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Clostridium difcile Infections in Veterans Health Administration Acute Care Facilities Martin E. Evans, Loretta A. Simbartl, Stephen M. Kralovic, Rajiv Jain and Gary A. Roselle Infection Control & Hospital Epidemiology / Volume 35 / Issue 08 / August 2014, pp 1037 - 1042 DOI: 10.1086/677151, Published online: 16 January 2015

Link to this article: http://journals.cambridge.org/abstract_S0195941700094947 How to cite this article: Martin E. Evans, Loretta A. Simbartl, Stephen M. Kralovic, Rajiv Jain and Gary A. Roselle (2014). Clostridium difcile Infections in Veterans Health Administration Acute Care Facilities. Infection Control & Hospital Epidemiology, 35, pp 1037-1042 doi:10.1086/677151 Request Permissions : Click here

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infection control and hospital epidemiology

august 2014, vol. 35, no. 8

original article

Clostridium difficile Infections in Veterans Health Administration Acute Care Facilities Martin E. Evans, MD;1 Loretta A. Simbartl, MS;2 Stephen M. Kralovic, MD, MPH;2,3 Rajiv Jain, MD;4 Gary A. Roselle, MD2,3

objective. An initiative was implemented in July 2012 to decrease Clostridium difficile infections (CDIs) in Veterans Affairs (VA) acute care medical centers nationwide. This is a report of national baseline CDI data collected from the 21 months before implementation of the initiative. methods. Personnel at each of 132 data-reporting sites entered monthly retrospective CDI case data from October 2010 through June 2012 into a central database using case definitions similar to those of the National Healthcare Safety Network multidrug-resistant organism/ CDI module. results. There were 958,387 hospital admissions, 5,286,841 patient-days, and 9,642 CDI cases reported during the 21-month analysis period. The pooled CDI admission prevalence rate (including recurrent cases) was 0.66 cases per 100 admissions. The nonduplicate/ nonrecurrent community-onset not-healthcare-facility-associated (CO-notHCFA) case rate was 0.35 cases per 100 admissions, and the community-onset healthcare facility–associated (CO-HCFA) case rate was 0.14 cases per 100 admissions. Hospital-onset healthcare facility– associated (HO-HCFA), clinically confirmed HO-HCFA (CC-HO-HCFA), and CO-HCFA rates were 9.32, 8.40, and 2.56 cases per 10,000 patient-days, respectively. There were significant decreases in admission prevalence (P p .0006, Poisson regression), HO-HCFA (P p .003), and CC-HO-HCFA (P p .004) rates after adjusting for type of diagnostic test. CO-HCFA and CO-notHCFA rates per 100 admissions also trended downward (P p .07 and .10, respectively). conclusions. VA acute care medical facility CDI rates were higher than those reported in other healthcare systems, but unlike rates in other venues, they were decreasing or trending downward. Despite these downward trends, there is still a substantial burden of CDI in the system supporting the need for efforts to decrease rates further. Infect Control Hosp Epidemiol 2014;35(8):1037-1042

Clostridium difficile infection (CDI) is increasing across the United States, especially in older age groups.1 This is of concern to the Veterans Health Administration (VA), because many VA patients are in older age groups. Retrospective analyses using International Classification of Diseases, 9th Revision, Clinical Modification coded diagnoses (008.45) indicated that C. difficile infection rates in VA facilities were increasing2 and were higher than methicillin-resistant Staphylococcus aureus (MRSA) healthcare-associated infection (HAI) rates.3 For these reasons, a “Guideline for the Prevention of Clostridium difficile infection in Veterans Health Administration Inpatient Acute-Care Facilities” was developed on the basis of published guidelines4 with expert input. The guideline, which emphasizes environmental management, molecular diagnostic ap-

proaches, and infection prevention and control strategies for the prevention of CDI, was implemented nationwide as the CDI prevention initiative in July 2012. This is a report of nationwide CDI data from VA acute care facilities collected retrospectively for the 21-month period before implementation of the initiative.

methods Multidrug-resistant organism (MDRO) prevention coordinators (MPCs) at facilities from each of the 132 VA reporting sites were trained through extensive webinars and face-toface meetings to implement the initiative locally and collect data on CDI cases from their facility. Data reporting was facilitated with an Excel spreadsheet (CDI reporting tool),

