Genomic Epidemiology of Carbapenemase-producing Klebsiella pneumoniae in China

The rapid spread of carbapenemase-producing Klebsiella pneumoniae (cpKP) poses serious threats to public health; however, the underlying genetic basis for its dissemination is still unknown. We conducted a comprehensive genomic epidemiology analysis on 420 cpKP isolates collected from 70 hospitals i...

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Main Authors: Cuidan Li, Xiaoyuan Jiang, Tingting Yang, Yingjiao Ju, Zhe Yin, Liya Yue, Guannan Ma, Xuebing Wang, Ying Jing, Xinhua Luo, Shuangshuang Li, Xue Yang, Fei Chen, Dongsheng Zhou
Format: Article
Language:English
Published: Elsevier 2022-12-01
Series:Genomics, Proteomics & Bioinformatics
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S1672022922000250
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author Cuidan Li
Xiaoyuan Jiang
Tingting Yang
Yingjiao Ju
Zhe Yin
Liya Yue
Guannan Ma
Xuebing Wang
Ying Jing
Xinhua Luo
Shuangshuang Li
Xue Yang
Fei Chen
Dongsheng Zhou
author_facet Cuidan Li
Xiaoyuan Jiang
Tingting Yang
Yingjiao Ju
Zhe Yin
Liya Yue
Guannan Ma
Xuebing Wang
Ying Jing
Xinhua Luo
Shuangshuang Li
Xue Yang
Fei Chen
Dongsheng Zhou
author_sort Cuidan Li
collection DOAJ
description The rapid spread of carbapenemase-producing Klebsiella pneumoniae (cpKP) poses serious threats to public health; however, the underlying genetic basis for its dissemination is still unknown. We conducted a comprehensive genomic epidemiology analysis on 420 cpKP isolates collected from 70 hospitals in 24 provinces/autonomous regions/municipalities of China during 2009–2017 by short-/long-read sequencing. The results showed that most cpKP isolates were categorized into clonal group 258 (CG258), in which ST11 was the dominant clone. Phylogenetic analysis revealed three major clades including the top one of Clade 3 for CG258 cpKP isolates. Additionally, carbapenemase gene analysis indicated that blaKPC was dominant in the cpKP isolates, and most blaKPC genes were located in five major incompatibility (Inc) groups of blaKPC-harboring plasmids. Importantly, three advantageous combinations of host–blaKPC-carrying plasmid (Clade 3.1+3.2–IncFIIpHN7A8, Clade 3.1+3.2–IncFIIpHN7A8:IncR, and Clade 3.3–IncFIIpHN7A8:IncpA1763-KPC) were identified to confer cpKP isolates the advantages in both genotypes (strong correlation/coevolution) and phenotypes (resistance/growth/competition) to facilitate the nationwide spread of ST11/CG258 cpKP. Intriguingly, Bayesian skyline analysis illustrated that the three advantageous combinations might be directly associated with the strong population expansion during 2007–2008 and subsequent maintenance of the population of ST11/CG258 cpKP after 2008. We then examined drug resistance profiles of these cpKP isolates and proposed combination treatment regimens for CG258/non-CG258 cpKP infections. Thus, the findings of our systematical analysis shed light on the molecular epidemiology and genetic basis for the dissemination of ST11/CG258 cpKP in China, and much emphasis should be given to the close monitoring of advantageous cpKP–plasmid combinations.
