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 Lavigne, J.-P.
Right arrow Articles by Sotto, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lavigne, J.-P.
Right arrow Articles by Sotto, A.

 Previous Article  |  Next Article 

Antimicrobial Agents and Chemotherapy, December 2006, p. 4224-4228, Vol. 50, No. 12
0066-4804/06/$08.00+0     doi:10.1128/AAC.00904-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

qnrA in CTX-M-Producing Escherichia coli Isolates from France{triangledown}

Jean-Philippe Lavigne,1,2 Hélène Marchandin,1,3 Julien Delmas,4,5 Nicole Bouziges,1,2 Evelyne Lecaillon,6 Laurent Cavalie,3 Hélène Jean-Pierre,1,3 Richard Bonnet,4,5 and Albert Sotto1*

Laboratoire Universitaire d'Antibiologie, UFR de Médecine, Avenue Kennedy, 30908 Nîmes Cedex 2, France,1 Laboratoire de Bactériologie, Virologie, Parasitologie, CHU de Nîmes, Groupe Hospitalo-Universitaire de Carémeau, Place du Professeur Robert Debré, 30029 Nîmes Cedex 9, France,2 Laboratoire de Bactériologie, CHU Arnaud de Villeneuve, 371, avenue du Doyen Gaston Giraud, 34295 Montpellier Cedex 5, France,3 Laboratoire de Bactériologie, CHU Clermont-Ferrand, 63003 Clermont-Ferrand, France,4 Laboratoire de Bactériologie, Université de Clermont 1, Faculté de médecine, 63001 Clermont-Ferrand, France,5 Service de Biologie Polyvalente, CHG Saint-Jean-Perpignan, 20 Avenue du Languedoc, 66046 Perpignan, France6

Received 22 July 2006/ Returned for modification 23 August 2006/ Accepted 5 September 2006


arrow
ABSTRACT
 
By PCR, we screened for qnr genes 112 clinical isolates of extended-spectrum ß-lactamase-producing Escherichia coli collected from hospitals in France during 2004. For the first time, 7.7% of CTX-M-producing E. coli isolates presented a plasmid-mediated resistance to quinolones. All strains harbored a qnrA gene located on a sul1-type class 1 integron with similar structure to the In36 integron.


arrow
TEXT
 
Recently, several studies revealed that CTX-M-type enzymes are becoming the most prevalent extended-spectrum ß-lactamases (ESBL) in Escherichia coli isolates in different geographic areas (5, 29, 32, 35, 36, 38). Localized outbreaks of CTX-M-producing E. coli infection have been reported in the north of France (12, 21, 22). However, the link between the increase in ESBL-producing E coli prevalence and the emergence of CTX-M enzyme is not yet established. Moreover ESBL-producing strains generally displayed a high level of resistance to several other non-ß-lactam antibiotic families, in particular, to quinolones. A plasmid-mediated quinolone resistance based on the Qnr production has been successively identified in the United States, in China, and recently in France. Interestingly, the qnr-containing plasmid was frequently associated with plasmid-mediated ESBLs (7, 16, 26, 31), but no search was focused on Qnr determinant detection in CTX-M-producing E. coli strains.

(This work was presented in part in 25th Réunion Interdiciplinaire de Chimiothérapie Anti-Infectieuse [RICAI], Paris, France, December 2005 [abstr. 222/520].)

