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T h e n e w e n g l a n d j o u r n a l o f medicine

n engl j med 364;15 nejm.org april 14, 2011 1419

original article

Veterans Affairs Initiative to Prevent Methicillin-

Resistant Staphylococcus aureusInfectionsRajiv Jain, M.D., Stephen M. Kralovic, M.D., M.P.H., Martin E. Evans, M.D.,

Meredith Ambrose, M.H.A., Loretta A. Simbartl, M.S., D. Scott Obrosky, M.S.,Marta L. Render, M.D., Ron W. Freyberg, M.S., John A. Jernigan, M.D.,

Robert R. Muder, M.D., LaToya J. Miller, M.P.H., and Gary A. Roselle, M.D.

From the Veterans Health Administra-tion MRSA Program Office, Patient CareServices, Veterans Affairs (VA) CentralOffice, and the VA Pittsburgh HealthcareSystem (R.J., M.E.E., M.A., L.J.M.); theDepartment of Internal Medicine, VAPittsburgh Healthcare System, and theUniversity of Pittsburgh School of Medi-cine (R.J., R.R.M.); and the Center forHealth Equity Research and Promotion,VA Pittsburgh Healthcare System (D.S.O.) all in Pittsburgh; the National Infec-tious Diseases Program Office, PatientCare Services, VA Central Office, and theCincinnati VA Medical Center (S.M.K.,L.A.S., G.A.R.); the Department of Inter-nal Medicine, University of Cincinnati

College of Medicine (S.M.K., M.L.R.,G.A.R.); and the VA Inpatient EvaluationCenter (M.L.R., R.W.F.) all in Cincin-nati; the Department of Internal Medi-cine, University of Kentucky School ofMedicine, Lexington (M.E.E.); and thePrevention and Response Branch, Divi-sion of Healthcare Quality Promotion,Centers for Disease Control and Preven-tion, Atlanta (J.A.J.). Address reprint re-quests to Dr. Evans at the VHA MDROProgram, Lexington VAMC, 1101 Veter-ans Dr., 11iCDD, Lexington, KY 40502,or at [email protected].

N Engl J Med 2011;364:1419-30.

Copyright 2011 Massachusetts Medical Society.

A b s t ra c t

Background

Health careassociated infections with methicillin-resistant Staphylococcus aureus

(MRSA) have been an increasing concern in Veterans Affairs (VA) hospitals.

Methods

A MRSA bundle was implemented in 2007 in acute care VA hospitals nationwidein an effort to decrease health careassociated infections with MRSA. The bundleconsisted of universal nasal surveillance for MRSA, contact precautions for patientscolonized or infected with MRSA, hand hygiene, and a change in the institutionalculture whereby infection control would become the responsibility of everyone whohad contact with patients. Each month, personnel at each facility entered into acentral database aggregate data on adherence to surveillance practice, the preva-lence of MRSA colonization or infection, and health careassociated transmissionsof and infections with MRSA. We assessed the effect of the MRSA bundle on health

careassociated MRSA infections.

Results

From October 2007, when the bundle was fully implemented, through June 2010,there were 1,934,598 admissions to or transfers or discharges from intensive careunits (ICUs) and non-ICUs (ICUs, 365,139; non-ICUs, 1,569,459) and 8,318,675 pa-tient-days (ICUs, 1,312,840; and non-ICUs, 7,005,835). During this period, the per-centage of patients who were screened at admission increased from 82% to 96%,and the percentage who were screened at transfer or discharge increased from 72%to 93%. The mean (SD) prevalence of MRSA colonization or infection at the timeof hospital admission was 13.63.7%. The rates of health careassociated MRSAinfections in ICUs had not changed in the 2 years before October 2007 (P = 0.50 for

trend) but declined with implementation of the bundle, from 1.64 infections per1000 patient-days in October 2007 to 0.62 per 1000 patient-days in June 2010, adecrease of 62% (P


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n engl j med 364;15 nejm.org april 14, 20111420

Methicillin-resistantStaphylococcus

aureus(MRSA) infections are a problem inthe United States1and elsewhere. MRSA

is one of the most common causes of ventilator-associated pneumonia, bloodstream infection as-sociated with central venous catheters, and surgi-cal-site infections.1,2

