Geoffrey W Coombs, Graeme R Nimmo, Julie C Pearson, Peter J Collignon, Jan M Bell, Mary-Louise McLaws, Keryn J Christiansen, John D Turnidge for the Australian Group on Antimicrobial Resistance
Abstract
In 2011, the Australian Group on Antimicrobial Resistance (AGAR) conducted a period-prevalence survey of clinical Staphylococcus aureus isolated from hospital inpatients. Twenty-nine microbiology laboratories from all states and mainland territories participated. Specimens were collected more than 48 hours post-admission. Isolates were tested by Vitek2® antimicrobial susceptibility card (AST-P612 card). Nationally, the proportion of S. aureus that were methicillin-resistant S. aureus (MRSA) was 30.3%; ranging from 19.9% in Western Australia to 36.8% in New South Wales/Australian Capital Territory. Resistance to the non-ß-lactam antimicrobials was common except for rifampicin, fusidic acid, high-level mupirocin and daptomycin. No resistance was detected for vancomycin, teicoplanin or linezolid. Antibiotic resistance in methicillin susceptible S. aureus (MSSA) was rare apart from erythromycin (13.2%) and there was no resistance to vancomycin, teicoplanin or linezolid. Inducible clindamycin resistance was the norm for erythromycin resistant, clindamycin intermediate/susceptible S. aureus in Australia with 90.6% of MRSA and 83.1% of MSSA with this phenotype having a positive double disc diffusion test (D-test). The proportion of S. aureus characterised as being healthcare-associated MRSA (HA-MRSA) was 18.2%, ranging from 4.5% in Western Australia to 28.0% in New South Wales/Australian Capital Territory. Four HA-MRSA clones were characterised and 98.8% of HA-MRSA isolates were classified as either ST22-IV [2B] (EMRSA-15) or ST239-III [3A] (Aus-2/3 EMRSA). Multiclonal community-associated MRSA (CA-MRSA) accounted for 11.7% of all S. aureus. In Australia, regional variation in resistance is due to the differential distribution of MRSA clones between regions, particularly for the major HA-MRSA clone, ST239-III [3A] (Aus-2/3 EMRSA), which is resistant to multiple non-ß-lactam antimicrobials. Commun Dis Intell 2013;37(3):E210–E218.
Keywords: antimicrobial resistance surveillance; Staphylococcus aureus; hospital-onset infections; methicillin susceptible, methicillin resistant
Introduction
Staphylococcus aureus is a major pathogen in the hospital environment, causing a wide variety of infections that are associated with considerable mortality. Several studies have indicated that mortality is higher for patients infected with methicillin-resistant S. aureus (MRSA) than methicillin-susceptible S. aureus (MSSA)1–4 and that MRSA infections are associated with increased costs due to longer hospital stays and the need for treatment with costly antimicrobials.5–7
The Australian Group on Antimicrobial Resistance (AGAR) has undertaken antimicrobial resistance period-prevalence surveys in Australia since 1986.8 Hospital inpatient surveys have been conducted biennially since 2005.9 The objectives of the hospital inpatient survey was to determine the prevalence of antimicrobial resistance in clinical isolates of S. aureus throughout Australia in hospital inpatients admitted for 48 hours or more and to describe the molecular epidemiology of the MRSA isolates.
The findings of the 2011 AGAR hospital inpatients survey are presented in this report.
Methods
Twenty-nine laboratories from all states and territories participated in the 2011 S. aureus AGAR survey. In the Northern Territory and the Australian Capital Territory only 1 laboratory participated in each region and in Tasmania only 2 laboratories participated. To ensure institutional anonymity data were combined as follows: New South Wales with the Australian Capital Territory, Victoria with Tasmania, and Queensland with the Northern Territory.
From 1 July to 30 November 2011 each laboratory collected up to 100 consecutive S. aureus isolates from hospital inpatients (hospital stay greater than 48 hours at the time of specimen collection). Only 1 isolate per patient was tested. Each S. aureus isolate was judged to come from a potentially infected site. Each hospital laboratory only collected from one institution. The three private laboratories collected from the multiple institutions that they serviced.
