Dissemination of blaNDM-5 and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China
Abstract
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 (IS 5 - bla NDM-5 - ble MBL - trpF - dsbD -IS 26 -IS Kox3 ) 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 IS 903 - orf - mcr-8.1-copR-baeS-dgkA - orf -IS 903 in three strains. Single nucleotide polymorphism (SNP) analysismore »
- Authors:
- Publication Date:
- Sponsoring Org.:
- USDOE Office of Electricity (OE), Advanced Grid Research & Development. Power Systems Engineering Research
- OSTI Identifier:
- 1893960
- Resource Type:
- Published Article
- Journal Name:
- Frontiers in Microbiology
- Additional Journal Information:
- Journal Name: Frontiers in Microbiology Journal Volume: 13; Journal ID: ISSN 1664-302X
- Publisher:
- Frontiers Media SA
- Country of Publication:
- Switzerland
- Language:
- English
Citation Formats
Yang, Chengxia, Han, Jingyi, Berglund, Björn, Zou, Huiyun, Gu, Congcong, Zhao, Ling, Meng, Chen, Zhang, Hui, Ma, Xianjun, and Li, Xuewen. Dissemination of blaNDM-5 and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China. Switzerland: N. p., 2022.
Web. doi:10.3389/fmicb.2022.1030490.
Yang, Chengxia, Han, Jingyi, Berglund, Björn, Zou, Huiyun, Gu, Congcong, Zhao, Ling, Meng, Chen, Zhang, Hui, Ma, Xianjun, & Li, Xuewen. Dissemination of blaNDM-5 and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China. Switzerland. https://doi.org/10.3389/fmicb.2022.1030490
Yang, Chengxia, Han, Jingyi, Berglund, Björn, Zou, Huiyun, Gu, Congcong, Zhao, Ling, Meng, Chen, Zhang, Hui, Ma, Xianjun, and Li, Xuewen. Wed .
"Dissemination of blaNDM-5 and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China". Switzerland. https://doi.org/10.3389/fmicb.2022.1030490.
@article{osti_1893960,
title = {Dissemination of blaNDM-5 and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China},
author = {Yang, Chengxia and Han, Jingyi and Berglund, Björn and Zou, Huiyun and Gu, Congcong and Zhao, Ling and Meng, Chen and Zhang, Hui and Ma, Xianjun and Li, Xuewen},
abstractNote = {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 (IS 5 - bla NDM-5 - ble MBL - trpF - dsbD -IS 26 -IS Kox3 ) 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 IS 903 - orf - mcr-8.1-copR-baeS-dgkA - orf -IS 903 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.},
doi = {10.3389/fmicb.2022.1030490},
journal = {Frontiers in Microbiology},
number = ,
volume = 13,
place = {Switzerland},
year = {Wed Oct 19 00:00:00 EDT 2022},
month = {Wed Oct 19 00:00:00 EDT 2022}
}
https://doi.org/10.3389/fmicb.2022.1030490
Works referenced in this record:
Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production
journal, February 2017
- Wang, Yang; Zhang, Rongmin; Li, Jiyun
- Nature Microbiology, Vol. 2, Issue 4
Detection of gyrA and parC Mutations and Prevalence of Plasmid-Mediated Quinolone Resistance Genes in Klebsiella pneumoniae
journal, February 2021
- Kareem, Sawsan Mohammed; Al-kadmy, Israa MS; Kazaal, Saba S.
- Infection and Drug Resistance, Vol. Volume 14
Antibiotic resistance gene reservoir in live poultry markets
journal, June 2019
- Wang, Yanan; Hu, Yongfei; Cao, Jian
- Journal of Infection, Vol. 78, Issue 6
Mutations in the quinolone resistance-determining regions of gyrA and parC in Enterobacteriaceae isolates from Brazil
journal, December 2012
- Minarini, Luciene A. R.; Darini, Ana Lucia C.
