Human Colonization with Extended-Spectrum Beta-Lactamase-Producing E. coli in Relation to Animal and Environmental Exposures in Bangladesh: An Observational One Health Study

Abstract

Background: Human exposure to intensively farmed livestock is a potential risk for transmission of antibiotic-resistant bacteria (ARB) but few studies have assessed the relative role of animal vs. environmental sources of ARB in low-resource community settings. Objectives: We conducted an observational study to compare ARB colonization and antibiotic-resistant gene prevalence and abundance in humans with high or low exposure to poultry in rural households, commercial poultry farms, and urban markets in Bangladesh. Methods: Extended-spectrum β-lactamase (ESBL)-producing and carbapenem-resistant E. coli were quantified in feces from adults with high or low poultry exposure (n=100, respectively), poultry (n=200), drinking water (n=120), and wastewater (n=120) from 40 rural households, 40 poultry farms, and 40 urban markets. Results: ESBL-producing E. coli (ESBL-EC) prevalence was 67.5% (95% CI: 61.0, 74.0) in samples from adults, 68.0% (95% CI: 61.5, 74.5) in samples from poultry, and 92.5% (95% CI: 87.7, 97.3) in wastewater samples. Carbapenem-resistant E. coli prevalence was high in market wastewaters [30% (95% CI: 15.0, 45.0)] but low in humans (1%) and poultry (1%). Human, poultry, and wastewater isolates shared common resistance genes: blaCTX-M-1, qnr, and blaTEM. Human colonization was not significantly associated with exposure to poultry or setting (rural, farm, or market). Ninety-five percent of commercial poultry farms routinely administered antibiotics. Susceptibility tests were significantly different in household vs. farm and market poultry isolates for four of seven antibiotic classes. In human isolates, there were no differences except aminoglycoside resistance (16.4% high vs. 4.4% low exposure, p=0.02). Urban market wastewaters and poultry samples had significantly higher concentrations of ESBL-EC (p<0.001) and blaCTX-M-1 (p<0.001) compared with samples from farms and rural households. Discussion: ESBL-EC colonization was high in humans but not significantly associated with exposure to poultry. Bidirectional transmission of antibiotic resistance is likely between humans, poultry, and the environment in these community settings, underlining the importance of One Health mitigation strategies.