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Journal of Clinical Microbiology, March 2007, p. 902-905, Vol. 45, No. 3
0095-1137/07/$08.00+0     doi:10.1128/JCM.01573-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Distinct Antimicrobial Resistance Patterns and Antimicrobial Resistance-Harboring Genes According to Genomic Species of Acinetobacter Isolates{triangledown}

Yu Mi Lim,1 Kyeong Seob Shin,2 and Jungmin Kim1*

Department of Microbiology, Kyungpook National University, School of Medicine, Daegu 700-422,1 Department of Laboratory Medicine, College of Medicine, Chungbuk National University, Cheongju 361-711, Republic of Korea2

Received 31 July 2006/ Returned for modification 28 September 2006/ Accepted 13 December 2006


   ABSTRACT
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Using 58 isolates of Acinetobacter species recovered from a university hospital between August 2004 and March 2005, we performed genomic identification by amplified rRNA gene restriction analysis (ARDRA) and investigated the existence of metallo-ß-lactamase (MBL) producers and extended-spectrum ß-lactamase (ESBL) producers. Genomic species identification of Acinetobacter strains using ARDRA showed that 40 strains were genomic species 2 (Acinetobacter baumannii), 9 were 13 sensu Tjernberg and Ursing (13TU), 5 were Acinetobacter phenon 6/ct 13TU, and 4 were Acinetobacter genospecies 3. Among 58 strains, 13 isolates were MBL producers carrying blaIMP-1 or blaVIM-2 and 13 isolates were ESBL producers carrying blaPER-1. Notably, the MBL producers were mostly 13TU, Acinetobacter phenon 6/ct 13TU, and Acinetobacter genospecies 3, which showed susceptibility to ciprofloxacin and ampicillin-sulbactam. However, 12 of 13 strains carrying blaPER-1 were A. baumannii, showing multidrug resistance. The data revealed that the antimicrobial resistance patterns and resistance-harboring genes of Acinetobacter species are remarkably distinct according to the genomic species of Acinetobacter isolates.


   INTRODUCTION
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Acinetobacter species are nonfermentative gram-negative coccobacilli. There are at least 21 different Acinetobacter genospecies, nine of which have been given formal species names (14). Within the genus, the vast majority of species of clinical origin belong to the genetically closely related genomic species 2 (Acinetobacter baumannii), 3, and 13 sensu Tjernberg and Ursing (13TU) (2, 8). These genomic species are phenotypically very similar and are collectively referred to as the Acinetobacter calcoaceticus-A. baumannii complex (ACB complex) with genomic species 1 (A. calcoaceticus) (7). The clinical relevance of other genomic species in the genus has not yet been elucidated.

For the identification of Acinetobacter species, most clinical microbiological laboratories use a commercial phenotypic identification method. The efficacy of the commercial phenotypic identification systems would be considerably higher if strains belonging to A. baumannii and genomic species 1, 3, and 13TU could be identified as members of the ACB complex rather than as genomic species, but these systems have a limited capacity for the differentiation of all genomic species (1, 5, 7, 21, 25). Apart from phenotypic identification methods, several genotypic identification methods have been developed for species identification (2, 6, 10, 22, 25). One of these, amplified rRNA gene restriction analysis (ARDRA), which consists of the amplification of the 16S rRNA gene followed by separate restriction digestions with different restriction enzymes, has been tested on a large set of reference strains and has shown good correlation with DNA-DNA hybridization results (3, 10, 25).

Over the last 15 years, interest in Acinetobacter species has grown rapidly, due to the emergence and outbreak of multidrug-resistant (MDR) Acinetobacter isolates. A. baumannii are intrinsically resistant to many antimicrobial agents, and resistance to ß-lactams is most commonly associated with the production of high levels of naturally produced cephalosporinase (AmpC). However, newly acquired enzymes are a recognized source of resistance to ß-lactam agents, including carbapenems. Among the acquired enzymes, the extended-spectrum ß-lactamases (ESBLs) and metallo-ß-lactamases (MBLs) are of particular concern. Most ESBLs, which are Ambler class A ß-lactamases, confer resistance to extended-spectrum cephalosporins. However, MBLs, which are class B ß-lactamases, confer resistance to carbapenem. Recent reports have shown that ESBLs (especially PER-1) and MBLs, such as VIM-2 and IMP-1, are widespread in Acinetobacter spp. in Turkey and Korea and are a growing source of resistance to extended-spectrum cephalosporins and carbapenem in these countries (9, 13, 24, 26, 27).

