JAC Advance Access published online on November 11, 2008
Journal of Antimicrobial Chemotherapy, doi:10.1093/jac/dkn463
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Original research |
Rapid change in the prevalence of extended-spectrum β-lactamase-producing Escherichia coli in Japan by clonal spread
1 Department of Bacterial Pathogenesis and Infection Control, National Institute of Infectious Diseases, 4-7-1 Musashi-murayama, Tokyo 208-0011, Japan 2 Infectious Disease Surveillance Centre, National Institute of Infectious Diseases, 4-7-1 Musashi-murayama, Tokyo 208-0011, Japan
* Corresponding author. Tel: +81-42-561-0771; Fax: +81-42-561-7173; E-mail: suzukiss{at}nih.go.jp
Received 23 July 2008; returned 5 September 2008; revised 14 October 2008; accepted 14 October 2008
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
|---|
Introduction: In the early 2000s, there was a rapid increase in extended-spectrum β-lactamase (ESBL)-producing Escherichia coli in hospital settings throughout Japan. The reasons for this rapid increase are unclear.
Methods: Between 2002 and 2003, 142 clinical isolates of E. coli suspected of producing ESBL were obtained from 37 hospitals and commercial clinical laboratories in geographically distinct regions throughout Japan. They were tested for ESBL types and further subtyped for serogroups, fimH single nucleotide polymorphism, pulsed-field gel electrophoresis patterns and multilocus sequence type (MLST). Representative isolates were also subjected to plasmid analysis.
Results: Of 142 E. coli isolates suspected of producing ESBL, 130 were confirmed as harbouring blaCTX-M by PCR analysis and sequencing. Of these, 84 (65%) harboured CTX-M-9-group blaCTX-M. Two serogroups O25 and O86 accounted for 41% of the 130 blaCTX-M-positive E. coli. All O86 serogroup strains belonged to ST38 by MLST and they formed 18% of all the blaCTX-M-positive E. coli. Serogroup O25 strains belonged to ST131 and ST73, and formed 21% and 1% of blaCTX-M-positive E. coli, respectively. Seven characterized plasmids carrying blaCTX-M genes belonged to three distinct incompatibility groups: IncF, IncN and IncI1.
Conclusions: In this study, clonally related strains of E. coli accounted for a large proportion of blaCTX-M-positive E. coli. This high proportion of clonal groups identified in different regions of Japan suggests their recent spread by mechanisms other than healthcare-associated transmission. These observations imply that restricting antimicrobial use in human clinical settings may have limited impact on the spread of ESBL-producing E. coli.
Key Words: E. coli , ESBLs , CTX-M
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
|---|
The incidence of hospital and community-acquired extraintestinal infections caused by multidrug-resistant Escherichia coli is increasing worldwide. The oxymino-cephalosporins, such as cefotaxime, ceftazidime and ceftriaxone, have potent activity against E. coli clinical isolates resistant to other β-lactam agents. However, even these antimicrobial agents have come to be challenged by the emergence of strains that produce extended-spectrum β-lactamases (ESBLs).1
ESBLs confer resistance by hydrolysing oxymino-cephalosporins but not cephamycins (e.g. cefoxitin, cefotetan) or carbapenems (e.g. imipenem, meropenem). Most ESBLs can be classified into three main groups: TEM, SHV and CTX-M.2,3 Worldwide, ESBL-producing organisms are most frequently found among the members of the family Enterobacteriaceae, especially E. coli and Klebsiella pneumoniae. There are now more than 60 different variants of CTX-M-type ESBLs, which can be further classified into five different subgroups based on their amino acid sequences: CTX-M-1, CTX-M-2, CTX-M-8, CTX-M-9 and CTX-M-25 groups. Of these, CTX-M-1, CTX-M-2 and CTX-M-9 groups are the most common.4,5
