Australian Enterococcal Sepsis Outcome Progamme, 2011

From 1 January to 31 December 2011, 29 institutions around Australia participated in the Australian Enterococcal Sepsis Outcome Programme (AESOP). Of the 1,079 unique episodes of bacteraemia investigated, 95.8% were caused by either Entorococcus faecalis (61.0%) or E. faecium (34.8%). Although polyclonal, enterococcal bacteraemias in Australia are frequently caused by ampicillin-resistant vanB E. faecium.

Page last updated: 07 November 2014

Geoffrey W Coombs, Julie C Pearson, Denise A Daley, Tam Le, James O Robinson, Thomas Gottlieb, Benjamin P Howden, Paul DR Johnson, Catherine M Bennett, Timothy P Stinear, John D Turnidge for the Australian Group on Antimicrobial Resistance

Abstract

From 1 January to 31 December 2011, 29 institutions around Australia participated in the Australian Enterococcal Sepsis Outcome Programme (AESOP). The aim of AESOP 2011 was to determine the proportion of enterococcal bacteraemia isolates in Australia that are antimicrobial resistant, with particular emphasis on susceptibility to ampicillin and the glycopeptides, and to characterise the molecular epidemiology of the Enterococcus faecalis and E. faecium isolates. Of the 1,079 unique episodes of bacteraemia investigated, 95.8% were caused by either E. faecalis (61.0%) or E. faecium (34.8%). Ampicillin resistance was detected in 90.4% of E. faecium but not detected in E. faecalis. Using Clinical and Laboratory Standards Institute breakpoints (CLSI), vancomycin non-susceptibility was reported in 0.6% and 31.4% of E. faecalis and E. faecium respectively and was predominately due to the acquisition of the vanB operon. Approximately 1 in 6 vanB E. faecium isolates however, had an minimum inhibitory concentration at or below the CLSI vancomycin susceptible breakpoint of ≤ 4 mg/L. Overall, 37% of E. faecium harboured vanA or vanB genes. Although molecular typing identified 126 E. faecalis pulsed-field gel electrophoresis (PFGE) pulsotypes, more than 50% belonged to 2 pulsotypes that were isolated across Australia. E. faecium consisted of 73 PFGE pulsotypes from which 43 multilocus sequence types were identified. Almost 90% of the E. faecium were identified as clonal complex 17 clones, of which approximately half were characterised as sequence type 203, which was isolated Australia-wide. In conclusion, the AESOP 2011 has shown that although polyclonal, enterococcal bacteraemias in Australia are frequently caused by ampicillin-resistant vanB E. faecium. Commun Dis Intell 2014;38(3):E247–E252.

Keywords: antimicrobial resistance surveillance; Enterococcus faecium, Enterococcus faecalis, vancomycin resistant, bacteraemia

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Introduction

Globally, enterococci are thought to account for approximately 10% of all bacteraemias,1 and in North America and Europe are the 4th and 5th leading cause of sepsis, respectively.2 Although in the 1970s, healthcare-associated enterococcal infections were primarily due to Enterococcus faecalis,3 there has been a steadily increasing prevalence of E. faecium nosocomial infections.4,5 While innately resistant to many classes of antibiotics, E. faecium has demonstrated a remarkable capacity to evolve new antimicrobial resistances. By the early 1990s vancomycin resistant E. faecium had become the 2nd most common nosocomial pathogen in the United States of America (USA),6 and was endemic in many North American hospitals.7 Vancomycin resistance in E. faecium bacteraemia isolates ranges from 5%–35% in Europe to 60% in North America.8,9 In 2009, the Infectious Diseases Society of America highlighted E. faecium as one of the key problem bacteria or ESKAPE (Enterococcus faecium, Staphylococcus aureus, Klebsiella pneumoniae, Acinetobacter baumanii, Pseudomonas aeruginosa, and Enterobacter species) pathogens requiring new therapies.10

The Australian Group on Antimicrobial Resistance (AGAR) is a network of laboratories located across Australia that commenced surveillance of antimicrobial resistance in Enterococcus species in 1995.11 In 2011, AGAR commenced the Australian Enterococcal Sepsis Outcome Programme (AESOP). The objective of the AESOP 2011 was to determine the proportion of E. faecalis and E. faecium bacteraemia isolates demonstrating antimicrobial resistance with particular emphasis on:

  • assessing susceptibility to ampicillin;
  • assessing susceptibility to glycopeptides; and
  • molecular epidemiology of E. faecalis and E. faecium.