In 2001, the Veterans Affairs (VA) PittsburghHealthcare System began working with the Pitts-burgh Regional Healthcare Initiative and theCenters for Disease Control and Prevention (CDC)to eliminate health careassociated MRSA infec-tions with the use of a MRSA bundle. The bun-dle, which was based on published guidelines,comprised universal nasal surveillance for MRSAcolonization, contact precautions for patients whowere carriers of MRSA, hand hygiene, and an in-stitutional culture change whereby infection con-trol became the responsibility of everyone who

had contact with patients.3After implementationof this approach in a pilot project, the rates ofhealth careassociated MRSA infections were re-duced by 60% on a surgical ward and by 75% in asurgical intensive care unit (ICU) within 4 years.4

On the basis of the success of the pilot studyin the VA Pittsburgh Healthcare System, and rec-ognizing the importance of preventing MRSAinfections for all veterans, the Veterans HealthAdministration (VHA), a division of the Depart-ment of Veterans Affairs, issued a directive (seethe Supplementary Appendix, available with thefull text of this article at NEJM.org) implement-ing a nationwide initiative to decrease healthcareassociated MRSA infections in acute carefacilities. In this article, we report an analysis ofthe effect of the MRSA Prevention Initiative dur-ing the period from October 2007, when theprogram was fully implemented in ICUs andnon-ICUs nationwide, through June 2010.

Methods

InterventionsMedical centers were directed to implement theMRSA bundle in one patient care unit (preferablyan ICU) beginning in March 2007 and to imple-ment the bundle in all remaining acute care units(with the exception of mental health units) byOctober 1, 2007. The bundle consisted of sur-veillance for nasal colonization with MRSA forall patients admitted to the hospital, all patientstransferred from one unit to another within thehospital, and all patients discharged from the

hospital; contact precautions for patients whowere either colonized or infected with MRSA;hand hygiene; and a change in the institutionalculture. The recommended approach to achieveculture change was positive deviance5 (a prob-lem-solving approach that is based on the obser-vation that in every community, there are certain

persons or groups whose uncommon behaviorsor strategies, as compared with those of theirpeers, enable them to find better solutions toproblems). The goal of the culture change was tofoster alterations in practice so that infectioncontrol and prevention would become the respon-sibility of everyone involved in the care of patientsand thus a natural component of patient care.

Patients

All patients admitted to VA acute health care fa-cilities (except patients admitted to mental

health units) were eligible to participate in theMRSA Prevention Initiative. Because this was nota research project, but rather a quality-improve-ment initiative, written informed consent fromindividual patients was not required, consistentwith VA policy.6Written information was avail-able for each patient or his or her caregiver, withdetails about MRSA, relevant principles of infec-tion control, the purpose and goals of the MRSAPrevention Initiative, and patients rights and oralassent (see the Supplementary Appendix).

Resources and Training

The VA Central Office provided funds to eachfacility in the United States for educational mate-rials, laboratory equipment and supplies, andsalaries for dedicated laboratory personnel andfor a newly created position, the MRSA preven-tion coordinator. The coordinator at each facilityoversaw implementation of the initiative at thatfacility, collected and reported data on the pro-gram at that facility, provided feedback to front-line health care workers, and dealt with local

challenges. Regional and national educationaland training sessions for the coordinators wereconducted by the MRSA Program Office.

Active Surveillance and Contact Precautions

Training on the method of obtaining nasal swabswas provided to all MRSA prevention coordinatorsthrough the MRSA Program Office. Samples ofnasal secretions were obtained with a swab fromboth anterior nares of patients within 24 hoursafter their admission to the hospital. Swabs were

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VA Initiative to Prev ent MRSA Infections


also obtained from patients who were not knownto be colonized or infected with MRSA when theywere transferred between, or discharged from,units within each facility. The local clinical micro-biology laboratory processed the swabs with theuse of standard or selective chromogenic agar forthe isolation of MRSA or with polymerase-chain-

reaction (PCR)based tests for rapid moleculardetection of the organism. Positive results werereported to the patients nursing unit and wererecorded in the electronic health record.

