This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Wu, J.-J.
Right arrow Articles by Yan, J.-J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Wu, J.-J.
Right arrow Articles by Yan, J.-J.

 Previous Article  |  Next Article 

Antimicrobial Agents and Chemotherapy, April 2007, p. 1223-1227, Vol. 51, No. 4
0066-4804/07/$08.00+0     doi:10.1128/AAC.01195-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Prevalence of Plasmid-Mediated Quinolone Resistance Determinants QnrA, QnrB, and QnrS among Clinical Isolates of Enterobacter cloacae in a Taiwanese Hospital{triangledown}

Jiunn-Jong Wu,1 Wen-Chien Ko,2 Shu-Huei Tsai,3 and Jing-Jou Yan3,4*

Departments of Medical Laboratory Science and Biotechnology,1 Internal Medicine,2 Pathology, College of Medicine, National Cheng Kung University,3 Department of Pathology, National Cheng Kung University Hospital, Tainan, Taiwan, Republic of China4

Received 23 September 2006/ Returned for modification 11 December 2006/ Accepted 15 January 2007


arrow
ABSTRACT
 
The prevalence of three plasmid-mediated quinolone resistance determinants, QnrA, QnrB, and QnrS, among 526 nonreplicate clinical isolates of Enterobacter cloacae collected at a Taiwanese university hospital in 2004 was determined by PCR and colony hybridization, and the association of Qnr with the IMP-8 metallo-ß-lactamase was investigated. Eighty-six (16.3%) of all isolates were qnr positive, and the qnrA1-like, qnrB2-like, and qnrS1-like genes were detected alone or in combination in 3 (0.6%), 53 (10.1%), and 34 (6.5%) isolates, respectively. Among 149 putative extended-spectrum-ß-lactamase-producing isolates, 59 (39.6%) isolates, all of which were SHV-12 producers, harbored qnrA (0.7%; 1 isolate), qnrB (28.9%; 43 isolates), or qnrS (12.1%; 18 isolates). Forty-four (78.6%) of 56 IMP-8 producers carried qnrB (58.9%; 33 isolates), qnrS (25.0%; 14 isolates), or both. PCR and sequence analysis revealed that qnrA1 was located in a complex sul1-type integron that contains dhr15, aadA2, qacE{Delta}1, sul1, orf513, qnrA1, ampR, and qacE{Delta}1. Conjugation experiments revealed the coexistence of qnrB and blaIMP-8 on the transferred plasmids and the absence of ß-lactamase content on the transferred qnrS-positive plasmids. The transferred blaIMP-8-positive plasmids with and without qnrB had very similar restriction patterns, suggesting the horizontal mobility of qnrB. Pulsed-field gel electrophoresis showed six major patterns among the 44 qnr-positive IMP-8-producing isolates. Thus, the extremely high prevalence of qnr among the metallo-ß-lactamase-producing E. cloacae isolates in the hospital may be due mainly to the intrahospital spread of a few clones and the dissemination of plasmids containing both qnrB and blaIMP-8.


arrow
INTRODUCTION
 
Since the first plasmid-mediated quinolone resistance determinant, Qnr (later termed QnrA), was described in a Klebsiella pneumoniae strain from the United States in 1998 (17), three major groups of Qnr determinants, QnrA, QnrB, and QnrS, have been identified in various enterobacterial species (3-14, 17, 20, 22, 33, 34). Qnr determinants may protect DNA gyrase directly from quinolone inhibition, leading to an 8- to 32-fold increase in MICs of quinolones (31). qnrA has been well known for its worldwide distribution and is located in complex sul1-type class 1 integrons (12, 16, 20, 22, 28, 33). Such integrons consist of duplicate qacE{Delta}1 and sul1 genes, which surround a putative recombinase gene, orf513 (23). At least five qnrB and two qnrS variants have been described (1, 7-9, 11, 26), among which only qnrB2 has been found in the complex sul1-type integron (7). QnrB and QnrS have been detected in Asia, Europe, and the United States (1, 4, 8, 9, 14, 24).

In Taiwan, qnrS on a plasmid encoding the SHV-2 extended-spectrum ß-lactamase (ESBL) from a K. pneumoniae strain has been described (4), and the presence of qnrA and qnrB has not been reported. The present study was conducted to determine the prevalence of the three groups of Qnr among Enterobacter cloacae isolates in a Taiwanese teaching hospital. An extraordinary high frequency of qnr among E. cloacae isolates with the IMP-8 metallo-ß-lactamase (MBL) was observed, and the emergence of qnrA and qnrB in Taiwan is reported first in this work.


arrow
MATERIALS AND METHODS
 
Bacterial isolates. A total of 526 nonreplicate clinical isolates of E. cloacae consecutively collected in 2004 at National Cheng Kung University Hospital were analyzed for the presence of qnr genes. Each isolate was obtained from a single patient.

