Abstract

The Australian Group for Antimicrobial Resistance conducted a survey of the prevalence of antimicrobial resistance in unique clinical isolates of Staphylococcus aureus from patients admitted to hospital for more than 48 hours. Thirty-two laboratories from all states and territories collected 2,908 isolates from 1 May 2005, of which 31.9% were methicillin-resistant Staphylococcus aureus (MRSA). The regional prevalence of MRSA varied significantly (P<0.0001) from 22.5% in Western Australia to 43.4% in New South Wales/Australian Capital Territory. Prevalence of MRSA from individual laboratories varied even more from 4% to 58%. This variation was explained in part by distribution of age with the risk of MRSA significantly (P<0.0001) increasing with age. Other unmeasured factors including hospital activity and infection control practices in the individual institution may have also contributed. Further investigation is warranted as reductions in prevalence would reduce morbidity, mortality and healthcare costs. Commun Dis Intell 2007;31:288–296.

Keywords: Staphylococcus aureus, MRSA, healthcare-acquired infection, antimicrobial resistance

Top of page

Introduction

Staphylococcus aureus remains a major bacterial pathogen and is associated with considerable morbidity and mortality. Manifestations of S. aureus infection range from mild to moderate skin and soft tissue infections such as impetigo and furunculosis to invasive and often life threatening infections such as osteomyelitis, necrotising pneumonia and infective endocarditis. Bacteraemia is also common. In the pre-antibiotic era the mortality of staphylococcal bacteraemia was as high as 90%.¹ With antibiotic treatment, mortality has fallen but remains a major issue. With methicillin-sensitive S. aureus (MSSA) the median associated mortality is 25% (range 4%–52%) while with methicillin-resistant S. aureus (MRSA) the median is 35% (range 0%–83%).² In Australia, as in most of the world, antimicrobial resistance in S. aureus is a major impediment to effective treatment. Hospital strains are frequently resistant to methicillin (and all other beta-lactams) and multiple other antimicrobials.³

Methicillin-resistant S. aureus was first reported in Australia in 1968.⁴ This archaic strain of MRSA was not usually resistant to other non-beta-lactam antimicrobials and was not resistant to gentamicin. The emergence of MRSA resistant to gentamicin and other classes of antimicrobials was first noted in eastern Australia in 1976. Outbreaks of hospital infection due to multi-resistant MRSA (mMRSA) occurred in the state of Victoria in the late 1970s and early 1980s.^5,6 mMRSA became endemic in hospitals in the eastern Australian states in the late 1980s and 1990s with some spread to hospitals in South Australia, the Northern Territory and Tasmania.^3,7 However, these strains did not become established in Western Australian hospitals due to active screening and infection control policies.^3,8 Eastern Australian MRSA has now been shown to be one clone by multi-locus sequence typing – ST239-MRSA-III.⁹ This is one of the most successful MRSA clones and is now found extensively in Europe, Asia, and South America. More recently, MRSA clones of overseas origin have also been found in Australia. Most notably the United Kingdom strain, EMRSA-15, has spread widely in Australia to become a major endemic cause of hospital sepsis.⁹

Vancomycin has been the mainstay of treatment for serious infections due to MRSA. However, there is evidence that vancomycin is less effective in the treatment of methicillin-sensitive S. aureus than anti-staphylococcal beta-lactams.^10,11 Failure of vancomycin treatment of MRSA has been associated with the emergence of strains with MICs to vancomycin in the intermediate range (VISA).^12,13 These strains have been described in many parts of the world including Australia.¹⁴ Isolation of VISA follows failure of prolonged treatment with vancomycin. One recent study has suggested that treatment failure is related to slightly higher vancomycin MICs (1.0–2.0 mg/L versus ≤0.5 mg/L) in pre-treatment isolates of MRSA.¹⁵ Few treatment options remain for multi-resistant MRSA and resistance to linezolid, one of the few new anti-staphylococcal agents of recent years, is already being reported.¹⁶

While it is well known that S. aureus is a major cause of severe sepsis, few population based estimates of its incidence or prevalence are available. A recent Australian survey of S. aureus bacteraemia from 1999 to 2002 documented 3,129 episodes.² Approximately 51% of bacteraemic episodes had their onset in hospitals. MRSA caused 40% of hospital-onset and 12% of community-onset episodes. The authors estimated that approximately 6,900 episodes of S. aureus bacteraemia occur in Australia annually. This equates to 35 episodes per 100,000 population. Meta-analysis of the outcomes of S. aureus bacteraemia has shown that the relative risk of death due to MRSA bacteraemia is approximately twice that due to MSSA.^17,18 It is widely acknowledged that nosocomial MRSA infection represents an additional burden of disease not just replacement of MSSA infection.¹⁹ The cost of these additional infections is substantial for hospitals, patients and society. While costs vary from country to country, annual additional hospital costs due to MRSA in the United States of America are estimated at between US$1.5 billion and US$4.2 billion.¹⁹ In Australia, the additional hospital costs associated with nosocomial S. aureus bacteraemia alone are estimated at approximately $150 million.² Effective infection control measures have been shown to reduce nosocomial infection significantly and to result in substantial savings.¹⁹

The objective of this study 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.

