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

SIMPLE SUMMARY: The 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 t...

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Autores principales: Kwon, Bo-Ram, Wei, Bai, Cha, Se-Yeoun, Shang, Ke, Zhang, Jun-Feng, Jang, Hyung-Kwan, Kang, Min
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8232285/
https://www.ncbi.nlm.nih.gov/pubmed/34198679
http://dx.doi.org/10.3390/ani11061778
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author Kwon, Bo-Ram
Wei, Bai
Cha, Se-Yeoun
Shang, Ke
Zhang, Jun-Feng
Jang, Hyung-Kwan
Kang, Min
author_facet Kwon, Bo-Ram
Wei, Bai
Cha, Se-Yeoun
Shang, Ke
Zhang, Jun-Feng
Jang, Hyung-Kwan
Kang, Min
author_sort Kwon, Bo-Ram
collection PubMed
description SIMPLE SUMMARY: The 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 bla(CMY-2) gene in vitro and in vivo. In addition, this study has demonstrated the ease with which a bla(CMY-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 bla(CMY-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. ABSTRACT: 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; bla(CTX-M-15) was the most prevalent gene and two strains carried bla(TEM-1)/bla(CTX-M-15) and bla(CMY-2), respectively. The transferable bla(CTX-M-15) gene was carried by IncFII plasmid in three isolates and the bla(CMY-2) gene carried by IncI1 plasmid in one isolate. bla(CMY-2) gene-harboring strain was selected as the donor based on the high frequency of bla(CMY-2) gene transfer in vitro and its transfer frequencies were determined at 10(−3) transconjugants per recipient. The transfer of bla(CMY-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; bla(CMY-2) gene-harboring transconjugant showed variable fitness burden depends on the parent strains. Our study demonstrated direct evidence that the bla(CMY-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.
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spelling pubmed-82322852021-06-26 Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of bla(CMY-2) Gene Harboring Plasmid In Vitro and In Vivo Kwon, Bo-Ram Wei, Bai Cha, Se-Yeoun Shang, Ke Zhang, Jun-Feng Jang, Hyung-Kwan Kang, Min Animals (Basel) Article SIMPLE SUMMARY: The 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 bla(CMY-2) gene in vitro and in vivo. In addition, this study has demonstrated the ease with which a bla(CMY-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 bla(CMY-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. ABSTRACT: 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; bla(CTX-M-15) was the most prevalent gene and two strains carried bla(TEM-1)/bla(CTX-M-15) and bla(CMY-2), respectively. The transferable bla(CTX-M-15) gene was carried by IncFII plasmid in three isolates and the bla(CMY-2) gene carried by IncI1 plasmid in one isolate. bla(CMY-2) gene-harboring strain was selected as the donor based on the high frequency of bla(CMY-2) gene transfer in vitro and its transfer frequencies were determined at 10(−3) transconjugants per recipient. The transfer of bla(CMY-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; bla(CMY-2) gene-harboring transconjugant showed variable fitness burden depends on the parent strains. Our study demonstrated direct evidence that the bla(CMY-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. MDPI 2021-06-14 /pmc/articles/PMC8232285/ /pubmed/34198679 http://dx.doi.org/10.3390/ani11061778 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Kwon, Bo-Ram
Wei, Bai
Cha, Se-Yeoun
Shang, Ke
Zhang, Jun-Feng
Jang, Hyung-Kwan
Kang, Min
Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of bla(CMY-2) Gene Harboring Plasmid In Vitro and In Vivo
title Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of bla(CMY-2) Gene Harboring Plasmid In Vitro and In Vivo
title_full Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of bla(CMY-2) Gene Harboring Plasmid In Vitro and In Vivo
title_fullStr Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of bla(CMY-2) Gene Harboring Plasmid In Vitro and In Vivo
title_full_unstemmed Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of bla(CMY-2) Gene Harboring Plasmid In Vitro and In Vivo
title_short Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of bla(CMY-2) Gene Harboring Plasmid In Vitro and In Vivo
title_sort characterization of extended-spectrum cephalosporin (esc) resistance in salmonella isolated from chicken and identification of high frequency transfer of bla(cmy-2) gene harboring plasmid in vitro and in vivo
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8232285/
https://www.ncbi.nlm.nih.gov/pubmed/34198679
http://dx.doi.org/10.3390/ani11061778
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