To investigate the relationship between CTX-M-producing E. coli and qnr genes, we undertook a prospective study of ESBL-producing E. coli isolates from 1 January 2004 until 31 December 2004 in three university hospitals (Clermont-Ferrand, Montpellier, and Nîmes) and one community hospital (Perpignan) in the south and center of France. Only one ESBL-producing isolate per sampling type and patient was included in the study. Patients were deemed to have community disease if the first culture found positive for ESBL-producing E. coli was obtained within 48 h of admission. The genus and species were determined biochemically either with the Vitek 2-ID-GNB identification card or the API 20E system (bioMérieux, Marcy-l'Etoile, France). Susceptibility to antimicrobial agents was tested by using the agar disk diffusion assay on Mueller-Hinton agar. Strains were classified as susceptible, intermediate resistant, or resistant to the antibiotics tested according to the recommendations of the Antibiotic Susceptibility Testing Committee of the French Society for Microbiology (40). ESBL production was confirmed by the double-disk synergy test using not only ceftazidime and cefotaxime but also cefpodoxime disks (39). Isoelectric focusing was performed with polyacrylamide gels as previously described (10). The genes blaTEM, blaSHV, and blaCTX-M were detected by PCR using specific primers as previously reported (3, 10, 11, 24) and further identified by sequencing the PCR products. A macrorestriction analysis of chromosomal DNA was performed using pulsed-field gel electrophoresis (PFGE) according to a previous published procedure after XbaI restriction (New England Biolabs, Inc.) by using the contour-clamped homogeneous electric field system (Bio-Rad SA, Ivry-sur-Seine, France) (20). The PFGE patterns were analyzed with Gel compar computer software (Applied Math, Kortrijk, Belgium) and an unweighted-pair group method with the Dice coefficient of similarity. Isolates were considered to be within a cluster if the coefficient of similarity was >80% (42). Phylogenetic grouping of the E. coli isolates was determined by a PCR-based method developed by Clermont et al. (8). The fingerprinting analysis of ESBL-carrying plasmid DNA was performed with the clinical isolates and their electroporants, after digestion with HindIII endonuclease (New England Biolabs, Inc.) and electrophoresis on 0.8% (wt/vol) agarose gels at 100 V for 2 h. The qnrA, qnrB, and qnrS genes were screened by PCR as previously described (15, 16, 34, 43, 44) in all quinolone-resistant strains and electroporants. For PCR mapping of the integrons that contained the blaCTX-M and the qnr genes, PCR primers were used in combination and studied by sequencing the PCR products (26). A search for additional chromosome-encoded quinolone resistance determinants (gyrA, gyrB, parC, and parE genes) was performed by PCR (26). PCR products were sequenced to detect mutations.

During the period studied, 112 ESBL-producing E. coli strains were isolated from 111 patients. The prevalence of the ESBL production in the E. coli isolates was <3% in the four centers. The distribution of the different types of ESBL according to the geographical origin of the corresponding strains is shown in Fig. 1. E. coli produced mainly CTX-M-ESBLs (58.0%), followed by TEM-type (34.8%) and SHV-type (7.2%) ß-lactamases. CTX-M-15 was the most prevalent ESBL in our study (57.0% of CTX-M ß-lactamases). We observed that 33.8% of the CTX-M-producing strains were isolated in outpatients compared to strains producing other ESBLs (6.4%), as previously noted by other authors (1, 30, 32, 35, 37, 45). PFGE revealed three independent clonal propagations of CTX-M-15-producing isolates in hospitals in Montpellier (19 isolates), Nîmes (4 isolates), and Perpignan (2 isolates) (Fig. 2). Twelve of these strains were shown to be of community origin, and seven patients infected by these strains had never been hospitalized. The clonal strains belonged to the B2 phylotyping group. No epidemiological link between patients could be demonstrated. The study on the CTX-M-15-producing plasmids revealed that all isolates had one or more plasmids. Electroporation of plasmid DNA from the clinical strains into E. coli DH5{alpha} successfully transferred the ESBL phenotype. Analysis of the resulting electroporants revealed the presence of large plasmids (>80 kb) (data not shown) and the same ESBL resistance pattern. Plasmids corresponding to the clonal CTX-M-15-producing E. coli strains yielded similar restriction patterns after digestion with HindIII, whereas those corresponding to the unrelated CTX-M-15-producing E. coli strains harbored different restriction patterns (data not shown).


