Secondary Logo

Co-existence of blaOXA-23 and blaVIM in carbapenem-resistant Acinetobacter baumannii isolates belonging to global complex 2 in a Chinese teaching hospital

Huang, Zi-Yan; Li, Jun; Shui, Jian; Wang, Hai-Chen; Hu, Yong-Mei; Zou, Ming-Xiang

Section Editor(s): Guo, Li-Shao

doi: 10.1097/CM9.0000000000000193
Original Articles

Background Carbapenem-resistant Acinetobacter baumannii (CRAB) have been a challenging concern of health-care associated infections. The aim of the current study was to investigate the molecular epidemiology and clonal dissemination of CRAB isolates in a Chinese teaching hospital.

Methods Non-duplicate clinical A. baumannii isolates were collected from inpatients, and we measured the minimal inhibitory concentrations to determine antimicrobial susceptibility. Polymerase chain reaction (PCR) and sequencing were performed to detect carbapenem-resistance genes and occurrence of transposons among CRAB isolates. Moreover, the genetic diversity among isolates and clonal dissemination were determined by repetitive element PCR-mediated DNA fingerprinting (rep-PCR) and multilocus sequence typing (MLST).

Results A total of 67 CRAB isolates displayed resistance to most of the antibiotics tested in this study, except tigecycline. We detected blaOXA-23, blaOXA-51, blaOXA-58, and blaVIM genes in 94.0%, 100.0%, 1.5%, and 80.6% of the CRAB isolates, respectively. Nevertheless, 74.6% of the CRAB isolates co-harbored the blaOXA-23 and blaVIM. Only one type of transposons was detected: Tn2008 (79.1%, 53/67). Although 12 distinctive types (A-L) were determined (primarily A type) ST195 was the most prevalent sequence type (ST). ST368, ST210, ST90, ST829, and ST136 were also detected, and all belonged to clonal complex 208 (CC208) and global complex 2 (GC2).

Conclusion The blaOXA-23 and blaVIM genes contributed to the resistance among CRAB isolates collected in our study. Notably, most of the CRAB strains co-harbored blaOXA-23 and blaVIM genes, as well as Tn2008, which could contribute to clonal dissemination. The prevalence of such organisms may underlie hospital acquired infections.

Department of Clinical Laboratory, Xiangya Hospital, Central South University, Changsha, Hunan 410008, China.

Correspondence to: Ming-Xiang Zou, Department of Clinical Laboratory, Xiangya Hospital, Central South University, No. 87 Xiangya Road, Kaifu District, Changsha, Hunan 410008, China E-Mail:

How to cite this article: Huang ZY, Li J, Shui J, Wang HC, Hu YM, Zou MX. Co-existence of blaOXA-23 and blaVIM in carbapenem-resistant Acinetobacter baumannii isolates belonging to global complex 2 in a Chinese teaching hospital. Chin Med J 2019;00:00–00. doi: 10.1097/CM9.0000000000000193

Received 6 December, 2018

This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

Back to Top | Article Outline


Acinetobacter baumannii (A. baumannii) is prevalent in the hospital environment and is the source of contamination in various clinical settings. A. baumannii has emerged as one of the most significant opportunistic pathogens of healthcare-associated infections (HAIs).[1,2] Other than bacteremia and secondary meningitis, A. baumannii is responsible for numerous infections of the urinary and respiratory tract, skin, soft tissues, solid organ transplant, and burn wounds.[3–7] During the last decade, rapid emergence of carbapenem-resistant A. baumannii (CRAB) has been reported as a global issue. A rapid increase of HAIs caused by CRAB, from 4.0% in 2003 to 62.0% in 2008 (P < 0.0001),[8] was reported in Taiwan, China. A US national surveillance study conducted in 2010 reported a prevalence of 44.7% and 49.0% among A. baumannii isolates resistant to imipenem and meropenem, respectively.[9] A dramatic increase in the mortality rate, from 16.0% to 76.0%, has been reported in cases of infections caused by CRAB compared to an increase from 5.0% to 53.0% in cases of infections caused by carbapenem susceptible pathogens.[10] Furthermore, high mortality rates recently reported in Taiwan, China (70%), and Korea (79.8%) have been attributed to CRAB infections in the blood, whereas lower mortality (24.5%) has been observed in similar infections where imipenem susceptible A. baumannii were involved.[11,12]

