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Does improving surface cleaning and disinfection reduce health care-associated infections?

2013; Elsevier BV; Volume: 41; Issue: 5 Linguagem: Inglês

10.1016/j.ajic.2012.12.010

1527-3296

Curtis J. Donskey,

Infection Control and Ventilation

Contaminated environmental surfaces provide an important potential source for transmission of health care-associated pathogens. In recent years, a variety of interventions have been shown to be effective in improving cleaning and disinfection of surfaces. This review examines the evidence that improving environmental disinfection can reduce health care-associated infections. Contaminated environmental surfaces provide an important potential source for transmission of health care-associated pathogens. In recent years, a variety of interventions have been shown to be effective in improving cleaning and disinfection of surfaces. This review examines the evidence that improving environmental disinfection can reduce health care-associated infections. Contaminated environmental surfaces provide an important potential source for transmission of many health care-associated pathogens.1Weber D.J. Rutala W.A. Miller M.B. Huslage K. Sickbert-Bennett E. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.Am J Infect Control. 2010; 38: S25-S33Abstract Full Text Full Text PDF PubMed Scopus (539) Google Scholar, 2Boyce J.M. Environmental contamination makes an important contribution to hospital infection.J Hosp Infect. 2007; 65: 50-54Abstract Full Text PDF PubMed Scopus (504) Google Scholar, 3Rutala W.A. Weber D.J. The role of the environment in transmission of Clostridium difficile infection in health care facilities.Infect Control Hosp Epidemiol. 2011; 32: 207-209Crossref PubMed Scopus (30) Google Scholar, 4Hota B. Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection?.Clin Infect Dis. 2004; 39: 1182-1189Crossref PubMed Scopus (477) Google Scholar, 5Dancer S.J. Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning.Lancet Infect Dis. 2008; 8: 101-113Abstract Full Text Full Text PDF PubMed Scopus (357) Google Scholar, 6Otter J.A. Yezli S. French G.L. The role played by contaminated surfaces in the transmission of nosocomial pathogens.Infect Control Hosp Epidemiol. 2011; 32: 687-699Crossref PubMed Scopus (426) Google Scholar These include Clostridium difficile, methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), gram-negative bacilli (eg, Acinetobacter baumannii and Pseudomonas aeruginosa), and norovirus.1Weber D.J. Rutala W.A. Miller M.B. Huslage K. Sickbert-Bennett E. Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.Am J Infect Control. 2010; 38: S25-S33Abstract Full Text Full Text PDF PubMed Scopus (539) Google Scholar, 2Boyce J.M. Environmental contamination makes an important contribution to hospital infection.J Hosp Infect. 2007; 65: 50-54Abstract Full Text PDF PubMed Scopus (504) Google Scholar, 3Rutala W.A. Weber D.J. The role of the environment in transmission of Clostridium difficile infection in health care facilities.Infect Control Hosp Epidemiol. 2011; 32: 207-209Crossref PubMed Scopus (30) Google Scholar, 4Hota B. Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection?.Clin Infect Dis. 2004; 39: 1182-1189Crossref PubMed Scopus (477) Google Scholar, 5Dancer S.J. Importance of the environment in meticillin-resistant Staphylococcus aureus acquisition: the case for hospital cleaning.Lancet Infect Dis. 2008; 8: 101-113Abstract Full Text Full Text PDF PubMed Scopus (357) Google Scholar, 6Otter J.A. Yezli S. French G.L. The role played by contaminated surfaces in the transmission of nosocomial pathogens.Infect Control Hosp Epidemiol. 2011; 32: 687-699Crossref PubMed Scopus (426) Google Scholar In recent years, a number of studies have demonstrated that environmental cleaning interventions can improve the thoroughness of cleaning and reduce contamination on surfaces.7Eckstein B.C. Adams D.A. Eckstein E.C. Rao A. Sethi A.K. Yadavalli G.K. Donskey C.J. Reduction of Clostridium Difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.BMC Infect Dis. 2007; 7: 61Crossref PubMed Scopus (200) Google Scholar, 8Carling P.C. Briggs J.L. Perkins J. Highlander D. Improved cleaning of patient rooms using a new targeting method.Clin Infect Dis. 2006; 42: 385-388Crossref PubMed Scopus (130) Google Scholar, 9Carling P.C. Parry M.F. Von Beheren S.M. Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.Infect Control Hosp Epidemiol. 2008; 29: 1-7Crossref PubMed Scopus (172) Google Scholar, 10Dumigan D.G. Boyce J.M. Havill N.L. Golebiewski M. Balogun O. Rizvani R. Who is really caring for your environment of care? Developing standardized cleaning procedures and effective monitoring techniques.Am J Infect Control. 2010; 38: 387-392Abstract Full Text Full Text PDF PubMed Scopus (30) Google Scholar, 11Hayden M.K. Bonten M.J. Blom D.W. Lyle E.A. van de Vijver D.A. Weinstein R.A. Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures.Clin Infect Dis. 2006; 42: 1552-1560Crossref PubMed Scopus (315) Google Scholar This review examines the evidence that such improvements in environmental disinfection may prevent transmission and reduce health care-associated infections. The review was not conducted as a systematic review, but the MEDLINE electronic database was searched using broad search terminologies and recent review articles, and their references were searched. Studies were included only if the impact of the intervention on rates of pathogen acquisition and/or infection was assessed and environmental cleaning and disinfection was the primary focus of an intervention (ie, Multifaceted infection control interventions were not included unless environmental disinfection was a central component of the intervention).Environmental disinfection strategiesFigure 1 provides an overview of common routes of transmission of health care-associated pathogens. Patients colonized or infected with health care-associated pathogens shed organisms onto their skin, clothing, bedding, and nearby environmental surfaces.12Donskey C.J. Preventing transmission of Clostridium difficile: is the answer blowing in the wind?.Clin Infect Dis. 2010; 50: 1458-1461Crossref PubMed Scopus (24) Google Scholar In addition to surfaces in rooms, portable equipment and other fomites often become contaminated after contact with patients or contaminated surfaces.12Donskey C.J. Preventing transmission of Clostridium difficile: is the answer blowing in the wind?.Clin Infect Dis. 2010; 50: 1458-1461Crossref PubMed Scopus (24) Google Scholar, 13Brooks S.E. Veal R.O. Kramer M. Dore L. Schupf N. Adachi M. Reduction in the incidence of Clostridium difficile-associated diarrhea in an acute care hospital and a skilled nursing facility following replacement of electronic thermometers with single-use disposables.Infect Control Hosp Epidemiol. 1992; 13: 98-103Crossref PubMed Scopus (116) Google Scholar, 14Jernigan J.A. Siegman-Igra Y. Guerrant R.C. Farr B.M. A randomized crossover study of disposable thermometers for prevention of Clostridium difficile and other nosocomial infections.Infect Control Hosp Epidemiol. 1998; 19: 494-499Crossref PubMed Scopus (60) Google Scholar Susceptible patients may acquire pathogens through direct contact with contaminated surfaces or equipment or via the hands of health care personnel that have become contaminated after contact with patients or environmental surfaces.15Hayden M.K. Blom D.W. Lyle E.A. Moore C.G. Weinstein R.A. Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant enterococcus or the colonized patients’ environment.Infect Control Hosp Epidemiol. 2008; 29: 149-154Crossref PubMed Scopus (223) Google Scholar, 16Stiefel U. Cadnum J.L. Eckstein B.C. Guerrero D.M. Tima M.A. Donskey C.J. Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients.Infect Control Hosp Epidemiol. 2011; 32: 185-187Crossref PubMed Scopus (120) Google Scholar, 17Guerrero D.M. Nerandzic M.M. Jury L.A. Jinno S. Chang S. Donskey C.J. Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.Am J Infect Control. 