American Journal of Infection Control 41 (2013) 1093-5
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Veterans Affairs methicillin-resistant Staphylococcus aureus prevention initiative associated with a sustained reduction in transmissions and health care-associated infections Martin E. Evans MD a, b, *, Stephen M. Kralovic MD, MPH c, d, Loretta A. Simbartl MS c, Ron W. Freyberg MS e, D. Scott Obrosky MS f, Gary A. Roselle MD c, d, Rajiv Jain MD g a
VHA MRSA/MDRO Program Office, the National Infectious Diseases Service, Patient Care Services, VA Central Office and the Lexington VA Medical Center, Lexington, KY Department of Internal Medicine, University of Kentucky School of Medicine, Lexington, KY National Infectious Diseases Service, Patient Care Services, VA Central Office and Cincinnati VA Medical Center, Cincinnati, OH d Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH e VA Office of Informatics and Analytics, Analytics and Business Intelligence, Cincinnati, OH f Center for Health Equity Research and Promotion, VA Pittsburgh Healthcare System, Pittsburgh, PA g Patient Care Services, VA Central Office, Washington, DC b c
Key Words: Veterans health care MDRO Methicillin-resistant organism Infection prevention
Implementation of a methicillin-resistant Staphylococcus aureus (MRSA) Prevention Initiative was associated with significant declines in MRSA transmission and MRSA health care-associated infection rates in Veterans Affairs acute care facilities nationwide in the 33-month period from October 2007 through June 2010. Here, we show continuing declines in MRSA transmissions (P ¼ .004 for trend, Poisson regression) and MRSA health care-associated infections (P < .001) from July 2010 through June 2012. The Veterans Affairs Initiative was associated with these effects, sustained over 57 months, in a large national health care system. Published by Elsevier Inc. on behalf of the Association for Professionals in Infection Control and Epidemiology, Inc.
We previously reported implementation of a methicillinresistant Staphylococcus aureus (MRSA) Prevention Initiative within Veterans Affairs (VA) medical centers nationwide.1 This Initiative featured a “bundle” of evidence-based practices consisting of (1) universal nasal surveillance for MRSA, (2) Contact Precautions for patients colonized or infected with MRSA, (3) hand hygiene, and (4) an institutional culture change where infection prevention and control became everyone’s responsibility. An additional component of this Initiative was investment in a dedicated new position, the MRSA Prevention Coordinator, at each medical center. The responsibility of this person was to oversee implementation of the Initiative at their facility, collect and report local data into a national database, provide feedback to local providers, and troubleshoot problems.
* Address correspondence to Martin E. Evans, MD, 1101 Veterans Drive, Lexington, KY. E-mail address: [email protected] (M.E. Evans). A portion of the information reported herein was presented at IDWeek 2012, San Diego, CA, October 2012. Conflicts of interest: None to report.
During the first 33 months of the MRSA Prevention Initiative from October 2007 through June 2010, in-hospital MRSA transmission rates declined 17% in intensive care units (ICUs) (P < .001 for trend, Poisson regression) and 21% in non-ICUs (P < .001). At the same time, MRSA health care-associated infection (HAI) rates declined 62% in ICUs (P < .001) and 45% in non-ICUs (P < .001), and, by the end of the analysis period, more than 70% of VA facilities nationwide reported zero MRSA HAIs each month.1,2 In this article, we report sustained declines in MRSA transmissions and MRSA HAIs nationwide over the next 24 months of the VA MRSA Prevention Initiative from July 2010 through June 2012. METHODS Implementation, data collection, and analysis of the first 33month period of the VA MRSA Prevention Initiative from October 2007 through June 2010 were reported previously.1 We now report a reanalysis of the data from October 2007 through June 2010 including the results of a subsequent 24-month period of the Initiative from July 2010 through June 2012. Data from all acute care VA facilities were pooled for the analyses. Monthly and quarterly
0196-6553/$00.00 - Published by Elsevier Inc. on behalf of the Association for Professionals in Infection Control and Epidemiology, Inc. http://dx.doi.org/10.1016/j.ajic.2013.04.015
