to young children, courtyard soil and flies. In the WSH arm, E. coli prevalence in stored drinking water was reduced by 62% (prevalence ratio=0.38 (0.32, 0.44)) and E. coli concentration by 1-log (log10 = -0.88 (-1.01, -0.75)). The interventions did not reduce E. coli along other sampled pathways. Ambient contamination remained high among intervention households. Potential reasons include non-community-level sanitation coverage, child open defecation, animal fecal sources or naturalized E. coli in the environment. Future studies should explore potential threshold effects of different levels of community sanitation coverage on environmental contamination.
View details for PubMedID 30256095
View details for PubMedCentralID PMC6222553
Where Children Play: Young Child Exposure to Environmental Hazards during Play in Public Areas in a Transitioning Internally Displaced Persons Community in Haiti
INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH
2018; 15 (8)
Globally, gastrointestinal (GI) infections by enteric pathogens are the second-leading cause of morbidity and mortality in children under five years of age (≤5 years). While GI pathogen exposure in households has been rigorously examined, there is little data about young children's exposure in public domains. Moreover, public areas in low-income settings are often used for other waste disposal practices in addition to human feces, such as trash dumping in areas near households. If young children play in public domains, they might be exposed to interrelated and highly concentrated microbial, chemical, and physical hazards. This study performed structured observations at 36 public areas in an internally displaced persons community that has transitioned into a formal settlement in Haiti. We documented how often young children played in public areas and quantified behaviors that might lead to illness and injury. Children ≤5 years played at all public sites, which included infants who played at 47% of sites. Children touched and mouthed plastic, metal and glass trash, food and other objects from the ground, ate soil (geophagia) and drank surface water. They also touched latrines, animals, animal feces and open drainage canals. Hand-to-mouth contact was one of the most common behaviors observed and the rate of contact significantly differed among developmental stages (infants: 18/h, toddlers: 11/h and young children: 9/h), providing evidence that children could ingest trace amounts of animal/human feces on hands that may contain GI pathogens. These findings demonstrate that water, sanitation and hygiene interventions could be more effective if they consider exposure risks to feces in public domains. Furthermore, this research highlights the need for waste-related interventions to address the broader set of civil conditions that create unsafe, toxic and contaminated public environments where young children play.
View details for PubMedID 30081490
- Fecal Indicator Bacteria along Multiple Environmental Transmission Pathways (Water, Hands, Food, Soil, Flies) and Subsequent Child Diarrhea in Rural Bangladesh ENVIRONMENTAL SCIENCE & TECHNOLOGY 2018; 52 (14): 7928–36
Fecal Indicator Bacteria along Multiple Environmental Transmission Pathways (Water, Hands, Food, Soil, Flies) and Subsequent Child Diarrhea in Rural Bangladesh.
Environmental science & technology
Enteric pathogens can be transmitted through multiple environmental pathways, yet little is known about the relative contribution of each pathway to diarrhea risk among children. We aimed to identify fecal transmission pathways in the household environment associated with prospectively measured child diarrhea in rural Bangladesh. We measured the presence and levels of Escherichia coli in tube wells, stored drinking water, pond water, child hand rinses, courtyard soil, flies, and food in 1843 households. Gastrointestinal symptoms among children ages 0-60 months were recorded concurrently at the time of environmental sample collection and again a median of 6 days later. Incident diarrhea (3 or more loose stools in a 24-h period) was positively associated with the concentration of E. coli on child hands measured on the first visit (incidence rate ratio [IRR] = 1.23, 95% CI 1.06, 1.43 for a log10 increase), while other pathways were not associated. In cross-sectional analysis, there were no associations between concurrently measured environmental contamination and diarrhea. Our findings suggest higher levels of E. coli on child hands are strongly associated with subsequent diarrheal illness rates among children in rural Bangladesh.
View details for PubMedID 29902374
Prevalence and Association of Escherichia coli and Diarrheagenic Escherichia coli in Stored Foods for Young Children and Flies Caught in the Same Households in Rural Bangladesh
AMERICAN JOURNAL OF TROPICAL MEDICINE AND HYGIENE
2018; 98 (4): 1031–38
Consumption of contaminated stored food can cause childhood diarrhea. Flies carry enteropathogens, although their contribution to food contamination remains unclear. We investigated the role of flies in contaminating stored food by collecting food and flies from the same households in rural Bangladesh. We selected 182 households with children ≤ 24 months old that had stored foods for later feeding at room temperature for ≥ 3 hours. We collected food samples and captured flies with fly tapes hung by the kitchen. We used the IDEXX Quanti-Tray System (Colilert-18 media; IDEXX Laboratories, Inc., Westbrook, ME) to enumerate Escherichia coli with the most probable number (MPN) method. Escherichia coli-positive IDEXX wells were analyzed by polymerase chain reaction for pathogenic E. coli genes (eae, ial, bfp, ipaH, st, lt, aat, aaiC, stx1, and stx2). Escherichia coli was detected in 61% (111/182) of food samples, with a mean of 1.1 log10 MPN/dry g. Fifteen samples (8%) contained pathogenic E. coli; seven (4%) had enteropathogenic E. coli (EPEC) genes (eae and/or bfp); and 10 (5%) had enteroaggregative E. coli genes (aat and/or aaiC). Of flies captured in 68 (37%) households, E. coli was detected in 41 (60%, mean 2.9 log10 MPN/fly), and one fly (1%) had an EPEC gene (eae). For paired fly-food samples, each log10 MPN E. coli increase in flies was associated with a 0.31 log10 MPN E. coli increase in stored food (95% confidence interval: 0.07, 0.55). In rural Bangladesh, flies possibly a likely route for fecal contamination of stored food. Controlling fly populations may reduce contamination of food stored for young children.
