Enterobacteriaceae Sepsis Outcome Programme annual report, 2013

Results of the Australian Group on Antimicrobial Resistance surveillance program of 2013 for Enterobacteriacae isolated from blood stream infections are presented. Low but growing rates of extended-spectrum ß-lactamases are now being observed, and carbapenemase-producing strains, although rare, are now being observed. Resistance to fluoroquinolones appears to be increasing.

Page last updated: 24 December 2014

John D Turnidge, Thomas Gottlieb, David H Mitchell, Geoffrey W Coombs, Denise A Daley, Jan M Bell for the Australian Group on Antimicrobial Resistance

Abstract

The Australian Group on Antimicrobial Resistance performs regular period-prevalence studies to monitor changes in antimicrobial resistance in selected enteric Gram-negative pathogens. The 2013 survey focussed for the first time on blood stream infections. Four thousand nine hundred and fifty-eight Enterobacteriaceae species were tested using commercial automated methods (Vitek® 2, BioMérieux; Phoenix™, BD). The results were analysed using Clinical and Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST) breakpoints (January 2014). Of the key resistances, non-susceptibility to the third-generation cephalosporin, ceftriaxone, was found in 7.5%/7.5% (CLSI/EUCAST criteria respectively) of Escherichia coli; 6.3%/6.3% of Klebsiella pneumoniae, and 7.4%/7.4% of K. oxytoca. Non-susceptibility rates to ciprofloxacin were 10.3%/11.3% for E. coli, 4.6%/7.5% for K. pneumoniae, 0.6%/0.6% for K. oxytoca, and 3.6%/6.1% in Enterobacter cloacae. Resistance rates to piperacillin-tazobactam were 3.1%/6.2%, 4.2%/7.0%, 11.9% /12.6%, and 17.3% /22.2% for the same 4 species respectively. Fourteen isolates were shown to harbour a carbapenemase gene, 9 blaIMP, 3 blaKPC, and 2 blaNDM. Commun Dis Intell 2014;38(4):E327–E333.

Keywords: antibiotic resistance; bacteraemia; gram-negative; Escherichia coli; Enterobacter; Klebsiella

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Introduction

Emerging resistance in common pathogenic members of the Enterobacteriaceae family is a worldwide phenomenon, and presents therapeutic problems for practitioners in both the community and in hospital practice. The Australian Group on Antimicrobial Resistance (AGAR) commenced surveillance of the key Gram-negative pathogens, Escherichia coli and Klebsiella species in 1992. Surveys were conducted biennially until 2008 when annual surveys commenced alternating between community– and hospital-onset infections (http://www.agargroup.org/surveys). In 2004, another genus of Gram-negative pathogens in which resistance can be of clinical importance, Enterobacter species, was added. E. coli is the most common cause of community-onset urinary tract infection, while Klebsiella species are less common but are known to harbour important resistances. Enterobacter species are less common in the community, but of high importance due to intrinsic resistance to first-line antimicrobials in the community. Taken together, the 3 groups of species surveyed are considered to be valuable sentinels for multi-resistance and emerging resistance in enteric Gram-negative bacilli. In 2013, AGAR commenced the Enterobacteriaceae Sepsis Outcome Programme, which focuses on the collection of resistance and some demographic data on all isolates prospectively from patients with bacteraemia.

Resistances of particular interest include resistance to ß-lactams due to ß-lactamases, especially extended-spectrum ß-lactamases (ESBL). These inactivate the third-generation cephalosporins that are normally considered reserve antimicrobials. Other resistances of interest are to agents important for treatment of these serious infections, such as gentamicin; and resistance to reserve agents such as ciprofloxacin and meropenem.

The objectives of the 2013 surveillance program were to:

  • monitor resistance in Enterobacteriaceae isolated from blood;
  • examine the extent of co-resistance and multi-resistance; and
  • detect emerging resistance to newer last-line agents such as carbapenems.

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Methods

Study design

From 1 January to 31 December 2013, 25 institutions across Australia collected either all or up to 200 isolates from different patient episodes of bacteraemia.

Species identification

Isolates were identified using the routine method for each institution; Vitek®, Phoenix™ Automated Microbiology System, or where available, mass spectrometry (MALDI-TOF).

