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Published in: BMC Infectious Diseases 1/2018

Open Access 01-12-2018 | Research article

Molecular characterization and epidemiology of carbapenem non-susceptible Enterobacteriaceae isolated from the Eastern region of Heilongjiang Province, China

Authors: Xue Gong, Jisheng Zhang, Shanshan Su, Yanjun Fu, Mingjia Bao, Yong Wang, Xiaoli Zhang

Published in: BMC Infectious Diseases | Issue 1/2018

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Abstract

Background

The aim of this study was to elucidate the molecular epidemiology of carbapenem non-susceptible Enterobacteriaceae(CNSE) isolated in the Eastern region of Heilongjiang Province, China, and the mechanism of carbapenem resistance.

Methods

A total of 53 CNSE isolates were collected in a grade-3 hospital in Heilongjiang province. Sensitivity to antibiotics was determined using the VITEK-2 Compact automatic system. The modified Hodge test (MHT) and modified carbapenem inactivation test (mCIM) were performed for phenotypic identification. Beta-lactamases gene were detected by Polymerase chain reaction(PCR) and DNA sequencing. The transfer of blaNDM and blaKPC was investigated through conjugation experiment. The clinical data of patients were retrospectively reviewed. Homology of Carbapenem-resistant Klebsiella pneumoniae(CRKP) was conducted by multilocus sequence typing (MLST).

Results

CNSE were highly resistant to the majority of antimicrobial agents. The resistance rate was 100% for first, third, fourth generation cephalosporins and enzyme inhibitor compounds. Gentamicin and tobramycin recorded a resistance rate higher than 80%. Less than 30% resistance was detected for amikacin and levofloxacin. Among CNSE 52(98.1%) and 48(90.6%) of CNSE were positive for mCIM and MHT respectively. There were 42 positive blaKPC genes, three blaNDM-1 genes, three blaNDM-5 genes, one blaNDM-7 gene, and six blaIMP-4 genes. Most isolates harbored multiple drug resistance gene, especially as related to extended-spectrum-β-lactamases, blaSHV, blaTEM and blaCTX-M-15 genes.The resistant gene was transferred into recipient Escherichia coli J53 through conjugation in 21.3% (10/47) of the strains. MLST revealed that ST76 (n = 36) was the most predominant clone, followed by ST896, ST323 and ST11. A new one ST 2946 was identity by this study.

Conclusion

The carbapenem resistance phenomenon is alarming and blaKPC-2 is the main resistant gene of CNSE in our hospital. This is the first report of an outbreak caused by blaKPC-2 positive K. pneumoniae ST76 in the Eastern region of Heilongjiang Province, China. Relevant departments should implement infection control and prevention measures to avoid further dissemination of the multi drug-resistant bacteria (MDR).
Literature
1.
go back to reference Falagas ME, Tansarli GS, Karageorgopoulos DE, Vardakas KZ. Deaths attributable to carbapenem-resistant Enterobacteriaceae infections. Emerg Infect Dis. 2014;20(7):1170–5.CrossRefPubMedPubMedCentral Falagas ME, Tansarli GS, Karageorgopoulos DE, Vardakas KZ. Deaths attributable to carbapenem-resistant Enterobacteriaceae infections. Emerg Infect Dis. 2014;20(7):1170–5.CrossRefPubMedPubMedCentral
2.
go back to reference Papadimitriou-Olivgeris M, Marangos M, Fligou F, Christofidou M, Bartzavali C, Anastassiou ED, Filos KS. Risk factors for KPC-producing Klebsiella pneumoniae enteric colonization upon ICU admission. J Antimicrob Chemother. 2012;67(12):2976–81.CrossRefPubMed Papadimitriou-Olivgeris M, Marangos M, Fligou F, Christofidou M, Bartzavali C, Anastassiou ED, Filos KS. Risk factors for KPC-producing Klebsiella pneumoniae enteric colonization upon ICU admission. J Antimicrob Chemother. 2012;67(12):2976–81.CrossRefPubMed
3.
go back to reference Xu Y, Gu B, Huang M, Liu H, Xu T, Xia W, Wang T. Epidemiology of carbapenem resistant Enterobacteriaceae (CRE) during 2000-2012 in Asia. Thoracic disease. 2015;7(3):376–85. Xu Y, Gu B, Huang M, Liu H, Xu T, Xia W, Wang T. Epidemiology of carbapenem resistant Enterobacteriaceae (CRE) during 2000-2012 in Asia. Thoracic disease. 2015;7(3):376–85.
