How to eradicate Clostridium difficile from the environment

  • F. Barbut
    Address: Hôpital Saint Antoine, UHLIN, 184, rue du faubourg Saint Antoine, 75012 Paris, France. Tel.: +33 1 49 28 30 11; fax: +33 1 49 28 30 09.
    National Reference Laboratory for C. difficile and Clinical Research Group EPIDIFF, University Pierre et Marie Curie, Paris, France

    Infection Control Unit, Hôpital Saint-Antoine, Paris, France
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Published:January 07, 2015DOI:


      During the last decade, Clostridium difficile has emerged as a major cause of healthcare-associated diarrhoea and death. Transmission of this spore-forming bacterium is thought to occur via the hands of healthcare providers or via the contaminated environment. Therefore, enhanced environmental cleaning/disinfection of the rooms housing C. difficile-infected patients is warranted. Guidelines from various scientific bodies have been published. They recommend performing environmental decontamination of rooms of patients with C. difficile infection (CDI) using hypochlorite (diluted 1/10) or a sporicidal product. Compliance with cleaning and disinfection is a critical point and is often suboptimal. Novel ‘no-touch’ methods for room disinfection have recently been introduced. Ultraviolet (UV) light or hydrogen peroxide systems are most widely used. In-vitro studies suggest that hydrogen peroxide vapour (from 30% hydrogen peroxide) methods achieve a >6 log10 reduction in C. difficile spores placed on carriers, and that aerosolized hydrogen peroxide systems (from 5% to 6% hydrogen peroxide) achieve ∼4 log10 reduction, whereas UV-based methods achieve ∼2 log10 reduction. Very few studies have assessed the impact of these devices on the transmission of C. difficile. Major limitations of these devices include the fact that they can only be used after the patient's discharge, because patients and staff must be removed from the room. The new no-touch methods for room disinfection supplement, but do not replace, daily cleaning.


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        • Zarb P.
        • Coignard B.
        • Griskeviciene J.
        • et al.
        The European Centre for Disease Prevention and Control (ECDC) pilot point prevalence survey of healthcare-associated infections and antimicrobial use.
        Euro Surveill. 2012; 17
      1. Davies KA, Davis GL, Ashwin HM, Lee F, Longshaw CM, Wilcox MH. Second report from the European, multi-centre, prospective bi-annual point prevalence study of Clostridium difficile infection in hospitalised patients with diarrhoea (EUCLID). 24th European Congress of Clinical Microbiology and Infectious Disease, Barcelona, 2014.

