An Evaluation of Environmental Decontamination With Hydrogen Peroxide Vapor for Reducing the Risk of Patient Acquisition of Multidrug-Resistant Organisms

Clinical Infectious Diseases, Jan 2013

Background. Admission to a room previously occupied by a patient with certain multidrug-resistant organisms (MDROs) increases the risk of acquisition. Traditional cleaning strategies do not remove all environmental MDROs. We evaluated the environmental and clinical impact of hydrogen peroxide vapor (HPV) room disinfection. Methods. We performed a 30-month prospective cohort intervention study on 6 high-risk units in a 994-bed tertiary care hospital. Following a 12-month preintervention phase, HPV was implemented on 3 units to decontaminate the rooms of patients known to be infected or colonized with epidemiologically important MDROs, following their discharge. Monthly environmental samples for MDROs were collected on all study units for 3 preintervention and 6 intervention months. The risk of MDRO acquisition in patients admitted to rooms decontaminated using HPV was compared with rooms disinfected using standard methods. Results. The prior room occupant was known to be infected or colonized with an MDRO in 22% of 6350 admissions. Patients admitted to rooms decontaminated using HPV were 64% less likely to acquire any MDRO (incidence rate ratio [IRR], 0.36; 95% confidence interval [CI], .19–.70; P < .001) and 80% less likely to acquire VRE (IRR, 0.20; 95% CI, .08–.52; P < .001) after adjusting for other factors. The risk of acquiring Clostridium difficile, methicillin-resistant Staphylococcus aureus, and multidrug-resistant gram-negative rods individually was reduced, but not significantly. The proportion of rooms environmentally contaminated with MDROs was reduced significantly on the HPV units (relative risk, 0.65, P = .03), but not on non-HPV units. Conclusions. HPV decontamination reduced environmental contamination and the risk of acquiring MDROs compared with standard cleaning protocols.

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An Evaluation of Environmental Decontamination With Hydrogen Peroxide Vapor for Reducing the Risk of Patient Acquisition of Multidrug-Resistant Organisms

Catherine L. Passaretti 0 1 2 3 Jonathan A. Otter 2 7 Nicholas G. Reich 2 5 6 Jessica Myers 2 6 John Shepard 2 3 Tracy Ross 2 4 Karen C. Carroll 2 4 Pam Lipsett 2 8 Trish M. Perl () 1 2 3 6 Patients shed gens including 2 0 Division of Infectious Diseases, Department of Medicine, Carolinas Medical Center , Charlotte, North Carolina 1 Department of Hospital Epidemiology and Infection Control, The Johns Hopkins Hospital , Baltimore, Maryland 2 Received 21 May 2012; accepted 14 August 2012; electronically published 5 October 2012. Presented in part: 48th Annual Interscience Conference on Antimicrobial Agents and Chemotherapy (25-28 October 2008) and the Infectious Diseases Society of America (IDSA) , Washington, DC, 2008. Abstract K4124b. Wolfe Street, 327 A Billings, Baltimore, MD 21287 3 Division of Infectious Diseases, Department of Medicine, Johns Hopkins University School of Medicine 4 Department of Pathology 5 Division of Biostatistics and Epidemiology, School of Public Health and Health Sciences, University of Massachusetts , Amherst 6 Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins University , Baltimore, Maryland 7 Bioquell Inc , Horsham, Pennsylvania 8 Department of Surgery, Johns Hopkins University School of Medicine , Baltimore, Maryland (See the Editorial Commentary by McDonald and Arduino, on pages 36-9.) Background. Admission to a room previously occupied by a patient with certain multidrug-resistant organisms (MDROs) increases the risk of acquisition. Traditional cleaning strategies do not remove all environmental MDROs. We evaluated the environmental and clinical impact of hydrogen peroxide vapor (HPV) room disinfection. Methods. We performed a 30-month prospective cohort intervention study on 6 high-risk units in a 994-bed tertiary care hospital. Following a 12-month preintervention phase, HPV was implemented on 3 units to decontaminate the rooms of patients known to be infected or colonized with epidemiologically important MDROs, following their discharge. Monthly environmental samples for MDROs were collected on all study units for 3 preintervention and 6 intervention months. The risk of MDRO acquisition in patients admitted to rooms decontaminated using HPV was compared with rooms disinfected using standard methods. Results. The prior room occupant was known to be infected or colonized with an MDRO in 22% of 6350 admissions. Patients admitted to rooms decontaminated using HPV were 64% less likely to acquire any MDRO (incidence rate ratio [IRR], 0.36; 95% confidence interval [CI], .19-.70; P < .001) and 80% less likely to acquire VRE (IRR, 0.20; 95% CI, .08-.52; P < .001) after adjusting for other factors. The risk of acquiring Clostridium difficile, methicillinresistant Staphylococcus