Community-Associated Methicillin-Resistant Staphylococcus aureus Skin and Soft Tissue Infections at a Public Hospital

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ORIGINAL INVESTIGATION

               Community-Associated Methicillin-Resistant
               Staphylococcus aureus Skin and Soft Tissue
               Infections at a Public Hospital
               Do Public Housing and Incarceration Amplify Transmission?
               Bala Hota, MD, MPH; Charlotte Ellenbogen, MD; Mary K. Hayden, MD; Alla Aroutcheva, MD, PhD;
               Thomas W. Rice, PhD; Robert A. Weinstein, MD

               Background: Community-associated methicillin-                           terval [CI], 1.00-3.67), African American race/ethnicity
               resistant Staphylococcus aureus (CA-MRSA) infections                    (OR, 1.91; 95% CI, 1.28-2.87), and residence at a group
               have emerged among patients without health care–                        of geographically proximate public housing complexes
               associated risk factors. Understanding the epidemiology                 (OR, 2.50; 95% CI, 1.25-4.98); older age was inversely
               of CA-MRSA is critical for developing control measures.                 related (OR, 0.89; 95% CI, 0.82-0.96 [for each decade
                                                                                       increase]). Of 73 strains tested, 79% were pulsed-field
               Methods: At a 464-bed public hospital in Chicago and                    gel electrophoresis type USA300.
               its more than 100 associated clinics, surveillance of soft
               tissue, abscess fluid, joint fluid, and bone cultures for               Conclusions: Clonal CA-MRSA infection has emerged
               S aureus was performed. We estimated rates of infection                 among Chicago’s urban poor. It has occurred in addi-
               and geographic and other risks for CA-MRSA through                      tion to, not in place of, methicillin-susceptible S aureus
               laboratory-based surveillance and a case-control study.                 infection. Epidemiological analysis suggests that con-
                                                                                       trol measures could focus initially on core groups that
               Results: The incidence of CA-MRSA skin and soft tis-                    have contributed disproportionately to risk, although
               sue infections increased from 24.0 cases per 100 000                    CA-MRSA becomes endemic as it disseminates within
               people in 2000 to 164.2 cases per 100 000 people in 2005                communities.
               (relative risk, 6.84 [2005 vs 2000]). Risk factors were in-
               carceration (odds ratio [OR], 1.92; 95% confidence in-                  Arch Intern Med. 2007;167:1026-1033

                                                  S
                                                                 INCE 1998, COMMUNITY -               help identify specific high-risk commu-
                                                                associated methicillin-               nity settings and groups.
                                                                resistant Staphylococcus au-             We conducted surveillance at a public
                                                                reus (CA-MRSA) infections             health care system for patients with CA-
                                                                have emerged among patient            MRSA isolated from soft tissue, abscess,
                                                  groups with risk factors unassociated with          joint, or bone specimens. We examined
                                                  health care, including sports exposure,1-5 in-      strain clonality, effect of community over-
                                                  carceration,6-10 intravenous drug use,11 over-      crowding and group housing, and changes
                                                  crowded housing,12-16 tattooing,17,18 and           in rates and geographic distribution of in-
                                                                                                      fection with CA-MRSA during 6 years, and
                                                     CME course available at                          we evaluated risk factors for infection in
                                                                                                      a nested case-control study.
                                                     www.archinternmed.com
               Author Affiliations: Division of                                                                         METHODS
               Infectious Diseases, Department    poor hygiene.11-13,19 An understanding of
               of Medicine, Rush University       factors promoting acquisition and emer-
               Medical Center (Drs Hota,          gence of CA-MRSA may aid in the devel-                                SETTING
               Ellenbogen, Hayden,                opment of prevention strategies. For some
               Aroutcheva, and Weinstein) and     infectious diseases, such as sexually trans-        The study was performed at John H. Stroger,
               Division of Infectious Diseases,                                                       Jr Hospital of Cook County (CCH), a 464-
               Department of Medicine,
                                                  mitted infections, transmission can occur           bed public hospital in Chicago, Ill, and its more
               John H. Stroger, Jr Hospital of    via infected core groups that contribute dis-       than 100 associated clinics; CCH primarily
               Cook County (Drs Hota,             proportionately to new cases.20 Surveil-            serves the urban poor (ie, uninsured or indi-
               Aroutcheva, Rice, and              lance of the geographic distribution and            gent individuals) in Cook County. The mean
               Weinstein), Chicago, Ill.          secular trends of CA-MRSA infection may             annual patient care volumes from 2001 through