Susceptibility methodology
All isolates were tested using the Vitek2® antimicrobial susceptibility card (AST-P612). All isolates with a penicillin minimum inhibitory concentration of ≤0.125 mg/L were screened for the presence of ß-lactamase using nitrocefin discs. To detect inducible clindamycin resistance a double disc diffusion test (D-test) was performed on all erythromycin resistant and clindamycin intermediate or susceptible S. aureus isolates. Clinical and Laboratory Standards Institute breakpoints10 were utilised for all antimicrobials excluding fusidic acid (http://www.eucast.org/clinical_breakpoints/). Isolates with an MIC in the intermediate resistance category have been called resistant in this report.
Epidemiological typing of methicillin-resistant Staphylococcus aureus
Of the 713 MRSA identified, 703 (98.6%) were referred to the Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research for epidemiological typing.
Electrophoresis of chromosomal DNA using a contour-clamped homogeneous electric field DRIII System (Bio-Rad Laboratories Pty Ltd) was performed as previously described11 on all MRSA isolates. Multilocus sequence typing (MLST) and SCCmec typing was performed as previously described12–14 on selected MRSA isolates.
PCR for the detection of Panton–Valentine leucocidin (PVL) determinants was performed as previously described15 on all MRSA isolates.
Methicillin-resistant Staphylococcus aureus nomenclature
MRSA clones were defined by the combination of the MLST and the SCCmec type.16 Clones were reported with their ST and SCCmec type followed by their colloquial name in parenthesis; e.g. ST22-IV [2B] (EMRSA-15). Clones were classified into 2 groups on the basis of previously published evidence; those implicated in healthcare-associated infection (HA-MRSA) and those implicated in community-associated infection (CA-MRSA).
Clones that diverged at no more than one of the 7 MLST loci were considered to belong to the same clonal complex. Double locus variants were included in the same clonal complex if the linking single locus variant was present in the MLST database (http://www.mlst.net/).
Statistical analysis
Differences between proportions were tested using a Chi-square test with alpha set at 5% and Fisher’s exact test for 95% confidence limits (GraphPad® Prism Software). Relative risk and 95% confidence intervals were calculated using VassarStats (http://vassarstats.net).
Results
There were 2,357 isolates included in the survey (Table 1). Skin and soft tissue infection specimens contributed the majority of isolates (70.5%) followed by respiratory specimens (17.1%). Blood culture isolates contributed 6.5% of the total. Significantly (P<0.0001) more isolates caused non-invasive (91.3%) than invasive (8.7%) infections (Table 2).
| Region | Number of institutions | Number of isolates | Per cent of total |
|---|---|---|---|
NSW/ACT |
8 |
639 |
27.1 |
Qld/NT |
7 |
591 |
25.1 |
SA |
3 |
254 |
10.8 |
Vic/Tas |
7 |
541 |
22.9 |
WA |
4 |
332 |
14.1 |
Total |
29 |
2,357 |
100.0 |
| Specimen site | Number of isolates | Per cent of total | 95%CI |
|---|---|---|---|
| * Blood/cerebrospinal fluid/sterile body cavity | |||
Skin and soft tissue |
1,661 |
70.5 |
68.6–72.3 |
Respiratory |
404 |
17.1 |
15.6–18.7 |
Blood |
153 |
6.5 |
5.5–7.6 |
Urine |
88 |
3.7 |
3.0–4.6 |
Sterile body cavity |
49 |
2.1 |
1.5–2.7 |
Cerebrospinal fluid |
2 |
0.1 |
0.01–0.3 |
Total |
2,357 |
100.0 |
|
Invasive* |
204 |
8.7 |
7.5–9.9 |
Non-invasive |
2,153 |
91.3 |
90.1–92.4 |
Methicillin-resistant Staphylococcus aureus
The proportion of S. aureus isolates that were MRSA was 30.3% nationally (Table 3) with significantly different (P<0.0001) proportions across Australia ranging from 19.9% in Western Australia to 36.8% in New South Wales/Australian Capital Territory. The proportion of S. aureus isolates that were MRSA at each institution ranged from 7% to 56%. The proportion of invasive S. aureus that were MRSA (30.9%) was not significantly higher than for non-invasive isolates (30.2%) (P=1). The proportion of MRSA isolated in the 5 sites of infection was similar (P=0.24) with MRSA ranging from 29.0% in skin and soft tissue infections to 36.4% in urine (Table 4). MRSA was not isolated from cerebrospinal fluid specimens.