M.E. Evans et al. / American Journal of Infection Control 41 (2013) 1093-5
From July 2010 through June 2012, there were 2,382,952 admissions to or transfers or discharges from VA ICUs and nonICUs (ICUs, 372,290; non-ICUs, 2,010,662) and 6,008,424 ptdays (ICUs, 921,543; non-ICUs, 5,086,881) nationwide. The mean monthly percentage of patients screened for MRSA upon facility admission was 96.2% (3.5% standard deviation). The prevalence of patients carrying MRSA at admission decreased 5.0% from 16.0% to 15.2% (P < .001). Monthly transmission rates in ICUs and non-ICUs combined declined 12.1% (2.31 to 2.03/ 1,000 pt-days; P ¼ .004). These rates did not change significantly in the ICUs (2.54 to 2.36/1,000 pt-days; P ¼ .69) but declined 13.7% in non-ICUs (2.27 to 1.96/1,000 pt-days; P < .001). Monthly MRSA HAI rates in ICUs and non-ICUs combined declined 36.4% (0.33 to 0.21/1,000 pt-days; P < .001). These rates did not decline significantly in the ICUs (0.54 to 0.46/1,000 pt-days, P ¼ .10) but decreased 44.8% in non-ICUs (0.29 to 0.16/1,000 pt-days, P < .001) (Fig 1). During the analysis interval, the quarterly rates of combined device- and nondevice-associated MRSA bloodstream HAIs in ICUs and non-ICUs fell 36.4% (0.11 to 0.07/1,000 pt-days, P ¼ .04), but there was no significant changes in pneumonia or urinary tract infection rates. There was no difference in bloodstream MRSA HAI rates when the infections were separated into device- and nondevice-associated infections. Trends in MRSA transmissions, MRSA HAIs, and MRSA admission prevalence over the 57 months of the VHA MRSA Prevention Initiative from its inception (October 2007) through the end of this report (June 2012) were as follows: overall MRSA transmissions declined 24.2% (P < .001 for trend by Poisson regression analysis); ICU MRSA transmissions declined 21.8% (P < .001), non-ICU MRSA transmissions declined 24.7% (P < .001); overall MRSA HAIs declined 68.6% (P < .001); ICU MRSA HAIs declined 71.9% (P < .001); and non-ICU MRSA HAIs declined 65.5% (P < .001). MRSA admission prevalence (from April 2008 with a definition change1 through June 2012) increased 15.2% (P < .001). DISCUSSION We previously reported that implementation of a VA MRSA Prevention Initiative was associated with significant decreases in MRSA transmissions and MRSA HAIs over a 33-month period in a large health care system.1 The analysis presented here shows that, over the ensuing 24 months, MRSA transmissions and MRSA HAI rates continued to decrease nationwide. Detailed analysis showed that there were statistically significant declines in MRSA transmissions and MRSA HAIs in non-ICUs but not in the ICUs. The absence of statistically significant trends in the ICUs may be because MRSA transmission and MRSA HAI rates were low and becoming asymptotic. As we previously stated,1 the VA MRSA Prevention Initiative is a quality improvement program rather than a prospectively designed trial, and data are not available to determine how much the decrease in observed MRSA transmissions and MRSA HAIs was due to the MRSA bundle, changes in MRSA in the community, or other HAI prevention efforts.
1.8 ICU
1.6
Non-ICU
1.4 1.2
P< 0.001
1.0 0.8
P =0.10
0.6 0.4 0.2 0.0
P< 0.001
P< 0.001
ct Fe 07 bJu 08 nO 08 ct Fe 08 bJu 09 nO 09 ct Fe 09 bJu 10 nO 10 ct Fe 10 bJu 11 nO 11 ct Fe 11 bJu 12 n12
RESULTS
MRSA Healthcare-Associated Infections
MRSA HAIs/1,000 pt-days
data were analyzed using the SAS statistical program, version 9.2 (SAS Institute, Cary NC). Rates of transmissions and MRSA HAIs were expressed as the number per 1,000 patient (pt)-days. Trends were examined by means of Poisson regression models. Analysis of these data was approved by the Cincinnati VA Medical Center Institutional Review Board.
O
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Fig 1. Nationwide VA ICU and non-ICU MRSA health care-associated infection (HAI) rates. Shaded area represents previously reported data from October 2007 after full implementation of the MRSA bundle through June 2010 when MRSA HAI rates declined 62% in the ICUs and 45% in non-ICUs. The nonshaded area represents MRSA HAIs from July 2010 through June 2012, which declined 14.8% in the ICUs and 44.8% in the non-ICUs. The respective P values for trends in the illustrated settings and periods, done using Poisson regression, are shown. Overall, from October 2007 through June 2012, MRSA HAIs in ICUs and non-ICUs combined declined 68.6% (P < .001).