4.
go back to reference Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, 27th ed CLSI supplement M100. Clinical and laboratory standards institute. Wayne: Clinical and Laboratory Standards Institute; 2017. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, 27th ed CLSI supplement M100. Clinical and laboratory standards institute. Wayne: Clinical and Laboratory Standards Institute; 2017.
5.
go back to reference Zhang JX. Study on bacterial resistance and transmission mechanism of carbapenem non-susceptible Enterobacteriaceae[D]. Beijing: Peking Union Medical College Hospital; 2012. Zhang JX. Study on bacterial resistance and transmission mechanism of carbapenem non-susceptible Enterobacteriaceae[D]. Beijing: Peking Union Medical College Hospital; 2012.
6.
go back to reference Yang QW. Epidemiology and drug resistance mechanism of carbapenem resistant Enterobacteriaceae in China [D]. Beijing: Peking Union Medical College Hospital; 2015. Yang QW. Epidemiology and drug resistance mechanism of carbapenem resistant Enterobacteriaceae in China [D]. Beijing: Peking Union Medical College Hospital; 2015.
7.
go back to reference Pu SL. Resistance Mechanism and Molecular Epidemiology of Carbapenem - resistant Klebsiell pneumoniae.[D]. Chongqing: Chongqing Medical University; 2015. Pu SL. Resistance Mechanism and Molecular Epidemiology of Carbapenem - resistant Klebsiell pneumoniae.[D]. Chongqing: Chongqing Medical University; 2015.
8.
go back to reference Wang X, Chen G, Wu X, et al. Increased prevalence of carbapenem resistant Enterobacteriaceae in hospital setting due to cross-species transmission of the blaNDM-1 element and clonal spread of progenitor resistant strains. Front Microbiol. 2015;6:595. Wang X, Chen G, Wu X, et al. Increased prevalence of carbapenem resistant Enterobacteriaceae in hospital setting due to cross-species transmission of the blaNDM-1 element and clonal spread of progenitor resistant strains. Front Microbiol. 2015;6:595.
9.
go back to reference Torres-Gonzalez P, Cervera-Hernandez M, Niembro-Ortega M, Leal-Vega F, Cruz-Hervert L, García-García L, Galindo-Fraga A, Martinez-Gamboa A, Bobadilla-Del Valle M, Sifuentes-Osornio J, Ponce-de-Leon A. Factors associated to prevalence and incidence of Carbapenem-resistant Enterobacteriaceae fecal carriage: a cohort study in a Mexican tertiary care hospital. PLoS One. 2015;10(10):e0139883.CrossRefPubMedPubMedCentral Torres-Gonzalez P, Cervera-Hernandez M, Niembro-Ortega M, Leal-Vega F, Cruz-Hervert L, García-García L, Galindo-Fraga A, Martinez-Gamboa A, Bobadilla-Del Valle M, Sifuentes-Osornio J, Ponce-de-Leon A. Factors associated to prevalence and incidence of Carbapenem-resistant Enterobacteriaceae fecal carriage: a cohort study in a Mexican tertiary care hospital. PLoS One. 2015;10(10):e0139883.CrossRefPubMedPubMedCentral
10.
11.
go back to reference Kazmierczak KM, Biedenbach DJ, Hackel M, Rabine S, de Jonge BL, Bouchillon SK, Sahm DF, Bradford PA. Global dissemination of blaKPC into bacterial species beyond Klebsiella pneumoniae and in vitro susceptibility to ceftazidime-avibactam and Aztreonam-avibactam. Antimicrob Agents Chemother. 2016;60(8):4490–500.CrossRefPubMedPubMedCentral Kazmierczak KM, Biedenbach DJ, Hackel M, Rabine S, de Jonge BL, Bouchillon SK, Sahm DF, Bradford PA. Global dissemination of blaKPC into bacterial species beyond Klebsiella pneumoniae and in vitro susceptibility to ceftazidime-avibactam and Aztreonam-avibactam. Antimicrob Agents Chemother. 2016;60(8):4490–500.CrossRefPubMedPubMedCentral
12.
