A Polyclonal Spread Emerged: Characteristics of Carbapenem-Resistant Klebsiella pneumoniae Isolates from the Intensive Care Unit in a Chinese Tertiary Hospital

Bradford PA, Bratu S, Urban C, Visalli M, Mariano N, Landman D, Rahal JJ, Brooks S, Cebular S, Quale J. Emergence of carbapenem-resistant Klebsiella species possessing the class A carbapenem-hydrolyzing KPC-2 and inhibitor-resistant TEM-30 beta-lactamases in New York City. Clin Infect Dis. 2004 Jul 01;39(1): 55–60. https://doi.org/10.1086/421495BradfordPABratuSUrbanCVisalliMMarianoNLandmanDRahalJJBrooksSCebularSQualeJ. Emergence of carbapenem-resistant Klebsiella species possessing the class A carbapenem-hydrolyzing KPC-2 and inhibitor-resistant TEM-30 beta-lactamases in New York City. Clin Infect Dis.2004Jul01;39(1): 55–60. https://doi.org/10.1086/42149510.1086/42149515206053Search in Google Scholar

Bratu S, Landman D, Haag R, Recco R, Eramo A, Alam M, Quale J. Rapid spread of carbapenem-resistant Klebsiella pneumoniae in New York City: a new threat to our antibiotic armamentarium. Arch Intern Med. 2005 Jun 27;165(12):1430–1435. https://doi.org/10.1001/archinte.165.12.1430BratuSLandmanDHaagRReccoREramoAAlamMQualeJ. Rapid spread of carbapenem-resistant Klebsiella pneumoniae in New York City: a new threat to our antibiotic armamentarium. Arch Intern Med.2005Jun27;165(12):1430–1435. https://doi.org/10.1001/archinte.165.12.143010.1001/archinte.165.12.143015983294Search in Google Scholar

Bush K, Jacoby GA. Updated functional classification of beta-lactamases. Antimicrob Agents Chemother. 2010 Mar;54(3):969–976. https://doi.org/10.1128/AAC.01009-09BushKJacobyGA. Updated functional classification of beta-lactamases. Antimicrob Agents Chemother.2010Mar;54(3):969–976. https://doi.org/10.1128/AAC.01009-0910.1128/AAC.01009-09282599319995920Search in Google Scholar

CLSI. Performance standards for antimicrobial susceptibility testing, 28th Inforational Supplement (M100-S28). Wayne (USA): Clinical and Laboratory Standards Institute; 2018.CLSI. Performance standards for antimicrobial susceptibility testing, 28th Inforational Supplement (M100-S28). Wayne (USA): Clinical and Laboratory Standards Institute; 2018.Search in Google Scholar

Debby BD, Ganor O, Yasmin M, David L, Nathan K, Ilana T, Dalit S, Smollan G, Galia R. Epidemiology of carbapenem resistant Klebsiella pneumoniae colonization in an intensive care unit. Eur J Clin Microbiol Infect Dis. 2012 Aug;31(8):1811–1817. https://doi.org/10.1007/s10096-011-1506-5DebbyBDGanorOYasminMDavidLNathanKIlanaTDalitSSmollanGGaliaR. Epidemiology of carbapenem resistant Klebsiella pneumoniae colonization in an intensive care unit. Eur J Clin Microbiol Infect Dis.2012Aug;31(8):1811–1817. https://doi.org/10.1007/s10096-011-1506-510.1007/s10096-011-1506-522246509Search in Google Scholar

Diago-Navarro E, Chen L, Passet V, Burack S, Ulacia-Hernando A, Kodiyanplakkal RP, Levi MH, Brisse S, Kreiswirth BN, Fries BC. Carbapenem-resistant Klebsiella pneumoniae exhibit variability in capsular polysaccharide and capsule associated virulence traits. J Infect Dis. 2014 Sep 01;210(5):803–813. https://doi.org/10.1093/infdis/jiu157Diago-NavarroEChenLPassetVBurackSUlacia-HernandoAKodiyanplakkalRPLeviMHBrisseSKreiswirthBNFriesBC. Carbapenem-resistant Klebsiella pneumoniae exhibit variability in capsular polysaccharide and capsule associated virulence traits. J Infect Dis.2014Sep01;210(5):803–813. https://doi.org/10.1093/infdis/jiu15710.1093/infdis/jiu157443239524634498Search in Google Scholar

