Sarah S. Lewis

Enhanced terminal room disinfection and acquisition and infection caused by multidrug-resistant organisms and Clostridium difficile (the Benefits of Enhanced Terminal Room Disinfection study): a cluster-randomised, multicentre, crossover study

BACKGROUND Patients admitted to hospital can acquire multidrug-resistant organisms and Clostridium difficile from inadequately disinfected environmental surfaces. We determined the effect of three enhanced strategies for terminal room disinfection (disinfection of a room between occupying patients) on acquisition and infection due to meticillin-resistant Staphylococcus aureus, vancomycin-resistant enterococci, C difficile, and multidrug-resistant Acinetobacter. METHODS We did a pragmatic, cluster-randomised, crossover trial at nine hospitals in the southeastern USA. Rooms from which a patient with infection or colonisation with a target organism was discharged were terminally disinfected with one of four strategies: reference (quaternary ammonium disinfectant except for C difficile, for which bleach was used); UV (quaternary ammonium disinfectant and disinfecting ultraviolet [UV-C] light except for C difficile, for which bleach and UV-C were used); bleach; and bleach and UV-C. The next patient admitted to the targeted room was considered exposed. Every strategy was used at each hospital in four consecutive 7-month periods. We randomly assigned the sequence of strategies for each hospital (1:1:1:1). The primary outcomes were the incidence of infection or colonisation with all target organisms among exposed patients and the incidence of C difficile infection among exposed patients in the intention-to-treat population. This trial is registered with ClinicalTrials.gov, NCT01579370. FINDINGS 31 226 patients were exposed; 21 395 (69%) met all inclusion criteria, including 4916 in the reference group, 5178 in the UV group, 5438 in the bleach group, and 5863 in the bleach and UV group. 115 patients had the primary outcome during 22 426 exposure days in the reference group (51·3 per 10 000 exposure days). The incidence of target organisms among exposed patients was significantly lower after adding UV to standard cleaning strategies (n=76; 33·9 cases per 10 000 exposure days; relative risk [RR] 0·70, 95% CI 0·50-0·98; p=0·036). The primary outcome was not statistically lower with bleach (n=101; 41·6 cases per 10 000 exposure days; RR 0·85, 95% CI 0·69-1·04; p=0·116), or bleach and UV (n=131; 45·6 cases per 10 000 exposure days; RR 0·91, 95% CI 0·76-1·09; p=0·303) among exposed patients. Similarly, the incidence of C difficile infection among exposed patients was not changed after adding UV to cleaning with bleach (n=38 vs 36; 30·4 cases vs 31·6 cases per 10 000 exposure days; RR 1·0, 95% CI 0·57-1·75; p=0·997). INTERPRETATION A contaminated health-care environment is an important source for acquisition of pathogens; enhanced terminal room disinfection decreases this risk. FUNDING US Centers for Disease Control and Prevention.

Rising Rates of Carbapenem-Resistant Enterobacteriaceae in Community Hospitals: A Mixed-Methods Review of Epidemiology and Microbiology Practices in a Network of Community Hospitals in the Southeastern United States

OBJECTIVE Describe the epidemiology of carbapenem-resistant Enterobacteriaceae (CRE) and examine the effect of lower carbapenem breakpoints on CRE detection. DESIGN Retrospective cohort. SETTING Inpatient care at community hospitals. PATIENTS All patients with CRE-positive cultures were included. METHODS CRE isolated from 25 community hospitals were prospectively entered into a centralized database from January 2008 through December 2012. Microbiology laboratory practices were assessed using questionnaires. RESULTS A total of 305 CRE isolates were detected at 16 hospitals (64%). Patients with CRE had symptomatic infection in 180 cases (59%) and asymptomatic colonization in the remainder (125 cases; 41%). Klebsiella pneumoniae (277 isolates; 91%) was the most prevalent species. The majority of cases were healthcare associated (288 cases; 94%). The rate of CRE detection increased more than fivefold from 2008 (0.26 cases per 100,000 patient-days) to 2012 (1.4 cases per 100,000 patient-days; incidence rate ratio (IRR), 5.3 [95% confidence interval (CI), 1.22-22.7]; P = .01). Only 5 hospitals (20%) had adopted the 2010 Clinical and Laboratory Standards Institute (CLSI) carbapenem breakpoints. The 5 hospitals that adopted the lower carbapenem breakpoints were more likely to detect CRE after implementation of breakpoints than before (4.1 vs 0.5 cases per 100,000 patient-days; P < .001; IRR, 8.1 [95% CI, 2.7-24.6]). Hospitals that implemented the lower carbapenem breakpoints were more likely to detect CRE than were hospitals that did not (3.3 vs 1.1 cases per 100,000 patient-days; P = .01). CONCLUSIONS The rate of CRE detection increased fivefold in community hospitals in the southeastern United States from 2008 to 2012. Despite this, our estimates are likely underestimates of the true rate of CRE detection, given the low adoption of the carbapenem breakpoints recommended in the 2010 CLSI guidelines.