Patients who were found to be colonized orinfected with MRSA or who were known to havebeen colonized or infected with MRSA withinthe previous 12 months were assigned to contactprecautions.7These patients were cared for withcontact precautions during their hospital stay andall subsequent hospitalizations. Contact precau-tions remained in effect until two nasal swabs

and cultures of infected sites (if still present),obtained 1 week apart, were negative, providedthat the patients were not receiving antibioticsfor an active MRSA (or other) infection at thetime of these subsequent surveillance tests. Rou-tine MRSA decolonization was not recommend-ed (see the Supplementary Appendix).

Definitions of Prevalence, Transmission,

and health careAssociated Infection

We calculated the facility-wide rate of coloniza-tion at admission by dividing the number of pa-tient admissions with MRSA, as detected by nasalswabbing or clinical cultures within 48 hours afteradmission, by the total number of admissions tothe facility. As of April 2008, all persons who hada history of colonization or infection with MRSAwithin the previous 12 months were also consid-ered to be positive for MRSA at the time of admis-sion. A clinical culture was defined as a speci-men obtained from any body site, fluid, or drainagearea other than specimens obtained for surveil-lance. If MRSA was detected in both the nasal-

swab specimen and a clinical culture, the eventwas counted once in the category of clinical cul-ture. Geographic variation in prevalence was ex-amined according to the four regions of the Unit-ed States (Northeast, South, Midwest, and West)defined by the Census Bureau (www.census.gov).

Patients who were negative for MRSA at thetime of admission and during the 12 monthsbefore admission and were found to be colonizedor infected with MRSA after they had been in aunit for more than 48 hours were considered to

have an event of MRSA transmission attributableto that unit. Patients not known to be colonizedor infected with MRSA who were readmitted tothe hospital within 48 hours after discharge andwere found to be positive at the time of readmis-sion were considered to have a transmission eventattributable to the unit from which they had

been discharged.Health careassociated MRSA infections were

defined according to guidelines of the CDCsNational Healthcare Safety Network (NHSN),8with the following adaptations: a diagnosis ofMRSA infection required a positive culture, ratherthan just a clinical diagnosis by a physician, anda positive clinical culture was considered to becommunity-associated if it was obtained within48 hours after admission. After 48 hours, a posi-tive clinical culture obtained from a patient inwhom infection was not present or incubating at

the time of admission, as defined by NHSN crite-ria,9was considered to be a health careassoci-ated event. No molecular typing of the MRSAisolates was performed. A physician or other pro-fessional in infection prevention and control re-viewed the patients record to determine whetherthe criteria for a health careassociated infectionhad been met.

Data Management

Beginning in October 2007, MRSA prevention co-ordinators at all facilities entered, for each month,aggregate data on active surveillance testing andon the prevalence and transmission of MRSA andhealth careassociated MRSA infections into adatabase that was developed and maintained bythe VA Inpatient Evaluation Center (IPEC). Thecoordinators at all facilities also collected retro-spective information on health careassociatedMRSA infections detected in ICUs between Octo-ber 2005 and the end of September 2007 in orderto establish a baseline before implementation ofthe MRSA Prevention Initiative. With the excep-

tion of the category of systemic infection, dataentered into the MRSA data management Website at IPEC included all major categories ofhealth careassociated infections surveyed by theNHSN (e.g., urinary tract infections, bloodstreaminfections, pneumonia, and skin and soft-tissueinfections).8

In addition to data on health careassociatedMRSA infections, MRSA prevention coordinatorswere asked to enter into the IPEC database, onan optional basis, data on health careassociated





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infections with vancomycin-resistant enterococ-cus (VRE) and Clostridium difficile(defined accord-ing to NHSN guidelines8), each month from Oc-tober 2007 through June 2010.

For the purpose of the dissemination of thisinformation beyond the programmatic needs ofthe MRSA Prevention Initiative, the analysis was

approved by the institutional review boards atthe VA Pittsburgh Healthcare System and theCincinnati VA Medical Center.

Statistical Analysis

We used the SASstatistical program, version 9.2(SAS Institute), to extract monthly data on facility-level and unit-level variables from a MicrosoftSQL Server 2005 Analysis Services online analyti-cal processing cube (Microsoft) that was main-tained in secure f iles on a server at IPEC.

