Characteristics of non-carbapenemase producing carbapenem-resistant Klebsiella pneumoniae from a tertiary hospital in China

Authors

  • Yongchun Ruan Department of Infectious Diseases, Shaoxing People’s Hospital (Shaoxing Hospital, Zhejiang University School of Medicine), Shaoxing, Zhejiang, China
  • Minghui Li Department of Infectious Diseases, Shaoxing People’s Hospital (Shaoxing Hospital, Zhejiang University School of Medicine), Shaoxing, Zhejiang, China
  • Dan Wang Department of Infectious Diseases, Shaoxing People’s Hospital (Shaoxing Hospital, Zhejiang University School of Medicine), Shaoxing, Zhejiang, China
  • Jinnan Duan Department of Infectious Diseases, Shaoxing People’s Hospital (Shaoxing Hospital, Zhejiang University School of Medicine), Shaoxing, Zhejiang, China
  • Haiwang Zhang Department of Infectious Diseases, Shaoxing People’s Hospital (Shaoxing Hospital, Zhejiang University School of Medicine), Shaoxing, Zhejiang, China
  • Yiqing Zhou Department of Infectious Diseases, Shaoxing People’s Hospital (Shaoxing Hospital, Zhejiang University School of Medicine), Shaoxing, Zhejiang, China https://orcid.org/0000-0002-5286-7939

DOI:

https://doi.org/10.3855/jidc.17779

Keywords:

Klebsiella pneumoniae, ertapenem, resistance, virulence, epidemiology

Abstract

Introduction: The spread of carbapenem-resistant Klebsiella pneumoniae (CRKP) is a substantial severe global public health burden. Non-carbapenemase-producing CRKP (non-CP-CRKP) is increasingly recognized as the source of severe infections.

Methodology: We analyzed the genotypic, and phenotypic profiles of non-CP-CRKP strains with the whole-genome sequences isolated between 2017 and 2019 and the clinical characterization of non-CP-CRKP infection.

Results: A total of 91 CRKP strains were collected, of which 5 (5.49%) strains were non-CP-CRKP. Four strains were from male patients; three strains were isolated from the bile of patients who underwent biliary interventional surgery and four had a history of antibiotic exposure. Three strains were sequence type (ST)11, one was ST1, and one was ST5523. The non-CP-CRKP strains were insusceptible to ertapenem. Three strains were susceptible to amikacin. All the strains were susceptible to imipenem, meropenem, tigecycline, ceftazidime/avibatam and polymyxin B. The β-lactamases of non-CP-CRKP predominantly included blaCTX-M, blaSHV, and blaTEM subtypes. Two site mutations in ompK36 (p.A217S and p.N218H) and four in ompK37 (p.I70M, p.I128M, p.N230G, and m233_None234insQ) were detected accounting for carbapenem resistance. Plasmids IncFI and IncFII were found in most strains. Genes encoding aerobactin, yersiniabactin and allantoin utilization were not detected in several isolates, and all non-CP-CRKP strains did not carry rmpA gene.

Conclusions: Non-CP-CRKP infected patients had a history of previous antibiotic exposure or invasive procedures. Non-CP-CRKP strains were insusceptible to ertapenem. The mechanism of resistance includes β-lactamases production and the site mutations in ompK36 and ompK37. Several virulence genes were not detected in non-CP-CRKP.

References

Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, Pulcini C, Kahlmeter G, Kluytmans J, Carmeli Y, Ouellette M, Outterson K, Patel J, Cavaleri M, Cox EM, Houchens CR, Grayson ML, Hansen P, Singh N, Theuretzbacher U, Magrini N, Aboderin AO, Al-Abri SS, Awang Jalil N, Benzonana N, Bhattacharya S, Brink AJ, Burkert FR, Cars O, Cornaglia G, Dyar OJ, Friedrich AW, Gales AC, Gandra S, Giske CG, Goff DA, Goossens H, Gottlieb T, Guzman Blanco M, Hryniewicz W, Kattula D, Jinks T, Kanj SS, Kerr L, Kieny M-P, Kim YS, Kozlov RS, Labarca J, Laxminarayan R, Leder K, Leibovici L, Levy-Hara G, Littman J, Malhotra-Kumar S, Manchanda V, Moja L, Ndoye B, Pan A, Paterson DL, Paul M, Qiu H, Ramon-Pardo P, Rodríguez-Baño J, Sanguinetti M, Sengupta S, Sharland M, Si-Mehand M, Silver LL, Song W, Steinbakk M, Thomsen J, Thwaites GE, van der Meer JWM, Van Kinh N, Vega S, Villegas MV, Wechsler-Fördös A, Wertheim HFL, Wesangula E, Woodford N, Yilmaz FO, Zorzet A (2018) Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 18: 318-327. doi: 10.1016/S1473-3099(17)30753-3.