Figure 1
View larger version (34K):
[in this window]
[in a new window]
  		FIG. 1. Distribution of ESBL-producing Escherichia coli strains found in four hospitals in France.


Figure 2
View larger version (23K):
[in this window]
[in a new window]
  		FIG. 2. Dendrogram of XbaI-digested genomic DNAs from all of the CTX-M-15-producing E. coli strains isolated in four hospitals in France. MTP, Montpellier; CF, Clermont-Ferrand; NEC, Nîmes; and PEC, Perpignan. Strains were clustered by the unweighted-pair group method using arithmetic averages (UPGMA). The scale indicates the percentage of genetic similarity. Max. tol., percent maximum tolerance of the curve that matches the bands; Min. surf., percent minimum surface area of a band. The four strains harboring the qnrA gene are noted with asterisks.

In the selected ESBL-producing E. coli strains, 64.3% of the isolates were resistant to nalidixic acid and 56.3% were resistant to ciprofloxacin. The comparison of susceptibility profiles observed for CTX-M- and other ESBL-producing strains indicates that CTX-M-producing strains had more associated resistances than the other ESBL-producing strains. A total of 73.8% of CTX-M-producing E. coli strains were resistant to quinolones versus 51.1% of TEM- and SHV-producing E. coli strains (P < 0.01). Similarly, 66.2% of CTX-M-producing isolates were resistant to ciprofloxacin versus 42.6% for TEM- and SHV-producing isolates (P < 0.01). With the aim of investigating an association between CTX-M production and resistance to quinolones, we screened for qnr genes and transfer of quinolone resistance. We detected the qnrA gene in 7.7% of CTX-M-producing E. coli strains, including four epidemiologically unrelated isolates (MECJ, MECT, MECA6, and NEC39) producing CTX-M-15 and strain NEC34 producing CTX-M-1. No TEM- or SHV-producing strains had qnr genes. In these five qnr-positive strains, MICs of nalidixic acid and ciprofloxacin varied between 64 to 256 µg/ml and 4 to 16 µg/ml, respectively. Except for strain NEC39, the resistance to nalidixic acid was cotransferred with the ESBL-type resistance phenotype for the qnrA-containing strains and the qnrA gene was detected by PCR in the transformants (Table 1). The clinical strains and electroporants harbored a similar qnrA gene to that originally identified in a Klebsiella pneumoniae isolate in United States (43) with a single functionally silent nucleotide change, CTA->CTG, at position 537. The qnrA gene was located on a sul1-type class 1 integron. The structures of the integrons were identical in the five strains and were homologous to the In36 integron (orf513 qnr ampR qacE{Delta}1 sul1) identified in E. coli isolates from Shanghai (44). The detection of an associated chromosomal quinolone resistance revealed the presence of GyrA in all five strains, with a mutation at codon 83 (Ser->Tyr) and a parC mutation in one strain (NEC39) at codon 80 (Ser->Ile).


View this table:
[in this window]
[in a new window]
  		TABLE 1. Characteristics of qnr-positive strainsa