| Region | All isolates | Invasive isolates* | Non-invasive isolates | ||||||
|---|---|---|---|---|---|---|---|---|---|
| n/N | % | 95%CI | n/N | % | 95%CI | n/N | % | 95%CI | |
| * Blood/cerebrospinal fluid/sterile body cavity | |||||||||
NSW/ACT |
235/639 |
36.8 |
33.1–40.6 |
29/65 |
44.6 |
33.2–56.7 |
206/574 |
35.9 |
32.1–39.9 |
Qld/NT |
180/591 |
30.5 |
26.9–34.3 |
11/41 |
26.8 |
15.7–41.9 |
169/550 |
30.7 |
27.0–34.7 |
SA |
55/254 |
21.7 |
17.0–27.1 |
10/28 |
35.7 |
20.7–54.2 |
45/226 |
19.9 |
15.2–25.6 |
Vic/Tas |
177/541 |
32.7 |
28.9–36.8 |
9/42 |
21.4 |
11.7–35.9 |
168/499 |
33.7 |
29.7–37.9 |
WA |
66/332 |
19.9 |
15.9–24.5 |
4/28 |
14.3 |
5.7–31.5 |
62/304 |
20.4 |
16.2–25.3 |
Aus |
713/2,357 |
30.3 |
28.4–32.1 |
63/204 |
30.9 |
24.9–37.5 |
650/2,153 |
30.2 |
28.3–32.2 |
| All Isolates | |||
|---|---|---|---|
Site of infection |
n/N | % | 95%CI |
Skin and soft tissue |
482/1,661 |
29.0 |
26.8–31.3 |
Respiratory |
136/404 |
33.7 |
29.1–38.5 |
Blood/cerebrospinal fluid |
46/155 |
29.7 |
22.6–37.5 |
Urine |
32/88 |
36.4 |
26.4–46.7 |
Sterile body cavity |
17/49 |
34.7 |
17.0–49.6 |
Amongst the MRSA isolates, resistance to the non-ß-lactam antimicrobials was common except for fusidic acid, rifampicin, high-level resistance to mupirocin and daptomycin, where resistance was below 4% nationally (Table 5). Resistance was not detected for vancomycin, teicoplanin or linezolid. Resistance levels varied significantly between regions with Victoria/Tasmania having the highest proportions for the top 6 antimicrobials.
| NSW/ACT (n=235) |
Qld/NT (n=180) |
SA (n=55) |
Vic/Tas (n=177) |
WA (n=66) |
Aus (n=713) |
Differences across regions | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Drug |
n | % | n | % | n | % | n | % | n | % | n | % | X2 | P |
| * Constitutive resistance † High-level resistance | ||||||||||||||
Erythromycin |
164 |
69.8 |
103 |
57.2 |
28 |
50.9 |
131 |
74.0 |
30 |
45.5 |
456 |
64.0 |
28.63 |
<0.0001 |
Clindamycin* |
89 |
37.9 |
43 |
23.9 |
10 |
18.2 |
68 |
38.4 |
2 |
3.0 |
212 |
29.7 |
42.82 |
<0.0001 |
Tetracycline |
91 |
38.7 |
59 |
32.8 |
12 |
21.8 |
76 |
42.9 |
1 |
1.5 |
239 |
33.5 |
43.66 |
<0.0001 |
Co-trimoxazole |
87 |
37.0 |
50 |
27.8 |
11 |
20.0 |
69 |
39.0 |
2 |
3.0 |
219 |
30.7 |
37.54 |
<0.0001 |
Ciprofloxacin |
188 |
80.0 |
85 |
47.2 |
34 |
61.8 |
150 |
84.7 |
20 |
30.3 |
477 |
66.9 |
115.7 |
<0.0001 |
Gentamicin |
85 |
36.2 |
58 |
32.2 |
7 |
12.7 |
66 |
37.3 |
1 |
1.5 |
217 |
30.4 |
42.07 |
<0.0001 |
Fusidic acid |
5 |
2.1 |
12 |
6.7 |
1 |
1.8 |
6 |
3.4 |
2 |
3.0 |
26 |
3.6 |
6.844 |
0.14 |
Rifampicin |
3 |
1.3 |
7 |
3.9 |
0 |
0.0 |
3 |
1.7 |
1 |
1.5 |
14 |
2.0 |
5.279 |
0.26 |
Mupirocin† |
4 |
1.7 |
5 |
2.8 |
0 |
0.0 |
0 |
0.0 |
0 |
0.0 |
9 |
1.3 |
7.492 |
0.11 |
Daptomycin |
0 |
0.0 |
2 |
1.1 |
0 |
0.0 |
0 |
0.0 |
0 |
0.0 |
2 |
0.3 |
5.939 |
0.20 |
Methicillin-susceptible Staphylococcus aureus
Resistance to non-ß-lactams amongst MSSA was rare apart from resistance to erythromycin (13.2% nationally) (Table 6). Resistance was not detected for vancomycin, teicoplanin or linezolid. Resistance levels between regions varied significantly for penicillin and high-level mupirocin. South Australia had the highest rate of resistance for penicillin and Queensland/Northern Territory was highest for high-level mupirocin. Multi-resistance was uncommon in MSSA (36/1,644 2.2%).