go back to reference Wei ZQ, Du XX, Yu YS, Shen P, Chen YG, Li LJ. Plasmid-mediated KPC-2 in a Klebsiella pneumoniae isolate from China. Antimicrob Agents Chemother. 2006;51(2):763–5.CrossRefPubMedPubMedCentral Wei ZQ, Du XX, Yu YS, Shen P, Chen YG, Li LJ. Plasmid-mediated KPC-2 in a Klebsiella pneumoniae isolate from China. Antimicrob Agents Chemother. 2006;51(2):763–5.CrossRefPubMedPubMedCentral
13.
go back to reference Feng J, Yin Z, Zhao Q, Zhao Y, Zhang D, Jiang X, Wu W, Chen W, Wang H, Song Y, Tong Y, Wang J, Li Y, Zhou D. Genomic characterization of novel IncFII-type multidrug resistant plasmids p0716-KPC and p12181-KPC from Klebsiella pneumoniae. Sci Rep. 2017;7(1):5830.CrossRefPubMedPubMedCentral Feng J, Yin Z, Zhao Q, Zhao Y, Zhang D, Jiang X, Wu W, Chen W, Wang H, Song Y, Tong Y, Wang J, Li Y, Zhou D. Genomic characterization of novel IncFII-type multidrug resistant plasmids p0716-KPC and p12181-KPC from Klebsiella pneumoniae. Sci Rep. 2017;7(1):5830.CrossRefPubMedPubMedCentral
14.
go back to reference Cai JC, Zhang R, Hu YY, Zhou HW, Chen GX. Emergence of Escherichia coli sequence type 131 isolates producing KPC-2 carbapenemase in China. Antimicrob Agents Chemother. 2014;58(2):1146–52.CrossRefPubMedPubMedCentral Cai JC, Zhang R, Hu YY, Zhou HW, Chen GX. Emergence of Escherichia coli sequence type 131 isolates producing KPC-2 carbapenemase in China. Antimicrob Agents Chemother. 2014;58(2):1146–52.CrossRefPubMedPubMedCentral
15.
go back to reference Tseng IL, Liu YM, Wang SJ, Yeh HY, Hsieh CL, Lu HL, Tseng YC, Mu JJ. Emergence of Carbapenemase producing Klebsiella pneumonia and spread of KPC-2 and KPC-17 in Taiwan: a Nationwide study from 2011 to 2013. PLoS One. 2015;10(9):e0138471.CrossRefPubMedPubMedCentral Tseng IL, Liu YM, Wang SJ, Yeh HY, Hsieh CL, Lu HL, Tseng YC, Mu JJ. Emergence of Carbapenemase producing Klebsiella pneumonia and spread of KPC-2 and KPC-17 in Taiwan: a Nationwide study from 2011 to 2013. PLoS One. 2015;10(9):e0138471.CrossRefPubMedPubMedCentral
16.
go back to reference Wu W, Feng Y, Carattoli A, Zong Z. Characterization of an Enterobacter cloacae strain producing both KPC and NDM Carbapenemases by whole-genome sequencing. Antimicrob Agents Chemother. 2015;59(10):6625–8.CrossRefPubMedPubMedCentral Wu W, Feng Y, Carattoli A, Zong Z. Characterization of an Enterobacter cloacae strain producing both KPC and NDM Carbapenemases by whole-genome sequencing. Antimicrob Agents Chemother. 2015;59(10):6625–8.CrossRefPubMedPubMedCentral
17.
go back to reference Baran I, Aksu N. Phenotypic and genotypic characteristics of carbapenem-resistant Enterobacteriaceae in a tertiary-level reference hospital in Turkey. Ann Clin Microbiol Antimicrob. 2016;15:20.CrossRefPubMedPubMedCentral Baran I, Aksu N. Phenotypic and genotypic characteristics of carbapenem-resistant Enterobacteriaceae in a tertiary-level reference hospital in Turkey. Ann Clin Microbiol Antimicrob. 2016;15:20.CrossRefPubMedPubMedCentral
18.