The aim of this study was to establish the dissemination of and a link between ESBL-producing E. coli isolates and quinolone plasmid resistance. The selected strains represented an actual evolution of E. coli in most parts of the world: increasing prevalence of ESBL-producing E. coli, emergence and diffusion of CTX-M-producing strains (4, 6, 9, 14, 18, 27-29, 38, 41), diffusion of CTX-M-15 (2, 5, 13, 17, 19, 20, 22, 23, 27, 29), and community outbreak of clonally CTX-M isolates (32). The strains were particularly interesting because the majority of CTX-M-producing strains displayed a high level of resistance to quinolones. This high level of resistance associated with CTX-M production was previously described (14), but the actual causes of this association remain not well known. Recently, a plasmid-mediated quinolone resistance determinant named Qnr has been described as leading to a low level of resistance to quinolones (43). Different studies throughout the world showed that the Qnr determinant occurred in between 0.3 and 48% of the strains (15, 26, 33, 43, 44). We found a high rate of qnrA genes (7.7%) associated with CTX-M-type ESBL, in comparison to 0.3% found in a first French study (26). However, we found that four out five strains transferred the two resistances in electroporant strains, suggesting colocalization of qnrA and blaCTX-M genes on the same plasmid. The majority of qnr-positive strains were associated with multidrug resistance and ESBL- or cephalosporinase-producing strains (15, 43). Interestingly, we have described how in the five strains, the qnrA gene is embedded in a complex sul1-type class 1 integron known to integrate numerous multidrug resistance genes as previously suggested (44). The integrons are frequent in strains of Enterobacteriaceae and in strains with multidrug resistance (25). This genetic support induces the transfer between bacteria of the same plasmid or integron and then the transmission and dissemination of these strains. The origin of the plasmid supporting the Qnr region has been detected in a waterborne species, Shewanella algae (31). Our study suggests that the plasmid-mediated Qnr-based mechanism of quinolone resistance could be emerging in France in CTX-M-producing strains. To date, no genetic link has been found between the two emerging mechanisms of resistance. However, recently qnrB has been detected on plasmids also encoding CTX-M-15 in Klebsiella pneumoniae isolates in India (16). Interestingly, an associated chromosomal quinolone resistance was detected in all our strains. This observation explains the higher level of resistance to quinolones in our isolates compared with those observed for qnr-positive transconjugants (Table 1).

In conclusion, CTX-M ß-lactamases were associated with quinolone/fluoroquinolone resistance, and in some cases, this association was linked to the Qnr determinant. The frequency of CTX-M strains in weakened patients and their community character invite examination of the epidemiological evolution of these strains and the necessity to inform the medical profession of these results.


arrow
ACKNOWLEDGMENTS
 
We are very grateful to A. Gouby for help with this work and Josiane Campos for technical assistance.

This work was supported by Université de Montpellier 1 (BQR, BQ 68, and 88), La Ville de Nîmes, Le CHU de Nîmes, and La Région Languedoc Roussillon.


arrow
FOOTNOTES
 
* Corresponding author. Mailing address: Laboratoire Universitaire d'Antibiologie, Faculté de Médecine, CS83021, Avenue Kennedy, 30908 Nîmes Cedex 02, France. Phone: (33) 4 66 68 32 31. Fax: (33) 4 66 68 38 24. E-mail: albert.sotto{at}chu-nimes.fr. Back