Of note, recent declines in MRSA HAI rates in the United States have been reported by others,3-5 but differences in methods, populations evaluated, and absence of information about infection control activities make it difficult to determine the relevance of these data to the VA experience. Declines in the prevalence of specific MRSA clones over time have also been reported, raising the possibility that declining MRSA HAI rates among veterans may merely reflect broader trends in bacterial populations.6 Although we do not have data on clonal trends from MRSA HAI isolates, the prevalence of patients carrying MRSA on admission to VA facilities increased by approximately 15% over the 57 months of the Initiative, suggesting that the declining MRSA HAI rates observed were not solely due to a decreasing prevalence of MRSA in the VA patient population served. Bloodstream infections accounted for most of the decline in MRSA HAIs observed in VA facilities from July 2010 through June 2012. The absence of a difference in the rates of device- and nondevice-associated bloodstream infections suggests that the decline observed was not due solely to implementation of a formalized approach to placing and maintaining central line intravascular catheters.7 This is consistent with the VA experience from 2005 to 2007 before implementation of the MRSA Prevention Initiative when MRSA bloodstream HAIs did not decrease despite the use of bundles for central-line associated bloodstream infections.1 In this case, MRSA HAI rates only began to decline significantly when the VA MRSA bundle, which included universal nasal surveillance for a single pathogend MRSAdwas added to Contact Precautions and hand hygiene, which had been in place for years as general strategies to control infection by multiple pathogens.1 If universal screening played an important role in decreasing rates, it may be because obtaining nasal surveillance on patients at admission, unit-tounit transfer, and discharge served to constantly remind staff of MRSA and the need to prevent transmissions and MRSA HAIs through good compliance with hand hygiene and Contact Precautions. This could reinforce institutional culture change, the fourth component of the VA MRSA bundle. The continued
M.E. Evans et al. / American Journal of Infection Control 41 (2013) 1093-5
high compliance with nasal surveillance at admission (96%) and at transfer and discharge (94%) in VA facilities nationwide suggests that health care workers continue to be fully engaged with the Initiative. Acknowledgment The authors thank Robert A. Petzel, MD, Under Secretary for Health, and Madhulika Agarwal, MD, MPH, Deputy Under Secretary for Health for Policy and Services, for support of the VA MRSA/ MDRO Prevention Initiative; and the MRSA/MDRO Prevention Initiative Taskforce, the MRSA/MDRO prevention coordinators, infection prevention and control professionals, infectious diseases specialists, and clinical laboratory personnel at each facility for their hard work and dedication toward improving the health care of America’s Veterans.
1095
References 1. 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. 2. Kralovic SM, Evans ME, Simbartl LA, Ambrose M, Jain R, Roselle GA. Zeroing in on methicillin-resistant Staphylococcus aureus: US Department of Veterans Affairs’ MRSA Prevention Initiative. Am J Infect Control 2013;41:456-8. 3. Kallen AJ, Mu Y, Bulens S, Reingold A, Petit S, Gershman K, et al. Health careassociated invasive MRSA infections, 2005-2008. JAMA 2010;304:641-8. 4. Landrum ML, Neumann C, Cook C, Chukwuma U, Ellis MW, Hospenthal DR, et al. Epidemiology of Staphylococcus aureus blood and skin and soft tissue infections in the US military health system, 2005-2010. JAMA 2012;308:50-9. 5. Hadler JL, Petit S, Mandour M, Cartter ML. Trends in invasive infection with methicillin-resistant Staphylococcus aureus, Connecticut, USA, 2001-2010. Emerg Infect Dis 2012;18:917-24. 6. Wyllie D, Paul J, Crook D. Waves of trouble: MRSA strain dynamics and assessment of the impact of infection control. J Antimicrob Chemother 2011;66:2685-8. 7. Pronovost P, Needham D, Berenholtz S, Sinopoli D, Chu H, Cosgrove S, et al. An intervention to decrease catheter-related bloodstream infections in the ICU. N Engl J Med 2006;355:2725-32.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Brief report