Affiliations: 1. Veterans Health Administration, Methicillin-Resistant Staphylococcus aureus/Multidrug-Resistant Organism Prevention Office, National Infectious Diseases Service, Patient Care Services, Veterans Affairs Central Office, Lexington, Kentucky; Lexington Veterans Affairs Medical Center, Lexington, Kentucky; and Division of Infectious Diseases, Department of Internal Medicine, University of Kentucky School of Medicine, Lexington, Kentucky; 2. National Infectious Diseases Service, Patient Care Services, Veterans Affairs Central Office, Cincinnati, Ohio; 3. Cincinnati Veterans Affairs Medical Center, Cincinnati, Ohio; and Division of Infectious Diseases, Department of Internal Medicine, University of Cincinnati College of Medicine, Cincinnati, Ohio; 4. Patient Care Services, Veterans Affairs Central Office, Washington, DC. Received October 15, 2013; accepted March 15, 2014; electronically published June 20, 2014. This article is in the public domain, and no copyright is claimed. 0899-823X/2014/3508-0015$15.00. DOI: 10.1086/677151

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figure 1. Laboratory diagnostic tests. Percentage of reporting facilities whose clinical laboratories used nucleic acid amplification tests (NAAT), toxin A/B enzyme immunoassay (EIA), or other tests (glutamate dehydrogenase [GDH] plus NAAT, GDH plus toxin A/ B EIA, cell culture cytotoxin assay, or anaerobic toxigenic culture) as the predominant testing modality for the diagnosis of Clostridium difficile infection, October 2010 through June 2012.

developed by the MDRO Prevention Office, that automatically categorizes cases using standardized definitions. Definitions for CDI cases were analogous to those of the Centers for Disease Control and Prevention (CDC) National Healthcare Safety Network MDRO/CDI module for facilitywide inpatient areas5 with modifications (see below) made possible by the availability of a universal electronic health record (computerized patient record system [CPRS] within the Veterans Health Information Systems and Technology Architecture). CDI case onset was defined as the time at which a stool was collected for C. difficile testing (LabID event). A duplicate case was one in which the number of days from a previous positive CDI LabID event to the current positive test result was 14 days or less. A recurrent case was defined as one in which the number of days from a previous positive CDI LabID event to the current positive test result was more than 14 and less than or equal to 56 days. The percentage admission CDI prevalence rate was calculated as the number of nonduplicate positive LabID events (inclusive of recurrent cases) collected 24 hours or less before to 48 hours or less after admission to the acute care facility per 100 admissions (excluding mental health and observation patients). A community-onset healthcare facility–associated (CO-HCFA) case was defined as any nonduplicate/nonrecurrent CDI LabID event collected 24 hours or less before to 48 hours or less after admission to the acute care facility in cases in which the patient had been discharged from the same facility within the past 28 days; a community-onset not-healthcare-facilityassociated (CO-notHCFA) case was defined exactly the same as a CO-HCFA case with the exception that the patient had not been discharged from the same facility within the past

28 days; a hospital-onset HCFA (HO-HCFA) case was defined as any nonduplicate/nonrecurrent positive LabID event collected more than 48 hours after admission, and a clinically confirmed HO-HCFA (CC-HO-HCFA) case was defined as an HO-HCFA case with diarrhea or histopathologic or colonoscopic evidence of pseudomembranous colitis.4 CC-HOHCFA cases were collected to estimate the number of individuals who actually had an illness consistent with CDI, because a positive laboratory result can sometimes be obtained from the stool of an asymptomatic patient. CO-HCFA and CO-notHCFA case rates were calculated as the number of cases per 100 admissions. HO-HCFA and CC-HO-HCFA case rates were calculated as the number of cases per 10,000 patient-days. CO-HCFA case rates were calculated as both the number of cases per 100 admissions and the number of cases per 10,000 patient-days. For this retrospective analysis of VA baseline data, MPCs at each facility obtained a list of CDI LabID events from October 2010 through June 2012 from their local clinical laboratory, entered test-specific data into the CDI reporting tool, and transferred the aggregate results each month into a national database maintained by the VA Inpatient Evaluation Center in Cincinnati, Ohio.3 All statistical analyses of CDI case rate trends were performed using SAS version 9.3 (SAS Institute). Poisson regression models, using a log-link function and either admis-

figure 2. Monthly pooled Clostridium difficile infection (CDI) admission prevalence. Nonduplicate CDI cases with positive CDI LabID event collected 24 hours or less before to 48 hours or less after admission to Veterans Affairs (VA) acute care inpatient facilities nationwide October 2010 through June 2012. Total admission prevalence included recurrent cases. Community-onset not-healthcarefacility-associated (CO-notHCFA) and community-onset healthcare facility–associated (CO-HCFA) rates do not include recurrent cases. All CO cases are a summation of CO-notHCFA and CO-HCFA cases. Total admission prevalence rate per 100 admissions decreased significantly (P p .0006, Poisson multivariable regression analysis after adjusting for type of diagnostic test), CO-notHCFA, and CO-HCFA rates per 100 admissions trended downward (P p .10 and .07, respectively).

