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Previous Volume 352:1436-1444 April 7, 2005 Number 14 Next

Abstract PDF PDA Full Text PowerPoint Slide Set Supplementary Material Editorial by Chambers, H. F. Letters Add to Personal Archive Add to Citation Manager Notify a Friend E-mail When Cited E-mail When Letters Appear Related Article PubMed Citation

ABSTRACT

Background Methicillin-resistant Staphylococcus aureus (MRSA) infection has emerged in patients who do not have the established risk factors. The national burden and clinical effect of this novel presentation of MRSA disease are unclear.

Methods We evaluated MRSA infections in patients identified from population-based surveillance in Baltimore and Atlanta and from hospital-laboratory–based sentinel surveillance of 12 hospitals in Minnesota. Information was obtained by interviewing patients and by reviewing their medical records. Infections were classified as community-acquired MRSA disease if no established risk factors were identified.

Results From 2001 through 2002, 1647 cases of community-acquired MRSA infection were reported, representing between 8 and 20 percent of all MRSA isolates. The annual disease incidence varied according to site (25.7 cases per 100,000 population in Atlanta vs. 18.0 per 100,000 in Baltimore) and was significantly higher among persons less than two years old than among those who were two years of age or older (relative risk, 1.51; 95 percent confidence interval, 1.19 to 1.92) and among blacks than among whites in Atlanta (age-adjusted relative risk, 2.74; 95 percent confidence interval, 2.44 to 3.07). Six percent of cases were invasive, and 77 percent involved skin and soft tissue. The infecting strain of MRSA was often (73 percent) resistant to prescribed antimicrobial agents. Among patients with skin or soft-tissue infections, therapy to which the infecting strain was resistant did not appear to be associated with adverse patient-reported outcomes. Overall, 23 percent of patients were hospitalized for the MRSA infection.

Conclusions Community-associated MRSA infections are now a common and serious problem. These infections usually involve the skin, especially among children, and hospitalization is common.

Over the past 40 years, MRSA infections have become endemic in most U.S. hospitals^1,2 and hospitals worldwide,⁷ striking, with rare exception, only patients with established risk factors.^8,9 More recently, however, MRSA infections have been described in patients without established risk factors who are living in the community.^{10,11,12,13,14,15,16,17,18,19} The current approach to suspected cases of community-associated (also referred to as community-acquired) S. aureus infections (suggested by findings of furuncles, abscesses, or cellulitis) commonly includes empirical treatment with -lactam antibiotics. This approach may need to be reconsidered if community-associated MRSA becomes a clinically significant pathogen.

The Centers for Disease Control and Prevention (CDC) and three sites participating in the Emerging Infections Program began a specialized MRSA surveillance project in 2001 using the Active Bacterial Core Surveillance program, a population-based surveillance component of the Emerging Infections Program Network designed to study the epidemiologic features of invasive bacterial disease and to track drug resistance in the United States. We used these data to evaluate the incidence of endemic community-associated MRSA infection, racial disparities in the incidence, patterns of antimicrobial susceptibility, and clinical outcomes in several areas in the United States.

Methods

Surveillance Population

The MRSA Active Bacterial Core Surveillance project monitored all MRSA isolates from all body sites from patients in 11 Baltimore hospitals serving a population of 700,000; Health District 3 in greater Atlanta, comprising eight counties with a total population of 3.3 million; and 12 sentinel hospital–based laboratories representative of the state in Minnesota (6 rural and 6 urban, representing 16 percent of the licensed hospital beds in the state). Laboratories served both outpatient clinic networks and hospital inpatients; sites in Atlanta included several referral laboratories serving predominantly ambulatory care settings. Surveillance was performed consecutively for 12 months in Baltimore (beginning February 2002), 18 months in Atlanta (beginning July 2001), and 24 months in Minnesota (beginning January 2001). In Baltimore, 1 of 12 eligible hospitals declined to participate in the MRSA study; however, this omission would be unlikely to have a substantial effect. The laboratory in that hospital historically reports only about 5 percent of the cases of infections with other pathogens under surveillance as part of the Active Bacterial Core Surveillance system in Baltimore.