2012; 40: 556-558Abstract Full Text Full Text PDF PubMed Scopus (77) Google Scholar For many pathogens, a majority of patients acquiring colonization do not develop clinically apparent infections. These asymptomatic carriers may shed pathogens into the environment and contribute to transmission.18Donskey C.J. Chowdhry T.K. Hecker M.T. Hoyen C.K. Hanrahan J.A. Hujer A.M. et al.Effect of antibiotic therapy on the density of vancomycin-resistant enterococci in the stool of colonized patients.N Engl J Med. 2000; 343: 1925-1932Crossref PubMed Scopus (525) Google Scholar, 19Riggs M.M. Sethi A.K. Zabarsky T.F. Eckstein E.C. Jump R.L. Donskey C.J. Asymptomatic carriers are a potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents.Clin Infect Dis. 2007; 45: 992-998Crossref PubMed Scopus (423) Google ScholarBased on these routes of transmission, Figure 1 highlights 4 potential environmental disinfection strategies to reduce transmission. First, improving cleaning and disinfection of rooms of patients known to carry health care-associated pathogens after discharge (ie, terminal cleaning) will reduce the risk that patients subsequently admitted to the same room will acquire pathogens from contaminated surfaces.20Shaughnessy M.K. Micielli R.L. DePestel D.D. Arndt J. Strachan C.L. Welch K.B. et al.Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.Infect Control Hosp Epidemiol. 2011; 32: 201-206Crossref PubMed Scopus (230) Google Scholar Second, daily disinfection of high-touch surfaces in isolation rooms may be useful to reduce the risk of contamination of the hands of health care personnel providing care for the patients.21Kundrapu S. Sunkesula V. Jury L.A. Sitzlar B.M. Donskey C.J. Daily disinfection of high-touch surfaces in isolation rooms to reduce contamination of healthcare personnel' hands.Infect Control Hosp Epidemiol. 2012; 33: 1039-1042Crossref PubMed Scopus (72) Google Scholar, 22Wilson A.P. Smyth D. Moore G. Singleton J. Jackson R. Gant V. et al.The impact of enhanced cleaning within the intensive care unit on contamination of the near-patient environment with hospital pathogens: a randomized crossover study in critical care units in two hospitals.Crit Care Med. 2011; 39: 651-658Crossref PubMed Scopus (84) Google Scholar This strategy is analogous to daily disinfection of the skin of patients as a means of source control to reduce transmission of MRSA and VRE.23Vernon M.O. Hayden M.K. Trick W.E. Hayes R.A. Blom D.W. Weinstein R.A. Chlorhexidine gluconate to cleanse patients in a medical intensive care unit: the effectiveness of source control to reduce the bioburden of vancomycin-resistant enterococci.Arch Int Med. 2006; 166: 306-312Crossref PubMed Scopus (236) Google Scholar, 24Climo M.W. Sepkowitz K.A. Zuccotti G. Fraser V.J. Warren D.K. Perl T.M. et al.The effect of daily bathing with chlorhexidine on the acquisition of methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus, and healthcare-associated bloodstream infections: results of a quasi-experimental multicenter trial.Crit Care Med. 2009; 37: 1858-1865Crossref PubMed Scopus (248) Google Scholar Third, disinfection of portable equipment between patients or use of disposable equipment in isolation rooms will reduce the risk for transmission.13Brooks S.E. Veal R.O. Kramer M. Dore L. Schupf N. Adachi M. Reduction in the incidence of Clostridium difficile-associated diarrhea in an acute care hospital and a skilled nursing facility following replacement of electronic thermometers with single-use disposables.Infect Control Hosp Epidemiol. 1992; 13: 98-103Crossref PubMed Scopus (116) Google Scholar, 14Jernigan J.A. Siegman-Igra Y. Guerrant R.C. Farr B.M. A randomized crossover study of disposable thermometers for prevention of Clostridium difficile and other nosocomial infections.Infect Control Hosp Epidemiol. 