{triangledown} Published ahead of print on 18 September 2006. Back


arrow
REFERENCES
 
    1
  1. Arpin, C., V. Dubois, L. Coulange, C. André, I. Fischer, P. Noury, F. Grobost, J.-P. Brochet, J. Jullin, B. Dutilh, G. Larribet, I. Lagrange, and C. Quentin. 2003. Extended-spectrum ß-lactamase-producing Enterobacteriaceae in community and private health care centers. Antimicrob. Agents Chemother. 47:3506-3514.[Abstract/Free Full Text]
    2. 2
  2. Baraniak, A., J. Fiett, A. Sulikowska, W. Hryniewicz, and M. Gniadkowski. 2002. Countrywide spread of CTX-M-3 extended-spectrum ß-lactamase-producing microorganisms of the family Enterobacteriaceae in Poland. Antimicrob. Agents Chemother. 46:151-159.[Abstract/Free Full Text]
    3. 3
  3. Bonnet, R., C. Dutour, J. L. M. Sampaio, C. Chanal, D. Sirot, R. Labia, C. De Champs, and J. Sirot. 2001. Novel cefotaximase (CTX-M-16) with increased catalytic efficiency due to substitution Asp-240->Gly. Antimicrob. Agents Chemother. 45:2269-2275.[Abstract/Free Full Text]
    4. 4
  4. Bonnet, R. 2004. Growing group of extended-spectrum ß-lactamases: the CTX-M enzymes. Antimicrob. Agents Chemother. 48:1-14.[Free Full Text]
    5. 5
  5. Brigante, G., F. Luzzaro, M. Perilli, G. Lombardi, A. Coli, G. M. Rossolini, G. Amicosante, and A. Toniolo. 2005. Evolution of CTX-M-type beta-lactamases in isolates of Escherichia coli infecting hospital and community patients. Int. J. Antimicrob. Agents 25:157-162.[CrossRef][Medline]
    6. 6
  6. Chanawong, A., F. H. M'Zali, J. Heritage, J.-H. Xiong, and P. M. Hawkey. 2002. Three cefotaximases, CTX-M-9, CTX-M-13, and CTX-M-14, among Enterobacteriaceae in the People's Republic of China. Antimicrob. Agents Chemother. 46:630-637.[Abstract/Free Full Text]
    7. 7
  7. 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]
    8. 8
  8. Clermont, O., S. Bonacorsi, and E. Bingen. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66:4555-4558.[Abstract/Free Full Text]
    9. 9
  9. De Champs, C., D. Sirot, C. Chanal, R. Bonnet, J. Sirot, and the French Study Group. 2000. A 1998 survey of extended-spectrum ß-lactamases in Enterobacteriaceae in France. Antimicrob. Agents Chemother. 44:3177-3179.[Abstract/Free Full Text]
    10. 10
  10. De Champs, C., C. Chanal, D. Sirot, R. Baraduc, J. P. Romaszko, R. Bonnet, A. Plaidy, M. Boyer, E. Carroy, M. C. Gbadamassi, S. Laluque, O. Oules, M. C. Poupart, M. Villemain, and J. Sirot. 2004. Frequency and diversity of class A extended-spectrum beta-lactamases in hospitals of the Auvergne, France: a 2 year prospective study. J. Antimicrob. Chemother. 54:634-639.[Abstract/Free Full Text]
    11. 11
  11. Dutour, C., R. Bonnet, H. Marchandin, M. Boyer, C. Chanal, D. Sirot, and J. Sirot. 2002. CTX-M-1, CTX-M-3, and CTX-M-14 ß-lactamases from Enterobacteriaceae isolated in France. Antimicrob. Agents Chemother. 46:534-537.[Abstract/Free Full Text]
    12. 12
  12. Eckert, C., V. Gautier, M. Saladin-Allard, N. Hidri, C. Verdet, Z. Ould-Hocine, G. Barnaud, F. Delisle, A. Rossier, T. Lambert, A. Philippon, and G. Arlet. 2004. Dissemination of CTX-M-type ß-lactamases among clinical isolates of Enterobacteriaceae in Paris, France. Antimicrob. Agents Chemother. 48:1249-1255.[Abstract/Free Full Text]
    13. 13
  13. Edelstein, M., M. Pimkin, I. Palagin, I. Edelstein, and L. Stratchounski. 2003. Prevalence and molecular epidemiology of CTX-M extended-spectrum ß-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob. Agents Chemother. 47:3724-3732.[Abstract/Free Full Text]
    14. 14
  14. Hernandez, J. R., L. Martinez-Martinez, R. Canton, T. M. Coque, A. Pascual, and the Spanish Group for Nosocomial Infections (GEIH). 2005. Nationwide study of Escherichia coli and Klebsiella pneumoniae producing extended-spectrum ß-lactamases in Spain. Antimicrob. Agents Chemother. 49:2122-2125.[Abstract/Free Full Text]