| NSW/ACT (n=404) |
Qld/NT (n=411) |
SA (n=199) |
Vic./Tas. (n=364) |
WA (n=266) |
Aus (n=1,644) |
Differences across regions | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Drug | n | % | n | % | n | % | n | % | n | % | n | % | X2 | P |
| * Constitutive resistance † High-level resistance | ||||||||||||||
Penicillin |
346 |
85.6 |
355 |
86.4 |
179 |
89.9 |
321 |
88.2 |
212 |
79.7 |
1,413 |
85.9 |
12.8 |
0.01 |
Erythromycin |
49 |
12.1 |
64 |
15.6 |
25 |
12.6 |
52 |
14.3 |
27 |
10.2 |
217 |
13.2 |
5.0 |
0.29 |
Clindamycin* |
10 |
2.5 |
8 |
1.9 |
3 |
1.5 |
9 |
2.5 |
7 |
2.6 |
37 |
2.3 |
1.0 |
0.91 |
Tetracycline |
13 |
3.2 |
9 |
2.2 |
2 |
1.0 |
13 |
3.6 |
9 |
3.4 |
46 |
2.8 |
4.3 |
0.37 |
Co-trimoxazole |
9 |
2.2 |
8 |
1.9 |
3 |
1.5 |
8 |
2.2 |
5 |
1.9 |
33 |
2.0 |
0.5 |
0.98 |
Ciprofloxacin |
15 |
3.7 |
12 |
2.9 |
5 |
2.5 |
15 |
4.1 |
8 |
3.0 |
55 |
3.3 |
1.6 |
0.81 |
Gentamicin |
5 |
1.2 |
7 |
1.7 |
1 |
0.5 |
3 |
0.8 |
2 |
0.8 |
18 |
1.1 |
1.1 |
0.29 |
Fusidic Acid |
11 |
2.7 |
24 |
5.8 |
8 |
4.0 |
3 |
0.8 |
9 |
3.4 |
55 |
3.3 |
1.8 |
0.18 |
Rifampicin |
0 |
0.0 |
0 |
0.0 |
1 |
0.5 |
0 |
0.0 |
0 |
0.0 |
1 |
0.1 |
7.3 |
0.12 |
Mupirocin† |
3 |
0.7 |
20 |
4.9 |
0 |
0.0 |
0 |
0.0 |
3 |
1.1 |
26 |
1.6 |
4.2 |
0.04 |
Daptomycin |
1 |
0.2 |
0 |
0.0 |
0 |
0.0 |
0 |
0.0 |
0 |
0.0 |
1 |
0.1 |
3.1 |
0.55 |
Inducible clinidamycin resistance
Overall, 348 of the 2,357 isolates (14.8%) were erythromycin resistant and clindamycin intermediate/susceptible S. aureus isolates. Of these, 306 (87.9%) were D-test positive indicating inducible clindamycin resistance. For MRSA the number that were D-test positive was 203/224 (90.6%) and for MSSA 103/124 (83.1%).
Molecular typing
Based on molecular typing, of the 703 MRSA referred to ACCESS Typing and Research, 428 (60.9%) and 275 (39.1%) were classified as HA-MRSA and CA-MRSA strains respectively.
Healthcare-associated methicillin-resistant Staphylococcus aureus
Throughout Australia the percentage of S. aureus characterised as HA-MRSA was 18.2% ranging from 4.5% in Western Australia to 28.0% in the New South Wales/Australian Capital Territory region (Figure).
