Context Efforts to reduce the frequency of methicillin-resistant Staphylococcus aureus (MRSA) infections have failed until now. Contribution After a baseline year, the authors screened all intensive care unit admissions for MRSA colonization using polymerase chain reaction. In year 3, they screened all hospital admissions. They placed patients who tested positive for MRSA on contact precautions. The prevalence density of MRSA clinical infection was 8.9, 7.4, and 3.9 per 10000 patient-days in years 1, 2, and 3, respectively. Methicillin-sensitive S. aureus infection rates did not change. Caution There was no concomitant, unscreened control group. Implication Screening for MRSA colonization is associated with substantially reduced rates of MRSA clinical infection. The Editors Methicillin-resistant Staphylococcus aureus (MRSA) is now endemic in many U.S. hospitals (1, 2). Colonization with this organism is a risk factor for eventual MRSA clinical infection (3), which is associated with high cost (4) and poor clinical outcomes (5). The burden of health careassociated MRSA disease is high and may be increasing: In their multiregion survey of invasive MRSA disease, investigators for the Centers for Disease Control and Prevention noted substantial increases in both community- and health careassociated infections at several sites when comparing data from 2001 to 2002 with data from 2004 to 2005 (6). Driven by the emerging concern that community-associated MRSA has entered the hospital environment (7), the medical community and the public are seeking to limit the spread of this organism with increasing urgency (8). In the United Kingdom, the Department of Health has instituted mandatory reporting of MRSA infections in hospitals (9), and in the United States, state legislatures are considering (or have passed bills) requiring active surveillance for MRSA (1012). Consumer organizations (13) and the media (14) also seek action. The Healthcare Infection Control Practices Advisory Committee of the Centers for Disease Control and Prevention (15) recently published guidelines recommending expanded surveillance of asymptomatic patients in settings in which multidrug-resistant organisms are poorly controlled with other measures. However, the evidence supporting this practice is limited to surveillance on circumscribed (for example, intensive care only) populations in small, single-center studies at large academic hospitals (1618). Because rates of MRSA infection remained unacceptably high despite conventional interventions, we implemented expanded surveillance at our 3-hospital health care organization in 2 steps. For 12 months, we implemented organization-wide, intensive care unit (ICU)based MRSA surveillance. On 1 August 2005, we initiated the first program (to our knowledge) of universal surveillance of all hospital admissions in the United States. We aimed to determine whether expanded surveillance was associated with changes in the rate of MRSA clinical disease. Methods We measured the utility of expanded surveillance for MRSA by using a 3-period before-and-after design (Figure 1). Period 1 (no active surveillance) was the baseline. In periods 2 and 3, we introduced ICU-based surveillance and universal admission surveillance, respectively. We compared MRSA disease rates during and after hospitalization in the 3 periods. Figure 1. Intervention timeline. ICU = intensive care unit; MRSA = methicillin-resistant Staphylococcus aureus. Outcomes The primary outcome was aggregate hospital-associated MRSA infection rate, defined as the sum of all MRSA bloodstream, respiratory, urinary tract, and surgical site clinical infections occurring more than 48 hours after admission through day 30 after discharge. Secondary outcomes were rates of health careassociated MRSA and methicillin-susceptible Staphylococcus aureus (MSSA) bacteremia, rates of aggregate MRSA infections occurring up to 180 days after discharge, and adherence to MRSA surveillance. We defined adherence as the percentage of admissions (ICU or whole house, depending on the period) in which surveillance testing was done. Study Sites Evanston Northwestern Healthcare, Evanston, Illinois, is a 3-hospital organization with approximately 40000 annual admissions, 75 affiliated off-site offices, 450 staff physicians, and more than 1000 affiliated physicians. Hospital 1 is an academic facility with several residency programs, 476 beds, and a high proportion of surgical patients. Hospital 2 is a primary care teaching hospital with 143 beds that serves a large population of long-term care facility residents (the elderly) relative to the other 2 hospitals. Hospital 3 is a community hospital with 239 beds. The total number of ICU beds was 45 (5.2% of all beds). Surveillance, Isolation, and Decolonization During the baseline year (period 1), routine surveillance for MRSA colonization did not occur. Patients who were MRSA-colonized on the basis of clinical cultures were placed in contact isolation, and decolonization