Community-acquired extraintestinal infections caused by E. coli and hospital-acquired K. pneumoniae strains harbouring plasmid-encoded blaCTX-M have been increasingly reported worldwide, from both developed and developing countries in the last decade.2,6 They have become the most prevalent type of ESBL-producing isolates belonging to the family Enterobacteriaceae during the past 5 years. In Japan, ESBL-producing E. coli were rarely isolated until the late 1990s, although strains producing FEC-1 and Toho-1, which were subsequently classified under the CTX-M-type ESBLs, were identified earlier.7,8 A report of nosocomial spread of Toho-1-like β-lactamase-producing E. coli and a preliminary survey in 1997–98 showed that E. coli strains producing CTX-M-2 were the predominant ESBL-producing E. coli strains in Japan.9 However, in the early 2000s, the dominant CTX-M group shifted from CTX-M-2 to CTX-M-9 among the E. coli isolates from clinical facilities.10 This change in the prevalence of the CTX-M group occurred nationwide in a relatively short period and cannot be solely explained by local and multiple person-to-person nosocomial transmissions. Thus, we characterized these E. coli isolates further to determine a possible explanation for this rapid emergence of CTX-M-9-group blaCTX-M-positive E. coli in hospital settings all over Japan.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
|---|
Surveillance data and bacterial strains
To estimate the prevalence of oxymino-cephalosporin resistance among the clinical isolates of E. coli in Japan, we reviewed data maintained by the Japan Nosocomial Infections Surveillance (JANIS), which includes participation of more than 200 hospitals across Japan.11 For microbiological characterization, a total of 142 clinical isolates of E. coli phenotypically positive for ESBL production were obtained between 2002 and 2003 from 37 hospitals and commercial clinical laboratories located in 15 Prefectures throughout Japan. ESBL production was screened by oxymino-cephalosporin resistance and double-disc diffusion synergy tests as recommended by the CLSI (formerly the NCCLS).12
To determine the genotype of ESBLs, we performed PCR using the TEM-, SHV-, CTX-M-1, CTX-M-2 and CTX-M-9 group-specific primers as reported previously.9,10 Sequencing was performed with PCR primers as follows: CTX-M-2sequenceF (5'-TTA ATG ATG ACT CAG AGC ATT C-3') and CTX-M-2sequenceR (5'-GAT ACC TCG CTC CAT TTA TTG-3'); CTX-M-9sequenceF (5'- GAT TGA CCG TAT TGG GAG TTT G-3') and CTX-M-9sequenceR (5'-ATT TAC TTC CAT TAC TTT GCG G-3'); CTX-M-14sequenceF (5'-GAT TGA CCG TAT TGG GAG TTT G-3') and CTX-M-14sequenceR (5'-TTG AAC TTT TGC TTT GCC ACG G-3'). PCR amplicons were purified with Wizard SV Gel and PCR Clean-up System (Promega, Madison, WI, USA) and were subsequently sequenced with the appropriate primers.
Serotyping was performed with the E. coli antisera ‘SEIKEN’ Set 1 (Denka Seiken, Tokyo, Japan) for O antigen and Set 2 (Denka Seiken) for H antigen according to the manufacturer's instructions.
Antimicrobial susceptibility testing
MICs were determined by the Etest (AB Biodisk, Solna, Sweden) method according to the manufacturer's instructions. Resistance was interpreted based on the recommended breakpoints of the CLSI (formerly the NCCLS).13
Genotypic analysis based on fimH single nucleotide polymorphism (SNP) was performed as reported previously, and multilocus sequence typing was performed according to the protocol described on the Max-Planck Institut für Infektionsbiologie web site.13,14 Pulsed-field gel electrophoresis (PFGE) analysis was performed as reported previously.15 A dendrogram was generated from the distance matrix by the unweighted pair-group method using arithmetic averages.
Broth mating method was used for conjugation experiments with E. coli DH10B as described previously.16 Transconjugants were selected on Luria–Bertani agar plates containing 16 mg/L cefotaxime and 800 mg/L streptomycin. Plasmid DNA was purified from transconjugant cells with the PureYield Plasmid Miniprep System (Promega), according to the manufacturer's instructions. Purified plasmid DNA was digested with PstI and EcoRI restriction enzymes (New England Biolabs, Beverly, MA, USA) for 2 h at 37°C. The digested plasmid DNA was electrophoresed in a 0.8% agarose gel for the restriction fragment length polymorphism (RFLP) analysis and hybridized with a digoxigenin-labelled DNA probe specific for CTX-M-2- or CTX-M-9-group blaCTX-M with the PCR DIG detection system (Roche Diagnostics, Indianapolis, IN, USA). The plasmids were also classified according to their incompatibility group by a PCR-based replicon-typing method.17
Comparisons of proportions were made by 
2 test with SPSS, version 14.0J for Windows (SPSS, Chicago, IL, USA).