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Methodology

Participants

Twenty-nine laboratories including 26 public and 3 private laboratories from all 8 Australian states and territories participated in the AESOP 2011 study.

Collection period

From 1 January to 31 December 2011, 29 laboratories collected all enterococcal species isolated from blood cultures. Enterococci with the same species and antimicrobial susceptibility profiles isolated from a patient’s blood culture within 14 days of the 1st positive culture were excluded. A new enterococcal sepsis episode in the same patient was recorded if it was confirmed by a further culture of blood taken more than 14 days after the initial positive culture.

Laboratory testing

Ampicillin susceptibility testing was performed according to each laboratory’s routine standardised methodology. Clinical and Laboratory Standards Institute (CLSI) breakpoints were utilised for interpretation.12 Of the 1,033 E. faecalis and E. faecium sepsis isolates, 963 (93.2%) were referred to the Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research for vancomycin and teicoplanin minimum inhibitory concentration (MIC) estimation by Etest (bioMérieux) according to the manufacturer’s guidelines. Isolates with a CLSI intermediate or resistant category were classified as non-susceptible. Molecular testing including vanA/B polymerase chain reaction, pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST) was performed as previously described.13–15

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Results

From 1 January to 31 December 2011, 1,079 unique episodes of enterococcal bacteraemia were identified. Although 8 Enterococcus species were identified, 61.0% (658 isolates) were E. faecalis and 34.8% (375) were E. faecium. Forty-five enterococci were identified either as E. casseliflavus (15 isolates), E. gallinarum (14), E. avium (8), E. raffinosus (4), E. durans (2) or E. hirae (2). One isolate could not be identified to the species level.

Phenotypic susceptibility results

Overall 90.4% (339) of the 375 isolates of E. faecium were ampicillin resistant. Ampicillin resistance was not detected in the 658 E. faecalis isolates. Vancomycin and teicoplanin MICs were performed on the 622 E. faecalis and 341 E. faecium referred to ACCESS Typing and Research. The vancomycin MICs for the E. faecalis isolates ranged from 0.25–>256 mg/L with a mode of 2 mg/L. The 3 vancomycin non-susceptible isolates (MIC >4 mg/L) had MICs of 16, 32 and >256 mg/L, respectively. The E. faecalis teicoplanin MICs ranged from 0.064–2 mg/L with a mode of 0.25 mg/L. None of the E. faecalis isolates had a teicoplanin MIC above the CLSI susceptible breakpoint of ≤8 mg/L. The vancomycin MICs for the E. faecium isolates ranged from 0.25–>256 mg/L with a mode of 1.0 mg/L. Overall, 31.4% (107 isolates) of E. faecium had a vancomycin MIC >4 mg/L. The E. faecium teicoplanin MICs ranged from 0.047–>256 mg/L, with a mode of 0.5 mg/L. Five isolates had a teicoplanin MIC >8 mg/L.

Genotypic vancomycin susceptibility results

The 3 vancomycin non-susceptible E. faecalis isolates harboured a vanB gene. Two and 104 of the 107 E. faecium vancomycin non-susceptible isolates harboured vanA and vanB genes respectively. The vanA/vanB negative vancomycin non-susceptible E. faecium isolate had a MIC of 6 mg/L. Twenty of the 234 vancomycin susceptible E. faecium isolates (MIC ≤4 mg/L) also harboured vanB genes. The 2 vanA E. faecium isolates had a vancomycin MIC >256 mg/L. Thirty-three vancomycin non-susceptible E. faecium isolates had a vancomycin MIC within the CLSI intermediate category of 8–16 mg/L. Only 71 (57.2%) of the 124 vanB E. faecium isolates had a MIC above the CLSI vancomycin resistant breakpoint (≥32 mg/L). The 2 vanA E. faecium isolates had teicoplanin MICs of 32 and 64 mg/L. Of the 124 vanB E. faecium isolates one was teicoplanin intermediate (MIC 16 mg/L) and three were resistant (MIC >32 mg/L) by CLSI criteria.