Top of page

Methods

Thirty-two laboratories from all six states, the Australian Capital Territory and the Northern Territory participated in the S. aureus Australian Group for Antimicrobial Resistance (AGAR) survey. From 1 May 2005, each laboratory collected up to 100 consecutive significant clinical isolates from hospital inpatients (hospital stay >48 hours at the time of specimen collection). Only one isolate per patient was tested and no isolates from screening swabs were included. If S. aureus was isolated from more than one site, then the isolate from the most significant clinical site was tested. Specimens received for the purpose of gathering surveillance data were excluded.

Species identification

S. aureus was identified by morphology and positive results of at least two of three tests: slide coagulase test, tube coagulase test, and demonstration of deoxyribonuclease production.²⁰ Additional tests such as fermentation of mannitol or growth on mannitol-salt agar may have been performed for confirmation.

Susceptibility testing methodology

Participating laboratories performed antimicrobial susceptibility tests using the Vitek2® AST-P545 card (BioMerieux, Durham, NC). Antimicrobials tested were benzylpenicillin, oxacillin, cefazolin, vancomycin, rifampicin, fusidic acid, gentamicin, erythromycin, clindamycin, tetracycline, trimethoprim/sulphamethoxazole (cotrimoxazole), ciprofloxacin, quinupristin/dalfopristin (Synercid®), teicoplanin, linezolid, imipenem, and nitrofurantoin. Results were interpreted for non-susceptibility according to CLSI breakpoints.^22,23 Penicillin susceptible strains were tested for β-lactamase production using nitrocefin. A cefoxitin disc diffusion test was used to confirm methicillin-resistance. Mupirocin and cefoxitin were tested by disc diffusion using the CLSI or CDS methods.^21–23 The minimum inhibitory concentration (MIC) of mupirocin resistant isolates was determined by Etest® (AB Biodisk, Solna, Sweden). The macro Etest® method was used to determine hetero-resistance to vancomycin.

Statistical analysis

The proportions and 95%confidence intervals (CI) were calculated for MRSA by laboratory, state or territory, age, source, invasiveness of infection (blood, sterile site or cerebrospinal fluid isolates) and antibiogram. Odds ratio for the association of age and MRSA was examined after age of patient was categorised into one of five age groups. All descriptive and inferential statistics were calculated using Epi Info version 6.0.4 (Centers for Disease Control and Prevention, Atlanta, Ga, USA) with the alpha level set at the 5% level for two-sided tests for significance.

Top of page

Results

Participating laboratories (27 public and 5 private) were located in New South Wales (8), the Australian Capital Territory (1), Queensland (6), Victoria (6), Tasmania (2), the Northern Territory (1), South Australia (4) and Western Australia (4). To ensure institutional anonymity data were combined for New South Wales and the Australian Capital Territory; Tasmania and Victoria; and Queensland and the Northern Territory (Table 1). There were 2,908 isolates included in the survey with the majority (76.1%) of isolates contributed by New South Wales/Australian Capital Territory (28.4%), Victoria/Tasmania (24.9%) and Queensland/ Northern Territory (22.8%).

Table 1. Isolates by region

Region	Number of Institutions	Total	% 95%CI
New South Wales/Australian Capital Territory	9	825	28.4 (26.7–30.0)
Queensland/Northern Territory	7	664	22.8 (21.3–24.4)
South Australia	4	340	11.7 (10.5–12.9)
Victoria/Tasmania	8	724	24.9 (23.3–26.5)
Western Australia	4	355	12.2 (11.0–13.4)
Total	32	2,908	100

Specimen source

The majority of S. aureus isolates (67.6%) were from skin and soft tissue infections (Table 2). Respiratory specimens were the second most common source (17.4%) followed by blood culture isolates, 6.7%, with significantly (P<0.0001) more isolates causing non-invasive (91.2%) than invasive (8.7%) infections.