Zhang YW, Wang Q, Yin YY, Chen HB, Jin LY, Gu B, Xie LY, Yang CX, Ma XB, Li HY, Li W, Zhang XQ, Liao K, Man S, Wang S, Wen H, Li B, Guo Z, Tian J, Pei F, Liu L, Zhang L, Zou C, Hu T, Cai J, Yang H, Huang J, Jia X, Huang W, Cao B, Wang H (2018) Epidemiology of carbapenem-resistant Enterobacteriaceae infections: report from the China CRE Network. Antimicrob Agents Chemother 62: e01882-01817. doi: 10.1128/AAC.01882-17.

Hu FP, Guo Y, Zhu DM, Wang F, Jiang XF, Xu YC, Zhang XJ, Zhang ZX, Ji P, Xie Y, Kang M, Wang CQ, Wang A, Yuanhong X, Ying H, Ziyong S, Zhongju C, Yuxing N, Jingyong S, Yunzhuo C, Sufei T, Zhidong H, Jin L, Yunsong Y, Jie L, Bin S, Yan D, Sufang G, Lianhua W, Fengmei Z, Hong Z, Chun W, Yunjian H, Xiaoman A, Chao Z, Danhong S, Dawen G, Jinying Z, Hua Y, Xiangning H, Wen'en L, Yanming L, Yan J, Chunhong S, Xuesong X, Chao Y, Shanmei W, Yafei C, Lixia Z, Juan M, Shuping Z, Yan Z, Lei Z, Jinhua M, Fang D, Hongyan Z, Fangfang H, Han S, Wanqing Z, Wei J, Gang L, Jinsong W, Yuemei L, Jihong L, Jinju D, Jianbang K, Xiaobo M, Yanping Z, Ruyi G, Yan Z, Yunsheng C, Qing M, Shifu W, Xuefei H, Jilu S, Ruizhong W, Hua F, Bixia Y, Yong Z, Ping G, Kaizhen W, Yirong Z, Jiangshan L, Longfeng L, Hongqin G, Lin J, Wen H, Shunhong X, Jiao F, Rui D, Chunlei Y (2021) CHINET surveillance of bacterial resistance: results of 2020. Chin J Infect Chemother 21: 377-387.

Suay-Garcia B, Perez-Gracia MT (2019) Present and future of carbapenem-resistant Enterobacteriaceae (CRE) infections. Antibiotics (Basel) 8: 122. doi: 10.3390/antibiotics8030122.

Black CA, So W, Dallas SS, Gawrys G, Benavides R, Aguilar S, Chen CJ, Shurko JF, Lee GC (2020) Predominance of non-carbapenemase producing carbapenem-resistant Enterobacterales in South Texas. Front Microbiol 11: 623574. doi: 10.3389/fmicb.2020.623574.

van Duin D, Arias CA, Komarow L, Chen L, Hanson BM, Weston G, Cober E, Garner OB, Jacob JT, Satlin MJ, Fries BC, Garcia-Diaz J, Doi Y, Dhar S, Kaye KS, Earley M, Hujer AM, Hujer KM, Domitrovic TN, Shropshire WC, Dinh A, Manca C, Luterbach CL, Wang M, Paterson DL, Banerjee R, Patel R, Evans S, Hill C, Arias R, Chambers HF, Fowler VG, Kreiswirth BN, Bonomo RA (2020) Molecular and clinical epidemiology of carbapenem-resistant Enterobacterales in the USA (CRACKLE-2): a prospective cohort study. Lancet Infect Dis 20: 731-741. doi: 10.1016/S1473-3099(19)30755-8.

Jean SS, Hsueh PR, Group SA-P (2020) Antimicrobial susceptibilities of the ertapenem-non-susceptible non-carbapenemase-producing Enterobacterales isolates causing intra-abdominal infections in the Asia-Pacific region during 2008-2014: results from the study for monitoring the antimicrobial resistance trends (SMART). J Glob Antimicrob Resist 21: 91-98. doi: 10.1016/j.jgar.2019.10.004.