baseline va c. difficile infection rates

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to degrees of freedom was used to check for overdispersion. All P values were based on 2-tailed tests, and P less than or equal to .05 was considered significant. The process of reviewing de-identified national data sets was approved by the Cincinnati VA Medical Center Institutional Review Board (05-6-29-2).

results

figure 3. Monthly pooled healthcare facility–associated Clostridium difficile infection (CDI) rates. Nationwide rates of hospital-onset healthcare facility–associated (HO-HCFA), clinically confirmed HOHCFA (CC-HO-HCFA), and community-onset healthcare facility– associated (CO-HCFA) cases per 10,000 patient-days from October 2010 through June 2012. There was a significant decrease in HOHCFA, CC-HO-HCFA, and CO-HCFA rates (P p .003, .004, and .05 respectively, by Poisson multivariable regression analysis after adjusting for type of diagnostic test).

sions or patient-days as the offset variable, were used to examine the change in infections over time. Because patientspecific information was not available to censor patient-days after a CDI diagnosis, the effect of censoring patient-days was simulated by recalculating HO-HCFA, CC-HO-HCFA, and CO-HCFA rates with a 20% and 40% reduction in patientdays using the same Poisson models. Poisson regression models included terms for the type of CDI diagnostic test (nucleic acid amplification test [NAAT] vs toxin A/B enzyme immunoassay [EIA] vs other [glutamate dehydrogenase (GDH) plus NAAT, GDH plus toxin A/B EIA, cell culture cytotoxin assay, or anaerobic toxigenic culture]), as well as a CDI testtime interaction term. A ratio of the scaled Pearson x2 value

Of the 132 VA reporting sites, 128 provided monthly data from October 2010 through June 2012 for this report. During the 21-month analysis period, there were 958,387 admissions and 5,286,841 patient-days in these VA acute care facilities nationwide. In October 2010, approximately 32% of facility clinical laboratories used a NAAT alone, 62% used a toxin A/B EIA alone, and 6% used other tests for the diagnosis of CDI. During the analysis period, NAAT was adopted by more laboratories, and by June 2012, 54% of clinical laboratories used a NAAT, 35% used a toxin A/B EIA, and 11% used other tests (Figure 1). There were 9,642 CDI cases during the 21-month analysis period. A total of 3,363 (35%) were CO-notHCFA CDI cases, 1,354 (14%) were CO-HCFA CDI cases, and 4,925 (51%) were HO-HCFA CDI cases. Of the latter, 4,439 (90%) were clinically confirmed (CC-HO-HCFA). The pooled CDI admission prevalence rate (including recurrent cases) was 0.66 cases per 100 admissions (Figure 2). Pooled nonduplicate/nonrecurrent CO-notHCFA, COHCFA, and all CO case rates per 100 admissions were 0.35, 0.14, and 0.49, respectively (Figure 2). Pooled HO-HCFA, CC-HO-HCFA, and CO-HCFA CDI case rates per 10,000 patient-days were 9.32, 8.40, and 2.56, respectively (Figure 3). Based on Poisson regression models that adjusted for the type of diagnostic test, admission CDI prevalence (nonduplicate, including recurrent cases) per 100 admissions decreased 23% over the 21-month analysis period (Table 1). The nonduplicate/nonrecurrent CO-notHCFA and CO-

table 1. Mean Number of Clostridium difficile Infections (CDIs), October 2010–June 2012, Based on Poisson Regression Model, Showing Effect of Time on CDI Rates Mean (95% CI) Variable CDI at admission, per 100 admissionsb CO-notHCFA, per 100 admissionsc CO-HCFA, per 100 admissionsc HO-HCFA, per 10,000 patient-days CC-HO-HCFA, per 10,000 patient-days CO-HCFA, per 10,000 patient-days