aureus, and multidrug-resistant gram-negative rods individually was reduced, but not significantly. The proportion of rooms environmentally contaminated with MDROs was reduced significantly on the HPV units (relative risk, 0.65, P = .03), but not on non-HPV units. Conclusions. HPV decontamination reduced environmental contamination and the risk of acquiring MDROs compared with standard cleaning protocols. - epidemiologically important patho vancomycin-resistant enterococci (VRE), Clostridium difficile, methicillin-resistant Staphylococcus aureus (MRSA), and Acinetobacter baumannii into their surrounding environment. These organisms remain viable on inanimate objects for days to months, and can be transferred from the environment to healthcare workers hands, providing a mode of transmission to other patients [13]. Contamination of hospital rooms and equipment can persist despite cleaning and disinfection [1, 4, 5]. Consequently, admission to a room previously occupied by a patient known to be colonized or infected with VRE, C. difficile, MRSA, and/or A. baumannii increases the chances of acquiring these pathogens [1, 610]. In light of these findings, terminal disinfection following patient discharge should be improved [11]. Educational campaigns, including the use of fluorescent or other markers, improve compliance with cleaning regimens and reduce environmental contamination, and there is evidence this reduces the acquisition of select pathogens [1215]. However, even aggressive cleaning protocols may not be sufficient to remove contamination with some pathogens [13, 16] and the impact of educational campaigns is difficult to sustain [5, 1114, 16]. Another approach is the use of automated room disinfection systems including those based on hydrogen peroxide or ultraviolet radiation. Automated systems do not rely on the operator to ensure all surfaces are disinfected and adequate contact time is achieved [11]. However, automated methods must be applied in addition to standard cleaning, require areas to be temporarily vacated of patients and staff ( potentially leading to delays in bed availability), and incur additional expense. Hydrogen peroxide vapor (HPV) decontamination is a sporicidal vapor-phase method that inactivates a range of hospital pathogens in vitro [17] and in situ including surfaces that are difficult to clean (eg, keyboards) [4, 1820]. HPV is used to eliminate environmental reservoirs contributing to multidrug-resistant organism (MDRO) outbreaks [2123], and regular use of HPV to decontaminate rooms of patients with MDROs has significantly reduced the incidence of C. difficile infection and VRE in some settings [19, 24]. However, these investigations were observational and subject to confounding factors, such as impact of other infection control interventions and lack of intervention control group [25, 26]. Hence, we specifically evaluated the impact of adjunctive use of HPV following standard cleaning on patient acquisition of MDROs in rooms treated with HPV vs those where HPV was not used. MATERIALS AND METHODS Setting The Johns Hopkins Hospital is a 994-bed tertiary referral center. We collected data for 12 months prior to the intervention ( January 2007 through December 2007) and subsequently for an 18-month intervention ( January 2008 through June 2009). Six high-risk units were included. HPV decontamination (Bioquell, Horsham, Pennsylvania) was performed after routine cleaning and disinfection when possible in 2 single-occupancy intensive care units (ICUs; 19-bed surgical and 22-bed neurosurgical) and a high-risk 30-bed surgical unit (73% single occupancy, 27% double occupancy) during the intervention phase. Standard cleaning and disinfection processes continued on the other 3 standard cleaning units (16-bed medical, 18-bed cardiothoracic surgery, and 20-bed surgical oncology ICUs) throughout all study periods. No other cleaning interventions occurred during the study. Of note, 2 of the standard cleaning units were also being studied for the impact of daily chlorhexidine bathing during part of the study [27]. All patients admitted to these units during the chlorhexidine interventions were excluded from the analysis. Policies and Practices MDRO Surveillance/Isolation On all study units, nurses collect perirectal swabs for VRE and nasal swabs for MRSA on admission and weekly in patients not known to be colonized. Rectal surveillance cultures were plated directly on Bile Esculin Azide agar with 6 mg/mL vancomycin (BD Diagnostics, Sparks, Maryland) for detection of VRE as described previously [28]. Anterior nares surveillance swabs were plated directly on MRSASelect agar (Bio-Rad Laboratories, Hercules, California) and MRSA was confirmed using standard methods. Compliance with surveillance was monitored, and varied among units. No screening was performed for multidrug-resistant gram-negative rods (MDRGNR, defined as any gram-negative rod susceptible to no more than 1 