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
|---|
A temporal change in prevalence of E. coli resistance to ceftazidime and cefotaxime
The JANIS, a sentinel hospital-based surveillance system established in Japan in 2000, shows that the prevalence of E. coli non-susceptible to cefotaxime increased from 2001 through 2006. In 2001, 3.8% and 0.7% of the E. coli isolates were non-susceptible to ceftazidime and cefotaxime, respectively. However, in 2004, the prevalence reversed, when ceftazidime-non-susceptible E. coli decreased to 1.1% and cefotaxime-non-susceptible isolates increased to 1.7%. Since then, the prevalence of E. coli non-susceptible to cefotaxime has continued to increase, reaching 4.6% in 2006. The prevalence of E. coli non-susceptible to ceftazidime remained virtually unchanged at 1.4% in the last 2 years of the surveillance.
PCR classification of CTX-M-type β-lactamases and serotyping
PCR analysis showed that 130 of the 142 E. coli isolates phenotypically positive for ESBL production harboured blaCTX-M. Among the 12 blaCTX-M-negative isolates, nine harboured blaSHV-12 and three were positive for blaTEM; in one of these, the sequence of the PCR amplicon was identical to the gene that encodes TEM-28. The sequence of the blaTEM PCR amplicon from the other two isolates was identical to that of the gene that encoded TEM-1, but the molecular mechanism for its resistance to oxymino-cephalosporin has not yet been determined.
Among the 130 blaCTX-M-positive E. coli isolates 84 (65%) strains harboured bla genes from the CTX-M-9 group, 25 (19%) from the CTX-M-1 group and 21 (16%) from the CTX-M-2 group. The most predominant serogroups O25 and O86 comprised 29 (22%) and 24 (18%) of the 130 blaCTX-M-positive isolates, respectively (Table 1). All of the O86 strains were H18, while three of the O25 isolates were non-motile and H untypeable. Others were H4. These two most prevalent E. coli serogroup isolates were, therefore, subjected to further genotypic analysis as outlined below.
|
Among the 130 blaCTX-M-positive E. coli isolates, all 24 E. coli O86 isolates harboured CTX-M-9-group blaCTX-M, while only 60 (57%) of the non-O86 isolates harboured the same gene (P < 0.001). CTX-M-9-group blaCTX-M was found in 22 (76%) of the 29 O25 E. coli isolates and in 62 (61%) of non-O25 isolates (P > 0.05).
Antimicrobial susceptibility profiles
Tests for susceptibility to 11 antimicrobial agents were conducted for 25 unduplicated E. coli O86 and O25 isolates harbouring blaCTX-M (Table 2). Duplication was defined as isolates belonging to the same O serogroup and CTX-M group from the same hospital. The drug susceptibility patterns between O25 and O86 isolates were distinct. All O86 isolates were resistant to sulfamethoxazole/trimethoprim, while O25 isolates were more frequently resistant to ceftazidime, cefoxitin, ciprofloxacin and chloramphenicol. There was no imipenem and fosfomycin resistance in any O86 or O25 strains.
|
Genotyping of E. coli O86 and O25 isolates
The fimH-sequence-based SNP analysis of all 53 E. coli O86 and O25 isolates revealed five distinct genotypes (designated A, B, C, D and E; Figure 1). All CTX-M-9-group blaCTX-M-positive E. coli O86 isolates (n = 24) belonged to a single fimH sequence type (cluster A). By multilocus sequence type (MLST), they were all found to belong to ST38. In contrast, 29 E. coli O25 isolates fell into four distinct fimH SNP types (cluster B, C, D and E). By MLST analysis, the fimH cluster C, D and E strains fell into ST131, while cluster B isolates belonged to ST73. By PFGE analysis of selected O86 and O25 isolates, the O86 isolates had similar electrophoretic banding patterns, but the O25 isolates showed more diverse patterns (Figure 2).