    15. 15
  15. 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]
    16. 16
  16. 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]
    17. 17
  17. Karim, A., L. Poirel, S. Nagarajan, and P. Nordmann. 2001. Plasmid-mediated extended-spectrum beta-lactamase (CTX-M-3 like) from India and gene association with insertion sequence ISEcp1. FEMS Microbiol. Lett. 201:237-241.[Medline]
    18. 18
  18. Kim, J., Y.-M. Lim, Y.-S. Jeong, and S.-Y. Seol. 2005. Occurrence of CTX-M-3, CTX-M-15, CTX-M-14, and CTX-M-9 extended-spectrum ß-lactamases in Enterobacteriaceae clinical isolates in Korea. Antimicrob. Agents Chemother. 49:1572-1575.[Abstract/Free Full Text]
    19. 19
  19. Lartigue, M. F., L. Poirel, C. Heritier, V. Tolun, and P. Nordmann. 2003. First description of CTX-M-15-producing Klebsiella pneumoniae in Turkey. J. Antimicrob. Chemother. 52:315-316.[Free Full Text]
    20. 20
  20. Lavigne, J.-P., N. Bouziges, C. Chanal, A. Mahamat, S. Michaux-Charachon, and A. Sotto. 2004. Molecular epidemiology of Enterobacteriaceae isolates producing extended-spectrum ß-lactamases in a French hospital. J. Clin. Microbiol.42:3805-3808.[Abstract/Free Full Text]
    21. 21
  21. Lavollay, M., K. Mamlouk, T. Frank, A. Akpabie, B. Burghoffer, S. Ben Redjeb, R. Bercion, V. Gautier, and G. Arlet. 2006. Clonal dissemination of a CTX-M-15 ß-lactamase-producing Escherichia coli strain in the Paris area, Tunis, and Bangui. Antimicrob. Agents Chemother. 50:2433-2438.[Abstract/Free Full Text]
    22. 22
  22. Leflon-Guibout, V., C. Jurand, S. Bonacorsi, F. Espinasse, M. C. Guelfi, F. Duportail, B. Heym, E. Bingen, and M.-H. Nicolas-Chanoine. 2004. Emergence and spread of three clonally related virulent isolates of CTX-M-15-producing Escherichia coli with variable resistance to aminoglycosides and tetracycline in a French geriatric hospital. Antimicrob. Agents Chemother. 48:3736-3742.[Abstract/Free Full Text]
    23. 23
  23. Livermore, D. M., and P. M. Hawkey. 2005. CTX-M: changing the face of ESBLs in the UK. J. Antimicrob. Chemother. 56:451-454.[Abstract/Free Full Text]
    24. 24
  24. Mabilat, C., S. Goussard, W. Sougakoff, R. C. Spencer, and P. Courvalin. 1990. Direct sequencing of the amplified structural gene and promoter for the extended-broad-spectrum beta-lactamase TEM-9 (RHH-1) of Klebsiella pneumoniae. Plasmid 23:27-34.[CrossRef][Medline]
    25. 25
  25. Machado, E., R. Cantón, F. Baquero, J.-C. Galan, A. Rollán, L. Peixe, and T. M. Coque. 2005. Integron content of extended-spectrum-ß-lactamase-producing Escherichia coli strains over 12 years in a single hospital in Madrid, Spain. Antimicrob. Agents Chemother. 49:1823-1829.[Abstract/Free Full Text]
    26. 26
  26. 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]
    27. 27
  27. Markovska, R., I. Schneider, E. Keuleyan, and A. Bauernfeind. 2004. Extended-spectrum beta-lactamase (ESBL) CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae in Sofia, Bulgaria. Clin. Microbiol. Infect. 10:752-755.[CrossRef][Medline]
    28. 28
  28. Moland, E. S., J. A. Black, A. Hossain, N. D. Hanson, K. S. Thomson, and S. Pottumarthy. 2003. Discovery of CTX-M-like extended-spectrum ß-lactamases in Escherichia coli isolates from five U.S. states. Antimicrob. Agents Chemother. 47:2382-2383. (Letter.)[Free Full Text]
    29. 29
  29. Moubareck, C., Z. Daoud, N. I. Hakimé, M. Hamzé, N. Mangeney, H. Matta, J. E. Mokhbat, R. Rohban, D. K. Sarkis, and F. Doucet-Populaire. 2005. Countrywide spread of community- and hospital-acquired extended-spectrum ß-lactamase (CTX-M-15)-producing Enterobacteriaceae in Lebanon. J. Clin. Microbiol. 43:3309-3313.[Abstract/Free Full Text]
