Universal rapid screening for methicillin-resistant Staphylococcus aureus in the intensive care units in a large community hospital

American Journal of Infection Control 41 (2013) 45-50

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American Journal of Infection Control

American Journal of Infection Control

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Major article

Universal rapid screening for methicillin-resistant Staphylococcus aureus in the intensive care units in a large community hospital Rebecca Kjonegaard RN, MSN a, *, Willa Fields RN, DNS a, b, c, K. Michael Peddecord DrPH c a

Sharp Healthcare, San Diego, CA School of Nursing, San Diego State University, San Diego, CA c Graduate School of Public Health, San Diego State University, San Diego, CA b

Key Words: MRSA Health care-associated infections Cost Mandated screening Surveillance

Background: Health care-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) infections constitute a significant risk for hospitalized patients. This study evaluates the costs and effects of comprehensive and state-mandated MRSA screening for intensive care unit (ICU) patients and subsequent contact precautions on the rate of HA-MRSA. Methods: A pre- and postimplementation study was conducted in a 24-bed medical intensive care unit (MICU) and a 15-bed surgical intensive care unit (SICU) at an acute care 536-bed community hospital. This study used computerized records for all patients admitted to ICUs. Costs were estimated from financial records. Results: HA-MRSA infection rates did not decline after implementation of ICU screening. Regression analysis demonstrated that patients admitted from skilled nursing facilities, assisted living, and similar facilities were 12 times more likely to screen positive for MRSA as compared with patients admitted from home. The costs to identify each MRSA positive patient were $1,650 and $953 for comprehensive and state-mandated periods, respectively. Conclusion: In low prevalence hospitals without MRSA outbreaks, it is recommended that MRSA screening be conducted on patients admitted from skilled nursing and similar facilities because they are most likely to be colonized with MRSA. Results do not support mandates to conduct screening on all patients admitted to critical care units. Copyright Ó 2013 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.

Health care-associated methicillin-resistant Staphylococcus aureus (HA-MRSA) infections constitute a significant risk for patients.1 The major reservoirs for MRSA are colonized or infected patients and, occasionally, personnel in the hospital.2 When contact precautions were implemented on colonized patients, the rate of MRSA transmission decreased.2,3 The risk of MRSA infection given MRSA colonization is variable, and, in a review of studies, colonization ranged from 10% to 30%, depending on the population studied and the length of follow-up.4 Active surveillance measures to identify patients colonized with MRSA and rapid implementation of contact precautions should result in a reduction of MRSA transmission in hospitals.5 Sometimes called active detection and isolation, these strategies are used

* Address correspondence to Rebecca Kjonegaard, RN, MSN, 3425 Fowler Canyon Road, Jamul, CA 91935. E-mail address: [email protected] (R. Kjonegaard). Conflicts of interest: None to report.

to identify patients at high risk for HA-MRSA to detect colonized patients and to then use isolation precautions to decrease MRSA transmission. The Society for Healthcare Epidemiology of America (SHEA) and the Association of Professionals in Infection Control and Epidemiology (APIC) have endorsed the use of active surveillance screening in appropriate circumstances.6 A long-standing debate exists as to which high-risk patients should be MRSA screened.7 When used, MRSA screening varies among institutions and may include all patients,8 all surgical patients,9 intensive care unit (ICU) patients,10-12 patients admitted from nursing homes or other institutional patients, and patients with a history of MRSA colonization or infection or a combination of these categories.13,14 The increased mortality, morbidity, and cost of MRSA infection are unquestioned15-18; however, the costs and benefits of MRSA screening are difficult to assess. Case studies in Canada19 and Germany20 as well as the United States12 have reported results that are effective in their unique situations. Studies that include multiple hospitals have also yielded variable results. In a randomized trial of 10 interventions and 8 control