1998; 19: 494-499Crossref PubMed Scopus (60) Google Scholar Finally, rather than focusing only on isolation rooms, efforts to improve cleaning and disinfection of all rooms may be beneficial if there is a concern that many carriers are not identified or are identified only after long delays.19Riggs M.M. Sethi A.K. Zabarsky T.F. Eckstein E.C. Jump R.L. Donskey C.J. Asymptomatic carriers are a potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents.Clin Infect Dis. 2007; 45: 992-998Crossref PubMed Scopus (423) Google Scholar, 25Orenstein R. Aronhalt K.C. McManus Jr., J.E. Fedraw L.A. A targeted strategy to wipe out.Clostridium difficile. Infect Control Hosp Epidemiol. 2011; 32: 1137-1139Crossref PubMed Scopus (60) Google ScholarMany environmental disinfection interventions reported in the literature have focused primarily on improving terminal cleaning of isolation rooms. It is plausible that more comprehensive interventions that include daily disinfection of high-touch surfaces, disinfection of portable equipment, and improved cleaning of nonisolation rooms might be most effective. However, studies have rarely compared the effectiveness of different disinfection strategies or combinations of strategies. When available, information on the different strategies included in disinfection interventions is included in this review.Environmental disinfection interventionsOverviewEnvironmental disinfection interventions range from simple interventions involving substitution of one disinfectant product for another to intensive efforts to improve cleaning performance through education plus monitoring and feedback to housekeepers. In this regard, disinfection interventions are analogous to antimicrobial stewardship interventions, which range from formulary substitutions to formal stewardship programs that include monitoring and feedback. For the purposes of this review, disinfection interventions were divided into 3 categories: (1) disinfectant product substitutions (ie, Although efforts may be undertaken to improve cleaning, the primary intervention is a change to a disinfectant with improved effectiveness against a particular pathogen), (2) interventions to improve effectiveness of cleaning and disinfection practices, and (3) use of automated disinfection technologies. In practice, disinfectant product substitutions have most often involved substitution of sporicidal for nonsporicidal products as a control strategy for C difficile. Interventions to improve effectiveness of cleaning and disinfection have more often been implemented for control of pathogens that are susceptible to a wide range of disinfectants (eg, MRSA, VRE, and gram-negative bacilli). Studies were included in this review if the impact of the intervention on rates of acquisition and/or infection was assessed.It should be appreciated that the studies reviewed here could potentially underestimate or overestimate the real-world benefits of environmental disinfection interventions. On one hand, environmental disinfection is often included as one component of multifaceted infection control interventions. Many such successful interventions are not included in this review because the contribution of environmental disinfection to the overall success of the programs is uncertain.26Weiss K. Boisvert A. Chagnon M. Duchesne C. Habash S. Lepage Y. et al.Multipronged intervention strategy to control an outbreak of Clostridium difficile infection (CDI) and its impact on the rates of CDI from 2002 to 2007.Infect Control Hosp Epidemiol. 2009; 30: 156-162Crossref PubMed Scopus (55) Google Scholar, 27Abbett S.K. Yokoe D.S. Lipsitz S.R. Bader A.M. Berry W.R. Tamplin E.M. et al.Proposed checklist of hospital interventions to decrease the incidence of healthcare-associated Clostridium difficile infection.Infect Control Hosp Epidemiol. 2009; 30: 1062-1069Crossref PubMed Scopus (49) Google Scholar, 28Salgado C.D. Mauldin P.D. Fogle P.J. Bosso J.A. Analysis of an outbreak of Clostridium difficile infection controlled with enhanced infection control measures.Am J Infect Control. 2009; 37: 458-464Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar, 29Cartmill T.D. Panigrahi H. Worsley M.A. McCann D.C. Nice C.N. Keith E. Management and control of a large outbreak of diarrhoea due to Clostridium difficile.J Hosp Infect. 