View details for PubMedID 29436348
View details for PubMedCentralID PMC5928814
Quantifying human-environment interactions using videography in the context of infectious disease transmission
2018; 13 (1): 195–97
Quantitative data on human-environment interactions are needed to fully understand infectious disease transmission processes and conduct accurate risk assessments. Interaction events occur during an individual's movement through, and contact with, the environment, and can be quantified using diverse methodologies. Methods that utilize videography, coupled with specialized software, can provide a permanent record of events, collect detailed interactions in high resolution, be reviewed for accuracy, capture events difficult to observe in real-time, and gather multiple concurrent phenomena. In the accompanying video, the use of specialized software to capture humanenvironment interactions for human exposure and disease transmission is highlighted. Use of videography, combined with specialized software, allows for the collection of accurate quantitative representations of human-environment interactions in high resolution. Two specialized programs include the Virtual Timing Device for the Personal Computer, which collects sequential microlevel activity time series of contact events and interactions, and LiveTrak, which is optimized to facilitate annotation of events in real-time. Opportunities to annotate behaviors at high resolution using these tools are promising, permitting detailed records that can be summarized to gain information on infectious disease transmission and incorporated into more complex models of human exposure and risk.
View details for DOI 10.4081/gh.2018.631
View details for Web of Science ID 000442360600024
View details for PubMedID 29772893
Animal Feces Contribute to Domestic Fecal Contamination: Evidence from E-coli Measured in Water, Hands, Food, Flies, and Soil in Bangladesh
ENVIRONMENTAL SCIENCE & TECHNOLOGY
2017; 51 (15): 8725–34
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.
View details for PubMedID 28686435
View details for PubMedCentralID PMC5541329
Detecting and enumerating soil-transmitted helminth eggs in soil: New method development and results from field testing in Kenya and Bangladesh.
PLoS neglected tropical diseases
2017; 11 (4)
Globally, about 1.5 billion people are infected with at least one species of soil-transmitted helminth (STH). Soil is a critical environmental reservoir of STH, yet there is no standard method for detecting STH eggs in soil. We developed a field method for enumerating STH eggs in soil and tested the method in Bangladesh and Kenya. The US Environmental Protection Agency (EPA) method for enumerating Ascaris eggs in biosolids was modified through a series of recovery efficiency experiments; we seeded soil samples with a known number of Ascaris suum eggs and assessed the effect of protocol modifications on egg recovery. We found the use of 1% 7X as a surfactant compared to 0.1% Tween 80 significantly improved recovery efficiency (two-sided t-test, t = 5.03, p = 0.007) while other protocol modifications-including different agitation and flotation methods-did not have a significant impact. Soil texture affected the egg recovery efficiency; sandy samples resulted in higher recovery compared to loamy samples processed using the same method (two-sided t-test, t = 2.56, p = 0.083). We documented a recovery efficiency of 73% for the final improved method using loamy soil in the lab. To field test the improved method, we processed soil samples from 100 households in Bangladesh and 100 households in Kenya from June to November 2015. The prevalence of any STH (Ascaris, Trichuris or hookworm) egg in soil was 78% in Bangladesh and 37% in Kenya. The median concentration of STH eggs in soil in positive samples was 0.59 eggs/g dry soil in Bangladesh and 0.15 eggs/g dry soil in Kenya. The prevalence of STH eggs in soil was significantly higher in Bangladesh than Kenya (chi-square, χ2 = 34.39, p < 0.001) as was the concentration (Mann-Whitney, z = 7.10, p < 0.001). This new method allows for detecting STH eggs in soil in low-resource settings and could be used for standardizing soil STH detection globally.
View details for DOI 10.1371/journal.pntd.0005522
View details for PubMedID 28379956
Escherichia coli contamination of child complementary foods and association with domestic hygiene in rural Bangladesh.
Tropical medicine & international health
To determine the frequency and concentration of Escherichia coli in child complementary food and its association with domestic hygiene practices in rural Bangladesh.A total of 608 households with children <2 years were enrolled. We collected stored complementary food samples, performed spot checks on domestic hygiene and measured ambient temperature in the food storage area. Food samples were analysed using the IDEXX most probable number (MPN) method with Colilert-18 media to enumerate E. coli. We calculated adjusted prevalence ratios (APR) to assess the relationship between E. coli and domestic hygiene practices using modified Poisson regression, adjusting for clustering and confounders.Fifty-eight percentage of stored complementary food was contaminated with E. coli, and high levels of contamination (≥100 MPN/dry g food) were found in 12% of samples. High levels of food contamination were more prevalent in compounds where the food was stored uncovered (APR: 2.0, 95% CI: 1.2-3.2), transferred from the storage pot to the serving dish using hands (APR: 2.0, 95% CI: 1.3-3.2) or stored for >4 h (APR: 2.5, 95% CI: 1.5, 4.2), in compounds where water was unavailable in the food preparation area (APR: 2.6, 95% CI: 1.6, 4.2), where ≥1 fly was captured in the food preparation area (APR: 1.6, 95% CI: 1.0, 2.6), or where the ambient temperature was high (>25-40 °C) in the food storage area (APR: 2.7, 95% CI: 1.5, 4.4).Interventions to keep stored food covered and ensure water availability in the food preparation area would be expected to reduce faecal contamination of complementary foods.
View details for DOI 10.1111/tmi.12849
View details for PubMedID 28164415
Hand- and Object-Mouthing of Rural Bangladeshi Children 3-18 Months Old
INTERNATIONAL JOURNAL OF ENVIRONMENTAL RESEARCH AND PUBLIC HEALTH
2016; 13 (6)
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.
View details for DOI 10.3390/ijerph13060563
View details for Web of Science ID 000378860100042
View details for PubMedID 27271651
View details for PubMedCentralID PMC4924020