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A Prospective Investigation of Outcomes after Hospital Discharge for Endemic, Community-Acquired Methicillin-Resistant and -Susceptible Staphylococcus aureus Skin Infection

  1. Loren G. Miller1,2,3,
  2. Clifford Quan2,
  3. Anthony Shay1,3,4,
  4. Katayoun Mostafaie4,
  5. Kiran Bharadwa6,
  6. Nelly Tan4,5,
  7. Kelli Matayoshi1,3,
  8. Jason Cronin1,3,4,
  9. Jennifer Tan1,3,
  10. Grace Tagudar1,3, and
  11. Arnold S. Bayer1,3,4
  1. 1Division of Infectious Diseases, Torrance
  2. 2Division of General Internal Medicine, Torrance
  3. 3Los Angeles Biomedical Research Institute, Harbor—University of California—Los Angeles Medical Center, Torrance
  4. 4David Geffen School of Medicine at the University of California, Los Angeles
  5. 5University of California, Riverside, California
  6. 6School of Medicine and Biomedical Sciences, State University of New York, Buffalo
  1. Reprints or correspondence: Dr. Loren G. Miller, Div. of Infectious Diseases, Harbor-UCLA Medical Center, 1000 W. Carson St., Box 466, Torrance, CA 90509 (lgmiller{at}ucla.edu).

  1. Presented in part: 43rd Annual Meeting of the Infectious Diseases Society of America, San Francisco, California, October 2005 (abstract 1059).

 
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Abstract

Background. Although community-acquired methicillin-resistant Staphylococcus aureus (CA-MRSA) infection has become increasingly common, prospective data on outcomes of patients with skin infection remain poorly defined.

Methods. We prospectively observed a cohort of 201 patients discharged after hospitalization for CA-MRSA infection or community-acquired methicillin-susceptible S. aureus (CA-MSSA) infection. Patients were interviewed 30 and 120 days after they received a diagnosis. Our primary outcome was clinical response, defined as no relapse, new S. aureus infection, or need for antibiotics at day 30.

Results. Among 117 patients with skin infection, the nonresponse rate at day 30 was similar among patients with CA-MRSA infection and those with CA-MSSA infection (23 [33%] of 70 vs. 13 [28%] of 47 patients; P = .55). Lack of incision and drainage was associated with nonresponse at day 30 (P = .005), but other clinical factors, including receipt of antibiotics inactive against the infecting strain, were not. Patients with CA-MSSA infection were more likely to be rehospitalized (P = .003) and to believe subjectively that they had not been cured (P = .002) at day 30. At day 30, there was a trend for close contacts of CA-MRSA—infected patients to develop a similar infection (13% vs. 4%; odds ratio, 3.3; 95% confidence interval, 0.7–15.8; P = .2).

Conclusion. Although it is believed patients with CA-MRSA skin infection may have more serious outcomes than those with CA-MSSA skin infection, we found similar outcomes in these 2 groups after hospital discharge. Clinical nonresponse at day 30 was associated with a lack of receipt of incision and drainage. Our data also suggest that close contacts of persons with CA-MRSA skin infection may have a higher likelihood of acquiring an infection.

Staphylococcus aureus is the most common identified cause of skin and soft-tissue infection [1, 2]. Infections caused by methicillin-resistant S. aureus (MRSA) were originally limited to hospital settings, but MRSA has emerged as a significant cause of community-acquired (CA) infection in the United States and worldwide [3–9]. Previously, risk factors for MRSA infection in the community were well defined and included prolonged prior hospitalization, prior admission to nursing home or long-term care facility, and injection drug use [9–11]. However, CA-MRSA infections have recently been reported among young, healthy individuals without risk factors [4, 12–16]. Most infections manifest as skin and soft-tissue infection. However, life-threatening invasive infections, such as necrotizing pneumonia [17, 18], necrotizing fasciitis [19], and sepsis-like syndromes [20–22], have been reported.

In many places, CA-MRSA infections have become endemic and more prevalent than CA infections with methicillin-susceptible S. aureus (MSSA) [7, 23–25]. There are suggestions that CA-MRSA infections may be more severe and transmittable and more likely to relapse than CA-MSSA infections [3, 26, 27]. However, these observations are anecdotal, and data from comparisons of MRSA versus CA-MSSA infection are lacking. In addition, there are virtually no prospective data on outcomes among patients with CA-MRSA infection, such as relapse rates and transmission of infection to close contacts. Furthermore, the response of CA-MRSA infection to antibiotics is poorly described and is limited to noncomparative descriptions [28] or chart reviews that do not standardize outcomes or explore important predictors of outcomes, such as comorbidities [29].