In the current study, we performed genomic identification of Acinetobacter species recovered from a university hospital between August 2004 and March 2005 using the ARDRA method. We also tested for the presence of MBL- or ESBL-producing Acinetobacter species and examined the phenotypic and genotypic characteristics of MBL- or ESBL-producing Acinetobacter species.


   MATERIALS AND METHODS
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Bacterial isolates. Fifty-eight isolates of Acinetobacter species were recovered from a university hospital in Korea between August 2004 and March 2005. The Vitek GNI card (bioMeriex Vitek Inc., Hazelwood, MO) was used to identify the bacterial species.

ARDRA. Genomic species of Acinetobacter species were determined by ARDRA, as developed by Vaneechoutte et al. (25). Genomic DNA was prepared using the Wizard genomic DNA preparation kit (Promega, Madison, WI) according to the manufacturer's instructions and was used as the template for PCR to amplify the 16S rRNA genes of Acinetobacter species. PCRs were performed with previously reported primers (25) under standard PCR conditions (18). PCR products were digested with CfoI, AluI, MboI, RsaI, and MspI (Fermentas), and each digested PCR product was loaded in a 2% agarose gel in 0.5x Tris-borate-EDTA buffer (Bio-Rad, CA) at 100 V and visualized with ethidium bromide. ARDRA profiles, defined as the combination of the restriction patterns obtained with the respective enzymes, were interpreted according to the scheme of Dijkshoorn et al. (3). A. baumannii ATCC 19606 and genospecies 13 ATCC 17803 were used as controls for ARDRA identification.

Antimicrobial susceptibility test. The determination of antimicrobial susceptibility and MICs of antimicrobial agents was performed by the agar-dilution method according to the CLSI (formerly NCCLS) guidelines (15). Pseudomonas aeruginosa ATCC 27853 and Escherichia coli ATCC 25922 were used as quality control strains. The antimicrobial agents included were piperacillin (MP Biomedicals, France), ticarcillin (MP Biomedicals, France), amikacin (ICN Biomedicals), gentamicin (Shinpoong Pharmaceutical), tobramycin (Dongkwang Pharmaceutical), ciprofloxacin (Sigma-Aldrich, China), ceftazidime (Greenford, England), cefepime (Boryoung Pharmaceutical), aztreonam (MP Biomedicals, France), imipenem (Merck & Co), meropenem (Yuhan Pharmaceutical), and ampicillin-sulbactam (at a ratio of 2:1; Korean Union Pharmaceutical).

Detection of MBL-producing strains. Thirty-six strains showing nonsusceptibility to imipenem were examined for the production of MBLs by an imipenem-EDTA disk synergy test as described by Lee and colleagues (12). Detection of blaVIM-2 or blaIMP-1 genes in MBL producers was performed under standard PCR conditions (18) using previously reported primers.

Detection of bla gene-carrying strains. Fifty-three strains showing nonsusceptibility to cefepime were examined by the PCR method for the production of ESBLs. Under standard PCR conditions (18), blaTEM, blaSHV, blaCTX-M-3, and blaPER-1 were amplified using previously reported primers (11, 17). Further determination of blaTEM alleles was performed by nucleotide sequencing of PCR products on both strands with the primers used for PCR, and sequencing was performed as described previously (11).

Clonal analysis by PFGE. For clonal analysis of Acinetobacter strains, genomic DNA was analyzed by pulsed-field gel electrophoresis (PFGE) according to the method of Gautom (4). The genomic DNA was digested with ApaI (Boerhinger Mannheim Co.) for 18 h and separated on a 1.0% InCert agarose gel using a contour-clamped homogeneous-field apparatus (CHEF DRIII systems; Bio-Rad Laboratories) in 0.5x Tris-borate-EDTA buffer. The conditions for electrophoresis were 6 V/cm for 18.5 h with an increasing pulse time from 5 to 20 s at 14°C with an angle of 120°. A lambda DNA ladder comprised of 48.5-kb concatemers (Bio-Rad Laboratories) was used as the size standard. Digital images were stored electronically as TIFF files and analyzed with GelCompar (Applied Maths).


   RESULTS
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Using 58 strains of Acinetobacter spp. identified by the Vitek GNI card as belonging to the ACB complex, we performed genomic identification using the ARDRA method. The results revealed that 40 strains were genomic species 2 (A. baumannii), 9 were 13TU, 5 were Acinetobacter phenon 6/ct 13TU, and 4 were genospecies 3.