As previously described, carbapenemases are responsible for the acquisition of carbapenem-resistance in A. baumannii.[13,14] According to the Ambler classification, carbapenemases mainly belong to class A, B, and D β-lactamases, and class D β-lactamases are commonly disseminated in A. baumannii, which are comprised of OXA-23-like, OXA-40-like, OXA-51-like, OXA-58-like, and OXA-23, which is the primary cause of carbapenem resistance in A. baumannii.[14,15] Another important type of carbapenemases, plasmid-mediated metallo-β-lactamases (MBLs), which hydrolyze carbapenems and all β-lactams except monobactams, were also increasingly reported in Acinetobacter spp. Presently, few reports have been published on the prevalence of MBLs in A. baumannii worldwide.[16–18]

In the current study, we investigated if two genes, blaOXA-23 and blaVIM, were co-harbored among CRAB isolates collected from patients admitted to different clinical departments at a Chinese teaching hospital. Furthermore, the molecular epidemiology and clonal dissemination of these isolates were determined.

Back to Top | Article Outline


Ethics approval

This study was approved by the Ethics Committee of Xiangya Hospital, Changsha, China. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards. Written informed consent was obtained from all individual participants included in the study.

Back to Top | Article Outline

Bacterial isolates

Non-repetitive A. baumannii isolates were collected consecutively from inpatient units between January 1st and December 31st in 2016 at Xiangya Hospital Central South University, a teaching hospital with a 3500-bed capacity located in Changsha, Hunan Province, China. Isolates were collected from different types of specimens from one patient or from the same specimen, but the interval collection time was at least 1 week. All isolates were identified by MALDI-TOF-MS (Bruker Daltonics GmbH, Bremen, Germany) and confirmed by polymerase chain reaction (PCR) by detecting 16S rRNA.[19]

Back to Top | Article Outline

Antimicrobial susceptibility testing

Minimal inhibitory concentrations (MICs) were measured using 10 representative antimicrobial agents, including imipenem, amikacin, cotrimoxazole, piperacillin/tazobactam, ceftazidime, gentamicin, cefepime, ciprofloxacin, tigecycline, and minocycline. The MICs were determined using VITEK 2 Compact (BioMérieux, Missouri, France), except for tigecycline, which was measured using E test (BioMérieux). Pseudomonas aeruginosa ATCC 27853 and Escherichia coli (E. coli) ATCC 25922 were used as the control organisms. Results were interpreted according to the Clinical and Laboratory Standards Institute (CLSI) guidelines.[20] For tigecycline, interpretive criteria was based on the United States Food and Drug Administration, where isolates having MIC ≥8, 4, and ≤2 μg/mL were considered resistant, intermediate, and sensitive, respectively.[21]

Back to Top | Article Outline

Phenotypic tests for MBLs production

MBLs production was performed using the double-disc synergy test (DDST) and the imipenem-EDTA combined disc test (CDT). In the DDST method, isolates (turbidity was adjusted to 0.5 McFarland) were cultured on Mueller-Hinton agar plates as recommended by the CLSI. After drying, two discs (one disc contained imipenem [10 μg], and the other contained only 10 μL of 0.5 mol/L EDTA [Sigma Chemicals, USA]) were placed on the culture plate at 20 mm from the center of the discs. After overnight incubation, the presence of even a small synergistic inhibition zone was interpreted as positive.[22] The CDT was carried out as follows: two discs (one disc contained imipenem [10 μg] and 5 μL of 0.5 mol/L EDTA [Sigma Chemicals], and the other disc contained only imipenem [10 μg]) were placed about 20 mm apart on a Mueller-Hinton agar plate inoculated with each test strain. The result was considered positive, meaning there was MLB hydrolysis activity, when the zone diameter around the imipenem-EDTA disc was >7.0 mm of the imipenem alone disc.[23]

Back to Top | Article Outline

PCR and sequencing of carbapenemase genes

PCR was conducted to detect the presence of carbapenemase genes in 67 CRAB isolates. blaOXA–23-like, blaOXA–24-like, blaOXA–51-like, blaOXA–58-like, blaIMP, blaVIM, blaSPM, and blaNDM were detected using previously described primers.[24] All PCR products were sequenced by Sangon Biotech (Sangon Biotech, Shanghai, China) and analyzed for similarity searches with the BLAST website (