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2004 were 749 992 clinic visits, 146 316 emergency depart-                      Community-associated methicillin-resistant S aureus iso-
               ment visits, and 23 041 hospital admissions.                               lates from patients with cultures performed on or after January
                  The study was reviewed by our institutional review board.               1, 2004, were available for further analysis. Isolates from pa-
               The need for informed consent was waived.                                  tients with recent incarceration, with cultures performed in July
                                                                                          2004, or with residence within the borders of 2 specific geo-
                                    CASE DEFINITION                                       graphic clusters were studied for pulsed-field gel electrophore-
                                                                                          sis type, staphylococcal chromosome cassette mec type, and pres-
               Using a previously validated electronic case definition (␬ statis-         ence of the Panton-Valentine leukocidin genes28-31 to assess
               tic, 0.97 [100% sensitive and 97% specific for community-                  clonality among isolates clustered geographically, temporally, and
               associated infection compared with medical record review]),21              with a common exposure (eg, incarceration). Antibiogram data
               we identified individuals without health care exposures with com-          were used to examine isolates before January 1, 2004.
               munity-onset S aureus infections. Individuals older than 1 year
               with MRSA or methicillin-susceptible S aureus (MSSA) grow-                                  STATISTICAL ANALYSIS
               ing from microbiological cultures of soft tissue, abscess fluid, joint
               fluid, or bone with (1) culture obtained while an outpatient or            Prevalence (the number of positive culture results divided by
               within the first 3 days of a hospitalization, (2) no clinical isolate      the number of cultured patients) and incidence (the number
               of MRSA in the last 6 months, (3) no hospitalization or surgery            of positive culture results among Cook County patients seen
               within 1 year, and (4) no hemodialysis were designated as hav-             at CCH divided by the CCH catchment population residing in
               ing community-associated infection; all other infections were de-          Cook County) of infection with CA-MRSA or CA-MSSA were
               fined as health care–associated infection.22,23 Only the first iso-        calculated. The CCH catchment population was calculated from
               late from a patient within 6 months was counted as CA-MRSA                 an estimation of the proportion of all Cook County residents
               or CA-MSSA.                                                                who seek care at CCH. This proportion was determined by di-
                                                                                          viding the number of Cook County residents hospitalized at
                                      STUDY DESIGN                                        CCH in 2004 for infections of skin or subcutaneous tissue or
                                                                                          erysipelas (International Classification of Diseases, Ninth Revi-
               Using the electronic case definition, we conducted surveil-                sion code 035 or 680-686) by the number with these diag-
               lance from January 1, 2000, through August 31, 2005, among                 noses hospitalized at all Cook County hospitals in that year,
               a cohort of individuals infected with community-associated                 stratified by ZIP code of residence. Data for all Cook County
               S aureus in clinical cultures of soft tissue, abscess fluid, joint         hospitalizations were obtained from the Illinois Hospital As-
               fluid, or bone specimens. Isolates were obtained from patients             sociation; 2004 was chosen because it was the first year avail-
               seen at the CCH emergency department, at affiliated clinics,               able with complete data. The proportion for each ZIP code was
               or on CCH inpatient wards. These clinical infection sites were             then multiplied by the total number of residents in each ZIP
               selected because they account for more than 90% of infections              code as reported in the most recent US census ZIP code tabu-
               and have a low likelihood of attribution to nosocomial acqui-              lation areas from 2000; these values were summed for all ZIP