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Molecular epidemiology

By PFGE, 618 of the 622 E. faecalis were classified into 126 pulsotypes of which 9 pulsotypes (Efs1 to Efs9) had 10 or more isolates. Four isolates could not be typed by PFGE. Of the 117 pulsotypes that have less than 10 isolates, 66 pulsotypes were represented by only 1 isolate. Geographically, the 9 major pulsotypes were widely distributed, with the 2 predominant pulsotypes EFs1 (191 isolates) and Efs2 (103 isolates), isolated across Australia (Table 1). The 3 vanB E. faecalis were detected in pulsotype Efs2.

Table 1: Number and proportion of major Enterococcus faecalis pulsed-field gel electrophoresis pulsotypes, Australia, 2011, by state or territory
ACT NSW NT Qld SA Tas. Vic. WA Aus.
Type n % n % n % n % n % n % n % n % n %
NT = Not typed.

The category type 'other' includes the 117 pulsed-field gel electrophoresis pulsotypes that had less than 10 isolates per pulsotype.
Efs1
10
30.3
57
33.3
2
28.6
55
32.2
18
25.4
6
40.0
31
33.7
12
19.4
191
30.7
Efs2
9
27.3
21
12.3
2
28.6
29
17.0
17
23.9
3
20.0
13
14.1
9
14.5
103
16.6
Efs3
0
0.0
6
3.5
0
0.0
1
0.6
2
2.8
1
6.7
2
2.2
1
1.6
13
2.1
Efs4
0
0.0
3
1.8
0
0.0
8
4.7
0
0.0
0
0.0
1
1.1
1
1.6
13
2.1
Efs5
0
0.0
11
6.4
0
0.0
1
0.6
0
0.0
0
0.0
0
0.0
0
0.0
12
1.9
Efs6
0
0.0
2
1.2
0
0.0
1
0.6
2
2.8
1
6.7
3
3.3
3
4.8
12
1.9
Efs7
1
3.0
3
1.8
0
0.0
5
2.9
2
2.8
0
0.0
1
1.1
0
0.0
12
1.9
Efs8
0
0.0
3
1.8
0
0.0
2
1.2
3
4.2
0
0.0
1
1.1
2
3.2
11
1.8
Efs9
0
0.0
4
2.3
0
0.0
3
1.8
2
2.8
0
0.0
0
0.0
1
1.6
10
1.6
Other
13
39.4
60
35.1
3
42.9
65
38.0
25
35.2
4
26.7
39
42.4
32
51.6
241
38.7
NT
0
0.0
1
0.6
0
0.0
1
0.6
0
0.0
0
0.0
1
1.1
1
1.6
4
0.6
Total
33
100.0
171
100.0
7
100.0
171
100.0
71
100.0
15
100.0
92
100.0
62
100.0
622
100.0

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By PFGE, the 341 E. faecium isolates were classified into 73 pulsotypes from which 43 multilocus sequence types (STs) were identified. Five STs had more than 10 isolates (Table 2). The 2 major STs, ST203 (159 isolates) and ST17 (47 isolates) were isolated across Australia. ST341 (38 isolates) and ST252 (11 isolates) were isolated only in the eastern regions of Australia, and ST555 (34 isolates) was isolated in the western and central regions. Using eBURST, 89.1% (304/341 isolates) of E. faecium isolates, including the 5 major STs, were grouped into clonal complex (CC) 17. Van genes were identified in the 5 major STs and in ST80 and ST414. Although only 8.5% (4/47) of ST17 isolates harboured vanB, vanB genes were identified in 50.6% (79/153) of ST203 isolates. Other STs harbouring the vanB genes included ST341 (33/38), ST555 (2/34), ST252 (1/11), ST80 (2/6), ST414 (2/2), and a single non-CC17 isolate, ST863. Two CC17 STs harboured the vanA gene; ST341 and ST80.

