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 ARCH INTERN MED/ VOL 167, MAY 28, 2007 WWW.ARCHINTERNMED.COM 1026 ©2007 American Medical Association. All rights reserved. (REPRINTED WITH CORRECTIONS) Downloaded From: https://jamanetwork.com/ on 03/11/2022
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 ARCH INTERN MED/ VOL 167, MAY 28, 2007 WWW.ARCHINTERNMED.COM 1027 ©2007 American Medical Association. All rights reserved. (REPRINTED WITH CORRECTIONS) Downloaded From: https://jamanetwork.com/ on 03/11/2022
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 ARCH INTERN MED/ VOL 167, MAY 28, 2007 WWW.ARCHINTERNMED.COM 1028 ©2007 American Medical Association. All rights reserved. (REPRINTED WITH CORRECTIONS) Downloaded From: https://jamanetwork.com/ on 03/11/2022
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. ARCH INTERN MED/ VOL 167, MAY 28, 2007 WWW.ARCHINTERNMED.COM 1029 ©2007 American Medical Association. All rights reserved. (REPRINTED WITH CORRECTIONS) Downloaded From: https://jamanetwork.com/ on 03/11/2022
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- ARCH INTERN MED/ VOL 167, MAY 28, 2007 WWW.ARCHINTERNMED.COM 1030 ©2007 American Medical Association. All rights reserved. (REPRINTED WITH CORRECTIONS) Downloaded From: https://jamanetwork.com/ on 03/11/2022
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- ARCH INTERN MED/ VOL 167, MAY 28, 2007 WWW.ARCHINTERNMED.COM 1031 ©2007 American Medical Association. All rights reserved. (REPRINTED WITH CORRECTIONS) Downloaded From: https://jamanetwork.com/ on 03/11/2022
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- ter 3 consistently exhibited higher rates of MRSA isola- REFERENCES tion than other areas, suggesting a true and dispropor- tionate secular trend. 1. Herold BC, Immergluck LC, Maranan MC, et al. Community-acquired methicillin- Second, we may be missing data that explain our find- resistant Staphylococcus aureus in children with no identified predisposing risk. ings further. For example, the interaction of recent in- JAMA. 1998;279:593-598. 2. Begier EM, Frenette K, Barrett NL, et al. A high-morbidity outbreak of methicillin- carceration and human immunodeficiency virus positiv- resistant Staphylococcus aureus among players on a college football team, fa- ity that reduced the risk of CA-MRSA could be explained cilitated by cosmetic body shaving and turf burns. Clin Infect Dis. 2004;39: by prescription of trimethoprim-sulfamethoxazole pro- 1446-1453. phylaxis to patients with AIDS in the jail.52 3. Kazakova SV, Hageman JC, Matava M, et al. A clone of methicillin-resistant Staphy- Third, we relied on electronic records for defining lococcus aureus among professional football players. N Engl J Med. 2005; 352:468-475. health care exposure. In a prospective study by Furuno 4. Lindenmayer JM, Schoenfeld S, O’Grady R, Carney JK. Methicillin-resistant Staphy- et al,52 an electronic rule did not always reliably detect lococcus aureus in a high school wrestling team and the surrounding community. health care exposures. However, a distinction of our data Arch Intern Med. 1998;158:895-899. set is that CCH is the county’s largest provider of indi- 5. Stacey AR, Endersby KE, Chan PC, Marples RR. An outbreak of methicillin re- sistant Staphylococcus aureus infection in a rugby football team. Br J Sports gent care and likely sees a “loyal” population of pa- Med. 1998;32:153-154. tients. Validation of our rule found only a 3% misclas- 6. Centers for Disease Control and Prevention (CDC). Methicillin-resistant Staphy- sification rate,21 in contrast to 29% demonstrated by lococcus aureus skin or soft tissue infections in a state prison: Mississippi, 2000. Furuno et al.53 MMWR Morb Mortal Wkly Rep. 2001;50:919-922. In conclusion, among CCH patients, the rate of CA- 7. Centers for Disease Control and Prevention (CDC). Outbreaks of community- associated methicillin-resistant Staphylococcus