               sition (ie, from intravenous catheters).                                   codes in Cook County to produce an unadjusted estimate of
                   A nested case-control study was conducted using CA-                    the catchment population for CCH.32 Two hundred nineteen
               MRSA cases compared with CA-MSSA controls. Cases and con-                  patients with addresses outside of Cook County or without ad-
               trols were identified from September 1, 2001, through August               dresses (ie, homeless) were excluded for these calculations.
               31, 2004, to ensure complete data for all covariates.                          Addresses were geocoded using commercially available soft-
                                                                                          ware (Arcview 9.0; ESRI, Redlands, Calif ), and these data were
                                                                                          entered using SaTScan software version 5.1.33,34 Clusters of cases
                                   DATA COLLECTION                                        of CA-MRSA were detected by the Bernoulli method of the spa-
                                                                                          tial scan statistic35; this analysis was stratified into 4 periods be-
               Data were collected from our clinical data repository.24 Elec-             cause of a temporal trend among cases. The periods, chosen a priori
               tronic records were queried for presence of diabetes melli-                to create approximately equal time frames, were period 1 ( Janu-
               tus,25 human immunodeficiency virus, chronic renal insuffi-                ary1,2000,throughJune30,2001),period2(July1,2001,through
               ciency, and infection relapses within 1 year. Prior antimicrobial          December 31, 2002), period 3 (January 1, 2003, through June 30,
               use was determined from antimicrobial prescriptions from in-               2004), and period 4 ( July 1, 2004, through August 31, 2005).
               patient or outpatient pharmacies and were categorized as hav-                  To assess the effect of overcrowding on risk of infection with
               ing been given within 1 week or within 1 year to 1 week be-                CA-MRSA, we used the Cook County US Census Bureau 2000
               fore the culture date. Exposures to the Cook County Jail within            occupancy data (percentage of the population living with ⬎1
               1 year before positive culture results were obtained from ar-              person per room36) for the block group of a patient’s resi-
               rest records of the Cook County Department of Corrections.                 dence. Strata were created based on quartiles of level of over-
               Home addresses were obtained from electronic data; if mul-                 crowding after examination of the frequency distribution of per-
               tiple addresses were available for a patient, the address histori-         sons per room in the cohort. Counts of MRSA cases were
               cally closest to the culture results was used.                             compared with counts of MSSA cases and with counts of all
                                                                                          patients who had had cultures performed for each strata of over-
                            MICROBIOLOGICAL ANALYSIS                                      crowding. The association of public housing and overcrowd-
                                                                                          ing with CA-MRSA infection was assessed using the ␹2 statis-
               Clinical isolates were identified as S aureus using routine meth-          tic for univariate analysis.
               ods.26 Antimicrobial resistance was determined by automated                    Logistic regression was used to perform multivariate analy-
               broth microdilution (MicroScan; Dade Behring, West Sacra-                  sis, with presence or absence of CA-MRSA as the outcome vari-
               mento, Calif ). Isolates were considered resistant to methicil-            able. Variables were those with P⬍.15 on univariate analysis
               lin if the oxacillin minimum inhibitory concentration was at               and year of culture. Antimicrobial use was excluded from mul-
               least 4 µg/mL. Clindamycin resistance was determined in all                tivariate analysis because differences were only noted within 1
               periods by automated broth microdilution. Inducible clinda-                week of culture, which may have reflected therapy for active
               mycin resistance was determined by D test27 when requested                 infections. Interaction was assessed for comorbidities and re-
               by clinicians.                                                             cent incarceration, as was collinearity.37 Residence in public