Diancourt L, Passet V, Verhoef J, Grimont PAD, Brisse S. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol. 2005 Aug 01;43(8):4178–4182. https://doi.org/10.1128/JCM.43.8.4178-4182.2005DiancourtLPassetVVerhoefJGrimontPADBrisseS. Multilocus sequence typing of Klebsiella pneumoniae nosocomial isolates. J Clin Microbiol.2005Aug01;43(8):4178–4182. https://doi.org/10.1128/JCM.43.8.4178-4182.200510.1128/JCM.43.8.4178-4182.2005123394016081970Search in Google Scholar

Filgona J, Banerjee T, Anupurba S. Role of efflux pumps inhibitor in decreasing antibiotic resistance of Klebsiella pneumoniae in a tertiary hospital in North India. J Infect Dev Ctries. 2015 Aug 29;9(08):815–820. https://doi.org/10.3855/jidc.6216FilgonaJBanerjeeTAnupurbaS. Role of efflux pumps inhibitor in decreasing antibiotic resistance of Klebsiella pneumoniae in a tertiary hospital in North India. J Infect Dev Ctries.2015Aug29;9(08):815–820. https://doi.org/10.3855/jidc.621610.3855/jidc.621626322872Search in Google Scholar

Gong X, Zhang J, Su S, Fu Y, Bao M, Wang Y, Zhang X. Molecular characterization and epidemiology of carbapenem non-susceptible Enterobacteriaceae isolated from the Eastern region of Heilongjiang Province, China. BMC Infect Dis. 2018 Dec;18(1):417. https://doi.org/10.1186/s12879-018-3294-3GongXZhangJSuSFuYBaoMWangYZhangX. Molecular characterization and epidemiology of carbapenem non-susceptible Enterobacteriaceae isolated from the Eastern region of Heilongjiang Province, China. BMC Infect Dis.2018Dec;18(1):417. https://doi.org/10.1186/s12879-018-3294-310.1186/s12879-018-3294-3610693830134844Search in Google Scholar

Hammerum AM, Hansen F, Lester CH, Jensen KT, Hansen DS, Dessau RB. Detection of the first two Klebsiella pneumoniae isolates with sequence type 258 producing KPC-2 carbapenemase in Denmark. Int J Antimicrob Agents. 2010 Jun;35(6):610–612. https://doi.org/10.1016/j.ijantimicag.2010.01.024HammerumAMHansenFLesterCHJensenKTHansenDSDessauRB. Detection of the first two Klebsiella pneumoniae isolates with sequence type 258 producing KPC-2 carbapenemase in Denmark. Int J Antimicrob Agents.2010Jun;35(6):610–612. https://doi.org/10.1016/j.ijantimicag.2010.01.02410.1016/j.ijantimicag.2010.01.02420206479Search in Google Scholar

Hu L, Liu Y, Deng L, Zhong Q, Hang Y, Wang Z, Zhan L, Wang L, Yu F. Outbreak by ventilator-associated ST11 K. pneumoniae with co-production of CTX-M-24 and KPC-2 in a SICU of a tertiary teaching hospital in central China. Front Microbiol. 2016 Aug 02; 7:1190. https://doi.org/10.3389/fmicb.2016.01190HuLLiuYDengLZhongQHangYWangZZhanLWangLYuF. Outbreak by ventilator-associated ST11 K. pneumoniae with co-production of CTX-M-24 and KPC-2 in a SICU of a tertiary teaching hospital in central China. Front Microbiol.2016Aug02; 7:1190. https://doi.org/10.3389/fmicb.2016.0119010.3389/fmicb.2016.01190497048727531996Search in Google Scholar

Hussein K, Sprecher H, Mashiach T, Oren I, Kassis I, Finkelstein R. Carbapenem resistance among Klebsiella pneumoniae isolates: risk factors, molecular characteristics, and susceptibility patterns. Infect Control Hosp Epidemiol. 2009 Jul;30(7):666–671. https://doi.org/10.1086/598244HusseinKSprecherHMashiachTOrenIKassisIFinkelsteinR. Carbapenem resistance among Klebsiella pneumoniae isolates: risk factors, molecular characteristics, and susceptibility patterns. Infect Control Hosp Epidemiol.2009Jul;30(7):666–671. https://doi.org/10.1086/59824410.1086/59824419496647Search in Google Scholar