        • Magill S.S.
        • Edwards J.R.
        • Bamberg W.
        • et al.
        Multistate point-prevalence survey of health care-associated infections.
        N Engl J Med. 2014; 370: 1198-1208
        • US Centers for Disease Control and Prevention
        Antibiotic resistance threats in the United States, 2013.
        US Department of Heath and Human Services, Atlanta2013
        • Gabriel L.
        • Beriot-Mathiot A.
        Hospitalization stay and costs attributable to Clostridium difficile infection: a critical review.
        J Hosp Infect. 2014; 88: 12-21
        • Kuijper E.J.
        • Coignard B.
        • Tull P.
        Emergence of Clostridium difficile-associated disease in North America and Europe.
        Clin Microbiol Infect. 2006; 12: 2-18
        • Dubberke E.R.
        • Reske K.A.
        • Olsen M.A.
        • McDonald L.C.
        • Fraser V.J.
        Short- and long-term attributable costs of Clostridium difficile-associated disease in nonsurgical inpatients.
        Clin Infect Dis. 2008; 46: 497-504
        • O'Brien J.A.
        • Lahue B.J.
        • Caro J.J.
        • Davidson D.M.
        The emerging infectious challenge of Clostridium difficile-associated disease in Massachusetts hospitals: clinical and economic consequences.
        Infect Control Hosp Epidemiol. 2007; 28: 1219-1227
        • Loo V.G.
        • Bourgault A.M.
        • Poirier L.
        • et al.
        Host and pathogen factors for Clostridium difficile infection and colonization.
        N Engl J Med. 2011; 365: 1693-1703
        • Kim K.H.
        • Fekety R.
        • Batts D.H.
        • et al.
        Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated colitis.
        J Infect Dis. 1981; 143: 42-50
        • Samore M.H.
        • Venkataraman L.
        • DeGirolami P.C.
        • Arbeit R.D.
        • Karchmer A.W.
        Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.
        Am J Med. 1996; 100: 32-40
        • McFarland L.V.
        • Mulligan M.E.
        • Kwok R.Y.
        • Stamm W.E.
        Nosocomial acquisition of Clostridium difficile infection.
        N Engl J Med. 1989; 320: 204-210
        • Riggs 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: 992-998
        • Best E.L.
        • Fawley W.N.
        • Parnell P.
        • Wilcox M.H.
        The potential for airborne dispersal of Clostridium difficile from symptomatic patients.
        Clin Infect Dis. 2010; 50: 1450-1457
        • Boyce J.M.
        • Havill N.L.
        • Otter J.A.
        • et al.
        Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
        Infect Control Hosp Epidemiol. 2008; 29: 723-729
        • Claro T.
        • Daniels S.
        • Humphreys H.
        Detecting Clostridium difficile spores from inanimate surfaces of the hospital environment: which method is best?.
        J Clin Microbiol. 2014; 52: 3426-3428
        • Lawley T.D.
        • Clare S.
        • Deakin L.J.
        • et al.
        Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.
        Appl Environ Microbiol. 2010; 76: 6895-6900
        • Otter J.A.
        • French G.L.
        Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor.
        J Clin Microbiol. 2009; 47: 205-207
        • Wagenvoort J.H.
        • De Brauwer E.I.
        • Penders R.J.
        • Willems R.J.
        • Top J.
        • Bonten M.J.
        Environmental survival of vancomycin-resistant Enterococcus faecium.
        J Hosp Infect. 2011; 77: 282-283
        • Fawley W.N.
        • Underwood S.
        • Freeman J.
        • et al.
        Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains.
        Infect Control Hosp Epidemiol. 2007; 28: 920-925
        • Shaughnessy M.K.
        • Micielli R.L.
        • DePestel D.D.
        • et al.
        Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.
        Infect Control Hosp Epidemiol. 2011; 32: 201-206
        • Rebmann T.
        • Carrico R.M.
        • Association for Professionals in Infection Control and Epidemiology
        Preventing Clostridium difficile infections: an executive summary of the Association for Professionals in Infection Control and Epidemiology's elimination guide.
        Am J Infect Control. 2011; 39: 239-242
        • Cohen S.H.
        • Gerding D.N.
        • Johnson S.
        • et al.
        Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA).
        Infect Control Hosp Epidemiol. 2010; 31: 431-455
        • Dubberke E.R.
        • Carling P.
        • Carrico R.
        • et al.
        Strategies to prevent Clostridium difficile infections in acute care hospitals: 2014 update.
        Infect Control Hosp Epidemiol. 2014; 35: 628-645
        • Vonberg R.P.
        • Kuijper E.J.
        • Wilcox M.H.
        • et al.
        Infection control measures to limit the spread of Clostridium difficile.
        Clin Microbiol Infect. 2008; 14: 2-20
        • Curry S.R.
        • Muto C.A.
        • Schlackman J.L.
        • et al.
        Use of multilocus variable number of tandem repeats analysis genotyping to determine the role of asymptomatic carriers in Clostridium difficile transmission.
        Clin Infect Dis. 2013; 57: 1094-1102
        • Perez J.
        • Springthorpe V.S.
        • Sattar S.A.
        Activity of selected oxidizing microbicides against the spores of Clostridium difficile: relevance to environmental control.
        Am J Infect Control. 2005; 33: 320-325
        • Speight S.
        • Moy A.
        • Macken S.
        • et al.
        Evaluation of the sporicidal activity of different chemical disinfectants used in hospitals against Clostridium difficile.
        J Hosp Infect. 2011; 79: 18-22
        • Kaatz G.W.
        • Gitlin S.D.
        • Schaberg D.R.
        • et al.
        Acquisition of Clostridium difficile from the hospital environment.
        Am J Epidemiol. 1988; 127: 1289-1294
        • Mayfield J.L.
        • Leet T.
        • Miller J.
        • Mundy L.M.
        Environmental control to reduce transmission of Clostridium difficile.
        Clin Infect Dis. 2000; 31: 995-1000
        • Wilcox 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: 109-114
        • McMullen 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: 205-207
        • Hacek 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: 350-353