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Year
                                                   2000                        2001                   2002                           2003                   2004               2005

                                  180                                                                                                                                                     180
                                            CA-MRSA Cases         CA-MRSA Incidence
                                            CA-MSSA Cases         CA-MSSA Incidence
                                  160                                                                                                                                                     160

                                  140                                                                                                                                                     140

                                                                                                                                                                                                No. of Cases per 100 000 People per Year
                                  120                                                                                                                                                     120
                   No. of Cases

                                  100                                                                                                                                                     100

                                   80                                                                                                                                                     80

                                   60                                                                                                                                                     60

                                   40                                                                                                                                                     40

                                   20                                                                                                                                                     20

                                    0                                                                                                                                                     0
                                        1      2          3   4      1     2          3   4   1   2          3     4        1    2          3   4   1   2          3   4   1    2     3
                                                                                                                 Quarter

               Figure 1. Counts and incidence of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) and community-associated methicillin-
               susceptible S aureus (CA-MSSA) skin and soft tissue infections among patients at John H. Stroger, Jr Hospital of Cook County (Illinois) from January 1, 2000,
               through August 31, 2005.

               housing regardless of period was used in multivariate analy-                                                CCH catchment population of 212 815, CA-MRSA skin
               sis, and interaction between period and residence was as-                                                   and soft tissue infections increased from 24.0 cases per
               sessed. Public housing units were categorized based on whether                                              100 000 people in 2000 to 164.2 cases per 100 000
               they were contained within clusters detected by SaTScan. Vari-                                              people in 2005, while the incidence of CA-MSSA skin
               ables were eliminated using backward elimination for P⬎.15.
                                                                                                                           and soft tissue infections was 90.7 cases per 100 000
               Statistical analyses were performed using SAS software ver-
               sion 8 (SAS institute, Cary, NC).                                                                           people in 2000 and 121.9 cases per 100 000 people in
                                                                                                                           2005. During this period, 56% of CA-MRSA infections
                                                                                                                           and 55% of CA-MSSA infections occurred in outpatients
                                                              RESULTS                                                      or in nonhospitalized emergency department patients,
                                                                                                                           while 44% of CA-MRSA infections and 45% of CA-MSSA
                                   LABORATORY-BASED SURVEILLANCE                                                           infections required hospitalization. There were 5 deaths
                                                                                                                           among CA-MSSA patients and 2 deaths among CA-
               During 6 years (January 1, 2000, through August 31, 2005),                                                  MRSA patients (mortality rates of 5 per 1000 and 1 per
               soft tissue, abscess fluid, joint fluid, or bone specimens from                                             1000, respectively).
               2346 (34.0%) of 6894 patients without health care–
               associated risk factors grew S aureus; 971 (41.4%) and 1375
                                                                                                                                                GEOGRAPHIC ANALYSIS
               (58.6%) isolates met our previously defined criteria for
               CA-MRSA and CA-MSSA, respectively. Community-
               associated methicillin-resistant S aureus isolates were                                                     Geographic analysis revealed 4 clusters of CA-MRSA in-
               mostly susceptible to aminoglycosides (95%), fluoroqui-                                                     fections (Figure 2). Cluster 1 (July 1, 2001, through
               nolones (76%), and trimethoprim-sulfamethoxazole                                                            December 31, 2002) had 15 patients with CA-MRSA
               (99%). Erythromycin resistance steadily increased from                                                      (10.7% of that period’s cases). Cluster 2 (January 1, 2003,
               51% in 2000 to 87% in 2004; erythromycin-resistant and                                                      through June 30, 2004) had 17 patients with CA-MRSA
               clindamycin-susceptible strains accounted for most of                                                       (6.4% of cases). Cluster 3 (January 1, 2003, through June
               this increase (25%, 28%, 54%, 69%, 80%, and 81% of                                                          30, 2004) had 44 patients with CA-MRSA (15.0% of
               CA-MRSA isolates during 2000, 2001, 2002, 2003, 2004,                                                       cases). Within the borders of cluster 3 were 5 high-rise
               and 2005, respectively). D test results were available for                                                  public housing complexes; 8 (18.2%) of 44 patients within
               47 isolates (performed between 2004 and 2005) and were                                                      cluster 3 were residents of this housing. Cluster 4 (July
               positive in only 2.                                                                                         1, 2004, through August 31, 2005) included a region with
                  Over time, CA-MRSA skin and soft tissue infections                                                       its center near CCH and a perimeter that included the
               increased 6.84-fold (Figure 1). Based on the estimated                                                      geographic area with the highest CCH use in Cook

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Cluster 3

                                                                                                Cluster 1

                        ZCTA Population at Risk
                                                                                                            Cluster 4
                                 0%

                                 0.1%-1.0%

                                 1.1%-1.5%

                                 1.6%-2.6%

                                                                                                                                                         Cluster 2
                                 2.7%-3.5%

                                 3.6%-5.8%

                                 5.9%-9.4%

                                 >9.4%

               Figure 2. John H. Stroger, Jr Hospital of Cook County (CCH) catchment by ZIP code tabulation area (ZCTA). Clusters of methicillin-resistant Staphylococcus
               aureus skin and soft tissue infections in Cook County (Illinois) from January 1, 2000, through August 31, 2005, identified by SaTScan. Cluster 1, P = .004; cluster
               2, P = .03; cluster 3, P =.06; and cluster 4, P=.004. See the “Geographic Analysis” subsection of the “Methods” section for explanation of cluster groups.