Ji S, Lv F, Du X, Wei Z, Fu Y, Mu X, Jiang Y, Yu Y. Cefepime combined with amoxicillin/clavulanic acid: a new choice for the KPC-producing K. pneumoniae infection. Int J Infect Dis. 2015 Sep;38:108–114. https://doi.org/10.1016/j.ijid.2015.07.024JiSLvFDuXWeiZFuYMuXJiangYYuY. Cefepime combined with amoxicillin/clavulanic acid: a new choice for the KPC-producing K. pneumoniae infection. Int J Infect Dis.2015Sep;38:108–114. https://doi.org/10.1016/j.ijid.2015.07.02410.1016/j.ijid.2015.07.02426255892Search in Google Scholar

Kaczmarek FM, Dib-Hajj F, Shang W, Gootz TD. High-level carbapenem resistance in a Klebsiella pneumoniae clinical isolate is due to the combination of bla(ACT-1) beta-lactamase production, porin OmpK35/36 insertional inactivation, and down-regulation of the phosphate transport porin phoe. Antimicrob Agents Chemother. 2006 Oct;50(10):3396–3406. https://doi.org/10.1128/AAC.00285-06KaczmarekFMDib-HajjFShangWGootzTD. High-level carbapenem resistance in a Klebsiella pneumoniae clinical isolate is due to the combination of bla(ACT-1) beta-lactamase production, porin OmpK35/36 insertional inactivation, and down-regulation of the phosphate transport porin phoe. Antimicrob Agents Chemother.2006Oct;50(10):3396–3406. https://doi.org/10.1128/AAC.00285-0610.1128/AAC.00285-06161009917005822Search in Google Scholar

Kitchel B, Rasheed JK, Patel JB, Srinivasan A, Navon-Venezia S, Carmeli Y, Brolund A, Giske CG. Molecular epidemiology of KPC-producing Klebsiella pneumoniae isolates in the United States: clonal expansion of multilocus sequence type 258. Antimicrob Agents Chemother. 2009 Aug;53(8):3365–3370. https://doi.org/10.1128/AAC.00126-09KitchelBRasheedJKPatelJBSrinivasanANavon-VeneziaSCarmeliYBrolundAGiskeCG. Molecular epidemiology of KPC-producing Klebsiella pneumoniae isolates in the United States: clonal expansion of multilocus sequence type 258. Antimicrob Agents Chemother.2009Aug;53(8):3365–3370. https://doi.org/10.1128/AAC.00126-0910.1128/AAC.00126-09271558019506063Search in Google Scholar

Kofteridis DP, Valachis A, Dimopoulou D, Maraki S, Christidou A, Mantadakis E, Samonis G. Risk factors for carbapenem-resistant Klebsiella pneumoniae infection/colonization: A case-case-control study. J Infect Chemother. 2014 May;20(5):293–297. https://doi.org/10.1016/j.jiac.2013.11.007KofteridisDPValachisADimopoulouDMarakiSChristidouAMantadakisESamonisG. Risk factors for carbapenem-resistant Klebsiella pneumoniae infection/colonization: A case-case-control study. J Infect Chemother.2014May;20(5):293–297. https://doi.org/10.1016/j.jiac.2013.11.00710.1016/j.jiac.2013.11.00724703709Search in Google Scholar

Kumar M, Shankar C, Baskaran A, Paul M, Ponmudi N, Santhanam S, Michael J, Veeraraghavan B. Molecular characterisation for clonality and transmission dynamics of an outbreak of Klebsiella pneumoniae amongst neonates in a tertiary care centre in South India. Indian J Med Microbiol. 2018;36(1):54–60. https://doi.org/10.4103/ijmm.IJMM_17_426KumarMShankarCBaskaranAPaulMPonmudiNSanthanamSMichaelJVeeraraghavanB. Molecular characterisation for clonality and transmission dynamics of an outbreak of Klebsiella pneumoniae amongst neonates in a tertiary care centre in South India. Indian J Med Microbiol.2018;36(1):54–60. https://doi.org/10.4103/ijmm.IJMM_17_42610.4103/ijmm.IJMM_17_42629735827Search in Google Scholar