- Brazilian Journal of Microbiology, Vol. 43, Issue 4
Characterization of an NDM-5 carbapenemase-producing Escherichia coli ST156 isolate from a poultry farm in Zhejiang, China
journal, April 2019
- Tang, Biao; Chang, Jiang; Cao, Liujie
- BMC Microbiology, Vol. 19, Issue 1
Clonal and plasmid-mediated dissemination of environmental carbapenem-resistant Enterobacteriaceae in large animal breeding areas in northern China
journal, March 2022
- Gu, Congcong; Li, Xuewen; Zou, Huiyun
- Environmental Pollution, Vol. 297
Genetic characterization and virulence of a carbapenem-resistant Raoultella ornithinolytica isolated from well water carrying a novel megaplasmid containing blaNDM-1
journal, May 2020
- Zou, Huiyun; Berglund, Björn; Xu, Hao
- Environmental Pollution, Vol. 260
Clonal Spread of Colistin-ResistantKlebsiella pneumoniaeCoproducing KPC and VIM Carbapenemases in Neonates at a Tunisian University Hospital
journal, June 2017
- Battikh, Hajer; Harchay, Chiraz; Dekhili, Amal
- Microbial Drug Resistance, Vol. 23, Issue 4
Identification of Biomarkers for Differentiation of Hypervirulent Klebsiella pneumoniae from Classical K. pneumoniae
journal, September 2018
- Russo, Thomas A.; Olson, Ruth; Fang, Chi-Tai
- Journal of Clinical Microbiology, Vol. 56, Issue 9
Draft Genome Sequence of NDM-5-Producing Escherichia coli Sequence Type 648 and Genetic Context of
bla
NDM-5
in Australia
journal, April 2015
- Wailan, Alexander M.; Paterson, David L.; Caffery, Michael
- Genome Announcements, Vol. 3, Issue 2
Complete sequencing of an IncX3 plasmid carrying blaNDM-5 allele reveals an early stage in the dissemination of the blaNDM gene
journal, January 2015
- Krishnaraju, M.; Kamatchi, C.; Jha, Ak
- Indian Journal of Medical Microbiology, Vol. 33, Issue 1
Travel and the Spread of Drug-Resistant Bacteria
journal, June 2018
- Schwartz, Kevin L.; Morris, Shaun K.
- Current Infectious Disease Reports, Vol. 20, Issue 9
BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons
journal, August 2011
- Alikhan, Nabil-Fareed; Petty, Nicola K.; Ben Zakour, Nouri L.
- BMC Genomics, Vol. 12, Issue 1
Cross-Border Emergence of Escherichia coli Producing the Carbapenemase NDM-5 in Switzerland and Germany
journal, February 2021
- Chakraborty, Trinad; Sadek, Mustafa; Yao, Yancheng
- Journal of Clinical Microbiology, Vol. 59, Issue 3
Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance
journal, March 2012
- Magiorakos, A. -P.; Srinivasan, A.; Carey, R. B.
- Clinical Microbiology and Infection, Vol. 18, Issue 3
Global Trends in Antimicrobial Use in Food Animals from 2017 to 2030
journal, December 2020
- Tiseo, Katie; Huber, Laura; Gilbert, Marius
- Antibiotics, Vol. 9, Issue 12
Co-Occurrence of NDM-5 and RmtB in a Clinical Isolate of Escherichia coli Belonging to CC354 in Latin America
journal, April 2021
- Costa, Agustina; Figueroa-Espinosa, Roque; Gaudenzi, Florencia
- Frontiers in Cellular and Infection Microbiology, Vol. 11
Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads
journal, June 2017
- Wick, Ryan R.; Judd, Louise M.; Gorrie, Claire L.
- PLOS Computational Biology, Vol. 13, Issue 6
Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study
journal, February 2016
- Liu, Yi-Yun; Wang, Yang; Walsh, Timothy R.
- The Lancet Infectious Diseases, Vol. 16, Issue 2
Heterogeneity and Diversity of
mcr-8
Genetic Context in Chicken-Associated Klebsiella pneumoniae
journal, December 2020
- Wu, Beibei; Wang, Yao; Ling, Zhuoren
- Antimicrobial Agents and Chemotherapy, Vol. 65, Issue 1
Determination of gyrA and parC mutations and prevalence of plasmid-mediated quinolone resistance genes in Escherichia coli and Klebsiella pneumoniae isolated from patients with urinary tract infection in Iran
journal, June 2018
- Mirzaii, Mehdi; Jamshidi, Sanaz; Zamanzadeh, Maryam
- Journal of Global Antimicrobial Resistance, Vol. 13
Dissemination of the
bla
NDM-5
Gene via IncX3-Type Plasmid among
Enterobacteriaceae
in Children
journal, February 2020
- Tian, Dongxing; Wang, Bingjie; Zhang, Hong
- mSphere, Vol. 5, Issue 1
The RAST Server: Rapid Annotations using Subsystems Technology
journal, January 2008
- Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A.
