Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of blaCMY-2 Gene Harboring Plasmid In Vitro and In Vivo.

Bo-Ram Kwon,Bai Wei,Min Kang,Jun-Feng Zhang,Ke Shang,Hyung-Kwan Jang,Se-Yeoun Cha

doi:10.3390/ani11061778

Bo-Ram Kwon, Bai Wei + Show 5 more

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https://doi.org/10.3390/ani11061778

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Abstract

Simple SummaryThe prevalence of extended-spectrum cephalosporin (ESC)-resistant Salmonella is of great concern, as these strains with the same β-lactamase (bla) genes were found in human and poultry. The objective is to characterize ESC-resistant Salmonella isolated from chicken and to determine the transferability of β-lactamase gene-harboring plasmid in vitro and in vivo. ESC resistance genes in Salmonella isolated from chickens and presented a comprehensive analysis of the highly frequent transfer of the blaCMY-2 gene in vitro and in vivo. In addition, this study has demonstrated the ease with which a blaCMY-2 gene-harboring plasmid can be rapidly transferred between Salmonella and pathogenic E. coli within the intestinal tracts of mice, even without antimicrobial selective pressure. Given the potential risk of the frequent transfer of the blaCMY-2 gene via the food chain to the human digestive tract, the molecular mechanism involved in the dissemination and maintenance of ESC resistance genes should be studied as further research in greater detail, and enhanced surveillance should be implemented to prevent the widespread of ESC resistant strains.A total of 136 Salmonella isolates from chicken feces and meat samples of the top 12 integrated chicken production companies throughout Korea were collected. Among the 17 ESC-resistant Salmonella; blaCTX-M-15 was the most prevalent gene and two strains carried blaTEM-1/blaCTX-M-15 and blaCMY-2, respectively. The transferable blaCTX-M-15 gene was carried by IncFII plasmid in three isolates and the blaCMY-2 gene carried by IncI1 plasmid in one isolate. blaCMY-2 gene-harboring strain was selected as the donor based on the high frequency of blaCMY-2 gene transfer in vitro and its transfer frequencies were determined at 10−3 transconjugants per recipient. The transfer of blaCMY-2 gene-harboring plasmid derived from chicken isolate into a human pathogen; enteroinvasive Escherichia coli (EIEC), presented in mouse intestine with about 10−1 transfer frequency without selective pressure. From the competition experiment; blaCMY-2 gene-harboring transconjugant showed variable fitness burden depends on the parent strains. Our study demonstrated direct evidence that the blaCMY-2 gene harboring Salmonella from chicken could frequently transfer its ESC-resistant gene to E. coli in a mouse intestine without antimicrobial pressure; resulting in the emergence of multidrug resistance in potentially virulent EIEC isolates of significance to human health; which can increase the risk of therapeutic inadequacy or failures.

Highlights

An increasing occurrence of extended-spectrum cephalosporins (ESC)-resistant strains has been recognized as a serious threat to human health [1]
There is a lack of in vivo studies focused on the blaCMY-2 gene, several studies for conjugal transfer of ESBL genes have been reported. blaTEM gene from Salmonella was transferred to E. coli recipient with the ratio of transconjugant per donor being 6.5 × 10−5 in mice without selective pressure [26], and blaCTX-M-9 gene derived from chicken-origin Salmonella to E. coli at a frequency range of about 5.4 × 10−5 in gnotobiotic rats [27]
This study showed the prevalence of ESC resistance genes in Salmonella isolated from chickens and presented a comprehensive analysis of the highly frequent transfer of the blaCMY-2 gene in vitro and in vivo

Summary

Introduction

An increasing occurrence of extended-spectrum cephalosporins (ESC)-resistant strains has been recognized as a serious threat to human health [1]. Extended-spectrum β-lactamases (ESBL) and AmpC β-lactamase (AmpC) are the major β-lactamases detected in ESC-resistant strains worldwide [3]. These enzymes are frequently encoded by genes that are located on a plasmid, which is a mobile genetic element that can transfer horizontally within and between different bacterial species [4]. Various studies have suggested that food-producing animals as a reservoir for ESBL/AmpC-producing strains that could promote the transmission of resistance determinants to humans [2]. Similar or identical ESC-resistant isolates or ESBL/AmpC plasmids were found in chicken meat and patients, suggesting poultry and poultry products play a pivotal role in the spread of ESC resistance genes to humans [2]

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