Susceptibility testing

Testing was performed by 2 commercial semi-automated methods, Vitek ® 2 (BioMérieux) or Phoenix™ (BD), which are calibrated to the ISO reference standard method of broth microdilution. Commercially available Vitek AST-N246, Vitek AST-N247, Phoenix NMIC/ID-80 or Phoenix NMIC-203 cards were utilised by all participants throughout the survey period. The Clinical and Laboratory Standards Institute (CLSI) M1001 and European Committee on Antimicrobial Susceptibility Testing (EUCAST) v4.02 breakpoints from January 2014 have been employed in the analysis. For analysis of cefazolin, breakpoints of ≤ 4 for susceptible and ≥ 8 for resistant were applied due to the restricted minimum inhibitory concentration (MIC) range available on the commercial cards, recognising that the January 2014 breakpoint is actually susceptible (≤ 2 mg/L).

Molecular confirmation of resistances

E. coli and Klebsiella isolates with ceftazidime or ceftriaxone MIC > 1 mg/L, or cefoxitin MIC > 8 mg/L; Enterobacter spp. with cefepime MIC > 1 mg/L; all isolates with ciprofloxacin MIC > 0.25 mg/L; and all isolates with meropenem MIC > 0.25 mg/L were referred to a central laboratory (SA Pathology) for molecular confirmation of resistance.

All referred isolates were screened for the presence of the blaTEM, and blaSHV genes using a real-time polymerase chain reaction (PCR) platform (LC-480) and published primers.3,4 A multiplex real-time TaqMan PCR was used to detect CTX-M-type genes.5 Strains were probed for plasmid-borne AmpC enzymes using the method described by Pérez-Pérez and Hanson,6 and subjected to molecular tests for MBL (blaVIM, blaIMP, and blaNDM), blaKPC, and blaOXA-48-like genes using real-time PCR.7,8 Known plasmid mediated quinolone resistance mechanisms (Qnr, efflux (qepA, oqxAB), and aac(6’)-Ib-cr) were examined by PCR on all referred isolates with ciprofloxacin MIC > 0.25 mg/L using published methods.9,10 All E. coli were examined for the presence of the O25b-ST131 clone and its H30- and H30-Rx subclones.11-13

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Results

A total of 4,958 Enterobacteriaceae species were tested. The species isolated and the numbers of each are listed in Table 1. Three genera, E. coli, Klebsiella spp. and Enterobacter spp. contributed 86.3% of all isolates. Major resistances and non-susceptibilities for the top 6 ranked species are listed in Table 2. Non-susceptibility, which includes intermediately resistant and resistant strains, has been included for some agents because these figures provide information about important emerging acquired resistances. Multiple acquired resistances by species are shown in Table 3. Multi-resistance was detected in 11.7% of E. coli isolates, 7.0% of K. pneumoniae, and 12.6% of Enterobacter cloacae. A more detailed breakdown of resistances and non-susceptibilities by state and territory is provided in the online report from the group (http://www.agargroup.org/surveys).

Table 1: Species tested
Species Total %
Escherichia coli
2,958
59.7
Klebsiella pneumoniae
727
14.7
Enterobacter cloacae
311
6.3
Proteus mirabilis
184
3.7
Klebsiella oxytoca
163
3.3
Serratia marcescens
156
3.1
Enterobacter aerogenes
98
2.0
Salmonella species (non Typhi)
78
1.6
Morganella morganii
54
1.1
Citrobacter koseri
51
1.0
Citrobacter freundii
38
0.8
Salmonella Typhi/paratyphi
23
0.5
Pantoea agglomerans
13
0.3
Raoultella ornithinolytica
11
0.2
Enterobacter asburiae
11
0.2
Other species (n = 31)
82
1.7
All species
4,958

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Table 2: Non-susceptibility and resistance rates for the top 6 ranked species tested
Antimicrobial Category* Escherichia coli
(%)
Klebsiella pneumoniae
(%)
Klebsiella oxytoca
(%)
Enterobacter cloacae
(%)
Proteus mirabilis
(%)
Serritia marcescens
(%)
CLSI EUCAST CLSI EUCAST CLSI EUCAST CLSI EUCAST CLSI EUCAST CLSI EUCAST
CLSI = Clinical and Laboratory Standards Institute.

EUCAST European Committee on Antimicrobial Susceptibility Testing.

* R = resistant, I = intermediate, NS = non-susceptible (intermediate + resistant), using criteria as published by the CLSI [2014] and EUCAST [2014].