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ICUs, intervention ICUs conducted universal MRSA screening followed by contact precautions and found no reduction in colonization or infection with MRSA or vancomycin-resistant Enterococcus.12 At all US Veterans Affairs hospitals, the implementation of a “MRSA bundle” was studied retrospectively.8 The bundle included universal MRSA screening, contact precautions for MRSA-positive patients, hand hygiene education enforcement, and other “culture changes” elements. These results showed a reduction of HA-MRSA infections; however, the extent of reduction related to universal screening and contact precautions was not determined. In a well-controlled study in Switzerland, all surgical patients were screened for MRSA over a 23-month period with no observed reduction in HA-MRSA infection.9 This study concluded that universal screening was unlikely to be effective in hospitals with relative low rates of MRSA infection. To increase effectiveness of screening, they suggested use of a predictive model that targets higher risk patients.21 In summary, the existing literature demonstrates that the “best-practice” use of rapid MRSA screening as an element in active surveillance is yet to be established, and, to date, there is no consensus on the cost-effectiveness of MRSA screening. In an effort to reduce health care-associated infections, the State of California enacted Senate Bill 1058, the “Medical Facility Infection Control and Prevention Act.”22 Effective January 1, 2009, this law required each patient admitted to an ICU be tested for MRSA within 24 hours of admission. The purpose of this study was to evaluate the effectiveness and costs of an active MRSA screening program and subsequent contact precautions on the transmission rate of HA-MRSA in ICU patients.

METHODS A pre- and postimplementation study was conducted in a 24bed medical intensive care unit (MICU) and 15-bed surgical intensive care unit (SICU) at a Southern California, acute care, 536bed community hospital. Three data collection periods included the following: pre-active surveillance (before January 7, 2009), comprehensive active surveillance (January 7-August 4, 2009), and state-mandated active surveillance (August 5, 2009-March 4, 2010). In the pre-active surveillance period, MICU and SICU patients were cultured for an infection when symptoms were present and there was a physician order. Any coronary artery bypass graft patient who tested positive for MRSA was placed in contact precautions, and a protocol to decolonize the patient was initiated prior to cardiac surgery. Other patients who tested positive or had a known history of MRSA were placed in contact precautions but were not routinely decolonized. During the comprehensive active surveillance, all patients admitted or transferred into MICU or SICU were screened for MRSA colonization. The goal was to obtain specimens within 24 hours of admission to the ICU. Rapid polymerase chain reaction (PCR) molecular screening for MRSA was completed using the BD GeneOhm (BD, Franklin Lake, NJ) MRSA Assay with samples from both nares and the perineal area. The manufacturer’s package insert reports a sensitivity of 92% and specificity 94.6%. Based on the low productivity of the perineum screening and the low conversion rates, the hospital’s Infection Prevention Committee suspended perineum and screening when the patient was discharged from the MICU or SICU on August 4, 2009. During the state-mandated surveillance, upon admission to MICU or SICU, patients were screened in the nares using the screening test described above. Data collection for this study ended March 4, 2010.

