Community-associated methicillin-resistant Staphylococcus aureus (MRSA) skin and soft tissue infections (SSTIs) have dramatically increased over the past decade and have become a major public health threat.10,24,30,37 Persons infected with the human immunodeficiency virus (HIV) are at heightened risk for MRSA SSTIs, with studies demonstrating both outbreaks6,13 and an approximately 18-fold higher incidence rate among this group.10 Several reports have suggested that men who have sex with men (MSM) may be at particular risk,13 with some retrospective studies associating high-risk sexual behaviors or recent sexually transmitted infections (STIs) with MRSA infections6,28; however, the precise nature of these associations is unclear.
Because staphylococcal carriage precedes and increases the risk of subsequent SSTIs,12,14,23,27,38,49 understanding the predictors for colonization may be important for devising preventive strategies against SSTIs. Studies have shown that the nares are the most common location for carriage; however, recent investigations have demonstrated the importance of carriage at other locations, including the perianal region.46 The exact link between S. aureus carriage and sexual risk factors remains unclear, with no study examining methicillin-sensitive S. aureus (MSSA) and MRSA colonization at multiple body sites (including the perigenital areas) and sexual risk factors. If high-risk sexual behaviors are associated with increased carriage rates, this could provide a link for the higher risk of groin and buttock infections reported among both heterosexuals and MSM with multiple sexual partners.9,10,13
Therefore, we evaluated the prevalence of and the factors associated with carriage of S. aureus at 5 body sites among HIV-infected adult outpatients at 4 military clinics across the United States. Our primary objective was to determine the associations of several sociodemographic, clinical, and behavioral factors (including high-risk sexual behaviors) with colonization.
We performed a cross-sectional study of 550 HIV-infected persons to determine the prevalence of and the factors associated with MRSA and S. aureus colonization. The study was designed to include a longitudinal component (2-year follow-up), which is currently ongoing. The study population included HIV outpatients at the Naval Medical Center of San Diego (NMCSD), Walter Reed Army Medical Center (WRAMC) in Washington, DC, San Antonio Military Medical Center (SAMMC), and the Naval Medical Center Portsmouth (NMCP). HIV patients were offered enrollment during their routine clinical care visits. Inclusion criteria included age ≥18 years and HIV positivity by enzyme linked immunosorbent assay and confirmatory Western blot. Exclusion criteria were being a health care provider, and a positive pregnancy test among women. Participants provided written informed consent and were enrolled between May 2007 and May 2010. The study was approved by the governing military institutional review boards, conducted in accordance with the principles of the Declaration of Helsinki and standards of Good Clinical Practice (as defined by the International Conference on Harmonization), and registered with the Clinical Trials network (registration NCT00631566).
At enrollment, 1 sterile culture swab (BBL CultureSwab Plus; Becton, Dickinson and Co., Sparks, MD) was collected from each of the following body sites: nares, throat, bilateral axilla areas, bilateral groin areas, and perirectal area. The term "perigenital site" was designated to represent colonization at the groin and/or perirectal sites. Swabs were sent to the microbiology laboratories of each clinical site for the determination of the presence of MSSA or MRSA by standard microbiologic methods employed at each site.3,8
During the baseline study visit, participants completed a questionnaire assessing demographics (for example, age, sex, self-reported race/ethnicity), and sociobehavioral factors within the last 6 months including tobacco use, illicit drug use, number of sexual partners, condom use, use of public baths, exercise habits, gym use, and hygienic practices (such as showering, antimicrobial soap use). Study coordinators collected data from the medical records including concurrent medical conditions, history of SSTIs and MRSA, current use of trimethoprim-sulfamethoxazole (TMP-SMX), current CD4 cell count (flow cytometry), plasma HIV RNA level (Roche Amplicor; Roche Molecular Systems, Inc., Pleasanton, CA; undetectable as <50 copies/mL), Centers for Disease Control and Prevention (CDC) stage,5 and receipt of highly active antiretroviral therapy (HAART) defined as ≥3 full-dose antiretroviral drugs in combination. Data on antibiotic use (classified as anti-MRSA or other antimicrobials), hospitalizations, and emergency room/acute care visits within the last year were recorded. Anti-MRSA antibiotics were defined based on local susceptibility patterns and included TMP-SMX, tetracyclines, vancomycin, linezolid, daptomycin, rifampin, and gentamicin. In addition, electronic military medical records and computerized laboratory reports were analyzed for STIs, which included syphilis, genital warts, gonorrhea, Chlamydia, clinical outbreaks of herpes simplex type 2 (HSV2), and nongonococcal urethritis (NGU).