Back to Top | Article Outline

Repetitive element PCR-mediated DNA fingerprinting (rep-PCR)

Extraction of bacterial genomic DNA and rep-PCR was performed with the GeneAmp PCR System 2720 (Applied Biosystems ABI, USA) using previously described methods. The primers were (REP1: 5′-IIIGCGCCGICATCAGGC-3′, REP2: 5′-ACGTCTTATCAGGCCTAC-3′; I represents hypoxanthine).[25,26] PCR-banding patterns were analyzed and interpreted using NTsys-2.10 software (Exeter Software, Stauket, NY, USA) for rep-PCR types.[26]

Back to Top | Article Outline

Multilocus sequence typing (MLST)

MLST was performed for molecular typing of 67 CRAB isolates by sequencing seven housekeeping genes of A. baumannii (cpn60, fusA, gltA, pyrG, recA, rplB, and rpoB) as previously described.[27] Primer sequences are available at The sequencing results were compared to the sequence types (STs) available on online databases at For investigation of genetic relationships and clonal complexes (CCs), all sequence data of the isolates included in this study were analyzed with eBURST.

Back to Top | Article Outline

Genetic environment of the blaOXA-23 gene

Genetic characterization of blaOXA-23-carrying transposons, Tn2006, Tn2007, Tn2008, and Tn2009, was conducted using PCR and sequencing with previously described primers.[28] The presence of insertion sequence ISAba1 upstream of transposons was also confirmed by PCR using previously described primers (F: 5′-CATTGGCATTAAACTGAGGAGAAA-3′, R: 5′-TTGGAAATGGGGAAAACGAA-3′).[29]

Back to Top | Article Outline


Samples and bacterial isolates

A total of 67 CRAB isolates were collected from 67 inpatients, including 47 male and 20 female patients. Approximately 70.1% (47/67) of the CRAB isolates were identified in patients from the intensive care unit (ICU), and the remaining isolates were acquired from patients in the emergency (9.0%), burn (6.0%), pancreatic surgery (3.0%), nose and skull base surgery (3.0%), infectious diseases (3.0%), rehabilitation (3.0%), brain trauma specialist (1.5%), and cerebrovascular surgery (1.5%) departments. The proportions of specimens included in this study were 35.8% each for blood and cerebrospinal fluid, followed by 11.9%, 7.5%, 7.5%, and 1.5% for pleural effusion, tissue block, ascitic fluid, and bile, respectively, as shown in Figure 1.

Figure 1

Figure 1

Back to Top | Article Outline

Antimicrobial susceptibility testing and detection of carbapenemase genes

The MICs of 10 antimicrobial agents were determined against all clinical A. baumannii isolates. The resistant rates of imipenem, trimethoprim/sulfamethoxazole, piperacillin/tazobactam, ceftazidime, gentamicin, amikacin, cefepime, ciprofloxacin, and minocycline were 100.0%, 53.7%, 98.5%, 95.5%, 86.6%, 77.6%, 98.5%, 83.6%, and 67.1%, respectively. Although only two isolates showed resistance to tigecycline, 40.3% of CRAB isolates exhibited an intermediate phenotype to tigecycline. Details of isolate susceptibility are shown in Table 1.

Table 1

Table 1

The DDST and imipenem-EDTA CDT were used to determine the prevalence of MBLs among CRAB; 77.6% of the isolates were positive for DDST, while 76.1% isolates were positive for CDT as shown in Figure 1.

blaOXA-23, blaOXA-51, and blaVIM genes were detected in 94.0%, 100.0%, and 80.6% of the 67 CRAB isolates, respectively, whereas only one isolate carried the blaOXA-58 gene. None of these isolates harbored blaOXA-24, blaIMP, blaSPM, and blaNDM. Notably, 74.6% of the CRAB isolates carried both the blaOXA-23 and blaVIM genes [Figure 1]. Moreover, isolates harboring blaVIM genes were positive in the DDST and CDT analysis, except for two isolates (CS24 and CS53).

