JOURNAL OF CLINICAL MICROBIOLOGY, Oct. 2010, p. 3470–3474 Vol. 48, No. 10 0095-1137/10/$12.00 doi:10.1128/JCM.00911-10 Copyright ? 2010, American Society for Microbiology. All Rights Reserved.
Incidence, Risk Factors, and Outcomes of Panton-Valentine
Staphylococcus aureus Infections in
Auckland, New Zealand
1213451S. Muttaiyah,* G. Coombs,S. Pandey,P. Reed,S. Ritchie,D. Lennon,and S. Roberts
1Department of Microbiology, Auckland City Hospital, Auckland, New Zealand; Department of Microbiology and Infectious Diseases,
PathWest Laboratory Medicine-WA, Royal Perth Hospital, and School of Pathology and Laboratory Medicine, University of 2Western Australia, Perth, Australia; Children’s Research Centre, Starship Children’s Health, Auckland City Hospital, 3Auckland, New Zealand; Department of Molecular Medicine and Pathology, University of Auckland, Auckland, 45New Zealand; and Community Paediatrics, University of Auckland, Auckland, New Zealand
Received 10 May 2010/Returned for modi？cation 1 June 2010/Accepted 28 July 2010
Panton-Valentine leukocidin (PVL) has been linked to invasive community-acquired methicillin-resistant Staph-
ylococcus aureusinfections. However, the association between disease and PVL-positive methicillin-susceptible Staphylococcus aureus (MSSA) has not been widely reported. We aimed to examine the epidemiology of PVL in
clinical MSSA isolates from patients presenting to Auckland City Hospital. Four hundred eleven MSSA clinical
isolates and 93 nasal carriage isolates were collected and tested for the presence of the lukSF-PV genes using PCR. The results were examined in light of host and disease factors. Multilocus sequence typing (MLST) was performed
on a random subset of isolates to ensure that there was no single PVL-positive MSSA clone responsible for disease
in Auckland. The prevalence of the lukSF-PV genes in MSSA isolates associated with disease (124/335; 37%) was not signi；cantly different from the prevalence of the lukSF-PV genes in MSSA nasal carriage isolates (29/93; 31% [P
0.33]). PVL-positive MSSA isolates in Auckland are genetically diverse and come from a number of different clonal
complexes. PVL-positive infections peaked at between 10 and 20 years of age, with a subsequent decline. Paci；c ethnicity, age, diagnosis of skin and soft tissue infection (SSTI), community-onset infection, and the need for
surgical intervention were found by multivariate analysis to be independently associated with PVL-positive MSSA
infection. More than one-third of MSSA infections in our patient population are caused by PVL-positive strains. Those patients with PVL-positive MSSA infection were more likely to be of Paci；c ethnicity, be younger in age, have
community-onset infection, have SSTI, and need surgical intervention.
Staphylococcus aureus is a nasal commensal that can be de- type IV and also SCCmec type V (4, 25). The epidemiology of PVL-positive methicillin-susceptible S. aureus (MSSA) has not tected in up to 20 to 30% of the general population, one-third of whom are persistently colonized (28). S. aureus produces a been reported as extensively, and the lukSF-PV genes are not exclusively linked to the presence of the SCCmec element. In wide variety of virulence factors that contribute to its ability to the 1950s MSSA ST80 strains, which were associated with colonize, invade, and evade the immune system, which includes outbreaks of SSTI, harbored the lukSF-PV genes (22). There Panton-Valentine leukocidin (PVL), a bicomponent, pore- forming toxin encoded by two contiguous genes, lukF-PV and have also been recent reports of PVL-positive MSSA causing lukS-PV. PVL can cause either neutrophil lysis or apoptosis clusters of SSTI and necrotizing pneumonia (5, 15). and contributes to tissue necrosis (25). PVL has been linked to The vast majority of S. aureus strains in New Zealand are skin and soft tissue infections (SSTIs), necrotizing pneumonia, methicillin susceptible (MSSA); the prevalence of methicillin- and bone and joint infections in humans (3, 11, 17). Rabbit and resistant S. aureus (MRSA) remains low, at about 5% (12). human leukocytes are highly sensitive to PVL-mediated leukocy- New Zealand has a high incidence of S. aureus disease; the tosis (18), and animal studies have shown that PVL causes more- incidence of S. aureus bacteremia in the late 1990s was 41 cases severe disease in dermonecrosis (7, 27), osteomyelitis (6), and per 100,000 adults per year (12). We aimed to examine the
necrotizing pneumonia models (B. A. Diep, L. Chan, and P. prevalence of the lukSF-PV genes in MSSA isolates responsi-
Tattevin, presented at the 49th Interscience Conference on An- ble for disease and asymptomatic nasal carriage, to determine
timicrobial Agents and Chemotherapy, San Francisco, CA, 2009). risk factors for infection with PVL-positive MSSA, and to
The presence of PVL has been extensively described for examine the association between PVL and severity of disease.