Assessing the relative burden of hospital-acquired infections in a network of community hospitals.

Hospital-acquired infections (HAIs) occur commonly, cause significant harm to patients, and result in excess healthcare expenditures.1 The urinary tract is frequently cited as the most common site of HAI, but these estimates were extrapolated from National Nosocomial Infection Surveillance (NNIS) data from the 1990s.1 Updated information regarding the relative burden of specific types of HAIs would help governmental agencies and other stakeholders within the field of infection prevention to prioritize areas for research and innovation. The objective of our study was to assess the relative proportion of HAIs attributed to each of the following 5 types of infection in a network of community hospitals: catheter-associated urinary tract infection (CAUTI), surgical site infection (SSI), ventilator-associated pneumonia (VAP), central line–associated bloodstream infection (CLABSI), and Clostridium difficile infection (CDI). We performed a retrospective cohort study using prospectively collected HAI surveillance data from hospitals participating in the Duke Infection Control Outreach Network (DICON). DICON hospital epidemiologists and liaison infection preventionists work directly with local hospital infection preventionists to provide surveillance data validation, benchmarking, and infection prevention consultation services to participating hospitals.2 Fifteen DICON-affiliated community hospitals (median size, 186 beds; range, 50–457 beds) that had continuously collected hospital-wide and surgical surveillance data from January 1, 2010, through June 30, 2012, were included in the study. Infection preventionists at each hospital prospectively identified all HAIs occurring in intensive care unit (ICU) and non-ICU locations using standardized National Healthcare Safety Network (NHSN) surveillance definitions.3,4 All adult and pediatric cases of CLABSI, CAUTI, VAP, and hospital-onset healthcare facility–associated (HO-HCFA) CDI identified during the study period were included in the analysis. SSIs identified after 37 procedure types performed during the study period were included in this analysis if they met the following criteria: (1) surgery did not involve implanted material, and SSI occurred within 30 days; or (2) surgery involved implanted material, and SSI occurred within 90 days. The 30-month healthcare exposure period included 100,449 surgical procedures, 135,716 ICU inpatient-days, 1,596,277 non-ICU inpatient-days, 244,105 central line-days, 393,948 urinary catheter–days, and 53,352 ventilator-days. A total of 2,345 HAIs were identified. SSIs were the most common HAI (n = 882; 38%). The second most common HAI was CAUTI (n = 611; 26%), followed by HO-HCFA CDI (n = 514; 22%), CLABSI (n = 280; 12%), and VAP (n = 58; 2%). The median percentage of HAIs due to SSIs at each hospital was 43% (range, 16%–63%). SSIs were the most frequent HAI for 12 hospitals (80%). The proportion of HAIs due to SSIs was not related to surgical volume or the ratio between surgical and inpatient volume at individual hospitals (data not shown). The overall prevalence rate of SSI in our cohort was 0.82 infections per 100 operations. The most common surgical procedures to result in infections are shown in Table 1 and include colon surgery (90 SSIs; 2.6 SSIs per 100 operations), open herniorrhaphy (69 SSIs; 0.7 SSIs per 100 operations), knee replacement surgery (63 SSIs; 0.8 SSIs per 100 operations), and Cesarean delivery (63 SSIs; 0.9 SSIs per 100 operations). One-third of all identified SSIs (n = 316) were superficial-incisional. A total of 600 SSIs (68%) were identified at the time of hospital readmission. Only 169 SSIs (19%) were identified in the outpatient setting. The incidence rates of other HAIs were comparable to or lower than rates published by the NHSN5 and included 1.6 CAUTIs per 1,000 urinary catheter-days, 1.1 CLABSIs per 1,000 central line-days, 1.1 VAPs per 1,000 ventilator-days, and 3.0 cases of HO-HCFA per 10,000 inpatient-days. TABLE 1 Prevalence Rates of Surgical Site Infection (SSI) for Select Surgical Procedures, Duke Infection Control Outreach Network, January 1, 2010–June 30, 2012 SSIs were the most frequently observed HAI in this large cohort of community hospitals in the southeastern United States. This finding is remarkable, because the overall rate of SSI in this cohort was low. However, because the surgical volume in these hospitals was relatively high, the total burden of HAIs due to SSI exceeded that of other HAIs. Our large, multicenter study validates the results of other recent investigations. For example, SSIs were the most common HAI and accounted for 39% of all HAIs reported to the NHSN at a single academic medical center.6 In another study, SSIs accounted for 31% of the 58 HAIs identified during a point prevalence survey of 9 acute care hospitals in a single city.7 Our study has important limitations. First, our cohort included only community hospitals in one region of the United States. Thus, even though the majority of hospitals in the United States are similar in size to the hospitals in our cohort, our results may not be generalizable to all settings. Second, we suspect that our data underestimate the true frequency with which SSIs actually occur. SSIs occurring in outpatients are underrecognized by current SSI surveillance mechanisms. This is particularly important because more than 50% of all SSIs occur after hospital discharge.8 Additionally, because non-ventilator-associated pneumonias, non-catheter-associated UTIs, and SSIs after procedure types not reported to the NHSN were not included in this data analysis, we may have undercounted the actual burden of SSIs and other types of HAIs in this cohort of hospitals.6 We believe, however, that it is unlikely that any one specific HAI not included in our analysis occurs frequently enough to supplant SSIs as the most common HAI. SSIs are now the most common HAI in our community hospital network. We believe that our findings highlight the need for improved and expanded evidence-based interventions to effectively reduce the rate of SSIs in real-world settings. Collectively, the infection prevention community has already made substantial and important progress in reducing HAIs due to CLABSI and CAUTI in the past decade. It is time to shift our focus to finding better and new ways to prevent SSI.

