Dissemination of blaNDM-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

doi:10.3389/fmicb.2022.1030490

Dissemination of blaNDM-5 and mcr-8.1 in carbapenem-resistant Klebsiella pneumoniae and Klebsiella quasipneumoniae in an animal breeding area in Eastern China

Journal Article · Wed Oct 19 00:00:00 EDT 2022 · Frontiers in Microbiology

DOI:https://doi.org/10.3389/fmicb.2022.1030490· OSTI ID:1893960

Yang, Chengxia; Han, Jingyi; Berglund, Björn; Zou, Huiyun; Gu, Congcong; Zhao, Ling; Meng, Chen; Zhang, Hui; Ma, Xianjun; Li, Xuewen

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.

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Sponsoring Organization:: USDOE Office of Electricity (OE), Advanced Grid Research & Development. Power Systems Engineering Research

OSTI ID:: 1893960

Journal Information:: Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 13; ISSN 1664-302X

Publisher:: Frontiers Media SACopyright Statement

Country of Publication:: Switzerland

Language:: English

References (56)

Mobilized colistin resistance (mcr) genes from 1 to 10: a comprehensive review Hussein, Nadheema Hammood; AL-Kadmy, Israa M. S.; Taha, Butheina Mohammed Molecular Biology Reports, Vol. 48, Issue 3 https://doi.org/10.1007/s11033-021-06307-y	journal	March 2021
Travel and the Spread of Drug-Resistant Bacteria Schwartz, Kevin L.; Morris, Shaun K. Current Infectious Disease Reports, Vol. 20, Issue 9 https://doi.org/10.1007/s11908-018-0634-9	journal	June 2018
Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections Li, Jian; Nation, Roger L.; Turnidge, John D. The Lancet Infectious Diseases, Vol. 6, Issue 9 https://doi.org/10.1016/S1473-3099(06)70580-1	journal	September 2006
Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study Liu, Yi-Yun; Wang, Yang; Walsh, Timothy R. The Lancet Infectious Diseases, Vol. 16, Issue 2 https://doi.org/10.1016/S1473-3099(15)00424-7	journal	February 2016
Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis Tacconelli, Evelina; Carrara, Elena; Savoldi, Alessia The Lancet Infectious Diseases, Vol. 18, Issue 3 https://doi.org/10.1016/S1473-3099(17)30753-3	journal	March 2018
Whole genome sequencing options for bacterial strain typing and epidemiologic analysis based on single nucleotide polymorphism versus gene-by-gene–based approaches Schürch, A. C.; Arredondo-Alonso, S.; Willems, R. J. L. Clinical Microbiology and Infection, Vol. 24, Issue 4 https://doi.org/10.1016/j.cmi.2017.12.016	journal	April 2018
Multiplex PCR for detection of acquired carbapenemase genes Poirel, Laurent; Walsh, Timothy R.; Cuvillier, Vincent Diagnostic Microbiology and Infectious Disease, Vol. 70, Issue 1 https://doi.org/10.1016/j.diagmicrobio.2010.12.002	journal	May 2011
Revealing the distribution characteristics of antibiotic resistance genes and bacterial communities in animal-aerosol-human in a chicken farm: From One-Health perspective Yang, Fan; Gao, Yanling; Zhao, Hongcheng Ecotoxicology and Environmental Safety, Vol. 224 https://doi.org/10.1016/j.ecoenv.2021.112687	journal	November 2021
Contaminated in-house environment contributes to the persistence and transmission of NDM-producing bacteria in a Chinese poultry farm Zhai, Ruidong; Fu, Bo; Shi, Xiaomin Environment International, Vol. 139 https://doi.org/10.1016/j.envint.2020.105715	journal	June 2020
Genetic characterization and virulence of a carbapenem-resistant Raoultella ornithinolytica isolated from well water carrying a novel megaplasmid containing blaNDM-1 Zou, Huiyun; Berglund, Björn; Xu, Hao Environmental Pollution, Vol. 260 https://doi.org/10.1016/j.envpol.2020.114041	journal	May 2020
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 Zhao, Qian; Berglund, Björn; Zou, Huiyun Environmental Pollution, Vol. 273 https://doi.org/10.1016/j.envpol.2020.116370	journal	March 2021