Detection of qnr genes. The qnrA, qnrB, and qnrS genes were detected by PCR with the primer sets shown in Table 1 and colony hybridization with a DIG DNA labeling and detection kit (Roche Applied Science, Mannheim, Germany) according to the manufacturer's instructions. qnrB-CS-1A and qnrB-CS-1B are consensus primers chosen from regions with high levels of sequence homology to the qnrB genes known in April 2006. Both strands of amplicons were sequenced with the same primers for PCR amplification, and all PCR experiments were performed at least twice. The qnr probes were prepared by using PCR products as the templates.


View this table:
[in this window]
[in a new window]

  		TABLE 1. Primers used for PCR amplification

Susceptibility testing. Isolates were screened for the production of ESBLs and MBLs by the double-disk synergy test and the 2-mercaptopropionic acid double-disk potentiation method, respectively, as described previously (32, 35). MICs of amikacin, ampicillin, aztreonam, cefepime, cefotaxime, ceftazidime, cephalothin, ciprofloxacin, gentamicin, imipenem, and nalidixic acid were determined by the agar dilution method according to CLSI (formerly NCCLS) guidelines (19).

ß-Lactamase characterization. The expression of ß-lactamases was detected by isoelectric focusing (IEF) using an LKB Multiphor apparatus (GE Healthcare Life Sciences, Hong Kong) as described previously (18, 36). The presence of blaSHV (21), blaTEM (15), and bla genes related to blaCTX-M-1 (29), blaCTX-M-9 (29), and blaIMP-2 (36) was detected by PCR and nucleotide sequencing with previously reported oligonucleotide primers (Table 1).

PFGE. Pulsed-field gel electrophoresis (PFGE) analysis of XbaI-digested genomic DNA was performed using a CHEF-DR 3 apparatus (Bio-Rad Laboratories, Hercules, CA) according to the instruction manual. PFGE patterns were interpreted according to criteria described previously by Tenover et al. (30). The patterns were considered to belong to the same type if there was a difference of no more than three bands.

Conjugation experiments and plasmid analysis. Conjugation experiments were performed by the liquid mating-out assay using streptomycin-resistant Escherichia coli C600 as the recipient as described previously (25, 36). Transconjugants were selected on tryptic soy agar plates containing 512 µg of streptomycin (Sigma Chemical Co., St. Louis, MO) per ml and 8 µg of nalidixic acid (Sigma) per ml or 2 µg of ceftazidime (Glaxo Group Research, Greenford, United Kingdom) per ml. Plasmid DNA samples extracted from transconjugants were digested with the endonuclease EcoRI (Roche Applied Science). The resulting fragments were loaded onto a 0.8% agarose gel and then subjected to Southern hybridization with the digoxigenin-labeled qnr probes. The sizes of transferred plasmids were estimated by adding up restriction fragments.

Structure analysis of the qnrA-containing integron. A qnrA-positive isolate was randomly selected for structure analysis of the qnrA-containing integron. PCR was performed with the primer pair Int1-6A and qnrA-1B and the primer pair Int1-6A and qacE-2B to amplify nucleotide sequences upstream and downstream, respectively, of qnrA (Table 1). Both strands of PCR products were sequenced by gene walking with custom sequencing primers. Nucleotide and amino acid sequences were analyzed and compared by use of the BLAST computer program (National Center for Biotechnology Information).

Nucleotide sequence accession number. The nucleotide sequence of the qnrA-positive integron from isolate EB715/04 has been submitted to the GenBank database and assigned accession number DQ989302.


arrow
RESULTS
 
Prevalence of qnr genes. The qnrA, qnrB, and qnrS genes were detected in 3 (0.6%), 53 (10.1%), and 34 (6.5%) of the isolates, respectively, by PCR and colony hybridization and were found to belong to the qnrA1, qnrB2, and qnrS1 alleles by subsequent sequencing of all PCR products. Since four isolates carried both qnrS and qnrB, the prevalence of any qnr gene was 86 (16.3%) of all isolates.

Association of qnr with MBL and ESBL production. Among the 526 E. cloacae isolates, the phenotypic screening tests suggested MBL and ESBL production in 56 (10.6%) and 149 (28.3%) isolates, respectively. Presumptive ESBLs were detected in 46 (82.1%) of the 56 putative MBL producers. The prevalence of the three qnr genes among putative ESBL, MBL, non-ESBL, and non-MBL producers is shown in Table 2. Overall, 44 (78.6%) of the 56 putative MBL producers and 59 (39.6%) of the 149 putative ESBL producers carried any of the three qnr genes.