methicillin-resistant S. aureus (MRSA), speci？cally in associa- tion with staphylococcal cassette chromosome mec (SCCmec) MATERIALS AND METHODS Clinical MSSA isolates. All MSSA isolates isolated from diagnostic specimens * Corresponding author. Mailing address: Department of Microbi- submitted to the Microbiology Laboratory of Auckland City Hospital from Feb- ology, Auckland City Hospital, Private Bag 92026, Grafton, Auckland, ruary to April 2008 were collected. These specimens were generally obtained at New Zealand. Phone: 3074949, ext. 25985. Fax: 3074940. E-mail: the request of the attending physician, midwife, or district nurse for clinical email@example.com. reasons. Duplicate isolates from the same patient were excluded. The isolates Published ahead of print on 4 August 2010. were stocked onto nutrient agar (Difco Laboratories, Detroit, MI).
VOL. 48, 2010 PANTON-VALENTINE LEUKOCIDIN IN MSSA 3471
Nasal carriage isolates. MSSA isolates from nasal carriers were obtained from and Fisher’s exact tests, and the results were expressed in terms of odds ratios healthy population volunteers in the Auckland community during a separate (ORs) and associated 95% con？dence intervals (CIs). For continuous variables, study performed to examine the demographic features of nasal carriers in Auck- the differences between patient groups were investigated by the parametric t test land. These volunteers were recruited in public places spread across the Auck- or the nonparametric Wilcoxon rank sum test as appropriate. Multivariate anal- land region between February and November 2008; people with hospital contact yses were undertaken by using nominal logistic regression and effect likelihood in the previous 3 months were excluded. ratio tests, with signi？cance set at a P value of 0.05. Detection of the lukSF-PV genes. All isolates were cultured onto tryptic soy Ethical approval. The regional ethics committee of the New Zealand Ministry agar with 5% sheep blood (Difco Laboratories, Detroit, MI) and incubated of Health provided ethical approval for the study. aerobically overnight at 35?C. Nucleic acid was extracted from MSSA isolates as previously described (20). The PVL and nuc probes were synthesized with the non？uorescent quencher BHQ1 (Biosearch Technologies, CA). Cal Fluor Gold RESULTS 540 and FAM (6-carboxy？uorescein) were utilized as reporter dyes. Primers were synthesized based on oligonucleotide sequences described previously (20). MSSA isolates were obtained from 411 patients for whom Data for the duplex PCR (for the simultaneous ampli？cation of the lukSF-PV clinical details were available. The majority of the patients, genes and the nuc gene) were collected with an ABI 7500 real-time PCR system 335/411 (81.5%), had a clearly identi？able focus of infection; (Applied Biosystems, CA). Reactions were performed with 1 universal master 76/411 (18.5%) patients were not considered to have S. aureus mix (Applied Biosystems, CA) under the following thermal cycling conditions: 15 min at 95?C, followed by 40 cycles of 95?C for 15 s and 55?C for 1 min. Ampli- infection and were excluded from analysis. We also obtained ？cation was con？rmed by the generation of a sigmoid ampli？cation plot. A 93 MSSA isolates from nasal carriers for comparison. The negative control was provided by use of negative blanks and PCR blanks. prevalence of the lukSF-PV genes among the clinical MSSA MLST. In order to ensure that there was no single dominant PVL-positive isolates, 124/335 (37%), was not signi？