Figure: Percentage of Staphylococcus aureus characterised as HA-MRSA and CA-MRSA strains, by region
Text version of Figure (TXT 1 KB)
Four HA-MRSA clones were identified: ST22-IV [2B] (EMRSA-15) (49.5% of HA-MRSA); ST239-III [3A] (Aus-2/3 EMRSA) (49.3%); 3 isolates of ST5-II [2A] (New York Japan MRSA/USA100) and 2 isolates of ST36-II [2A] (EMRSA-16/USA200).
ST22-IV [2B] (EMRSA-15) has become the predominant HA-MRSA clone in Australia accounting for 30.2% of MRSA ranging from 15.6% in Queensland/Northern Territory to 40.2% in New South Wales/Australian Capital Territory (Table 7). ST22-IV [2B] are typically PVL negative, and 99% and 66% of these were resistant to ciprofloxacin and erythromycin respectively.
ST239-III [3A] (Aus-2/3 EMRSA) accounted for 30.0% of MRSA ranging from 0% in Western Australia to 36.2% in Victoria/Tasmania (Table 7). PVL negative ST239-III [3A] (Aus -2/3 EMRSA was typically resistant to tetracycline (100%), erythromycin (97%), ciprofloxacin (96%), cotrimoxazole (94%), and gentamicin (94%).
| NSW/ACT | Qld/NT | SA | Vic/Tas | WA | Aust | |
|---|---|---|---|---|---|---|
ST22-IV [2B] |
40.2% |
15.6% |
34.5% |
33.3% |
22.7% |
30.2% |
ST239-III [3A] |
35.8% |
31.3% |
18.2% |
36.2% |
0% |
30.0% |
Community-associated-methicillin-resistant Staphylococcus aureus
Throughout Australia the percentage of S. aureus characterised as CA-MRSA was 11.7% ranging from 7.8% in New South Wales/Australian Capital Territory to 16.1% in Queensland/Northern Territory. Thirty-two CA-MRSA clones were identified by pulsed field gel electrophoresis, corresponding to 25 MLST/SCCmec clones (Table 8). Overall, 79.6% of CA-MRSA were classified into 6 clones.
| Clone | Clonal complex | Alternative name | n | % | PVL Pos |
|---|---|---|---|---|---|
| Percentage figures in parenthesis relate to community-associated-methicillin-resistant Staphylococcus aureus isolates. PVL Panton–Valentine leucocidin. | |||||
ST1-IV [2B] |
1 |
WA-1 |
63 |
22.9 |
3 (4.8%) |
ST93-IV [2B] |
Singleton |
Queensland MRSA |
51 |
18.6 |
51 (100%) |
ST5-IV [2B] |
5 |
WA-3 |
34 |
12.4 |
2 (5.9%) |
ST78-IV [2B] |
88 |
WA-2 |
25 |
9.1 |
0 |
ST45-V [5C2] |
45 |
WA-84 (Vic CA-MRSA) |
25 |
9.1 |
0 |
ST30-IV [2B] |
30 |
SWP MRSA |
21 |
7.6 |
18 (85.7%) |
ST73-IV [2B] |
5 |
WA-65 |
10 |
3.6 |
0 |
ST8-IV [2B] |
8 |
USA300 |
8 |
2.9 |
8 (100%) |
ST772-V [5C2] |
1 |
Bengal Bay |
3 |
1.1 |
3 (100%) |
ST835-IV [2B] |
5 |
WA-48 |
3 |
1.1 |
0 |
ST45-V [5C2] |
45 |
WA-4 |
3 |
1.1 |
0 |
ST45-IV [2B] |
45 |
WA-75 |
3 |
1.1 |
0 |
ST1-V [5C2] |
1 |
2 |
0.7 |
0 |
|
ST5-V [5C2] |
5 |
WA-90 |
2 |
0.7 |
0 |
ST59-IV [2B] |
59 |
WA-15 |
2 |
0.7 |
0 |
ST72-IV [2B] |
72 |
WA-44 |
2 |
0.7 |
0 |
ST75-IV [2B] |
75 |
WA-8 |
2 |
0.7 |
0 |
ST45-V [5C2] |
45 |
2 |
0.7 |
0 |