View this table:
[in this window]
[in a new window]

  		TABLE 2. Distribution of qnrA, qnrB, and qnrS among ESBL-producing, MBL-producing, and non-ESBL- and non-MBL-producing E. cloacae isolates

The ß-lactamase contents of all putative MBL producers and all qnr-positive ESBL-producing isolates were determined according to the results of IEF and PCR experiments (2, 36). The IMP-8-type MBL (pI 8.2) was detected in all 56 putative MBL producers, and the SHV-12-type ESBL (pI 8.2) was detected in all 59 qnr-positive ESBL producers. Moreover, the TEM-1-type narrow-spectrum ß-lactamase (pI 5.4) was detected in all MBL producers and 11 of the 25 non-MBL-producing ESBL producers, and a pI 8.0 ß-lactamase that might represent the chromosomal AmpC ß-lactamase of E. cloacae was detected in all test isolates. The blaCTX-M genes were not detected by PCR. Accordingly, one of the three qnrA1-like-positive isolates expressed SHV-12; 43 (81.1%) and 33 (62.3%) of the 53 qnrB2-like-positive isolates and 18 (52.9%) and 14 (41.2%) of the 34 qnrS1-like-positive isolates produced SHV-12 and IMP-8, respectively.

PFGE. The 44 qnr-positive IMP-8-producing isolates gave six major patterns, designated patterns I to VI, and various subtypes were observed in patterns I to IV and VI (Fig. 1). Among the 14 qnrS-positive MBL producers, all 11 isolates that were negative for qnrB belonged to pattern II; the remaining 3 isolates that were positive for qnrB belonged to three different patterns. The 33 qnrB-positive isolates belonged to five major patterns, patterns I and III to VI, and 18 of them belonged to pattern IV.


Figure 1
View larger version (49K):
[in this window]
[in a new window]

  		FIG. 1. PFGE patterns of 44 qnr-positive IMP-8-producing E. cloacae isolates. Lane M, lambda ladder. The numbers of isolates that were represented by each pattern are shown below the gel.

Conjugation experiments and plasmid analysis. The results of conjugation experiments and plasmid analysis for the 56 IMP-8-producing isolates are shown in Fig. 2 and Table 3. Five qnrS-positive transconjugants were obtained and revealed no ß-lactamase activity in the IEF analysis. All qnrS-positive plasmids showed the same restriction pattern and were about 7 kb in size. Eight qnrB-positive transconjugants were obtained, and blaTEM-1, blaSHV-12, and blaIMP-8 were found to be cotransferred with qnrB. blaIMP-8-positive plasmids that were negative for any qnr gene were also obtained from 4 of 12 qnr-negative and 11 of 14 qnrS-positive isolates; these conjugable plasmids were all greater than 150 kb in size and gave 12 restriction patterns, designated B1 to B12. With only one to three band differences, the qnrB-positive plasmids with patterns B3 to B5 were very similar to the qnrB-negative plasmids with patterns B6 to B8. The qnrB probe hybridized with a 2.4-kb restricted fragment in all qnrB-positive plasmids.


Figure 2
View larger version (80K):
[in this window]
[in a new window]

  		FIG. 2. EcoRI restriction patterns of conjugative plasmids. The results of Southern hybridization with the digoxigenin-labeled qnr probes are shown below the gels. Asterisks indicate the hybridized restriction fragments. Lane M1, molecular marker II (Roche Applied Science); lane M2, 1-kb molecular marker (Promega Co., Taipei, Taiwan, Republic of China). (A) Transferred qnrS-positive plasmids and hybridization with the qnrS probe. Lanes 1 and 2, restriction pattern A. (B) Transferred blaIMP-8-positive plasmids that were positive (lanes 1 to 5) and negative (lanes 6 to 12) for qnrB and hybridization with the qnrB probe. Lanes 1 to 12, restriction patterns B1 to B12.


View this table:
[in this window]
[in a new window]

  		TABLE 3. Restriction patterns of conjugative plasmids and transferred resistance genes in conjugation experiments

Susceptibility testing. Of the 86 qnr-positive isolates, 100% and 43.0% were nonsusceptible (resistant or intermediately resistant) to nalidixic acid (MIC, 32 to >256 µg/ml; MIC90, >256 µg/ml) and ciprofloxacin (MIC, 0.13 to 32 µg/ml; MIC90, 16 µg/ml), respectively, and 86.0% were nonsusceptible to ceftazidime, 97.8% to cefotaxime, 33.7% to cefepime, 77.9% to aztreonam, 9.3% to imipenem, 75.6% to gentamicin, and 3.5% to amikacin. Eight imipenem-nonsusceptible isolates were all MBL producers. Among the 86 qnr-positive isolates, the 69 isolates that were positive for IMP-8 and/or SHV-12 had remarkably higher rates than the 17 isolates that were negative for MBL and ESBL in nonsusceptibilities to ceftazidime (100% versus 29.4%), cefepime (40.6% versus 5.9%), aztreonam (85.5% versus 47.1%), and gentamicin (89.9% versus 17.6%).

The five qnrS-positive and eight qnrB-positive transconjugants revealed decreased susceptibilities to nalidixic acid (MIC, 16 to 32 µg/ml) and ciprofloxacin (MIC, 0.25 to 0.5 µg/ml). All qnrB-positive transconjugants revealed resistance or decreased susceptibilities to extended-spectrum cephalosporins, imipenem, and gentamicin; all qnrS-positive transconjugants showed no decreased susceptibilities to ampicillin, cephalothin, extended-spectrum cephalosporins, and aminoglycosides (data not shown).