Two-Phase Hospital-Associated Outbreak of Mycobacterium abscessus: Investigation and Mitigation

Background Nontuberculous mycobacteria (NTM) commonly colonize municipal water supplies and cause healthcare-associated outbreaks. We investigated a biphasic outbreak of Mycobacterium abscessus at a tertiary care hospital. Methods Case patients had recent hospital exposure and laboratory-confirmed colonization or infection with M. abscessus from January 2013 through December 2015. We conducted a multidisciplinary epidemiologic, field, and laboratory investigation. Results The incidence rate of M. abscessus increased from 0.7 cases per 10000 patient-days during the baseline period (January 2013-July 2013) to 3.0 cases per 10000 patient-days during phase 1 of the outbreak (August 2013-May 2014) (incidence rate ratio, 4.6 [95% confidence interval, 2.3-8.8]; P < .001). Thirty-six of 71 (51%) phase 1 cases were lung transplant patients with positive respiratory cultures. We eliminated tap water exposure to the aerodigestive tract among high-risk patients, and the incidence rate decreased to baseline. Twelve of 24 (50%) phase 2 (December 2014-June 2015) cases occurred in cardiac surgery patients with invasive infections. Phase 2 resolved after we implemented an intensified disinfection protocol and used sterile water for heater-cooler units of cardiopulmonary bypass machines. Molecular fingerprinting of clinical isolates identified 2 clonal strains of M. abscessus; 1 clone was isolated from water sources at a new hospital addition. We made several water engineering interventions to improve water flow and increase disinfectant levels. Conclusions We investigated and mitigated a 2-phase clonal outbreak of M. abscessus linked to hospital tap water. Healthcare facilities with endemic NTM should consider similar tap water avoidance and engineering strategies to decrease risk of NTM infection.

Epidemiology of methicillin-resistant Staphylococcus aureus pneumonia in community hospitals.