go back to reference 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;53(12):5046–54.CrossRefPubMedPubMedCentral 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;53(12):5046–54.CrossRefPubMedPubMedCentral
19.
go back to reference Poirel L, Yilmaz M, Istanbullu A, Arslan F, Mert A, Bernabeu S, Nordmann P. Spread of NDM-1-producing Enterobacteriaceae in a neonatal intensive care unit in Istanbul, Turkey. Antimicrob Agents Chemother. 2014;58(5):2929–33.CrossRefPubMedPubMedCentral Poirel L, Yilmaz M, Istanbullu A, Arslan F, Mert A, Bernabeu S, Nordmann P. Spread of NDM-1-producing Enterobacteriaceae in a neonatal intensive care unit in Istanbul, Turkey. Antimicrob Agents Chemother. 2014;58(5):2929–33.CrossRefPubMedPubMedCentral
20.
go back to reference Yousfi M, Mairi A, Bakour S, Touati A, Hassissen L, Hadjadj L, Rolain J. First report of NDM-5-producing Escherichia coli ST1284 isolated from dog in Bejaia, Algeria. New Microbes New Infect. 2015;8:17–8.CrossRefPubMedPubMedCentral Yousfi M, Mairi A, Bakour S, Touati A, Hassissen L, Hadjadj L, Rolain J. First report of NDM-5-producing Escherichia coli ST1284 isolated from dog in Bejaia, Algeria. New Microbes New Infect. 2015;8:17–8.CrossRefPubMedPubMedCentral
21.
go back to reference Van der Mee-Marquet N, Diene SM, Chopin F, Goudeau A, Francois P. Enigmatic occurrence of NDM-7 enzyme in the community. Int J Antimicrob Agents. 2016;47(6):505–7.CrossRefPubMed Van der Mee-Marquet N, Diene SM, Chopin F, Goudeau A, Francois P. Enigmatic occurrence of NDM-7 enzyme in the community. Int J Antimicrob Agents. 2016;47(6):505–7.CrossRefPubMed
22.
go back to reference Bitar I, Piazza A, Gaiarsa S, Villa L, Pedroni P, Oliva E, Nucleo E, Pagani L, Carattoli A, Migliavacca R. ST405 NDM-5 producing Escherichia coli in northern Italy: the first two clinical cases. Clin Microbiol Infect. 2017;23(7):489–90.CrossRefPubMed Bitar I, Piazza A, Gaiarsa S, Villa L, Pedroni P, Oliva E, Nucleo E, Pagani L, Carattoli A, Migliavacca R. ST405 NDM-5 producing Escherichia coli in northern Italy: the first two clinical cases. Clin Microbiol Infect. 2017;23(7):489–90.CrossRefPubMed
23.
go back to reference Spyropoulou A, Bartzavali C, Vamvakopoulou S, Marangos M, Anastassiou E, Spiliopoulou I, Christofidou M. The first NDM metallo-β-lactamase producing Klebsiella pneumoniae isolate in a University Hospital of Southwestern Greece. J Chemother. 2016;28(4):350–1.CrossRefPubMed Spyropoulou A, Bartzavali C, Vamvakopoulou S, Marangos M, Anastassiou E, Spiliopoulou I, Christofidou M. The first NDM metallo-β-lactamase producing Klebsiella pneumoniae isolate in a University Hospital of Southwestern Greece. J Chemother. 2016;28(4):350–1.CrossRefPubMed
24.
go back to reference Howard JC, Creighton J, Heffernan H, Werno A. Evidence of transmission of an NDM-5-producing Klebsiella pneumoniae in a healthcare facility in New Zealand. Antimicrob Chemother. 2017;72(3):949–51. Howard JC, Creighton J, Heffernan H, Werno A. Evidence of transmission of an NDM-5-producing Klebsiella pneumoniae in a healthcare facility in New Zealand. Antimicrob Chemother. 2017;72(3):949–51.