MRSA isolates were saved and frozen at −70°C. Molecular analyses were performed using pulse-field gel electrophoresis (PFGE). Polymerase chain reaction (PCR) was performed to determine the staphylococcal cassette chromosome mec (SCCmec) type and to detect the presence of genes for Panton-Valentine leukocidin (PVL) and the arginine catabolic mobile element (ACME). Antimicrobial susceptibility testing was performed using the BD Phoenix Automated Microbiology System (Becton, Dickinson and Co., Franklin Lakes, NJ). In cases of erythromycin resistance and clindamycin susceptibility, D-tests were performed to confirm clindamycin sensitivity. All molecular and antimicrobial testing was conducted at the Molecular Biology Laboratory at SAMMC.
Descriptive statistical analyses were performed evaluating the baseline characteristics of the study population; statistics were presented as numbers (percentages) and medians (interquartile ranges [IQR]) for categorical and continuous variables, respectively. The prevalence of S. aureus (MRSA or MSSA) carriage was determined by the number of participants with at least 1 positive swab divided by the total study population. Univariate associations between MRSA carriage and variables of interest were performed using logistic regression. Full multivariate logistic regression models included factors with a p value of < 0.10 on univariate testing and other relevant factors (age, ethnicity, and clinical site) to control for potential confounding. The clinical sites were grouped as NMCSD/SAMMC and WRAMC/NMCP due to similarities in climate. Highly correlated variables (assessed by chi-square tests) were evaluated using separate multivariate models. The final multivariate models were derived using a stepwise backward elimination approach. Similar models were developed examining S. aureus (MRSA or MSSA) carriage as the outcome of interest. Odds ratios (ORs), 95% confidence intervals (CI), and p values were reported. Only those variables with a final 2-sided p value < 0.05 were considered significantly associated with colonization. The goodness of fit for each multivariate model was determined using the Hosmer-Lemeshow test; a p value > 0.10 indicated a good fit. All statistical analyses were performed using SAS version 9.2 (SAS Institute, Cary, NC).
Study Population Characteristics
We enrolled 550 HIV-infected persons with a median age of 42 years (IQR, 33-49 yr); 93% were male; and race/ethnicity was white for 46%, African American for 35%, and other for 19% (Table 1). Fourteen percent were hospitalized in the last 12 months, 36% received an anti-MRSA antibiotic in the last 12 months, and 8% were currently receiving TMP-SMX. Regarding HIV factors, the current median CD4 count was 529 (IQR, 404-704) cells/mm3, 60% had an undetectable plasma HIV RNA level, and 70% were receiving HAART. The median duration of HIV infection was 9 years (IQR, 3-17 yr), and 42% had a history of acquired immunodeficiency syndrome (AIDS).
Eleven percent of participants had a history of a MRSA infection that occurred a median of 1 year before enrollment. Prior MRSA infections most commonly consisted of a SSTI in the buttocks/genital area (22%), followed by the lower extremities (19%), trunk (16%), head/neck (12%), upper extremities (8%), axilla (7%), or an undocumented location (10%); 5% had a lung or bloodstream infection.
Within the last year, 21% had a documented STI, including 8% with syphilis, 6% with genital warts, 4% with NGU, 3% with Chlamydia, 2% with HSV2, and 2% with gonorrhea; some participants had more than 1 type of STI in the last year. Self-reported number of sexual partners in the last 6 months was ≥2 partners for 20%, 1 partner for 30%, no partner for 33%, and not reported for 17%. Other baseline characteristics are shown in Table 1.
Prevalence of Staphylococcus aureus (MRSA or MSSA) Carriage
Carriage with either MRSA or MSSA was noted among 180 (33%) participants; 27% were colonized at the nares, 5% the perirectal area, 5% the throat, 4% the groin area, and 2% the axillae; some participants were colonized at multiple body sites (Table 2). Regarding the number of body sites colonized, 142 (26%) were colonized at 1 body site, 26 (5%) at 2 body sites, 9 (2%) at 3 body sites, 2 (0.4%) at 4 body sites, and 1 (0.2%) at all 5 body sites. Thirteen (50%) of the 26 participants with throat carriage did not have nares colonization. Among nares carriers, 19/147 (13%) had concurrent carriage in the perigenital region. Carriage at the perigenital site was overall found among 37 (7%) participants, of whom 19 (51%) had nares colonization and 18 (49%) had perigenital colonization with negative nares culture (see Table 2).