class of antimicrobial agents tested). Clostridium difficile testing is only performed when clinically indicated using previously described methods [29]. When patients are identified as colonized or infected with MRSA, VRE, C. difficile, and MDR-GNR, they are placed on contact precautions. Patients known to be colonized with MRSA or VRE are flagged in the medical record. Standard Cleaning Practices Floors and surfaces are cleaned/disinfected daily and after discharge using a quaternary ammonium compound (QAC; 3M, St Paul, Minnesota). The QAC is applied using WetTask wipes (Kimberly-Clark, Roswell, Georgia) for surfaces, where the cleaner/disinfectant is poured into the WetTask bucket to impregnate disposable wipes, and a mop and bucket for floors. A hydrogen peroxidecontaining liquid cleaner/disinfectant (Oxivir, Johnson Diversity, Sturtevant, Wisconsin) is used to clean the rooms of patients with C. difficile. Study personnel periodically monitored compliance with cleaning and disinfection policies by observing housekeepers. Environmental Sampling Monthly sampling was performed in all study units over the last 3 months of the preintervention phase and the first 6 months of the intervention phase. Premoistened swabs (BBL CultureSwab with Liquid Stuart, BD Diagnostics) were used to sample standard environmental surfaces and equipment for MRSA, VRE, and MDR-GNR. Cultured sites on each unit included 1 composite swab from 25-cm2 areas of the bedrail, computer keyboard, and electronic monitoring equipment in each patient room and separate samples from 3 communal surfaces (telephone, computer keyboard, and keypad of a drug administration station). Following swab collection, premoistened cellulose sponges (Solar Biologicals, Ogdensburg, New York) were used to culture the same surfaces for C. difficile and processed in our laboratory using previously described methods [19]. All swabs were incubated overnight in brainheart infusion broth and then plated onto selective media for MRSA, VRE, and MDR-GNR, then cultured and identified using standard microbiologic methods. After each set of cultures, results were fed back to unit staff. Definition of Acquisition Patient data relating to MDROs were obtained through analysis of electronic patient records (Theradoc, Salt Lake City, Utah). All patients without a history of a given MDRO in our records and with a room stay of >48 hours were considered at risk for acquisition of that MDRO and included in the analysis. Acquisitions were defined as identification of an MDRO after 48 hours of admission in a patient with no known prior history of that organism. Each patient admitted to any of the 6 evaluation units during the study period was assigned to one of 3 cohorts, regardless of study unit or phase: (1) MDRO-standard, for patients admitted to a room where the prior room occupant had an MDRO and the room was cleaned and disinfected using standard methods; (2) MDROHPV, for patients admitted to a room where the prior room occupant had an MDRO and the room was cleaned and disinfected using standard methods followed by HPV decontamination; and (3) No MDRO-standard, for patients admitted to a room where the prior room occupant was not known to have an MDRO and the room was cleaned and disinfected using standard methods (see Figure 1). HPV Decontamination The surgical ICU was vacated and the entire unit, including common areas, decontaminated using HPV at the start of the intervention. Each room on the other 2 HPV units was decontaminated individually using HPV as patients were discharged at the start of the intervention. During the intervention, when possible, the rooms of patients known to be colonized or infected with MDROs were decontaminated using HPV after patient discharge and before the next admission on the 3 HPV units. Equipment from other patient rooms and equipment shared by multiple patients was commonly placed in rooms during decontamination. HPV decontamination was conducted by dedicated personnel as described previously [19] following standard cleaning/disinfection. HPV decontamination required approximately 1.53 hours. Each cycle was validated using one 6-log Geobacillus stearothermophilus biological indicator (Apex Laboratories, Sanford, North Carolina) that were placed in the corner of the room and cultured according to the manufacturers instructions after HPV exposure. The hours of operation of the HPV decontamination service were 8 AM8 PM, Monday to Friday. Data Management and Statistical Methods All data were entered into an Excel (Microsoft Corporation, Redmond, Washington) database. Acquisition rates of MDROs (both separately and combined) were compared across the 3 cohorts. Raw incidence rates in each cohort were measured as the number of MDRO acquisitions per 1000 patient-days. Incidence rate ratios (IRRs) were estimated by Poisson generalized linear models, adjusting for hospital unit, age, mortality risk score, human immunodeficiency