               County; 185 patients with CA-MRSA (47.1% of cases)                                    through 2005, which was statistically significant in 2005
               were within this cluster.                                                             (P⬍.001) (Figure 3).
                                                                                                        We found no association between case status and over-
                         RISKS OF PUBLIC HOUSING,                                                    crowding; patients with S aureus infections from census
                    INCARCERATION, AND OVERCROWDING                                                  block groups that were more overcrowded were not more
                                                                                                     likely to be infected with CA-MRSA. Similarly, we found
               The proportion of community-associated S aureus skin                                  no association between high-occupancy block groups and
               and soft tissue isolates that was methicillin resistant was                           CA-MRSA infection regardless of whether the compari-
               higher among residents who lived in public housing com-                               son group was patients with CA-MSSA infections or all
               plexes in cluster 3 (55.4%) than among non–public hous-                               patients from whom cultures were obtained, nor did we
               ing residents (41.6%). Public housing residents in clus-                              find an association when occupancy was stratified by race/
               ter 3 had a higher prevalence of CA-MRSA from 2000                                    ethnicity or by year of culture.

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Table 1. Univariate Analysis of Demographic and Clinical
                                         Non–Public Housing
                                         Cluster 3 Public Housing
                                                                                                            Characteristics of Patients With Community-Associated
                                100      Non–Cluster 3 Public Housing                                       Staphylococcus aureus Skin and Soft Tissue Infections
                                                                                                            From September 1, 2001, Through August 31, 2004*

                                 75                                                                                                            CA-MRSA       CA-MSSA
                                                                                                            Characteristic                     (n = 518)     (n = 704)    P Value
                   CA-MRSA, %