Teo J, Cai YY, Tang S, Lee W, Tan TY, Tan TT, Kwa AL (2012) Risk factors, molecular epidemiology and outcomes of ertapenem-resistant, carbapenem-susceptible Enterobacteriaceae: a case-case-control study. PLoS One 7: e34254. doi: 10.1371/journal.pone.0034254.

Yeh KM, Kurup A, Siu LK, Koh YL, Fung CP, Lin JC, Chen TL, Chang FY, Koh TH (2007) Capsular serotype K1 or K2, rather than magA and rmpA, is a major virulence determinant for Klebsiella pneumoniae liver abscess in Singapore and Taiwan. J Clin Microbiol 45: 466-471. doi: 10.1128/JCM.01150-06.

Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, Jenney A, Connor TR, Hsu LY, Severin J, Brisse S, Cao H, Wilksch J, Gorrie C, Schultz MB, Edwards DJ, Nguyen KV, Nguyen TV, Dao TT, Mensink M, Minh VL, Nhu NT, Schultsz C, Kuntaman K, Newton PN, Moore CE, Strugnell RA, Thomson NR (2015) Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci USA 112: E3574-3581. doi: 10.1073/pnas.1501049112.

Gu D, Dong N, Zheng Z, Lin D, Huang M, Wang L, Chan EW-C, Shu L, Yu J, Zhang R, Chen S (2018) A fatal outbreak of ST11 carbapenem-resistant hypervirulent Klebsiella pneumoniae in a Chinese hospital: a molecular epidemiological study. Lancet Infect Dis 18: 37-46. doi: 10.1016/S1473-3099(17)30489-9.

Liao WJ, Liu Y, Zhang W (2020) Virulence evolution, molecular mechanisms of resistance and prevalence of ST11 carbapenem-resistant Klebsiella pneumoniae in China: a review over the last 10 years. J Glob Antimicrob Resist 23: 174-180. doi: 10.1016/j.jgar.2020.09.004.

Lan P, Jiang Y, Zhou JC, Yu YS (2021) A global perspective on the convergence of hypervirulence and carbapenem resistance in Klebsiella pneumoniae. J Glob Antimicrob Resist 25: 26-34. doi: 10.1016/j.jgar.2021.02.020.

Wyres KL, Lam MMC, Holt KE (2020) Population genomics of Klebsiella pneumoniae. Nat Rev Microbiol 18: 344-359. doi: 10.1038/s41579-019-0315-1.

Clinical and Laboratory Standards Institute (CLSI) (2019) Performance standards for antimicrobial susceptibility testing, M100 29th edition. Wayne, PA.

Centers for Disease Control and Prevention Facility (2015) Guidance for control of carbapenem-resistant Enterobacteriaceae (CRE) - November 2015 update - CRE toolkit. Available: https://www.cdc.gov/infectioncontrol/guidelines/pdf/cre/CRE-guidance-508.pdf. Accessed: 11 December 2022.

Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13: e1005595. doi: 10.1371/journal.pcbi.1005595.

Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, Meyer F, Olsen GJ, Olson R, Osterman AL, Overbeek RA, McNeil LK, Paarmann D, Paczian T, Parrello B, Pusch GD, Reich C, Stevens R, Vassieva O, Vonstein V, Wilke A, Zagnitko O (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9: 75. doi: 10.1186/1471-2164-9-75.

Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, Jelsbak L, Sicheritz-Pontén T, Ussery DW, Aarestrup FM, Lund O (2012) Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol 50: 1355-1361. doi: 10.1128/JCM.06094-11.

Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, Philippon A, Allesoe RL, Rebelo AR, Florensa AF, Fagelhauer L, Chakraborty T, Neumann B, Werner G, Bender JK, Stingl K, Nguyen M, Coppens J, Xavier BB, Malhotra-Kumar S, Westh H, Pinholt M, Anjum MF, Duggett NA, Kempf I, Nykäsenoja S, Olkkola S, Wieczorek K, Amaro A, Clemente L, Mossong J, Losch S, Ragimbeau C, Lund O, Aarestrup FM (2020) ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 75: 3491-3500. doi: 10.1093/jac/dkaa345.