Data from all facilities were pooled for the

analyses. Facility-specific data were available forstratification when necessary. Adherence to activesurveillance testing was reported as the percentageof eligible patients who were tested, and the ratesof transmission and health careassociated infec-tion were expressed as the number per 1000 pa-tient-days. The rates of ventilator-associated pneu-monia and bloodstream infection associated withcentral venous catheters were expressed as thenumber per 1000 device-days. All data were ana-lyzed monthly except for data on MRSA blood-stream infections not associated with a device,pneumonias, urinary tract infections, and skin andsoft-tissue infections (defined according to NHSNguidelines8), which were evaluated quarterly owingto the small numbers of events.

Quantitative and qualitative variables are re-ported with the use of descriptive statistics.Trends were examined by means of Poisson re-gression models, and Students t-tests and analy-ses of variance with Duncans multiple-compar-isons method were used to compare groups ofinterest. The DurbinWatson (d) statistic was used

to test for the presence of autocorrelation in therates of health careassociated infections. Nostrong evidence was found; therefore, data trans-formations were deemed to be unnecessary.

Results

Characteristics of Patients and Facilities

The mean (SD) age of patients admitted to VAacute care facilities during the period included inthe analysis (October 2007 through June 2010)

was 62.614.4 years; 95% of the patients weremen. The median length of stay was 3.0 days(interquartile range, 2.0 to 7.0).

The VA has 153 hospitals nationwide. Duringthe period included in the analysis, 196 medical,coronary care, and surgical ICUs and 428 medi-cal, surgical, rehabilitation medicine, and spinal-cord injury units provided data to IPEC. Theseunits represented all VA medical centers nation-wide except for 3 that were exempted from par-ticipation.

There were 1,934,598 admissions to, transferswithin, or discharges from these units (ICUs,365,139; non-ICUs, 1,569,459) and 8,318,675 pa-tient-days (ICUs, 1,312,840; non-ICUs, 7,005,835).

Active SurveillanceA total of 1,712,537 surveillance screening testswere obtained during the analysis period frompatients who were admitted to or transferred ordischarged from acute care facilities nationwide(329,903 obtained in ICUs and 1,382,634 in non-ICUs). During this period, the percentage of pa-tients who were screened at admission increasedfrom 82% to 96%, and the percentage who werescreened at transfer or discharge increased from72% to 93% (Fig. 1).

Figure 1 (facing page).Active Surveillance Testing forMethicillin-Resistant Staphylococcus aureus(MRSA)

among Patients Admitted to and Those Transferredor Discharged from Acute Care Veterans Affairs (VA)

Medical Units Nationwide.

A MRSA bundle, comprising universal nasal surveil-lance for MRSA colonization, contact precautions for

patients who were carriers of MRSA, hand hygiene,and an institutional culture change whereby infection

control became the responsibility of everyone who hadcontact with patients, was implemented in 2007 in

acute care VA hospitals nationwide. The shaded arearepresents the transition period between the time

when all hospitals were required to have the programfunctional in at least one intensive care unit (ICU)

(March 2007) to full implementation of the MRSA bun-dle in all ICUs and non-ICUs (October 2007). The period

of analysis was from October 2007 through June 2010.

The number of patients who were screened at admis-sion and the number who were screened at transfer or

discharge are shown in Panel A; the rates at screeningat admission and at transfer or discharge are shown in

Panel B. Although only 35% of patients admitted to thehospital were being screened when the MRSA Preven-

tion Directive was issued in January 2007, this percent-age rapidly increased to 82% by October 2007 and to

96% by June 2010. The surveillance rate at the time oftransfer or discharge increased from 72% in October

2007 to 93% in June 2010.





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Prevalence of MRSA Colonization

or Infection at Admission

The mean (SD) monthly prevalence of MRSAcolonization or infection at admission in allmedical centers during the analysis period was13.63.7% (range of means across facilities, 5.4 to28.1). The ratio of patients with MRSA coloniza-tion or infection who were identified by active

surveillance to those identified by clinical cul-tures alone was 10:1 (Fig. 2). The prevalence ofcolonization or infection at admission was high-er among patients living in southern or north-eastern regions of the United States than amongthose living in western or midwestern regions(15.3% and 14.6%, respectively, for southern andnortheastern regions vs. 11.3% and 12.5%, re-

No.ofPatientsScreened

65,000

58,500

52,000

45,500

39,000

32,500

26,000

19,500

13,000

6,500

0

Oct.20

06

Dec.20

06

Feb.