October 2010

June 2012

P value for time effecta

0.69 (0.65–0.74) 0.36 (0.33–0.39) 0.14 (0.12–0.17) 11 (10–12) 10 (9–10) 3 (2–3)

0.53 (0.50–0.57) 0.34 (0.31–0.37) 0.11 (0.09–0.13) 8 (8–9) 8 (7–8) 2 (2–2)

.0006 .10 .07 .003 .004 .05

note. CI, confidence interval; CO, community onset; HCFA, healthcare facility associated; HO, hospital onset. a Wald x2 test. b Nonduplicate, including recurrent. c Nonduplicate, nonrecurrent.

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table 2. Mean Number of Clostridium difficile Infections (CDIs), October 2010–June 2012, Based on Poisson Regression Model, Showing Effect of Time–Test Type Interaction on CDI Rates Toxin A/B EIA Variable

Other testsa

NAAT

Oct 2010

Jun 2012

Oct 2010

Jun 2012

Oct 2010

Jun 2012

0.45 0.21 0.11 7 7 2

0.35 0.19 0.08 6 5 2

0.94 0.47 0.19 13 11 3

0.72 0.45 0.14 10 9 2

0.79 0.47 0.14 13 12 3

0.61 0.44 0.10 10 10 2

b

Nonduplicate CDI at admission, cases per 100 admissions CO-notHCFA, cases per 100 admissionsc CO-HCFA, cases per 100 admissionsc HO-HCFA, cases per 10,000 patient-days CC-HO-HCFA, cases per 10,000 patient-days CO-HCFA, cases per 10,000 patient-days

note. CC, clinically confirmed; CO, community onset; HCFA, healthcare facility associated; HO, hospital onset; EIA, enzyme immunoassay; NAAT, nucleic acid amplification test. a Glutamate dehydrogenase (GDH) plus NAAT, GDH plus toxin A/B EIA, cell culture cytotoxin assay, or anaerobic toxigenic culture. b Nonduplicate, including recurrent. c Nonduplicate, nonrecurrent.

HCFA rates per 100 admissions decreased 6% and 21%, respectively, although the trend for decrease was not significant for either. Rates of HO-HCFA, CC-HO-HCFA, and COHCFA cases per 10,000 patient-days decreased 27%, 20%, and 33%, respectively (Table 1). Significant CDI test-time interaction terms were only present in the models for COnotHCFA per 100 admissions and HO-HCFA per 10,000 patient-days (P p .03 and .02, respectively; Table 2). Examination of the parameter estimates associated with these terms revealed that the significant decreases indicated by the time effect results did not differ among the CDI testing modalities. Therefore, the decrease in CDI rates was evident regardless of test type used. Reducing the patient-days by 20% and 40% to simulate censoring patient days after a CDI diagnosis did not change the significance of HO-HCFA, CC-HO-HCFA, or CO-HCFA rate trends over time.

discussion A nationwide initiative for the prevention of CDI in VA acute care facilities was implemented, and baseline data from the 21-month period preceding implementation were collected and analyzed. We obtained data on CDI admission prevalence, laboratory testing, and CDI case rates. Admission prevalence for acute care VA facilities was 0.66 cases per 100 admissions over the 21-month analysis period. This statistic included recurrent CDI cases and was 35% higher than the admission prevalence would have been if calculated using a summation of CO-HCFA and COnotHCFA rates, which do not include recurrent cases. To our knowledge, admission prevalence calculations that include recurrent cases have not been reported before. Including recurrent cases when assessing admission prevalence may be important if these cases are a significant pool from which subsequent healthcare transmission occurs. Others have reported admission prevalence in terms of community-onset cases that did not include recurrent cases. Although comparisons with others are compromised by nuances in defi-