Because of the limited prospective data regarding CA-MRSA infection, we sought to study the long-term outcomes of patients with CA-MRSA skin infection and to compare these outcomes to the outcomes among patients with CA-MSSA skin infection.

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Methods

Study population. We examined the outcomes among a well-described cohort of 202 patients who had been hospitalized for CA-MRSA or CA-MSSA infection. Details of this investigation have been described elsewhere [23]. In brief, from 23 February through 15 October 2004, we screened the clinical microbiology laboratory at Harbor—University of California—Los Angeles (UCLA) Medical Center (Torrance), a public hospital in Los Angeles County, daily for cultures of wound, blood, urine, or sputum samples newly positive for S. aureus. We approached patients with a positive culture result if they were still hospitalized and if the culture sample had been obtained within 72 h after hospital admission. Patients were excluded from the study if (1) the patient had previously enrolled in the study, (2) S. aureus had been previously isolated from the patient during the present hospitalization, or (3) if the patient had previously refused participation. The Institutional Review Board at Harbor-UCLA Medical Center approved the study.

A total of 409 patients had cultures positive for S. aureus within 72 h after hospital admission; 326 patients (80%) were queried for study enrollment. The remaining 83 patients (20%) were unavailable to study personnel because of discharge (n = 74), death (n = 6), or hospital transfer (n = 3). The informed consent process was not completed by 23 of the subjects queried for study enrollment, largely for reasons of altered mental status. Of the 303 patients who completed the informed consent process, 280 subjects (92%) consented and 23 (8%) refused.

Categorization of CA, MRSA, and MSSA. CA infection was defined using the Centers for Disease Control and Prevention's ABC criteria [30]. However, we considered patients who had been hospitalized in the prior 12 months to have had CA infection, as described elsewhere [23]. Antibiotic susceptibility was determined using the Vitek system (bioMérieux), in accordance with Clinical and Laboratory Standards Institute protocols; isolates that were resistant to oxacillin were considered to be MRSA, and isolates that were susceptible to oxacillin were considered to be MSSA. Antibiotic treatment was determined by the patients' providers.

Data collection. At the time of enrollment, patients were administered a standardized survey in their preferred language (English or Spanish). This questionnaire explored a wide variety of exposures that are hypothesized or known to be associated with risk for CA-MRSA. Additional clinical information was obtained using a standardized chart abstraction instrument.

We examined a limited number of baseline factors (i.e., those collected before the outcome) that have been hypothesized to be associated with postdischarge outcomes on the basis of the literature [3, 9, 25, 27]; these included demographic factors, clinical factors, a measure of comorbidities [31], and preinfection health-related quality of life (HRQOL, measured using the SF-12 survey) [32]. Other exposures associated with a risk of S. aureus or CA-MRSA infection were measured, including injection drug use, homelessness, hygiene, and prior contact with a person with a skin infection (table 1).

Postdischarge follow-up survey. After hospital discharge, a research assistant contacted patients via telephone 30 and 120 days after enrollment. Using a standard questionnaire, patients were asked questions regarding their health, health care, clinical outcomes, antibiotic use, new infections among household contacts, and HRQOL. Subjects were compensated for each interview. To ensure the accuracy of information, a physician-investigator reviewed subjects' medical records for objective outcomes (e.g., antibiotic prescription). For discrepancies between the survey and the chart, we referred to the medical record.

Primary outcome: clinical nonresponse at 30 days. We hypothesized that clinical outcomes among patients with skin infection due to CA-MRSA would be worse than the outcomes among patients with CA-MSSA skin infection. Our primary outcome was clinical nonresponse at day 30, defined as presence of ≥1 of the following events 30 days after enrollment: (1) infection relapse at the original site, (2) new S. aureus skin infection at a separate body site, and/or (3) need for a new or unplanned course of antibiotic treatment for S. aureus infection after completion of the initial antibiotic regimen. Patients treated for infections that required antibiotic courses that exceeded 30 days in duration were excluded from analysis.