Table 2. Source of isolates

Specimen source	n	%
Skin and soft tissue	1,967	67.6
Respiratory	506	17.4
Blood	194	6.7
Urine	92	3.2
Eye	62	2.1
Sterile site	50	1.7
Ear	13	0.4
Cerebrospinal fluid	8	0.3
Other	11	0.4
Unknown	5	0.2
Total	2,908
Invasive	252	8.7
Non-invasive	2,651	91.2
Not specified	5	0.2

Top of page

Susceptibility results

Nationally, 31.9% of S. aureus isolates were MRSA (Table 3) with the proportion varying significantly between states and territories (X2 = 110.54, P<0.0001). The proportion of MRSA in New South Wales/Australian Capital Territory hospitals (43.4%) was significantly higher (P<0.001) than the Australian average of 31.9%. There was no significant difference in the proportion of MRSA isolates that caused invasive infections (20.0% to 41.2% respectively, P=0.267) while the proportion of non-invasive infections ranged from 22.8% in Western Australia to 43.7% in New South Wales/Australian Capital Territory (P<0.0001). There was a wide range in the proportions of MRSA isolated by institutions with 31.0%–58.0% in New South Wales/Australian Capital Territory, 19.0%–36.0% in Queensland/Northern Territory, 15.0%–29.0% in South Australia, 4.0%–53.5% in Victoria/Tasmania and 14.5%–29.2% in Western Australia (Table 4).

Table 3. Proportion of methicillin-resistant Staphylococcus aureus for all isolates, invasive isolates and non-invasive isolates, by region

	All Isolates		Invasive		Non-invasive
NSW/ACT	358/825	43.4%	35/85	41.2%	323/739	43.7%
Qld/NT	177/664	26.7%	13/36	36.1%	164/628	26.1%
SA	84/340	24.7%	10/34	29.4%	73/304	24.0%
Vic/Tas	229/724	31.6%	23/59	39.0%	206/664	31.0%
WA	80/355	22.5%	6/30	20.0%	74/325	22.8%
Aus	928/2,908	31.9%	87/244	35.7%	840/2,660	31.6%
Difference across regions χ2	81.01		5.20		78.81
P value	<0.0001		0.267		<0.0001

Table 4. Proportion of methicillin-resistant Staphylococcus aureus, by institution

Region	Laboratory code	% MRSA
NSW/ACT	1	31.0
	2	50.0
	3	31.3
	4	47.0
	5	58.0
	6	51.0
	7	38.5
	8	46.0
	9	34.0
Qld/NT	10	30.0
	11	19.0
	12	20.0
	13	29.9
	28	23.2
	29	28.8
	30	36.0
SA	14	29.0
	15	29.0
	16	15.0
	17	27.5
Vic/Tas	18	4.0
	19	45.0
	20	23.1
	21	10.0
	22	43.0
	23	53.5
	31	35.0
	32	33.0
WA	24	14.5
	25	25.0
	26	22.0
	27	29.2
Australia		31.9

Resistance in MRSA to non-beta-lactam antimicrobials varied significantly between states with the exception of mupirocin (Table 5). Resistance with the widest range was identified for gentamicin (5.0% to 79.5%, P<0.0001), tetracycline (6.3% to 83.0%, P<0.0001), cotrimoxazole (7.5% to 80.8%, P<0.0001) and clindamycin (8.3% to 68.7%, P<0.0001). Resistance to ciprofloxacin was also common ranging from 42.5%–89.4% (P<0.0001). Resistance to fusidic acid across the states varied significantly (P=0.0023) with the highest proportion in South Australia (11.9%). There was no significant difference (P=0.713) in the low levels of mupirocin resistance. One isolate from Victoria/Tasmania had a quinupristin/dalfopristin MIC of >2 mg/L by broth micro-dilution and an Etest MIC of 6 mg/L. In addition, one result for quinupristin/dalfospristin was missing. One isolate from New South Wales/Australian Capital Territory had Vitek MIC results of 4 mg/L for vancomycin and teicoplanin (non-susceptible). The broth dilution MIC of both agents was 2 mg/L and the isolate was confirmed as a hetero-vancomycin intermediate S. aureus (hVISA) by the macro Etest method.

MSSA were generally susceptible to most non-beta-lactam antimicrobials with no significant difference in proportion across all regions with the exception of the level of resistance in tetracycline (P=0.0005) with New South Wales/Australian Capital Territory having the highest level at 3.6%, and gentamicin (P=0.0047) with Victoria/Tasmania having the highest level at 3.2% (Table 6).