aureus skin infections: Los An- MRSA skin and soft tissue infections increased rapidly geles County, California, 2002-2003. MMWR Morb Mortal Wkly Rep. 2003; between 2000 and 2005, adding significantly to the over- 52:88. all burden of staphylococcal disease. Incarceration and 8. Centers for Disease Control and Prevention (CDC). Methicillin-resistant Staphy- residence at some public housing complexes increased lococcus aureus infections in correctional facilities: Georgia, California, and Texas, 2001-2003. MMWR Morb Mortal Wkly Rep. 2003;52:992-996. the chance of infection with CA-MRSA, perhaps as a con- 9. Baillargeon J, Kelley MF, Leach CT, Baillargeon G, Pollock BH. Methicillin- sequence of the “epidemiological weight”43 of these lo- resistant Staphylococcus aureus infection in the Texas prison system. Clin In- cations. Whether strategies directed at prevention of trans- fect Dis. 2004;38:e92-e95. mission in these settings will be effective in slowing the 10. Pan ES, Diep BA, Carleton HA, et al. Increasing prevalence of methicillin- emergence of CA-MRSA remains to be determined. resistant Staphylococcus aureus infection in California jails. Clin Infect Dis. 2003; 37:1384-1388. 11. Charlebois ED, Bangsberg DR, Moss NJ, et al. Population-based community preva- Accepted for Publication: January 23, 2007. lence of methicillin-resistant Staphylococcus aureus in the urban poor of San Correspondence: Bala Hota, MD, MPH, Rush Univer- Francisco. Clin Infect Dis. 2002;34:425-433. sity Medical Center and John H. Stroger, Jr Hospital of 12. Groom AV, Wolsey DH, Naimi TS, et al. Community-acquired methicillin- resistant Staphylococcus aureus in a rural American Indian community. JAMA. Cook County, 637 S Wood St, Chicago, IL 60612 (bhota 2001;286:1201-1205. @rush.edu). 13. Shukla SK, Stemper ME, Ramaswamy SV, et al. Molecular characteristics of noso- Author Contributions: Dr Hota had full access to all of comial and Native American community-associated methicillin-resistant Staphy- the data in the study and takes responsibility for the in- lococcus aureus clones from rural Wisconsin. J Clin Microbiol. 2004;42:3752- tegrity of the data and the accuracy of the data analysis. 3757. 14. Campbell KM, Vaughn AF, Russell KL, et al. Risk factors for community-associated Study concept and design: Hota, Hayden, Aroutcheva, and methicillin-resistant Staphylococcus aureus infections in an outbreak of disease among Weinstein. Acquisition of data: Hota, Ellenbogen, military trainees in San Diego, California, in 2002. J Clin Microbiol. 2004;42:4050- Aroutcheva, and Rice. Analysis and interpretation of data: 4053. ARCH INTERN MED/ VOL 167, MAY 28, 2007 WWW.ARCHINTERNMED.COM 1032 ©2007 American Medical Association. All rights reserved. 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6. Fletcher KE, Davis SQ, Underwood W, Mangrulkar RS, McMahon LF, Saint S. surgical faculty: results of a multi-institutional study. Acad Med. 2006;81(1): Systematic review: effects of resident work hours on patient safety. Ann Intern 50-56. Med. 2004;141(11):851-857. 9. Hutter MM, Kellogg KL, Ferguson CM, Abbott WM, Warshaw AL. The impact of 7. Shojania KG, Fletcher KE, Saint S. Graduate medical education and patient safety: the 80-hour resident workweek on surgical residents and attending surgeons. a busy—and occasionally hazardous—intersection. Ann Intern Med. 2006; Ann Surg. 2006;243(6):864-875. 145(8):592-598. 10. Ryan J. Unintended consequences: the accreditation council for graduate edu- 8. Coverdill JE, Finlay W, Adrales GL, et al. Duty-hour restrictions and the work of cation work-hour rules in practice. Ann Intern Med. 2005;143(1):82-83. 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. (REPRINTED) ARCH INTERN MED/ VOL 167 (NO. 14), JULY 23, 2007 WWW.ARCHINTERNMED.COM 1455 ©2007 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 03/11/2022
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