Structure of the qnrA1-containing integron. Primers Int1-6A and qnrA-1B generated an approximately 5.8-kb amplicon and primers qnrA-1A and qacE-2B generated an approximately 2-kb amplicon from a qnrA-positive strain, EB715/04. Nucleotide sequencing revealed that qnrA1 was located in a complex sul1-type integron that contains dhr15, aadA2, qacE{Delta}1, sul1, orf513, qnrA1, ampR, and qacE{Delta}1. The integron and In36 of an E. coli isolate from the People's Republic of China differed only by the first gene cassette, which is the dhr16 cassette in In36 (33).


arrow
DISCUSSION
 
The present study demonstrated the high prevalence (16.3%) of plasmid-mediated quinolone resistance among E. cloacae isolates in a Taiwanese university hospital. The prevalence rates of qnr among putative ESBL producers (39.6%) and MBL producers (78.6%) were much higher than that among putative non-ESBL and non-MBL producers (4.6%) (Table 2). The high prevalence of qnr among E. cloacae isolates, and extended-spectrum-cephalosporin-resistant or ESBL-producing isolates in particular, has also been described in several reports (6, 22, 26). Three Qnr groups were all detected, and QnrA and QnrB are described for the first time in Taiwan in this report. Among all isolates, qnrB was the most prevalent (10.1%), followed by qnrS (6.5%); however, qnrS was the most prevalent among the putative non-ESBL and non-MBL producers. qnrA was uncommon (0.6%) in this study, and the low rates of qnrA have been observed in most surveillance studies (10, 12, 16, 20, 27). The qnrA1 gene of our isolate is also located in a complex sul1-type integron, which is different from In36 of an E. coli isolate from the People's Republic of China only in the first gene cassette (33).

Only one qnrA1-positive isolate from Australia has been reported to express an MBL (IMP-4), and this is the first report of the association of qnrB and qnrS with genes encoding MBLs. IMP-8 is an IMP-2 variant that is unique in Taiwan (36). The coexistence of the qnrB2-like gene and blaIMP-8 on the same plasmids and only five major PFGE patterns among the 33 qnrB-positive IMP-8-producing isolates suggest that the high prevalence of qnrB among MBL producers was due to the horizontal transfer of plasmids containing both qnrB and blaIMP-8 and the intrahospital spread of several clones. The high prevalence of qnrS among MBL producers may be due mainly to intrahospital spread or nosocomial outbreaks of an E. cloacae clone that carried qnrS and blaIMP-8 on different plasmids.

Previous studies showed that qnr-positive strains frequently expressed ESBLs, such as SHV-2 (4), SHV-7 (34), SHV-12 (11, 26), CTX-M-9 (22), CTX-M-14 (5), CTX-M-15 (11), and VEB-1 (16), and QnrA has also been linked to genes encoding plasmid-mediated cephalosporinases (20, 27, 34). All our qnr-positive ESBL-producing isolates carried blaSHV-12. The qnrB2-like gene was more prevalent than the qnrS1-like gene among the 149 putative ESBL producers (28.9% versus 12.1%) (Table 2). The prevalence rate of qnrS among the non-MBL-producing ESBL producers was very close to that among the non-MBL- and non-ESBL-producing isolates (4.9% versus 4.1%). Among the 18 qnrS-positive ESBL producers, 13 (72.2%) isolates were also MBL producers. Moreover, 46 of the 56 MBL producers carried blaSHV-12, and the coexistence of blaSHV-12 and blaIMP-8 on the transferred plasmids was observed as described previously (36). Thus, the finding that qnrS was common among the ESBL producers may result from the clonal spread of E. cloacae isolates that harbored plasmids with both blaSHV-12 and blaIMP-8.

Although the qnrS1 gene first reported in Taiwan was identified on a plasmid encoding the SHV-2-type ESBL (4), all transferable qnrS-positive plasmids in our isolates appeared to contain no ß-lactamase gene. The restriction patterns of the transferred qnrB-positive, blaIMP-8-positive plasmids were very similar to those of qnrB-negative, blaIMP-8-positive plasmids (Fig. 2), suggesting the occurrence of horizontal mobility of the qnrB2-like gene. The qnrB2 gene has been located in a complex sul1-type integron of a Salmonella enterica serovar Keurmassar strain (7). The association of qnrS and qnrB with integrons was not found in our isolates by PCR mapping (unpublished data). The genetic mechanisms responsible for the mobility of the two qnr genes in Taiwan need further studies.


arrow
ACKNOWLEDGMENTS
 
This work was supported by grant NSC89-2314-B-006-031 from the National Science Council, Taiwan.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Department of Pathology, National Cheng Kung University Hospital, 138 Sheng-Li Road, Tainan 70428, Taiwan, Republic of China. Phone: 886-6-2353535, ext. 2634. Fax: 886-6-2766195. E-mail: jingjou{at}mail.ncku.edu.tw Back