                                                                                                            Age, mean ± SD, y                  35.4 ± 7.0   39.5 ± 18.2    ⬍.001
                                 50                                                                         Male-female ratio                     1:6           1:82        .30
                                                                                                            Race/ethnicity
                                                                                                               African American                389 (75.1) 372 (52.8)
                                                                                                              White                             45 (8.7)   88 (12.5)
                                 25                                                                                                                                        ⬍.001
                                                                                                              Hispanic                          62 (12.0) 177 (25.1)
                                                                                                              Other                             22 (4.2)   67 (9.5)
                                                                                                            Incarceration within 1 y†           32 (6.2)   22 (3.1)          .007
                                  0                                                                         Residence in public housing         21 (4.1)   14 (2.0)          .04
                                      2000       2001        2002          2003   2004   2005                 within cluster 3‡
                                                                    Year                                    Degree of overcrowding in
                                                                                                              census block group of
               Figure 3. Community-associated methicillin-resistant Staphylococcus                            patients, % of units with more
               aureus (CA-MRSA) as a proportion of all community-associated S aureus                          than 1 person per room§
               skin and soft tissue infections in relation to public housing from January 1,                     0-5.1                         119 (24.7)   158 (25.2)
               2000, through August 31, 2005. CI indicates confidence interval. See the                          ⬎5.1-11.1                     132 (27.4)   148 (23.6)
                                                                                                                                                                             .08
               “Geographic Analysis” subsection of the “Methods” section for explanation                         ⬎11.1-18.5                    134 (27.9)   147 (23.5)
               of cluster groups.                                                                                ⬎18.5                          96 (20.0)   163 (26.0)
                                                                                                            Diabetes mellitus㛳                 118 (22.8)   235 (33.4)     ⬍.001
                                                                                                            Human immunodeficiency virus        49 (9.5)     44 (6.3)       .04
                                      NESTED CASE-CONTROL STUDY                                               infection¶
                                                                                                            Chronic renal insufficiency          4 (0.8)      9 (1.3)        .39
               On univariate analysis, the following variables were as-                                     Associated bacteremia               11 (2.1)     12 (1.7)        .75
               sociated with CA-MRSA skin and soft tissue infections:                                       Relapse
               younger age, incarceration within 1 year, African Ameri-                                       ⬍1 mo                              9 (1.7)     18 (2.6)        .43
               can race/ethnicity, and human immunodeficiency virus                                           1 mo to ⬍6 mo                     25 (4.8)     39 (5.5)        .61
                                                                                                              6 mo to 1 y                       12 (2.3)     14 (2.0)        .69
               infection (Table 1). More patients with CA-MRSA re-
               ceived an antibiotic within 1 week before cultures were                                     Abbreviations: CA-MRSA, community-associated methicillin-resistant
               performed (9% vs 6%, P =.03), and 44% of patients with                                    Staphylococcus aureus; CA-MSSA, community-associated
               CA-MRSA infections received inadequate therapy with                                       methicillin-susceptible S aureus.
               a ␤-lactam antibiotic following culture (no differences                                     *Data are given as number (percentage) unless otherwise indicated.
                                                                                                           †Odds ratio, 2.04; 95% confidence interval, 1.13-3.69.
               in deaths or readmissions were noted as a result of in-                                     ‡Odds ratio, 2.06; 95% confidence interval, 1.03-4.09.
               adequate therapy). Residence in the 5 public housing com-                                   §The numbers of subjects differ for this variable because of missing data
               plexes within cluster 3 during any period was associ-                                     (MRSA, 481 subjects; MSSA, 626 subjects).
                                                                                                            㛳Odds ratio, 0.59; 95% confidence interval, 0.45-0.77.
               ated with CA-MRSA skin and soft tissue infections on                                        ¶Odds ratio, 1.57; 95% confidence interval, 1.00-2.45.
               univariate analysis, while residence in public housing de-
               velopments outside of cluster 3 was not.
                                                                                                         cently incarcerated subjects, 8 of 11 isolates from cluster
                                         MULTIVARIATE ANALYSIS
                                                                                                         2, 16 of 23 isolates from cluster 3, and 24 of 28 isolates
                                                                                                         obtained in July 2004). USA300 isolates were erythro-
               On multivariate analysis (Table 2), year of culture
                                                                                                         mycin resistant, did not carry inducible clindamycin re-
               showed a strong secular trend. Residence in the public
                                                                                                         sistance, and were positive for staphylococcal chromo-
               housing complexes within cluster 3 was also a risk fac-
                                                                                                         some cassette mec type IV and Panton-Valentine
               tor for MRSA skin and soft tissue infections (odds ratio,
                                                                                                         leukocidin genes. USA400 strains were found in 6 infec-
               2.50; 95% confidence interval, 1.25-4.98) regardless of
                                                                                                         tions. Regardless of pulsed-field gel electrophoresis type,
               year of culture, as was recent incarceration (odds ratio,
                                                                                                         most isolates from all groups were positive for staphy-
               1.92; 95% confidence interval, 1.00-3.67). African Ameri-
                                                                                                         lococcal chromosome cassette mec type IV (67 of 73) and
               can race/ethnicity increased the risk of CA-MRSA infec-
                                                                                                         Panton-Valentine leukocidin genes (65 of 73).
               tion, and older age and Hispanic race/ethnicity were pro-
               tective. Human immunodeficiency virus status and recent
               incarceration exhibited interaction and resulted in de-                                                                 COMMENT
               creased risk when both were present.
                                                                                                         In the major public safety net health care system of Cook
                                      MICROBIOLOGICAL ANALYSIS                                           County, we noted a 6.84-fold increase in the risk of skin
                                                                                                         and soft tissue infections with CA-MRSA from 2000 through
               Community-associated methicillin-resistant S aureus iso-                                  2005. This increase occurred in addition to a stable rate of
               lates tested were predominantly pulsed-field gel electro-                                 CA-MSSA infections. Although at the start of the surveil-
               phoresis type USA300 (ie, 10 of 11 isolates from re-                                      lance period our incidence of CA-MRSA infections was simi-