Secondary outcomes. We examined several secondary outcomes that we hypothesized might differ between patients with CA-MRSA skin infection and those with CA-MSSA skin infection; these included (1) a need for additional surgery, (2) rehospitalization, (3) subjective sense of infection cure, (4) new skin infection among household members, and (5) changes in HRQOL. All outcomes were measured at 30 and 120 days. We also compared rates of nonresponse (as defined above) at 120 days.

In addition, we examined factors associated with clinical nonresponse at 30 and 120 days. These included factors hypothesized to be associated with clinical nonresponse on the basis of the literature [3, 9, 25, 27] and clinical judgment. Finally, because of the paucity of literature about clinical outcomes of CA-MRSA skin infection according to antibiotic treatment received, we examined the response rate at day 30 stratified by antibiotic regimen.

Statistical analysis. Comparisons between groups were performed using the χ2 test, Fisher's exact test, or Student's t test, as appropriate. Associations with a P value <.05 were considered to be statistically significant. Data analysis was performed using SAS software, version 8.2 (SAS Institute).

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Results

Among the 280 patients who provided consent for our parent study, 202 had CA S. aureus infection, and 78 had health care—acquired S. aureus infection. Among 202 subjects with CA S. aureus infection, 22 were children, and 180 were adults. One hundred twenty patients (60%) had CA-MRSA infection, and the remaining 82 (40%) had CA-MSSA infection.

Among the 202 patients with CA S. aureus infection, 201 were discharged from the hospital alive; 132 (66%) of these patients completed the day 30 survey, and 98 (48%) completed the day 120 survey. We excluded 4 subjects from our analysis because of need for antibiotics for>30 days (n = 1) or because the patient was still hospitalized at day 30 (n = 3) (figure 1). Among the 128 subjects who completed the day 30 survey, we excluded 11 subjects who had non—skin infection. Of those with skin infection who completed the day 30 survey, 70 (60%) were infected with CA-MRSA, and 47 (40%) were infected with CA-MSSA. Ninety-eight patients (84%) were adults, and 19 (16%) were children. Patients infected with CA-MSSA had a longer duration of hospitalization than did those infected with CA-MRSA (median duration of hospitalization, 5.2 vs. 4.5 days; P = .02). There was a nonsignificant trend for patients with CA-MRSA infection to have a higher physical component of the HRQOL before infection (median score, 52 vs. 46; P = .08).

Figure 1
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Figure 1

Schema of patient follow-up data after discharge from the hospital community-acquired Staphylococcus aureus infection. *Four patients were excluded from analysis of day 30 outcomes because they required a prolonged course of antibiotics, making determination of day 30 response not applicable (n = 1, for a subject with endocarditis) and because hospitalization was still required after 30 days (n = 3). **Eleven patients were excluded because they had non—skin infections (3 patients with methicillin-resistant S. aureus [MRSA] infection and 8 patients with methicillin-susceptible S. aureus [MSSA] infection).

We compared demographic and selected clinical characteristics among patients who completed at least 1 follow-up visit with the characteristics among those who did not. Patients without at least 1 follow-up visit were more likely to use injection drugs (26% vs. 13%; P = .02), to be homeless (37% vs. 16%; P = .001), or to be African American (25% vs. 13%; P = .03). Latinos were more likely to complete at least 1 follow-up visit than not (60% vs. 38%; P = .01). There were no significant differences between the 2 groups with regard to sex, whether they snorted or smoked drugs, recent incarceration, HIV status, or the presence of cancer or diabetes mellitus.

Differences in baseline characteristics among CA-MRSA—infected and CA-MSSA—infected patients. In table 1, we present the demographic and clinical characteristics of subjects who completed the day 30 survey. Subjects with CA-MRSA infection were younger than those with CA-MSSA infection (median age, 37 vs. 46 years; P = .004), less likely to have diabetes (20% vs. 49%; P = .001), and more likely to report a history of snorting drugs (30% vs. 10%; P = .02). Otherwise, there were no significant differences between the 2 groups with regard to demographic characteristics or other clinical manifestations (e.g., abscess or cellulitis). When examining patients who had follow-up to day 120, the groups were similar, except that persons with CA-MRSA infection were more likely to report contact with a person who had a skin infection in the month prior to admission (24% vs. 7%; P = .05).

