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      Interventions to reduce colonisation and transmission of antimicrobial-resistant bacteria in intensive care units: an interrupted time series study and cluster randomised trial

      research-article
      , MD a , * , , PhD d , , PhD e , , PhD e , , PhD b , , PhD f , , PhD g , , PhD f , , MD c , , PhD h , , MD i , , MD j , , MD k , , MD l , , PhD m , , PhD n , , PhD o , , PhD p , , PhD q , , PhD r , , MD s , , PhD t , , , PhD b , c , , on behalf of the MOSAR WP3 Study Team
      The Lancet Infectious Diseases
      Elsevier Science, The Lancet Pub. Group

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          Summary

          Background

          Intensive care units (ICUs) are high-risk areas for transmission of antimicrobial-resistant bacteria, but no controlled study has tested the effect of rapid screening and isolation of carriers on transmission in settings with best-standard precautions. We assessed interventions to reduce colonisation and transmission of antimicrobial-resistant bacteria in European ICUs.

          Methods

          We did this study in three phases at 13 ICUs. After a 6 month baseline period (phase 1), we did an interrupted time series study of universal chlorhexidine body-washing combined with hand hygiene improvement for 6 months (phase 2), followed by a 12–15 month cluster randomised trial (phase 3). ICUs were randomly assigned by computer generated randomisation schedule to either conventional screening (chromogenic screening for meticillin-resistant Staphylococcus aureus [MRSA] and vancomycin-resistant enterococci [VRE]) or rapid screening (PCR testing for MRSA and VRE and chromogenic screening for highly resistant Enterobacteriaceae [HRE]); with contact precautions for identified carriers. The primary outcome was acquisition of resistant bacteria per 100 patient-days at risk, for which we calculated step changes and changes in trends after the introduction of each intervention. We assessed acquisition by microbiological surveillance and analysed it with a multilevel Poisson segmented regression model. We compared screening groups with a likelihood ratio test that combined step changes and changes to trend. This study is registered with ClinicalTrials.gov, number NCT00976638.

          Findings

          Seven ICUs were assigned to rapid screening and six to conventional screening. Mean hand hygiene compliance improved from 52% in phase 1 to 69% in phase 2, and 77% in phase 3. Median proportions of patients receiving chlorhexidine body-washing increased from 0% to 100% at the start of phase 2. For trends in acquisition of antimicrobial-resistant bacteria, weekly incidence rate ratio (IRR) was 0·976 (0·954–0·999) for phase 2 and 1·015 (0·998–1·032) for phase 3. For step changes, weekly IRR was 0·955 (0·676–1·348) for phase 2 and 0·634 (0·349–1·153) for phase 3. The decrease in trend in phase 2 was largely caused by changes in acquisition of MRSA (weekly IRR 0·925, 95% CI 0·890–0·962). Acquisition was lower in the conventional screening group than in the rapid screening group, but did not differ significantly (p=0·06).

          Interpretation

          Improved hand hygiene plus unit-wide chlorhexidine body-washing reduced acquisition of antimicrobial-resistant bacteria, particularly MRSA. In the context of a sustained high level of compliance to hand hygiene and chlorhexidine bathings, screening and isolation of carriers do not reduce acquisition rates of multidrug-resistant bacteria, whether or not screening is done with rapid testing or conventional testing.

          Funding

          European Commission.

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          Most cited references35

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          Targeted versus universal decolonization to prevent ICU infection.