In an antimicrobial susceptibility test, most strains of Acinetobacter spp. were resistant to piperacillin, amikacin, gentamicin, tobramicin, and ceftazidime, showing resistance rates of more than 80% (Table 1). Forty strains of A. baumannii showed resistance to most antimicrobial agents except carbapenems, and 13 of 40 strains were resistant to all tested antimicrobial agents including carbapenems. Acinetobacter phenon 6/ct 13TU showed resistance to gentamicin, tobramycin, piperacillin, and imipenem, but was susceptible to other agents, such as ciprofloxacin, extended-spectrum ß-lactams, ampicillin/sulbactam, and meropenem. The antimicrobial agents to which A. baumannii strains were most susceptible were meropenem and imipenem, but the agents to which non-baumannii Acinetobacter strains were most susceptible were ciprofloxacin and ampicillin/sulbactam.


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  		TABLE 1. Antimicrobial susceptibilities of clinical isolates of Acinetobacter species for which genomic species were identified by amplified rRNA gene restriction analysis

 
Thirty-six strains showing nonsusceptibility to imipenem were examined for the production of MBLs by an imipenem-EDTA synergy test, and 13 of the 36 strains tested positive (Table 2). They were subjected to PCR for the detection of the MBL-encoding genes blaVIM-2 and blaIMP-1. The blaVIM-2 gene was detected in five strains of Acinetobacter phenon 6/ct 13TU and three strains of 13TU. The blaIMP-1 gene was detected in two strains of genospecies 3, two strains of 13TU, and one strain of A. baumannii.


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  		TABLE 2. Resistance to imipenem and cefepime and PCR detection of acquired class B metallo-ß-lactamase genes and class A ß-lactamase genes in clinical isolates of Acinetobacter species

 
Fifty-three strains showing nonsusceptibility to cefepime were subjected to PCR for the detection of bla genes, including blaTEM, blaSHV, blaCTX-M-3, and blaPER-1 (Table 2). Thirteen strains were found to have blaPER-1, and 12 of them were A. baumannii. In 27 strains of A. baumannii, the blaTEM gene was detected and confirmed to be blaTEM-1 by a further sequencing analysis. No strains carried blaSHV or blaCTX-M-3.

The level of resistance to each antimicrobial agent for Acinetobacter strains was determined by the MIC of each drug. As shown in Table 3, the strains carrying blaPER-1 showed a remarkably high level of resistance to extended-spectrum ß-lactams, such as ceftazidime, cefepime, and aztreonam (MIC50, ≥128 µg/ml). In addition, 12 of 13 strains carrying blaPER-1, with the exception being one strain of 13TU, were resistant to all antimicrobial agents tested including ampicillin/sulbactam and imipenem. The strains carrying blaVIM-2 or blaIMP-1 showed intermediate susceptibilities to extended-spectrum ß-lactams and ampicillin/sulbactam, and they were highly susceptible to ciprofloxacin.


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  		TABLE 3. MICs for Acinetobacter isolates grouped by resistance-harboring gene

 
By PFGE analysis, 40 strains of A. baumannii revealed five distinct PFGE patterns, and 11 of 12 strains of A. baumannii carrying blaPER-1 showed the same PFGE pattern. Five strains of Acinetobacter phenon 6/ct 13TU revealed three distinct patterns and nine strains of 13TU showed five distinct PFGE patterns. Four strains of Acinetobacter genospecies 3 showed patterns different from each other.


   DISCUSSION
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In the current study, we performed genotypic identification of Acinetobacter species using the ARDRA method and analyzed them for their antimicrobial resistance characteristics according to the genomic species. Significantly, the antimicrobial resistance patterns and resistance-harboring genes were remarkably distinct according to the genomic species of Acinetobacter isolates. Whereas 40 strains of A. baumannii showed resistance to most antimicrobial agents except carbapenems, non-baumannii Acinetobacter strains, such as Acinetobacter phenon 6/ct 13TU, genospecies 3, and 13TU, were susceptible to ciprofloxacin and ampicillin/sulbactam. In addition, 39 of 40 A. baumannii strains carried bla genes such as blaPER-1 or blaTEM-1. Twelve of 18 non-baumannii Acinetobacter strains carried MBL genes such as blaVIM-2 or blaIMP-1, which confer resistance to carbapenems. Therefore, ESBL-producing Acinetobacter strains were mostly A. baumannii strains showing MDR characteristics. MBL-producing Acinetobacter strains were mostly non-baumannii Acinetobacter strains showing lower levels of resistance to most antimicrobial agents than did A. baumannii strains, except for the level of resistance to imipenem. The current results suggest the importance of genomic identification of Acinetobacter species for the elucidation of the clinical significance of the genomic species within the genus Acinetobacter and of considering different treatment regimens according to the genomic species for treating Acinetobacter infections.