- BMC Genomics, Vol. 9, Issue 1, Article No. 75
Multiplex PCR for detection of acquired carbapenemase genes
journal, May 2011
- Poirel, Laurent; Walsh, Timothy R.; Cuvillier, Vincent
- Diagnostic Microbiology and Infectious Disease, Vol. 70, Issue 1
Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis
journal, March 2018
- Tacconelli, Evelina; Carrara, Elena; Savoldi, Alessia
- The Lancet Infectious Diseases, Vol. 18, Issue 3
Emergence of Mobile Colistin Resistance (
mcr-8
) in a Highly Successful Klebsiella pneumoniae Sequence Type 15 Clone from Clinical Infections in Bangladesh
journal, April 2020
- Farzana, Refath; Jones, Lim S.; Barratt, Andrew
- mSphere, Vol. 5, Issue 2
Prokka: rapid prokaryotic genome annotation
journal, March 2014
- Seemann, T.
- Bioinformatics, Vol. 30, Issue 14
Scientific Opinion on Carbapenem resistance in food animal ecosystems
journal, December 2013
- ,
- EFSA Journal, Vol. 11, Issue 12
Global distribution of plasmid‐mediated colistin resistance
mcr
gene in
Salmonella
: A systematic review
journal, September 2021
- Portes, Ana Beatriz; Rodrigues, Grazielle; Leitão, Mylenna Palma
- Journal of Applied Microbiology, Vol. 132, Issue 2
Mobilized colistin resistance (mcr) genes from 1 to 10: a comprehensive review
journal, March 2021
- Hussein, Nadheema Hammood; AL-Kadmy, Israa M. S.; Taha, Butheina Mohammed
- Molecular Biology Reports, Vol. 48, Issue 3
Emergence of blaNDM-carrying IncX3 plasmid in Klebsiella pneumoniae and Klebsiella quasipneumoniae from duck farms in Guangdong Province, China
journal, September 2020
- Ma, Zhenbao; Liu, Jiao; Yang, Jintao
- Journal of Global Antimicrobial Resistance, Vol. 22
Contaminated in-house environment contributes to the persistence and transmission of NDM-producing bacteria in a Chinese poultry farm
journal, June 2020
- Zhai, Ruidong; Fu, Bo; Shi, Xiaomin
- Environment International, Vol. 139
Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections
journal, September 2006
- Li, Jian; Nation, Roger L.; Turnidge, John D.
- The Lancet Infectious Diseases, Vol. 6, Issue 9
Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance
journal, May 2017
- Navon-Venezia, Shiri; Kondratyeva, Kira; Carattoli, Alessandra
- FEMS Microbiology Reviews, Vol. 41, Issue 3
Whole genome sequencing options for bacterial strain typing and epidemiologic analysis based on single nucleotide polymorphism versus gene-by-gene–based approaches
journal, April 2018
- Schürch, A. C.; Arredondo-Alonso, S.; Willems, R. J. L.
- Clinical Microbiology and Infection, Vol. 24, Issue 4
Diversity, abundance, and persistence of antibiotic resistance genes in various types of animal manure following industrial composting
journal, February 2018
- Qian, Xun; Gu, Jie; Sun, Wei
- Journal of Hazardous Materials, Vol. 344
Emergence and clonal spread of colistin resistance due to multiple mutational mechanisms in carbapenemase-producing Klebsiella pneumoniae in London
journal, October 2017
- Otter, Jonathan A.; Doumith, Michel; Davies, Frances
- Scientific Reports, Vol. 7, Issue 1
Occurrence of
bla
KPC-2
,
bla
CTX-M
, and
mcr-1
in Enterobacteriaceae from Well Water in Rural China
journal, April 2017
- Sun, Pan; Bi, Zhenwang; Nilsson, Maud
- Antimicrobial Agents and Chemotherapy, Vol. 61, Issue 4
Co-existence of a novel plasmid-mediated efflux pump with colistin resistance gene mcr in one plasmid confers transferable multidrug resistance in Klebsiella pneumoniae
journal, January 2020
- Sun, Shijun; Gao, Hua; Liu, Yudong
- Emerging Microbes & Infections, Vol. 9, Issue 1
Revealing the distribution characteristics of antibiotic resistance genes and bacterial communities in animal-aerosol-human in a chicken farm: From One-Health perspective
journal, November 2021
- Yang, Fan; Gao, Yanling; Zhao, Hongcheng
- Ecotoxicology and Environmental Safety, Vol. 224
Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase
journal, December 2005
- Robicsek, Ari; Strahilevitz, Jacob; Jacoby, George A.
