Predictors of Enteric Pathogens in the Domestic Environment from Human and Animal Sources in Rural Bangladesh

Fuhrmeister, Erica R.; Ercümen, Ayşe; Pickering, Amy J.; Jeanis, Kaitlyn M.; Ahmed, Mahaa; Brown, Sara; Arnold, Benjamin F.; Hubbard, Alan; Alam, Mohammad Murshid; Sen, Debashis; Islam, Sharmin; Kabir, Mir Himayet; Kwong, Laura H.; Islam, Mahfuza; Unicomb, Leanne; Rahman, Mahbubur; Boehm, Alexandria B.; Luby, Stephen P.; Colford, John M.; Nelson, Kara L.

doi:10.1021/acs.est.8b07192

Cited by 56 publications

(65 citation statements)

References 66 publications

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“…The finding that regular interaction with animals may put children at a higher risk of exposure to fecal contamination is consistent with several recent studies examining zoonotic disease transmission in LMICs. 11,45,46 Although the risk was elevated, we find that this exposure is not significantly associated with self-reported child diarrhea in the previous seven days (PR = 2.27; 95% CI: 0.91, 5.67), suggesting that many children are asymptomatic carriers of zoonotic enteric pathogens.…”

Section: Discussionmentioning

confidence: 54%

Determinants of Childhood Zoonotic Enteric Infections in a Semirural Community of Quito, Ecuador

Lowenstein

Vasco

Sarzosa

et al. 2020

The American Journal of Tropical Medicine and Hygiene

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Domestic animals in the household environment have the potential to affect a child's carriage of zoonotic enteric pathogens and risk of diarrhea. This study examines the risk factors associated with pediatric diarrhea and carriage of zoonotic enteric pathogens among children living in communities where smallholder livestock production is prevalent. We conducted an observational study of children younger than 5 years that included the analysis of child (n = 306) and animal (n = 480) fecal samples for Campylobacter spp., atypical enteropathogenic Escherichia coli, Shiga toxin-producing E. coli, Salmonella spp., Yersinia spp., Cryptosporidium parvum, and Giardia lamblia. Among these seven pathogens, Giardia was the most commonly identified pathogen among children and animals in the same household, most of which was found in child-dog pairs. Campylobacter spp. was also relatively common within households, particularly among child-chicken and child-guinea pig pairs. We used multivariable Poisson regression models to assess risk factors associated with a child being positive for at least one zoonotic enteric pathogen or having diarrhea during the last week. Children who interacted with domestic animals-a behavior reported by nearly three-quarters of households owning animals-were at an increased risk of colonization with at least one zoonotic enteric pathogen (prevalence ratio [PR] = 1.56, 95% CI: 1.00-2.42). The risk of diarrhea in the last seven days was elevated but not statistically significant (PR = 2.27, CI: 0.91, 5.67). Interventions that aim to reduce pediatric exposures to enteric pathogens will likely need to be incorporated with approaches that remove animal fecal contamination from the domestic environment and encourage behavior change aimed at reducing children's contact with animal feces through diverse exposure pathways.

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Section: Discussionmentioning

confidence: 54%

Determinants of Childhood Zoonotic Enteric Infections in a Semirural Community of Quito, Ecuador

Lowenstein

Vasco

Sarzosa

et al. 2020

The American Journal of Tropical Medicine and Hygiene

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“…Evidence of soap served as an indicator for hand washing, thus lack of soap suggests reduced hand washing by the household. Handwashing with soap is especially critical in preventing food and water contamination [7] by ruminants [60], can reduce diarrheal disease risk by between 40% and 65% [61,62], and can protect against exposure to enteric zoonoses found in animal waste [63]. Although good hand hygiene is particularly protective at certain critical times [59], self-reported handwashing rates in this study population were only 20% before food preparation, 27% before eating, 20% before feeding children, 42% after cleaning children, and 76% after using the toilet.…”

Section: Discussionmentioning

confidence: 99%

Ruminant Fecal Contamination of Drinking Water Introduced Post-Collection in Rural Kenyan Households