Carattoli A, Zankari E, García-Fernández A, Voldby Larsen M, Lund O, Villa L, Møller Aarestrup F, Hasman H (2014) In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob Agents Chemother 58: 3895-3903. doi: 10.1128/AAC.02412-14.

Liu B, Zheng D, Zhou S, Chen L, Yang J (2022) VFDB 2022: a general classification scheme for bacterial virulence factors. Nucleic Acids Res 50: D912-D917. doi: 10.1093/nar/gkab1107.

Kaas RS, Leekitcharoenphon P, Aarestrup FM, Lund O (2014) Solving the problem of comparing whole bacterial genomes across different sequencing platforms. PLoS One 9: e104984. doi: 10.1371/journal.pone.0104984.

Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49: W293-w296. doi: 10.1093/nar/gkab301.

National Center for Biotechnology Information, National Library of Medicine (US) (1988) National Center for Biotechnology Information. Available: https://www.ncbi.nlm.nih.gov/. Accessed: 19 January 2021.

Doi Y (2019) Treatment options for carbapenem-resistant Gram-negative bacterial infections. Clin Infect Dis 69 Suppl 7: S565-S575. doi: 10.1093/cid/ciz830.

Bonomo RA, Burd EM, Conly J, Limbago BM, Poirel L, Segre JA, Westblade LF (2018) Carbapenemase-producing organisms: a global scourge. Clin Infect Dis 66: 1290-1297. doi: 10.1093/cid/cix893.

Su CF, Chuang C, Lin YT, Chan YJ, Lin JC, Lu PL, Huang CT, Wang JT, Chuang YC, Siu LK, Fung CP (2018) Treatment outcome of non-carbapenemase-producing carbapenem-resistant Klebsiella pneumoniae infections: a multicenter study in Taiwan. Eur J Clin Microbiol Infect Dis 37: 651-659. doi: 10.1007/s10096-017-3156-8.

McGettigan SE, Andreacchio K, Edelstein PH (2009) Specificity of ertapenem susceptibility screening for detection of Klebsiella pneumoniae carbapenemases. J Clin Microbiol 47: 785-786. doi: 10.1128/JCM.02143-08.

Hyle EP, Ferraro MJ, Silver M, Lee H, Hooper DC (2010) Ertapenem-resistant Enterobacteriaceae: risk factors for acquisition and outcomes. Infect Control Hosp Epidemiol 31: 1242-1249. doi: 10.1086/657138.

Lim CL-L, Lee W, Lee AL-C, Liew LT-T, Nah SC, Wan CN, Chlebicki MP, Kwa AL-H (2013) Evaluation of ertapenem use with impact assessment on extended-spectrum beta-lactamases (ESBL) production and Gram-negative resistance in Singapore General Hospital (SGH). BMC Infect Dis 13: 523. doi: 10.1186/1471-2334-13-523.

Tangden T, Adler M, Cars O, Sandegren L, Lowdin E (2013) Frequent emergence of porin-deficient subpopulations with reduced carbapenem susceptibility in ESBL-producing Escherichia coli during exposure to ertapenem in an in vitro pharmacokinetic model. J Antimicrob Chemother 68: 1319-1326. doi: 10.1093/jac/dkt044.

Jean SS, Lee WS, Hsueh PR, Group SA-P (2018) Ertapenem non-susceptibility and independent predictors of the carbapenemase production among the Enterobacteriaceae isolates causing intra-abdominal infections in the Asia-Pacific region: results from the study for monitoring antimicrobial resistance trends (SMART). Infect Drug Resist 11: 1881-1891. doi: 10.2147/IDR.S181085.

Hawser SP, Bouchillon SK, Lascols C, Hackel M, Hoban DJ, Badal RE, Woodford N, Livermore DM (2011) Susceptibility of Klebsiella pneumoniae isolates from intra-abdominal infections and molecular characterization of ertapenem-resistant isolates. Antimicrob Agents Chemother 55: 3917-3921. doi: 10.1128/AAC.00070-11.

Rodrigues C, Machado E, Ramos H, Peixe L, Novais A (2014) Expansion of ESBL-producing Klebsiella pneumoniae in hospitalized patients: a successful story of international clones (ST15, ST147, ST336) and epidemic plasmids (IncR, IncFIIK). Int J Med Microbiol 304: 1100-1108. doi: 10.1016/j.ijmm.2014.08.003.