Table 1
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Table 1

Demographic and clinical characteristics of patients hospitalized for community-associated (CA) Staphylococcus aureus skin infection.

As described elsewhere [23], among CA-MRSA isolates, there was a high degree of antimicrobial resistance to fluoroquinolones and macrolides, a high degree of susceptibility to clindamycin and tetracycline, and universal susceptibility to trimethoprim-sulfamethoxazole (TMP-SMX), rifampin, and vancomycin. In comparison, CA-MSSA isolates were largely susceptible to all antibiotics tested except penicillin.

Primary outcome: clinical nonresponse at day 30. Among all subjects, 36 (31%) of 117 patients met our definition of clinical nonresponse at day 30. The rates of nonresponse at day 30 were similar among patients with CA-MRSA infection and those with CA-MSSA infection (23 [33%] of 70 vs. 13 [28%] of 47 patients; P = .55).

Factors associated with clinical nonresponse. When examining differences between nonresponders and responders at day 30, we found that nonresponders were less likely to undergo incision and drainage, compared with responders (20 [80%] of 25 vs. 66 [99%] of 67; P = .005). However, we found no other difference between nonresponders and responders at day 30 in terms of demographic characteristics, clinical factors, and antimicrobial susceptibility of the S. aureus strain (table 2). Somewhat surprisingly, receipt of discordant antibiotic therapy (defined as postdischarge treatment with an antibiotic that was inactive against the infecting strain) was not associated with a higher nonresponse rate. When examining differences between responders and nonresponders at day 120, we found no significant differences between responders and nonresponders (table 2). In a post-hoc analysis of only patients with CA-MRSA infection, we found no variables that were significantly associated with nonresponse at day 30 or 120 (data not shown).

Table 2
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Table 2

Characteristics of nonresponders and responders at days 30 and 120 among patients with community-associated Staphylococcus aureus infection.

Other outcomes and self-reported outcomes at day 30 and day 120. As noted above, our definition of clinical nonresponse is derived from a composite of 3 separate questions relating to infection relapse and nonresponse. When examining for differences between each of these separate components—requirement for additional antibiotics, recurrence of infection at the same body site, and new infection—we found no differences in rates between CA-MRSA—infected patients and CA-MSSA—infected patients at day 30 or 120 (table 3).

Table 3
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Table 3

Additional outcomes among patients with community-associated (CA) methicillin-resistant Staphylococcus aureus (MRSA) infection or CA methicillin-susceptible S. aureus (MSSA) infection at follow-up days 30 and 120.

CA-MSSA—infected patients were more likely than CA-MRSA—infected patients to be rehospitalized during the 30 days after their initial hospitalization (23% vs. 4%; P = .003) (table 3). The proportion of persons who self-reported cure at day 30 was higher among patients with CA-MRSA infection than among CA-MSSA—infected patients (83% vs. 57%; P = .002). There was a nonsignificant trend for patients with CA-MRSA infection to be more likely to report a household contact with a person with a new skin infection at day 30, compared with patients infected with CA-MSSA (9 [13%] of 70 vs. 2 [4%] of 46; OR, 3.3; 95% CI, 0.7–15.8; P = .2). We found no differences in any of these outcomes at day 120, although the sample size was smaller.

Antibiotic response rate at day 30. In table 4, we present the response rates at day 30, stratified by antibiotic treatment and CA-MRSA versus CA-MSSA infection status. Among patients with CA-MRSA infection, 7 (88%) of 8 of those who were not prescribed antibiotics at hospital discharge had a clinical response at day 30. It must be emphasized that antibiotic therapy (or lack thereof) at the time of hospital discharge was determined by the patients' physicians. Therefore, it is likely that patients who were not given antibiotics at hospital discharge had a clinically resolved infection (e.g., after incision and drainage and receipt of some antibiotic therapy). Among patients who were prescribed antibiotics, the response rates were 54% (15 of 28 patients) for those given TMP-SMX plus rifampin, 70% (7 of 10 patients) for TMP-SMX recipients, and 67% (6 of 9 patients) for clindamycin recipients. Eleven patients with CA-MRSA infection were prescribed β-lactams, largely because culture results were not available at the time of hospital discharge, and presumably, the patients were not suspected to have MRSA infection. Among these patients, 9 (82%) of 11 had a response at day 30.