Table 2: Number and proportion of major Enterococcus faecium multilocus sequence types, Australia, 2011, by state or territory
ACT NSW NT Qld SA Tas. Vic. WA Aus.
Type n % n % n % n % n % n % n % n % n %
The category type 'other' includes the 38 multilocus sequence types that had less than 10 isolates per sequence type.
Efm ST203
9
40.9
37
39.8
2
33.3
34
60.7
14
25.9
2
50.0
36
57.1
25
58.1
159
46.6
Efm ST17
3
13.6
19
20.4
0
0.0
7
12.5
2
3.7
2
50.0
7
11.1
7
16.3
47
13.8
Efm ST341
7
31.8
26
28.0
0
0.0
3
5.4
0
0.0
0
0.0
2
3.2
0
0.0
38
11.1
Efm ST555
0
0.0
0
0.0
3
50.0
0
0.0
27
50.0
0
0.0
0
0.0
4
9.3
34
10.0
Efm ST252
0
0.0
2
2.1
0
0
3
5.4
0
0.0
0
0.0
6
9.5
0
0.0
11
3.2
Other
3
13.6
9
9.7
1
16.7
9
16.0
11
20.4
0
0.0
12
19.1
7
16.3
52
15.2
Total
22
100.0
93
100.0
6
100.0
56
100.0
54
100.0
4
100.0
63
100.0
43
100.0
341
100.0

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Discussion

AESOP 2011 was the 1st ongoing sepsis program performed by AGAR, and was conducted primarily to determine the proportion of E. faecalis and E. faecium bacteraemia isolates demonstrating antimicrobial resistance, with particular emphasis on assessing susceptibility to penicillin and the glycopeptides and the distribution of different enterococcal clones. As this is the 1st year of an ongoing program, it is difficult to determine the public health significance of these results. We suggest these results should be used as a marker for future AESOPs.

Similar to the situation in the USA and in Europe,16,17 enterococcal bacteraemia in Australia, and notably bacteraemia caused by multidrug-resistant E. faecium, has become a significant problem. In the AESOP 2011 study, approximately 1 in 3 cases of enterococcal bacteraemia was due to E. faecium, of which 90.4% (339 of 375 episodes) were ampicillin resistant and 36.9% (126 of 341 episodes) harboured either vanA or vanB genes. However, unlike Europe and the USA, where vancomycin resistance in E. faecium has predominately been due to the acquisition of the vanA operon, almost all of the AESOP 2011 E. faecium blood culture isolates harbouring van genes carried the vanB operon (98.4%). Recent studies however, have demonstrated a significant presence of vanB E. faecium in both North America and Europe.18–20

VanB vancomycin resistant enterococci (VRE) is now more prevalent than vanA VRE in several European centres including Sweden, Spain and Germany,21–23 whilst recent Canadian national surveillance demonstrates vanB comprises 10% of their VRE.24 It is thought this increased occurrence of vanB-positive E. faecium in the Northern Hemisphere may be due to the increased use of antibiotics selecting enterococci and VRE as well as to methodological reasons (e.g. reduced European Committee on Antimicrobial Susceptibility Testing (EUCAST) MIC breakpoints for glycopeptides; increased use and sensitive performance of chromogenic VRE agars; increased use of molecular diagnostic assays).25 Twenty (16.1%) of the 124 vanB E. faecium isolates had a vancomycin MIC at or below the CLSI and the EUCAST susceptible breakpoint ( ≤4 mg/L) and would not have been identified using routine phenotypic antimicrobial susceptibility methods.

With the use of PFGE, both enterococcal species were shown to be very polyclonal, confirming the enormous plasticity of the enterococcal genome. The majority of E. faecium isolates formed part of CC17, a global hospital-derived lineage that has successfully adapted to hospital environments. CC17 is characteristically ampicillin and quinolone resistant and subsequent acquisition of vanA– or vanB-containing transposons by horizontal transfer in CC17 clones has resulted in VRE with pandemic potential.

The study has a number of limitations. Although achieving national coverage, the participating laboratories service only a minority of the Australian hospitalised population. Further, MIC assays for vancomycin and teicoplanin were performed by a commercial gradient diffusion method and not the standard reference broth microdilution method.