Clonal and plasmid-mediated dissemination of environmental carbapenem-resistant Enterobacteriaceae in large animal breeding areas in northern China Gu, Congcong; Li, Xuewen; Zou, Huiyun Environmental Pollution, Vol. 297 https://doi.org/10.1016/j.envpol.2022.118800	journal	March 2022
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 Mirzaii, Mehdi; Jamshidi, Sanaz; Zamanzadeh, Maryam Journal of Global Antimicrobial Resistance, Vol. 13 https://doi.org/10.1016/j.jgar.2018.04.017	journal	June 2018
Emergence of blaNDM-carrying IncX3 plasmid in Klebsiella pneumoniae and Klebsiella quasipneumoniae from duck farms in Guangdong Province, China Ma, Zhenbao; Liu, Jiao; Yang, Jintao Journal of Global Antimicrobial Resistance, Vol. 22 https://doi.org/10.1016/j.jgar.2020.07.001	journal	September 2020
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 Zhao, Yanan; Liu, Lingli; Wang, Shaohui Journal of Global Antimicrobial Resistance, Vol. 24 https://doi.org/10.1016/j.jgar.2021.01.006	journal	March 2021
Emergence of mcr-1- and blaNDM-5-harbouring IncHI2 plasmids in Escherichia coli strains isolated from meat in Zhejiang, China Wang, Jingge; Tang, Biao; Lin, Rumeng Journal of Global Antimicrobial Resistance, Vol. 30 https://doi.org/10.1016/j.jgar.2022.06.002	journal	September 2022
Diversity, abundance, and persistence of antibiotic resistance genes in various types of animal manure following industrial composting Qian, Xun; Gu, Jie; Sun, Wei Journal of Hazardous Materials, Vol. 344 https://doi.org/10.1016/j.jhazmat.2017.11.020	journal	February 2018
Antibiotic resistance gene reservoir in live poultry markets Wang, Yanan; Hu, Yongfei; Cao, Jian Journal of Infection, Vol. 78, Issue 6 https://doi.org/10.1016/j.jinf.2019.03.012	journal	June 2019
Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China Zhao, Ling; Dong, Yuan Hua; Wang, Hui Science of The Total Environment, Vol. 408, Issue 5 https://doi.org/10.1016/j.scitotenv.2009.11.014	journal	February 2010
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega Sievers, Fabian; Wilm, Andreas; Dineen, David Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.75	journal	January 2011
Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase Robicsek, Ari; Strahilevitz, Jacob; Jacoby, George A. Nature Medicine, Vol. 12, Issue 1 https://doi.org/10.1038/nm1347	journal	December 2005
Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production Wang, Yang; Zhang, Rongmin; Li, Jiyun Nature Microbiology, Vol. 2, Issue 4 https://doi.org/10.1038/nmicrobiol.2016.260	journal	February 2017
Emergence of a novel mobile colistin resistance gene, mcr-8 , in NDM-producing Klebsiella pneumoniae Wang, Xiaoming; Wang, Yao; Zhou, Ying Emerging Microbes & Infections, Vol. 7, Issue 1 https://doi.org/10.1038/s41426-018-0124-z	journal	December 2018
Emergence and clonal spread of colistin resistance due to multiple mutational mechanisms in carbapenemase-producing Klebsiella pneumoniae in London Otter, Jonathan A.; Doumith, Michel; Davies, Frances Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-12637-4	journal	October 2017
Co-existence of a novel plasmid-mediated efflux pump with colistin resistance gene mcr in one plasmid confers transferable multidrug resistance in Klebsiella pneumoniae Sun, Shijun; Gao, Hua; Liu, Yudong Emerging Microbes & Infections, Vol. 9, Issue 1 https://doi.org/10.1080/22221751.2020.1768805	journal	January 2020
Clonal Spread of Colistin-ResistantKlebsiella pneumoniaeCoproducing KPC and VIM Carbapenemases in Neonates at a Tunisian University Hospital Battikh, Hajer; Harchay, Chiraz; Dekhili, Amal Microbial Drug Resistance, Vol. 23, Issue 4 https://doi.org/10.1089/mdr.2016.0175	journal	June 2017