Regarding MRSA carriage specifically, 22 (4%) participants were colonized with MRSA at 1 or more body site (see Table 2). The site most frequently colonized was the nares, followed by the throat, groin, perirectal, and axillary areas (Figure 1). Sixteen participants were colonized with MRSA at a single location, 5 participants had MRSA detected at 2 sites, and 1 participant at 4 body sites. Of the 22 MRSA carriers, 2 (9.1%) were also carrying MSSA: 1 person with MRSA at the perigenital area and MSSA at the axillae, and the other with MRSA at the nares and MSSA at the perigenital region.
Characterization of MRSA Isolates
Twenty-eight of the 30 MRSA isolates were available for molecular characterization and antimicrobial susceptibility testing. USA300 was the most common PFGE type (n = 14), followed by strains that have PFGE patterns similar to USA300 (n = 5), USA1000 (n = 4), USA100 (n = 2), USA700 (n = 2), and USA800 (n = 1). All participants colonized with MRSA at more than 1 site had the same USA type at each area. All isolates were SCCmec type IV, except the 2 USA100 isolates, which were SCCmec type II. Of the USA300 isolates, 85% (12/14) contained PVL and 93% (13/14) contained ACME. None of the other USA types contained either PVL or ACME.
All isolates were sensitive to vancomycin (minimum inhibitory concentration [MIC] ≤1 μg/mL), linezolid, daptomycin, rifampin, and gentamicin. All isolates (n = 28) were resistant to erythromycin, 32% (n = 9) resistant to clindamycin, 21% (n = 6) resistant to tetracyclines, 43% (n = 12) resistant and 7% (n = 2) intermediate to levofloxacin, and 7% (n = 2) resistant to TMP-SMX.
Factors Associated With MRSA Colonization
Factors associated with MRSA carriage compared to non-carriage in the univariate analyses included African American compared to white race/ethnicity (OR, 2.8; p < 0.01), history of MRSA infection (OR, 6.6; p < 0.01), hospitalization within the last year (OR, 3.1; p = 0.02), history of STIs in the last year (OR, 3.7; p < 0.01), history of syphilis in the last year (OR, 6.6; p < 0.01), history of NGU in the last year (OR, 4.2; p = 0.03), and public bath use in the last 6 months (OR, 6.9; p < 0.01) (see Table 1). AIDS diagnosis (OR, 2.1; p = 0.09) and anti-MRSA antibiotic use (OR, 2.3; p = 0.06) had a borderline association with MRSA carriage. Age, sex, clinical site, tobacco or illicit drug use, self-reported number of recent sexual partners, condom use, current CD4 cell count, or HAART use were not associated with MRSA carriage in the univariate models. We also examined other individual STI events (gonorrhea, Chlamydia, and HSV2) in the last year, but found no associations, likely due to the small number of each of these individual events (data not shown).
In the multivariate models, any STI, individual STIs, and public bath use were highly correlated and therefore placed in separate models. The first full multivariate model included age, race/ethnicity, clinical site, recent hospitalization, history of MRSA infection, AIDS diagnosis, anti-MRSA antibiotic use, and STI in the last year. In the final model, history of a MRSA infection (OR, 9.4; p < 0.01), recent STI (OR, 4.2; p < 0.01), and African American versus white race/ethnicity (OR, 3.5; p = 0.01) remained significantly associated with MRSA colonization (Table 3).
In a second multivariate model, the same variables were analyzed but included syphilis in the last year (instead of STI). Syphilis in the last year was significantly associated with MRSA colonization (OR, 9.3; p < 0.01); similar findings regarding other factors were noted (Table 4). Likewise, in separate multivariate models, NGU was associated with MRSA carriage (OR, 7.5; p < 0.01) as well as public bath use (OR, 8.9; p < 0.01) (data not shown).