Muggeo A, Guillard T, Klein F, Reffuveille F, Francois C, Babosan A, Bajolet O, Bertrand X, de Champs C, CarbaFrEst G (2018) Spread of Klebsiella pneumoniae ST395 non-susceptible to carbapenems and resistant to fluoroquinolones in North-Eastern France. J Glob Antimicrob Resist 13: 98-103. doi: 10.1016/j.jgar.2017.10.023.

Al-Agamy MH, Aljallal A, Radwan HH, Shibl AM (2018) Characterization of carbapenemases, ESBLs, and plasmid-mediated quinolone determinants in carbapenem-insensitive Escherichia coli and Klebsiella pneumoniae in Riyadh hospitals. J Infect Public Health 11: 64-68. doi: 10.1016/j.jiph.2017.03.010.

Shields RK, Clancy CJ, Press EG, Nguyen MH (2016) Aminoglycosides for treatment of bacteremia due to carbapenem-resistant Klebsiella pneumoniae. Antimicrob Agents Chemother 60: 3187-3192. doi: 10.1128/AAC.02638-15.

Hu F, Guo Y, Zhu DM, Wang F, Jiang XF, Xu YC, Zhang XJ, Zhang ZX, Ji P, Xie Y, Kang M, Wang CQ, Wang AM, Xu YH, Huang Y, Sun ZY, Chen ZJ, Ni YX, Sun JY, Chu YZ, Tian SF, Hu ZD, Li J, Yu YS, Lin J, Shan B, Du Y, Guo SF, Wei LH, Zou FM, Zhang H, Wang C, Hu YJ, Ai XM, Zhuo C, Su DH, Guo DW, Zhao JY, Yu H, Huang XN, Liu WE, Li YM, Jin Y, Shao CH, Xu XS, Yan C, Wang SM, Chu YF, Zhang LX, Ma J, Zhou SP, Zhou Y, Zhu L, Meng JH, Dong F, Zheng HY, Hu FF, Shen H, Zhou WQ, Jia W, Li G, Wu JS, Lu YM, Li JH, Duan JJ, Kang JB, Ma XB, Zheng YP, Guo RY, Zhu Y, Chen YS, Meng Q (2020) CHINET surveillance of bacterial resistance across tertiary hospitals in 2019. Chin J Infect Chemother 20: 233-243.

Nasiri G, Peymani A, Farivar TN, Hosseini P (2018) Molecular epidemiology of aminoglycoside resistance in clinical isolates of Klebsiella pneumoniae collected from Qazvin and Tehran provinces, Iran. Infect Genet Evol 64: 219-224. doi: 10.1016/j.meegid.2018.06.030.

Juan CH, Huang YW, Lin YT, Yang TC, Wang FD (2016) Risk factors, outcomes, and mechanisms of tigecycline-nonsusceptible Klebsiella pneumoniae bacteremia. Antimicrob Agents Chemother 60: 7357-7363. doi: 10.1128/AAC.01503-16.

Ye MP, Ding BX, Qian HL, Xu QQ, Jiang J, Huang JW, Ou HY, Hu FP, Wang MG (2017) In vivo development of tigecycline resistance in Klebsiella pneumoniae owing to deletion of the ramR ribosomal binding site. Int J Antimicrob Agents 50: 523-528. doi: 10.1016/j.ijantimicag.2017.04.024.

Chew KL, Lin RTP, Teo JWP (2017) Klebsiella pneumoniae in Singapore: hypervirulent infections and the carbapenemase threat. Front Cell Infect Microbiol 7: 515. doi: 10.3389/fcimb.2017.00515.

Karlsson M, Stanton RA, Ansari U, McAllister G, Chan MY, Sula E, Grass JE, Duffy N, Anacker ML, Witwer ML, Rasheed JK, Elkins CA, Halpin AL (2019) Identification of a carbapenemase-producing hypervirulent Klebsiella pneumoniae isolate in the United States. Antimicrob Agents Chemother 63: e00519-00519. doi: 10.1128/AAC.00519-19.

Zhu J, Wang T, Chen L, Du H (2021) Virulence factors in hypervirulent Klebsiella pneumoniae. Front Microbiol 12: 642484. doi: 10.3389/fmicb.2021.642484.