nitions and differences in diagnostic testing, the respective VA CO-HCFA and CO-notHCFA rates of 0.14 and 0.35 per 100 admissions were approximately double the corresponding rates of 0.084 and 0.155 cases per 100 admissions reported by Zilberberg et al6 among 85 hospitals reporting to a large electronic database from 2007 to 2008. VA CO-notHCFA rates were also approximately double the rate of 0.19 cases per 100 admissions reported among 5 academic medical centers from 2000 to 2006 by Dubberke et al.7 CO-HCFA rates have also been reported per 10,000 patient-days instead of per 100 admissions. In that context, the VA rate of 2.6 cases per 10,000 patient-days was twice the 1.3 cases per 10,000 patient-days reported by Dubberke et al7 but similar to the 2.7 cases per 10,000 patient-days reported by Benoit et al8 and the 2.4 cases per 10,000 patient-days reported by the New York State Department of Health9 (Table 3). The HO-HCFA CDI rate of 9.3 cases per 10,000 patientdays in VA facilities was higher than those reported by others outside the VA since 2000 (Table 3). Dubberke et al7 found that symptomatic HO-HCFA CDI rates ranged from 7.0 to 8.5 cases per 10,000 patient-days, and Campbell et al10 reported rates ranging from 6.4 to 7.9 cases per 10,000 patientdays in Ohio acute care hospitals in 2006. Others reported HO-HCFA CDI rates of 6.3 cases per 10,000 patient-days in a large private electronic database from 2007 to 2008,6 7.8 cases per 10,000 patient-days in the CDC BioSense database from 2007 to 2008,8 and 2.8 cases per 10,000 patient-days in 28 community hospitals from 2008 to 2009.11 The pooled rate for HO-HCFA cases among 711 acute care hospitals reporting to the National Healthcare Safety Network in 2010 was 7.4 cases per 10,000 patient-days,12 and most recently, the New York State Department of Health reported a rate of 8.5 cases per 10,000 patient-days.9 Use of NAATs, cleared by the US Food and Drug Administration within the past several years for the diagnosis of CDI, has been associated with increased CDI rates, possibly because of the increased sensitivity of the test relative to toxin A/B EIA.13 Longtin et al14 showed that the incidence of CDI

baseline va c. difficile infection rates

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table 3. Reported Prevalence of Clostridium difficile Infection (CDI)

Report Dubberke et al7 Campbell et al10 Zilberberg et al6 Benoit et al8 Miller et al11 McDonald et al12 New York State Department of Health9 Veterans Health Administration (this study)

Data collection dates 2000–2006 2006 2007–2008 2007–2008 2008–2009 2010

HO-HCFA rate per 10,000 patient-days

CO-HCFA rate per 10,000 patient-days

0 0 35

7.0–8.5 6.4–7.9 6.3 7.8 2.8 7.4

1.3 NR NR 2.7 NR NR

No. of facilities (no. of patient-days) 5 210 85 34 28 711

Diagnosis by NAAT, %

(5,476,405)

NR NR NR

(7,906,463) (2,755,865) (3,007,457) (NR)

2011

177 (12,242,504)

41

8.5

2.4

2010–2012

128 (5,286,841)

47 (range, 31–61)

9.3

2.6

note. CO, community onset; HCFA, healthcare facility associated; HO, hospital onset; NAAT, nucleic acid amplification test; NR, not reported.

increased by 50% or greater when NAAT came into widespread use, and Moehring et al15 reported a 56% increase in CDI incidence with the use of NAAT. The data in this report support higher CDI rates when using NAAT as opposed to toxin A/B EIA (Table 2). Increasing use of NAAT for CDI diagnosis may account, in part, for the experience of the New York State Department of Health and the VA, which both had relatively high rates of CDI (Table 3). Analyses of trends in VA CDI case rates showed a significant decrease in HO-HCFA rate over the analysis period after controlling for the type of diagnostic test performed. It is not clear why this rate decreased before implementation of the CDI prevention initiative, because rates have been increasing in older populations in the United States.1 We previously showed a decrease in CDI rates after implementation of the VA MRSA prevention initiative in 2007,3,16 suggesting that the “MRSA bundle,” which includes an emphasis on hand hygiene and an institutional culture transformation where infection control becomes everyone’s business, may have had an effect. The addition of an MPC to each facility for the MRSA prevention initiative and implementation of nationwide hand hygiene and antibiotic stewardship directives in the VA may have enhanced infection prevention and control efforts in facilities as well, resulting in a decrease in CDI rates.17-19 There are a number of potential limitations to this analysis. First, the results from a cohort of over 6 million veterans served by the VA may not be generalizable to other populations in the United States. However, because CDI tends to affect the elderly population disproportionately to other age groups, and 40% of veterans are 65 years of age or older, the data from this report may be of value. The data were collected retrospectively and entered by hand by MPCs at each local facility, introducing the possibility of transcription errors. The CDI reporting tool, which accurately categorizes each case on the basis of patient admission history and the LabID event time stamp, should have greatly facilitated the accuracy of case categorization. The large number of data points may