Table 4
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Table 4

Day 30 response rates of subjects, stratified by antibiotic treatment.

Because of the limited sample size for each treatment stratum, we did not perform formal comparisons of antibiotic therapies. In addition, because comorbidities, severity of illness, and other important clinical factors may differ among patients prescribed certain antibiotic regimens, we felt that, if treatment comparisons were performed, any statistical differences may have been due to nontherapeutic (e.g., host-related) factors rather than differences in efficacy between the antibiotic regimens themselves.

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Discussion

Despite the increasing number of CA-MRSA skin infections, there are very limited data detailing posthospitalization outcomes. The few available data are from retrospective case studies. One investigation, a retrospective analysis of 39 patients in a dermatology practice, observed outcomes after treatment for CA-MRSA infection but did not control for comorbidities and other factors [29]. To our knowledge, no study has compared outcomes among CA-MRSA—infected patients and CA-MSSA—infected patients, and none have examined outcomes prospectively. Furthermore, none have examined the role of comorbidities and other factors that may be associated with clinical outcomes.

Several interesting observations were made in this study. We found that lack of incision and drainage was associated with nonresponse, but we found no other host or treatment factors associated with nonresponse. Our findings are consistent with other investigations that suggest that surgical drainage, rather than antibiotic therapy, is the cornerstone of treatment of drainable skin infection [33, 34].

Some of our secondary outcomes had findings supporting hypothesized differences between CA-MRSA and CA-MSSA. For example, we found a trend toward patients with CA-MRSA being more likely to report household contacts with a new skin infection in the month after hospital discharge, compared with CA-MSSA—infected patients (13% vs. 4%). Although proof of mode of transmission between the subjects and household contacts cannot be definitively established, our findings do suggest that CA-MRSA may be more transmissible than CA-MSSA. Others investigations have found that close contact with persons with skin infection appears to be a risk factor for epidemic CA-MRSA [35, 36].

Interestingly, patients with CA-MSSA infection were more likely to report a need for rehospitalization and were less likely to report cure at day 30. Although the reason for this is unclear, we observed that CA-MSSA—infected patients tended to have more comorbidities and a lower physical component score in the HRQOL survey. These differences suggest that patients with CA-MSSA infection were less healthy than patients with CA-MRSA infection at baseline.

In terms of measuring response to antibiotic therapy, it should be emphasized that our outcomes were not based on responses to initial therapy; instead, they were based on postdischarge therapy. Although the purpose of our study was not to examine differences in antibiotic treatments, there were interesting observations relating to therapy. It is likely that patients who were less ill or who had fewer underlying comorbidities were given less aggressive therapy, as witnessed by the relatively high response rate (80%) among patients who were discharged without receiving antibiotics. Nevertheless, there appeared to be no trends in response rates based on antibiotic therapy. Surprisingly, patients with CA-MRSA infection who were treated with β-lactams had an 83% response rate. In a post-hoc analysis, all of the patients in this category underwent incision and drainage, which may have been the key treatment modality in these cases. Why the rate of response among patients with CA-MSSA infection given β-lactams was lower (72%) is unclear, although some patients (7%) did not undergo incision and drainage, which may have contributed to the lower response. Response despite receipt of discordant antibiotic therapy further underscores the notion that incision and drainage was likely the most critical part of many patients' therapy. Aggressive combinations of therapies, such as TMP-SMX plus rifampin, had relatively poor response rates (15 [54%] of 28 patients). These results contrast those of Iyer and Jones [29], who found that 6 of 6 patients who received this regimen responded. Our low response rate may be because a more ill population was given this regimen.