Screening, infection, and cost data Patient information was obtained from electronic medical records and included ICU and hospital admission, discharge date and time, presence or absence of MRSA on day of admission and discharge or transfer from the MICU and SICU, age, gender, sample source (nares, perineum), diagnosis, and admission and discharge location. Rates for HA-MRSA infections were generated using standard case definitions by infection control staff as a part of their routine duties. The case definitions were divided into 3 categories: health care associated (previous negative result and now positive), community acquired (positive result less than 3 days following admission), and unknown (positive result after 48 hours in the hospital and no previous admission result). Total hospital discharges were used as the denominator. Costs of MRSA screening were obtained from hospital financial records provided during the final phase of the study.23 Specimens were collected by nurses, and the additional time to inform patients, collect specimens (for nares, perineum, or both), and handle specimens and paperwork was estimated to average approximately 20 minutes per patient. Average salary and benefits for nurses on critical care units were estimated at $54/hour or $18/ patient. The cost of the PCR rapid test that was conducted at a centralized laboratory included processing, transportation, reagent and analysis costs, and pathologists’ professional fees ($49/ test). To assure rapid contact precautions for MRSA-positive screens, laboratory staff called these results to the patients’ units at an added cost of $6/positive screen. After notification, MRSA screen-positive patients were placed in contact protections. Our analysis underestimates the total number of MRSA screening tests done. The hospital policy was to screen for MRSA on each admission to a critical care unit. This procedure was followed even when a patient was transferred from another unit in the hospital. For example, if a patient was initially admitted to the SICU from the emergency department then stabilized in the SICU and found to be MRSA negative and then was transferred to another unit and was later readmitted to an ICU, the patient was still required to be rescreened for MRSA. For purposes of this study, we examined MRSA testing dates and consolidated all critical care unit admissions into a single hospital stay record. Regardless of repeated screens for these patients, only a single admission MRSA screen was used in this analysis. During the intensive period when screens were completed upon discharge or transfer from the MICU and SICU, only 2 tests would have been recorded for any patient’s hospitalization. Thus, our study did not account for these additional tests. We consolidated records of 442 patients who had multiple stays in an ICU. These represented 208 unique patient hospital admissions. The costs of 246 additional MRSA screens for these patients were not included in cost or usage estimates. Statistical analysis Descriptive and multivariate analyses were conducted using SPSS software (version 17; SPSS Inc, Chicago, IL). Rates and costs were estimated using Excel 2007 (Microsoft Inc, Redmond, WA). RESULTS Patient characteristics Characteristics of critical care patients admitted during the comprehensive active surveillance (January 7-August 4, 2009) and the state-mandated periods (August 5, 2009-March 4, 2010) are displayed in Table 1. Patient demographics were similar for both

R. Kjonegaard et al. / American Journal of Infection Control 41 (2013) 45-50 Table 1 MICU/SICU admissions and patient characteristics, Sharp Grossmont Hospital, January 7, 2009, to March 4, 2010

Indicator MICU/SICU admissions Median age, yr Age range Percent female Admission source, % SNF, board and care, assisted living* Emergency room Home direct admission Patient MICU/SICU stay data Mean LOS hours Mean LOS days Standard deviation LOS hours Mean hospital LOS days Median hospital LOS days

Comprehensive

State mandate

January 7August 4, 2009

August 5, 2009March 4, 2010

1,654 63 16-99 49.1

1,687 63 17-101 50.9

14.8

14.5

70.4 14.4

68.0 17.6

94 3.9 116.2 9.2 6.7

93 3.9 125.5 8.7 6.3

LOS, Length of stay. *Also includes other facilities.

periods as were the sources of admission. Reflective of the severity of patient conditions, the mean hospital length of stay was just less than 10 days (9.2 and 8.7 days, respectively). The average patient spent 3.9 days in an ICU. Screening costs Costs for comprehensive and state-mandated levels of screening are presented in Table 2, along with estimated costs for screening only patients from skilled nursing facilities (SNFs), assisted living, and board and care and similar facilities. Costs during the comprehensive active surveillance reflect the additional costs of screening nares and perineum sites as well as screening at both sites at discharge from the ICU. Screening costs during the comprehensive period were $193 per admission or $1,648 per patient who screened positive for MRSA. The addition of perineum screening added 24 MRSA-positive patients not identified with nares specimens. The estimated cost per each added MRSA positive was $3,961. Screening during the state-mandated period reflects the costs required by the state mandate. Only nares specimens were collected during this period and with an average cost of $64 per admission or $953 per positive MRSA screen patient. Table 2 also displays the estimated cost of selective screening for the 14.5% of patients admitted from SNFs, assisted living, board and care homes, and other facilities. If only these admissions were screened for MRSA, the mean cost per admission would be $69 per admission with a cost per positive MRSA screen of $212. Screening yield and MRSA conversion rates Screening results and MRSA conversion rates during the comprehensive phase of the study are displayed in Table 3. During this period, the procedure was to screen both nares and perineum sites upon admission. At discharge, the procedure was to rescreen only those who were MRSA negative on their admission screen. At admission, 89.1% and 86.3% of the 1,654 admissions were screened at nares and perineum sites, respectively. Failure to screen was the result of patient refusal, other more urgent events during care (eg, patient death), staff misinformation, or lack of attention to screening. The electronic medical records did not specify reasons for failure to screen. Positive MRSA screens at admission were 11.6% for nares and 8.3% for perineum. Among patients screened at