25.
go back to reference Torres-Gonzalez P, Bobadilla-Del Valle M, Tovar-Calderon E, Leal-Vega F, Hernandez-Cruz A, Martinez-Gamboa A, Niembro-Ortega MD, Sifuentes-Osornio J, Ponce-de-Leon A. Outbreak caused by Enterobacteriaceae harboring NDM-1 metallo-beta-lactamase carried in an IncFII plasmid in a tertiary care hospital in Mexico City. Antimicrob Agents Chemother. 2015;59(11):7080–3.CrossRefPubMedPubMedCentral Torres-Gonzalez P, Bobadilla-Del Valle M, Tovar-Calderon E, Leal-Vega F, Hernandez-Cruz A, Martinez-Gamboa A, Niembro-Ortega MD, Sifuentes-Osornio J, Ponce-de-Leon A. Outbreak caused by Enterobacteriaceae harboring NDM-1 metallo-beta-lactamase carried in an IncFII plasmid in a tertiary care hospital in Mexico City. Antimicrob Agents Chemother. 2015;59(11):7080–3.CrossRefPubMedPubMedCentral
26.
go back to reference Ho PL, Li Z, Lo WU, Cheung YY, Lin CH, Sham PC, Cheng VC, Ng TK, Que TL, Chow KH. Identification and characterization of a novel incompatibility group X3 plasmid carrying Bla NDM-1 in Enterobacteriaceae isolates with epidemiological links to multiple geographical areas in China. Emerg Microbes Infect. 2012;1(11):e39.CrossRefPubMedPubMedCentral Ho PL, Li Z, Lo WU, Cheung YY, Lin CH, Sham PC, Cheng VC, Ng TK, Que TL, Chow KH. Identification and characterization of a novel incompatibility group X3 plasmid carrying Bla NDM-1 in Enterobacteriaceae isolates with epidemiological links to multiple geographical areas in China. Emerg Microbes Infect. 2012;1(11):e39.CrossRefPubMedPubMedCentral
27.
go back to reference Chen Y, Zhou Z, Jiang Y, Yu Y. Emergence of NDM-1-producing Acinetobacter baumannii in China. J Antimicrob Chemother. 2011;66(6):1255–9.CrossRefPubMed Chen Y, Zhou Z, Jiang Y, Yu Y. Emergence of NDM-1-producing Acinetobacter baumannii in China. J Antimicrob Chemother. 2011;66(6):1255–9.CrossRefPubMed
28.
go back to reference Liu C, Qin S, Xu H, Xu L, Zhao D, Liu X, Lang S, Feng X, Liu HM. New Delhi Metallo-beta-Lactamase 1(NDM-1), the Dominant Carbapenemase Detected in Carbapenem-Resistant Enterobacter cloacae from Henan Province, China. PloS one. 2015;10(8):e0135044.CrossRefPubMedPubMedCentral Liu C, Qin S, Xu H, Xu L, Zhao D, Liu X, Lang S, Feng X, Liu HM. New Delhi Metallo-beta-Lactamase 1(NDM-1), the Dominant Carbapenemase Detected in Carbapenem-Resistant Enterobacter cloacae from Henan Province, China. PloS one. 2015;10(8):e0135044.CrossRefPubMedPubMedCentral
29.
go back to reference Yang Q, Fang L, Fu Y, Du X, Shen Y, Yu Y. Dissemination of NDM-1-producing Enterobacteriaceae mediated by the IncX3-type plasmid. PLoS One. 2015;10(6):e0129454.CrossRefPubMedPubMedCentral Yang Q, Fang L, Fu Y, Du X, Shen Y, Yu Y. Dissemination of NDM-1-producing Enterobacteriaceae mediated by the IncX3-type plasmid. PLoS One. 2015;10(6):e0129454.CrossRefPubMedPubMedCentral
30.
go back to reference Zheng R, Zhang Q, Guo Y, Feng Y, Liu L, Zhang A, Zhao Y, Yang X, Xia X. Outbreak of plasmid-mediated NDM-1-producing Klebsiella pneumoniae ST105 among neonatal patients in Yunnan. China Ann Clin Microbiol Antimicrob. 2016;15:10.CrossRefPubMed Zheng R, Zhang Q, Guo Y, Feng Y, Liu L, Zhang A, Zhao Y, Yang X, Xia X. Outbreak of plasmid-mediated NDM-1-producing Klebsiella pneumoniae ST105 among neonatal patients in Yunnan. China Ann Clin Microbiol Antimicrob. 2016;15:10.CrossRefPubMed
31.