|
|
Sequence analysis of blaCTX-M
Half of 46 CTX-M-9-group blaCTX-M-positive E. coli O86 and O25 isolates harboured blaCTX-M-9 that was 100% identical in sequence; the rest had a variant blaCTX-M-9 sequence designated as blaCTX-M-14.18,19 All but one of the E. coli O86 isolates harboured the prototype blaCTX-M-9, and all O25 E. coli isolates positive for CTX-M-9-group ESBL harboured the variant blaCTX-M-14. The enzyme CTX-M-14 differs from CTX-M-9 by only one amino acid at position 234 (Ala
Val) and two silent mutations at nucleotide positions 372 (AG) and 570 (GA). However, the nucleotide sequence of a 20–30 bp downstream region of blaCTX-M differed completely between blaCTX-M-9 and blaCTX-M-14 genes (data not shown).
In isolates positive for the CTX-M-2-group ESBL gene, which were all E. coli O25, four and three isolates harboured blaCTX-M-35 and blaCTX-M-2, respectively (GenBank accession number AB176534
[GenBank]
).20 The enzyme encoded by blaCTX-M-35 differs from that encoded by blaCTX-M-2 also by only one amino acid substitution at position 170 (ProSer).
Eight isolates from five fimH sequence type clusters were subjected to conjugation experiments and seven transconjugants were obtained. Transconjugants were not obtained from isolates belonging to fimH sequence type B. Among seven plasmids purified from the transconjugants, four carrying CTX-M-9-group blaCTX-M belonged to the IncF group, two carrying CTX-M-2-group blaCTX-M belonged to the IncN group and one carrying blaCTX-M-14 belonged to the IncI1-group plasmids according to the PCR-based replicon typing. Restriction fragment length polymorphism analysis of the plasmid DNA showed different patterns and digoxigenin-labelled blaCTX-M probe also hybridized to bands of different molecular weight in all seven plasmids (data not shown).
Epidemiological information on the E. coli O86 and O25 isolates
Epidemiological and clinical information on the 53 E. coli O86 and O25 isolates harbouring blaCTX-M are summarized in Table 3. Twenty-four E. coli O86:H18 isolates, which belonged to a single fimH cluster A, ST38 by MLST analysis and having a similar PFGE band pattern with higher than 90% similarity, were isolated from 14 different hospitals and a commercial laboratory in seven different Prefectures. These Prefectures are located in geographically distant regions of Japan. However, 11 (46%) of these were isolated from six hospitals located in one Prefecture, Ishikawa Prefecture, over a 1 year period, which suggests a regional outbreak. Two E. coli O25:H- isolates belonging to fimH cluster B were isolated from two different patients in one hospital, and two E. coli O25:H4 isolates belonging to fimH cluster D were isolated from different patients in another hospital, which suggests nosocomial transmissions. Four E. coli O25:H4 isolates and one E. coli O25:HNM isolate, which belonged to a single fimH cluster C and ST131, were isolated from four different hospitals in three Prefectures. Twenty E. coli O25:H4 isolates in fimH cluster E were obtained from three hospitals located in three different Prefectures. Of these, 15 (75%) were isolated during an outbreak in a haematology unit. Four (20%) isolates with blaCTX-M-35 were isolated from different patients admitted to a single hospital.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
|---|
CTX-M-9-group ESBL-producing E. coli were not common in Japan prior to 2000.9 According to the JANIS, E. coli isolates non-susceptible to cefotaxime increased by more than 6-fold between 2001 and 2006. In this study, we found a cluster of E. coli O86 isolates, obtained from recognized outbreaks as well as from sporadic cases from hospitals all across Japan. These isolates were highly clonal, as evidenced by the multiple subtyping tests we used. This single clonal group accounted for 18% of all the blaCTX-M-positive E. coli isolates obtained during 2002–03. Its high clonality suggests that this epidemic strain spread throughout Japan relatively recently in a short period. As far as we know, this is the first documented report of a clonal spread of E. coli O86:H18-ST38 harbouring CTX-M-9-group blaCTX-M anywhere.