Conclusions

The AESOP 2011 study has shown though predominately caused by E. faecalis, enterococcal bacteraemia in Australia is frequently caused by ampicillin-resistant vanB E. faecium. Molecular typing characterised over 50% of E. faecalis isolates as 2 PFGE pulsotypes and almost 90% of E. faecium isolates as CC17 clones of which approximately half were ST203. Further studies of the enterococcal genome will contribute to our understanding of the evolution of enterococci in the hospital environment and assist in preventing their nosocomial transmission.

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Acknowledgements

We gratefully acknowledge Hui-leen Tan, Yung Ching Lee and Lynne Wilson from the Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine WA, Royal Perth Hospital; Frances O’Brien and Ka Yan Wong from the Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research, School of Biomedical Sciences, Curtin University; and the Western Australia Genome Resource Centre, Department of Clinical Immunology and Biochemical Genetics, Royal Perth Hospital for the molecular typing of enterococci.

Members of the AGAR in 2011 were:

Australian Capital Territory

Peter Collignon and Susan Bradbury, The Canberra Hospital

New South Wales

Tom Gottlieb and Graham Robertson, Concord Hospital

Miriam Paul and Richard Jones, Douglass Hanly Moir Pathology

James Branley and Donna Barbaro, Nepean Hospital

George Kotsiou and Peter Huntington, Royal North Shore Hospital

Colin MacLeod and Bradley Watson, Royal Prince Alfred Hospital

Iain Gosbell and Annabelle LeCordier, Liverpool Hospital

David Mitchell and Lee Thomas, Westmead Hospital

Northern Territory

Jann Hennessy and Rob Baird, Royal Darwin Hospital

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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 Sonali Coulter, Pathology Queensland Prince Charles Hospital

Joan Faoagali and Joel Douglas, Pathology Queensland Princess Alexandra Hospital

Jenny Robson and Georgia Peachey, Sullivan Nicolaides Pathology

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

Mhisti Rele and Kathy Wilcox, Launceston General Hospital

Louise Cooley and Rob Peterson, Royal Hobart Hospital

Victoria

Denis Spelman and Michael Huysmans, The Alfred Hospital

Benjamin Howden and Peter Ward, Austin Hospital

Tony Korman and Despina Kotsanas, Monash Medical Centre

Suzanne Garland and Gena Gonis, Royal Women’s Hospital

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

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Western Australia

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

Barbara Henderson and Ronan Murray, PathWest Laboratory Medicine, Queen Elizabeth II Hospital

Keryn Christiansen, Denise Daley and Geoffrey Coombs, PathWest Laboratory Medicine, Royal Perth Hospital

Victoria D’Abrera and Sindy Budalich, St John of God Pathology

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Author details

Dr Geoffrey W Coombs1,2

Ms Julie C Pearson2

Ms Denise A Daley3

Ms Tam Le1

Dr James O Robinson1,2

Dr Thomas Gottlieb4

Dr Benjamin P Howden5,6

Dr Paul DR Johnson5

Dr Catherine M Bennett7

Dr Timothy P Stinear6

Prof John D Turnidge8,9

  1. Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research, School of Biomedical Sciences, Curtin University, Perth, Western Australia
  2. Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine, WA, Royal Perth Hospital, Perth, Western Australia
  3. Australian Group on Antimicrobial Resistance, Royal Perth Hospital, Perth, Western Australia
  4. Department of Microbiology and Infectious Diseases, Concord Hospital, Concord, New South Wales
  5. Microbiology Department, Austin Health, Heidelberg, Victoria
  6. Department of Microbiology and Immunology, University of Melbourne, Melbourne, Victoria
  7. Population Health, Deakin University, Melbourne
  8. SA Pathology, Department of Microbiology and Infectious Diseases, Women’s and Children’s Hospital, North Adelaide, South Australia
  9. Departments of Pathology, Paediatrics and Molecular and Biomedical Sciences, University of Adelaide, Adelaide, South Australia

Corresponding author: Dr Geoffrey Coombs, Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research, School of Biomedical Sciences, Curtin University, Perth, Western Australia. Telephone: +61 8 9224 2446. Facsimile: +61 8 9224 1989. Email: Geoff.Coombs@curtin.edu.au

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