{triangledown} Published ahead of print on 22 January 2007. Back


arrow
REFERENCES
 
    1
  1. Bönemann, G., M. Stiens, A. Pühler, and A. Schlüter. 2006. Mobilizable IncQ-related plasmid carrying a new quinolone resistance gene, qnrS2, isolated from the bacterial community of a wastewater treatment plant. Antimicrob. Agents Chemother. 50:3075-3080.[Abstract/Free Full Text]
    2. 2
  2. Bush, K., G. A. Jacoby, and A. A. Medeiros. 1995. A functional classification scheme for ß-lactamases and its correlation with molecular structure. Antimicrob. Agents Chemother. 39:1211-1233.[Medline]
    3. 3
  3. Cambau, E., C. Lascols, W. Sougakoff, C. Bebear, R. Bonnet, J. D. Cavallo, L. Gutmann, M. C. Ploy, V. Jarlier, C. J. Soussy, and J. Robert. 2006. Occurrence of qnrA-positive clinical isolates in French teaching hospitals during 2002-2005. Clin. Microbiol. Infect. 12:1013-1020.[CrossRef][Medline]
    4. 4
  4. Chen, Y.-T., H.-Y. Shu, L.-H. Li, T.-L. Liao, K.-M. Wu, Y.-R. Shiau, J.-J. Yan, I.-J. Su, S.-F. Tsai, and T.-L. Lauderdale. 2006. Complete nucleotide sequence of pK245, a 98-kilobase plasmid conferring quinolone resistance and extended-spectrum-ß-lactamase activity in a clinical Klebsiella pneumoniae isolate. Antimicrob. Agents Chemother. 50:3861-3866.[Abstract/Free Full Text]
    5. 5
  5. Cheung, T. K., Y. W. Chu, M. Y. Chu, C. H. Ma, R. W. Yung, and K. M. Kam. 2005. Plasmid-mediated resistance to ciprofloxacin and cefotaxime in clinical isolates of Salmonella enterica serotype Enteritidis in Hong Kong. J. Antimicrob. Chemother. 56:586-589.[Abstract/Free Full Text]
    6. 6
  6. Corkill, J. E., J. J. Anson, and C. A. Hart. 2005. High prevalence of the plasmid-mediated quinolone resistance determinant qnrA in multidrug-resistant Enterobacteriaceae from blood cultures in Liverpool, UK. J. Antimicrob. Chemother. 56:1115-1117.[Abstract/Free Full Text]
    7. 7
  7. Garnier, F., N. Raked, A. Gassama, F. Denis, and M.-C. Ploy. 2006. Genetic environment of quinolone resistance gene qnrB2 in a complex sul1-type integron in the newly described Salmonella enterica serovar Keurmassar. Antimicrob. Agents Chemother. 50:3200-3202.[Abstract/Free Full Text]
    8. 8
  8. Gay, K., A. Robicsek, J. Strahilevitz, C.-.H. Park, G. Jacoby, T. J. Barrett, F. Medalla, T. M. Chiller, and D. C. Hooper. 2006. Plasmid-mediated quinolone resistance in non-Typhi serotypes of Salmonella enterica. Clin. Infect. Dis. 43:297-304.[CrossRef][Medline]
    9. 9
  9. Hata, M., M. Suzuki, M. Matsumoto, M. Takahashi, K. Sato, S. Ibe, and K. Sakae. 2005. Cloning of a novel gene for quinolone resistance from a transferable plasmid in Shigella flexneri 2b. Antimicrob. Agents Chemother. 49:801-803.[Abstract/Free Full Text]
    10. 10
  10. Jacoby, G. A., N. Chow, and K. B. Waites. 2003. Prevalence of plasmid-mediated quinolone resistance. Antimicrob. Agents Chemother. 47:559-562.[Abstract/Free Full Text]
    11. 11
  11. Jacoby, G. A., K. E. Walsh, D. M. Mills, V. J. Walker, H. Oh, A. Robicsek, and D. C. Hooper. 2006. qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob. Agents Chemother. 50:1178-1182.[Abstract/Free Full Text]
    12. 12
  12. Jeong, J.-Y., H. J. Yoon, E. S. Kim, Y. Lee, S.-H. Choi, N. J. Kim, J. H. Woo, and Y. S. Kim. 2005. Detection of qnr in clinical isolates of Escherichia coli from Korea. Antimicrob. Agents Chemother. 49:2522-2524.[Abstract/Free Full Text]
    13. 13
  13. Jonas, D., K. Biehler, D. Hartung, B. Spitzmüller, and F. D. Daschner. 2005. Plasmid-mediated quinolone resistance in isolates obtained in German intensive care units. Antimicrob. Agents Chemother. 49:773-775.[Abstract/Free Full Text]
    14. 14
  14. Kehrenberg, C., S. Friederichs, A. de Jong, G. B. Michael, and S. Schwarz. 2006. Identification of the plasmid-borne quinolone resistance gene qnrS in Salmonella enterica serovar Infantis. J. Antimicrob. Chemother. 58:18-22.[Abstract/Free Full Text]
    15. 15
  15. Mabilat, C., and S. Goussard. 1993. PCR detection and identification of genes for extended-spectrum ß-lactamases, p. 553-559. In D. H. Persing, T. F. Smith, F. C. Tenover, and T. J. White (ed.), Diagnostic molecular microbiology: principles and applications. American Society for Microbiology, Washington, DC.
    16. 16
  16. Mammeri, H., M. Van De Loo, L. Poirel, L. Martinez-Martinez, and P. Nordmann. 2005. Emergence of plasmid-mediated quinolone resistance in Escherichia coli in Europe. Antimicrob. Agents Chemother. 49:71-76.[Abstract/Free Full Text]
    17. 17
  17. Martínez-Martínez, L., A. Pascual, and G. A. Jacoby. 1998. Quinolone resistance from a transferable plasmid. Lancet 351:797-799.[CrossRef][Medline]
    18. 18
  18. Matthew, M., M. Harris, M. J. Marshall, and G. W. Rose. 1975. The use of analytical isoelectric focusing for detection and identification of ß-lactamases. J. Gen. Microbiol. 88:169-178.[Medline]