Case Definitions and Ascertainment

A community-associated MRSA isolate was defined as an MRSA isolate recovered from a clinical culture from a patient residing in the surveillance area who had no established risk factors for MRSA infection. Established risk factors included the isolation of MRSA two or more days after hospitalization; a history of hospitalization, surgery, dialysis, or residence in a long-term care facility within one year before the MRSA-culture date; the presence of a permanent indwelling catheter or percutaneous medical device (e.g., tracheostomy tube, gastrostomy tube, or Foley catheter) at the time of culture; or previous isolation of MRSA. We reviewed the medical records of patients with suspected community-associated MRSA isolates to identify risk factors for infection. We attempted to interview by telephone all patients for whom no risk factors were identified to confirm the absence of established risk factors and to obtain a brief history of the clinical outcome. At least 15 attempts were made, after which suspected community-associated MRSA isolates were classified as confirmed in the case of patients who were successfully interviewed and confirmed to have no established risk factors or as probable in the case of patients who were not interviewed but who had no established risk factors on a review of medical records. The remaining isolates were classified as either health care–associated when established risk factors were identified or indeterminate if no information on the patient could be obtained.

A case of community-associated MRSA disease was defined as illness compatible with staphylococcal disease in a patient residing in the surveillance areas and isolation of community-associated MRSA from a clinically relevant site. Only a subgroup of patients with community-associated MRSA isolates had actual disease and achieved case status.

To identify cases, surveillance personnel routinely contacted all clinical microbiology laboratories serving residents of each catchment area regarding MRSA isolated from clinical cultures (infection-control surveillance cultures were excluded). Periodic audits of laboratory records were conducted by surveillance personnel to identify any unreported cases and ensure the completeness of reporting. Surveillance personnel collected information on patients using a standardized questionnaire that included demographic and isolate data on all MRSA isolates; information on antimicrobial-susceptibility testing (with results characterized as susceptible, intermediate, or resistant) and clinical characteristics were obtained from available medical records (e.g., emergency room, primary care, or hospital) only for patients with confirmed or probable community-associated MRSA isolates. The collection of additional data on disease outcome, employment status, household structure, socioeconomic status, and level of education was limited to patients with confirmed cases of community-associated MRSA disease.

The study was approved by the appropriate institutional review boards at the participating sites, including all participating Baltimore hospitals, the Maryland Department of Health and Mental Hygiene, Johns Hopkins University Bloomberg School of Public Health, the Georgia Department of Human Resources, Emory University School of Medicine, the Minnesota Department of Health, and the CDC. Oral informed consent was obtained from all those who were interviewed.

Statistical Analysis

Statistical analysis was conducted with SAS software (SAS Institute). Annual cumulative incidence rates were calculated, after adjustment for the study period at each site, with the use of projections of the 2001 and 2002 population from the Census Bureau. Initial therapy was categorized as active if the patient received an antimicrobial agent with activity against S. aureus and to which the MRSA was susceptible in vitro. Therapy was categorized as inactive if initial therapy consisted of antimicrobial agents to which the isolate had intermediate resistance on testing or was resistant in vitro. If the results of susceptibility testing were not available for a prescribed agent or the patient received no antimicrobial agents, the patient was excluded from analyses correlating inactive therapy and outcomes. The Mantel–Haenszel chi-square test was used to compare the incidence according to race and other categorical data, and the t-test was used for continuous data. All comparisons were initially stratified according to the reporting area, and rate ratios were pooled if there were no significant differences between areas according to the Breslow–Day test for homogeneity of the rate ratios.

Results

Surveillance

During the study period, 12,553 patients with MRSA isolates were reported. Of these patients, 9972 (79 percent) were immediately classified as having health care–associated MRSA infection and did not require interviews. Interviews were attempted with 2581 patients with suspected cases of community-associated MRSA infection; 1063 of these patients (41 percent) were interviewed, allowing 280 (11 percent) to be reclassified as having health care–associated MRSA. Among the remaining patients with suspected cases of community-associated MRSA infection, 2107 (17 percent) were classified as having confirmed or probable community-associated MRSA isolates (Atlanta, 1590 of 7819 [20 percent]; Minnesota, 370 of 3714 [12 percent]; and Baltimore, 147 of 1720 [8 percent]; P<0.001). MRSA isolates in 196 patients were classified as indeterminate (2 percent).

The overall incidence of invasive MRSA infection (i.e., MRSA recovered from a normally sterile site), regardless of whether the infection was acquired in the community or at a health care facility, was 19.3 infections per 100,000 population in Atlanta and 40.4 infections per 100,000 in Baltimore.