OBJECTIVE Describe the epidemiology of healthcare-related (ie, healthcare-associated and hospital-acquired) pneumonia due to methicillin-resistant Staphylococcus aureus (MRSA) among hospitalized patients in community hospitals. DESIGN Retrospective cohort study. SETTING Twenty-four community hospitals in the southeastern United States affiliated with the Duke Infection Control Outreach Network (median size, 211 beds; range, 103-658 beds). METHODS Adult patients with healthcare-related MRSA pneumonia admitted to study hospitals from January 1, 2008, to December 31, 2012, were identified using surveillance data. Seasonal and annual incidence rates (cases per 100,000 patient-days) were estimated using generalized estimating equation models. Characteristics of community-onset and hospital-onset cases were compared. RESULTS A total of 1,048 cases of healthcare-related pneumonia due to MRSA were observed during 5,863,941 patient-days. The annual incidence rate of healthcare-related MRSA pneumonia increased from 11.3 cases per 100,000 patient-days (95% confidence interval [CI], 6.8-18.7) in 2008 to 15.5 cases per 100,000 patient-days (95% CI, 8.4-28.5) in 2012 (P = .055). The incidence rate was highest in winter months and lowest in summer months (15.4 vs 11.1 cases per 100,000 patient-days; incidence rate ratio, 1.39 [95% CI, 1.06-1.82]; P = .016). A total of 814 cases (77.7%) were community-onset healthcare-associated pneumonia cases; only 49 cases (4.7%) were ventilator-associated cases. Of 811 patients whose disposition was known, 240 (29.6%) died during hospitalization or were discharged to hospice. CONCLUSIONS From 2008 through 2012, the incidence of healthcare-related MRSA pneumonia among patients who were admitted to a large network of community hospitals increased, despite the decreasing incidence of invasive MRSA infections nationwide. Additional study is warranted to evaluate trends in this important and potentially modifiable public health problem.

Seasonal Variation of Common Surgical Site Infections: Does Season Matter?

OBJECTIVE To evaluate seasonal variation in the rate of surgical site infections (SSI) following commonly performed surgical procedures. DESIGN Retrospective cohort study. METHODS We analyzed 6 years (January 1, 2007, through December 31, 2012) of data from the 15 most commonly performed procedures in 20 hospitals in the Duke Infection Control Outreach Network. We defined summer as July through September. First, we performed 3 separate Poisson regression analyses (unadjusted, multivariable, and polynomial) to estimate prevalence rates and prevalence rate ratios of SSI following procedures performed in summer versus nonsummer months. Then, we stratified our results to obtain estimates based on procedure type and organism type. Finally, we performed a sensitivity analysis to test the robustness of our findings. RESULTS We identified 4,543 SSI following 441,428 surgical procedures (overall prevalence rate, 1.03/100 procedures). The rate of SSI was significantly higher during the summer compared with the remainder of the year (1.11/100 procedures vs 1.00/100 procedures; prevalence rate ratio, 1.11 [95% CI, 1.04-1.19]; P=.002). Stratum-specific SSI calculations revealed higher SSI rates during the summer for both spinal (P=.03) and nonspinal (P=.004) procedures and revealed higher rates during the summer for SSI due to either gram-positive cocci (P=.006) or gram-negative bacilli (P=.004). Multivariable regression analysis and sensitivity analyses confirmed our findings. CONCLUSIONS The rate of SSI following commonly performed surgical procedures was higher during the summer compared with the remainder of the year. Summer SSI rates remained elevated after stratification by organism and spinal versus nonspinal surgery, and rates did not change after controlling for other known SSI risk factors.

Postoperative infection in spine surgery: does the month matter?

OBJECT The relationship between time of year and surgical site infection (SSI) following neurosurgical procedures is poorly understood. Authors of previous reports have demonstrated that rates of SSI following neurosurgical procedures performed during the summer months were higher compared with rates during other seasons. It is unclear, however, if this difference was related to climatological changes or inexperienced medical trainees (the July effect). The aim of this study was to evaluate for seasonal variation of SSI following spine surgery in a network of nonteaching community hospitals. METHODS The authors analyzed 6 years of prospectively collected surveillance data (January 1, 2007, to December 31, 2012) from all laminectomies and spinal fusions from 20 hospitals in the Duke Infection Control Outreach Network of community hospitals. Surgical site infections were defined using National Healthcare Safety Network criteria and identified using standardized methods across study hospitals. Regression models were then constructed using Poisson distribution to evaluate for seasonal trends by month. Each analysis was first performed for all SSIs and then for SSIs caused by specific organisms or classes of organisms. Categorical analysis was performed using two separate definitions of summer: June through September (definition 1), and July through September (definition 2). The prevalence rate of SSIs during the summer was compared with the prevalence rate during the remainder of the year by calculating prevalence rate ratios and 95% confidence intervals. RESULTS The authors identified 642 SSIs following 57,559 neurosurgical procedures (overall prevalence rate = 1.11/100 procedures); 215 occurred following 24,466 laminectomies (prevalence rate = 0.88/100 procedures), and 427 following 33,093 spinal fusions (prevalence rate = 1.29/100 procedures). Common causes of SSI were Staphylococcus aureus (n = 380; 59%), coagulase-negative staphylococci (n = 90; 14%), and Escherichia coli (n = 41; 6.4%). Poisson regression models demonstrated increases in the rates of SSI during each of the summer months for all SSIs and SSIs due to gram-positive cocci, S. aureus, and methicillin-sensitive S. aureus. Categorical analysis confirmed that the rate of SSI during the 4-month summer period was higher than the rate during the remainder of the year, regardless of which definition for summer was used (definition 1, p = 0.008; definition 2, p = 0.003). Similarly, the rates of SSI due to grampositive cocci and S. aureus were higher during the summer months than the remainder of the year regardless of which definition of summer was used. However, the rate of SSI due to gram-negative bacilli was not. CONCLUSIONS The rate of SSI following fusion or spinal laminectomy/laminoplasty was higher during the summer in this network of community hospitals. The increase appears to be related to increases in SSIs caused by gram-positive cocci and, more specifically, S. aureus. Given the nonteaching nature of these hospitals, the findings demonstrate that increases in the rate of SSI during the summer are more likely related to ecological and/or environmental factors than the July effect.