Lester CH, Olsen SS, Jakobsen L, Arpi M, Fuursted K, Hansen DS, Heltberg O, Holm A, Højbjerg T, Jensen KT, et al. Emergence of extended-spectrum β-lactamase (ESBL)-producing Klebsiella pneumoniae in Danish hospitals; this is in part explained by spread of two CTX-M-15 clones with multilocus sequence types 15 and 16 in Zealand. Int J Antimicrob Agents. 2011 Aug;38(2):180–182. https://doi.org/10.1016/j.ijantimicag.2011.03.018LesterCHOlsenSSJakobsenLArpiMFuurstedKHansenDSHeltbergOHolmAHøjbjergTJensenKT. Emergence of extended-spectrum β-lactamase (ESBL)-producing Klebsiella pneumoniae in Danish hospitals; this is in part explained by spread of two CTX-M-15 clones with multilocus sequence types 15 and 16 in Zealand. Int J Antimicrob Agents.2011Aug;38(2):180–182. https://doi.org/10.1016/j.ijantimicag.2011.03.01810.1016/j.ijantimicag.2011.03.01821612893Search in Google Scholar

Logan LK, Weinstein RA. The epidemiology of carbapenem-resistant Enterobacteriaceae: The impact and evolution of a global menace. J Infect Dis. 2017. 215(suppl_1):S28-S36.LoganLKWeinsteinRA. The epidemiology of carbapenem-resistant Enterobacteriaceae: The impact and evolution of a global menace. J Infect Dis.2017. 215(suppl_1):S28-S36.10.1093/infdis/jiw282585334228375512Search in Google Scholar

Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, Lynfield R, Maloney M, McAllister-Hollod L, Nadle J, et al.; Emerging Infections Program Healthcare-Associated Infections and Antimicrobial Use Prevalence Survey Team. Multistate point-prevalence survey of health care-associated infections. N Engl J Med. 2014 Mar 27;370(13):1198–1208. https://doi.org/10.1056/NEJMoa1306801MagillSSEdwardsJRBambergWBeldavsZGDumyatiGKainerMALynfieldRMaloneyMMcAllister-HollodLNadleJet al.; Emerging Infections Program Healthcare-Associated Infections and Antimicrobial Use Prevalence Survey Team. Multistate point-prevalence survey of health care-associated infections. N Engl J Med.2014Mar27;370(13):1198–1208. https://doi.org/10.1056/NEJMoa130680110.1056/NEJMoa1306801464834324670166Search in Google Scholar

Maltezou HC, Giakkoupi P, Maragos A, Bolikas M, Raftopoulos V, Papahatzaki H, Vrouhos G, Liakou V, Vatopoulos AC. Outbreak of infections due to KPC-2-producing Klebsiella pneumoniae in a hospital in Crete (Greece). J Infect. 2009 Mar;58(3):213–219. https://doi.org/10.1016/j.jinf.2009.01.010MaltezouHCGiakkoupiPMaragosABolikasMRaftopoulosVPapahatzakiHVrouhosGLiakouVVatopoulosAC. Outbreak of infections due to KPC-2-producing Klebsiella pneumoniae in a hospital in Crete (Greece). J Infect.2009Mar;58(3):213–219. https://doi.org/10.1016/j.jinf.2009.01.01010.1016/j.jinf.2009.01.01019246099Search in Google Scholar

Martin RM, Bachman MA. Colonization, infection, and the accessory genome of Klebsiella pneumoniae. Front Cell Infect Microbiol. 2018 Jan 22;8:4. https://doi.org/10.3389/fcimb.2018.00004MartinRMBachmanMA. Colonization, infection, and the accessory genome of Klebsiella pneumoniae. Front Cell Infect Microbiol.2018Jan22;8:4. https://doi.org/10.3389/fcimb.2018.0000410.3389/fcimb.2018.00004578654529404282Search in Google Scholar