cantly different from the MSSA clone that caused disease in Auckland, all of the lukSF-PV MSSA carriage prevalence of the lukSF-PV genes among the nasal carriage isolates were genotyped by using multilocus sequence typing (MLST) (9). A similar number of randomly selected lukSF-PV-positive clinical MSSA isolates isolates, 29/93 (31%) (P 0.33). MLST con？rmed that a were also genotyped. To assign a clonal complex (CC), sequences were com- diverse range of MSSA genotypes was PVL positive in Auck- pared with the sequences in the S. aureus MLST database (http://saureus.mlst land: the 29 lukSF-PV-positive nasal carriage isolates belonged .net/) (10). to eight clonal complexes (CC5, 9/29 isolates [31%]; CC30, Clinical data. Electronic clinical records were reviewed to ascertain the fol- lowing demographic data: patient age, gender, ethnicity, and place of domicile. 7/29 [24%]; CC1, 6/29 [21%]; CC22, 2/29 [7%]; CC78, 2/29 The NZDep2006 (New Zealand Deprivation 2006) score was calculated for each [7%]; CC15, 1/29 [3%]; CC97, 1/29 [3%]; CC121, 1/29 [3%]), patient; the NZDep2006 score is derived from population data for each neigh- and the 24 randomly selected lukSF-PV-positive clinical iso- borhood (23). This score ranges from 1 to 10, where 1 represents the least lates belonged to six clonal complexes (CC1, 12/24 isolates deprived areas of Auckland and 10 represents the most deprived areas of Auck- [50%]; CC121, 6/24 [25%]; CC30, 3/24 [13%]; CC5, 1/24 [4%]; land. The source of infection was also recorded. In order to evaluate potential risk factors associated with S. aureus disease, the following data were ascertained: CC8, 1/24 [4%]; CC78, 1/24 [4%]). Several predominant clonal community versus hospital onset, Charlson weighted index of comorbidity (16), complexes contained the majority of the lukSF-PV-positive the presence of an implanted medical device, recent trauma with breach of skin MSSA isolates: 88% of the clinical isolates belonged to three within 30 days, the presence of a noninfective chronic skin condition, or a predominant clonal complexes (CC1, CC30, and CC121), and history of alcoholism or intravenous drug use. Disease severity was measured by means of the following data: requirement for surgical intervention, num- 76% of the nasal carriage isolates belonged to three predom- ber of surgical procedures, bloodstream invasion, duration of admission, inant clonal complexes (CC1, CC5, and CC30). 30-day readmission rate, and 30-day mortality rate. The prevalences of PVL-positive MSSA for patients within De；nitions used. Skin and soft tissue infection was de？ned as the presence of each infection group were 112/235 (48%) with skin and soft a cutaneous abscess or other signs of in？ammation and a culture positive for tissue infection, 4/13 (31%) with bone and joint disease, 2/11 MSSA. Bone infection was de？ned as radiologic or surgical evidence of osteomyelitis (18%) with pneumonia, 2/36 (2%) with surgical-site infection, and MSSA-positive blood or aspirate culture. 1/13 (1%) with catheter-related infection, and 0/6 (0%) with Joint infection was de？ned as pain with, or limitation of, joint movement and primary bacteremia and endocarditis. Univariate analysis was MSSA-positive aspirate or blood cultures. performed to compare features of the PVL-positive MSSA Pneumonia was de？ned as the presence of fever with radiographic changes consistent with pneumonia and MSSA-positive sputum, tracheal aspirate, bron- infections (n 124) to the features of the PVL-negative MSSA chial washing, or blood cultures. infections (n 211) (Table 1). Histories of alcoholism and Surgical-site infection and catheter-related infection were de？