Veterans Affairs methicillin-resistant Staphylococcus aureus prevention initiative associated with a sustained reduction in transmissions and health care-associated infections Martin E. Evans MD a, b, *, Stephen M. Kralovic MD, MPH c, d, Loretta A. Simbartl MS c, Ron W. Freyberg MS e, D. Scott Obrosky MS f, Gary A. Roselle MD c, d, Rajiv Jain MD g a
VHA MRSA/MDRO Program Office, the National Infectious Diseases Service, Patient Care Services, VA Central Office and the Lexington VA Medical Center, Lexington, KY Department of Internal Medicine, University of Kentucky School of Medicine, Lexington, KY National Infectious Diseases Service, Patient Care Services, VA Central Office and Cincinnati VA Medical Center, Cincinnati, OH d Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, OH e VA Office of Informatics and Analytics, Analytics and Business Intelligence, Cincinnati, OH f Center for Health Equity Research and Promotion, VA Pittsburgh Healthcare System, Pittsburgh, PA g Patient Care Services, VA Central Office, Washington, DC b c
Key Words: Veterans health care MDRO Methicillin-resistant organism Infection prevention
Implementation of a methicillin-resistant Staphylococcus aureus (MRSA) Prevention Initiative was associated with significant declines in MRSA transmission and MRSA health care-associated infection rates in Veterans Affairs acute care facilities nationwide in the 33-month period from October 2007 through June 2010. Here, we show continuing declines in MRSA transmissions (P ¼ .004 for trend, Poisson regression) and MRSA health care-associated infections (P < .001) from July 2010 through June 2012. The Veterans Affairs Initiative was associated with these effects, sustained over 57 months, in a large national health care system. Published by Elsevier Inc. on behalf of the Association for Professionals in Infection Control and Epidemiology, Inc.
We previously reported implementation of a methicillinresistant Staphylococcus aureus (MRSA) Prevention Initiative within Veterans Affairs (VA) medical centers nationwide.1 This Initiative featured a “bundle” of evidence-based practices consisting of (1) universal nasal surveillance for MRSA, (2) Contact Precautions for patients colonized or infected with MRSA, (3) hand hygiene, and (4) an institutional culture change where infection prevention and control became everyone’s responsibility. An additional component of this Initiative was investment in a dedicated new position, the MRSA Prevention Coordinator, at each medical center. The responsibility of this person was to oversee implementation of the Initiative at their facility, collect and report local data into a national database, provide feedback to local providers, and troubleshoot problems.
* Address correspondence to Martin E. Evans, MD, 1101 Veterans Drive, Lexington, KY. E-mail address: [email protected] (M.E. Evans). A portion of the information reported herein was presented at IDWeek 2012, San Diego, CA, October 2012. Conflicts of interest: None to report.
During the first 33 months of the MRSA Prevention Initiative from October 2007 through June 2010, in-hospital MRSA transmission rates declined 17% in intensive care units (ICUs) (P < .001 for trend, Poisson regression) and 21% in non-ICUs (P < .001). At the same time, MRSA health care-associated infection (HAI) rates declined 62% in ICUs (P < .001) and 45% in non-ICUs (P < .001), and, by the end of the analysis period, more than 70% of VA facilities nationwide reported zero MRSA HAIs each month.1,2 In this article, we report sustained declines in MRSA transmissions and MRSA HAIs nationwide over the next 24 months of the VA MRSA Prevention Initiative from July 2010 through June 2012. METHODS Implementation, data collection, and analysis of the first 33month period of the VA MRSA Prevention Initiative from October 2007 through June 2010 were reported previously.1 We now report a reanalysis of the data from October 2007 through June 2010 including the results of a subsequent 24-month period of the Initiative from July 2010 through June 2012. Data from all acute care VA facilities were pooled for the analyses. Monthly and quarterly
0196-6553/$00.00 - Published by Elsevier Inc. on behalf of the Association for Professionals in Infection Control and Epidemiology, Inc. http://dx.doi.org/10.1016/j.ajic.2013.04.015
M.E. Evans et al. / American Journal of Infection Control 41 (2013) 1093-5