We also examined the relationship of STIs in the last year with self-reported condom use among MRSA carriers and among all participants, but found no statistically significant relationships (λ2, 0.41; p = 0.82 and λ2, 5.75; p = 0.06, respectively). Finally, we examined a combined variable accounting for both self-reported number of sexual partners and condom use, and found no associations with MRSA carriage.
Factors Associated With S. Aureus Colonization
We evaluated factors associated with S. aureus (MRSA or MSSA) colonization. No factor was significantly associated (p < 0.05) with carriage in the univariate models, with the exception of genital warts in the last year (OR, 2.0; p = 0.04). Borderline associations with syphilis in the last year (OR, 1.6; p = 0.14) and number of different sexual partners (OR, 1.04; p = 0.13) were observed (data not shown).
Given our interest in the potential association between S. aureus colonization and sexual factors, we examined factors associated with S. aureus carriage at the perigenital site. In the univariate analyses, syphilis in the last year was significantly associated with S. aureus carriage at this site (OR, 3.2; p = 0.01). In the final model adjusted for age, race/ethnicity, and clinical site, syphilis in the last year remained significantly associated with perigenital carriage (OR, 3.3; p = 0.01) (Table 5).
Recent studies by our group and others have suggested that sexual factors such as anonymous sex, multiple sexual partners, and a history of syphilis are associated with MRSA infections among HIV-infected persons.10,13,28 Further support that MRSA infections might be sexually transmitted is the large percentage of SSTIs located in the groin and buttocks areas.9,10,13 The current study provides additional evidence by examining staphylococcal colonization at several different sites, including the perigenital area. Our results show that MRSA carriage at any site and perigenital S. aureus carriage are both significantly associated with recent STIs, including syphilis. These data suggest that S. aureus may be transferred during sexual activities, and that high-risk behaviors (that place individuals at risk for STIs) may also increase the risk of staphylococcal transmission.
The pathogenesis of MRSA transmission in the setting of sexual contact may be due to several mechanisms. First, S. aureus and MRSA may colonize the gastrointestinal tract-for example, a review showed that 20% of patients have S. aureus intestinal colonization, and 9% carry MRSA at this site.1 Hence, perigenital carriage and subsequent staphylococcal transmission may occur during sexual activities including anal sex. Second, S. aureus may be transmitted during intimate skin-to-skin contact, colonizing the perigenital regions with secondary transfer to the nares, which may serve as a preferred reservoir given the high prevalence of carriage at this site. Finally, skin abrasions associated with sexual practices may enhance the likelihood of colonization and/or infection.13,28
Longitudinal studies are needed to determine if public health efforts to decrease traditional STIs (such as syphilis) will also affect the transmission of MRSA and ultimately decrease the incidence of SSTIs, particularly those occurring in the perigenital area. In addition, studies are needed to determine whether decolonization strategies can prevent these SSTIs. A 2010 study18 among HIV-positive drug users found no benefit from nares decolonization in reducing infection rates, although the study did not address other sites of colonization (such as the perigenital area).
Of interest is that the sexual factors associated with MRSA carriage in the current study involved clinical events (for example, diagnosis of syphilis, NGU) obtained by medical record review. Associations between self-reported sexual risk factors (such as number of partners, condom use) were not significantly associated with MRSA carriage. The reasons for these findings are unknown, but may be related to reporting bias. For example, our patients regularly undergo counseling on condom use and are potentially subject to legal consequences for failing to adhere to safe sexual practices. Although our study questionnaires were confidentially administered and maintained, self-reporting biases may have occurred. This is suggested by the lack of correlation between STIs and sexual practices in our analyses, and that nearly 20% of participants declined to provide information regarding self-reported sexual behaviors. On the other hand, screening for STIs in our HIV population is routinely performed and may more reliably indicate high-risk behaviors in our patient population. Of note, our study did find that public bath use was associated with MRSA carriage, which may be a covert marker for high-risk sexual behaviors.