1994; 27: 1-15Abstract Full Text PDF PubMed Scopus (132) Google Scholar, 30Muto C.A. Blank M.K. Marsh J.W. Vergis E.N. O’Leary M.M. Shutt K.A. et al.Control of an outbreak of infection with the hypervirulent Clostridium difficile BI strain in a university hospital using a comprehensive “bundle” approach.Clin Infect Dis. 2007; 45: 1266-1273Crossref PubMed Scopus (205) Google Scholar On the other hand, the published literature might provide an overly optimistic assessment of the impact of environmental disinfection interventions. Many institutions have implemented environmental disinfection interventions without reducing colonization or infection with health care-associated pathogens but have not published their findings (author’s unpublished data). Successful interventions are more likely to be submitted for publication than those that fail.Disinfectant product substitutionsTable 1 provides an overview of 7 studies that involved disinfectant substitutions.25Orenstein R. Aronhalt K.C. McManus Jr., J.E. Fedraw L.A. A targeted strategy to wipe out.Clostridium difficile. Infect Control Hosp Epidemiol. 2011; 32: 1137-1139Crossref PubMed Scopus (60) Google Scholar, 31Dharan S. Mourouga P. Copin P. Bessmer G. Tschanz B. Pittet D. Routine disinfection of patients’ environmental surfaces. Myth or reality?.J Hosp Infect. 1999; 42: 113-117Abstract Full Text PDF PubMed Scopus (116) Google Scholar, 32Kaatz G.W. Gitlin S.D. Schaberg D.R. Wilson K.H. Kauffman C.A. Seo S.M. et al.Acquisition of Clostridium difficile from the hospital environment.Am J Epidemiol. 1988; 127: 1289-1294Crossref PubMed Scopus (196) Google Scholar, 33Mayfield J.L. Leet T. Miller J. Mundy L.M. Environmental control to reduce transmission of Clostridium difficile.Clin Infect Dis. 2000; 31: 995-1000Crossref PubMed Scopus (233) Google Scholar, 34Wilcox M.H. Fawley W.N. Wigglesworth N. Parnell P. Verity P. Freeman J. Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection.J Hosp Infect. 2003; 54: 109-114Abstract Full Text Full Text PDF PubMed Scopus (217) Google Scholar, 35McMullen K.M. Zack J. Coopersmith C.M. Kollef M. Dubberke E. Warren D.K. Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea.Infect Control Hosp Epidemiol. 2007; 28: 205-207Crossref PubMed Scopus (54) Google Scholar, 36Hacek D.M. Ogle A.M. Fisher A. Robicsek A. Peterson L.R. Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile.Am J Infect Control. 2010; 38: 350-353Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar In one intervention, an active oxygen-based compound was substituted for a detergent for daily cleaning of floors and furniture, and a quaternary ammonium compound was continued for floors on a second ward.31Dharan S. Mourouga P. Copin P. Bessmer G. Tschanz B. Pittet D. Routine disinfection of patients’ environmental surfaces. Myth or reality?.J Hosp Infect. 1999; 42: 113-117Abstract Full Text PDF PubMed Scopus (116) Google Scholar The active oxygen-based product was associated with better eradication of bacteria from surfaces but no reduction in nosocomial bloodstream infections or MRSA colonization and infection. In the other interventions, hypochlorite was substituted for a nonsporicidal product as a strategy to control C difficile. The concentration of hypochlorite ranged from 500 to 5,500 parts per million (ppm). In each of the C difficile infection (CDI) interventions, there was a reduction in infections on 1 or more wards. Mayfield et al33Mayfield J.L. Leet T. Miller J. Mundy L.M. Environmental control to reduce transmission of Clostridium difficile.Clin Infect Dis. 2000; 31: 995-1000Crossref PubMed Scopus (233) Google Scholar found that CDI rates decreased significantly on a bone marrow transplant with a relatively high endemic incidence of CDI but not on a medical ward or intensive care unit with lower baseline rates. Similarly, in a crossover study on 2 medical wards in a nonoutbreak setting, Wilcox et al34Wilcox M.H. Fawley W.N. Wigglesworth N. Parnell P. Verity P. Freeman J. Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection.J Hosp Infect. 2003; 54: 109-114Abstract Full Text Full Text PDF PubMed Scopus (217) Google Scholar found that the incidence of CDI decreased only on the ward with the higher baseline CDI rate. These results suggest that environmental disinfection interventions may have greater impact in settings where the baseline incidence is high. However, Hacek et al36Hacek D.M. Ogle A.M. Fisher A. Robicsek A. Peterson L.R. Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile.Am J Infect Control. 2010; 38: 350-353Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar reported a significant reduction in CDI incidence from a relatively low endemic baseline rate when hypochlorite was substituted for a quaternary ammonium product in 3 hospitals.Table 1Studies involving disinfectant product substitutionsRefSetting and organismProductPracticeMonitoring of disinfectionEffect31Dharan S. Mourouga P. Copin P. Bessmer G. Tschanz B. Pittet D. Routine disinfection of patients’ environmental surfaces. Myth or reality?.J Hosp Infect. 1999; 42: 113-117Abstract Full Text PDF PubMed Scopus (116) Google Scholar2 Hospital wardsNosocomial infectionsActive oxygen-based compoundDaily cleaning of floors and furnitureCultures: decreased bacterial load on surfacesNo reduction in bloodstream infections or MRSA colonization or infection32Kaatz G.W. Gitlin S.D. Schaberg D.R. Wilson K.H. Kauffman C.A. Seo S.M. et al.Acquisition of Clostridium difficile from the hospital environment.Am J Epidemiol. 1988; 127: 1289-1294Crossref PubMed Scopus (196) Google ScholarMedical wardClostridium difficileHypochlorite 500 ppmTerminal CDI roomsCultures: surface contamination decreased to 21% of initial levelsOutbreak ended33Mayfield J.L. Leet T. Miller J. Mundy L.M. Environmental control to reduce transmission of Clostridium difficile.Clin Infect Dis. 2000; 31: 995-1000Crossref PubMed Scopus (233) Google ScholarBone marrow transplant (BMT) unit, Medical Ward, ICUClostridium difficileHypochlorite 5,000 ppmTerminal CDI roomsNoSignificant decrease on BMT unit but not on the other 2 wards34Wilcox M.H. Fawley W.N. Wigglesworth N. Parnell P. Verity P. Freeman J. Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection.J Hosp Infect. 2003; 54: 109-114Abstract Full Text Full Text PDF PubMed Scopus (217) Google Scholar2 Medical wards (crossover study)Clostridium difficileHypochlorite 1,000 ppmTerminal CDI roomsCultures: no decrease in the percentage of positive environmental culturesDecreased on 1 of 2 wards35McMullen K.M. Zack J. Coopersmith C.M. Kollef M. Dubberke E. Warren D.K. Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea.Infect Control Hosp Epidemiol. 2007; 28: 205-207Crossref PubMed Scopus (54) Google ScholarMedical and surgical ICUsClostridium difficileHypochlorite 5,000 ppmWard 1: terminal CDI rooms; ward 2: all roomsNoDecreased on both units36Hacek D.M. Ogle A.M. Fisher A. Robicsek A. Peterson L.R. Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile.Am J Infect Control. 2010; 38: 350-353Abstract Full Text Full Text PDF PubMed Scopus (72) Google Scholar3 HospitalsClostridium difficileHypochlorite 5,000 ppmTerminal CDI roomsNo48% decrease in prevalence density of CDI25Orenstein R. Aronhalt K.C. McManus Jr., J.E. Fedraw L.A. A targeted strategy to wipe out.Clostridium difficile. Infect Control Hosp Epidemiol. 2011; 32: 1137-1139Crossref PubMed Scopus (60) Google Scholar2 Medical wardsClostridium difficileHypochlorite 5,500 ppm (wipes)Terminal and daily CDI and non-CDI roomsYes (ATP bioluminescence)85% decrease in hospital acquired CDIATP, Adenosine triphosphate; BMT, Bone marrow transplant; CDI, C difficile infection; ICU, intensive care unit; PPM, parts per million; Ref, reference number.NOTE. 5,000 ppm = 1:10 dilution of household bleach. Open table in a new tab Reductions in CDI were achieved with a variety of disinfection strategies. Kaatz et al32Kaatz G.W. Gitlin S.D. Schaberg D.R. Wilson K.H. Kauffman C.A. Seo S.M. et al.Acquisition of Clostridium difficile from the hospital environment.Am J Epidemiol. 