Back to Top | Article Outline

Homology analysis

Based on rep-PCR results, 12 (A-L) genetically different profiles were observed among 67 CRAB isolates. The 56.6% of the isolates were linked to the type A profile. However, type A and I were further divided into three subtypes. Similarly, type H, J, and K were distributed into two subtypes, whereas type B into G and L was not divided into subtypes. A large number of isolates from each profile was derived from the ICU samples [Figure 1].

Among the 67 CRAB isolates, six STs – ST195 (41.8%), ST368 (13.4%), ST210 (3.0%), ST90 (3.0%), ST829 (11.9%), and ST136 (3.0%) – were detected by MLST. The eBURST analysis indicated that all STs belonged to the CC208 clonal complex and originated from the CC92 clonal complex, corresponding to global clone 2 (GC2) [Figure 2].

Figure 2

Figure 2

Back to Top | Article Outline

Genetic environment of the blaOXA-23 gene

Among the four common transposons tested in this study, only Tn2008 was identified in 53 isolates by PCR analysis. Nevertheless, insertion sequence ISAba1 located upstream of the transposons was characterized among all the CRAB isolates.

Back to Top | Article Outline


A. baumannii is a significant opportunistic pathogen associated with HAIs. A. baumannii has the ability to adapt to its environment and acquire drug resistance genes from its surroundings. As such, A. baumannii can lead to multiple drug-resistant (MDR) and even extensively drug-resistant (XDR) isolates in the hospital setting.[30] Carbapenemase production is considered the primary underlying cause of the CRAB, oxacillinase (OXA), especially OXA-23.[14] However, MBLs are another common carbapenemase in the Acinetobacter calcoaceticus-A. baumannii complex (ACB), but few reports of MBL prevalence in A. baumannii have been found. In New Delhi in 2009, Metallo-β-lactamases (NDM, common MBL) was first discovered in Klebsiella pneumoniae. Since then, it has disseminated to other species including A. baumannii, E. coli, and Enterobacter cloacae.[31] However, another MBL gene, blaVIM, has rarely been identified in A. baumannii.[32,33] In this study, we identified MDR A. baumannii isolated in patients from different clinical departments of a teaching hospital. Moreover, we investigated the molecular characteristics and clonal dissemination of these isolates.

In the current study, three types of OXA genes were detected, including OXA-23 (94.0%), OXA-51 (100.0%), and OXA-58 (1.5%), in the CRAB isolates. The occurrence of OXA-23 was considered the main reason of carbapenem resistance in A. baumannii.[14] CRAB isolates carrying-blaOXA-23 genes are disseminated worldwide due to the transposons. Five transposons have been identified, Tn2006, Tn2007, Tn2008, Tn2008B, and Tn2009, among bacterial isolates; however, Tn2006 and Tn2008 were globally disseminated,[34] and Tn2006 was the most prevalent transposon in China.[35] In contrast, we identified Tn2008, rather than Tn2006, in 79.1% of CRAB isolates, in accordance with Chen et al,[28] indicating that Tn2008 could be involved in the transmission of the blaOXA-23 gene among CRAB isolates, and also closely related to the molecular epidemiological characteristics of the strains in this area of China. Tn2008B is the most recently identified structure containing blaOXA-23. To date, Tn2008B was only reported in China;[36] however, we did not detect Tn2008B in our study. In addition, we found that ISAba1 was located upstream of the blaOXA-23 gene, which could facilitate the mobilization of blaOXA-23 and provide promoters for its expression.[37] The blaOXA-51 gene is unique to A. baumannii and may be used as a marker to identify this species.[38] Moreover, some previous studies reported that OXA-51 carbapenemases had minimal ability to hydrolyze carbapenems when ISAba1 was upstream of the blaOXA-51 gene.[39] In contrast, we showed in this study that 88.9% of the CRAB isolates carried ISAba1 upstream of the blaOXA-51 gene. Hence, there may be contribution of OXA-51 in CRAB. Isolates carrying blaOXA-24/58-like genes are typically resistant to carbapenems. Fortunately, they have not been commonly identified in China. In the current study, only one isolate carried OXA-58. Our results also demonstrated that blaOXA-24, blaNDM, blaSPM, and blaIMP were not expressed in our isolates. However, due to their plasmid location, the distribution of these genes in A. baumannii should be monitored early.