Top of page

 

Table 5. Number and proportion non-susceptible methicillin-resistant Staphylococcus aureus isolates, by region

Region	Em		Cm*		Tc		Tmp-SXT		Cf		Gm		Fa		Mp
	n	%	n	%	n	%	n	%	n	%	n	%	n	%	n	%
NSW/ACT	309/357	86.6	193/281	68.7	247/358	69.0	251/358	70.1	320/358	89.4	250/358	69.8	13/358	3.6	12/358	3.4
Qld/NT	129/177	72.9	74/177	41.8	79/177	44.6	91/177	51.4	111/177	62.7	98/177	55.4	10/177	5.6	4/177	2.3
SA	51/84	60.7	7/84	8.3	30/84	35.7	27/84	32.1	46/84	54.8	28/84	33.3	10/84	11.9	1/84	1.2
Vic/Tas	207/229	90.4	94/228	41.2	190/229	83.0	185/229	80.8	202/229	88.2	182/229	79.5	4/229	1.7	6/229	2.6
WA	46/80	57.5	8/80	10.0	5/80	6.3	6/80	7.5	34/80	42.5	4/80	5.0	3/80	3.8	1/80	1.3
Aus	742/927	80.0	376/850	44.2	551/928	59.4	560/928	60.3	713/928	76.8	562/928	60.6	40/928	4.3	24/928	2.6
Difference across regions χ2	75.61		151.25		201.42		181.44		144.13		178.66		16.63		2.13
P value	<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		<0.0001		0.0023		0.713

Em: erythromycin, Cm: clindamycin, Tc: tetracycline, Tmp-SXT: trimethoprim/sulphamethoxazole, Cf: ciprofloxacin, Gm: gentamicin, Fa: fusidic acid, Mp: mupirocin

* Constitutive resistance.

Table 6. Number and proportion non-susceptible methicillin sensitive Staphylococcus aureus isolates, by region

Region	Pc		Em		Cm		Tc		Tmp-SXT		Cf		Gm		Fa		Mp
	n	%	n	%	n	%	n	%	n	%	n	%	n	%	n	%	n	%
NSW/ACT	405/467	86.7	60/467	12.8	8/448	1.8	17/467	3.6	12/467	2.6	18/466	3.9	5/467	1.1	13/467	2.8	4/467	0.9
Qld/NT	416/487	85.4	63/487	12.9	2/487	0.4	8/487	1.6	3/487	0.6	8/487	1.6	5/487	1.0	18/487	3.7	5/487	1.0
SA	219/256	85.5	22/256	8.6	3/256	1.2	7/256	2.7	3/256	1.2	6/256	2.3	2/256	0.8	7/256	2.7	2/256	0.8
Vic/Tas	406/495	82.0	66/495	13.3	8/495	1.6	25/495	5.1	8/495	1.6	10/495	2.0	16/495	3.2	18/495	3.6	6/495	1.2
WA	241/275	87.6	21/275	7.6	4/275	1.5	0/275	0.0	2/275	0.7	6/275	2.2	1/275	0.4	15/275	5.5	3/275	1.1
Aus	1,687/1,980	85.2	232/1,980	11.7	25/1,961	1.3	57/1,980	2.9	28/1,980	1.4	48/1,979	2.4	29/1,980	1.5	71/1,980	3.6	20/1,980	1.0
Difference across regions χ2	6.17		9.37		4.37		20.15		7.88		5.75		15.01		4.20		0.47
P value	0.187		0.052		0.358		0.0005		0.096		0.219		0.0047		0.379		0.977

Em: erythromycin, Cm: clindamycin, Tc: tetracycline, Tmp-SXT: trimethoprim/sulphamethoxazole, Cf: ciprofloxacin, Gm: gentamicin, Fa: fusidic acid, Mp: mupirocin

* Constitutive resistance.

Top of page

Relationship of age to methicillin-resistant Staphylococcus aureus prevalence

Patients with MRSA ranged in age from less than one year to 100 years, with a mean of 54.3 years. The distribution of age was skewed towards the elderly with the 25th percentile at 35 years, the 50th at 61 years and the 75th at 77 years. MSSA was significantly (P<0.0001) more common than MRSA in all five age groups; neonatal (<1–1 year), paediatric (2–16 years), adult (17–40 years), middle-age (41–61 years) and the older (62–100 years) (Table 7).