Mathers AJ, Peirano G, Pitout JDD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015 Jul;28(3):565–591. https://doi.org/10.1128/CMR.00116-14MathersAJPeiranoGPitoutJDD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev.2015Jul;28(3):565–591. https://doi.org/10.1128/CMR.00116-1410.1128/CMR.00116-14440562525926236Search in Google Scholar

Nordmann P, Poirel L, Carrër A, Toleman MA, Walsh TR. How to detect NDM-1 producers. J Clin Microbiol. 2011 Feb 01;49(2): 718–721. https://doi.org/10.1128/JCM.01773-10NordmannPPoirelLCarrërATolemanMAWalshTR. How to detect NDM-1 producers. J Clin Microbiol.2011Feb01;49(2): 718–721. https://doi.org/10.1128/JCM.01773-1010.1128/JCM.01773-10304350721123531Search in Google Scholar

Papadimitriou-Olivgeris M, Marangos M, Fligou F, Christofidou M, Sklavou C, Vamvakopoulou S, Anastassiou ED, Filos KS. KPC-producing Klebsiella pneumoniae enteric colonization acquired during intensive care unit stay: the significance of risk factors for its development and its impact on mortality. Diagn Microbiol Infect Dis. 2013 Oct;77(2):169–173. https://doi.org/10.1016/j.diagmicrobio.2013.06.007Papadimitriou-OlivgerisMMarangosMFligouFChristofidouMSklavouCVamvakopoulouSAnastassiouEDFilosKS. KPC-producing Klebsiella pneumoniae enteric colonization acquired during intensive care unit stay: the significance of risk factors for its development and its impact on mortality. Diagn Microbiol Infect Dis.2013Oct;77(2):169–173. https://doi.org/10.1016/j.diagmicrobio.2013.06.00710.1016/j.diagmicrobio.2013.06.00723886789Search in Google Scholar

Qi Y, Wei Z, Ji S, Du X, Shen P, Yu Y. ST11, the dominant clone of KPC-producing Klebsiella pneumoniae in China. J Antimicrob Chemother. 2011 Feb;66(2):307–312. https://doi.org/10.1093/jac/dkq431QiYWeiZJiSDuXShenPYuY. ST11, the dominant clone of KPC-producing Klebsiella pneumoniae in China. J Antimicrob Chemother.2011Feb;66(2):307–312. https://doi.org/10.1093/jac/dkq43110.1093/jac/dkq43121131324Search in Google Scholar

Queenan AM, Bush K. Carbapenemases: the versatile β-Lactamases. Clin Microbiol Rev. 2007 Jul;20(3):440–458. https://doi.org/10.1128/CMR.00001-07QueenanAMBushK. Carbapenemases: the versatile β-Lactamases. Clin Microbiol Rev.2007Jul;20(3):440–458. https://doi.org/10.1128/CMR.00001-0710.1128/CMR.00001-07193275017630334Search in Google Scholar

Schwaber MJ, Klarfeld-Lidji S, Navon-Venezia S, Schwartz D, Leavitt A, Carmeli Y. Predictors of carbapenem-resistant Klebsiella pneumoniae acquisition among hospitalized adults and effect of acquisition on mortality. Antimicrob Agents Chemother. 2008 Mar;52(3):1028–1033. https://doi.org/10.1128/AAC.01020-07SchwaberMJKlarfeld-LidjiSNavon-VeneziaSSchwartzDLeavittACarmeliY. Predictors of carbapenem-resistant Klebsiella pneumoniae acquisition among hospitalized adults and effect of acquisition on mortality. Antimicrob Agents Chemother.2008Mar;52(3):1028–1033. https://doi.org/10.1128/AAC.01020-0710.1128/AAC.01020-07225852718086836Search in Google Scholar

Snitkin ES, Zelazny AM, Thomas PJ, Stock F, Henderson DK, Palmore TN, Segre JA; NISC Comparative Sequencing Program Group. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med. 2012 Aug 22;4(148):148ra116. https://doi.org/10.1126/scitranslmed.3004129SnitkinESZelaznyAMThomasPJStockFHendersonDKPalmoreTNSegreJA; NISC Comparative Sequencing Program Group. Tracking a hospital outbreak of carbapenem-resistant Klebsiella pneumoniae with whole-genome sequencing. Sci Transl Med.2012Aug22;4(148):148ra116. https://doi.org/10.1126/scitranslmed.300412910.1126/scitranslmed.3004129352160422914622Search in Google Scholar