We examined other potential associations of a large number of sociodemographic, clinical, and behavioral factors with MRSA carriage. Beyond the STIs being associated with MRSA carriage, we found that a history of a MRSA infection was associated with MRSA carriage, a finding concordant with other studies.4,21 In addition, African American race/ethnicity was associated with a higher prevalence of MRSA carriage, similar to results of other reports.15,36 The reason for this association is unclear, but the higher colonization rate may explain the higher risk of infections in this racial/ethnic group.26,45
We did not find any specific HIV clinical factors, such as low CD4 counts, detectable plasma HIV RNA levels, or lack of HAART, associated with MRSA colonization in our analyses. These factors have been previously noted in some, but not all, studies.4,31,40 Potential reasons for the lack of association in the current study include that our population had robust CD4 counts and high antiretroviral coverage; that we evaluated a contemporary cohort, whereas many prior studies were conducted in the pre- or early HAART eras; or that these variables were previously associated with other unmeasured risk factors for MRSA carriage.4,31
The overall prevalence of S. aureus (MRSA or MSSA) carriage among our population (33%) was similar to that in the general population and was concordant with that in other HIV cohorts.31,35,38,47 MRSA carriage was noted among 4% of our participants, compared to a prevalence rate of 0-13% in other studies in HIV-infected persons,2,4,7,16,25,29,31,33,35,40-43,44,46,47 and was nearly identical to that in a 2009 study46 from Boston in HIV-infected MSM. Table 6 provides a review of the published literature examining S. aureus carriage among HIV-infected persons.2,4,7,16,17,22,25,31,33,41-44,46-48 Of note, the prevalence of MSSA was approximately 7-fold higher than that of MRSA across all body sites examined in our study, a finding consistent with that in other studies among the general population and in HIV-infected persons.2,17,20,31,46,47
The current study was unique in that we evaluated S. aureus at multiple sites (5 sites), whereas most studies among HIV patients examined only the nares,17,31 with an occasional study evaluating perianal2,16,46 or axillae4,25 sites. Regarding site-specific carriage, the nares colonization rate of S. aureus (MRSA or MSSA) in the current study was slightly lower than that reported in the general population20 (27% vs. 32%, respectively); however, our MRSA nares carriage rate was higher than typically reported among healthy HIV-uninfected persons (3% vs. 0.8%, respectively), which is consistent with the observation that HIV-infected persons are at increased risk for MRSA colonization compared to the general population.20 Previous investigations among HIV-infected persons in the HAART era have reported MSSA and MRSA nasal carriage rates similar to those found in the current study (see Table 6); for example, a study47 among HIV-infected outpatients reported an MSSA nasal carriage rate of 20% and a MRSA rate of 3%, and another study31 reported MSSA and MRSA nasal carriage rates of 24% and 6%, respectively. Of note, some studies have shown a higher rate of MRSA colonization at the nares.4 The MRSA rate found in the current study may be influenced by relatively low rates of comorbidities in our cohort, such as illicit drug use, skin disease, and diabetes, which are known risk factors for MRSA nasal colonization.21,22,27,39,47
Studies have indicated that throat carriage may represent an important reservoir for S. aureus carriage.34 We found a S. aureus throat carriage rate of 5%, with the majority of isolates being MSSA. The overall rate in the current study is similar to that reported in an early (1989) study, which found an 8% carriage rate among HIV-infected persons.16 It is noteworthy that half of the throat carriers in the current study were not colonized at the nares, suggesting that throat carriage may be an important and hidden reservoir for S. aureus. On the other hand, we noted a low axillae MRSA carriage rate (0.2%), concurrent with that in another study4 among HIV-infected ambulatory patients (0.7%).
Regarding perigenital carriage, 6% were colonized with MSSA and 0.9% with MRSA at this site. A study2 among HIV-infected MSM reported similar rates of MRSA rectal carriage (1%), and another study46 reported a higher carriage rate of MSSA compared to MRSA at this site. Although the prevalence of carriage detected only at the perigenital region was low, approximately 50% of carriers at these sites had negative nares cultures, suggesting that screening this additional area could enhance the likelihood of detecting carriage. Furthermore, given the presence of S. aureus at the perigenital area and the increasing rate of S. aureus SSTIs in the groin and buttock regions among HIV-infected persons,10 prospective studies examining the role of colonizing strains at these areas on the future development of soft tissue infections are needed.
MRSA isolates underwent molecular characterization, and the majority had USA and SCCmec types consistent with community-acquired strains. For example, most MRSA isolates were SCCmec type IV and USA300, the strain type that has been linked to the rapid increase in community-acquired MRSA infections in the United States.13,24,37 As in other studies,14,37 the majority of USA300 strains among HIV patients in the current study were positive for PVL and ACME, factors associated with necrotizing SSTIs. Participants of the current study are being followed prospectively for 2 years to determine the impact of MRSA carriage and strain type on subsequent SSTIs.