47

both sites, 24 (1.7%) had positive perineum but negative nares screens. The MRSA-positive rate at discharge was 6.0% for nares and 4.0% for perineum. Fewer patients were MRSA screened at discharge from the ICU. Also, the lower percents in positive screening at discharge from the MICU and SICU is a result of the standing order that reserved discharge screening only for those who were MRSA negative at admission. Not all eligible MRSAnegative patients were screened at exit because of the same reasons for nonscreening at admission listed above. Among the 931 patients who completed nares screens at admission and exit, 17 (1.7%) converted to positive. For the 816 patients who had perineum screens at admission and exit, 16 (1.9%) rescreened positive at discharge from the ICU. Patient characteristics associated with positive MRSA screening Table 4 displays patient characteristics associated with positive MRSA screens at admission to the MICU and SICU during the study period from January 7, 2009, through March 4, 2010. For this analysis, the patient had to have an admission nares and/or a perineum screen as well as data on gender, source of admission, and age. Positive patients are defined as having a positive nares or a perineum MRSA screen. In total, 2,938 admissions were available for regression analyses. Table 4 displays the percent positive by source of admission, age group, sex, and the probability from c2 tests of association. Admissions from SNFs, assisted living, board and care, and similar facilities had the highest MRSA positive rates with the lowest among patients admitted directly from home. Those over 50 years were also more likely to be positive, and there was no difference between males and females. The adjusted odds ratios (AOR) from multiple logistic regression quantifies the independent association of the preadmission characteristics for patients and a positive MRSA screen. The right side of Table 4 displays the AOR, the significance (P value), and the 95% confidence intervals for the AOR. Compared with patients admitted from home, patients from SNFs, assisted living, board and care, and similar facilities were more than 12 times more likely to screen positive for MRSA (AOR, 12.5; 95% CI: 7.5-20.8). Compared with the 18- to 49-year-old group, those who were in the 65- to 70-year-old group were 1.5 times more likely to screen MRSA positive (AOR, 1.5; 95% CI: 1.0-2.2). Hospital-wide MRSA infection rates Health care-associated (HA) MRSA infections before, during comprehensive screening, and during the period of state-mandated MRSA screening rates were calculated by hospital infection prevention staff. Figure 1 displays hospital monthly HA-MRSA infection rates per 1,000 discharges between January 2008 and February 2010 along with marks to identify the prescreening period, the comprehensive screening, and the state-mandated level of MRSA screening for all MICU and SICU admissions. The mean number of hospital admissions per month was 2,235 with a range from 2,081 to 2,459. An average of 2.4 HA-MRSA infections per month was identified (range, 0-7). The small numbers of infections and the large number of admissions yield rates that are highly sensitive to small changes in infections, thus making any test of significance on HA-MRSA rates problematic. The rate of HA-MRSA infections during the prescreening period (0.8/ 1,000 admissions) is statistically lower than the rate of 1.6/1,000 during the intensive screening period January through July 2009 (c2 test, 4.28; P ¼ .037). There was no statistical difference between comprehensive screening and the rate during the state-mandated period (1.6/1,000 vs 1.1/1,000, respectively). Likewise, there was

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Table 2 MRSA screening costs, MICU/SICU admissions Sharp Grossmont Hospital, January 7, 2009, to March 4, 2010

Admissions to MICU/SICU MRSA screening Total patients tested Percent positive Percent of admissions screened MRSA screening costs Laboratory testing, cost/specimen Calls for positives at 10 min/call Specimen collection costs Mean staff nurse cost at $54 per hour 20 Min/patient Total screening costs Testing cost/admission Testing cost/positive MRSA Patients added with perineum MRSA screening No. of perineum tests Cost/patient per screens Total costs Cost per added positive