Tian L, Zhang Z, Sun Z. Antimicrobial resistance trends in bloodstream infections at a large teaching hospital in China: a 20-year surveillance study (1998–2017). Antimicrob Resist Infect Control. 2019 Dec;8(1):86. https://doi.org/10.1186/s13756-019-0545-zTianLZhangZSunZ. Antimicrobial resistance trends in bloodstream infections at a large teaching hospital in China: a 20-year surveillance study (1998–2017). Antimicrob Resist Infect Control.2019Dec;8(1):86. https://doi.org/10.1186/s13756-019-0545-z10.1186/s13756-019-0545-z654053631161033Search in Google Scholar

uz Zaman T, Aldrees M, Al Johani SM, Alrodayyan M, Aldughashem FA, Balkhy HH. Multi-drug carbapenem-resistant Klebsiella pneumoniae infection carrying the OXA-48 gene and showing variations in outer membrane protein 36 causing an outbreak in a tertiary care hospital in Riyadh, Saudi Arabia. Int J Infect Dis. 2014 Nov;28:186–192. https://doi.org/10.1016/j.ijid.2014.05.021uz ZamanTAldreesMAl JohaniSMAlrodayyanMAldughashemFABalkhyHH. Multi-drug carbapenem-resistant Klebsiella pneumoniae infection carrying the OXA-48 gene and showing variations in outer membrane protein 36 causing an outbreak in a tertiary care hospital in Riyadh, Saudi Arabia. Int J Infect Dis.2014Nov;28:186–192. https://doi.org/10.1016/j.ijid.2014.05.02110.1016/j.ijid.2014.05.02125245001Search in Google Scholar

Vardakas KZ, Matthaiou DK, Falagas ME, Antypa E, Koteli A, Antoniadou E. Characteristics, risk factors and outcomes of carbapenem-resistant Klebsiella pneumoniae infections in the intensive care unit. J Infect. 2015 Jun;70(6):592–599. https://doi.org/10.1016/j.jinf.2014.11.003VardakasKZMatthaiouDKFalagasMEAntypaEKoteliAAntoniadouE. Characteristics, risk factors and outcomes of carbapenem-resistant Klebsiella pneumoniae infections in the intensive care unit. J Infect.2015Jun;70(6):592–599. https://doi.org/10.1016/j.jinf.2014.11.00310.1016/j.jinf.2014.11.00325447713Search in Google Scholar

Wang Z, Li M, Shen X, Wang L, Liu L, Hao Z, Duan J, Yu F. Outbreak of blaNDM-5 -Harboring Klebsiella pneumoniae ST290 in a Tertiary Hospital in China. Microb Drug Resist. 2019 Dec 01;25(10):1443–1448. https://doi.org/10.1089/mdr.2019.0046WangZLiMShenXWangLLiuLHaoZDuanJYuF. Outbreak of bla_NDM-5 -Harboring Klebsiella pneumoniae ST290 in a Tertiary Hospital in China. Microb Drug Resist.2019Dec01;25(10):1443–1448. https://doi.org/10.1089/mdr.2019.004610.1089/mdr.2019.004631334685Search in Google Scholar

WHO. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics [Internet]. Geneva (Switzerland): World Health Organization; 2017 [cited 2017 February 27]. Available from https://www.who.int/medicines/publications/global-priority-list-antibiotic-resistant-bacteria/en/WHO. Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics [Internet]. Geneva (Switzerland): World Health Organization; 2017[cited 2017 February 27]. Available fromhttps://www.who.int/medicines/publications/global-priority-list-antibiotic-resistant-bacteria/en/Search in Google Scholar

Wu W, Feng Y, Tang G, Qiao F, McNally A, Zong Z. NDM metallo-β-Lactamases and their bacterial producers in health care settings. Clin Microbiol Rev. 2019 Jan 30;32(2):e00115-18. https://doi.org/10.1128/CMR.00115-18WuWFengYTangGQiaoFMcNallyAZongZ. NDM metallo-β-Lactamases and their bacterial producers in health care settings. Clin Microbiol Rev.2019Jan30;32(2):e00115-18. https://doi.org/10.1128/CMR.00115-1810.1128/CMR.00115-18643112430700432Search in Google Scholar