1988; 127: 1289-1294Crossref PubMed Scopus (196) Google Scholar ended a CDI outbreak on a medical ward by disinfecting the entire unit with hypochlorite. Orenstein et al25Orenstein R. Aronhalt K.C. McManus Jr., J.E. Fedraw L.A. A targeted strategy to wipe out.Clostridium difficile. Infect Control Hosp Epidemiol. 2011; 32: 1137-1139Crossref PubMed Scopus (60) Google Scholar achieved an 85% reduction in hospital-acquired CDI when hypochlorite wipes were used for daily and terminal disinfection of CDI and non-CDI rooms on 2 medical wards. However, McMullen et al35McMullen K.M. Zack J. Coopersmith C.M. Kollef M. Dubberke E. Warren D.K. Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea.Infect Control Hosp Epidemiol. 2007; 28: 205-207Crossref PubMed Scopus (54) Google Scholar found that CDI rates decreased on a unit that used hypochlorite for all rooms and on a second unit that used hypochlorite only for CDI rooms. In the other 3 reports, reductions in CDI were achieved with use of hypochlorite for terminal disinfection of CDI rooms. These results suggest that it may be sufficient to focus disinfection efforts on CDI rooms.Six of the 7 interventions in Table 1 were quasiexperimental studies in which rates were compared before and after interventions with no concurrent control group. Quasiexperimental studies are subject to a number of limitations, including difficulty in controlling for confounding factors and regression to the mean.37Harris A.D. Bradham D.D. Baumgarten M. Zuckerman I.H. Fink J.C. Perencevich E.N. The use and interpretation of quasi-experimental studies in infectious diseases.Clin Infect Dis. 2004; 38: 1586-1591Crossref PubMed Scopus (230) Google Scholar In the studies reviewed, a number of potential confounding factors were not reported. For example, compliance with hand hygiene or contact precautions could impact infection or colonization rates, but detailed information on these measures was not provided in any of the studies. Of the studies reviewed, the intervention of Mayfield et al33Mayfield J.L. Leet T. Miller J. Mundy L.M. Environmental control to reduce transmission of Clostridium difficile.Clin Infect Dis. 2000; 31: 995-1000Crossref PubMed Scopus (233) Google Scholar unintentionally achieved a higher study design quality by having a repeated-treatment design. As shown in Figure 2, the incidence of CDI decreased when hypochlorite was substituted for a quaternary ammonium product, increased again when the quaternary ammonium product was reinstituted in response to an increase in VRE infections, and finally was again reduced with reinstitution of hypochlorite.33Mayfield J.L. Leet T. Miller J. Mundy L.M. Environmental control to reduce transmission of Clostridium difficile.Clin Infect Dis. 2000; 31: 995-1000Crossref PubMed Scopus (233) Google ScholarFig 2Incidence of Clostridium difficile infection (CDI) on a bone marrow transplant unit during periods when different disinfectant products were used (adapted from Mayfield et al33Mayfield J.L. Leet T. Miller J. Mundy L.M. Environmental control to reduce transmission of Clostridium difficile.Clin Infect Dis. 2000; 31: 995-1000Crossref PubMed Scopus (233) Google Scholar). The 4 periods included the following: (1) period 1: quaternary ammonium disinfectant; period 2: bleach containing 5,000 parts per million hypochlorite used for CDI rooms; period 3: quaternary ammonium disinfectant used daily for all rooms in response to an outbreak of vancomycin-resistant enterococci; and period 4: reinstitution of bleach for CDI rooms. Quat, quaternary ammonium disinfectant.View Large Image Figure ViewerDownload Hi-res image Download (PPT)An important limitation of many of these studies is the absence of adequate monitoring to ensure that disinfectants were being applied effectively. In 3 of the 6 CDI studies, no routine monitoring of cleaning performance was reported. Only 2 of these studies included the use of environmental cultures to assess the impact of the intervention on surface disinfection. Kaatz et al32Kaatz G.W. Gitlin S.D. Schab