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lar to that found in a recent multicity population-based
               study,23 by 2005 it was higher, which may reflect our high-               Table 2. Multivariate Analysis of Risk Factors
               risk patient population (62% African American, 5% re-                     for Community-Associated Methicillin-Resistant
                                                                                         Staphylococcus aureus Skin and Soft Tissue Infections
               cent incarceration, and 6% public housing residents).
                  African American race/ethnicity and recent incarcera-                                                          Odds Ratio
               tion were risk factors for CA-MRSA skin and soft tissue                                                        (95% Confidence
               infections; Hispanic race/ethnicity was protective, a find-               Risk Factor                              Interval)       P Value
               ing consistent with the results of prior studies.6-10,23,38 Resi-         Age, each decade increase, y          0.89 (0.82-0.96)     .004
               dence in specific public housing complexes was also a                     Diabetes mellitus                     0.75 (0.55-1.02)     .07
               risk factor and increased the odds of CA-MRSA infec-                      HIV infection                         1.45 (0.91-2.31)     .12
               tion almost 3-fold (Table 2), even after adjustment for                   Incarceration within 1 y              1.92 (1.00-3.67)     .05
               the countywide secular increase.                                          HIV-positive and incarceration        0.16 (0.04-0.71)     .03
                                                                                           within 1 y
                  Why CA-MRSA has emerged at such a rapid pace re-
                                                                                         Race/ethnicity
               mains unclear. Cross-sectional studies38,39 examining other                 Other                               0.62 (0.33-1.17)     .14
               community populations have found MRSA colonization                          Hispanic                            0.61 (0.37-0.99)     .048
               rates far below those of MSSA, generally not exceeding                      African American                    1.91 (1.28-2.87)     .002
               4% for CA-MRSA compared with 30% for CA-MSSA. De-                           White                               1 [Reference]        ...
               spite the apparently lower prevalence of MRSA coloni-                     Culture obtained
                                                                                           August 2003 to July 2004            2.77 (2.04-3.75)   ⬍.001
               zation, infection rates are approaching or exceeding those
                                                                                           August 2002 to July 2003            1.94 (1.39-2.69)   ⬍.001
               of CA-MSSA. Potential host or pathogen explanations for                     August 2001 to July 2002            1 [Reference]       ...
               this discordance include CA-MRSA colonization at sites                    Residence
               not tested (eg, skin, gastrointestinal tract, or deeper than                Public housing in cluster 3         2.50 (1.25-4.98)     .009
               the anterior nares), greater risk of person-to-person spread                Public housing not in cluster 3     1.24 (0.58-2.67)     .57
               from infected patients or of spread from contaminated                       Not in public housing               1 [Reference]        ...
               fomites (eg, towels in locker rooms),3,40 virulence fac-
               tors (eg, Panton-Valentine leukocidin genes) that trump                   Abbreviation: HIV, human immunodeficiency virus.
               the traditional colonization before infection sequence (ie,
               “hit-and-run” infections),41 or yet-to-be-measured in-
               creasing rates of CA-MRSA colonization.42                               housing complexes,45 potentially contributing to over-
                  An additional explanation for rapid emergence of CA-                 crowding not measured by census data. In addition, pub-
               MRSA is that some community settings may promote                        lic housing residents are part of a network associated with
               cross-transmission. Hospitals and long-term care facili-                inmates; in a 2002 study,46 29% of respondents reported
               ties have long been considered “epicenters” for antimi-                 that they had been incarcerated or were expecting a
               crobial resistance, housing colonized and noncolonized                  resident to arrive from jail or prison. Public housing may
               individuals in close proximity, and offering the oppor-                 also house individuals with severe drug problems, and
               tunity for cross-transmission. Hartley et al43 suggested                squatters (or nonlease tenants) may transiently reside in
               that prisons, with their large at-risk populations and long             nondemolished public housing between episodes of home-
               lengths of stay, can be sources of MRSA-colonized indi-                 lessness.45 Triangulation of risks for CA-MRSA transmis-
               viduals at rates comparable to those of hospitals. Other                sion47 may occur in the public housing complexes iden-
               community settings such as public housing and halfway                   tified in cluster 3, with personal contacts or contaminated
               houses may amplify CA-MRSA spread; for example, the                     fomites promoting cross-transmission among suscep-
               geographic clusters of CA-MRSA detected in our study                    tible host populations. However, whether and what in-
               that were not related to public housing may represent                   teractions among these populations have contributed to
               foci of increased cross-transmission.                                   CA-MRSA dissemination require further study.
                  The concept of a “core group” of colonized or in-                        Strain typing by pulsed-field gel electrophoresis did
               fected individuals that is responsible for many new in-                 not discriminate between the various populations as-
               fections is basic to the epidemiology of sexually trans-                sessed in our study; however, it confirmed that most iso-
               mitted and some viral infections (eg, severe acute                      lates tested were strain type USA300, whether or not re-
               respiratory syndrome)20,44; geographically disparate clus-              lated to incarceration or public housing exposure. These
               ters of infection may represent networks of individuals                 findings are consistent with those of a 31⁄2-month labo-
               who transmit infection through person-to-person con-                    ratory-based survey from Atlanta, Ga,48 and a cross-
               tact, with further spread by individuals who bridge these               sectional study49 among emergency department pa-
               networks.44 In the case of CA-MRSA, geographically closed               tients in which most CA-MRSA skin and soft tissue
               community foci (eg, prisons) may be promoting spread,                   infections were caused by USA300.
               while other settings or factors (eg, athletics or intrave-                  Because of a lack of historical isolates available for typ-
               nous drug use) act as bridges for transmission.                         ing, we were unable to ascertain if USA300 replaced other
                  Public housing also may represent a bridge between                   CA-MRSA strains in the community. Prior work exam-
               high-risk individuals in Chicago. Since the late 1990s,                 ining CA-MRSA among Chicago children found clonal-
               demolition of high-rise public housing complexes and                    ity in one instance: 69 (78.4%) of 88 clindamycin-
               widespread relocation of public housing residents have                  susceptible CA-MRSA isolates obtained from 1987 to 2000
               occurred as part of the HOPE VI plan.45 In 2003, 62% of                 were USA400, 70% were erythromycin-susceptible, and
               relocated families were moved to other Chicago public                   D test results were positive in 31 of 33 isolates with dis-