Notably, MBLs, which are rarely reported in A. baumannii,[16,17] widely existed in the CRAB isolates included in this study, and 80.6% of these CRAB isolates harbored blaVIM genes and produced MBLs confirmed by DDST and CDT, which have been considered the standardized methods for detecting MBL production.[40] Notably, 74.6% of the CRAB isolates co-harbored blaOXA-23 and blaVIM. However, the globally disseminated NDMs, including K. pneumoniae, A. baumannii, E. coli and E. cloacae,[31] were not detected in any of the isolates included in this study.

We analyzed 67 CRAB isolates using rep-PCR, which has been widely used in molecular typing of A. baumannii.[41] Additionally, 12 distinctive types of profiles obtained by rep-PCR indicated that genetically diversified CRAB isolates are prevalent in our teaching hospital. Three European clones (EC I, II, and III) of A. baumannii have been reported;[42] EC I (GC1) and EC II (GC2) are globally propagated.[43] Of particular interest, six STs (ST195, ST368, ST210, ST90, ST829, and ST136) were found by MLST, all of which belong to CC208 and are generally linked to GC2. Although ST195 (41.8%) was the predominant ST in the current study, ST92 is among the most prevalent CRAB isolates in China.[44] We did not detect ST92 in the current study; we detected ST208 using the Institute Pasteur scheme (compared to ST92; Oxford scheme). Actually, ST92 may not exist.[45]

There are also some limitations in this study. We did not analyze the plasmid where the drug resistance gene is located. In addition, we only studied the CRAB isolated from our hospital and did not include other hospitals in our region.

In summary, blaOXA-23, blaOXA-51, and blaVIM may be responsible for CRAB. ST195 was the most prevalent clonal complex found in our teaching hospital and could disseminate in this area of China. Remarkably, the clonal dissemination of GC2 isolates co-harboring blaOXA-23 and blaVIM genes among A. baumannii strains may be responsible for the rapid acquisition of carbapenem resistance. Furthermore, the detection of Tn2008 suggests that dissemination of blaOXA-23 might be facilitated by these transposons. Therefore, some infection control measures should be reinforced to reduce the further spread of A. baumannii, including rapid identification of blaOXA-23, hand hygiene, and environmental disinfection.

Back to Top | Article Outline


This study was supported by grants from the Hunan Provincial Natural Science Foundation (No. 2017JJ3478) and the National Natural Science Foundation of China (No. 81702068).