2007

April

2007

June

2007

Aug.20

07

Oct.20

07

Dec.20

07

Feb.

2008

April

2008

June

2008

Aug.20

08

Oct.

2008

Dec.20

08

Feb.

2009

April

2009

June

2009

Feb.

2010

April

2010

June

2010

Aug.20

09

Oct.

2009

Dec.20

09

Screening at admission

Screening rate at admission

Screening at transfer or discharge

Screening rate at transfer or discharge

ScreeningRate(%)

0

100

80

90

70

60

40

30

10

50

20

Oct.2

006

Dec.2

006

Feb.2

007

April2

007

June2

007

Aug.2

007

Oct.2

007

Dec.2

007

Feb.2

008

April2

008

June2

008

Aug.2

008

Oct.2

008

Dec.2

008

Feb.2

009

April2

009

June2

009

Feb.2

010

April2

010

June2

010

Aug.2

009

Oct.2

009

Dec.2

009

A

B





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spectively, for western and midwestern regions;P


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lated to a device, from 0.16 to 0.06 per 1000 pa-tient-days, a decrease of 62% (P


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In non-ICUs, the rate of health careassoci-ated MRSA infection fell from 0.47 per 1000patient-days in October 2007 to 0.26 per 1000patient-days in June 2010, a decrease of 45%

(P


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in the second quarter (April through June) of2010, a decrease of 58% (P = 0.11). During thesame period, there were declines in the quar-terly rates of pneumonia, from 0.08 to 0.05 per1000 patient-days, a decrease of 38% (P = 0.02);urinary tract infection, from 0.09 to 0.05 per1000 patient-days, a decrease of 44% (P = 0.43);and skin and soft-tissue infections, from 0.15 to0.07 per 1000 patient-days, a decrease of 53%(P = 0.009) (Fig. 4B).

A total of 16 hospitals entered data on the

incidence of health careassociated VRE andC. diff icileinfections in ICUs consistently duringthe analysis period, and 17 hospitals entered dataon the incidence of these infections in non-ICUs.Poisson regression analysis for this subgroup ofhospitals showed that between October 2007and June 2010, there was a decline in the rate ofhealth careassociated MRSA infection from 2.81to 0.22 per 1000 patient-days in the ICUs, a de-crease of 92% (P


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care system. These declines were sustained dur-ing the 33 months of the analysis and were great-er than those reported recently in other U.S. ven-ues.10,11Investigations in smaller settings havealso shown reductions in health careassociatedMRSA infections when an approach similar tothat of the VA was used.12-20

The prevalence of MRSA carriage among VApatients at admission was 13.6%, as comparedwith a prevalence of 1.5% in the general U.S.population and 6.3% among patients in non-VAhospitals, as determined, in both cases, by meansof universal surveillance.16,21 We might haveseen a larger decrease in health careassociatedinfections if the prevalence had been lower, sincethere is a correlation between the prevalence ofcarriers and the incidence of health careassoci-ated infections.22,23

Because this VA initiative was a quality-im-

provement program rather than a prospectivelydesigned trial, data are not available to evaluatethe extent to which each component of thebundle may have contributed to the overall re-duction in health careassociated infections. Ad-herence to surveillance at admission, transfer,and discharge may be a surrogate marker for ad-herence to the bundle.

Active surveillance identified more than 90%of MRSA carriers who would have been missedwith clinical cultures alone. The sensitivity andspecificity of direct plating to a chromogenicmedium are similar to those of PCR, which rangefrom about 81% to 100% and 93% to 100%, re-spectively.24Identifying patients who were colo-nized with MRSA and isolating them with con-tact precautions was probably important, sincethe environment surrounding asymptomatic car-riers can be contaminated to the same extent asthe environment surrounding infected patients.25

Preventing transmission and subsequent coloni-zation with MRSA reduces the risk of infection,which may occur in more than a third of recent-

ly colonized patients,16,26-30

and decreases thereservoir of patients who can transmit MRSAduring future health care encounters.