Like all studies, the current study had potential limitations. We performed a cross-sectional study; hence, causal relationships could not be determined, nor could we determine the role of intermittent compared with persistent carriage. However, a longitudinal evaluation of risk factors, colonization, and subsequent SSTIs is currently underway. Given the low prevalence of MRSA colonization in the current study, we were unable to assess factors associated with MRSA colonization at individual sites. We also could not address the impact of sexual orientation on MRSA carriage due to the prior military policy of "don't ask, don't tell." Finally, our HIV population consisted of primarily men and included few illicit drug users; hence our findings may not be generalizable to some other groups.
The current study had several strengths. We assessed both MRSA and MSSA carriage at multiple body sites; we evaluated a large number of participants (n = 550) at geographically diverse locations in the United States; and we studied a comprehensive set of sociodemographic, clinical, and behavioral factors for their association with colonization. Furthermore, our assessment of high-risk sexual behaviors evaluated both self-reported and clinical events. Finally, since a relationship between sexual factors and S. aureus infections has only recently been proposed, our study provides useful new information on this topic.
In summary, STIs were associated with MRSA carriage in the current study, suggesting that MRSA may be transmitted in the setting of sexual contact. These results have several potential public health and clinical implications. First, sexual activity may be an important factor in the dissemination of S. aureus and subsequent infections in the community.9 Second, understanding patterns of S. aureus carriage is important among HIV patients, given their heightened risk for both infection and recurrent disease.10,11,19 Finally, given the rising resistance patterns and morbidity associated with these infections,13 longitudinal evaluations of sexual risks and MRSA transmission are essential, as are prevention studies. In the interim, messages advocating heightened safe sex, which not only may decrease STIs, but also may prevent the transmission of MRSA, should be instituted among HIV-infected persons.
The authors thank Renato Reyles for his support of microbiology work in this study.
APPENDIX A. THE INFECTIOUS DISEASE CLINICAL RESEARCH PROGRAM HIV WORKING GROUP
The members of the Infectious Disease Clinical Research Program HIV Working Group are as follows: Susan Banks RN, CAPT Mary Bavaro, MD, LCDR Helen Chun, MD, Denise Cole, Cathy Decker, MD, Lynn Eberly, PhD, Conner Eggleston, COL Susan Fraser, MD, Heather Hairston, MAJ Joshua Hartzell, MD, LTC Gunther Hsue, MD, Kathy Huppler Hullsiek, PhD, Arthur Johnson, MD, COL Mark Kortepeter, MD, MPH, Micheal Landrum, MD, Alan Lifson, MD, MPH, Michelle Linfesty, Grace Macalino, PhD, Sheila Medina, Scott Merritt, Barbara Nagaraj, LTC Robert O'Connell, MD, Cpt Jason Okulicz, MD, Sheila Peel, PhD, Michael Polis, MD, John Powers, MD, MAJ Roseanne Ressner, MD, Gabriela Sanguineti, Terry Sjoberg, ret CAPT Sybil Tasker, MD, ret COL Edmund Tramont, MD, David Wallace, LT Tyler Warkentien, MD, MAJ Paige Waterman, MD, CDR Timothy Whitman, MD, COL Glenn Wortmann, MD, and LTC Michael Zapor, MD.
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2. Antoniou T, Devlin R, Gough K, Mulvey M, Katz KC, Zehtabchi M, Polsky J, Tilley D, Brunetta J, Arbess G, Guiang C, Chang B, Kovacs C, Ghavam-Rassoul A, Cavacuiti C, Corneslon B, Berger P, Loutfy MR. Prevalence of community-associated methicillin-resistant Staphylococcus aureus colonization in men who have sex with men. Int J STD AIDS
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25. Klein PA, Greene WH, Fuhrer J, Clark RA. Prevalence of methicillin-resistant Staphylococcus aureus in outpatients with psoriasis, atopic dermatitis, or HIV infection. Arch Dermatol
26. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK. Active Bacterial Core surveillance (ABCs) MRSA Investigators. Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA
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28. Lee NE, Taylor MM, Bancroft E, Ruane PJ, Morgan M, McCoy L, Simon PA. Risk factors for community-associated methicillin-resistant Staphylococcus aureus skin infections among HIV-positive men who have sex with men. Clin Infect Dis
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