ned in accor- intravenous drug use were excluded from Table 1, as they were dance with the criteria of the Australian Council of Healthcare Standards (1). not routinely documented in clinical records. Factors associ- Primary bacteremia was de？ned as the presence of a blood culture positive for ated with PVL-positive infections in the univariate analysis MSSA with no identi？able focus of infection. The diagnosis of endocarditis was based on modi？ed Dukes’ criteria (8). were investigated further by employing multivariate analysis. A Community-onset, not health care-associated, infections were de？ned as those diagnosis of SSTI, Paci？c ethnicity, younger age, community- episodes with an MSSA-positive culture within 48 h of admission without a onset infection, and need for surgical intervention were all history of a health care-associated risk factor. independently associated with the presence of a PVL-positive Community-onset, health care-associated infections were de？ned as those episodes with an MSSA-positive culture within 48 h of admission with a history MSSA infection. The incidence of PVL-positive MSSA infec- of a health care-associated risk factor. Health care-associated risk factors were as tions over the 2-month study period was 8.7 per 1,000 patients; follows: history of hospitalization in the past year, requirement for renal dialysis, it peaked for those individuals aged between 10 and 20 years, residence in a long-term care facility, and the presence of percutaneous medical at 15.4 per 1,000 patients, and steadily decreased to 0.77 per devices. 1,000 patients for those aged between 80 and 90 years (r Hospital-onset, health care-associated infections were de？ned as those epi- sodes with an MSSA-positive culture more than 48 h after admission to hospital. 0.79; P 0.01). The incidence of PVL-negative infections All other infections were classi？ed following review by an infectious disease showed no trend with age (r 0.20; P 0.60). physician. The majority of our MSSA infections, 232/335 (70%), pre- Statistical analysis. Data analyses were undertaken by using JMP 5.1 (SAS sented as SSTIs, and univariate analysis of this subset was Inc., NC) and StatsDirect 2.5.7 (StatsDirect Ltd., Cheshire, United Kingdom) performed to directly compare features of PVL-positive MSSA software. For categorical variables, analysis was performed by using chi-square
3472 MUTTAIYAH ET AL. J. CLIN. MICROBIOL.
TABLE 1. Univariate analysis of patients with PVL-positive MSSA infection versus PVL-negative MSSA infection
No. (%) of PVL- No. (%) of PVL- OR (95% CI) of PVL-positive P value of PVL-positive Patient characteristic positive patients negative patients compared to PVL-negative compared to PVL- (n 124) (n 211) patients negative patients
55 (44) 98 (46) 0.92 (0.59–1.44) 0.73 Female gender aEthnicity 41 (33) 116 (55) 0.40 (0.25–0.64) 0.0001 European Maori 22 (18) 22 (10) 1.85 (0.98–3.51) 0.09 Paci？c 50 (40) 46 (22) 2.42 (1.49–3.94) 0.0007 Asian 4 (3) 17 (8) 0.38 (0.13–1.16) 0.10 Other 7 (6) 10 (5) 1.20 (0.45–3.24) 0.14
aAge (yr),b 40 (33) 55 (26) 1.35 (0.83–2.20) 0.21 0–9 10–19 27 (22) 23 (11) 2.28 (1.24–4.18) 0.01 20–29 11 (9) 18 (9) 1.04 (0.48–2.29) 0.99 30–39 17 (14) 18 (9) 1.70 (0.84–3.44) 0.14 40–49 13 (11) 18 (9) 1.66 (0.59–2.66) 0.56 50–59 1 (1) 15 (7) 0.11 (0.11–0.81) 0.007 60–69 10 (8) 22 (11) 0.75 (0.34–1.65) 0.57 70–79 1 (1) 23 (11) 0.07 (0.01–0.50) 0.0003 80–89 1 (1) 16 (8) 0.10 (0.01–0.76) 0.008
cNZDep2006 score 22 (18) 52 (25) 0.66 (0.38–1.15) 0.17 1–3 (low deprivation) 4–7 (medium deprivation) 42 (34) 69 (33) 1.05 (0.65–1.68) 0.90 8–10 (high deprivation) 58 (48) 86 (42) 1.28 (0.81–2.00) 0.30