Yong D, Toleman MA, Giske CG, Cho HS, Sundman K, Lee K, Walsh TR. Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother. 2009 Dec;53(12): 5046–5054. https://doi.org/10.1128/AAC.00774-09YongDTolemanMAGiskeCGChoHSSundmanKLeeKWalshTR. Characterization of a new metallo-beta-lactamase gene, bla(NDM-1), and a novel erythromycin esterase gene carried on a unique genetic structure in Klebsiella pneumoniae sequence type 14 from India. Antimicrob Agents Chemother.2009Dec;53(12): 5046–5054. https://doi.org/10.1128/AAC.00774-0910.1128/AAC.00774-09278635619770275Search in Google Scholar

Yu F, Hu L, Zhong Q, Hang Y, Liu Y, Hu X, Ding H, Chen Y, Xu X, Fang X, et al. Dissemination of Klebsiella pneumoniae ST11 isolates with carbapenem resistance in integrated and emergency intensive care units in a Chinese tertiary hospital. J Med Microbiol. 2019 Jun 01;68(6):882–889. https://doi.org/10.1099/jmm.0.000981YuFHuLZhongQHangYLiuYHuXDingHChenYXuXFangX. Dissemination of Klebsiella pneumoniae ST11 isolates with carbapenem resistance in integrated and emergency intensive care units in a Chinese tertiary hospital. J Med Microbiol.2019Jun01;68(6):882–889. https://doi.org/10.1099/jmm.0.00098110.1099/jmm.0.00098131050634Search in Google Scholar

Yu F, Ying Q, Chen C, Li T, Ding B, Liu Y, Lu Y, Qin Z, Parsons C, Salgado C, et al. Outbreak of pulmonary infection caused by Klebsiella pneumoniae isolates harbouring blaIMP-4 and blaDHA-1 in a neonatal intensive care unit in China. J Med Microbiol. 2012 Jul 01;61(7):984–989. https:0/doi.org/10.1099/jmm.0.043000-0YuFYingQChenCLiTDingBLiuYLuYQinZParsonsCSalgadoC. Outbreak of pulmonary infection caused by Klebsiella pneumoniae isolates harbouring bla_IMP-4 and bla_DHA-1 in a neonatal intensive care unit in China. J Med Microbiol.2012Jul01;61(7):984–989. https:0/doi.org/10.1099/jmm.0.043000-010.1099/jmm.0.043000-022466031Search in Google Scholar

Zhang P, Shi Q, Hu H, Hong B, Wu X, Du X, Akova M, Yu Y. Emergence of ceftazidime/avibactam resistance in carbapenem-resistant Klebsiella pneumoniae in China. Clin Microbiol Infect. 2020 Jan;26(1):124.e1-124.e4. https://doi.org/10.1016/j.cmi.2019.08.020ZhangPShiQHuHHongBWuXDuXAkovaMYuY. Emergence of ceftazidime/avibactam resistance in carbapenem-resistant Klebsiella pneumoniae in China. Clin Microbiol Infect.2020Jan;26(1):124.e1-124.e4. https://doi.org/10.1016/j.cmi.2019.08.02010.1016/j.cmi.2019.08.02031494252Search in Google Scholar

Zhang R, Wang XD, Cai JC, Zhou HW, Lv HX, Hu QF, Chen GX. Outbreak of Klebsiella pneumoniae carbapenemase 2-producing K. pneumoniae with high qnr prevalence in a Chinese hospital. J Med Microbiol. 2011 Jul 01;60(7):977–982. https://doi.org/10.1099/jmm.0.015826-0ZhangRWangXDCaiJCZhouHWLvHXHuQFChenGX. Outbreak of Klebsiella pneumoniae carbapenemase 2-producing K. pneumoniae with high qnr prevalence in a Chinese hospital. J Med Microbiol.2011Jul01;60(7):977–982. https://doi.org/10.1099/jmm.0.015826-010.1099/jmm.0.015826-021393450Search in Google Scholar