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cordant erythromycin and clindamycin susceptibili-                     Hota, Rice, and Weinstein. Drafting of the manuscript: Hota
               ties.50 Prior work examining CA-MRSA among Chicago                     and Aroutcheva. Critical revision of the manuscript for im-
               children in one instance found clonality: 69 (78%) of 88               portant intellectual content: Hota, Ellenbogen, Hayden,
               clindamycin-susceptible CA-MRSA isolates obtained from                 Rice, and Weinstein. Statistical analysis: Hota. Obtained
               1987 to 2000 were USA-400, 70% were erythromycin-                      funding: Weinstein. Administrative, technical, and mate-
               susceptible, and D-test results were positive for 31 of 33             rial support: Ellenbogen, Aroutcheva, Rice, and Wein-
               isolates with discordant erythromycin and clindamycin                  stein. Study supervision: Weinstein.
               susceptiblities.50 In another instance, however, poly-                 Financial Disclosure: None reported.
               clonal infection was described.51 Given the rapid in-                  Previous Presentation: This study was presented in part
               creases among our patients in prevalence of clindamycin-               at the 45th Interscience Conference on Antimicrobial
               susceptible, erythromycin-resistant isolates and the low               Agents and Chemotherapy; December 14, 2005; Wash-
               rate of inducible clindamycin-resistance, replacement of               ington, DC (abstract L-142).
               another CA-MRSA strain (possibly USA400) by USA300                     Acknowledgment: Control strains for staphylococcal
               as the major cause of CA-MRSA infection seems to have                  chromosome cassette mec types and subtypes, Panton-
               occurred between 2000 and 2006 in our patients.                        Valentine leukocidin genes, and pulsed-field gel electro-
                   Our data should be interpreted in light of several epi-            phoresis were received from the Network for Antimicro-
               demiological limitations. First, geographic clustering                 bial Resistance in S aureus repository and from colleagues.
               among cases may have been because of the differences                   Cook County admission diagnosis information was ob-
               between cases and controls in the use of CCH unrelated                 tained through the assistance of the Illinois Hospital As-
               to infection status. The stability of MSSA rates over time             sociation. We appreciate the assistance of Ellen Holfels
               argues against systematic changes in health care use, and              in the preparation of the manuscript.
               Figure 3 shows that public housing complexes in clus-
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                                                                                                Correction

                                                                  Error in Figure Key. In the article titled “Community-
                                                                  Associated Methicillin-Resistant Staphylococcus aureus
                                                                  Skin and Soft Tissue Infections at a Public Hospital: Do
                                                                  Public Housing and Incarceration Amplify Transmis-
                                                                  sion?” by Hota et al, published in the May 28 issue of
                                                                  the Archives (2007;167[10]:1026-1033), the symbols for
                                                                  the right side of the key in Figure 1 (page 1028) should
                                                                  have been switched. Therefore, the circles indicate CA-
                                                                  MRSA incidence; squares, the CA-MSSA incidence. The
                                                                  online version of this article was corrected for typo-
                                                                  graphical errors on May 28, 2007.

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