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spelling doaj.art-5367d33d1e07488784bcfd6631434d832024-02-03T04:04:51ZengElsevierGenomics, Proteomics & Bioinformatics1672-02292022-12-0120611541167Genomic Epidemiology of Carbapenemase-producing Klebsiella pneumoniae in ChinaCuidan Li0Xiaoyuan Jiang1Tingting Yang2Yingjiao Ju3Zhe Yin4Liya Yue5Guannan Ma6Xuebing Wang7Ying Jing8Xinhua Luo9Shuangshuang Li10Xue Yang11Fei Chen12Dongsheng Zhou13CAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, China; State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, ChinaState Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, ChinaCAS Key Laboratory of Genome Sciences & Information, Beijing Institute of Genomics, Chinese Academy of Sciences and China National Center for Bioinformation, Beijing 100101, China; University of Chinese Academy of Sciences, Beijing 100049, China; State Key Laboratory of Pathogenesis, Prevention and Treatment of High Incidence Diseases in Central Asia, Urumqi 830011, China; Beijing Key Laboratory of Genome and Precision Medicine Technologies, Beijing 100101, China; Corresponding authors.State Key Laboratory of Pathogen and Biosecurity, Beijing Institute of Microbiology and Epidemiology, Beijing 100071, China; Corresponding authors.The rapid spread of carbapenemase-producing Klebsiella pneumoniae (cpKP) poses serious threats to public health; however, the underlying genetic basis for its dissemination is still unknown. We conducted a comprehensive genomic epidemiology analysis on 420 cpKP isolates collected from 70 hospitals in 24 provinces/autonomous regions/municipalities of China during 2009–2017 by short-/long-read sequencing. The results showed that most cpKP isolates were categorized into clonal group 258 (CG258), in which ST11 was the dominant clone. Phylogenetic analysis revealed three major clades including the top one of Clade 3 for CG258 cpKP isolates. Additionally, carbapenemase gene analysis indicated that blaKPC was dominant in the cpKP isolates, and most blaKPC genes were located in five major incompatibility (Inc) groups of blaKPC-harboring plasmids. Importantly, three advantageous combinations of host–blaKPC-carrying plasmid (Clade 3.1+3.2–IncFIIpHN7A8, Clade 3.1+3.2–IncFIIpHN7A8:IncR, and Clade 3.3–IncFIIpHN7A8:IncpA1763-KPC) were identified to confer cpKP isolates the advantages in both genotypes (strong correlation/coevolution) and phenotypes (resistance/growth/competition) to facilitate the nationwide spread of ST11/CG258 cpKP. Intriguingly, Bayesian skyline analysis illustrated that the three advantageous combinations might be directly associated with the strong population expansion during 2007–2008 and subsequent maintenance of the population of ST11/CG258 cpKP after 2008. We then examined drug resistance profiles of these cpKP isolates and proposed combination treatment regimens for CG258/non-CG258 cpKP infections. Thus, the findings of our systematical analysis shed light on the molecular epidemiology and genetic basis for the dissemination of ST11/CG258 cpKP in China, and much emphasis should be given to the close monitoring of advantageous cpKP–plasmid combinations.http://www.sciencedirect.com/science/article/pii/S1672022922000250Klebsiella pneumoniaeDrug resistanceCarbapenemasePlasmidGenomic epidemiology
spellingShingle Cuidan Li
Xiaoyuan Jiang
Tingting Yang
Yingjiao Ju
Zhe Yin
Liya Yue
Guannan Ma
Xuebing Wang
Ying Jing
Xinhua Luo
Shuangshuang Li
Xue Yang
Fei Chen
Dongsheng Zhou
Genomic Epidemiology of Carbapenemase-producing Klebsiella pneumoniae in China
Genomics, Proteomics & Bioinformatics
Klebsiella pneumoniae
Drug resistance
Carbapenemase
Plasmid
Genomic epidemiology
title Genomic Epidemiology of Carbapenemase-producing Klebsiella pneumoniae in China
title_full Genomic Epidemiology of Carbapenemase-producing Klebsiella pneumoniae in China
title_fullStr Genomic Epidemiology of Carbapenemase-producing Klebsiella pneumoniae in China
title_full_unstemmed Genomic Epidemiology of Carbapenemase-producing Klebsiella pneumoniae in China
title_short Genomic Epidemiology of Carbapenemase-producing Klebsiella pneumoniae in China
title_sort genomic epidemiology of carbapenemase producing klebsiella pneumoniae in china
topic Klebsiella pneumoniae
Drug resistance
Carbapenemase
Plasmid
Genomic epidemiology
url http://www.sciencedirect.com/science/article/pii/S1672022922000250
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