Comprehensive

State mandated

Estimated

January 7-August 4, 2009

August 5, 2009-March 4, 2010

Costs for focused screening*

$42.60 $49 $6

$18

1,654

1,687

1,464 11.6 88.8

1,449 9.1 85.9

245 32.5 100

$231,659 $2,413

$77,870 $988

$11,927 $503

$85,708 $319,780 $193 $1,648

$28,810 $107,668 $64 $953

$4,413 $16,844 $69 $212

n ¼ 24 1,423 $67 $95,056 $3,961

*Assumes that 100% of MICU/SICU admits are from high-risk settings; SNFs, assisted living, board and care, and similar facilities are screened. These represented 14.5% of admits to MICU/SICU during study period. Assumes that 32.5% of these high-risk admits will be MRSA positive.

Table 3 Comprehensive MRSA screening, 1,648 MICU/SICU unit admissions, Sharp Grossmont Hospital, January 7 to August 4, 2009 Admission Exit screen Both entry and % screen at discharge exit screens Converted Total admissions Nares Negative Positive Converted negative to positive Reverted and Total tested Percent positive Percent of admissions with nares screen Perineum Negative Positive Converted negative to positive Reverted* Total tested Percent positive Percent of admissions with perineum screen Additional positive screens with perineum screening

1,654 1,298 170

880 56

1,468 11.6 89.1

936 6.0 56.8

1,305 118

877 37

1,423 8.3 86.3

914 4.0 55.5

881 29 17

1.9

4 931 4.9 56.5

824 20 16

1.9

1 861 4.2 52.2

24 (1.7%)

NOTE. Per procedures, MRSA-positive individuals at admission should not screened on exit from CCU. Thirty-one patients who were nares positive at admission were inadvertently retested at discharge, and 4 were negative on their second MRSA nares screen. *Twenty-one patients who were perineum positive at admission were inadvertently retested at discharge, and 1 was negative on their second MRSA perineum screen.

no statistical difference in the prescreening period (0.8/1,000) versus the state-mandated period (1.1/1,000).

DISCUSSION These results document the complexities of implementing MRSA screening for all patients admitted to ICU. With a state mandate, full support of hospital administration, and oversight by

infection prevention staff, completion of screening was at 89% of ICU patients, a reflection of the dynamic care environment with life-saving priorities. In addition, some patients refused screening. Less than 100% screening completion numbers reflects the realities of hospital operations, and there is no reason to suspect that MRSApositive rates would have been biased. This study did not find added value in screening with perineal in addition to nares specimens. During the 7 months of comprehensive screening, perineal screening added only 1.7% additional MRSA-positive screens with a cost of $3,961 per added MRSApositive screen. Likewise, we found a low conversion rate of 1.9% from MRSA negative to MRSA positive between admission and discharge from the ICU. There are other conversion studies; however, they are not comparable because of differences in patient mix and MRSA screening methods.24 Studies of the effectiveness of MRSA screening have yielded variable results and strong opinions about the value of MRSA screening.7 Inconsistent results may be attributed to the difficulty in assessing the contribution of various components of interventions (screening, hand hygiene, contact precautions), variability in research design, difficult in measuring changes in relatively low HA-MRSA infection rates, and hospital or ICU settings with vastly different baseline rates and variable in patient mix (source of admissions, age, other risk factors). Robicsek et al25 reported the results of ICU and universal (hospital wide) screening results in a 3hospital, 850-bed organization. The baseline rate for hospitalassociated MRSA disease (all body sites) was 8.9 per 10,000 patient-days. After 12 months of ICU screening, an all-hospital rate of 7.4 was observed. After an additional 12 months with universal MRSA screening, a rate of 3.9 was observed. In contrast, during our 14-month study period with ICU screening, we observed an allhospital HA-MRSA rate of 13.2/10,000 patient discharges (Fig 1), a rate that was unchanged from the pre-active surveillance period. Although these hospital settings are not comparable, several other hospitals or health system studies have found no association between targeted screening and HA-MRSA rates.26 Statistical modeling of the costs and benefits of rapid MRSA screening has also yielded highly variable results.10,27,28 In general, statistical modeling seems to conclude that, whereas targeted screening is preferred, screening in low prevalence HA-MRSA settings is not