† Considered largely intrinsically resistant due to natural β-lactamases; - no intermediate category; / no breakpoints defined.
Ampicillin
I
2.0
-
2.8
-
Ampicillin
R
50.2
52.2
17.0
19.8
Amoxycillinclavulanate
I
12.7
-
5.5
-
4.3
-
5.5
-
Amoxycillinclavulanate
R
8.8
21.5
6.0
11.5
8.7
13.0
5.0
10.5
Ticarcillin-clavulanate
R
8.1
18.3
5.9
9.6
10.6
12.5
23.3
27.5
0.6
1.7
1.9
5.1
Piperacillintazobactam
R
3.1
6.2
4.2
7.0
11.9
12.6
17.3
22.2
0.6
1.1
0.0
2.1
Cefazolin
R
19.1
/
10.0
/
62.1
/
24.2
/
Cefoxitin
R
2.9
/
4.2
/
0.0
/
1.1
/
Ceftriaxone
NS
7.5
7.5
6.3
6.3
7.4
7.4
26.8
26.8
1.6
1.6
5.1
5.1
Ceftazidime
NS
4.1
7.0
4.9
6.6
1.3
1.9
23.3
26.9
0.5
1.1
0.6
1.9
Cefepime
NS
3.5
6.0
2.8
5.0
0.6
0.6
4.5
12.0
0.5
1.1
0.6
1.3
Meropenem
NS
0.1
0.1
0.7
0.5
0.0
0.0
4.2
3.9
0.0
0.0
1.3
1.3
Ciprofloxacin
NS
10.3
11.3
4.6
7.5
0.6
0.6
3.6
6.1
2.2
3.8
1.3
2.6
Norfloxacin
NS
10.0
17.0
4.0
13.0
0.7
1.4
2.8
13.8
1.7
4.7
0.7
5.6
Gentamicin
NS
7.9
8.4
3.9
4.2
0.6
0.6
9.4
9.7
3.8
7.1
1.3
1.9
Trimethoprim
R
26.9
28.7
14.1
15.9
3.2
3.8
19.7
21.4
20.8
21.4
1.3
1.3
Nitrofurantoin
NS
6.1
1.3
81.6
36.7
41.0
2.5
73.4
20.1

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Table 3: Multiple acquired resistances, by species
Species Total Number of acquired resistances (CLSI breakpoints)
Non-multi-resistant Multi-resistant
0 1 2 3 Cumulative
%
4 5 6 7 8 9 10 11 12 Cumulative
%
CLSI = Clinical and Laboratory Standards Institute.

* Antibiotics included: amoxycillin-clavulanate, piperacillin-tazobactam, cefazolin, cefoxitin, ceftriaxone, ceftazidime, cefepime, gentamicin, amikacin, ciprofloxacin, nitrofurantoin, trimethoprim, meropenem;.
Antibiotics excluded: ampicillin (intrinsic resistance), ticarcillin-clavulanate, tobramycin, norfloxacin, nalidixic acid, sulfamethoxazole-trimethoprim (high correlation with antibiotics in the included list).

† Antibiotics included: piperacillin-tazobactam, ceftriaxone, ceftazidime, cefepime, gentamicin, amikacin, ciprofloxacin, nitrofurantoin, trimethoprim, meropenem
Antibiotics excluded: ampicillin, amoxycillin-clavulanate, cefazolin, and cefoxitin, (all four due to intrinsic resistance); also excluded were ticarcillin-clavulanate, tobramycin, norfloxacin, nalidixic acid, sulfamethoxazole-trimethoprim (high correlation with antibiotics in the included list).
Escherichia coli
2,434
1,031
490
431
197
101
54
65
37
19
7
2
%
42.4
20.1
17.7
8.1
88.3
4.1
2.2
2.7
1.5
0.8
0.3
0.1
11.7
Klebsiella pneumonia
598
328
163
53
12
7
13
8
5
2
2
1
2
2
%
54.8
27.3
8.9
2.0
93.0
1.2
2.2
1.3
0.8
0.3
0.3
0.2
0.3
0.3
7.0
Enterobacter cloacae
301
162
55
13
33
16
13
4
2
3
%
53.8
18.3
4.3
11.0
87.4
5.3
4.3
1.3
0.7
1.0
12.6
Proteus mirabilis
151
8
78
41
12
9
1
0
0
1
0
1
%
5.3
51.7
27.2
7.9
92.1
6.0
0.7
0.0
0.0
0.7
0.0
0.7
7.9
Serritia marcescens
142
1
134
5
1
0
0
1
%
0.7
94.4
3.5
0.7
99.3
0.0
0.0
0.7
0.7
Klebsiella oxytoca*
139
47
70
10
5
7
%
33.8
50.4
7.2
3.6
95.0
5.0
5.0
Enterobacter aerogenes
94
30
36
4
14
10
%
31.9
38.3
4.3
14.9
89.4
10.6
10.6
Salmonella spp. (non Typhi)
65
53
8
2
1
1
%
81.5
12.3
3.1
1.5
98.5
1.5
1.5