Prokka: rapid prokaryotic genome annotation Seemann, T. Bioinformatics, Vol. 30, Issue 14 https://doi.org/10.1093/bioinformatics/btu153	journal	March 2014
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 Onishi, Reo; Shigemura, Katsumi; Osawa, Kayo Pathogens and Disease, Vol. 80, Issue 1 https://doi.org/10.1093/femspd/ftac030	journal	July 2022
Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance Navon-Venezia, Shiri; Kondratyeva, Kira; Carattoli, Alessandra FEMS Microbiology Reviews, Vol. 41, Issue 3 https://doi.org/10.1093/femsre/fux013	journal	May 2017
Occurrence and characterization ofbla_NDM-5-positiveKlebsiella pneumoniaeisolates from dairy cows in Jiangsu, China He, Tao; Wang, Yang; Sun, Lichang Journal of Antimicrobial Chemotherapy, Vol. 72, Issue 1 https://doi.org/10.1093/jac/dkw357	journal	September 2016
Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance Magiorakos, A. -P.; Srinivasan, A.; Carey, R. B. Clinical Microbiology and Infection, Vol. 18, Issue 3 https://doi.org/10.1111/j.1469-0691.2011.03570.x	journal	March 2012
Global distribution of plasmid‐mediated colistin resistance mcr gene in Salmonella : A systematic review Portes, Ana Beatriz; Rodrigues, Grazielle; Leitão, Mylenna Palma Journal of Applied Microbiology, Vol. 132, Issue 2 https://doi.org/10.1111/jam.15282	journal	September 2021
Prevalence of Plasmid-Mediated Quinolone Resistance Determinants over a 9-Year Period Kim, Hong Bin; Park, Chi Hye; Kim, Chung Jong Antimicrobial Agents and Chemotherapy, Vol. 53, Issue 2 https://doi.org/10.1128/AAC.01051-08	journal	December 2008
Heterogeneity and Diversity of mcr-8 Genetic Context in Chicken-Associated Klebsiella pneumoniae Wu, Beibei; Wang, Yao; Ling, Zhuoren Antimicrobial Agents and Chemotherapy, Vol. 65, Issue 1 https://doi.org/10.1128/AAC.01872-20	journal	December 2020
Occurrence of bla _KPC-2 , bla _CTX-M , and mcr-1 in Enterobacteriaceae from Well Water in Rural China Sun, Pan; Bi, Zhenwang; Nilsson, Maud Antimicrobial Agents and Chemotherapy, Vol. 61, Issue 4 https://doi.org/10.1128/AAC.02569-16	journal	April 2017
Identification of Biomarkers for Differentiation of Hypervirulent Klebsiella pneumoniae from Classical K. pneumoniae Russo, Thomas A.; Olson, Ruth; Fang, Chi-Tai Journal of Clinical Microbiology, Vol. 56, Issue 9 https://doi.org/10.1128/JCM.00776-18	journal	September 2018
Cross-Border Emergence of Escherichia coli Producing the Carbapenemase NDM-5 in Switzerland and Germany Chakraborty, Trinad; Sadek, Mustafa; Yao, Yancheng Journal of Clinical Microbiology, Vol. 59, Issue 3 https://doi.org/10.1128/JCM.02238-20	journal	February 2021
Draft Genome Sequence of NDM-5-Producing Escherichia coli Sequence Type 648 and Genetic Context of bla _NDM-5 in Australia Wailan, Alexander M.; Paterson, David L.; Caffery, Michael Genome Announcements, Vol. 3, Issue 2 https://doi.org/10.1128/genomeA.00194-15	journal	April 2015
Emergence of Mobile Colistin Resistance ( mcr-8 ) in a Highly Successful Klebsiella pneumoniae Sequence Type 15 Clone from Clinical Infections in Bangladesh Farzana, Refath; Jones, Lim S.; Barratt, Andrew mSphere, Vol. 5, Issue 2 https://doi.org/10.1128/mSphere.00023-20	journal	April 2020
Dissemination of the bla _NDM-5 Gene via IncX3-Type Plasmid among Enterobacteriaceae in Children Tian, Dongxing; Wang, Bingjie; Zhang, Hong mSphere, Vol. 5, Issue 1 https://doi.org/10.1128/mSphere.00699-19	journal	February 2020
BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons Alikhan, Nabil-Fareed; Petty, Nicola K.; Ben Zakour, Nouri L. BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-402	journal	August 2011
The RAST Server: Rapid Annotations using Subsystems Technology Aziz, Ramy K.; Bartels, Daniela; Best, Aaron A. BMC Genomics, Vol. 9, Issue 1, Article No. 75 https://doi.org/10.1186/1471-2164-9-75	journal	January 2008