was not attempted. During all periods, contact isolation consisted of a private room or a shared room with another MRSA-colonized patient. Gowns and gloves were required for all room entries, and patient rooms were supplied with dedicated equipment (for example, stethoscopes) for staff use. During period 2, a policy of nasal surveillance for MRSA colonization was enforced for all ICU admissions. Test turnaround time was 2.5 days. Colonized patients were isolated; decolonization therapy was not standard policy. During period 3, a policy of nasal surveillance for MRSA colonization was enforced for all hospitalizations on entry into a ward room (that is, day 1 of admission). A nurse or patient care technician obtained the specimen. Average test turnaround time was 0.67 day. Nursing staff were notified of results by telephone. Adherence was promoted through in-service education for all nursing staff and educational rounds for physicians (19). During this period, we monitored adherence and provided feedback in real time to underperforming nursing units. The infection control department recommended treatment of colonized patients with a 5-day regimen comprising mupirocin calcium, 2% twice daily to the nares, and a chlorhexidine 4% wash or shower every 2 days during period 3. Patients who were discharged before therapy was complete were sent home with prescriptions to complete this regimen. Because we felt that the decision to decolonize should be at the discretion of the physician, we did not monitor adherence to decolonization, nor did we define it as an outcome of the study. However, we had access to pharmacy data for most patients who tested positive for MRSA during the first 12 months of period 3, and we used it to determine adherence to at least 1 chlorhexidine wash and 4 or more doses of mupirocin (a quantity that seems as effective as 10 doses [20]). Patients were not removed from isolation after decolonization therapy unless another test (done at least 7 days after decolonization therapy during the same hospitalization or on repeated hospitalization) was negative for MRSA. Laboratory Methods Polymerase chain reaction tests for S. aureus colonization have better sensitivity than culture-based assays, but they may yield more false-positive results (21). Real-time polymerase chain reaction was used for MRSA detection in periods 2 (22) and 3 (21). Our in-house method and the commercial assay (BD-GeneOhm real-time polymerase chain reaction test, Becton Dickinson, Franklin Lakes, New Jersey) have equal sensitivity (21, 22). For the commercial assay, we modified the package insert protocol for specimen processing to facilitate high-volume testing (21). Data Collection Demographic Characteristics Administrative data were used to determine admission, procedure, and demographic data for all patients hospitalized from 1 August 2003 to 30 April 2007. We used International Classification of Diseases, Ninth Revision, diagnostic and procedure codes to generate comorbidity data according to the method of Elixhauser and coworkers (23) with Healthcare Cost and Utilization Project comorbidity software, version 3.2 (Agency for Healthcare Research and Quality, Rockville, Maryland) (24). Infections To measure the effect of our intervention, we were interested in true clinical disease due to MRSA. Therefore, we reviewed the records of all patients with positive inpatient or outpatient clinical cultures for MRSA from 1 August 2003 to 30 April 2007. Infections were determined as follows: bacteremia = any positive blood culture; bloodstream infection = positive blood culture in the absence of a positive clinical culture from another site; respiratory tract infection = positive respiratory culture, compatible chest radiograph, and decision to treat; urinary tract infection = positive urine culture and either a decision to treat or growth of more than 100000 colony-forming units/mL plus at least 50 leukocytes per high-power field; and surgical site infection = positive culture of a surgical site. These infection types, although not encompassing all MRSA infections at our organization, represent the major body sites affected by culture-demonstrable MRSA disease. Our primary outcome measure was the rate of clinical hospital-associated MRSA infections. Infections occurring more than 2 days after the admission date and within 30 days after discharge were considered hospital-associated. Rates of hospital-associated MRSA and hospital-associated MSSA were expressed as prevalence density of infections, that is, the number of infections per 10000 inpatient-days. Patients were counted once every 30-day period. In a separate analysis of the timing of MRSA infections, disease prevalence (that is, infections per 10000 admissions) was measured during admission and in 6 postdischarge, 30-day time frames. Statistical Analysis Rates of MRSA Infection For 1 hospital-associated infection analysis, we compared infection
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