virus status, end-stage renal disease status, compliance with MDRO surveillance procedures, and calendar time. The analysis was performed using acquisitions of each of the 4 MDROs separately as the outcome and once using acquisition of any MDRO as the outcome. Table 1. Demographic Characteristics of Study Patients No MDROStandard MDROStandard Abbreviations: ESRD, end-stage renal disease; HIV, human immunodeficiency virus; HPV, hydrogen peroxide vapor; MDRO, multidrug-resistant organism. a Five rooms on non-HPV units were decontaminated for infection prevention and control reasons during the study period. Patients admitted to these rooms were included in the MDRO-HPV cohort. b These rooms were not able to be decontaminated using HPV for logistical reasons so were cleaned and disinfected using standard methods. Patients admitted to these rooms were included in the MDRO-standard cohort. Statisticians who had not been involved in the clinical activities of the study performed the analysis. The Sweave package [30] in R, version 12.1 [31] was used. The evaluation was approved by the Institutional Review Board of the Johns Hopkins University. Overall, 8813 room occupations of 48 hours were included in the study (Figure 1); 1777 (20.2%) with a known history of an MDRO and 686 (7.8%) involved in a chlorhexidine study were excluded. Following exclusions, 6350 (72.0%) room occupations by 5378 patients were at risk of nosocomial MDRO acquisition (Figure 1). Patients at risk of acquiring 1 MDRO were not necessarily at risk of acquiring another MDRO, hence: 6936, 7514, 7928, and 8117 room occupations VRE Acquisitions, No. Patient-Days, No. Acquired, % Crude IR per 1000 Patient-Days Adj IRRa were at risk of acquiring VRE, MRSA, C. difficile, and MDRGNR, respectively. Impact on MDRO Acquisition in Subsequent Room Occupants Throughout the evaluation period, 497 of 6350 (7.8%) room occupations by patients without a history of an MDRO resulted in the acquisition of at least 1 MDRO; 333 of 6936 (4.8%) acquired VRE, 121 of 7514 (1.6%) acquired MRSA, 130 of 7928 (1.6%) acquired C. difficile, and 111 of 8117 (1.4%) acquired an MDR-GNR. The patient demographics of the 3 cohorts were similar (Table 1). Patients admitted to rooms decontaminated using HPV (MDRO-HPV cohort) were significantly less likely to acquire any MDRO when compared with patients admitted to rooms cleaned and disinfected using standard methods (MDRO-standard cohort) before and after adjusting for possible confounders (adjusted IRR, 0.36; 95% confidence interval [CI], .19.70; Table 2). The significant reduction in MDRO acquisitions was mainly driven by the reduced incidence of VRE acquisition, which was approximately 5 times less likely in the MDROHPV cohort before and after adjusting for possible confounders (adjusted IRR, 0.20; 95% CI, .08.52; Table 3). The risk of acquisition was lower in the MDRO-HPV cohort than in the MDRO-standard cohort for MRSA, MDRGNR, and C. difficile, although these differences were not statistically significant (Table 2). Restricting the analysis for VRE and MRSA to patients with an admission surveillance culture indicated that the differences in rates between the cohorts were similar to the full analysis; MDRO-standard vs MDROHPV for VRE was the only significant difference (IRR, 0.19; 95% CI, .05.53; P < .001; data not shown). Reduced acquisition associated with HPV disinfection occurred independently of changes in rates on each unit and over time (Table 3). There were no significant changes in the rates of acquisition in the MDRO-standard and No MDRO-standard cohorts Table 3. Adjusted Incidence Rate Ratioa of Vancomycin Mort Riskb 2 Abbreviations: ESRD, end-stage renal disease; HIV, human immunodeficiency virus; HPV, hydrogen peroxide vapor; IRR, incidence rate ratio; No MDRO-standard, patients admitted to a room when the prior room occupant was not known to have an MDRO and the room was cleaned using standard methods; VRE-HPV, patients admitted to a room when the prior room occupant had VRE and the room was decontaminated using HPV; Other MDRO-HPV, patients admitted to a room when the prior room occupant had Clostridium difficile, multidrug-resistant gram-negative rods, or methicillinresistant Staphylococcus aureus and the room was decontaminated using HPV; VRE, vancomycin-resistant enterococci. a Model was adjusted to take into account potential clustering within units and also included quarterly indicators; data not included in table. Exposure was compared to MDRO-standard for VRE. bMort Risk, risk of mortality as calculated by 3M APR-DRG software. comparing the preintervention and intervention study phases on the HPV and non-HPV units (Table 4). particular, rooms contaminated with multiple MDROs (RR, 0.16; P < .01), MDROs cultured from a room that differed from the room occupants known MDRO (RR, 0.37; P = .01), and MDROs cultured from empty rooms (RR, 0.31; P = .05) were less frequent on HPV units during the