    30. 30
  30. Munday, C. J., J. Xiong, C. Li, D. Shen, and P. M. Hawkey. 2004. Dissemination of CTX-M type beta-lactamases in Enterobacteriaceae isolates in the People's Republic of China. Int. J. Antimicrob. Agents 23:175-180.[CrossRef][Medline]
    31. 31
  31. 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]
    32. 32
  32. Pitout, J. D. D., D. B. Gregson, D. L. Church, S. Elsayed, and K. B. Laupland. 2005. Community-wide outbreaks of clonally related CTX-M-14 ß-lactamase-producing Escherichia coli strains in the Calgary health region. J. Clin. Microbiol. 43:2844-2849.[Abstract/Free Full Text]
    33. 33
  33. Poirel, L., J.-M. Rodriguez-Martinez, H. Mammeri, A. Liard, and P. Nordmann. 2005. Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob. Agents Chemother. 49:3523-3525.[Abstract/Free Full Text]
    34. 34
  34. Poirel, L., A. Liard, J. M. Rodriguez-Martinez, and P. Nordmann. 2005. Vibrionaceae as a possible source of Qnr-like quinolone resistance determinants. J. Antimicrob. Chemother. 56:1118-1121.[Abstract/Free Full Text]
    35. 35
  35. Pournaras, S., A. Ikonomidis, D. Sofianou, A. Tsakris, and A. N. Maniatis. 2004. CTX-M-type beta-lactamases affect community Escherichia coli treatment, Greece. Emerg. Infect. Dis. 10:1163-1164.[Medline]
    36. 36
  36. Quinteros, M., M. Radice, N. Gardella, M. M. Rodriguez, N. Costa, D. Korbenfeld, E. Couto, G. Gutkind, and the Microbiology Study Group. 2003. Extended-spectrum ß-lactamases in Enterobacteriaceae in Buenos Aires, Argentina, public hospitals. Antimicrob. Agents Chemother. 47:2864-2867.[Abstract/Free Full Text]
    37. 37
  37. Rodriguez-Baño, J., M. D. Navarro, L. Romero, L. Martinez-Martinez, M. A. Muniain, E. J. Perea, R. Pérez-Cano, and A. Pascual. 2004. Epidemiology and clinical features of infections caused by extended-spectrum beta-lactamase-producing Escherichia coli in nonhospitalized patients. J. Clin. Microbiol. 42:1089-1094.[Abstract/Free Full Text]
    38. 38
  38. Romero, L., L. Lopez, J. Rodriguez-Bano, J. Ramon Hernandez, L. Martinez-Martinez, and A. Pascual. 2005. Long-term study of the frequency of Escherichia coli and Klebsiella pneumoniae isolates producing extended-spectrum beta-lactamases. Clin. Microbiol. Infect. 11:625-631.[CrossRef][Medline]
    39. 39
  39. Sirot, J. 1996. Detection of extended-spectrum plasmid-mediated beta-lactamases by disk diffusion. Clin. Microbiol. Infect. 2:S35-S39.
    40. 40
  40. Soussy, C. J., G. Carret, J. D. Cavallo, et al. January 2005. Antibiotic Susceptibility Testing Committee of the French Society for Microbiology. Report. [Online.] http://www.sfm.asso.fr.
    41. 41
  41. Spanu, T., F. Luzzaro, M. Perilli, G. Amicosante, A. Toniolo, G. Fadda, and the Italian ESBL Study Group. 2002. Occurrence of extended-spectrum ß-lactamases in members of the family Enterobacteriaceae in Italy: implications for resistance to ß-lactams and other antimicrobial drugs. Antimicrob. Agents Chemother. 46:196-202.[Abstract/Free Full Text]
    42. 42
  42. 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]
    43. 43
  43. Wang, M., D. F. Sahm, G. 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]
    44. 44
  44. 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]
    45. 45
  45. Woodford, N., M. E. Ward, M. E. Kaufmann, J. Turton, E. J. Fagan, D. James, A. P. Johnson, R. Pike, M. Warner, T. Cheasty, A. Pearson, S. Harry, J. B. Leach, A. Loughrey, J. A. Lowes, R. E. Warren, and D. M. Livermore. 2004. Community and hospital spread of Escherichia coli producing CTX-M extended-spectrum beta-lactamases in the UK. J. Antimicrob. Chemother. 54:735-743.[Abstract/Free Full Text]