Table 7. Age by methicillin susceptibility of Staphylococcus aureus

Age	Total			MRSA			MSSA			Difference in isolates by age category (row)
	n	%	95% CI	n	Row %	Column %	n	Row %	Column %	χ2	P
0–1	264	9.1	8.1–10.2	17	6.4	1.8	247	93.6	12.5	400.76	<0.0001
2–16	132	4.5	3.8–5.4	29	22.0	3.1	103	78.0	5.2	82.97	<0.0001
17–40	426	14.7	13.4–16.0	113	26.5	12.2	313	73.5	15.8	187.79	<0.0001
41–61	642	22.1	20.6–23.6	207	32.2	22.3	435	67.8	22.0	161.94	<0.0001
62–100	1,443	49.6	47.8–51.5	562	38.9	60.6	881	61.1	44.5	1142.81	<0.0001
Total	2,907	100	–	928	31.9	100	1,979	68.1	100	103.96	<0.0001

When the relationship between mean age and proportion of MRSA in institutions was examined, a significant (P two tailed = 0.02), but weak linear trend (r = 0.4195), was identified (Figure 1). The sample sizes contributed by the member hospitals were small with a wide dispersion of the mean age (Figure 2) across the 32 facilities. However, when age was categorised into five ranges for the aggregated data from all hospitals and odds ratio of MRSA cases for each age group was examined against the youngest, MRSA was significantly more likely to occur in patients in successively older age groups compared with MSSA (Table 8). Advancing age is a strongly significant risk factor for acquisition with patients aged between 62 years and 100 years being 10.33 (P<0.0001) times more likely to have MRSA (not MSSA) compared with babies.

Figure 1. Relationship of mean age and proportion of methicillin-resistant Staphylococcus aureus for 32 institutions

Figure 2. Mean age compared with proportion of methicillin-resistant Staphylococcus aureus in participating institutions

Table 8. Risk of methicillin-resistant Staphylococcus aureus, by age groups

Age	Unadjusted Odds Ratio	95% CI	P	Adjusted Odds Ratio*	95%CI	P
0–1	1 (referent group)	–	–	1 (referent group)	–	–
2–16	4.09	2.06 – 8.16	<0.0001	4.25	2.22 – 8.11	<0.0001
17–40	5.25	2.99 – 9.32	<0.0001	5.72	3.22 – 9.85	<0.0001
41–61	6.91	4.02 – 12.04	<0.0001	7.37	4.36 – 12.46	<0.0001
62–100	9.27	5.49 – 15.86	<0.0001	10.33	6.21 – 17.10	<0.0001
	P<0.0001, χ2 for linearity = 119.729			* Adjusted for state and territories

Top of page

Discussion

Surveys conducted by AGAR from 1986 to 1999 included all consecutive clinical isolates of S. aureus during the survey period regardless of acquisition.^3,7,24 Participating laboratories did not need to acquire any additional information to distinguish between inpatients and outpatients and so an overall MRSA prevalence was derived. Compliance with methodology was a potential issue particularly in the early days of the surveys but this simple data collection was reliably achieved. It also allowed for comparison of results over a prolonged period. The advent of community strains of MRSA during the 1990s^25,26 however, led to interest in studying the prevalence of MRSA in outpatient infections alone. AGAR responded by conducting biennial outpatient surveys from 2000 onwards.^9,27 Since then evidence has emerged that strains that initially were acquired almost exclusively in the community were now being acquired in the health care setting with increasing frequency.²⁸ Therefore, in 2005 a survey of hospital-acquired S. aureus infection was undertaken. The results provide us with the first accurate estimates at a national level of the proportion of hospital-acquired S. aureus infection that are due to MRSA.

In this survey 2,908 isolates were collected in 32 laboratories covering all states and territories. Overall, 31.9% of isolates were MRSA. While there was a significant difference in the proportion of MRSA between regions (from 22.5% in Western Australia to 43.4% in New South Wales), this may have been due in part to different age distributions. The overall proportion of MRSA in invasive (mainly bacteraemia) isolates was similar to that of non-invasive isolates (35.7% and 31.6% respectively, P=0.195. The high proportion of MRSA in invasive isolates is of concern as MRSA bacteraemia is associated with increased mortality compared with MSSA.^17,18,31 Direct comparison with prevalence in other countries is difficult due to methodological differences. For example, the European surveillance system reports the proportion of MRSA in bacteraemia isolates in both inpatients and outpatients in 23 countries.³² Even so, the overall proportion in Europe in 2005 varied from 1.7% in Denmark to 55% in Malta. The Netherlands and the Scandinavian countries have been consistently able to keep MRSA at very low levels in their hospitals over long periods.

Resistance to non-beta-lactams in MRSA was common for erythromycin, clindamycin, tetracycline, cotrimoxazole, ciprofloxacin and gentamicin and varied considerably from region to region. This regional variability is due to the differential distribution of MRSA clones in the major cities. For example, ST239-MRSA-III (AUS-2 and AUS-3 strains), which is resistant to multiple non-beta-lactams including gentamicin, erythromycin and tetracycline, is endemic in the eastern states but is less common in Western Australia and South Australia. ST22-MRSA-IV (UK EMRSA-15), which is resistant to ciprofloxacin and often erythromycin but susceptible to all other non-beta-lactams, is more common in Western Australia as are other non-multi-resistant strains.^9,27 Resistance of MSSA to non-beta-lactam antimicrobials was uncommon except for erythromycin. There was little variability between regions in the low levels of resistance to other agents, with the exception of tetracycline and gentamicin. Once again this may be due to regional variations in the prevalence of strains of MSSA carrying different combinations of resistance genes.

