Abstract

Combatting antimicrobial resistant (AMR) using a One-Health approach is essential as various bacteria, including Escherichia coli, a common bacteria, are becoming increasingly resistant and livestock may be a reservoir. The AMR gene content of 492 E. coli, isolated from 56 pig farms across Great Britain in 2014–2015, and purified on antibiotic selective and non-selective plates, was determined using whole genome sequencing (WGS). The E. coli were phylogenetically diverse harboring a variety of AMR profiles with widespread resistance to “old” antibiotics; isolates harbored up to seven plasmid Inc-types. None showed concurrent resistance to third-generation cephalosporins, fluoroquinolones and clinically relevant aminoglycosides, although ∼3% harbored AMR genes to both the former two. Transferable resistance to carbapenem and colistin were absent, and six of 117 E. coli STs belonged to major types associated with human disease. Prevalence of genotypically MDR E. coli, gathered from non-selective media was 35% and that of extended-spectrum-beta-lactamase E. coli was low (∼2% from non-selective). Approximately 72.6% of E. coli from ciprofloxacin plates and only 8.5% from the other plates harbored fluoroquinolone resistance due to topoisomerase mutations; the majority were MDR. In fact, multivariable analysis confirmed E. coli purified from CIP enrichment plates were more likely to be MDR, and suggested MDR isolates were also more probable from farms with high antibiotic usage, specialist finisher farms, and farms emptying their manure pits only after each batch. Additionally, farms from the South East were more likely to have MDR E. coli, whereas farms in Yorkshire and the Humber were less likely. Future investigations will determine whether suggested improvements such as better biosecurity or lower antimicrobial use decreases MDR E. coli on pig farms. Although this study focuses on pig farms, we believe the methodology and findings can be applied more widely to help livestock farmers in the United Kingdom and elsewhere to tackle AMR.

Highlights

  • Escherichia coli is a key species associated with antimicrobial resistance (AMR), including multidrug resistance (World Health Organisation [WHO], 2014), threatening delivery of effective healthcare and challenging basic procedures used in modern human and veterinary medicine (O’Neill, 2016).In Europe, since 2006, non-therapeutic use of antimicrobials has been limited in livestock (Cogliani et al, 2011)

  • None of the porcine E. coli concurrently harbored resistance genes to ESBL, fluoroquinolone, and clinically relevant aminoglycosides, but 15 isolates from five farms carried AMR genes to the former two antimicrobials. This is in contrast to the AST data reported by Public Health England (PHE) for humans between 2012 and 2016 where ∼5% of E. coli isolated from blood and cerebrospinal fluid showed resistance to third-generation cephalosporin, fluoroquinolones, and aminoglycosides, gentamicin and/or tobramycin, which have previously been reported from livestock (Szmolka et al, 2012)

  • Several E. coli STs that have been isolated from humans were present, including seven collected from bacteraemia or feces of people admitted to UK hospitals, indicating some overlap between these compartments; many of these isolates were genotypically multidrug resistance (MDR) and included resistance to high priority critically important antibiotics (HP-CIAs)

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Summary

Introduction

Escherichia coli is a key species associated with AMR, including multidrug resistance (resistance to 3 or more antimicrobial classes; MDR) (World Health Organisation [WHO], 2014), threatening delivery of effective healthcare and challenging basic procedures used in modern human and veterinary medicine (O’Neill, 2016).In Europe, since 2006, non-therapeutic use of antimicrobials has been limited in livestock (Cogliani et al, 2011). Recent livestock studies in Great Britain (GB), suggest that E. coli, chosen as an indicator organism for monitoring AMR in commensal bacteria in the gut flora of livestock, may carry resistance to high priority critically important antibiotics (HP-CIAs) such as cefotaxime or colistin (Anjum et al, 2011; Randall et al, 2014; Card et al, 2016; Duggett et al, 2017; Kirchner et al, 2017), that may spread horizontally to pathogens. Harmonized monitoring of AMR across Europe has indicated resistance of E. coli to HP-CIAs varies from country to country in humans, animals, and food (European Food Safety Authority [EFSA], and European Centre for Disease Prevention and Control [ECDC], 2017); but typically only phenotypic analysis of AMR is performed on isolate(s) from a single representative animal on farm, recovered from selective and/or non-selective media. Mobile genetic elements such as plasmids that play a key role in AMR dispersal could not be classified further

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