Of the 2107 confirmed or probable isolates of community-associated MRSA, 1647 (78 percent) were associated with clinical illness and were classified as cases of community-associated MRSA disease. Among these cases, the confirmed and the probable community-associated MRSA isolates were obtained from similar body sites and demonstrated similar susceptibilities to antimicrobial agents with one exception, i.e., there was variable sensitivity to erythromycin (details are provided in the Supplementary Appendix, available with the full text of this article at www.nejm.org). The annual incidence of community-associated MRSA disease in the two areas that performed population-based surveillance was 25.7 cases per 100,000 in Atlanta and 18.0 per 100,000 in Baltimore (rate ratio, 0.70; 95 percent confidence interval, 0.58 to 0.85) (Figure 1). In both surveillance areas, the incidence was significantly higher among persons who were less than two years old than among those who were two years of age or older (unadjusted relative risk, 1.51; 95 percent confidence interval, 1.19 to 1.92) (Figure 1). Incidence rates were significantly higher among blacks than whites in Atlanta among all age groups (age-adjusted relative risk, 2.74; 95 percent confidence interval, 2.44 to 3.07); racial differences in incidence were not significant in the Baltimore population, even in the youngest age group (relative risk, 2.58; 95 percent confidence interval, 0.31 to 21.5).

View larger version (12K): [in this window] [in a new window]   Figure 1. Incidence of Community-Associated MRSA Disease in Atlanta and Baltimore, According to Race and Age Group. The horizontal line in each graph is the overall site-specific annual incidence. Race was determined in most cases by study personnel.

 
Clinical Characteristics

The type of infection varied slightly among the surveillance areas (Table 1); of the 1647 patients with community-associated MRSA disease, most (1266 [77 percent]) were categorized as having skin or soft-tissue infections. Specific types included abscess in 751 patients (59 percent), cellulitis in 528 patients (42 percent), folliculitis in 88 patients (7 percent), and impetigo in 33 patients (3 percent). Among the other types of infection reported, 103 (6 percent) were invasive, including bacteremia, septic arthritis, and osteomyelitis; 157 were in wounds (10 percent); and 31 were pneumonia (2 percent) (Table 1).

View this table: [in this window] [in a new window]   Table 1. Infections and Outcomes Associated with Community-Associated MRSA Disease, 2001–2002.

 
Most patients (1333 [81 percent]) were treated with antimicrobial agents; specific antimicrobial agents were documented for 1297 patients (97 percent). Among these 1297 patients, 757 (58 percent) received -lactam antibiotics alone, 199 (15 percent) received a -lactam with a non–-lactam agent, and 341 (26 percent) received only non–-lactam therapy. Among the patients whose antibiotic regimens were documented, significantly more of the 1099 patients with skin infections than of the 198 patients with other types of infection received -lactam agents alone (64 percent vs. 28 percent, P<0.001).

Antimicrobial susceptibilities were obtained from the medical records of 1345 of the 1647 patients with community-associated MRSA disease (82 percent). With few exceptions, the patterns of susceptibility were similar among the study areas. However, isolates from patients in Atlanta and Baltimore were significantly less likely than those from Minnesota to be susceptible to erythromycin and ciprofloxacin (Table 2). Susceptibility data and documented information on empirical therapy were available for most patients who received empirical therapy (1215 of 1297 [94 percent]); 884 (73 percent) received inactive therapy.

View this table: [in this window] [in a new window]   Table 2. Number of Community-Associated MRSA Isolates That Were Susceptible to Selected Antimicrobial Agents, 2001–2002.

 
Limited information on the effect of the disease was available from the medical records; 506 patients (31 percent) were hospitalized, including 371 (23 percent) who were hospitalized specifically for MRSA disease (Table 1). For these 371 patients, hospitalization was unlikely to be the result of the clinician's receiving the MRSA-culture report. The interval between specimen collection and admission was less than one day for 226 of the 371 patients (61 percent), one to two days for 115 (31 percent), and more than two days for 22 (6 percent) (2 percent had missing data). A total of 37 patients (10 percent) required hospitalization in the intensive care unit. Hospitalization lasted a median of four days, and only 1 of the 37 patients who died during hospitalization had documentation that the community-associated MRSA was causal or contributory to the death.

Information on other outcomes associated with community-associated MRSA infection was available for 575 patients with confirmed cases (i.e., interviewed patients). Among these patients, 560 (97 percent) received some antimicrobial agents, 136 (24 percent) were hospitalized, 226 (39 percent) underwent incision and drainage, and 176 (31 percent) required a follow-up visit with their physician.