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Escherichia coli

Moderately high levels of resistance to ampicillin (and therefore amoxycillin) were observed (50.2%/52.2%, CLSI/EUCAST criteria), with lower rates for amoxycillin-clavulanate (12.7%/– intermediate, 8.8%/21.5% resistant). Non-susceptibility to third-generation cephalosporins was low (ceftriaxone 7.5%/7.5%, ceftazidime 4.1%/7.0%). Moderate levels of resistance were detected to cefazolin (19.1%/–) and trimethoprim (26.9%/28.7%). Ciprofloxacin non-susceptibility was found in 10.3%/11.3% of E. coli isolates. Resistance to ticarcillin-clavulanate (8.1%/18.3%), gentamicin (7.7%/7.9%), piperacillin-tazobactam (3.1%/6.2%), cefepime (1.9%/2.8%) were low. Four isolates had elevated meropenem MICs (≥ 0.5 mg/L). For the ESBL-producing strains. ciprofloxacin and gentamicin resistance was found in 57.3%/59.0% and 41.0%/41.4% respectively.

In line with international trends among community strains of E. coli, most of the strains with ESBL genes harboured genes of the CTX-M type (171/229 = 75%). Over half of the E. coli with CTX-M group 1 types were found to belong to sequence type 131 (O25b-ST131). ST131 accounted for 66% of E. coli ESBL phenotypes that were ciprofloxacin resistant (MIC > 1 mg/L), and only 2% of ciprofloxacin susceptible ESBL phenotypes. Ninety-eight per cent and 57% of O25b-ST131 were associated with the H30 and H30-Rx subclones, respectively, with their reported association with more antibiotic resistances and greater virulence potential.12

Klebsiella pneumoniae

K. pneumoniae showed slightly higher levels of resistance to piperacillin-tazobactam and ceftazidime compared with E. coli, but lower rates of resistance to amoxycillin-clavulanate, ticarcillin-clavulanate, cefazolin, ceftriaxone ciprofloxacin, gentamicin, and trimethoprim. Four K. pneumoniae isolates had elevated meropenem MICs (see below). ESBLs were present in 38 of 45 (84%) presumptively ESBL-positive isolates of K. pneumoniae, 31 of which proved to be of the CTX-M type.

Enterobacter species

Acquired resistance was common to ticarcillin-clavulanate (23.3%/27.5% and 27.8%/32.0%), piperacillin-tazobactam (17.3%/22.2% and 20.6%/28.9%), ceftriaxone (26.5%/26.5% and 28.9%/28.9%), ceftazidime (22.7%/23.3% and 28.9%/28.9%) and trimethoprim (19.7/21.4% and 3.2%/3.2%) for Ent. cloacae and Ent. aerogenes, respectively. Cefepime, ciprofloxacin, and gentamicin resistance were all less than 10%. Fifteen of 33 Ent. cloacae tested for ESBLs based on a suspicious phenotype, harboured ESBL-encoding genes. Thirteen Ent. cloacae strains had elevated meropenem MICs.

Carbapenemase resistance

Overall, 14 isolates from 12 patients were found to harbour a carbapenemase gene. blaIMP was detected in 9 strains (Ent. cloacae (4), Citrobacter spp. (2) E. coli (1), S. marcescens (1), K. pneumoniae (1); blaKPC was detected in 3 K. pneumoniae isolates (1 patient with multiple admission); and blaNDM in 1 patient with 2 bacteraemic episodes.