    19. 19
  19. National Committee for Clinical Laboratory Standards. 2003. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, 6th ed. Approved standard M7-A6. National Committee for Clinical Laboratory Standards, Wayne, PA.
    20. 20
  20. Nordmann, P., and L. Poirel. 2005. Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae. J. Antimicrob. Chemother. 56:463-469.[Abstract/Free Full Text]
    21. 21
  21. Nüesch-Inderbinen, M. T., H. Hächler, and F. H. Kayser. 1996. Detection of genes coding for extended-spectrum SHV beta-lactamases in clinical isolates by a molecular genetic method, and comparison with the E test. Eur. J. Clin. Microbiol. Infect. Dis. 15:398-402.[CrossRef][Medline]
    22. 22
  22. Paauw, A., A. C. Fluit, J. Verhoef, and M. A. Leverstein-van Hall. 2006. Enterobacter cloacae outbreak and emergence of quinolone resistance gene in Dutch hospital. Emerg. Infect. Dis. 12:807-812.[Medline]
    23. 23
  23. Partridge, S. R., and R. M. Hall. 2003. In34, a complex In5 family class 1 integron containing orf513 and dfrA10. Antimicrob. Agents Chemother. 47:342-349.[Abstract/Free Full Text]
    24. 24
  24. Poirel, L., T. V. Nguyen, A. Weintraub, C. Leviandier, and P. Nordmann. 2006. Plasmid-mediated quinolone resistance determinant qnrS in Enterobacter cloacae. Clin. Microbiol. Infect. 12:1021-1023.[CrossRef][Medline]
    25. 25
  25. Provence, D. L., and R. Curtiss III. 1994. Gene transfer in gram-negative bacteria, p. 319-347. In P. Gerhardt, R. G. E. Murray, W. A. Wood, and N. R. Krieg (ed.), Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC.
    26. 26
  26. Robicsek, A., J. Strahilevitz, D. F. Sahm, G. A. Jacoby, and D. C. Hooper. 2006. qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States. Antimicrob. Agents Chemother. 50:2872-2874.[Abstract/Free Full Text]
    27. 27
  27. Rodríguez-Martínez, J.-M., A. Pascual, I. García, and L. Martínez-Martínez. 2003. Detection of the plasmid-mediated quinolone resistance determinant qnr among clinical isolates of Klebsiella pneumoniae producing AmpC-type ß-lactamase. J. Antimicrob. Chemother. 52:703-706.[Abstract/Free Full Text]
    28. 28
  28. Rodriguez-Martinez, J.-M., L. Poirel, A. Pascual, and P. Nordmann. 2006. Plasmid-mediated quinolone resistance in Australia. Microb. Drug Resist. 12:99-102.[CrossRef][Medline]
    29. 29
  29. Saladin, M., V. T. B. Cao, T. Lambert, J.-L. Donay, J.-L. Herrmann, Z. Ould-Hocine, C. Verdit, F. Delisle, A. Philippon, and G. Arlet. 2002. Diversity of CTX-M ß-lactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals. FEMS Microbiol. Lett. 209:161-168.[Medline]
    30. 30
  30. Tenover, F. C., R. D. Arbeit, R. V. Goering, P. A. Mickelsen, B. E. Murray, D. H. Persing, and B. Swaminathan. 1995. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33:2233-2239.[Medline]
    31. 31
  31. Tran, J. H., and G. A. Jacoby. 2002. Mechanism of plasmid-mediated quinolone resistance. Proc. Natl. Acad. Sci. USA 99:5638-5642.[Abstract/Free Full Text]
    32. 32
  32. Tzelepi, E., P. Giakkoupi, D. Sofianou, V. Loukova, A. Kemeroglou, and A. Tsakris. 2000. Detection of extended-spectrum ß-lactamases in clinical isolates of Enterobacter cloacae and Enterobacter aerogenes. J. Clin. Microbiol. 38:542-546.[Abstract/Free Full Text]
    33. 33
  33. Wang, M., J. H. Tran, G. A. Jacoby, Y. Zhang, F. Wang, and D. C. Hooper. 2003. Plasmid-mediated quinolone resistance in clinical isolates of Escherichia coli from Shanghai, China. Antimicrob. Agents Chemother. 47:2242-2248.[Abstract/Free Full Text]
    34. 34
  34. Wang, M., D. F. Sahm, J. A. Jacoby, and D. C. Hooper. 2004. Emerging plasmid-mediated quinolone resistance associated with the qnr gene in Klebsiella pneumoniae clinical isolates in the United States. Antimicrob. Agents Chemother. 48:1295-1299.[Abstract/Free Full Text]
    35. 35
  35. Yan, J.-J., J.-J. Wu, S.-H. Tsai, and C.-L. Chuang. 2004. Comparison of the double-disk, combined disk, and Etest methods for detecting metallo-ß-lactamases in gram-negative bacilli. Diagn. Microbiol. Infect. Dis. 49:5-11.[CrossRef][Medline]
    36. 36
  36. Yan, J.-J., W.-C. Ko, S.-H. Tsai, H.-M. Wu, and J.-J. Wu. 2001. Outbreak of infection with multidrug-resistant Klebsiella pneumoniae carrying blaIMP-8 in a university medical center in Taiwan. J. Clin. Microbiol. 39:4433-4439.[Abstract/Free Full Text]
    37. 37
  37. Yan, J.-J., P.-R. Hsueh, J.-J. Lu, F.-Y. Chang, W.-C. Ko, and J.-J. Wu. 2006. Characterization of acquired ß-lactamases and their genetic support in multidrug-resistant Pseudomonas aeruginosa isolates in Taiwan: the prevalence of unusual integrons. J. Antimicrob. Chemother. 58:530-536.[Abstract/Free Full Text]