intervention phase (Table 5). HPV Decontamination Of the 8813 discharges during the entire study period, 1872 rooms housed patients with MDROs on HPV units during the intervention phase; 1334 (71.3%) of these were decontaminated using HPV, comprising 91.7% single-occupancy rooms. Two-thirds (n = 355) of the missed decontaminations occurred during hours when the HPV service was not available and 4.1% (n = 22) due to an urgent admission. Of the rooms decontaminated using HPV, 62.1%, 38.4%, 19.1%, and 10.5% had previously housed patients with VRE, MRSA, MDRGNR, and C. difficile, respectively. There was no significant difference in the type of MDRO in HPV compared with missed decontaminations (data not shown). One brand of paint used on the walls of one of the HPV units showed some incompatibility with the process; once this was replaced, there were no reports of damage to materials or equipment. No health and safety incidents were associated with HPV during the study. All biological indicators were inactivated. The technology was well accepted by unit staff (data not shown). DISCUSSION Environmental Findings Overall, 218 (21.0%) of the 1039 patient rooms sampled were contaminated with 1 MDRO. The overall proportion of rooms contaminated with MDROs reduced significantly on the HPV units during the intervention phase, but not on the non-HPV units (relative risk [RR], 0.65; P = .03; Table 5). In The role of environmental contamination in the transmission of healthcare-acquired pathogens is increasingly recognized [13, 7]. However, the best interventions to prevent transmission remain controversial because data on clinical outcomes are limited. We found that HPV decontamination decreased environmental contamination, particularly of rooms Multidrug Resistant Organism Acquisition by Cohort, Study Phase, and Unit MDRO-standard No MDRO-standard Non-HPV units Non-HPV units Study Phase Preintervention Intervention Preintervention Intervention Preintervention Intervention Preintervention Intervention IR/1000 Patient-Days Total No. of rooms sampled Occupied rooms on precautions Rooms contaminated with any MDRO Multiple MDROs VRE MDR-GNR MRSA C. difficile MDRO matches the current room occupant MDRO differs from the current room occupant Contaminated empty roomsa Contaminated communal sites Preintervention Phase 170 49 (36.8) HPV Units Preintervention Phase RR Non-HPV Units contaminated with multiple MDROs, which may have survived from previous room occupants [4] and of empty rooms. Most importantly, we found that HPV used as an adjunct to a standard environmental cleaning and disinfection program reduced the risk of patient acquisition of MDROs by 64% in a large number of patients in busy, high-risk units. VRE, an organism with a known predilection for the environment [1, 6, 7], is endemic in our institution and was the organism most commonly isolated from the environment and most commonly acquired. Not surprisingly, VRE was the MDRO acquisition most markedly reduced by adjunctive HPV use in our institution. Comparison of the rates between the cohorts indicates that 28 MDRO transmissions were prevented by HPV on the 3 HPV units over the 18 months. Recent findings that admission to a room where the prior room occupant was infected or colonized with an MDRO increases the risk of subsequent room occupant acquiring that MDRO provides compelling evidence that contaminated surfaces contribute to transmission [1, 69, 15]. Our findings extend these earlier studies, by showing that the risk from the prior room occupant is mitigated by effectively removing the environmental reservoir through the use of HPV decontamination [4, 19, 22]. Similarly, a recent study provides evidence that efforts to improve the efficacy of conventional cleaning and disinfection mitigated the increased risk of acquisition from an MRSA-colonized prior room occupant, but not from a VRE-colonized prior room occupant [15]. A surprising finding of our study was that HPV may protect patients even when the prior room occupant was not known to be colonized with an MDRO (ie, acquisition rates were lower in the MDRO-HPV cohort than in the No MDRO-standard cohort). Whether this was the result of unidentified MDRO carriers, residual contamination from previous room occupants, or contamination of healthcare workers hands is not known [3, 6, 32]. Further work is required to explore this association. MRSA, MDR-GNR, and C. difficile acquisitions were not independently reduced when HPV was used. We attribute these findings to the relatively low incidence of MDRO acquisition in a setting of enhanced focus on infection prevention and control strategies, including improved cleaning and disinfection of the environment [69, 15]. Therefore, whether HPV decontamination mitigates risk of acquisition conferred by a prior room occupant infected or colonized with MRSA, C. difficile, and MDR-GNRs should be investigated in more detail. Studies in endemic settings with a