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Discussion

AGAR has been tracking resistance in sentinel enteric Gram-negative bacteria since 1992. From 2008, surveillance was segregated into hospital- versus community-onset infections. The last year of hospital-onset only surveillance was 2011.14 This is the first comprehensive survey of antimicrobial resistance among Enterobacteriaceae isolates from bacteraemic patients throughout Australia, using an approach similar to that conducted by the European EARS-Net program (http://www.ecdc.europa.eu/en/healthtopics/antimicrobial_resistance/database/Pages/database.aspx).

CTX-M-producing E. coli and Klebsiella species and gentamicin- and ciprofloxacin-resistant E. coli are well established among bacteraemic patients. Of concern is the high proportion of E. coli that belong to the ST131 H30-Rx subclone, and its reported association with more antibiotic resistance and greater virulence potential.12 Carbapenem resistance attributable to acquired carbapenemases are still rare in patients with bacteraemia in Australia, although 3 different types (IMP, KPC, and NDM) were detected from seven of the participating institutions. Compared with many other countries in our region, resistance rates in Australian Gram-negative bacteria are still relatively low,15 but similar to those observed in 2012 in many Western European countries (http://ecdc.europa.eu/en/publications/Publications/antimicrobial-resistance-surveillance-europe-2012.pdf).

Multi-resistance is being increasingly observed, especially in E. coli and Ent. cloacae, both of which have multi-resistance rates (as defined by AGAR) above 10%. This is likely to drive more broad-spectrum antibiotic use, and increase the resistance selection pressure for important reserve classes, especially the carbapenemases.

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Agar participants

Australian Capital Territory

Peter Collignon and Susan Bradbury, The Canberra Hospital

New South Wales

Thomas Gottlieb and Graham Robertson, Concord Hospital

James Branley and Donna Barbaro, Nepean Hospital

George Kotsiou and Peter Huntington, Royal North Shore Hospital

David Mitchell and Lee Thomas, Westmead Hospital

Northern Territory

Rob Baird and Jann Hennessy, Royal Darwin Hospital

Queensland

Enzo Binotto and Bronwyn Thomsett, Pathology Queensland Cairns Base Hospital

Graeme Nimmo and Narelle George, Pathology Queensland Central Laboratory

Petra Derrington and Sharon Dal-Cin, Pathology Queensland Gold Coast Hospital

Chris Coulter and Tobin Hillier, Pathology Queensland Prince Charles Hospital

Naomi Runnegar and Joel Douglas, Pathology Queensland Princess Alexandra Hospital

Jenny Robson and Georgia Peachey, Sullivan Nicolaides Pathology

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South Australia

Kelly Papanoum and Nicholas Wells, SA Pathology, Flinders Medical Centre

Morgyn Warner and Fleur Manno, SA Pathology, Royal Adelaide Hospital

John Turnidge and Jan Bell, SA Pathology, Women’s and Children’s Hospital

Tasmania

Louise Cooley and Rob Peterson, Royal Hobart Hospital

Victoria

Denis Spelman and Christopher Lee Alfred Hospital

Benjamin Howden and Peter Ward, Austin Hospital

Tony Korman and Despina Kotsanas, Southern Health, Monash Medical Centre

Andrew Daley and Gena Gonis, Royal Women’s Hospital

Mary Jo Waters and Linda Joyce, St Vincent’s Hospital

Western Australia

David McGechie and Rebecca Wake, PathWest Laboratory Medicine WA, Fremantle Hospital

Michael Leung, Barbara Henderson and Ronan Murray, PathWest Laboratory Medicin, WA, Queen Elizabeth II Hospital

Owen Robinson, Geoffrey Coombs and Denise Daley, PathWest Laboratory Medicine WA, Royal Perth Hospital

Sudha Pottumarthy-Boddu and Fay Kappler, St John of God Pathology

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Author details

John Turnidge1,2

Thomas Gottlieb3

David Mitchell4

Geoffrey Coombs5,6

Denise Daley6

Jan Bell1

  1. Microbiology and Infectious Diseases, SA Pathology, Women’s and Children’s Hospital, North Adelaide, South Australia
  2. Departments of Pathology, Paediatrics and Molecular Biosciences, University of Adelaide, South Australia
  3. Department of Microbiology and Infectious Diseases, Concord, Concord, New South Wales
  4. Centre for Infectious Diseases and Microbiology, Westmead Hospital, Westmead, New South Wales
  5. Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research, School of Biomedical Sciences, Curtin University, Perth, Western Australia
  6. Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine-WA, Royal Perth Hospital, Perth, Western Australia