          Both targeted decolonization and universal decolonization of patients in intensive care units (ICUs) are candidate strategies to prevent health care-associated infections, particularly those caused by methicillin-resistant Staphylococcus aureus (MRSA). We conducted a pragmatic, cluster-randomized trial. Hospitals were randomly assigned to one of three strategies, with all adult ICUs in a given hospital assigned to the same strategy. Group 1 implemented MRSA screening and isolation; group 2, targeted decolonization (i.e., screening, isolation, and decolonization of MRSA carriers); and group 3, universal decolonization (i.e., no screening, and decolonization of all patients). Proportional-hazards models were used to assess differences in infection reductions across the study groups, with clustering according to hospital. A total of 43 hospitals (including 74 ICUs and 74,256 patients during the intervention period) underwent randomization. In the intervention period versus the baseline period, modeled hazard ratios for MRSA clinical isolates were 0.92 for screening and isolation (crude rate, 3.2 vs. 3.4 isolates per 1000 days), 0.75 for targeted decolonization (3.2 vs. 4.3 isolates per 1000 days), and 0.63 for universal decolonization (2.1 vs. 3.4 isolates per 1000 days) (P=0.01 for test of all groups being equal). In the intervention versus baseline periods, hazard ratios for bloodstream infection with any pathogen in the three groups were 0.99 (crude rate, 4.1 vs. 4.2 infections per 1000 days), 0.78 (3.7 vs. 4.8 infections per 1000 days), and 0.56 (3.6 vs. 6.1 infections per 1000 days), respectively (P<0.001 for test of all groups being equal). Universal decolonization resulted in a significantly greater reduction in the rate of all bloodstream infections than either targeted decolonization or screening and isolation. One bloodstream infection was prevented per 54 patients who underwent decolonization. The reductions in rates of MRSA bloodstream infection were similar to those of all bloodstream infections, but the difference was not significant. Adverse events, which occurred in 7 patients, were mild and related to chlorhexidine. In routine ICU practice, universal decolonization was more effective than targeted decolonization or screening and isolation in reducing rates of MRSA clinical isolates and bloodstream infection from any pathogen. (Funded by the Agency for Healthcare Research and the Centers for Disease Control and Prevention; REDUCE MRSA ClinicalTrials.gov number, NCT00980980).
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            Interrupted time series designs in health technology assessment: lessons from two systematic reviews of behavior change strategies.

            In an interrupted time series (ITS) design, data are collected at multiple instances over time before and after an intervention to detect whether the intervention has an effect significantly greater than the underlying secular trend. We critically reviewed the methodological quality of ITS designs using studies included in two systematic reviews (a review of mass media interventions and a review of guideline dissemination and implementation strategies). Quality criteria were developed, and data were abstracted from each study. If the primary study analyzed the ITS design inappropriately, we reanalyzed the results by using time series regression. Twenty mass media studies and thirty-eight guideline studies were included. A total of 66% of ITS studies did not rule out the threat that another event could have occurred at the point of intervention. Thirty-three studies were reanalyzed, of which eight had significant preintervention trends. All of the studies were considered "effective" in the original report, but approximately half of the reanalyzed studies showed no statistically significant differences. We demonstrated that ITS designs are often analyzed inappropriately, underpowered, and poorly reported in implementation research. We have illustrated a framework for appraising ITS designs, and more widespread adoption of this framework would strengthen reviews that use ITS designs.
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              Effect of Daily Chlorhexidine Bathing on Hospital-Acquired Infection

              Results of previous single-center, observational studies suggest that daily bathing of patients with chlorhexidine may prevent hospital-acquired bloodstream infections and the acquisition of multidrug-resistant organisms (MDROs). We conducted a multicenter, cluster-randomized, nonblinded crossover trial to evaluate the effect of daily bathing with chlorhexidine-impregnated washcloths on the acquisition of MDROs and the incidence of hospital-acquired bloodstream infections. Nine intensive care and bone marrow transplantation units in six hospitals were randomly assigned to bathe patients either with no-rinse 2% chlorhexidine-impregnated washcloths or with nonantimicrobial washcloths for a 6-month period, exchanged for the alternate product during the subsequent 6 months. The incidence rates of acquisition of MDROs and the rates of hospital-acquired bloodstream infections were compared between the two periods by means of Poisson regression analysis. A total of 7727 patients were enrolled during the study. The overall rate of MDRO acquisition was 5.10 cases per 1000 patient-days with chlorhexidine bathing versus 6.60 cases per 1000 patient-days with nonantimicrobial washcloths (P=0.03), the equivalent of a 23% lower rate with chlorhexidine bathing. The overall rate of hospital-acquired bloodstream infections was 4.78 cases per 1000 patient-days with chlorhexidine bathing versus 6.60 cases per 1000 patient-days with nonantimicrobial washcloths (P=0.007), a 28% lower rate with chlorhexidine-impregnated washcloths. No serious skin reactions were noted during either study period. Daily bathing with chlorhexidine-impregnated washcloths significantly reduced the risks of acquisition of MDROs and development of hospital-acquired bloodstream infections. (Funded by the Centers for Disease Control and Prevention and Sage Products; ClinicalTrials.gov number, NCT00502476.).
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                Author and article information