Characterization of an NDM-5 carbapenemase-producing Escherichia coli ST156 isolate from a poultry farm in Zhejiang, China Tang, Biao; Chang, Jiang; Cao, Liujie BMC Microbiology, Vol. 19, Issue 1 https://doi.org/10.1186/s12866-019-1454-2	journal	April 2019
Distribution of fluoroquinolone resistance determinants in Carbapenem-resistant Klebsiella pneumoniae clinical isolates associated with bloodstream infections in China Zhan, Qing; Xu, Yanlei; Wang, Bingjie BMC Microbiology, Vol. 21, Issue 1 https://doi.org/10.1186/s12866-021-02238-7	journal	June 2021
Unicycler: Resolving bacterial genome assemblies from short and long sequencing reads Wick, Ryan R.; Judd, Louise M.; Gorrie, Claire L. PLOS Computational Biology, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pcbi.1005595	journal	June 2017
Solving the Problem of Comparing Whole Bacterial Genomes across Different Sequencing Platforms Kaas, Rolf S.; Leekitcharoenphon, Pimlapas; Aarestrup, Frank M. PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0104984	journal	August 2014
Mutations in the quinolone resistance-determining regions of gyrA and parC in Enterobacteriaceae isolates from Brazil Minarini, Luciene A. R.; Darini, Ana Lucia C. Brazilian Journal of Microbiology, Vol. 43, Issue 4 https://doi.org/10.1590/S1517-83822012000400010	journal	December 2012
Detection of gyrA and parC Mutations and Prevalence of Plasmid-Mediated Quinolone Resistance Genes in Klebsiella pneumoniae Kareem, Sawsan Mohammed; Al-kadmy, Israa MS; Kazaal, Saba S. Infection and Drug Resistance, Vol. Volume 14 https://doi.org/10.2147/idr.s275852	journal	February 2021
Scientific Opinion on Carbapenem resistance in food animal ecosystems No authors listed EFSA Journal, Vol. 11, Issue 12 https://doi.org/10.2903/j.efsa.2013.3501	journal	December 2013
Co-Occurrence of NDM-5 and RmtB in a Clinical Isolate of Escherichia coli Belonging to CC354 in Latin America Costa, Agustina; Figueroa-Espinosa, Roque; Gaudenzi, Florencia Frontiers in Cellular and Infection Microbiology, Vol. 11 https://doi.org/10.3389/fcimb.2021.654852	journal	April 2021
Co-occurrence of Variants of mcr-3 and mcr-8 Genes in a Klebsiella pneumoniae Isolate From Laos Hadjadj, Linda; Baron, Sophie Alexandra; Olaitan, Abiola Olumuyiwa Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02720	journal	November 2019
Prolonged Outbreak of Carbapenem and Colistin-Resistant Klebsiella pneumoniae at a Large Tertiary Hospital in Brazil Rocha, Verônica França Diniz; Barbosa, Matheus Sales; Leal, Helena Ferreira Frontiers in Microbiology, Vol. 13 https://doi.org/10.3389/fmicb.2022.831770	journal	March 2022
Transmissibility and Persistence of the Plasmid-Borne Mobile Colistin Resistance Gene, mcr-1, Harbored in Poultry-Associated E. coli Al Mana, Hassan; Johar, Alreem A.; Kassem, Issmat I. Antibiotics, Vol. 11, Issue 6 https://doi.org/10.3390/antibiotics11060774	journal	June 2022
Global Trends in Antimicrobial Use in Food Animals from 2017 to 2030 Tiseo, Katie; Huber, Laura; Gilbert, Marius Antibiotics, Vol. 9, Issue 12 https://doi.org/10.3390/antibiotics9120918	journal	December 2020
Treatment Options for Colistin Resistant Klebsiella pneumoniae: Present and Future No authors listed Journal of Clinical Medicine, Vol. 8, Issue 7 https://doi.org/10.3390/jcm8070934	journal	June 2019
Complete sequencing of an IncX3 plasmid carrying blaNDM-5 allele reveals an early stage in the dissemination of the blaNDM gene Krishnaraju, M.; Kamatchi, C.; Jha, Ak Indian Journal of Medical Microbiology, Vol. 33, Issue 1 https://doi.org/10.4103/0255-0857.148373	journal	January 2015

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