aSource of infection 112 (90) 122 (58) 6.81 (3.54–13.11) 0.0001 Skin and soft tissue infection Surgical site infection 2 (2) 34 (16) 0.09 (0.02–0.36) 0.0001 Catheter-related infection 1 (1) 12 (6) 0.13 (0.02–1.05) 0.04 Bone and joint infection 4 (3) 9 (4) 0.75 (0.23–2.48) 0.78 Pneumonia 2 (2) 9 (4) 0.37 (0.08–1.73) 0.22 Primary bacteremia or endocarditis 0 (0) 6 (3) 0.25 (0.07–0.86) 0.02 Other 3 (2) 19 (9)
aOnset 69 (56) 79 (37) 2.10 (1.34–3.29) 0.001 Community onset, not health care associated Community onset, health care associated 43 (35) 52 (25) 1.62 (1.00–2.64) 0.06 Hospital onset, health care associated 12 (10) 80 (38) 0.18 (0.09–0.34) 0.0001 Comorbidities (Charlson score of 3) 112 (90) 155 (73) 3.37 (1.73–6.58) 0.0002 Implanted medical device 3 (2) 23 (11) 0.20 (0.06–0.69) 0.005 Trauma with breach of skin 30 days 19 (15) 21 (10) 1.64 (0.84–3.18) 0.16 Chronic noninfective skin condition 6 (5) 32 (15) 0.28 (0.12–0.70) 0.004 aRequired surgical procedure 75 (60) 59 (28) 3.94 (2.47–6.30) 0.0001 2 surgical procedures 4/75 (5) 10/59 (17) 0.28 (0.08–0.93) 0.04 Presence of bacteremia 4/35 (11) 19/92 (21) 0.50 (0.16–1.58) 0.43
Duration of admission (days) 45 (36) 72 (34) 1.1 (0.69–1.75) 0.73 1 2–4 63 (51) 46 (22) 6.00 (3.40–10.59) 0.0001 5 16 (13) 93 (44) 0.19 (0.10–0.34) 0.0001 Readmitted within 30 days 6 (5) 9 (4) 1.14 (0.40–3.29) 0.79 30-day mortality 1 (1) 10 (5) 0.16 (0.02–1.29) 0.06 a Found to be independent associations upon multivariate analysis adjusted for gender, ethnicity, age, deprivation score, onset, comorbidities, implanted medical device, trauma with breach of skin, chronic noninfective skin conditions, surgical requirement, duration of admission, 30-day readmission, and 30-day mortality. b Six patients aged greater than 90 years were excluded from analysis due to low numbers. c NZDep2006 score was not available for six patients.
SSTIs to features of PVL-negative MSSA SSTIs. Of note, DISCUSSION 112/232 (48%) of our patients presenting with MSSA SSTI had We found similar prevalences of lukSF-PV genes in both infection with a PVL-positive strain. Patients with PVL-positive clinical and nasal carriage isolates of MSSA among a diverse MSSA SSTI were also 7.4 times as likely to required surgical genetic range of MSSA in Auckland. The prevalence of PVL- drainage of cutaneous abscesses compared to patients with PVL- negative MSSA SSTI (95% con？dence interval, 4.1 to 13.3). positive MSSA among clinical isolates of MSSA in Auckland,
VOL. 48, 2010 PANTON-VALENTINE LEUKOCIDIN IN MSSA 3473
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Vandenesch, and J. Etienne. 1999. Involvement of Panton-Valentine leu- hood and young adulthood, with a decline in later years. Fur- kocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. J. Clin. Infect. Dis. 29:1128–1132. ther studies are required to elucidate the underlying reasons 18. Lo?f？er, B., M. Hussain, M. Grundmeier, M. Bru?ck, D. Holzinger, G. Varga, for this ？nding. J. Roth, B. C. Kahl, R. A. Proctor, and G. Peters. 2010. Staphylococcus aureus Panton-Valentine leukocidin is a very potent cytotoxic factor for human neutrophils. PLoS Pathog. 6:e1000715. 19. Lowy, F. D., A. E. Aiello, M. Bhat, V. D. Johnson-Lawrence, M. H. Lee, E. ACKNOWLEDGMENTS Burrell, L. N. Wright, G. Vasquez, and E. L. Larson. 2007. Staphylococcus aureus colonization and infection in New York State prisons. J. Infect. Dis. We thank James Bower and Gillian Henderson, Molecular Micro- 196:911–918. 20. McDonald, R. R., N. A. Antonishyn, T. Hansen, L. A. Snook, E. Nagle, M. 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