Back to Top | Article Outline

Conflicts of interest


Back to Top | Article Outline


1. Balkhy HH, Bawazeer MS, Kattan RF, Tamim HM, Al Johani SM, Aldughashem FA, et al. Epidemiology of Acinetobacter spp.-associated healthcare infections and colonization among children at a tertiary-care hospital in Saudi Arabia: a 6-year retrospective cohort study. Eur J Clin Microbiol Infect Dis 2012; 31:2645–2651. doi: 10.1007/s10096-012-1608-8.
2. El-Shazly S, Dashti A, Vali L, Bolaris M, Ibrahim AS. Molecular epidemiology and characterization of multiple drug-resistant (MDR) clinical isolates of Acinetobacter baumannii. Int J Infect Dis 2015; 41:42–49. doi: 10.1016/j.ijid.2015.10.016.
3. Roca I, Espinal P, Vila-Farres X, Vila J. The Acinetobacter baumannii oxymoron: commensal hospital dweller turned pan-drug-resistant menace. Front Microbiol 2012; 3:148doi: 10.3389/fmicb.2012.00148.
4. Kempf M, Rolain JM, Azza S, Diene S, Joly-Guillou ML, Dubourg G, et al. Investigation of Acinetobacter baumannii resistance to carbapenems in Marseille hospitals, south of France: a transition from an epidemic to an endemic situation. APMIS 2013; 121:64–71. doi: 10.1111/j.1600-0463.2012.02935.x.
5. Yuan X, Liu T, Wu D, Wan Q. Epidemiology, susceptibility, and risk factors for acquisition of MDR/XDR Gram-negative bacteria among kidney transplant recipients with urinary tract infections. Infect Drug Resist 2018; 11:707–715. doi: 10.2147/IDR.S163979.
6. Gao F, Ye Q, Wan Q, Liu S, Zhou J. Distribution and resistance of pathogens in liver transplant recipients with Acinetobacter baumannii infection. Ther Clin Risk Manag 2015; 11:501–505. doi: 10.2147/TCRM.S82251.
7. Nie XM, Huang PH, Ye QF, Wan QQ. The distribution, drug resistance, and clinical characteristics of Acinetobacter baumannii infections in solid organ transplant recipients. Transplant Proc 2015; 47:2860–2864. doi: 10.1016/j.transproceed.2015.09.037.
8. Su CH, Wang JT, Hsiung CA, Chien LJ, Chi CL, Yu HT, et al. Increase of carbapenem-resistant Acinetobacter baumannii infection in acute care hospitals in Taiwan: association with hospital antimicrobial usage. PLoS One 2012; 7:e37788doi: 10.1371/journal.pone.0037788.
9. Queenan AM, Pillar CM, Deane J, Sahm DF, Lynch AS, Flamm RK, et al. Multidrug resistance among Acinetobacter spp. in the USA and activity profile of key agents: results from CAPITAL Surveillance 2010. Diagn Microbiol Infect Dis 2012; 73:267–270. doi: 10.1016/j.diagmicrobio.2012.04.002.
10. Lemos EV, de la Hoz FP, Einarson TR, McGhan WF, Quevedo E, Castaneda C, et al. Carbapenem resistance and mortality in patients with Acinetobacter baumannii infection: systematic review and meta-analysis. Clin Microbiol Infect 2014; 20:416–423. doi: 10.1111/1469-0691.12363.
11. Lee HY, Chen CL, Wu SR, Huang CW, Chiu CH. Risk factors and outcome analysis of Acinetobacter baumannii complex bacteremia in critical patients. Crit Care Med 2014; 42:1081–1088. doi: 10.1097/CCM.0000000000000125.
12. Kim SY, Jung JY, Kang YA, Lim JE, Kim EY, Lee SK, et al. Risk factors for occurrence and 30-day mortality for carbapenem-resistant Acinetobacter baumannii bacteremia in an intensive care unit. J Korean Med Sci 2012; 27:939–947. doi: 10.3346/jkms.2012.27.8.939.
13. Vijayakumar S, Gopi R, Gunasekaran P, Bharathy M, Walia K, Anandan S, et al. Molecular characterization of invasive carbapenem-resistant Acinetobacter baumannii from a tertiary care hospital in South India. Infect Dis Ther 2016; 5:379–387. doi: 10.1007/s40121-016-0125-y.
14. Al Atrouni A, Hamze M, Jisr T, Lemarie C, Eveillard M, Joly-Guillou ML, et al. Wide spread of OXA-23-producing carbapenem-resistant Acinetobacter baumannii belonging to clonal complex II in different hospitals in Lebanon. Int J Infect Dis 2016; 52:29–36. doi: 10.1016/j.ijid.2016.09.017.
