Abstract

This study aimed to describe the distribution and characterization of fecal extended-spectrum β-lactamase (ESBL)- and AmpC-producing Escherichia coli isolates from healthy companion animals and cohabiting humans. A total of 968 rectal swab samples from 340 participants, including healthy companion animals and cohabiting humans, were collected from 130 households in South Korea from 2018 to 2019. To determine the bacterial profiles of the participants, several experiments were performed as follows: antimicrobial susceptibility testing, PCR and direct sequencing for ESBL/AmpC production, PFGE, MLST, whole genome sequencing and qRT-PCR. A total of 24.9 and 21.5% of the E. coli isolates from healthy companion animals and cohabiting humans were ESBL/AmpC producers, respectively. The blaCTX–M–14 gene was the most prevalent ESC resistance gene in both pets (n = 25/95, 26.3%) and humans (n = 44/126, 34.9%). The blaCMY–2 gene was also largely detected in pets (n = 19, 20.0%). Overall, intrahousehold pet-human sharing of ESBL/AmpC E. coli isolates occurred in 4.8% of households, and the isolates were all CTX-M-14 producers. In particular, ten CMY-2-producing E. coli isolates from seven dogs and three humans in the different households belonged to the same pulsotype. The MIC values of cefoxitin and the transcription level in CMY-2-producing E. coli isolates were proportional to the blaCMY–2 copy number on the chromosome. Our results showed that the clonal spread of fecal ESBL/AmpC-producing E. coli households’ isolates between healthy companion animals and cohabiting humans was rare, but it could happen. In particular, E. coli ST405 isolates carrying multiple blaCMY–2 genes on the chromosome was sporadically spread between companion animals and humans in South Korea.

Highlights

  • The close contact between companion animals and humans may cause bacterial transmission across animals or humans by horizontal transfer and clonal spread (Damborg et al, 2016)

  • extendedspectrum cephalosporin (ESC) resistance in Enterobacteriaceae is often associated with extended-spectrum β-lactamase (ESBL) and AmpC β-lactamase production, mainly CTX-M-type for ESBL in Enterobacteriaceae, CMY-type for AmpC in Escherichia coli, and DHA-type for AmpC in Klebsiella pneumoniae (Lartigue et al, 2004; Verdet et al, 2009; Kameyama et al, 2013)

  • The transcription of the blaCMY−2 gene could be altered by a putative promoter within ISEcp1, the correlation between ISEcp1 and CMY-2 called the spacer sequence, and the copy number of the blaCMY−2 gene (Smet et al, 2008; Ma et al, 2011; Kurpiel and Hanson, 2012; Manageiro et al, 2015)

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Summary

Introduction

The close contact between companion animals and humans may cause bacterial transmission across animals or humans by horizontal transfer (indirect transmission) and clonal spread (direct transmission) (Damborg et al, 2016). Since the late 1900s, third- and fourth-generation extendedspectrum cephalosporin (ESC)-resistant Enterobacteriaceae have been frequently reported in both human and veterinary fields (Schmiedel et al, 2014; Lee et al, 2018). ESC resistance in Enterobacteriaceae is often associated with extended-spectrum β-lactamase (ESBL) and AmpC β-lactamase production, mainly CTX-M-type for ESBL in Enterobacteriaceae, CMY-type for AmpC in Escherichia coli, and DHA-type for AmpC in Klebsiella pneumoniae (Lartigue et al, 2004; Verdet et al, 2009; Kameyama et al, 2013). CMY-2 is the most prevalent AmpC β-lactamase in ESCresistant E. coli isolates in animals and humans worldwide (Ewers et al, 2012; Lazarus et al, 2015). The transcription of the blaCMY−2 gene could be altered by a putative promoter within ISEcp, the correlation between ISEcp and CMY-2 called the spacer sequence, and the copy number of the blaCMY−2 gene (Smet et al, 2008; Ma et al, 2011; Kurpiel and Hanson, 2012; Manageiro et al, 2015)

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