To assess the relationship between inactive antimicrobial therapy and outcome more closely, we attempted to identify a homogeneous group of patients in which to compare clinical outcomes on the basis of empirical antimicrobial treatment. We limited further analysis to 453 patients with confirmed cases of community-associated MRSA disease involving skin or soft-tissue infections who received antimicrobial therapy at the time of the isolation of community-associated MRSA and for whom information on initial treatment and clinical outcome was available from the interview. Neither initial incision and drainage nor initial antimicrobial therapy that was inactive was significantly associated with an increased frequency of the following patient-reported outcomes after the initial evaluation for illness: follow-up visits to a health care provider, subsequent incision and drainage, or subsequent change in antimicrobial therapy (Table 3). Also, among the subgroup of patients who did not initially undergo incision and drainage, there were no significant differences in outcomes according to whether the initial therapy was inactive (Table 3).

View this table: [in this window] [in a new window]   Table 3. Effect of Initial Therapy on Selected Outcomes among 453 Patients with Confirmed Skin or Soft-Tissue Infections Due to Community-Associated MRSA, 2001–2002.

 
Potential Exposures to MRSA

Although none of the established risk factors for MRSA infection were documented in any patient, 744 patients (45 percent) had underlying conditions or factors that were associated with skin infections or suggested some contact with the health care system. Among the 1250 patients whose age was known to be at least 18 years, 653 (52 percent) reported 1249 underlying conditions, including smoking (35 percent), previous skin infections (21 percent), diabetes (19 percent), asthma (12 percent), infection with the human immunodeficiency virus (HIV) (9 percent), intravenous drug use (7 percent), alcohol abuse (6 percent), and coronary vascular disease (5 percent). Among 345 patients who were younger than 18 years old, 76 (22 percent) reported 90 preexisting conditions, including skin disease (42 percent), asthma (35 percent), and smoking (7 percent). Among the 575 patients with confirmed community-associated MRSA disease, detailed information on household characteristics and employment status was obtained from the interview, and several points of contact with the health care system exclusive of established risk factors for MRSA infection were identified (Table 4).

View this table: [in this window] [in a new window]   Table 4. Frequency of Characteristics Potentially Related to Infection among 575 Patients with Confirmed Community-Associated MRSA Disease, 2001–2002.

 
Discussion

In this study, 8 to 20 percent of all MRSA isolates collected as part of prospective population-based surveillance were not associated with traditional risk factors and were classified as community-associated MRSA. Most of these isolates were associated with clinically relevant infections that required treatment. The most common infections involved skin and soft tissues; however, 6 percent were considered invasive. Attributable mortality was low, but 23 percent of patients were hospitalized for these infections.

The incidence of clinically relevant community-associated MRSA disease varied between the Atlanta surveillance area (25.7 per 100,000) and the Baltimore surveillance area (18.0 per 100,000), and we found marked disparity in the incidence of community-associated MRSA disease between blacks and whites in Atlanta but not in Baltimore, even among the youngest age group. Several reports have highlighted the increased incidence of staphylococcal disease among Pacific Islanders, American Indians, and Alaskan Natives.^16,18,22,23 Black race was associated with increased rates of invasive S. aureus disease in 1998 in one population-based study in Connecticut²⁴ and in other studies evaluating invasive pneumococcal disease.^25,26,27,28 The increased prevalence of certain underlying diseases (e.g., diabetes and HIV infection), differences in immune response, or differences in other socioeconomic factors (e.g., crowding in the household or decreased access to medical care), which are correlated with black race, may contribute to these findings.²⁹

The differences observed in incidence rates between Baltimore and Atlanta can probably be explained on the basis of the different populations under surveillance. The lower overall incidence of community-associated MRSA disease in Baltimore suggests that this surveillance population may be more likely to have established risk factors for MRSA infection. The incidence may also be falsely low, since 1 of 12 eligible laboratories declined to participate in the study. However, it is unlikely that the Baltimore surveillance underreported cases from the remaining laboratories, since the rates of invasive MRSA disease (regardless of whether the infection was acquired in the community or at a health care facility) were higher in Baltimore (40 per 100,000) than Atlanta (19 per 100,000). The Atlanta surveillance area encompassed an eight-county urban and suburban area and included a large referral laboratory; the Baltimore surveillance area was limited to urban hospital-based laboratories likely to serve persons with more frequent contact with the hospitals.