The prevalence of MRSA isolates varied from 4.0% to 58.0% between institutions. The high levels in some institutions are a cause for concern given the increased mortality, morbidity and cost associated with MRSA infection.^19,33 While it is generally accepted that the prevalence of MRSA in an institution reflects the effectiveness of infection control practice,³⁴ it is also true that age is a risk factor or proxy for MRSA infection.³⁵ Analysis of the 2005 survey data confirmed that risk of MRSA did increase significantly with age (P<0.0001). There was also a weak association between mean age and proportion of MRSA in institutions. The weakness of the association was due in part to the low sample size resulting in variability in the mean age. Equally, other factors such as variability in activity, acuity and infection control practice may also have contributed. Given the marked variability in prevalence between institutions it seems unlikely that mean age alone could explain the difference. Until other risk factors have been accurately identified, the elderly should be considered to be at highest risk when developing strategies for the control of MRSA. The possibility of controlling MRSA in the health care setting was demonstrated quite early in Australia.⁸ There is now ample and consistent evidence that infection control strategies based on screening, isolation and decolonisation are successful and highly cost effective.¹⁹ The reasons for significant variability between regional and institutional prevalence of MRSA is worthy of further study. Reduction of MRSA infection in high prevalence institutions is likely to result in lower levels of morbidity and mortality and in lower health care costs.

A full detailed report of this study may be found under 'AMR surveillance' on the Australian Group on Antimicrobial Resistance website: http://www.antimicrobial-resistance.com/

Top of page

Acknowledgements

This study was fully supported by a grant from the Australian Government Department of Health and Ageing.

The AGAR participants were:

Joan Faoagali, Narelle George, QHPS, Royal Brisbane Hospital, Qld; Graeme Nimmo, Jacqueline Schooneveldt, QHPS, Princess Alexandra Hospital, Qld; Chris Coulter, Sonali Gribble, QHPS, Prince Charles Hospital, Qld; Dale Thorley, QHPS, Gold Coast Hospital, Qld; Enzo Binotto, Bronwyn Thomsett, QHPS, Cairns Hospital, Qld; Jenny Robson, Renee Bell, Sullivan Nicolaides Pathology, Qld; Peter Collignon, Susan Bradbury, The Canberra Hospital, ACT; John Ferguson, Jo Anderson, Hunter Area Pathology Service, NSW; Tom Gottlieb, Glenn Funnell, Concord Repatriation General Hospital, NSW; George Kotsiou, Clarence Fernandes, Royal North Shore Hospital, NSW; Richard Benn, Barbara Yan, Royal Prince Alfred Hospital, NSW; Iain Gosbell, Helen Ziochos, South Western Area Pathology Service, NSW; David Mitchell, Lee Thomas, Westmead Hospital, NSW; Samantha Ryder, James Branley, Nepean Hospital, NSW; Miriam Paul, Richard Jones, Douglass Hanly Moir Pathology, NSW; Denis Spelman, Clare Franklin, Alfred Hospital, Vic; Suzanne Garland, Gena Gonis, Royal Children's and Women's Hospitals, Vic; Mary Jo Waters, Linda Joyce, St Vincent's Hospital, Vic; Barrie Mayall, Peter Ward, Austin Health, Vic; John Andrew, Di Olden, Gribbles Pathology (Vic) Pty Ltd, Vic; Tony Korman, Despina Kotsanas, Monash Medical Centre, Vic; Alistair McGregor, Rob Peterson, Royal Hobart Hospital, Tas; Erika Cox, Kathy Wilcox, Launceston General Hospital, Tas; John Turnidge, Jan Bell, Women's and Children's Hospital, SA; Ivan Bastian, Rachael Pratt, Institute of Medical & Veterinary Science, SA; David Gordon, Hendrik Pruul, Flinders Medical Centre, SA; PC Lee, Barbara Koldej, Gribbles Pathology (SA), SA; Clay Gollege, Barbara Henderson, PathCentre, WA; Keryn Christiansen, Geoff Coombs, Julie Pearson, Royal Perth Hospital, WA; David McGechie, Graham Francis, Fremantle Hospital, WA; Sue Benson, Janine Fenton, St John of God Pathology, WA; Gary Lum, Paul Southwell, Royal Darwin Hospital, NT.