On the other hand, E. coli O25:H4-ST131 has been already recognized as an emerging intercontinental clonal group expressing CTX-M-type ESBL.6,21 In our study, we also found a cluster of O25 isolates but they were composed of multiple lineages—two different MLST groups (ST131 and ST73), four distinct fimH SNP genotypes, diverse PFGE patterns and two different flagella types (H4 and HNM). This suggests that E. coli O25 serogroup strains may have been circulating in Japan for a longer period. E. coli O25 is increasingly recognized in recent decades and is now the second to third most frequent serogroup among clinical E. coli isolates in Japan.22
In addition, all the E. coli O25:H4-ST131 isolates in our study harboured CTX-M-2-group blaCTX-M or blaCTX-M-14, which are the dominant CTX-M types in Asia including Japan. Most of the previously reported E. coli O25:H4-ST131 strains are CTX-M-15 producers. CTX-M-15 is a member of the CTX-M-1 group, which is dominant in European countries.23 In addition, plasmid analyses in this study revealed that even among the clonal E. coli strains, blaCTX-M genes were carried by different plasmids. Thus, E. coli O25:H4-ST131 strains could have multiple reservoirs from which they spread to different regions of the world acquiring different plasmids carrying different blaCTX-M types.
Clonal spread of other antimicrobial-resistant E. coli strains causing community- and hospital-acquired extraintestinal infections has been reported previously. Clusters of multidrug-resistant community-acquired E. coli O15:K52:H1 and O78:H10 extraintestinal infections have been reported in the 1990s in the UK and continental Europe.24,25 A clonally related group of multidrug-resistant uropathogenic E. coli called CgA has been reported throughout the USA and some parts of Europe, as well as from animals and the environment in the USA.26,27 The nationwide and intercontinental spread, as well as sporadic occurrences of unrelated clusters of community-acquired infections caused by ESBL-producing E. coli strains belonging to identical clonal lineages suggest that such strains are spread not just by person-to-person transmission or in hospital settings, but by some widely distributed contaminated ingestible products. Indeed, CTX-M-type ESBL-producing E. coli isolates have been isolated from food animals, usually from chickens but also from calves.28–31 This observation further supports the idea that the use of antimicrobial agents as growth promoters in animal food or as veterinary medicines contributes to the initial selection of these resistant organisms.
Our findings that a single clonal strain can abruptly change the prevalence of infections with ESBL-producing E. coli in different regions of a country suggest that restricting antimicrobial use in human clinical settings may have minimal impact on the spread of ESBL-producing E. coli that cause healthcare-associated infections in Japan and elsewhere. The control of antimicrobial resistance may require monitoring of antimicrobial use and surveillance of drug-resistant pathogens in the veterinary environment.
|
Funding |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
|---|
This work was supported by a grant from the Ministry of Health, Labour and Welfare of Japan (H18-Shinkou-011).
|
Transparency declarations |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
|---|
None to declare.
|
Acknowledgements |
|---|
We thank Dr Lee W. Riley, School of Public Health, University of California, Berkeley, for critical review of the manuscript; all medical institutions for submitting the bacterial strains and clinical information; Kumiko Kai, Yumiko Yoshimura and Yoshie Taki for technical assistance.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionFundingTransparency declarationsReferences |
|---|
1 . Philippon A, Labia R, Jacoby G. Extended-spectrum β-lactamases. Antimicrob Agents Chemother (1989) 33:1131–6.
2
.
Paterson DL, Bonomo RA. Extended-spectrum β-lactamases: a clinical update. Clin Microbiol Rev (2005) 18:657–86.
3 . Pitout JD, Laupland KB. Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis (2008) 8:159–66.[CrossRef][Web of Science][Medline]
4 . Jacoby G, Bush K. Amino Acid Sequences for TEM, SHV and OXA Extended-Spectrum and Inhibitor Resistant β-Lactamases. (7 October 2008, date last accessed).
5
.
Bonnet R. Growing group of extended-spectrum β-lactamases: the CTX-M enzymes. Antimicrob Agents Chemother (2004) 48:1–14.
6
.
Nicolas-Chanoine MH, Blanco J, Leflon-Guibout V, et al. Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. J Antimicrob Chemother (2008) 61:273–81.
7
.
Matsumoto Y, Ikeda F, Kamimura T, et al. Novel plasmid-mediated β-lactamase from Escherichia coli that inactivates oxyimino-cephalosporins. Antimicrob Agents Chemother (1988) 32:1243–6.