Outbreak of Bacteremia Due to Burkholderia contaminans Linked to Intravenous Fentanyl From an Institutional Compounding Pharmacy

IMPORTANCE Many health care facilities compound medications on site to fulfill local demands when customized formulations are needed, national supply is critically low, or costs for manufactured pharmaceuticals are excessive. Small, institutional compounding facilities may perform the same high-risk procedures as large distributors of compounded medications. OBJECTIVES To investigate an outbreak related to contamination of compounded sterile preparations and to determine processes to prevent future outbreaks. DESIGN, SETTING, AND PARTICIPANTS We performed an outbreak investigation of inpatients at Duke University Hospital from August 31 through September 6, 2012. The investigation included a case-control study, compounding facility inspection and environmental sampling, observation of a mock compounding demonstration, and microbiologic and molecular testing of sequestered medication. EXPOSURES Intravenous fentanyl prepared by an institutional compounding pharmacy. MAIN OUTCOMES AND MEASURES Microbiologic and molecular evidence of contamination of a compounded sterile preparation and failure of routine sterility testing. RESULTS Blood cultures of 7 patients during a 7-day period at Duke University Hospital yielded pan-susceptible Burkholderia cepacia complex bacteria. The risk factor common to all patients was receipt of continuous fentanyl infusion prepared by our institutional compounding pharmacy (odds ratio, 11.22; 95% CI, 2.09-∞; P = .01). The outbreak was terminated after sequestration of compounded fentanyl. An intensive evaluation of the compounding facility, its practice, and its procedures was completed. Investigators evaluated the clean room, collected targeted microbiologic samples within the compounding pharmacy environment, and observed a mock demonstration of compounding practice. The B cepacia complex was found in the anteroom sink drain and pH probe calibration fluid from the compounding clean room. Multiple microbiologic analyses of sequestered fentanyl initially failed. Ultimately, a batched, vacuum-assisted filtration method produced B cepacia complex from a single lot. Molecular analyses using repetitive element polymerase chain reaction and pulsed-field gel electrophoresis confirmed a clonal Burkholderia contaminans strain from patients, fentanyl, and environmental samples. CONCLUSIONS AND RELEVANCE An outbreak of B contaminans bacteremia was linked to contamination of locally compounded intravenous fentanyl. Health care facilities that house institutional compounding facilities must be vigilant in efforts to prevent, recognize, and terminate medication-related outbreaks.

Surveying the Surveillance: Surgical Site Infections Excluded by the January 2013 Updated Surveillance Definitions

The updated 2013 Centers for Disease Control and Prevention/National Healthcare Safety Network definitions for surgical site infections (SSIs) reduced the duration of prolonged surveillance from 1 year to 90 days and defined which procedure types require prolonged surveillance. Applying the updated 2013 SSI definitions to cases analyzed using the pre-2013 surveillance definitions excluded 10% of previously identified SSIs.

Comparison of Non-Intensive Care Unit (ICU) versus ICU Rates of Catheter-Associated Urinary Tract Infection in Community Hospitals

We describe and compare the epidemiology of catheter-associated urinary tract infection (CAUTI) occurring in non-intensive care unit (ICU) versus ICU wards in a network of community hospitals over a 2-year period. Overall, 72% of cases of CAUTI occurred in non-ICU patients, which indicates that this population is an important target for dedicated surveillance and prevention efforts.