From July 2010 through June 2012, there were 2,382,952 admissions to or transfers or discharges from VA ICUs and nonICUs (ICUs, 372,290; non-ICUs, 2,010,662) and 6,008,424 ptdays (ICUs, 921,543; non-ICUs, 5,086,881) nationwide. The mean monthly percentage of patients screened for MRSA upon facility admission was 96.2% (3.5% standard deviation). The prevalence of patients carrying MRSA at admission decreased 5.0% from 16.0% to 15.2% (P < .001). Monthly transmission rates in ICUs and non-ICUs combined declined 12.1% (2.31 to 2.03/ 1,000 pt-days; P ¼ .004). These rates did not change significantly in the ICUs (2.54 to 2.36/1,000 pt-days; P ¼ .69) but declined 13.7% in non-ICUs (2.27 to 1.96/1,000 pt-days; P < .001). Monthly MRSA HAI rates in ICUs and non-ICUs combined declined 36.4% (0.33 to 0.21/1,000 pt-days; P < .001). These rates did not decline significantly in the ICUs (0.54 to 0.46/1,000 pt-days, P ¼ .10) but decreased 44.8% in non-ICUs (0.29 to 0.16/1,000 pt-days, P < .001) (Fig 1). During the analysis interval, the quarterly rates of combined device- and nondevice-associated MRSA bloodstream HAIs in ICUs and non-ICUs fell 36.4% (0.11 to 0.07/1,000 pt-days, P ¼ .04), but there was no significant changes in pneumonia or urinary tract infection rates. There was no difference in bloodstream MRSA HAI rates when the infections were separated into device- and nondevice-associated infections. Trends in MRSA transmissions, MRSA HAIs, and MRSA admission prevalence over the 57 months of the VHA MRSA Prevention Initiative from its inception (October 2007) through the end of this report (June 2012) were as follows: overall MRSA transmissions declined 24.2% (P < .001 for trend by Poisson regression analysis); ICU MRSA transmissions declined 21.8% (P < .001), non-ICU MRSA transmissions declined 24.7% (P < .001); overall MRSA HAIs declined 68.6% (P < .001); ICU MRSA HAIs declined 71.9% (P < .001); and non-ICU MRSA HAIs declined 65.5% (P < .001). MRSA admission prevalence (from April 2008 with a definition change1 through June 2012) increased 15.2% (P < .001). DISCUSSION We previously reported that implementation of a VA MRSA Prevention Initiative was associated with significant decreases in MRSA transmissions and MRSA HAIs over a 33-month period in a large health care system.1 The analysis presented here shows that, over the ensuing 24 months, MRSA transmissions and MRSA HAI rates continued to decrease nationwide. Detailed analysis showed that there were statistically significant declines in MRSA transmissions and MRSA HAIs in non-ICUs but not in the ICUs. The absence of statistically significant trends in the ICUs may be because MRSA transmission and MRSA HAI rates were low and becoming asymptotic. As we previously stated,1 the VA MRSA Prevention Initiative is a quality improvement program rather than a prospectively designed trial, and data are not available to determine how much the decrease in observed MRSA transmissions and MRSA HAIs was due to the MRSA bundle, changes in MRSA in the community, or other HAI prevention efforts.
1.8 ICU
1.6
Non-ICU
1.4 1.2
P< 0.001
1.0 0.8
P =0.10
0.6 0.4 0.2 0.0
P< 0.001
P< 0.001
ct Fe 07 bJu 08 nO 08 ct Fe 08 bJu 09 nO 09 ct Fe 09 bJu 10 nO 10 ct Fe 10 bJu 11 nO 11 ct Fe 11 bJu 12 n12
RESULTS
MRSA Healthcare-Associated Infections
MRSA HAIs/1,000 pt-days
data were analyzed using the SAS statistical program, version 9.2 (SAS Institute, Cary NC). Rates of transmissions and MRSA HAIs were expressed as the number per 1,000 patient (pt)-days. Trends were examined by means of Poisson regression models. Analysis of these data was approved by the Cincinnati VA Medical Center Institutional Review Board.
O
1094
Fig 1. Nationwide VA ICU and non-ICU MRSA health care-associated infection (HAI) rates. Shaded area represents previously reported data from October 2007 after full implementation of the MRSA bundle through June 2010 when MRSA HAI rates declined 62% in the ICUs and 45% in non-ICUs. The nonshaded area represents MRSA HAIs from July 2010 through June 2012, which declined 14.8% in the ICUs and 44.8% in the non-ICUs. The respective P values for trends in the illustrated settings and periods, done using Poisson regression, are shown. Overall, from October 2007 through June 2012, MRSA HAIs in ICUs and non-ICUs combined declined 68.6% (P < .001).