Antimicrobial Agents and Chemotherapy, December 2006, p. 4224-4228, Vol. 50, No. 12
0066-4804/06/$08.00+0     doi:10.1128/AAC.00904-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • 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]  
  • Yumuk, Z., Afacan, G., Nicolas-Chanoine, M.-H., Sotto, A., Lavigne, J.-P. (2008). Turkey: a further country concerned by community-acquired Escherichia coli clone O25-ST131 producing CTX-M-15. J Antimicrob Chemother 62: 284-288 [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]  
  • Fang, H., Ataker, F., Hedin, G., Dornbusch, K. (2008). Molecular Epidemiology of Extended-Spectrum {beta}-Lactamases among Escherichia coli Isolates Collected in a Swedish Hospital and Its Associated Health Care Facilities from 2001 to 2006. J. Clin. Microbiol. 46: 707-712 [Abstract] [Full Text]  
  • Brasme, L., Nordmann, P., Fidel, F., Lartigue, M. F., Bajolet, O., Poirel, L., Forte, D., Vernet-Garnier, V., Madoux, J., Reveil, J. C., Alba-Sauviat, C., Baudinat, I., Bineau, P., Bouquigny-Saison, C., Eloy, C., Lafaurie, C., Simeon, D., Verquin, J. P., Noel, F., Strady, C., De Champs, C. (2007). Incidence of class A extended-spectrum {beta}-lactamases in Champagne-Ardenne (France): a 1 year prospective study. J Antimicrob Chemother 60: 956-964 [Abstract] [Full Text]  
  • Lartigue, M.-F., Zinsius, C., Wenger, A., Bille, J., Poirel, L., Nordmann, P. (2007). Extended-Spectrum {beta}-Lactamases of the CTX-M Type Now in Switzerland. Antimicrob. Agents Chemother. 51: 2855-2860 [Abstract] [Full Text]  
  • Cavaco, L. M., Hansen, D. S., Friis-Moller, A., Aarestrup, F. M., Hasman, H., Frimodt-Moller, N. (2007). First detection of plasmid-mediated quinolone resistance (qnrA and qnrS) in Escherichia coli strains isolated from humans in Scandinavia. J Antimicrob Chemother 59: 804-805 [Full Text]  
  • Lavigne, J.-P., Marchandin, H., Delmas, J., Moreau, J., Bouziges, N., Lecaillon, E., Cavalie, L., Jean-Pierre, H., Bonnet, R., Sotto, A. (2007). CTX-M {beta}-Lactamase-Producing Escherichia coli in French Hospitals: Prevalence, Molecular Epidemiology, and Risk Factors. J. Clin. Microbiol. 45: 620-626 [Abstract] [Full Text]  
  • Livermore, D. M., Canton, R., Gniadkowski, M., Nordmann, P., Rossolini, G. M., Arlet, G., Ayala, J., Coque, T. M., Kern-Zdanowicz, I., Luzzaro, F., Poirel, L., Woodford, N. (2007). CTX-M: changing the face of ESBLs in Europe. J Antimicrob Chemother 59: 165-174 [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 Lavigne, J.-P.
Right arrow Articles by Sotto, A.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Lavigne, J.-P.
Right arrow Articles by Sotto, A.

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