Antimicrobial Agents and Chemotherapy, April 2007, p. 1223-1227, Vol. 51, No. 4
0066-4804/07/$08.00+0     doi:10.1128/AAC.01195-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Strahilevitz, J., Jacoby, G. A., Hooper, D. C., Robicsek, A. (2009). Plasmid-Mediated Quinolone Resistance: a Multifaceted Threat. Clin. Microbiol. Rev. 22: 664-689 [Abstract] [Full Text]  
  • Chen, Y.-T., Liao, T.-L., Liu, Y.-M., Lauderdale, T.-L., Yan, J.-J., Tsai, S.-F. (2009). Mobilization of qnrB2 and ISCR1 in Plasmids. Antimicrob. Agents Chemother. 53: 1235-1237 [Abstract] [Full Text]  
  • Ma, J., Zeng, Z., Chen, Z., Xu, X., Wang, X., Deng, Y., Lu, D., Huang, L., Zhang, Y., Liu, J., Wang, M. (2009). High Prevalence of Plasmid-Mediated Quinolone Resistance Determinants qnr, aac(6')-Ib-cr, and qepA among Ceftiofur-Resistant Enterobacteriaceae Isolates from Companion and Food-Producing Animals. Antimicrob. Agents Chemother. 53: 519-524 [Abstract] [Full Text]  
  • Kim, H. B., Park, C. H., Kim, C. J., Kim, E.-C., Jacoby, G. A., Hooper, D. C. (2009). Prevalence of Plasmid-Mediated Quinolone Resistance Determinants over a 9-Year Period. Antimicrob. Agents Chemother. 53: 639-645 [Abstract] [Full Text]  
  • Shen, P., Jiang, Y., Zhou, Z., Zhang, J., Yu, Y., Li, L. (2008). Complete nucleotide sequence of pKP96, a 67 850 bp multiresistance plasmid encoding qnrA1, aac(6')-Ib-cr and blaCTX-M-24 from Klebsiella pneumoniae. J Antimicrob Chemother 62: 1252-1256 [Abstract] [Full Text]  
  • Wu, J.-J., Ko, W.-C., Chiou, C.-S., Chen, H.-M., Wang, L.-R., Yan, J.-J. (2008). Emergence of Qnr determinants in human Salmonella isolates in Taiwan. J Antimicrob Chemother 62: 1269-1272 [Abstract] [Full Text]  
  • Yang, H., Chen, H., Yang, Q., Chen, M., Wang, H. (2008). High Prevalence of Plasmid-Mediated Quinolone Resistance Genes qnr and aac(6')-Ib-cr in Clinical Isolates of Enterobacteriaceae from Nine Teaching Hospitals in China. Antimicrob. Agents Chemother. 52: 4268-4273 [Abstract] [Full Text]  
  • Tamang, M. D., Seol, S. Y., Oh, J.-Y., Kang, H. Y., Lee, J. C., Lee, Y. C., Cho, D. T., Kim, J. (2008). Plasmid-Mediated Quinolone Resistance Determinants qnrA, qnrB, and qnrS among Clinical Isolates of Enterobacteriaceae in a Korean Hospital. Antimicrob. Agents Chemother. 52: 4159-4162 [Abstract] [Full Text]  
  • Rice, L. B., Carias, L. L., Hutton, R. A., Rudin, S. D., Endimiani, A., Bonomo, R. A. (2008). The KQ Element, a Complex Genetic Region Conferring Transferable Resistance to Carbapenems, Aminoglycosides, and Fluoroquinolones in Klebsiella pneumoniae. Antimicrob. Agents Chemother. 52: 3427-3429 [Abstract] [Full Text]  
  • Liu, J.-H., Deng, Y.-T., Zeng, Z.-L., Gao, J.-H., Chen, L., Arakawa, Y., Chen, Z.-L. (2008). Coprevalence of Plasmid-Mediated Quinolone Resistance Determinants QepA, Qnr, and AAC(6')-Ib-cr among 16S rRNA Methylase RmtB-Producing Escherichia coli Isolates from Pigs. Antimicrob. Agents Chemother. 52: 2992-2993 [Full Text]  