|
ST188-IV [2B] |
1 |
WA-38 |
1 |
0.4 |
0 |
ST573-V [5C2] |
1 |
WA-10 |
1 |
0.4 |
1 (100%) |
ST5-V [5C2] |
5 |
WA-14 |
1 |
0.4 |
0 |
ST575-IV [2B] |
5 |
WA-25 |
1 |
0.4 |
0 |
ST5-V [5C2] |
5 |
WA-35 |
1 |
0.4 |
0 |
ST5-V [5C2] |
5 |
WA-108 |
1 |
0.4 |
0 |
ST5-V [5C2] |
5 |
WA-109 |
1 |
0.4 |
0 |
ST1756-V [5C2] |
5 |
1 |
0.4 |
0 |
|
ST7-V [5C2] |
7 |
1 |
0.4 |
0 |
|
ST45-IV [2B] |
45 |
WA-23 |
1 |
0.4 |
0 |
ST1970-V [5C2] |
45 |
WA-106 |
1 |
0.4 |
0 |
ST59-IV [2B] |
59 |
WA-55 |
1 |
0.4 |
1 (100%) |
ST1304-IV [2B] |
75 |
WA-72 |
1 |
0.4 |
0 |
ST953-IV [2B] |
97 |
WA-54 |
1 |
0.4 |
0 |
Total |
275 |
87 (31.6%) |
|||
ST1-IV [2B] (WA1) accounted for 9.0% of MRSA ranging from 3.5% in Victoria/Tasmania to 31.8% in Western Australia (Table 9). Typically PVL negative, 95.2% of isolates were non-multi-resistant. Eighty- nine per cent of isolates were resistant to the ß-lactam antimicrobials only or additionally to erythromycin (16%) or fusidic acid only (6%), or to both (8%). Two isolates were resistant to mupirocin, gentamicin and erythromycin, and a single isolate resistant to mupirocin, gentamicin and fusidic acid.
ST93-IV [2B] (Qld CA-MRSA) accounted for 7.3% of MRSA ranging from 1.7% in Victoria/Tasmania to 14.5% Queensland/Northern Territory (Table 9). PVL positive ST93-IV (Qld CA-MRSA) were typically resistant to the ß-lactams only (41/51) or additionally to erythromycin (10/51).
| NSW/ACT | Qld/NT | SA | Vic/Tas | WA | Aus | |
|---|---|---|---|---|---|---|
| ST1-IV [2B] | 4.8% |
11.2% |
9.1% |
3.5% |
31.8% |
9.0% |
| ST93-IV [2B] | 5.7% |
14.5% |
9.1% |
1.7% |
6.1% |
7.3% |
ST5-IV [2B] (WA3) and ST78-IV [2B] (WA2) although predominantly isolated in Western Australia (9.1% and 18.2% of MRSA respectively), were also isolated in most regions of Australia. ST45-V [5C2] (WA84) and ST30-IV [2B] (SWP MRSA) were predominantly isolated in Victoria/Tasmania (11.5% of MRSA) and Queensland/Northern Territory (8.4% of MRSA) respectively.
Overall, 92.7% of CA-MRSA were non-multi-resistant and 50.9% of isolates were resistant to ß-lactam antimicrobials only. However, 20 isolates (7.3% of CA-MRSA) were multiresistant including 3 PVL positive ST772-V [5C2] (Bengal Bay MRSA) isolates, which in addition to ß-lactam antimicrobials were resistant to gentamicin, erythromycin, ciprofloxacin and cotrimoxazole. One CA-MRSA (ST7-V [5C2]) isolate was resistant to 5 non-ß-lactam antimicrobials; gentamicin, erythromycin, ciprofloxacin, cotrimoxazole and tetracycline.
Panton–Valentine leucocidin
In 2011, 13.5% of MRSA were PVL positive. Eighty-seven (31.6%) CA-MRSA (Table 8) and 8 ST22-IV [2B] were PVL positive. PVL-positive CA-MRSA clones included the international clones ST8-IV [2B] (USA300) and ST772-V [5C2] (Bengal Bay MRSA).