Of note, recent declines in MRSA HAI rates in the United States have been reported by others,3-5 but differences in methods, populations evaluated, and absence of information about infection control activities make it difficult to determine the relevance of these data to the VA experience. Declines in the prevalence of specific MRSA clones over time have also been reported, raising the possibility that declining MRSA HAI rates among veterans may merely reflect broader trends in bacterial populations.6 Although we do not have data on clonal trends from MRSA HAI isolates, the prevalence of patients carrying MRSA on admission to VA facilities increased by approximately 15% over the 57 months of the Initiative, suggesting that the declining MRSA HAI rates observed were not solely due to a decreasing prevalence of MRSA in the VA patient population served. Bloodstream infections accounted for most of the decline in MRSA HAIs observed in VA facilities from July 2010 through June 2012. The absence of a difference in the rates of device- and nondevice-associated bloodstream infections suggests that the decline observed was not due solely to implementation of a formalized approach to placing and maintaining central line intravascular catheters.7 This is consistent with the VA experience from 2005 to 2007 before implementation of the MRSA Prevention Initiative when MRSA bloodstream HAIs did not decrease despite the use of bundles for central-line associated bloodstream infections.1 In this case, MRSA HAI rates only began to decline significantly when the VA MRSA bundle, which included universal nasal surveillance for a single pathogend MRSAdwas added to Contact Precautions and hand hygiene, which had been in place for years as general strategies to control infection by multiple pathogens.1 If universal screening played an important role in decreasing rates, it may be because obtaining nasal surveillance on patients at admission, unit-tounit transfer, and discharge served to constantly remind staff of MRSA and the need to prevent transmissions and MRSA HAIs through good compliance with hand hygiene and Contact Precautions. This could reinforce institutional culture change, the fourth component of the VA MRSA bundle. The continued
M.E. Evans et al. / American Journal of Infection Control 41 (2013) 1093-5
high compliance with nasal surveillance at admission (96%) and at transfer and discharge (94%) in VA facilities nationwide suggests that health care workers continue to be fully engaged with the Initiative. Acknowledgment The authors thank Robert A. Petzel, MD, Under Secretary for Health, and Madhulika Agarwal, MD, MPH, Deputy Under Secretary for Health for Policy and Services, for support of the VA MRSA/ MDRO Prevention Initiative; and the MRSA/MDRO Prevention Initiative Taskforce, the MRSA/MDRO prevention coordinators, infection prevention and control professionals, infectious diseases specialists, and clinical laboratory personnel at each facility for their hard work and dedication toward improving the health care of America’s Veterans.
1095
References 1. 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. 2. Kralovic SM, Evans ME, Simbartl LA, Ambrose M, Jain R, Roselle GA. Zeroing in on methicillin-resistant Staphylococcus aureus: US Department of Veterans Affairs’ MRSA Prevention Initiative. Am J Infect Control 2013;41:456-8. 3. Kallen AJ, Mu Y, Bulens S, Reingold A, Petit S, Gershman K, et al. Health careassociated invasive MRSA infections, 2005-2008. JAMA 2010;304:641-8. 4. Landrum ML, Neumann C, Cook C, Chukwuma U, Ellis MW, Hospenthal DR, et al. Epidemiology of Staphylococcus aureus blood and skin and soft tissue infections in the US military health system, 2005-2010. JAMA 2012;308:50-9. 5. Hadler JL, Petit S, Mandour M, Cartter ML. Trends in invasive infection with methicillin-resistant Staphylococcus aureus, Connecticut, USA, 2001-2010. Emerg Infect Dis 2012;18:917-24. 6. Wyllie D, Paul J, Crook D. Waves of trouble: MRSA strain dynamics and assessment of the impact of infection control. J Antimicrob Chemother 2011;66:2685-8. 7. Pronovost P, Needham D, Berenholtz S, Sinopoli D, Chu H, Cosgrove S, et al. An intervention to decrease catheter-related bloodstream infections in the ICU. N Engl J Med 2006;355:2725-32.