have helped to ensure that occasional errors would have minimal impact on the database as a whole. When comparing the VA experience to that of other healthcare systems, strict comparisons may have been limited because of nuances in definitions, the possible use of a calendar day rule to operationalize a 48-hour rule without time stamps, and different diagnostic assays. Sohn et al20 reported that different definitions of healthcare-associated CDI resulted in a 30% difference in rates. Finally, we do not have an explanation for the low number of HO-HCFA cases reported in the summer of 2011. It was not the result of missing data or outliers in the database. All of our regression models were evaluated for goodness-of-fit, and this one month did not have an undue influence on our results. Others have reported that rates of healthcare-acquired CDI now exceed those of MRSA HAIs.11 This is the case in VA acute care facilities. In June 2012, MRSA HAI rates in VA intensive care units (ICUs) and non-ICUs combined was 2.1 cases per 10,000 patient-days.21 Our retrospective analysis suggests that the baseline HO-HCFA CDI case rate (9.32 cases per 10,000 patient-days) is more than 4 times higher. This information supports the need for an aggressive CDI prevention initiative.

acknowledgments We wish to thank the VA Under Secretary for Health, the Deputy Under Secretary for Health for Policy and Services, the VA MRSA/MDRO Taskforce, the MRSA/MDRO Prevention Coordinators, Infection Prevention and Control Professionals, Infectious Diseases specialists, and clinical laboratory personnel at each facility for support of the MDRO prevention initiatives and their hard work and dedication toward improving the health care of America’s Veterans. Thank you also to the CDI Data Workgroup and MDRO Prevention Office staff for their educational activities and help with data validation and cleaning. Potential conflicts of interest. All authors report no conflicts of interest relevant to this article. All authors submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and the conflicts that the editors consider relevant to this article are disclosed here.

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Address correspondence to Martin E. Evans, MD, Room B415, 1101 Veterans Drive, Lexington, KY 40502 ([email protected]).

11.

references 1. Centers for Disease Control and Prevention. QuickStats: rates of Clostridium difficile infection among hospitalized patients aged ≥65 years, by age group—National Hospital Discharge Survey, United States, 1996–2009. MMWR Morb Mortal Wkly Rep 2011;60:1171. 2. Kralovic SM, Simbartl LA, Danko LH, et al. Clostridium difficile infections in U.S. Department of Veterans Affairs medical centers— nationwide trends for acute care hospitalizations. In: Program and abstracts of IDWeek 2012. San Diego, CA: IDWeek, 2012. Abstract 345. 3. Jain R, Kralovic SM, Evans ME, et al. Veterans Affairs initiative to prevent methicillin-resistant Staphylococcus aureus infections. N Engl J Med 2011;364:1419–1430. 4. Cohen SH, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA). Infect Control Hosp Epidemiol 2010;31:431–455. 5. National Healthcare Safety Network. Multidrug-resistant organism & Clostridium difficile–infection (MDRO/CDI) module. http://www.cdc.gov/nhsn/PDFs/pscManual/12pscMDRO _CDADcurrent.pdf. Published January 2014. Accessed March 10, 2014. 6. Zilberberg MD, Tabak YP, Sievert DM, et al. Using electronic health information to risk-stratify rates of Clostridium difficile infection in US hospitals. Infect Control Hosp Epidemiol 2011; 32:649–655. 7. Dubberke ER, Butler AM, Yokoe DS, et al. Multicenter study of Clostridium difficile infection rates from 2000 to 2006. Infect Control Hosp Epidemiol 2010;31:1030–1037. 8. Benoit SR, McDonald LC, English R, Tokars JI. Automated surveillance of Clostridium difficile infections using BioSense. Infect Control Hosp Epidemiol 2011;32:26–33. 9. New York State Department of Health. Hospital-acquired infections, New York State, 2011. http://www.health.ny.gov /statistics/facilities/hospital/hospital_acquired_infections/2011 /docs/hospital_acquired_infection.pdf. Published September 2012. Accessed March 10, 2014. 10. Campbell RJ, Giljahn L, Machesky K, et al. Clostridium difficile

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Clostridium difficile infections in Veterans Health Administration acute care facilities.

An initiative was implemented in July 2012 to decrease Clostridium difficile infections (CDIs) in Veterans Affairs (VA) acute care medical centers nat...
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