Abstract

Antimicrobial use in livestock production is a driver for the development and proliferation of antimicrobial resistance (AMR). Wildlife interactions with livestock, acquiring associated AMR bacteria and genes, and wildlife’s subsequent dispersal across the landscape are hypothesized to play an important role in the ecology of AMR. Here, we examined priority AMR phenotypes and genotypes of Escherichia coli isolated from the gastrointestinal tracts of European starlings (Sturnus vulgaris) found on concentrated animal feeding operations (CAFOs). European starlings may be present in high numbers on CAFOs (>100,000 birds), interact with urban environments, and can migrate distances exceeding 1,500 km in North America. In this study, 1,477 European starlings from 31 feedlots in five U.S. states were sampled for E. coli resistant to third generation cephalosporins (3G-C) and fluoroquinolones. The prevalence of 3G-C and fluoroquinolone-resistant E. coli was 4% and 10%, respectively. Multidrug resistance in the E. coli isolates collected (n = 236) was common, with the majority of isolates displaying resistance to six or more classes of antibiotics. Genetic analyses of a subset of these isolates identified 94 genes putatively contributing to AMR, including seven class A and C β-lactamases as well as mutations in gyrA and parC recognized to confer resistance to quinolones. Phylogenetic and subtyping assessments showed that highly similar isolates (≥99.4% shared core genome, ≥99.6% shared coding sequence) with priority AMR were found in birds on feedlots separated by distances exceeding 150 km, suggesting that European starlings could be involved in the interstate dissemination of priority AMR bacteria.

Highlights

  • Antimicrobial use in livestock production is a driver for the development and proliferation of antimicrobial resistance (AMR)

  • Phylogenetic and subtyping assessments showed that highly similar isolates (≥99.4% shared core genome, ≥99.6% shared coding sequence) with priority AMR were found in birds on feedlots separated by distances exceeding 150 km, suggesting that European starlings could be involved in the interstate dissemination of priority AMR bacteria

  • We examined the AMR phenotypes and molecular epidemiology of CTX and CIP-resistant E. coli at the interface of livestock and European starlings

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Summary

Introduction

Antimicrobial use in livestock production is a driver for the development and proliferation of antimicrobial resistance (AMR). Wildlife interactions with livestock, acquiring associated AMR bacteria and genes, and wildlife’s subsequent dispersal across the landscape are hypothesized to play an important role in the ecology of AMR. Antibiotic use in animal agriculture for prophylaxis, therapy, and growth promotion is generally recognized to coincide with the proliferation of antimicrobial resistance (AMR) in associated bacterial communities[1,2,3]. European starlings thrive in urban landscapes, where food, water, and nesting resources are met[21] Given these behavioral and ecological propensities, European starlings were hypothesized to play an important role in the dissemination of pathogenic bacteria, including AMR bacteria, to livestock and subsequently humans[24,25,26,27]. We identified that the total population of European starlings found on CAFOs was positively correlated with cattle fecal shedding of ciprofloxacin (CIP)-resistant Escherichia coli (E. coli), further highlighting an important role of these birds in the maintenance and dissemination of AMR28

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