8 . Ishi Y, Ohno A, Taguchi H, et al. Cloning and sequence of the gene encoding a cefotaxime-hydrolyzing class A β-lactamase isolated from Escherichia coli. Antimicrob Agents Chemother (1995) 39:2269–75.[Abstract]
9 . Yagi T, Kurokawa H, Shibata N, et al. A preliminary survey of extended-spectrum β-lactamases (ESBLs) in clinical isolates of Klebsiella pneumoniae and Escherichia coli in Japan. FEMS Microbiol Lett (2000) 184:53–6.[Web of Science][Medline]
10
.
Shibata N, Kurokawa H, Doi Y, et al. PCR classification of CTX-M-type β-lactamase genes identified in clinically isolated Gram-negative bacilli in Japan. Antimicrob Agents Chemother (2006) 50:791–5.
11 . Ministry of Health Labour and Welfare. The Japan Nosocomial Infections Surveillance. (7 October 2008, date last accessed).
12 . National Committee for Clinical Laboratory Standards. Performance Standards for Antimicrobial Susceptibility Testing: Fourteenth Informational Supplement M100-S14. (2004) Wayne, PA, USA: NCCLS.
13 . Max-Planck Institut für Infektionsbiologie. MLST Databases at the MPI für Infektionsbiologie. (7 October 2008, date last accessed).
14
.
Tartof SY, Solberg OD, Riley LW. Genotypic analyses of uropathogenic Escherichia coli based on fimH single nucleotide polymorphisms (SNPs). J Med Microbiol (2007) 56:1363–9.
15
.
Bender JB, Hedberg CW, Besser JM, et al. Surveillance by molecular subtype for Escherichia coli O157:H7 infections in Minnesota by molecular subtyping. N Engl J Med (1997) 337:388–94.
16 . Yagi T, Kurokawa H, Senda K, et al. Nosocomial spread of cephem-resistant Escherichia coli strains carrying multiple Toho-1-like β-lactamase genes. Antimicrob Agents Chemother (1997) 41:2606–11.[Abstract]
17 . Carattoli A, Bertini A, Villa L, et al. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods (2005) 63:219–28.[CrossRef][Web of Science][Medline]
18
.
Sabate M, Tarrago R, Navarro F, et al. Cloning and sequence of the gene encoding a novel cefotaxime-hydrolyzing β-lactamase (CTX-M-9) from Escherichia coli in Spain. Antimicrob Agents Chemother (2000) 44:1970–3.
19
.
Chanawong A, M'Zali FH, Heritage J, et al. Three cefotaximases, CTX-M-9, CTX-M-13, and CTX-M-14, among Enterobacteriaceae in the People's Republic of China. Antimicrob Agents Chemother (2002) 46:630–7.
20 . Bauernfeind A, Stemplinger I, Jungwirth R, et al. Sequences of β-lactamase genes encoding CTX-M-1 (MEN-1) and CTX-M-2 and relationship of their amino acid sequences with those of other beta-lactamases. Antimicrob Agents Chemother (1996) 40:509–13.[Abstract]
21 . Coque TM, Novais A, Carattoli A, et al. Dissemination of clonally related Escherichia coli strains expressing extended-spectrum β-lactamase CTX-M-15. Emerg Infect Dis (2008) 14:195–200.[Web of Science][Medline]
22 . BML, Inc. BML Microbiological Tests Information. (7 October 2008, date last accessed).
23
.
Livermore DM, Canton R, Gniadkowski M, et al. CTX-M: changing the face of ESBLs in Europe. J Antimicrob Chemother (2007) 59:165–74.
24
.
O'Neill PM, Talboys CA, Roberts AP, et al. The rise and fall of Escherichia coli O15 in a London teaching hospital. J Med Microbiol (1990) 33:23–7.
25 . Olesen B, Kolmos HJ, Orskov F, et al. A comparative study of nosocomial and community-acquired strains of Escherichia coli causing bacteraemia in a Danish University Hospital. J Hosp Infect (1995) 31:295–304.[CrossRef][Web of Science][Medline]
26
.
Manges AR, Johnson JR, Foxman B, et al. Widespread distribution of urinary tract infections caused by a multidrug-resistant Escherichia coli clonal group. N Engl J Med (2001) 345:1007–13.
27 . Ramchandani M, Manges AR, DebRoy C, et al. Possible animal origin of human-associated, multidrug-resistant, uropathogenic Escherichia coli. Clin Infect Dis (2005) 40:251–7.[CrossRef][Web of Science][Medline]
28
.
