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Dissemination of bla(NDM-5) and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China

Animal farms have become one of the most important reservoirs of carbapenem-resistant Klebsiella spp. (CRK) owing to the wide usage of veterinary antibiotics. “One Health”-studies observing animals, the environment, and humans are necessary to understand the dissemination of CRK in animal breeding a...

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Autores principales: Yang, Chengxia, Han, Jingyi, Berglund, Björn, Zou, Huiyun, Gu, Congcong, Zhao, Ling, Meng, Chen, Zhang, Hui, Ma, Xianjun, Li, Xuewen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9627307/
https://www.ncbi.nlm.nih.gov/pubmed/36338046
http://dx.doi.org/10.3389/fmicb.2022.1030490
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author Yang, Chengxia
Han, Jingyi
Berglund, Björn
Zou, Huiyun
Gu, Congcong
Zhao, Ling
Meng, Chen
Zhang, Hui
Ma, Xianjun
Li, Xuewen
author_facet Yang, Chengxia
Han, Jingyi
Berglund, Björn
Zou, Huiyun
Gu, Congcong
Zhao, Ling
Meng, Chen
Zhang, Hui
Ma, Xianjun
Li, Xuewen
author_sort Yang, Chengxia
collection PubMed
description Animal farms have become one of the most important reservoirs of carbapenem-resistant Klebsiella spp. (CRK) owing to the wide usage of veterinary antibiotics. “One Health”-studies observing animals, the environment, and humans are necessary to understand the dissemination of CRK in animal breeding areas. Based on the concept of “One-Health,” 263 samples of animal feces, wastewater, well water, and human feces from 60 livestock and poultry farms in Shandong province, China were screened for CRK. Five carbapenem-resistant Klebsiella pneumoniae (CRKP) and three carbapenem-resistant Klebsiella quasipneumoniae (CRKQ) strains were isolated from animal feces, human feces, and well water. The eight strains were characterized by antimicrobial susceptibility testing, plasmid conjugation assays, whole-genome sequencing, and bioinformatics analysis. All strains carried the carbapenemase-encoding gene bla(NDM-5), which was flanked by the same core genetic structure (IS5-bla(NDM-5)-ble(MBL)-trpF-dsbD-IS26-ISKox3) and was located on highly related conjugative IncX3 plasmids. The colistin resistance gene mcr-8.1 was carried by three CRKP and located on self-transmissible IncFII(K)/IncFIA(HI1) and IncFII(pKP91)/IncFIA(HI1) plasmids. The genetic context of mcr-8.1 consisted of IS903-orf-mcr-8.1-copR-baeS-dgkA-orf-IS903 in three strains. Single nucleotide polymorphism (SNP) analysis confirmed the clonal spread of CRKP carrying-bla(NDM-5) and mcr-8.1 between two human workers in the same chicken farm. Additionally, the SNP analysis showed clonal expansion of CRKP and CRKQ strains from well water in different farms, and the clonal CRKP was clonally related to isolates from animal farms and a wastewater treatment plant collected in other studies in the same province. These findings suggest that CRKP and CRKQ are capable of disseminating via horizontal gene transfer and clonal expansion and may pose a significant threat to public health unless preventative measures are taken.
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spelling pubmed-96273072022-11-03 Dissemination of bla(NDM-5) and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China Yang, Chengxia Han, Jingyi Berglund, Björn Zou, Huiyun Gu, Congcong Zhao, Ling Meng, Chen Zhang, Hui Ma, Xianjun Li, Xuewen Front Microbiol Microbiology Animal farms have become one of the most important reservoirs of carbapenem-resistant Klebsiella spp. (CRK) owing to the wide usage of veterinary antibiotics. “One Health”-studies observing animals, the environment, and humans are necessary to understand the dissemination of CRK in animal breeding areas. Based on the concept of “One-Health,” 263 samples of animal feces, wastewater, well water, and human feces from 60 livestock and poultry farms in Shandong province, China were screened for CRK. Five carbapenem-resistant Klebsiella pneumoniae (CRKP) and three carbapenem-resistant Klebsiella quasipneumoniae (CRKQ) strains were isolated from animal feces, human feces, and well water. The eight strains were characterized by antimicrobial susceptibility testing, plasmid conjugation assays, whole-genome sequencing, and bioinformatics analysis. All strains carried the carbapenemase-encoding gene bla(NDM-5), which was flanked by the same core genetic structure (IS5-bla(NDM-5)-ble(MBL)-trpF-dsbD-IS26-ISKox3) and was located on highly related conjugative IncX3 plasmids. The colistin resistance gene mcr-8.1 was carried by three CRKP and located on self-transmissible IncFII(K)/IncFIA(HI1) and IncFII(pKP91)/IncFIA(HI1) plasmids. The genetic context of mcr-8.1 consisted of IS903-orf-mcr-8.1-copR-baeS-dgkA-orf-IS903 in three strains. Single nucleotide polymorphism (SNP) analysis confirmed the clonal spread of CRKP carrying-bla(NDM-5) and mcr-8.1 between two human workers in the same chicken farm. Additionally, the SNP analysis showed clonal expansion of CRKP and CRKQ strains from well water in different farms, and the clonal CRKP was clonally related to isolates from animal farms and a wastewater treatment plant collected in other studies in the same province. These findings suggest that CRKP and CRKQ are capable of disseminating via horizontal gene transfer and clonal expansion and may pose a significant threat to public health unless preventative measures are taken. Frontiers Media S.A. 2022-10-19 /pmc/articles/PMC9627307/ /pubmed/36338046 http://dx.doi.org/10.3389/fmicb.2022.1030490 Text en Copyright © 2022 Yang, Han, Berglund, Zou, Gu, Zhao, Meng, Zhang, Ma and Li. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Yang, Chengxia
Han, Jingyi
Berglund, Björn
Zou, Huiyun
Gu, Congcong
Zhao, Ling
Meng, Chen
Zhang, Hui
Ma, Xianjun
Li, Xuewen
Dissemination of bla(NDM-5) and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China
title Dissemination of bla(NDM-5) and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China
title_full Dissemination of bla(NDM-5) and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China
title_fullStr Dissemination of bla(NDM-5) and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China
title_full_unstemmed Dissemination of bla(NDM-5) and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China
title_short Dissemination of bla(NDM-5) and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China
title_sort dissemination of bla(ndm-5) and mcr-8.1 in carbapenem-resistant klebsiella pneumoniae and klebsiella quasipneumoniae in an animal breeding area in eastern china
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9627307/
https://www.ncbi.nlm.nih.gov/pubmed/36338046
http://dx.doi.org/10.3389/fmicb.2022.1030490
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