Corresponding author: Professor John Turnidge, Microbiology and Infectious Diseases, SA Pathology, Women’s and Children’s Hospital, 72 King William Road, NORTH ADELAIDE SA 6001. Telephone: +61 8 8161 6873 Email: john.turnidge@health.sa.gov.au

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References

  1. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. Twenty-Forth Informational Supplement M100–S24. Villanova, PA, USA 2014.
  2. European Committee on Antimicrobial Susceptibility Testing (2014). Breakpoint tables for interpretation of MICs and zone diameters. Version 4.0, January 2014. Accessed on 1 January 2014. Available from: http://www.eucast.org/clinical_breakpoints/
  3. Hanson ND, Thomson KS, Moland ES, Sanders CC, Berthold G, Penn RG. Molecular characterization of a multiply resistant Klebsiella pneumoniae encoding ESBLs and a plasmid-mediated AmpC. J Antimicrob Chemother 1999;44(3):377–380.
  4. Chia JH, Chu C, Su LH, Chiu CH, Kuo AJ, Sun CF, et al. Development of a multiplex PCR and SHV melting-curve mutation detection system for detection of some SHV and CTX-M b-lactamases of Escherichia coli, Klebsiella pneumoniae, and Enterobacter cloacae in Taiwan. J Clin Microbiol 2005;43(9):4486–4491.
  5. Birkett CI, Ludlam HA, Woodford N, Brown DFJ, Brown NM, Roberts MTM, et al. Real-time TaqMan PCR for rapid detection and typing of genes encoding CTX-M extended-spectrum ß-lactamases. J Med Microbiol 2007;56(Pt 1):52–55.
  6. Perez-Perez FJ, Hanson ND. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002;40(6):2153–2162.
  7. Poirel L, Héritier C, Tolün V, Nordmann P. Emergence of oxacillinase-mediated resistance to imipenem in Klebsiella pneumoniae. Antimicrob Agents Chemother 2004;48(1):15–22.
  8. Mendes RE, Kiyota KA, Monteiro J, Castanheira M, Andrade SS, Gales AC, et al. Rapid detection and identification of metallo-ß-lactamase-encoding genes by multiplex real-time PCR assay and melt curve analysis. J Clin Microbiol 2007;45(2):544–547.
  9. Cattoir V, Poirel L, Rotimi V, Soussy C-J, Nordmann P. Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 2007;60(2):394-397.
  10. Ciesielczuk H, Hornsey M, Choi V, Woodford N, Wareham DW. Development and evaluation of a multiplex PCR for eight plasmid-mediated quinolone-resistance determinants. J Med Microbiol 2013;62(Pt 12):1823-1827.
  11. Dhanjii H, Doumith M, Clermont O, Denamur E, Hope R, Livermore DM, et al. Real-time PCR for detection of the O25b-ST131 clone of Escherichia coli and its CTX-M-15-like extended-spectrum ß-lactamases. J Antimicrob Agents 2010;36(4):355-358.
  12. Banerjee R, Robicsek A, Kuskowski MA, Porter S, Johnston BD, Sokurenko E, et al. Molecular epidemiology of Escherichia coli sequence type 131 and Its H30 and H30-Rx subclones among extended-spectrum-ß-lactamase-positive and -negative E. coli clinical Isolates from the Chicago region, 2007 to 2010. Antimicrob Agents Chemother 2013;57(12):6385–6388.
  13. Colpan A, Johnston B, Porter S, Clabots C, Anway R, Thao L, et al. Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans. Clin Infect Dis 2013;57(9):1256–65.
  14. Turnidge J, Gottlieb T, Mitchell D, Pearson J, Bell J, for the Australian Group for Antimicrobial Resistance. Gram-negative Survey 2011 Antimicrobial Susceptibility Report. 2011 Adelaide. Available from: http://www.agargroup.org/files/AGAR%20GNB08%20Report%20FINAL.pdf
  15. Sheng WH, Badal RE, Hsueh PR; SMART Program. Distribution of extended-spectrum ß-lactamases, AmpC ß-lactamases, and carbapenemases among Enterobacteriaceae isolates causing intra-abdominal infections in the Asia–Pacific region: results of the study for Monitoring Antimicrobial Resistance Trends (SMART). Antimicrob Agents Chemother 2013;57(7):2981–2988.

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