go back to reference Zhang X, Li X, Wang M, Yue H, Li P, Liu Y, Cao W, Yao D, Liu L, Zhou X, et al. Outbreak of NDM-1-producing Klebsiella pneumoniae causing neonatal infection in a teaching hospital in mainland China. Antimicrob Agents Chemother. 2015;59(7):4349–51.CrossRefPubMedPubMedCentral Zhang X, Li X, Wang M, Yue H, Li P, Liu Y, Cao W, Yao D, Liu L, Zhou X, et al. Outbreak of NDM-1-producing Klebsiella pneumoniae causing neonatal infection in a teaching hospital in mainland China. Antimicrob Agents Chemother. 2015;59(7):4349–51.CrossRefPubMedPubMedCentral
32.
go back to reference Netikul T, Kiratisin P. Genetic characterization of Carbapenem-resistant Enterobacteriaceae and the spread of Carbapenem-resistant Klebsiella pneumonia ST340 at a University Hospital in Thailand. PLoS One. 2015;10(9):e0139116.CrossRefPubMedPubMedCentral Netikul T, Kiratisin P. Genetic characterization of Carbapenem-resistant Enterobacteriaceae and the spread of Carbapenem-resistant Klebsiella pneumonia ST340 at a University Hospital in Thailand. PLoS One. 2015;10(9):e0139116.CrossRefPubMedPubMedCentral
33.
go back to reference Shen P, Wei Z, Jiang Y, Du X, Ji S, Yu Y, Li L. Novel genetic environment of the carbapenem-hydrolyzing beta-lactamase KPC-2 among Enterobacteriaceae in China. Antimicrob Agents Chemother. 2009;53(10):4333–8.CrossRefPubMedPubMedCentral Shen P, Wei Z, Jiang Y, Du X, Ji S, Yu Y, Li L. Novel genetic environment of the carbapenem-hydrolyzing beta-lactamase KPC-2 among Enterobacteriaceae in China. Antimicrob Agents Chemother. 2009;53(10):4333–8.CrossRefPubMedPubMedCentral
34.
go back to reference Rossolini GM, D'Andrea MM, Mugnaioli C. The spread of CTX-M-type extended-spectrum beta-lactamases. Clin Microbiol Infect. 2008;14(Suppl 1):33–41.CrossRefPubMed Rossolini GM, D'Andrea MM, Mugnaioli C. The spread of CTX-M-type extended-spectrum beta-lactamases. Clin Microbiol Infect. 2008;14(Suppl 1):33–41.CrossRefPubMed
35.
go back to reference Zhao XJ, Deng LH, Shi DS, Kang HQ, Jiang F, Ma P. Mechanism of drug resistance of Klebsiella pneumoniae resistant carbapenem pneumonia. Chin J Infect Sci. 2015;25(17):3851–3. Zhao XJ, Deng LH, Shi DS, Kang HQ, Jiang F, Ma P. Mechanism of drug resistance of Klebsiella pneumoniae resistant carbapenem pneumonia. Chin J Infect Sci. 2015;25(17):3851–3.
36.
go back to reference Datta S, Roy S, Chatterjee S, Saha A, Sen B, Pal T, Som T, Basu S. A five-year experience of carbapenem resistance in Enterobacteriaceae causing neonatal septicaemia: predominance of NDM-1. PLoS One. 2014;9(11):e112101.CrossRefPubMedPubMedCentral Datta S, Roy S, Chatterjee S, Saha A, Sen B, Pal T, Som T, Basu S. A five-year experience of carbapenem resistance in Enterobacteriaceae causing neonatal septicaemia: predominance of NDM-1. PLoS One. 2014;9(11):e112101.CrossRefPubMedPubMedCentral
37.