Top of page

Author details

Graeme R Nimmo, Director¹

Julie C Pearson, Scientific Officer for the Australian Group on Antimicrobial Resistance²

Peter J Collignon, Director³

Keryn J Christiansen, Director²

Geoffrey W Coombs, Principal Scientist²

Jan M Bell, Senior Scientist⁴

Mary-Louise McLaws, Director⁵

1. Division of Microbiology, Herston, Queensland

2. Department of Microbiology and Infectious Diseases, PathWest Laboratory Medicine WA, Royal Perth Hospital, Western Australia

3. Infectious Diseases Unit and Microbiology Department, The Canberra Hospital, Garran, Australian Capital Territory

4. Department of Microbiology and Infectious Diseases, Women's and Children's Hospital, North Adelaide, South Australia

5. Hospital Infection Epidemiology and Surveillance Unit, University of New South Wales, Sydney, New South Wales

Corresponding author: Assoc. Professor GR Nimmo, Division of Microbiology, Queensland Health Pathology Service – Central Laboratory, Block 7, Herston Hospitals Complex, HERSTON QLD 4029. Telephone: +61 7 3636 8050. Facsimile: +61 7 3636 1336. Email: Graeme_Nimmo@health.qld.gov.au .

Top of page

References

1. Smith IM, Vickers AB. Natural history of 338 treated and untreated patients with staphylococcal septicaemia (1936–1955). Lancet 1960;1:1318–1322.

2. Collignon P, Nimmo GR, Gottlieb T, Gosbell IB, Australian Group on Antimicrobial Resistance. Staphylococcus aureus bacteraemia, Australia. Emerg Infect Dis 2005;11:554–561.

3. Nimmo GR, Bell JM, Mitchell D, Gosbell IB, Pearman JW, Turnidge JD. Antimicrobial resistance in Staphylococcus aureus in Australian teaching hospitals 1989–1999. Microb Drug Resist 2003;9:155–160.

4. Rountree PM, Beard MA. Hospital strains of Staphylococcus aureus with particular reference to methicillin-resistant strains. Med J Aust 1968;2:1163–1168.

5. Pavillard R, Harvey K, Douglas D, Hewstone A, Andrew J, Collopy B, et al. Epidemic of hospital-acquired infection due to methicillin-resistant Staphylococcus aureus in major Victorian hospitals. Med J Aust 1982;1:451–454.

6. Perceval A, McLean AJ, Wellington CV. Emergence of gentamicin resistance in Staphylococcus aureus. Med J Aust 1976;2:74.

7. Turnidge JD, Nimmo GR, Francis G. Evolution of resistance in Staphylococcus aureus in Australian teaching hospitals. Australian Group on Antimicrobial Resistance. Med J Aust 1996;164:68–71.

8. Pearman JW, Christiansen KJ, Annear DI, Goodwin CS, Metcalf C, Donovan FP, et al. Control of methicillin-resistant Staphylococcus aureus (MRSA) in an Australian metropolitan teaching hospital complex. Med J Aust 1985;142:103–108.

9. Coombs GW, Nimmo GR, Bell JM, Huygens F, O'Brien FG, Malkowski MJ, et al. Genetic diversity among community methicillin-resistant Staphylococcus aureus strains causing outpatient infections in Australia. J Clin Microbiol 2004;42:4735–4743.

10. Chambers HF, Miller RT, Newman MD. Right-sided Staphylococcus aureus endocarditis in intravenous drug abusers: two-week combination therapy. Ann Intern Med 1988;109:619–624.

11. Levine DP, Fromm BS, Reddy BR. Slow response to vancomycin or vancomycin plus rifampin in methicillin-resistant Staphylococcus aureus endocarditis. Ann Intern Med 1991;115:674–680.

12. Hiramatsu K, Aritaka N, Hanaki H, Kawasaki S, Hosoda Y, Hori S, et al. Dissemination in Japanese hospitals of strains of Staphylococcus aureus heterogeneously resistant to vancomycin. Lancet 1997;350:1670–1673.

13. Hiramatsu K, Hanaki H, Ino T, Yabuta K, Oguri T, Tenover FC. Methicillin-resistant Staphylococcus aureus clinical strain with reduced vancomycin susceptibility. J Antimicrob Chemother 1997;40:135–136.

14. Ward PB, Johnson PD, Grabsch EA, Mayall BC, Grayson ML. Treatment failure due to methicillin-resistant Staphylococcus aureus (MRSA) with reduced susceptibility to vancomycin. Med J Aust 2001;175:480–483.