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Table 4 MRSA screening results and associated patient characteristics, MICU/SICU admissions, Sharp Grossmont Hospital, January 7, 2009, to March 4, 2010 Descriptive analysis

Multiple Logistic Regression 95% CI for AOR

Admitted from: Home Emergency department SNF, assisted living, board and care Other facility Age group, yr 18-49 50-64 65-70 80 Sex Male Female

No. screened

% Positive

P value*

Adjusted odds ratio

P value

Lower

Upper

478 2,022 363 58

3.8 9.0 32.5 15.5

<.001

1.0 2.6 12.5 4.9

Reference <.001 <.001 <.001

NA 1.6 7.5 2.1

NA 4.2 20.8 11.3

596 884 879 581

7.9 11.4 12.6 11.7

.035

1.0 1.4 1.5 1.1

Reference .1 <.037 .7

NA 0.9 1.0 0.7

NA 2.0 2.2 1.6

1,570 1,368

10.6 11.8

.332

1.0 1.1

Reference .3

NA 0.9

NA 1.4

NA, not applicable. NOTE. N for regression ¼ 2,938. *P value from c2 analysis.

Fig 1. Monthly health care-associated MRSA infections per 100 discharges. Pre-active MRSA surveillance period prior to January 1, 2008, to December 31, 2008; comprehensive active surveillance: January 1 to August 4, 2009; state mandated active surveillance: August 5 to March 4, 2010.

likely to be cost-effective.27 These results provide additional cost information. Empirical studies have uniformly documented the increased yield of MRSA carriers using rapid screening.29 ICU and universal screening interventions appear to be most effective in settings with historically high rates of HA-MRSA.26,29,30 The Robicsek et al study may have identified more HA-MRSA because the screening included all body sites; however, our study revealed only a small increase in yield by adding a body site (perineum) to the screening.25 Our study did not assess changes in handwashing and other protective measures that may have improved as an indirect result of more intensive screening and the increased precautions provided to patients who screened positive. Other comprehensive interventions in ICU settings have reported no association of HAMRSA infection and MRSA screening plus added precautions.12 In institutions without MRSA outbreaks, it is unclear how much of the reduction of HA-MRSA infection may be attributed to

screening versus other infection control interventions. MRSA screening is never independent from other infection prevention activities and is always a part of a set of infection prevention practices. For example, in a recent study of MRSA prevention efforts in Veterans Affairs hospitals,8 reductions in HA-MRSA rates were observed following implementation of a “MRSA bundle” that included universal screening, hand hygiene, precautions, and “culture change.” Like other studies, this observational study did not address the relative contribution of the various components of the “bundle.” Several reports have cautioned against the overemphasis of MRSA screen at the expense of other important precautions.7,30 Information from both experimental and observational research studies in multiple settings is needed to identify what levels of MRSA screening provide the most cost-effective improvements in reduced HA-MRSA infections and overall patient safety. Risk factors for MRSA colonization identified in this study are similar to those identified in other studies.21,29 Compared with patients admitted from their homes, patients admitted from institutional settings were significantly more likely to be MRSA positive. In this study, almost one third (32.5%) of patients admitted from SNFs, assisted living, and board and care facilities screened MRSA positive. In contrast, only 3.8% of those admitted from home were MRSA colonized. This and other findings call into question the costeffectiveness of any state mandate that requires 100% of ICU patients to be MRSA screened. Basic nares screening added $64 to each ICU admission with a cost of $953 for each MRSA-positive patient identified. If only the higher risk patients from institutional settings had been screened, the total costs for this hospital would have been reduced from $107,668 to $16,844, a savings of $90,824 or about $150,000 on an annualized basis. This institution observed no reduction in HA-MRSA infections, and, as discussed above, these results are reflective of other studies leading to the conclusion there is currently not good evidence or a consensus from empirical studies that 100% screening of ICU patients is associated with reduction in HA-MRSA infection.7 Major infection prevention professional organizations do not support government mandates for MRSA screening.31 Extrapolating our results to the approximately 300 other California hospitals with intensive care beds emphasizes the significance of potential savings with a focused screening requirement. If the 300 hospitals conservatively saved an average of $50,000 per year the total savings would be about $15 million dollars per year. In a fiscally strained environment, these savings might be better used for other