The increase in adherence to active surveil-lance in the months after issuance of the VHAdirective and the subsequent declines in healthcareassociated MRSA infections were consis-tent with an institutional culture change thatresulted in health care workers being more aware

of health careassociated MRSA infections andincreasing their adherence to hand hygiene andcontact precautions. The MRSA Prevention Ini-tiative may have also affected the rates of healthcareassociated C. difficileand VRE infections. Itis known that hand hygiene reduces health careassociated infections, and contact precautions are

effective in preventing the transmission of MRSAand other pathogens.31,32

We do not know the extent to which concomi-tant infection-control initiatives may have con-tributed to the decrease in health careassociatedMRSA infections that we observed. Guidelineswere given for decolonization (see the Supple-mentary Appendix). Data from the national VHAPharmacy Benefits Management database showedthat, nationwide, inpatient orders for 2% mupi-rocin ointment, a surrogate for decolonizationefforts, were reduced from 0.013 orders per

unique patient in October 2007 to 0.009 ordersper unique patient in April 2010, suggesting thatthe use of decolonization regimens did not in-crease during the analysis period. Recommenda-tions for hand hygiene and transmission pre-cautions had been in place for years, and as partof a program to improve outcomes in VA ICUs,initiatives to decrease overall rates of bloodstreaminfection associated with central venous cathe-ters and ventilator-associated pneumonia wereimplemented in all VA ICUs as of April 2006.However, device-associated and nondevice-as-sociated MRSA infections did not decline sig-nificantly until after full implementation of theMRSA bundle in October 2007. The MRSA bun-dle may have had a complementary or synergisticeffect when it was added to the other initiativesthat were already in place.

An important approach to dealing with multi-drug-resistant bacteria is to control their spreadamong patients. The data from the VA suggestthat proactive efforts to prevent the transmis-sion of MRSA are associated with a reduction in

health careassociated MRSA infections. Patientsin acute care hospitals outside the VA systemmay also benefit from the implementation of anaggressive campaign to eradicate health careassociated MRSA infections that uses a strategysimilar to the VA strategy, but this would needto be tested. A phased-in approach targetinghigh-risk patients may be reasonable initially,but optimal control of health careassociated





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MRSA infections and the best ratio of cost tobenefit may be realized only with universal sur-veillance.16,33Although we did not make a for-mal costbenefit assessment of the VA MRSAPrevention Initiative, others have reported thatprograms of active surveillance are cost-effectiveover a wide range of prevalence and transmis-

sion rates.34,35Expanding elements of the pro-gram to long-term and ambulatory care settingsmay be necessary to deal with reservoirs of MRSAthroughout the health care system.

Presented in part at the Fifth Decennial International Confer-ence on Healthcare-Associated Infections, Atlanta, March 1822,2010.

No potential conf lict of interest relevant to this article wasreported.

Disclosure forms provided by the authors are available withthe full text of this article at NEJM.org.

We thank former Under Secretary for Health Michael J. Kuss-man, M.D., current Under Secretary for Health Robert A. Petzel,M.D., and Deputy Under Secretary for Health for Policy and Ser-vices Madhulika Agarwal, M.D., M.P.H., for support of the VHAMRSA Prevention Initiat ive; Jerry and Monique Sternin for intro-ducing the concept of positive deviance culture transforma-tion to our program; members of the MRSA Prevention Init iative

Data Workgroup (Caroline Sausman, R.N., Cheryl L. Squier,R.N., Mary Jane Rubino, R.N., Judith Whitlock, R.N., and KellyH. Burkitt, Ph.D.); Kathleen J. Risa, M.S.N., C.R.N.P., C.I.C., forproviding education on MRSA to all involved with the MRSAPrevention Initiative; Alan A. Celestino, Jr., R.Ph., research phar-macist specialist, VHA Pharmacy Benefits Management, for pro-viding data on national inpatient mupirocin use; and the MRSATaskforce and the MRSA prevention coordinators, infection pre-vention and control professionals, and infectious diseases spe-cialists at each facility for their efforts in improving the healthcare of U.S. veterans.

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