15. Sakoulas G, Moise-Broder PA, Schentag J, Forrest A, Moellering RC, Jr. Eliopoulos GM. Relationship of MIC and bactericidal activity to efficacy of vancomycin for treatment of methicillin-resistant Staphylococcus aureus bacteremia. J Clin Microbiol 2004;42:2398–2402.

16. Meka VG, Pillai SK, Sakoulas G, Wennersten C, Venkatarman L, DeGirolami PC, et al. Linezolid resistance in sequential Staphylococcus aureus isolates associated with a T2500A mutation in the 23S rRNA gene and loss of a single copy of rRNA. J Infect Dis 2004;190:311–317.

17. Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber MJ, Karchmer AW, Carmeli Y. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 2003;36:53–59.

18. Whitby M, McLaws ML, Berry G. Risk of death from methicillin-resistant Staphylococcus aureus bacteraemia: a meta-analysis. Med J Aust 2001;175:264–267.

19. Gould IM. Costs of hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) and its control. Int J Antimicrob Agents 2006;28:379–384.

20. Kloos WE, Bannerman TL. Staphylococcus and Micrococcus. In: Murray PR, Barron EJ, Pfaller MA, Tenover FC, Yolken RH, eds. Manual of Clinical Microbiology. 7th ed. Washington, D.C: ASM Press; 1999:264–282.

21. Bell SM, Gatus BJ, Pham JN, Rafferty DL. Antibiotic Susceptibility Testing by the CDS Method: A Manual for Medical and Veterinary Laboratories 2004. 3rd ed. Randwick, NSW: South Eastern Area Laboratory Services; 2004.

22. National Committee on Clinical Laboratory Standards. Performance standards for antimicrobial disk susceptibility tests. Approved standard, 8th ed. NCCLS document M2-A8. In. Wayne, Pa: National Committee on Clinical Laboratory Standards; 2003.

23. National Committee on Clinical Laboratory Standards. Performance standards for antimicrobial disk susceptibility testing. Fourteenth informational supplement. NCCLS document M100-514. Wayne, Pa: National Committee on Clinical Laboratory Standards; 2004.

24. Turnidge J, Lawson P, Munro R, Benn R. A national survey of antimicrobial resistance in Staphylococcus aureus in Australian teaching hospitals. Med J Aust 1989;150:65–72.

25. Collignon P, Gosbell I, Vickery A, Nimmo G, Stylianopoulos T, Gottlieb T. Community-acquired methicillin-resistant Staphylococcus aureus in Australia. Australian Group on Antimicrobial Resistance. Lancet 1998;352:146–147.

26. Riley TV, Pearman JW, Rouse IL. Changing epidemiology of methicillin-resistant Staphylococcus aureus in Western Australia. Med J Aust 1995;163:412–414.

27. Nimmo GR, Coombs GW, Pearson JC, O'Brien FG, Christiansen KJ, Turnidge JD, et al. Methicillin-resistant Staphylococcus aureus in the Australian community: an evolving epidemic. Med J Aust 2006;184:384–388.

28. Klevens RM, Edwards JR, Tenover FC, McDonald LC, Horan T, Gaynes R. Changes in the epidemiology of methicillin-resistant Staphylococcus aureus in intensive care units in US hospitals, 1992–2003. Clin Infect Dis 2006;42:389–391.

29. Collignon PJ, Bell JM, MacInnes SJ, Gilbert GL, Toohey M. A national collaborative study of resistance to antimicrobial agents in Haemophilus influenzae in Australian hospitals. The Australian Group for Antimicrobial Resistance (AGAR). J Antimicrob Chemother 1992;30:153–163.

30. Turnidge JD, Bell JM, Collignon PJ. Rapidly emerging antimicrobial resistances in Streptococcus pneumoniae in Australia. Pneumococcal Study Group. Med J Aust 1999;170:152–155.

31. Ellis MW, Hospenthal DR, Dooley DP, Gray PJ, Murray CK. Natural history of community-acquired methicillin-resistant Staphylococcus aureus colonization and infection in soldiers. Clin Infect Dis 2004;39:971–979.

32. EARSS interactive database. RIVM, 2005.Available from: http://www.rivm.nl/earss/database/ Accessed on 9 February 2007.

33. Cosgrove SE. The relationship between antimicrobial resistance and patient outcomes: mortality, length of hospital stay, and health care costs. Clin Infect Dis 2006;42 Suppl 2:S82–S89.

34. Herwaldt LA. Control of methicillin-resistant Staphylococcus aureus in the hospital setting. Am J Med 1999;106(5A):11S–8S; discussion 48S–52S. Review.

35. Doebbeling BN. The epidemiology of methicillin-resistant Staphylococcus aureus colonisation and infection. J Chemother 1995;7 Suppl 3:99–103. Review.