Our large, prospective series of community-associated MRSA infections identified with the use of standardized methods to measure rates of endemic disease allows for an accurate description of the clinical course and effect of these infections. In a manner consistent with previous reports from outbreaks and smaller surveillance studies, we found that most patients who were treated empirically received -lactam antimicrobial agents. Measuring the effect of inactive therapy on these infections has been difficult owing to the small numbers of cases and imprecise outcome measurements.^{30,31,32,33,34,35} Although we relied on self-reported measures, our data suggest that patients with community-associated MRSA skin or soft-tissue disease who initially receive inactive antimicrobial therapy have outcomes similar to those among patients who are treated with antimicrobial agents to which the organism is susceptible in vitro. Prospective evaluations with more objective measurements are needed to clarify whether the addition of active systemic therapy to topical agents or surgical drainage increases the beneficial effect in patients with community-associated MRSA infections involving the skin and soft tissues.

Our report reflects the results of one to two years of active surveillance in three large and diverse geographic areas. However, certain limitations should be borne in mind. First, we were unable to perform population-based estimates in Minnesota, where sentinel surveillance was conducted. However, the descriptive data probably reflect the patient mix in that state. Second, our surveillance required isolation of MRSA from a clinically relevant culture; since S. aureus skin disease is often treated empirically without a diagnostic test, our results probably underestimate the true burden of disease. Some caution must be taken in generalizing our findings to the U.S. population. First, we were able to interview only 41 percent of eligible patients, eliminating a majority of patients from the outcome analysis. Second, although there were rarely significant differences among the reporting areas, the majority of cases were reported in the Atlanta area. Also, patients who could not be interviewed may have been misclassified as having community-associated MRSA infection, since no interview data were available. However, we believe pooling the patients with probable and confirmed cases of community-associated MRSA disease was justified on the basis of the similarities between both patients' and isolates' characteristics, reflecting a pattern typically seen in previously reported outbreaks of community-associated MRSA infection.^{10,11,15,36,37,38}

To avoid clinical complications from community-acquired MRSA infections, clinicians should now consider MRSA as a potential pathogen in patients with suspected S. aureus infections in the community setting. Clinicians should obtain appropriate material for bacterial culture; should follow up on the results of susceptibility testing of all S. aureus isolates, since by definition MRSA organisms are not susceptible to -lactam antibiotics; and should recommend surgical drainage of infections when feasible. The choice of appropriate antimicrobial agents for suspected S. aureus infections of skin and soft tissue in patients in the community must now take into account the emergence of community-associated MRSA; providers should be aware that several available antimicrobial agents should be effective in treating these infections.

Supported by the CDC Emerging Infections Program. (The use of product names in this article does not imply their endorsement by the Public Health Service or the Department of Health and Human Services.)

We are indebted to Virginia Rego, Wendy Baughman, Christina Payne, Matthew Johns, Margaret Pass, Elizabeth Hopewell, Chris Van Beneden, Tami Hilger, Anne Schuchat, and personnel in hospitals and laboratories participating in the Community-Associated MRSA Special Project of the Active Bacterial Core Surveillance program for their contributions to this project.

Source Information

From the Division of Bacterial and Mycotic Diseases (S.K.F.) and Division of Healthcare Quality Promotion (J.C.H., M.M., J.A.J.), National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta; Emory University School of Medicine and the Veterans Affairs Medical Center, Atlanta (M.M., J.A.J., M.M.F.); Johns Hopkins University Bloomberg School of Public Health, Baltimore (L.T.S., L.H.H.); and the Minnesota Department of Health, Minneapolis (K.C.-S., K.H., R.L.).

Address reprint requests to Dr. Fridkin at the CDC, NCID, DBMD, MDB, MS C-09, 1600 Clifton Rd., NE, Atlanta, GA 30333, or at skf0{at}cdc.gov.

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Abstract PDF PDA Full Text PowerPoint Slide Set Supplementary Material Editorial by Chambers, H. F. Letters Add to Personal Archive Add to Citation Manager Notify a Friend E-mail When Cited E-mail When Letters Appear Related Article PubMed Citation

Related Letters:

MRSA in the Community
Chapman A. L.N., Greig J. M., Innes J. A., Hageman J. C., Lynfield R., Fridkin S. K., Miller L. G., Perdreau-Remington F., Spellberg B.
Extract | Full Text | PDF  
N Engl J Med 2005; 353:530-532, Aug 4, 2005. Correspondence

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