In this study, the blaVIM-2 gene was detected in five isolates of Acinetobacter phenon 6/ct 13TU and three isolates of Acinetobacter strain 13TU, whereas the blaIMP-1 gene was detected in two isolates of Acinetobacter genospecies 3, two isolates of 13TU, and one isolate of A. baumannii. The results clearly showed that the majority of MBL-producing Acinetobacter were non-baumannii Acinetobacter strains, mainly Acinetobacter phenon 6/ct 13TU, genospecies 3, and 13TU. This finding is highly significant because the antimicrobial susceptibilities of non-baumannii Acinetobacter strains are usually much higher than those of A. baumannii, thus enabling us to use more effective antimicrobial agents for treating MBL-producing Acinetobacter isolates. In fact, many studies of the MBL-producing Acinetobacter strains have applied conventional phenotypic methods or commercial kits such as the ATB 32 GN system, which are inappropriate for genomic species identification (12, 24, 26, 27). Therefore, it is not always clear which of the genomic species were involved in those cases. Yum et al. (27) reported that the blaVIM-2 gene was detected in 11 isolates of A. baumannii and 2 isolates of Acinetobacter genospecies 3 and the blaIMP-1 gene in one isolate of A. baumannii. They used the ATB 32 GN system to identify Acinetobacter species in that report. However, in a previous study comparing the ID 32 GN system with ARDRA for the identification of A. baumannii (19), 9 of 78 strains identified as A. baumannii by the ID 32 GN system were identified as Acinetobacter 13TU by ARDRA, suggesting that the ID 32 GN system is inappropriate for the differentiation of A. baumannii from 13TU. Therefore, it is possible that some of the 11 strains of A. baumannii carrying the blaVIM-2 gene that were detected by Yum and his colleagues belonged to Acinetobacter 13TU strains.

PER-1 is an ESBL which was first found in a P. aeruginosa strain from a Turkish patient in France (16) and which was subsequently found in Acinetobacter species and P. aeruginosa in Turkey, Korea, and Italy (13, 24, 26). Although the double-disk synergy test (DDST) has been used to detect ESBL producers among gram-negative pathogens, detection of ESBL-producing Acinetobacter species by DDST appears to be difficult and unreliable. Yong et al. showed that DDST is unreliable for the screening of PER-1-producing Acinetobacter strains and that only PCR reliably detected PER-1 producers (26). In this study, the blaPER-1 gene was detected by PCR in 13 of 58 strains of Acinetobacter species and 12 of 13 isolates carrying the blaPER-1 gene were A. baumannii isolates. A number of researchers (20, 24, 26) have shown that the blaPER-1-positive A. baumannii isolates used in this study were resistant to all cephalosporins, including cefepime, and to aminoglycosides, ampicillin/sulbactam, ciprofloxacin, and even imipenem. Besides the multidrug resistance of PER-1 producers, PER-1 production can cause serious therapeutic problems and has been found to be an independent indicator of poor prognosis (23). Therefore, it is important to have effective control measures, such as detecting infected patients early, finding the source of colonization or infection, implementing appropriate guidelines for antimicrobial use, and using antimicrobial agents prudently, to avoid spreading this troublesome pathogen.


   FOOTNOTES
 
* Corresponding author. Mailing address: Department of Microbiology, Kyungpook National University, School of Medicine, 101, Dongin-2Ga, Junggu, Daegu 700-422, Republic of Korea. Phone: 82-53-420-4845. Fax: 82-53-427-5664. E-mail: minkim{at}knu.ac.kr. Back

{triangledown} Published ahead of print on 27 December 2006. Back


   REFERENCES
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 Results
 Discussion
 References
 

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Journal of Clinical Microbiology, March 2007, p. 902-905, Vol. 45, No. 3
0095-1137/07/$08.00+0     doi:10.1128/JCM.01573-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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