There are limitations to our investigation. First, our study was observational; thus, differences between patients with CA-MRSA infection and those with CA-MSSA infection may be associated with unmeasured host factors and behaviors rather than the susceptibility of the infecting S. aureus strain. Nevertheless, data suggesting differences between CA-MRSA and CA-MSSA are based on hypothesis, extrapolations from outbreaks of CA-MRSA infection, and expert opinion [15, 27, 35]. Our investigation is, to our knowledge, the first to systematically study such differences. A second limitation is that some patients did not complete follow-up visits. Of our patients, 66% completed the day 30 interview. This may reflect the fact that many persons in our cohort were poor, uninsured, and homeless; therefore, follow-up can be challenging. Nevertheless, to our knowledge, our follow-up is the longest of any investigation studying CA-MRSA and CA-MSSA. A third limitation is that our outcome is based on telephone interviews, which are limited by patient recall and subjectivity. However, to minimize subjectivity, we performed chart reviews to verify objective data, when feasible. Finally, we did not examine strain characteristics associated with clinical response. We should note that many of the infecting strains from our cohort have been previously characterized [23]. Almost all (>90%) CA-MRSA strains were the USA300 genotype, whereas the CA-MSSA strains were very diverse. Strain analysis demonstrated that strain type and virulence factors were highly correlated with methicillin resistance (data not shown). Thus, because CA-MRSA was not correlated with clinical response, it would have been highly unlikely that the virulence factors of CA-MRSA strains would have been correlated with response. Therefore, we did not further examine this relationship.

There are strengths to our investigation. First, our study is prospective; therefore, the baseline data were systematically collected during hospitalization. Second, we collected highly detailed clinical and epidemiological data, which are not typically documented accurately in the medical record and almost impossible to collect with a retrospective design. Third, our study design focused on patients with endemic (i.e., nonoutbreak) CA-MRSA infection and contrasted outcomes with those among patients infected with CA-MSSA. To date, most studies of CA-MRSA infection are focused on epidemics or outbreaks [15, 35, 37].

In summary, we found that 30-day response rates among patients with CA-MRSA infection are similar to those among patients with CA-MSSA infection. Our data also suggest that patients with CA-MRSA infection may be more likely to report new skin infections in close household contacts. Larger investigations are needed to assess for predictors of nonresponse to CA S. aureus infection, so that we can identify patients who may be at high risk for clinical failure and require more-aggressive treatment and monitoring.

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Acknowledgments

We thank Jennifer Tan, Claudia Morales, Jenna Hua, Jennifer Tsui, and Dr. Josh Perlroth, Dr. Uzoma Ibebuogu, and Dr. Robert Yoshimori and the Clinical Microbiology Laboratory at Harbor-UCLA for their assistance with this investigation. We would also like to thank the patients and their families for participating in this investigation.

Financial support. Centers for Disease Control and Prevention (R01/ CCR923419 to L.G.M.) and National Institutes of Health (K23AI0183 to L.G.M.). J.T. was supported in part by the Short Term Training Program at the David Geffen School of Medicine at the University of California, Los Angeles.

Potential conflicts of interest. All authors: no conflicts.

  • Received August 4, 2006.
  • Accepted November 7, 2006.
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References