  • Sanchez-Cespedes, J., Blasco, M. D., Marti, S., Alba, V., Alcalde, E., Esteve, C., Vila, J. (2008). Plasmid-Mediated QnrS2 Determinant from a Clinical Aeromonas veronii Isolate. Antimicrob. Agents Chemother. 52: 2990-2991 [Full Text]  
  • Chmelnitsky, I., Navon-Venezia, S., Strahilevitz, J., Carmeli, Y. (2008). Plasmid-Mediated qnrB2 and Carbapenemase Gene blaKPC-2 Carried on the Same Plasmid in Carbapenem-Resistant Ciprofloxacin-Susceptible Enterobacter cloacae Isolates. Antimicrob. Agents Chemother. 52: 2962-2965 [Abstract] [Full Text]  
  • Iabadene, H., Messai, Y., Ammari, H., Ramdani-Bouguessa, N., Lounes, S., Bakour, R., Arlet, G. (2008). Dissemination of ESBL and Qnr determinants in Enterobacter cloacae in Algeria. J Antimicrob Chemother 62: 133-136 [Abstract] [Full Text]  
  • Wu, J.-J., Ko, W.-C., Wu, H.-M., Yan, J.-J. (2008). Prevalence of Qnr determinants among bloodstream isolates of Escherichia coli and Klebsiella pneumoniae in a Taiwanese Hospital, 1999-2005. J Antimicrob Chemother 61: 1234-1239 [Abstract] [Full Text]  
  • Jiang, Y., Zhou, Z., Qian, Y., Wei, Z., Yu, Y., Hu, S., Li, L. (2008). Plasmid-mediated quinolone resistance determinants qnr and aac(6')-Ib-cr in extended-spectrum {beta}-lactamase-producing Escherichia coli and Klebsiella pneumoniae in China. J Antimicrob Chemother 61: 1003-1006 [Abstract] [Full Text]  
  • Yamane, K., Wachino, J.-i., Suzuki, S., Arakawa, Y. (2008). Plasmid-Mediated qepA Gene among Escherichia coli Clinical Isolates from Japan. Antimicrob. Agents Chemother. 52: 1564-1566 [Abstract] [Full Text]  
  • Aschbacher, R., Doumith, M., Livermore, D. M., Larcher, C., Woodford, N. (2008). Linkage of acquired quinolone resistance (qnrS1) and metallo-{beta}-lactamase (blaVIM-1) genes in multiple species of Enterobacteriaceae from Bolzano, Italy. J Antimicrob Chemother 61: 515-523 [Abstract] [Full Text]  
  • Mendes, R. E., Bell, J. M., Turnidge, J. D., Yang, Q., Yu, Y., Sun, Z., Jones, R. N. (2008). Carbapenem-Resistant Isolates of Klebsiella pneumoniae in China and Detection of a Conjugative Plasmid (blaKPC-2 plus qnrB4) and a blaIMP-4 Gene. Antimicrob. Agents Chemother. 52: 798-799 [Full Text]  
  • Xu, X., Wu, S., Ye, X., Liu, Y., Shi, W., Zhang, Y., Wang, M. (2007). Prevalence and Expression of the Plasmid-Mediated Quinolone Resistance Determinant qnrA1. Antimicrob. Agents Chemother. 51: 4105-4110 [Abstract] [Full Text]  
  • Ahmed, A. M., Motoi, Y., Sato, M., Maruyama, A., Watanabe, H., Fukumoto, Y., Shimamoto, T. (2007). Zoo Animals as Reservoirs of Gram-Negative Bacteria Harboring Integrons and Antimicrobial Resistance Genes. Appl. Environ. Microbiol. 73: 6686-6690 [Abstract] [Full Text]  

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Wu, J.-J.
Right arrow Articles by Yan, J.-J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Wu, J.-J.
Right arrow Articles by Yan, J.-J.

Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»