go back to reference Del Franco M, Paone L, Novati R, Giacomazzi CG, Bagattini M, Galotto C, Montanera PG, Triassi M, Zarrilli R. Molecular epidemiology of carbapenem resistant Enterobacteriaceae in Valle d'Aosta region, Italy, shows the emergence of KPC-2 producing Klebsiella pneumoniae clonal complex 101 (ST101 and ST1789). BMC Microbiol. 2015;15(1):260.CrossRefPubMedPubMedCentral Del Franco M, Paone L, Novati R, Giacomazzi CG, Bagattini M, Galotto C, Montanera PG, Triassi M, Zarrilli R. Molecular epidemiology of carbapenem resistant Enterobacteriaceae in Valle d'Aosta region, Italy, shows the emergence of KPC-2 producing Klebsiella pneumoniae clonal complex 101 (ST101 and ST1789). BMC Microbiol. 2015;15(1):260.CrossRefPubMedPubMedCentral
38.
go back to reference Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015;28(3):565–91.CrossRefPubMedPubMedCentral Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev. 2015;28(3):565–91.CrossRefPubMedPubMedCentral
39.
go back to reference Daikos GL, Petrikkos P, Psichogiou M, Kosmidis C, Vryonis E, Skoutelis A, Georgousi K, Tzouvelekis LS, Tassios PT, Bamia C, et al. Prospective observational study of the impact of VIM-1 metallo-beta-lactamase on the outcome of patients with Klebsiella pneumoniae bloodstream infections. Antimicrob Agents Chemother. 2009;53(5):1868–73.CrossRefPubMedPubMedCentral Daikos GL, Petrikkos P, Psichogiou M, Kosmidis C, Vryonis E, Skoutelis A, Georgousi K, Tzouvelekis LS, Tassios PT, Bamia C, et al. Prospective observational study of the impact of VIM-1 metallo-beta-lactamase on the outcome of patients with Klebsiella pneumoniae bloodstream infections. Antimicrob Agents Chemother. 2009;53(5):1868–73.CrossRefPubMedPubMedCentral
41.
go back to reference Girlich D, Poirel L, Nordmann P. Value of the modified Hodge test for detection of emerging carbapenemases in Enterobacteriaceae. J Clin Microbiol. 2012;50(2):477–9.CrossRefPubMedPubMedCentral Girlich D, Poirel L, Nordmann P. Value of the modified Hodge test for detection of emerging carbapenemases in Enterobacteriaceae. J Clin Microbiol. 2012;50(2):477–9.CrossRefPubMedPubMedCentral
42.
go back to reference Bengoechea JA, Bowers JR, Kitchel B, Driebe EM, MacCannell DR, Roe C, Lemmer D, de Man T, Rasheed JK, Engelthaler DM, et al. Genomic analysis of the emergence and rapid global dissemination of the clonal group 258 Klebsiella pneumoniae pandemic. PLoS One. 2015;10(7):e0133727.CrossRef Bengoechea JA, Bowers JR, Kitchel B, Driebe EM, MacCannell DR, Roe C, Lemmer D, de Man T, Rasheed JK, Engelthaler DM, et al. Genomic analysis of the emergence and rapid global dissemination of the clonal group 258 Klebsiella pneumoniae pandemic. PLoS One. 2015;10(7):e0133727.CrossRef
43.
go back to reference Pasteran FG, Otaegui L, Guerriero L, Radice G, Maggiora R, Rapoport M, Faccone D, Di Martino A, Galas M. Klebsiella pneumoniae Carbapenemase–2, Buenos Aires. Argentina Emerg Infect Dis. 2008;14(7):1178–18.CrossRefPubMed Pasteran FG, Otaegui L, Guerriero L, Radice G, Maggiora R, Rapoport M, Faccone D, Di Martino A, Galas M. Klebsiella pneumoniae Carbapenemase–2, Buenos Aires. Argentina Emerg Infect Dis. 2008;14(7):1178–18.CrossRefPubMed
44.
go back to reference Li J, Zou MX, Wang HC, Dou QY, Hu YM, Yan Q, Liu WE. An outbreak of infections caused by a Klebsiella pneumoniae ST11 clone coproducing Klebsiella pneumoniae Carbapenemase-2 and RmtB in a Chinese teaching hospital. Chin Med J. 2016;129(17):2033–9.CrossRefPubMedPubMedCentral Li J, Zou MX, Wang HC, Dou QY, Hu YM, Yan Q, Liu WE. An outbreak of infections caused by a Klebsiella pneumoniae ST11 clone coproducing Klebsiella pneumoniae Carbapenemase-2 and RmtB in a Chinese teaching hospital. Chin Med J. 2016;129(17):2033–9.CrossRefPubMedPubMedCentral
45.