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infection prevention and safety strategies that individual hospitals select based on their annual risk analysis, which includes their community, the patient population, and other emergencies they need to prepare for to meet their hospital’s specific needs. Acknowledgment The authors thank staff members Dr. Gonzalo R. Ballon-Landa, Shauna Tarrac, and Bo Zhou for their support in completion of this project and all hospital staff who aided in the completion of this project. References 1. Clancy M, Graepler A, Wilson M, Douglas I, Johnson J, Price CS. Active screening in high-risk units is an effective and cost-avoidant method to reduce the rate of methicillin-resistant Staphylococcus aureus infection in the hospital. Infect Control Hosp Epidemiol 2006;27:1009-17. 2. Peterson A, Patricia M, Dawn T, Lauren B, Laurene M. Hospital methicillinresistant Staphylococcus aureus active surveillance practices in Los Angeles County: implications of legislation-based infection control, 2008. Am J Infect Control 2010;38:653-6. 3. Institute for Healthcare Improvement. 5 Million Lives Campaign. Getting started kit: Reduce methicillin-resistant Staphylococcus aureus (MRSA) infection how-to guide. Cambridge [MA]: IHI; 2008. Available from: www.ihi.org. Accessed April 10, 2012. 4. Hota B. Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis 2004;39:1182-9. 5. Muto CA, Jernigan JA, Ostrowsky BE, Richet HM, Jarvis WR, Boyce JM, et al. SHEA guideline for preventing nosocomial transmission of multidrug-resistant strains of Staphylococcus aureus and enterococcus. Infect Control Hosp Epidemiol 2003;24:362-86. 6. Siegel J, Rhinehart E, Jackson M, Chiarello L, Hospital Infection Control and Preventions Advisory Committee (HICPAC). 2007 Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Healthcare Settings. Centers for Disease Control and Prevention. Available from: http:// www.cdc.gov/ncidod/dhqp/pdf/isolation2007.pdf. Accessed April 4, 2012. 7. Peterson LR, Diekema DJ. To screen or not to screen for methicillin-resistant Staphylococcus aureus. J Clin Microbiol 2010;48:683-9. 8. Jain R, Kralovic SM, Evans ME, Ambrose M, Simbartl LA, Obrosky DS, et al. Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. N Engl J Med 2011;364:1419-30. 9. Harbarth S, Fankhauser C, Schrenzel J, Christenson J, Gervaz P, Bandiera-Clerc C, et al. Universal screening for methicillin-resistant Staphylococcus aureus at hospital admission and nosocomial infection in surgical patients. JAMA 2008; 299:1149-57. 10. Nyman JA, Lees CH, Bockstedt LA, Filice GA, Lexau C, Lesher LJ, et al. Cost of screening intensive care unit patients for methicillin-resistant Staphylococcus aureus in hospitals. Am J Infect Control 2011;39:27-34. 11. Cunningham R, Jenks P, Northwood J, Wallis M, Ferguson S, Hunt S. Effect on MRSA transmission of rapid PCR testing of patients admitted to critical care. J Hosp Infect 2007;65:24-8. 12. Huskins WC, Huckabee CM, O’Grady NP, Murray P, Kopetskie H, Zimmer L, et al. Intervention to reduce transmission of resistant bacteria in intensive care. N Engl J Med 2011;364:1407-18. 13. Cosgrove SE, Sakoulas G, Perencevich EN, Schwaber MJ, Karchmer AW, Carmeli Y. Comparison of mortality associated with methicillin-resistant and methicillin-susceptible Staphylococcus aureus bacteremia: a meta-analysis. Clin Infect Dis 2003;36:53-9.

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