Reduced Antibacterial Drug Resistance and <i>bla</i> _CTX-M β-Lactamase Gene Carriage in Cattle-Associated Escherichia coli at Low Temperatures, at Sites Dominated by Older Animals, and on Pastureland: Implications for Surveillance

Abstract

Little is known about the drivers of critically important antibacterial resistance in species with zoonotic potential present on farms (e.g., CTX-M β-lactamase-positive <i>Escherichia coli</i>). We collected samples monthly between January 2017 and December 2018 on 53 dairy farms in South West England, along with data for 610 variables concerning antibacterial usage, management practices, and meteorological factors. We detected <i>E. coli</i> resistant to amoxicillin, ciprofloxacin, streptomycin, and tetracycline in 2,754/4,145 (66%), 263/4,145 (6%), 1,475/4,145 (36%), and 2,874/4,145 (69%), respectively, of samples from fecally contaminated on-farm and near-farm sites. <i>E. coli</i> positive for <i>bla</i>_CTX-M were detected in 224/4,145 (5.4%) of samples. Multilevel, multivariable logistic regression showed antibacterial dry cow therapeutic choice (including use of cefquinome or framycetin) to be associated with higher odds of <i>bla</i>_CTX-M positivity. Low average monthly ambient temperature was associated with lower odds of <i>bla</i>_CTX-M<i>E. coli</i> positivity in samples and with lower odds of finding <i>E. coli</i> resistant to each of the four test antibacterials. This was in addition to the effect of temperature on total <i>E. coli</i> density. Furthermore, samples collected close to calves had higher odds of having <i>E. coli</i> resistant to each antibacterial, as well as <i>E. coli</i> positive for <i>bla</i>_CTX-M Samples collected on pastureland had lower odds of having <i>E. coli</i> resistant to amoxicillin or tetracycline, as well as lower odds of being positive for <i>bla</i>_CTX-M<b>IMPORTANCE</b> Antibacterial resistance poses a significant threat to human and animal health and global food security. Surveillance for resistance on farms is important for many reasons, including tracking impacts of interventions aimed at reducing the prevalence of resistance. In this longitudinal survey of dairy farm antibacterial resistance, we showed that local temperature-as it changes over the course of a year-was associated with the prevalence of antibacterial-resistant <i>E. coli</i> We also showed that prevalence of resistant <i>E. coli</i> was lower on pastureland and higher in environments inhabited by young animals. These findings have profound implications for routine surveillance and for surveys carried out for research. They provide important evidence that sampling at a single time point and/or single location on a farm is unlikely to be adequate to accurately determine the status of the farm regarding the presence of samples containing resistant <i>E. coli</i>.