Discussion
This survey demonstrates that MRSA remains a significant burden in Australian hospitals. For 2011, the national proportion of S. aureus that were MRSA was 30.3%, which was not significantly different to the proportions seen in past AGAR hospital inpatient surveys (X2 for trend 0.7527, P=0.3856).9 Differences between regions in the 2011 survey were significant with South Australia and Western Australia having a lower proportion than other regions. Although the proportion of MRSA amongst the different specimen types was similar, the high proportion of MRSA in invasive isolates is of concern as MRSA bacteraemia is associated with increased mortality compared with MSSA.1–4
More than 60% of the MRSA in the 2011 study were resistant to erythromycin and ciprofloxacin, and more than 30% were resistant to tetracycline, co-trimoxazole and gentamicin. Regional differences were again common due to different MRSA clones circulating in Australia. Erythromycin and ciprofloxacin resistance was more widespread in this survey with at least 30% of MRSA with this profile in any region. Erythromycin and ciprofloxacin resistance is common in ST239-III [3A] (Aus 2/3 EMRSA) isolates but is also characteristic of ST22-IV [2B] (EMRSA-15). ST22-IV [2B] (EMRSA-15) is a frequently isolated HA-MRSA in Australia and was found in all regions. Resistance was not detected for vancomycin, teicoplanin or linezolid. Compared with previous AGAR hospital inpatient surveys, the proportion of MRSA resistant to erythromycin, clindamycin, tetracycline, co-trimoxazole, ciprofloxacin, gentamicin and rifampicin has decreased nationally with significant decreases in New South Wales/Australian Capital Territory and Victoria/Tasmania. The proportion of S. aureus that are MRSA has remained stable in all regions and nationally. This finding is due to non-multi-resistant CA-MRSA increasing in Australian hospitals at the expense of the long-established multi-resistant ST239-III [3A].
Given that reports of outbreaks of CA-MRSA in Australian hospitals are thought to be rare17,18 it is likely that many infections in hospital inpatients are caused by the patients’ own colonising strains acquired prior to admission. Community clones such as PVL negative ST1-IV [2B] (WA1) and PVL positive ST93-IV [2B] (Qld CA-MRSA) are well established in Australia,19,20 and therefore it is important to monitor antimicrobial resistance patterns to MRSA over time as this information will guide therapeutic practices.
Acknowledgements
This study was primarily funded by a grant from the Australian Government Department of Health.
We gratefully acknowledge Hui-leen Tan, Lynne Wilson, Yung Lee, Denise Daley, Tam Le and Ka Yan Wong from the Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research; Frances O’Brien from the 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 MRSA.
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, South West Area Pathology Service
David Mitchell and Lee Thomas, Westmead Hospital
Northern Territory
Jann Hennessy and Rob Baird, 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 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, Alfred Hospital
Benjamin Howden and Peter Ward, Austin Hospital
Tony Korman and Despina Kotsanas, Monash Hospital Medical Centre
Sue Garland 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
Barbara Henderson and Ronan Murray, PathWest Laboratory Medicine, WA Queen Elizabeth II Hospital
Keryn Christiansen and Geoffrey Coombs, PathWest Laboratory Medicine, WA Royal Perth Hospital
Victoria D’Abrera and Sindy Budalich, St John of God Pathology
Author details
Dr Geoffrey W Coombs1,2
Prof Graeme R Nimmo3
Ms Julie C Pearson1,2
Prof Peter J Collignon4
Ms Jan M Bell5
Prof Mary-Louise McLaws6
Prof Keryn J Christiansen1,2
Prof John D Turnidge5
- Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research, School of Biomedical Sciences, Curtin University, Perth, Western Australia
- Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine, WA, Royal Perth Hospital, Perth, Western Australia
- Division of Microbiology, Pathology Queensland Central Laboratory, Herston Hospitals Campus, Herston, Queensland
- Infectious Diseases Unit and Microbiology Department, The Canberra Hospital, Garran, Australian Capital Territory
- Department of Microbiology and Infectious Diseases SA Pathology, Women’s and Children’s Hospital, North Adelaide, South Australia
- Healthcare Associated Infection and Infectious Diseases Control, University of New South Wales, Sydney, New South Wales
Corresponding author: Dr Geoffrey Coombs, Australian Collaborating Centre for Enterococcus and Staphylococcus Species (ACCESS) Typing and Research, School of Biomedical Sciences, Curtin University, PERTH WA 8000. Telephone: +61 8 9224 2446. Facsimile: +61 8 9224 1989. Email: Geoff.Coombs@curtin.edu.au
References
- Whitby M, McLaws ML, Berry G. Risk of death from methicillin-resistant Staphylococcus aureus bacteraemia: a meta-analysis. Med J Aust 2001;175(5):264–267.
- Lawes T, Edwards B, Lopez-Lozano JM, Gould I. Trends in Staphylococcus aureus bacteraemia and impacts of infection control practices including universal MRSA admission screening in a hospital in Scotland, 2006–2010: retrospective cohort study and time-series intervention analysis. BMJ Open 2012;2(3): pii: e000797.