15. Chen Z, Liu W, Zhang Y, Li Y, Jian Z, Deng H, et al. Molecular epidemiology of carbapenem-resistant Acinetobacter spp. from XiangYa Hospital, in Hunan Province, China. J Basic Microbiol 2013; 53:121–127. doi: 10.1002/jobm.201100420.
16. Huang YM, Zhong LL, Zhang XF, Hu HT, Li YQ, Yang XR, et al. NDM-1-Producing Citrobacter freundii, Escherichia coli, and Acinetobacter baumannii identified from a single patient in China. Antimicrob Agents Chemother 2015; 59:5073–5077. doi: 10.1128/AAC.04682-14.
17. Cicek AC, Saral A, Iraz M, Ceylan A, Duzgun AO, Peleg AY, et al. OXA- and GES-type beta-lactamases predominate in extensively drug-resistant Acinetobacter baumannii isolates from a Turkish University Hospital. Clin Microbiol Infect 2014; 20:410–415. doi: 10.1111/1469-0691.12338.
18. Chen F, Wang L, Wang M, Xie Y, Xia X, Li X, et al. Genetic characterization and in vitro activity of antimicrobial combinations of multidrug-resistant Acinetobacter baumannii from a general hospital in China. Oncol Lett 2018; 15:2305–2315. doi: 10.3892/ol.2017.7600.
19. Vaneechoutte M, Dijkshoorn L, Tjernberg I, Elaichouni A, de Vos P, Claeys G, et al. Identification of Acinetobacter genomic species by amplified ribosomal DNA restriction analysis. J Clin Microbiol 1995; 33:11–15.
20. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, document M100-26. Wayne: Clinical and Laboratory Standards Institute; 2016.
21. Jones RN, Ferraro MJ, Reller LB, Schreckenberger PC, Swenson JM, Sader HS. Multicenter studies of tigecycline disk diffusion susceptibility results for Acinetobacter spp. J Clin Microbiol 2007; 45:227–230. doi: 10.1128/JCM.01588-06.
22. Rizvi M, Fatima N, Rashid M, Shukla I, Malik A, Usman A, et al. Extended spectrum AmpC and metallo-beta-lactamases in Serratia and Citrobacter spp. in a disc approximation assay. J Infect Dev Ctries 2009; 3:285–294.
23. Kotwal A, Biswas D, Kakati B, Singh M. ESBL and MBL in Cefepime Resistant Pseudomonas aeruginosa: an update from a rural area in Northern India. J Clin Diagn Res 2016; 10:DC09–DC11. doi: 10.7860/JCDR/2016/18016.7612.
24. Joshi PR, Acharya M, Kakshapati T, Leungtongkam U, Thummeepak R, Sitthisak S. Co-existence of blaOXA-23 and blaNDM-1 genes of Acinetobacter baumannii isolated from Nepal: antimicrobial resistance and clinical significance. Antimicrob Resist Infect Control 2017; 6:21doi: 10.1186/s13756-017-0180-5.
25. Bou G, Cervero G, Dominguez MA, Quereda C, Martinez-Beltran J. Characterization of a nosocomial outbreak caused by a multiresistant Acinetobacter baumannii strain with a carbapenem-hydrolyzing enzyme: high-level carbapenem resistance in A. baumannii is not due solely to the presence of beta-lactamases. J Clin Microbiol 2000; 38:3299–3305.
26. Grundmann HJ, Towner KJ, Dijkshoorn L, Gerner-Smidt P, Maher M, Seifert H, et al. Multicenter study using standardized protocols and reagents for evaluation of reproducibility of PCR-based fingerprinting of Acinetobacter spp. J Clin Microbiol 1997; 35:3071–3077.
27. Diancourt L, Passet V, Nemec A, Dijkshoorn L, Brisse S. The population structure of Acinetobacter baumannii: expanding multiresistant clones from an ancestral susceptible genetic pool. PLoS One 2010; 5:e10034doi: 10.1371/journal.pone.0010034.
28. Chen Y, Gao J, Zhang H, Ying C. Spread of the blaOXA-23-containing Tn2008 in carbapenem-resistant Acinetobacter baumannii isolates grouped in CC92 from China. Front Microbiol 2017; 8:163doi: 10.3389/fmicb.2017.00163.
29. Ruiz M, Marti S, Fernandez-Cuenca F, Pascual A, Vila J. Prevalence of IS(Aba1) in epidemiologically unrelated Acinetobacter baumannii clinical isolates. FEMS Microbiol Lett 2007; 274:63–66. doi: 10.1111/j.1574-6968.2007.00828.x.
30. Li YJ, Pan CZ, Fang CQ, Zhao ZX, Chen HL, Guo PH, et al. Pneumonia caused by extensive drug-resistant Acinetobacter baumannii among hospitalized patients: genetic relationships, risk factors and mortality. BMC Infect Dis 2017; 17:371doi: 10.1186/s12879-017-2471-0.