  1. ↵
    1. Mandell GL,
    2. Bennett JE,
    3. Dolin R
    1. Waldvogel F
    . Staphylococcus aureus (including toxic shock syndrome). In: Mandell GL, Bennett JE, Dolin R, editors. Mandell, Douglas, and Bennett's principles and practice of infectious diseases. 5th ed. Vol. 1. Philadelphia: Churchill Livingstone; 2000. p. 2072-83.
  2. ↵
    1. Brook I,
    2. Frazier EH
    . Clinical features and aerobic and anaerobic microbiological characteristics of cellulitis. Arch Surg 1995;130:786-92.
    Abstract/FREE Full Text
  3. ↵
    1. Chambers HF
    . The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis 2001;7:178-82.
    MedlineWeb of Science
  4. ↵
    Centers for Disease Control and Prevention. Outbreaks of community-associated methicillin-resistant Staphylococcus aureus skin infections—Los Angeles County, California, 2002–2003. MMWR Morb Mortal Wkly Rep 2003;52:88.
    Medline
    1. Murray RJ,
    2. Lim TT,
    3. Pearson JC,
    4. Grubb WB,
    5. Lum GD
    . Community-onset methicillin-resistant Staphylococcus aureus bacteremia in Northern Australia. Int J Infect Dis 2004;8:275-83.
    CrossRefMedlineWeb of Science
    1. Fang YH,
    2. Hsueh PR,
    3. Hu JJ,
    4. et al
    . Community-acquired methicillin-resistant Staphylococcus aureus in children in northern Taiwan. J Microbiol Immunol Infect 2004;37:29-34.
    Medline
  7. ↵
    1. Sattler CA,
    2. Mason EO Jr,
    3. Kaplan SL
    . Prospective comparison of risk factors and demographic and clinical characteristics of community-acquired, methicillin-resistant versus methicillin-susceptible Staphylococcus aureus infection in children. Pediatr Infect Dis J 2002;21:910-7.
    CrossRefMedlineWeb of Science
    1. Fridkin SK,
    2. Hageman JC,
    3. Morrison M,
    4. et al
    . Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med 2005;352:1436-44.
    CrossRefMedlineWeb of Science
  9. ↵
    1. Weber JT
    . Community-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis 2005;41(Suppl 4):269-72.
    FREE Full Text
    1. Charlebois ED,
    2. Bangsberg DR,
    3. Moss NJ,
    4. et al
    . Population-based community prevalence of methicillin-resistant Staphylococcus aureus in the urban poor of San Francisco. Clin Infect Dis 2002;34:425-33.
    Abstract/FREE Full Text
  11. ↵
    1. Mulligan ME,
    2. Murray-Leisure KA,
    3. Ribner BS,
    4. et al
    . Methicillin-resistant Staphylococcus aureus: a consensus review of the microbiology, pathogenesis, and epidemiology with implications for prevention and management. Am J Med 1993;94:313-28.
    CrossRefMedlineWeb of Science
  12. ↵
    1. Eguia JM,
    2. Chambers HF
    . Community-acquired methicillin-resistant Staphylococcus aureus: epidemiology and potential virulence factors. Curr Infect Dis Rep 2003;5:459-66.
    Medline
    1. Mongkolrattanothai K,
    2. Daum RS
    . Impact of community-associated, methicillin-resistant Staphylococcus aureus on management of the skin and soft tissue infections in children. Curr Infect Dis Rep 2005;7:381-9.
    CrossRefMedline
    1. Begier EM,
    2. Frenette K,
    3. Barrett NL,
    4. et al
    . A high-morbidity outbreak of methicillin-resistant Staphylococcus aureus among players on a college football team, facilitated by cosmetic body shaving and turf burns. Clin Infect Dis 2004;39:1446-53.
    Abstract/FREE Full Text
  15. ↵
    1. Kazakova SV,
    2. Hageman JC,
    3. Matava M,
    4. et al
    . A clone of methicillin-resistant Staphylococcus aureus among professional football players. N Engl J Med 2005;352:468-75.
    CrossRefMedlineWeb of Science
  16. ↵
    Methicillin-resistant Staphylococcus aureus infections in correctional facilities—Georgia, California, and Texas, 2001–2003. MMWR Morb Mortal Wkly Rep 2003; 52:992-6.
  17. ↵
    1. Frazee BW,
    2. Salz TO,
    3. Lambert L,
    4. Perdreau-Remington F
    . Fatal community-associated methicillin-resistant Staphylococcus aureus pneumonia in an immunocompetent young adult. Ann Emerg Med 2005;46:401-4.
    CrossRefMedlineWeb of Science
  18. ↵
    1. van der Flier M,
    2. van Dijk NB,
    3. Fluit AC,
    4. Fleer A,
    5. Wolfs TF,
    6. van Gestel JP
    . Fatal pneumonia in an adolescent due to community-acquired methicillin-resistant Staphylococcus aureus positive for Panton-Valentine-leukocidin. Ned Tijdschr Geneeskd 2003;147:1076-9.
    Medline
  19. ↵
    1. Miller LG,
    2. Perdreau-Remington F,
    3. Rieg G,
    4. et al
    . Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 2005;352:1445-53.
