Assessing the occurrence and transfer dynamics of ESBL/pAmpC-producing Escherichia coli across the broiler production pyramid.

Ilias Apostolakos,Lapo Mughini-Gras,Luca Fasolato,Alessandra Piccirillo,Grzegorz Woźniakowski

doi:10.1371/journal.pone.0217174

Abstract

Extended-spectrum β-lactamase (ESBL)- and plasmid mediated AmpC-type cephalosporinase (pAmpC)-producing Escherichia coli (ESBL/pAmpC E. coli) in food-producing animals is a major public health concern. This study aimed at quantifying ESBL/pAmpC-E. coli occurrence and transfer in Italy’s broiler production pyramid. Three production chains of an integrated broiler company were investigated. Cloacal swabs were taken from parent stock chickens and offspring broiler flocks in four fattening farms per chain. Carcasses from sampled broiler flocks were collected at slaughterhouse. Samples were processed on selective media, and E. coli colonies were screened for ESBL/pAmpC production. ESBL/pAmpC genes and E. coli phylogroups were determined by PCR and sequencing. Average pairwise overlap of ESBL/pAmpC E. coli gene and phylogroup occurrences between subsequent production stages was estimated using the proportional similarity index, modelling uncertainty in a Monte Carlo simulation setting. In total, 820 samples were processed, from which 513 ESBL/pAmpC E. coli isolates were obtained. We found a high prevalence (92.5%, 95%CI 72.1–98.3%) in day-old parent stock chicks, in which blaCMY-2 predominated; prevalence then dropped to 20% (12.9–29.6%) at laying phase. In fattening broilers, prevalence was 69.2% (53.6–81.3%) at the start of production, 54.2% (38.9–68.6%) at slaughter time, and 61.3% (48.1–72.9%) in carcasses. Significantly decreasing and increasing trends for respectively blaCMY-2 and blaCTX-M-1 gene occurrences were found across subsequent production stages. ESBL/pAmpC E. coli genetic background appeared complex and bla-gene/phylogroup associations indicated clonal and horizontal transmission. Modelling revealed that the average transfer of ESBL/pAmpC E. coli genes between subsequent production stages was 47.7% (42.3–53.4%). We concluded that ESBL/pAmpC E. coli in the broiler production pyramid is prevalent, with substantial transfer between subsequent production levels.

Highlights

Extended spectrum cephalosporins (ESCs) are considered critically important antimicrobials (CIAs) in both human and veterinary medicine [1,2]
At the end of the production pyramid, ESBL/pAmpC E. coli was isolated from 61.3% of carcasses (Fig 1)
The overlap increased with decreasing time elapsed between two sampling stages (Fig 4). This is the first study investigating the occurrence and potential transfer of ESBL/pAmpC E. coli across the whole broiler production pyramid in Italy

Summary

Introduction

Extended spectrum cephalosporins (ESCs) are considered critically important antimicrobials (CIAs) in both human and veterinary medicine [1,2]. Resistance in Enterobacteriaceae, such as Escherichia coli, caused by production of extended-spectrum β-lactamases (ESBLs) or AmpC β-lactamases (pAmpCs) and transferability of resistance mechanisms are of particular importance, as the encoding genes (hereafter ESBL/pAmpC genes) are often located in promiscuous plasmids [4]. This property of EBSL/pAmpC genes enables their exchange between bacteria, including pathogens, and favours transmission between animals and humans [5]. The authors stressed the need for more quantitative data on these transmission pathways

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Conclusion