31. Hammerum AM, Littauer P, Hansen F. Detection of Klebsiella pneumoniae co-producing NDM-7 and OXA-181, Escherichia coli producing NDM-5 and Acinetobacter baumannii producing OXA-23 in a single patient. Int J Antimicrob Agents 2015; 46:597–598. doi: 10.1016/j.ijantimicag.2015.07.008.
32. Ikonomidis A, Ntokou E, Maniatis AN, Tsakris A, Pournaras S. Hidden VIM-1 metallo-beta-lactamase phenotypes among Acinetobacter baumannii clinical isolates. J Clin Microbiol 2008; 46:346–349. doi: 10.1128/JCM.01670-07.
33. Purohit M, Mendiratta DK, Deotale VS, Madhan M, Manoharan A, Narang P. Detection of metallo-beta-lactamases producing Acinetobacter baumannii using microbiological assay, disc synergy test and PCR. Indian J Med Microbiol 2012; 30:456–461. doi: 10.4103/0255-0857.103770.
34. Lee MH, Chen TL, Lee YT, Huang L, Kuo SC, Yu KW, et al. Dissemination of multidrug-resistant Acinetobacter baumannii carrying blaOXA-23 from hospitals in central Taiwan. J Microbiol Immunol Infect 2013; 46:419–424. doi: 10.1016/j.jmii.2012.08.006.
35. Lee HY, Chang RC, Su LH, Liu SY, Wu SR, Chuang CH, et al. Wide spread of Tn2006 in an AbaR4-type resistance island among carbapenem-resistant Acinetobacter baumannii clinical isolates in Taiwan. Int J Antimicrob Agents 2012; 40:163–167. doi: 10.1016/j.ijantimicag.2012.04.018.
36. Nigro SJ, Hall RM. Structure and context of Acinetobacter transposons carrying the oxa23 carbapenemase gene. J Antimicrob Chemother 2016; 71:1135–1147. doi: 10.1093/jac/dkv440.
37. Lopes BS, Amyes SG. Role of ISAba1 and ISAba125 in governing the expression of blaADC in clinically relevant Acinetobacter baumannii strains resistant to cephalosporins. J Med Microbiol 2012; 61:1103–1108. doi: 10.1099/jmm.0.044156-0.
38. Heritier C, Poirel L, Fournier PE, Claverie JM, Raoult D, Nordmann P. Characterization of the naturally occurring oxacillinase of Acinetobacter baumannii. Antimicrob Agents Chemother 2005; 49:4174–4179. doi: 10.1128/AAC.49.10.4174-4179.2005.
39. Nowak P, Paluchowska P, Budak A. Distribution of blaOXA genes among carbapenem-resistant Acinetobacter baumannii nosocomial strains in Poland. New Microbiol 2012; 35:317–325.
40. Behera B, Mathur P, Das A, Kapil A, Sharma V. An evaluation of four different phenotypic techniques for detection of metallo-beta-lactamase producing Pseudomonas aeruginosa. Indian J Med Microbiol 2008; 26:233–237.
41. Pasanen T, Koskela S, Mero S, Tarkka E, Tissari P, Vaara M, et al. Rapid molecular characterization of Acinetobacter baumannii clones with rep-PCR and evaluation of carbapenemase genes by new multiplex PCR in Hospital District of Helsinki and Uusimaa. PLoS One 2014; 9:e85854doi: 10.1371/journal.pone.0085854.
42. van Dessel H, Dijkshoorn L, van der Reijden T, Bakker N, Paauw A, van den Broek P, et al. Identification of a new geographically widespread multiresistant Acinetobacter baumannii clone from European hospitals. Res Microbiol 2004; 155:105–112. doi: 10.1016/j.resmic.2003.10.003.
43. Higgins PG, Dammhayn C, Hackel M, Seifert H. Global spread of carbapenem-resistant Acinetobacter baumannii. J Antimicrob Chemother 2010; 65:233–238. doi: 10.1093/jac/dkp428.
44. Huang L, Sun L, Yan Y. Clonal spread of carbapenem resistant Acinetobacter baumannii ST92 in a Chinese Hospital during a 6-year period. J Microbiol 2013; 51:113–117. doi: 10.1007/s12275-013-2341-4.
45. Hamidian M, Nigro SJ, Hall RM. Problems with the Oxford multilocus sequence typing scheme for Acinetobacter baumannii: do sequence type 92 (ST92) and ST109 exist? J Clin Microbiol 2017; 55:2287–2289. doi: 10.1128/JCM.00533-17.

Acinetobacter baumannii; blaOXA-23 and blaVIM genes; rep-PCR; Transposons

© 2019 Chinese Medical Association