go back to reference Yan JJ, Zheng PX, Wang MC, Tsai SH, Wang LR, Wu JJ. Allocation of Klebsiella pneumoniae bloodstream isolates into four distinct groups by ompK36 typing in a Taiwanese University hospital. J Clin Microbiol. 2015;53(10):3256–63.CrossRefPubMedPubMedCentral Yan JJ, Zheng PX, Wang MC, Tsai SH, Wang LR, Wu JJ. Allocation of Klebsiella pneumoniae bloodstream isolates into four distinct groups by ompK36 typing in a Taiwanese University hospital. J Clin Microbiol. 2015;53(10):3256–63.CrossRefPubMedPubMedCentral
46.
go back to reference Davis GS, Waits K, Nordstrom L, Weaver B, Aziz M, Gauld L, Grande H, Bigler R, Horwinski J, Porter S, et al. Intermingled Klebsiella pneumoniae populations between retail meats and human urinary tract infections. Clin Infect Dis. 2015;61(6):892–9.CrossRefPubMedPubMedCentral Davis GS, Waits K, Nordstrom L, Weaver B, Aziz M, Gauld L, Grande H, Bigler R, Horwinski J, Porter S, et al. Intermingled Klebsiella pneumoniae populations between retail meats and human urinary tract infections. Clin Infect Dis. 2015;61(6):892–9.CrossRefPubMedPubMedCentral
47.
go back to reference Nakano R, Nakano A, Hikosaka K, Kawakami S, Matsunaga N, Asahara M, Ishigaki S, Furukawa T, Suzuki M, Shibayama K, et al. First report of metallo-beta-lactamase NDM-5-producing Escherichia coli in Japan. Antimicrob Agents Chemother. 2014;58(12):7611–2.CrossRefPubMedPubMedCentral Nakano R, Nakano A, Hikosaka K, Kawakami S, Matsunaga N, Asahara M, Ishigaki S, Furukawa T, Suzuki M, Shibayama K, et al. First report of metallo-beta-lactamase NDM-5-producing Escherichia coli in Japan. Antimicrob Agents Chemother. 2014;58(12):7611–2.CrossRefPubMedPubMedCentral
48.
go back to reference Zhu J, Sun L, Ding B, Yang Y, Xu X, Liu W, Zhu D, Yang F, Zhang H, Hu F. Outbreak of NDM-1-producing Klebsiella pneumoniae ST76 and ST37 isolates in neonates. Eur J Clin Microbiol Infect Dis. 2016;35(4):611–8.CrossRefPubMed Zhu J, Sun L, Ding B, Yang Y, Xu X, Liu W, Zhu D, Yang F, Zhang H, Hu F. Outbreak of NDM-1-producing Klebsiella pneumoniae ST76 and ST37 isolates in neonates. Eur J Clin Microbiol Infect Dis. 2016;35(4):611–8.CrossRefPubMed
49.
go back to reference Sahin K, Tekin A, Ozdas S, Akin D, Yapislar H, Dilek AR, Sonmez E. Evaluation of carbapenem resistance using phenotypic and genotypic techniques in Enterobacteriaceae isolates. Ann Clin Microbiol Antimicrob. 2015;14:44.CrossRefPubMedPubMedCentral Sahin K, Tekin A, Ozdas S, Akin D, Yapislar H, Dilek AR, Sonmez E. Evaluation of carbapenem resistance using phenotypic and genotypic techniques in Enterobacteriaceae isolates. Ann Clin Microbiol Antimicrob. 2015;14:44.CrossRefPubMedPubMedCentral
50.
Metadata
Title
Molecular characterization and epidemiology of carbapenem non-susceptible Enterobacteriaceae isolated from the Eastern region of Heilongjiang Province, China
Authors
Xue Gong
Jisheng Zhang
Shanshan Su
Yanjun Fu
Mingjia Bao
Yong Wang
Xiaoli Zhang
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-018-3294-3

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