- Nature Medicine, Vol. 12, Issue 1
Prevalence of Plasmid-Mediated Quinolone Resistance Determinants over a 9-Year Period
journal, December 2008
- Kim, Hong Bin; Park, Chi Hye; Kim, Chung Jong
- Antimicrobial Agents and Chemotherapy, Vol. 53, Issue 2
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
Occurrence and characterization ofblaNDM-5-positiveKlebsiella pneumoniaeisolates from dairy cows in Jiangsu, China
journal, September 2016
- He, Tao; Wang, Yang; Sun, Lichang
- Journal of Antimicrobial Chemotherapy, Vol. 72, Issue 1
Dissemination of blaNDM-5 via IncX3 plasmids in carbapenem-resistant Enterobacteriaceae among humans and in the environment in an intensive vegetable cultivation area in eastern China
journal, March 2021
- Zhao, Qian; Berglund, Björn; Zou, Huiyun
- Environmental Pollution, Vol. 273
Treatment Options for Colistin Resistant Klebsiella pneumoniae: Present and Future
journal, June 2019
- Petrosillo,
- Journal of Clinical Medicine, Vol. 8, Issue 7
Emergence of a novel mobile colistin resistance gene, mcr-8 , in NDM-producing Klebsiella pneumoniae
journal, December 2018
- Wang, Xiaoming; Wang, Yao; Zhou, Ying
- Emerging Microbes & Infections, Vol. 7, Issue 1
Transmissibility and Persistence of the Plasmid-Borne Mobile Colistin Resistance Gene, mcr-1, Harbored in Poultry-Associated E. coli
journal, June 2022
- Al Mana, Hassan; Johar, Alreem A.; Kassem, Issmat I.
- Antibiotics, Vol. 11, Issue 6
Impact on quinolone resistance of plasmid-mediated quinolone resistance gene and mutations in quinolone resistance-determining regions in extended spectrum beta lactamase-producing Klebsiella pneumoniae isolated from urinary tract infection patients
journal, July 2022
- Onishi, Reo; Shigemura, Katsumi; Osawa, Kayo
- Pathogens and Disease, Vol. 80, Issue 1
Solving the Problem of Comparing Whole Bacterial Genomes across Different Sequencing Platforms
journal, August 2014
- Kaas, Rolf S.; Leekitcharoenphon, Pimlapas; Aarestrup, Frank M.
- PLoS ONE, Vol. 9, Issue 8
Prolonged Outbreak of Carbapenem and Colistin-Resistant Klebsiella pneumoniae at a Large Tertiary Hospital in Brazil
journal, March 2022
- Rocha, Verônica França Diniz; Barbosa, Matheus Sales; Leal, Helena Ferreira
- Frontiers in Microbiology, Vol. 13
Emergence of mcr-1- and blaNDM-5-harbouring IncHI2 plasmids in Escherichia coli strains isolated from meat in Zhejiang, China
journal, September 2022
- Wang, Jingge; Tang, Biao; Lin, Rumeng
- Journal of Global Antimicrobial Resistance, Vol. 30
Co-occurrence of Variants of mcr-3 and mcr-8 Genes in a Klebsiella pneumoniae Isolate From Laos
journal, November 2019
- Hadjadj, Linda; Baron, Sophie Alexandra; Olaitan, Abiola Olumuyiwa
- Frontiers in Microbiology, Vol. 10
Distribution of fluoroquinolone resistance determinants in Carbapenem-resistant Klebsiella pneumoniae clinical isolates associated with bloodstream infections in China
journal, June 2021
- Zhan, Qing; Xu, Yanlei; Wang, Bingjie
- BMC Microbiology, Vol. 21, Issue 1
Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China
journal, February 2010
- Zhao, Ling; Dong, Yuan Hua; Wang, Hui
- Science of The Total Environment, Vol. 408, Issue 5
Draft genome sequence analysis of a novel MLST (ST5028) and multidrug-resistant Klebsiella quasipneumoniae subsp. similipneumoniae (Kp4) strain 456S1 isolated from a pig farm in China
journal, March 2021
- Zhao, Yanan; Liu, Lingli; Wang, Shaohui
- Journal of Global Antimicrobial Resistance, Vol. 24