    CrossRefMedlineWeb of Science
  20. ↵
    1. Mongkolrattanothai K,
    2. Boyle S,
    3. Kahana MD,
    4. Daum RS
    . Severe Staphylococcus aureus infections caused by clonally related community-acquired methicillin-susceptible and methicillin-resistant isolates. Clin Infect Dis 2003;37:1050-8.
    Abstract/FREE Full Text
    1. Kravitz GR,
    2. Dries DJ,
    3. Peterson ML,
    4. Schlievert PM
    . Purpura fulminans due to Staphylococcus aureus. Clin Infect Dis 2005;40:941-7.
    Abstract/FREE Full Text
  22. ↵
    1. Adem PV,
    2. Montgomery CP,
    3. Husain AN,
    4. et al
    . Staphylococcus aureus sepsis and the Waterhouse-Friderichsen syndrome in children. N Engl J Med 2005;353:1245-51.
    CrossRefMedlineWeb of Science
  23. ↵
    1. Miller LG,
    2. Perdreau-Remington F,
    3. Bayer AS,
    4. et al
    . Clinical and epidemiologic characteristics cannot distinguish community-associated methicillin-resistant Staphylococcus aureus infection from methicillin-susceptible S. aureus infection: a prospective investigation. Clin Infect Dis 2007;45:471-82. (in this issue).
    1. Moran GJ,
    2. Amii RN,
    3. Abrahamian FM,
    4. Talan DA
    . Methicillin-resistant Staphylococcus aureus in community-acquired skin infections. Emerg Infect Dis 2005;11:928-30.
    MedlineWeb of Science
  25. ↵
    1. Deresinski S
    . Methicillin-resistant Staphylococcus aureus: an evolutionary, epidemiologic, and therapeutic odyssey. Clin Infect Dis 2005;40:562-73.
    Abstract/FREE Full Text
  26. ↵
    1. Kaplan SL,
    2. Hulten KG,
    3. Gonzalez BE,
    4. et al
    . Three-year surveillance of community-acquired Staphylococcus aureus infections in children. Clin Infect Dis 2005;40:1785-91.
    Abstract/FREE Full Text
  27. ↵
    1. Kaplan SL
    . Treatment of community-associated methicillin-resistant Staphylococcus aureus infections. Pediatr Infect Dis J 2005;24:457-8.
    CrossRefMedlineWeb of Science
  28. ↵
    1. Frank AL,
    2. Marcinak JF,
    3. Mangat PD,
    4. et al
    . Clindamycin treatment of methicillin-resistant Staphylococcus aureus infections in children. Pediatr Infect Dis J 2002;21:530-4.
    CrossRefMedlineWeb of Science
  29. ↵
    1. Iyer S,
    2. Jones DH
    . Community-acquired methicillin-resistant Staphylococcus aureus skin infection: a retrospective analysis of clinical presentation and treatment of a local outbreak. J Am Acad Dermatol 2004;50:854-8.
    CrossRefMedlineWeb of Science
  30. ↵
    Minnesota Department of Health. Community-associated methicillin-resistant Staphylococcus aureus in Minnesota. Minnesota Department of Health Disease Control Newsletter 2004;32:61-72.
  31. ↵
    1. Charlson ME,
    2. Pompei P,
    3. Ales KL,
    4. MacKenzie CR
    . A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987;40:373-83.
    CrossRefMedlineWeb of Science
  32. ↵
    1. Ware J Jr,
    2. Kosinski M,
    3. Keller SD
    . A 12-item short-form health survey: construction of scales and preliminary tests of reliability and validity. Med Care 1996;34:220-33.
    CrossRefMedlineWeb of Science
  33. ↵
    1. Llera JL,
    2. Levy RC
    . Treatment of cutaneous abscess: a double-blind clinical study. Ann Emerg Med 1985;14:15-9.
    CrossRefMedlineWeb of Science
  34. ↵
    1. Lee MC,
    2. Rios AM,
    3. Aten MF,
    4. et al
    . Management and outcome of children with skin and soft tissue abscesses caused by community-acquired methicillin-resistant Staphylococcus aureus. Pediatr Infect Dis J 2004;23:123-7.
    MedlineWeb of Science
  35. ↵
    1. Lee NE,
    2. Taylor MM,
    3. Bancroft E,
    4. et al
    . Risk factors for community-associated methicillin-resistant Staphylococcus aureus skin infections among HIV-positive men who have sex with men. Clin Infect Dis 2005;40:1529-34.
    Abstract/FREE Full Text
  36. ↵
    Methicillin-resistant Staphylococcus aureus infections among competitive sports participants—Colorado, Indiana, Pennsylvania, and Los Angeles County, 2000–2003. MMWR Morb Mortal Wkly Rep 2003;52:793-5.
    Medline
  37. ↵
    1. Baggett HC,
    2. Hennessy TW,
    3. Rudolph K,
    4. et al
    . Community-onset methicillin-resistant Staphylococcus aureus associated with antibiotic use and the cytotoxin Panton-Valentine leukocidin during a furunculosis outbreak in rural Alaska. J Infect Dis 2004;189:1565-73.
    Abstract/FREE Full Text
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  1. Clin Infect Dis. (2007) 44 (4): 483-492. doi: 10.1086/511041
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