Martin RM, Bachman MA (2018) Colonization, infection, and the accessory genome of Klebsiella pneumoniae. Front Cell Infect Microbiol 8: 4. doi: 10.3389/fcimb.2018.00004.

Zhang YW, Zhao CJ, Wang Q, Wang XJ, Chen HB, Li HN, Zhang FF, Li SG, Wang RB, Wang H (2016) High prevalence of hypervirulent Klebsiella pneumoniae infection in China: geographic distribution, clinical characteristics, and antimicrobial resistance. Antimicrob Agents Chemother 60: 6115-6120. doi: 10.1128/AAC.01127-16.

Russo TA, MacDonald U (2020) The Galleria mellonella infection model does not accurately differentiate between hypervirulent and classical Klebsiella pneumoniae. mSphere 5: e00850-00819. doi: 10.1128/mSphere.00850-19.

Hu D, Li Y, Ren P, Tian D, Chen W, Fu P, Wang W, Li X, Jiang X (2021) Molecular epidemiology of hypervirulent carbapenemase-producing Klebsiella pneumoniae. Front Cell Infect Microbiol 11: 661218. doi: 10.3389/fcimb.2021.661218.

Hsieh PF, Lin TL, Lee CZ, Tsai SF, Wang JT (2008) Serum-induced iron-acquisition systems and TonB contribute to virulence in Klebsiella pneumoniae causing primary pyogenic liver abscess. J Infect Dis 197: 1717-1727. doi: 10.1086/588383.

Chou HC, Lee CZ, Ma LC, Fang CT, Chang SC, Wang JT (2004) Isolation of a chromosomal region of Klebsiella pneumoniae associated with allantoin metabolism and liver infection. Infect Immun 72: 3783-3792. doi: 10.1128/IAI.72.7.3783-3792.2004.

Wang MG, Earley M, Chen L, Hanson BM, Yu YS, Liu ZY, Salcedo S, Cober E, Li LJ, Kanj SS, Gao H, Munita JM, Ordoñez K, Weston G, Satlin MJ, Valderrama-Beltrán SL, Marimuthu K, Stryjewski ME, Komarow L, Luterbach C, Marshall SH, Rudin SD, Manca C, Paterson DL, Reyes J, Villegas MV, Evans S, Hill C, Arias R, Baum K, Fries BC, Doi Y, Patel R, Kreiswirth BN, Bonomo RA, Chambers HF, Fowler VG, Arias CA, van Duin D, Abbo LM, Anderson DJ, Arias R, Arias CA, Baum K, Bonomo RA, Chambers HF, Chen L, Chew KL, Cober E, Cross HR, De PP, Desai S, Dhar S, Di Castelnuovo V, Diaz L, Dinh AQ, Doi Y, Earley M, Eilertson B, Evans B, Evans S, Fowler Jr VG, Fries BC, Gao H, Garcia-Diaz J, Garner OB, Greenwood-Quaintance K, Hanson B, Herc E, Hill C, Jacob JT, Jiang J, Kalayjian RC, Kanj SS, Kaye KS, Kim A, Komarow L, Kreiswirth BN, Lauterbach C, Li L, Liu Z, Manca C, Marimuthu K, Marshall SH, McCarty T, Munita J, Ng OT, Oñate Gutierrez JM, Ordoñez K, Patel R, Paterson DL, Peleg A, Reyes J, Rudin SD, Salata RA, Salcedo S, Satlin MJ, Schmidt-Malan S, Smitasin N, Spencer M, Stryjewski M, Su J, Tambyah PA, Valderrama S, van Duin D, Villegas Botero MV, Wang M, Waters M, Weston G, Wong D, Wortmann G, Yang Y, Yu Y, Zhang F (2021) Clinical outcomes and bacterial characteristics of carbapenem-resistant Klebsiella pneumoniae complex among patients from different global regions (CRACKLE-2): a prospective, multicentre, cohort study. Lancet Infect Dis 22: 401-412. doi: 10.1016/S1473-3099(21)00399-6.s

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2024-01-31

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Ruan Y, Li M, Wang D, Duan J, Zhang H, Zhou Y (2024) Characteristics of non-carbapenemase producing carbapenem-resistant Klebsiella pneumoniae from a tertiary hospital in China. J Infect Dev Ctries 18:106–115. doi: 10.3855/jidc.17779

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