- Hanberger H, Walther S, Leone M, Barie PS, Rello J, Lipman J, et al. Increased mortality associated with methicillin-resistant Staphylococcus aureus (MRSA) infection in the intensive care unit: results from the EPIC II study. Inter J Antimicrob Agents 2011;38(4):331–335.
- de Kraker ME, Wolkewitz M, Davey PG, Koller W, Berger J, Nagler J, et al. Clinical impact of antimicrobial resistance in European hospitals: excess mortality and length of hospital stay related to methicillin-resistant Staphylococcus aureus bloodstream infections. Antimicrob Agents Chemother 2011;55(4):1598–1605.
- Cosgrove SE, Qi Y, Kaye KS, Harbarth S, Karchmer AW, Carmeli Y. The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: mortality, length of stay, and hospital charges. Infect Cont Hosp Epidemiol 2005;26(2):166–174.
- Anderson DJ, Kaye KS, Chen LF, Schmader KE, Choi Y, Sloane R, et al. Clinical and financial outcomes due to methicillin resistant Staphylococcus aureus surgical site infection: a multi-center matched outcomes study. PloS one 2009;4(12):e8305.
- Rubio-Terres C, Garau J, Grau S, Martinez-Martinez L. Cost of bacteraemia caused by methicillin-resistant vs. methicillin-susceptible Staphylococcus aureus in Spain: a retrospective cohort study. Clin Microbiol Infect 2010;16(6):722–728.
- Nimmo GR, Bell JM, Collignon PJ. Fifteen years of surveillance by the Australian Group for Antimicrobial Resistance (AGAR). Commun Dis Intell 2003;27 Suppl:S47–S54.
- Nimmo GR, Pearson JC, Collignon PJ, Christiansen KJ, Coombs GW, Bell JM, et al. Antimicrobial susceptibility of Staphylococcus aureus isolated from hospital inpatients, 2009: report from the Australian Group on Antimicrobial Resistance. Commun Dis Intell 2011;35(3):237–243.
- CLSI. Performance standards for antimicrobial susceptibility testing. Twenty-second informational supplement M100-S22. Villanova, PA, USA 2012.
- O’Brien FG, Udo EE, Grubb WB. Contour-clamped homogeneous electric field electrophoresis of Staphylococcus aureus. Nat Protoc 2006;1(6):3028–3033.
- Goh SH, Byrne SK, Zhang JL, Chow AW. Molecular typing of Staphylococcus aureus on the basis of coagulase gene polymorphisms. J Clin Microbiol. 1992;30(7):1642–1645.
- Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 2000;38(3):1008–1015.
- Coombs GW, Monecke S, Ehricht R, Slickers P, Pearson JC, Tan HL, et al. Differentiation of clonal complex 59 community-associated methicillin-resistant Staphylococcus aureus in Western Australia. Antimicrob Agents Chemother 2010;54(5):1914–1921.
- Fey PD, Said-Salim B, Rupp ME, Hinrichs SH, Boxrud DJ, Davis CC, et al. Comparative molecular analysis of community- or hospital-acquired methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 2003;47(1):196–203.
- Enright MC, Robinson DA, Randle G, Feil EJ, Grundmann H, Spratt BG. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc Natl Acad Sci U S A 2002;99(11):7687–7692.
- O’Brien FG, Pearman JW, Gracey M, Riley TV, Grubb WB. Community strain of methicillin-resistant Staphylococcus aureus involved in a hospital outbreak. J Clinical Microbiol 1999;37(9):2858–2862.
- Schlebusch S, Price GR, Hinds S, Nourse C, Schooneveldt JM, Tilse MH, et al. First outbreak of PVL-positive nonmultiresistant MRSA in a neonatal ICU in Australia: comparison of MALDI-TOF and SNP-plus-binary gene typing. Euro J Clini Microbiol Infect Dis 2010;29(10):1311–1314.
- Nimmo GR, Coombs GW. Community-associated methicillin-resistant Staphylococcus aureus in Australia. Inter J Antimicrob Agents 2008;31(5):401–410.
- Coombs GW, Goering RV, Chua KY, Monecke S, Howden BP, Stinear TP, et al. The molecular epidemiology of the highly virulent ST93 Australian community Staphylococcus aureus strain. PloS one 2012;7(8):e43037.
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