Kojima A, Ishii Y, Ishihara K, et al. Extended-spectrum-β-lactamase-producing Escherichia coli strains isolated from farm animals from 1999 to 2002: report from the Japanese Veterinary Antimicrobial Resistance Monitoring Program. Antimicrob Agents Chemother (2005) 49:3533–7.
29
.
Smet A, Martel A, Persoons D, et al. Diversity of extended-spectrum β-lactamases and class C β-lactamases among cloacal Escherichia coli isolates in Belgian broiler farms. Antimicrob Agents Chemother (2008) 52:1238–43.
30
.
Warren RE, Ensor VM, O'Neill P, et al. Imported chicken meat as a potential source of quinolone-resistant Escherichia coli producing extended-spectrum β-lactamases in the UK. J Antimicrob Chemother (2008) 61:504–8.
31 . Shiraki Y, Shibata N, Doi Y, et al. Escherichia coli producing CTX-M-2 β-lactamase in cattle, Japan. Emerg Infect Dis (2004) 10:69–75.[Web of Science][Medline]
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  A. Valverde, R. Canton, M. P. Garcillan-Barcia, A. Novais, J. C. Galan, A. Alvarado, F. de la Cruz, F. Baquero, and T. M. Coque Spread of blaCTX-M-14 Is Driven Mainly by IncK Plasmids Disseminated among Escherichia coli Phylogroups A, B1, and D in Spain Antimicrob. Agents Chemother., December 1, 2009; 53(12): 5204 - 5212. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. E. Sidjabat, D. L. Paterson, J. M. Adams-Haduch, L. Ewan, A. W. Pasculle, C. A. Muto, G.-B. Tian, and Y. Doi Molecular Epidemiology of CTX-M-Producing Escherichia coli Isolates at a Tertiary Medical Center in Western Pennsylvania Antimicrob. Agents Chemother., November 1, 2009; 53(11): 4733 - 4739. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
N. Woodford, A. Carattoli, E. Karisik, A. Underwood, M. J. Ellington, and D. M. Livermore Complete Nucleotide Sequences of Plasmids pEK204, pEK499, and pEK516, Encoding CTX-M Enzymes in Three Major Escherichia coli Lineages from the United Kingdom, All Belonging to the International O25:H4-ST131 Clone Antimicrob. Agents Chemother., October 1, 2009; 53(10): 4472 - 4482. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 O. Clermont, H. Dhanji, M. Upton, T. Gibreel, A. Fox, D. Boyd, M. R. Mulvey, P. Nordmann, E. Ruppe, J. L. Sarthou, et al. Rapid detection of the O25b-ST131 clone of Escherichia coli encompassing the CTX-M-15-producing strains J. Antimicrob. Chemother., August 1, 2009; 64(2): 274 - 277. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. D. D. Pitout, D. B. Gregson, L. Campbell, and K. B. Laupland Molecular Characteristics of Extended-Spectrum-{beta}-Lactamase-Producing Escherichia coli Isolates Causing Bacteremia in the Calgary Health Region from 2000 to 2007: Emergence of Clone ST131 as a Cause of Community-Acquired Infections Antimicrob. Agents Chemother., July 1, 2009; 53(7): 2846 - 2851. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. F. Mataseje, N. Neumann, B. Crago, P. Baudry, G. G. Zhanel, M. Louie, M. R. Mulvey, and and the ARO Water Study Group Characterization of Cefoxitin-Resistant Escherichia coli Isolates from Recreational Beaches and Private Drinking Water in Canada between 2004 and 2006 Antimicrob. Agents Chemother., July 1, 2009; 53(7): 3126 - 3130. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Blanco, M. P. Alonso, M.-H. Nicolas-Chanoine, G. Dahbi, A. Mora, J. E. Blanco, C. Lopez, P. Cortes, M. Llagostera, V. Leflon-Guibout, et al. Molecular epidemiology of Escherichia coli producing extended-spectrum {beta}-lactamases in Lugo (Spain): dissemination of clone O25b:H4-ST131 producing CTX-M-15 J. Antimicrob. Chemother., June 1, 2009; 63(6): 1135 - 1141. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||