high incidence of acquisition of these pathogens or in outbreak settings will be helpful in addressing the impact of HPV on organisms besides VRE. Regular use of HPV presents several practical challenges, including the need to vacate areas for the duration of the decontamination and the need to seal air vents and doors. Importantly, the HPV service did not impact the day-to-day work of the staff. There were no safety, equipment, or ongoing material compatibility problems reported. We were able to decontaminate 71% of the rooms that met the criteria for HPV decontamination using 2 trained individuals with 2 suites of equipment from 8 PM to 8 AM 5 days per week. Only a small proportion (4.1%) of rooms that were vacated by patients with MDROs were not decontaminated owing to an urgent need to admit the next patient, which concurs with other findings [33]. Our study has several limitations. First, this is a single-institution study, so results may not be generalizable to other institutions that may have a different MDRO profile or lower acquisition rates. Second, neither rooms nor units were randomly assigned the intervention, which may have introduced bias. Third, as with many infection prevention studies, there were multiple infection prevention initiatives ongoing during the study period. In particular, another intervention, chlorhexidine daily bathing of patients, was introduced on some non-HPV units. While we attempted to control for this intervention by removing those patients receiving chlorhexidine baths from the analysis and this likely biased our results towards the null, we could not completely remove all impact. Fourth, while our analysis attempted to adjust for compliance with VRE and MRSA surveillance cultures, rates of compliance varied and improved during the study period in all units, potentially impacting our acquisition rates. Fifth, our environmental sampling methods did not quantify the contamination level, but the use of broth enrichment would have improved the sensitivity of the method [4]. Finally, given that some rooms were missed (ie, not decontaminated despite prior occupant known to have an MDRO) and the low prevalence of acquisition (especially for MDROs besides VRE), detecting changes in incidence was difficult. In settings with lower acquisition rates, a larger, multicenter trial would be necessary to show a significant impact. In summary, HPV decontamination used as an adjunct to standard cleaning and disinfection reduced the risk of MDRO acquisition among high-risk patients when patients are admitted to a room previously occupied by a patient infected or colonized with an MDRO. These findings suggest that HPV should be considered for decontamination of MDRO patient rooms. Given the rising issue of resistant gram-negative organisms, the continued impact of other MDROs and a patient population that is increasingly susceptible to infection, strategies to optimally clean and disinfect the environment are essential. The results of our study, one of the few to evaluate not just environmental contamination but also patient outcomes, suggest that HPV in addition to a thorough infection prevention program should be implemented in high-risk environments to maximize patient safety. Acknowledgments. We thank K. Alex Shangraw, who helped with data management; the nurses and unit leadership and the personnel who facilitated the study, including Elaine Nowakowski, Wendy Ziai, Karen Earsing, Gail Biba, and Lisa Purdy; and Nick Adams, James Salkeld, Mike Duclos, and the other Bioquell personnel who facilitated the study. Author contributions. C. L. P., J. A. O., N. G. R., J. M., J. S., T. R., K. C. C., P. L., and T. M. P. contributed to the study design, analysis, interpretation, and drafting the of manuscript. C. L. P., J. A. O., J. S., and T. R. performed data collection. J. M. and N. G. R. performed statistical analysis. Disclaimer. Bioquell contributed to the study design, collection of data, and the writing of the report. Although Bioquell contributed to the writing of the manuscript, the writing and analysis was done by employees or students at Johns Hopkins University. All statistical analysis was done by the Johns Hopkins employees and Bioquell personnel were not involved. Financial support. HPV decontamination services were provided by Bioquell without charge for the duration of the study. Potential conflicts of interest. J. A. O. is employed by Bioquell. All other authors report no potential conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.


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Catherine L. Passaretti, Jonathan A. Otter, Nicholas G. Reich, Jessica Myers, John Shepard, Tracy Ross, Karen C. Carroll, Pam Lipsett, Trish M. Perl. An Evaluation of Environmental Decontamination With Hydrogen Peroxide Vapor for Reducing the Risk of Patient Acquisition of Multidrug-Resistant Organisms, Clinical Infectious Diseases, 2013, 27-35, DOI: 10.1093/cid/cis839