Hamzah

Boehm

Davis

et al. 2020

IJERPH

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In sub-Saharan Africa, many families travel to collect water and store it in their homes for daily use, presenting an opportunity for the introduction of fecal contamination. One stored and one source water sample were each collected from 45 households in rural Kenya. All 90 samples were analyzed for fecal indicator bacteria (E. coli and enterococci) and species-specific contamination using molecular microbial source tracking assays. Human (HF183), avian (GFD), and ruminant (BacR) contamination were detected in 52, two, and four samples, respectively. Stored water samples had elevated enterococci concentrations (p < 0.01, Wilcoxon matched pairs test) and more frequent BacR detection (89% versus 27%, p < 0.01, McNemar's exact test) relative to source water samples. fsQCA (fuzzy set qualitative comparative analysis) was conducted on the subset of households with no source water BacR contamination to highlight combinations of factors associated with the introduction of BacR contamination to stored water supplies. Three combinations were identified: (i) ruminants in the compound, safe water extraction methods, and long storage time, (ii) ruminants, unsafe water extraction methods, and no soap at the household handwashing station, and (iii) long storage time and no soap. This suggests that multiple pathways contribute to the transmission of ruminant fecal contamination in this context, which would have been missed if data were analyzed using standard regression techniques.

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“…For example, one study in Bangladesh showed that animal feces contribute to higher loads of E. coli in soil, water, and food (18). Contributions of animals to E. coli in soil households in rural Bangladesh were further supported by evidence of ruminant-and avian-associated microbial source tracking markers (BacR and avian-GFD, respectively) in soils (20), and an adjunct study to the water, sanitation, and hygiene (WASH) Benefits Trial in rural Bangladesh stressed the importance of animal feces containment (domestic animals were found to be the key contributors to enteric pathogens in household environments) to reduce transmission of pathogens (21). Moreover, increased prevalence and transmission of resistant E. coli variants have also been linked to the use of antimicrobials, which are often unregulated in LMICs (22,23).…”

mentioning

confidence: 89%

High Genomic Diversity and Heterogenous Origins of Pathogenic and Antibiotic-Resistant Escherichia coli in Household Settings Represent a Challenge to Reducing Transmission in Low-Income Settings

Montealegre

Talavera-Rodríguez

Roy

et al. 2020

mSphere

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Escherichia coli is present in multiple hosts and environmental compartments as a normal inhabitant, temporary or persistent colonizer, and as a pathogen. Transmission of E. coli between hosts and with the environment is considered to occur more often in areas with poor sanitation. We performed whole-genome comparative analyses on 60 E. coli isolates from soils and fecal sources (cattle, chickens, and humans) in households in rural Bangladesh. Isolates from household soils were in multiple branches of the reconstructed phylogeny, intermixed with isolates from fecal sources. Pairwise differences between all strain pairs were large (minimum, 189 single nucleotide polymorphisms [SNPs]), suggesting high diversity and heterogeneous origins of the isolates. The presence of multiple virulence and antibiotic resistance genes is indicative of the risk that E. coli from soil and feces represent for the transmission of variants that pose potential harm to people. Analysis of the accessory genomes of the Bangladeshi E. coli relative to E. coli genomes available in NCBI identified a common pool of accessory genes shared among E. coli isolates in this geographic area. Together, these findings indicate that in rural Bangladesh, a high level of E. coli in soil is likely driven by contributions from multiple and diverse E. coli sources (human and animal) that share an accessory gene pool relatively unique to previously published E. coli genomes. Thus, interventions to reduce environmental pathogen or antimicrobial resistance transmission should adopt integrated One Health approaches that consider heterogeneous origins and high diversity to improve effectiveness and reduce prevalence and transmission. IMPORTANCE Escherichia coli is reported in high levels in household soil in low-income settings. When E. coli reaches a soil environment, different mechanisms, including survival, clonal expansion, and genetic exchange, have the potential to either maintain or generate E. coli variants with capabilities of causing harm to people. In this study, we used whole-genome sequencing to identify that E. coli isolates collected from rural Bangladeshi household soils, including pathogenic and antibiotic-resistant variants, are diverse and likely originated from multiple diverse sources. In addition, we observed specialization of the accessory genome of this Bangladeshi E. coli compared to E. coli genomes available in current sequence databases. Thus, to address the high level of pathogenic and antibiotic-resistant E. coli transmission in low-income settings, interventions should focus on addressing the heterogeneous origins and high diversity.

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Predictors of Enteric Pathogens in the Domestic Environment from Human and Animal Sources in Rural Bangladesh

Cited by 56 publications

References 66 publications

Determinants of Childhood Zoonotic Enteric Infections in a Semirural Community of Quito, Ecuador

Determinants of Childhood Zoonotic Enteric Infections in a Semirural Community of Quito, Ecuador

Ruminant Fecal Contamination of Drinking Water Introduced Post-Collection in Rural Kenyan Households

High Genomic Diversity and Heterogenous Origins of Pathogenic and Antibiotic-Resistant Escherichia coli in Household Settings Represent a Challenge to Reducing Transmission in Low-Income Settings

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