                Journal
                Lancet Infect Dis
                Lancet Infect Dis
                The Lancet Infectious Diseases
                Elsevier Science, The Lancet Pub. Group
                1473-3099
                1474-4457
                1 January 2014
                January 2014
                : 14
                : 1
                : 31-39
                Affiliations
                [a ]Department of Intensive Care Medicine, University Medical Center Utrecht, Utrecht, Netherlands
                [b ]Department of Medical Microbiology, University Medical Center Utrecht, Utrecht, Netherlands
                [c ]Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, Netherlands
                [d ]Centre for Clinical Vaccinology and Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK
                [e ]Department of Medical Microbiology, Vaccine & Infectious Disease Institute, Antwerp University, University Hospital Antwerp, Antwerp, Belgium
                [f ]Department of Molecular Microbiology, National Medicines Institute, Warsaw, Poland
                [g ]Division of Microbiology and Infection Prevention, National Medicines Institute, Warsaw, Poland
                [h ]Service de Réanimation Médicale, Hôpital Raymond Poincaré, Garches, France
                [i ]Polyvalent Intensive Care Unit, Central Hospital of Porto, Porto, Portugal
                [j ]Infection Control Unit, Groupe Hospitalier Paris—Saint Joseph, Paris, France
                [k ]Department of Infection Control, Paul Stradins University Hospital, Riga, Latvia
                [l ]ICU and Emergency Department, Centro Hospitalar Trás-os-Montes e Alto Douro, Vila Real, Portugal
                [m ]4th Department of Internal Medicine, Athens University Medical School, Attikon General Hospital, Athens, Greece
                [n ]Clinic for Infectious Diseases and Febrile Illnesses, University Medical Centre Ljubljana, Ljubljana, Slovenia
                [o ]Shock and Trauma Unit, Intensive Care Unit, Azienda Ospedaliera S Camillo Forlanini, Rome, Italy
                [p ]Infectious Diseases Unit, Laikon General Hospital, University of Athens, Athens, Greece
                [q ]Laboratory for Respiratory Microbiology, University Clinic of Respiratory and Allergic Diseases, Golnik, Slovenia
                [r ]Pneumology Department, Hospital Clinic of Barcelona, Institut d'Investigacions Biomèdiques August Pi i Sunyer, Ciber de Enfermedades Respiratorias, University of Barcelona, Barcelona, Spain
                [s ]Intensive Care Unit, Centre Hospitalier de Luxembourg, Luxembourg, Luxembourg
                [t ]Service de réanimation médicale and INSERM U657, Institut Pasteur, APHP GH Henri Mondor, Université Paris Est-Créteil, Creteil, France
                Author notes
                [* ]Correspondence to: Lennie P G Derde, Department of Intensive Care Medicine, University Medical Center Utrecht, Universiteitsweg 100, 3584 CG Utrecht, Netherlands lderde@ 123456umcutrecht.nl
                [†]

                Equally responsible for supervising the study

                Article
                S1473-3099(13)70295-0
                10.1016/S1473-3099(13)70295-0
                3895323
                24161233
                2601fe57-5e16-4477-815f-e2c237c4e1fa
                © 2014 Derde et al. Open Access article distributed under the terms of CC BY-NC-SA

                This document may be redistributed and reused, subject to certain conditions.

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                Infectious disease & Microbiology
                Infectious disease & Microbiology

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