        • Manian F.A.
        • Griesnauer S.
        • Bryant A.
        Implementation of hospital-wide enhanced terminal cleaning of targeted patient rooms and its impact on endemic Clostridium difficile infection rates.
        Am J Infect Control. 2013; 41: 537-541
        • Orenstein 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: 1137-1139
        • Passaretti C.L.
        • Otter J.A.
        • Reich N.G.
        • et al.
        An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.
        Clin Infect Dis. 2012; 56: 27-35
        • Levin J.
        • Riley L.S.
        • Parrish C.
        • English D.
        • Ahn S.
        The effect of portable pulsed xenon ultraviolet light after terminal cleaning on hospital-associated Clostridium difficile infection in a community hospital.
        Am J Infect Control. 2013; 41: 746-748
        • Barbut F.
        • Menuet D.
        • Verachten M.
        • Girou E.
        Comparison of the efficacy of a hydrogen peroxide dry-mist disinfection system and sodium hypochlorite solution for eradication of Clostridium difficile spores.
        Infect Control Hosp Epidemiol. 2009; 30: 507-514
        • Carling 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: 1-7
        • Carling P.C.
        • Von Beheren S.
        • Kim P.
        • Woods C.
        Intensive care unit environmental cleaning: an evaluation in sixteen hospitals using a novel assessment tool.
        J Hosp Infect. 2008; 68: 39-44
        • Eckstein B.C.
        • Adams D.A.
        • Eckstein E.C.
        • et al.
        Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
        BMC Infect Dis. 2007; 7: 61
        • Boyce J.M.
        • Havill N.L.
        • Moore B.A.
        Terminal decontamination of patient rooms using an automated mobile UV light unit.
        Infect Control Hosp Epidemiol. 2011; 32: 737-742
        • Nerandzic M.M.
        • Cadnum J.L.
        • Pultz M.J.
        • Donskey C.J.
        Evaluation of an automated ultraviolet radiation device for decontamination of Clostridium difficile and other healthcare-associated pathogens in hospital rooms.
        BMC Infect Dis. 2010; 10: 197
        • Rutala W.A.
        • Weber D.J.
        Guideline for disinfection and sterilization of prion-contaminated medical instruments.
        Infect Control Hosp Epidemiol. 2010; 31: 107-117
        • Barbut F.
        • Yezli S.
        • Otter J.A.
        Activity in vitro of hydrogen peroxide vapour against Clostridium difficile spores.
        J Hosp Infect. 2012; 80: 85-87
        • Fu T.Y.
        • Gent P.
        • Kumar V.
        Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
        J Hosp Infect. 2012; 80: 199-205
        • Havill N.L.
        • Moore B.A.
        • Boyce J.M.
        Comparison of the microbiological efficacy of hydrogen peroxide vapor and ultraviolet light processes for room decontamination.
        Infect Control Hosp Epidemiol. 2012; 33: 507-512
        • Nerandzic M.M.
        • Cadnum J.L.
        • Eckart K.E.
        • Donskey C.J.
        Evaluation of a hand-held far-ultraviolet radiation device for decontamination of Clostridium difficile and other healthcare-associated pathogens.
        BMC Infect Dis. 2012; 12: 120
        • Anderson D.J.
        • Gergen M.F.
        • Smathers E.
        • et al.
        Decontamination of targeted pathogens from patient rooms using an automated ultraviolet-C-emitting device.
        Infect Control Hosp Epidemiol. 2013; 34: 466-471
        • Haas J.P.
        • Menz J.
        • Dusza S.
        • Montecalvo M.A.
        Implementation and impact of ultraviolet environmental disinfection in an acute care setting.
        Am J Infect Control. 2014; 42: 586-590
        • Linley E.
        • Denyer S.P.
        • McDonnell G.
        • Simons C.
        • Maillard J.Y.
        Use of hydrogen peroxide as a biocide: new consideration of its mechanisms of biocidal action.
        J Antimicrob Chemother. 2012; 67: 1589-1596
        • Hall L.
        • Otter J.A.
        • Chewins J.
        • Wengenack N.L.
        Use of hydrogen peroxide vapor for deactivation of Mycobacterium tuberculosis in a biological safety cabinet and a room.
        J Clin Microbiol. 2007; 45: 810-815
        • Holmdahl T.
        • Lanbeck P.
        • Wullt M.
        • Walder M.H.
        A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
        Infect Control Hosp Epidemiol. 2011; 32: 831-836
        • Shapey S.
        • Machin K.
        • Levi K.
        • Boswell T.C.
        Activity of a dry mist hydrogen peroxide system against environmental Clostridium difficile contamination in elderly care wards.
        J Hosp Infect. 2008; 70: 136-141
        • Boyce J.M.
        Environmental contamination makes an important contribution to hospital infection.
        J Hosp Infect. 2007; 65: 50-54
        • Cooper T.
        • O'Leary M.
        • Yezli S.
        • Otter J.A.
        Impact of environmental decontamination using hydrogen peroxide vapour on the incidence of Clostridium difficile infection in one hospital Trust.
        J Hosp Infect. 2011; 78: 238-240
        • Otter J.A.
        • Barnicoat M.
        • Down J.
        • Smyth D.
        • Yezli S.
        • Jeanes A.
        Hydrogen peroxide vapour decontamination of a critical care unit room used to treat a patient with Lassa fever.
        J Hosp Infect. 2010; 75: 335-337
        • Barbut F.
        • Yezli S.
        • Mimoun M.
        • Pham J.
        • Chaouat M.
        • Otter J.A.
        Reducing the spread of Acinetobacter baumannii and methicillin-resistant Staphylococcus aureus on a burns unit through the intervention of an infection control bundle.
        Burns. 2013; 39: 395-403
        • Boyce J.M.
        • Havill N.L.
        • Cianci V.
        • Flanagan G.
        Compatibility of hydrogen peroxide vapor room decontamination with physiological monitors.
        Infect Control Hosp Epidemiol. 2014; 35: 92-93
        • Moat J.
        • Cargill J.
        • Shone J.
        • Upton M.
        Application of a novel decontamination process using gaseous ozone.
        Can J Microbiol. 2009; 55: 928-933
        • Sharma M.
        • Hudson J.B.
        Ozone gas is an effective and practical antibacterial agent.
        Am J Infect Control. 2008; 36: 559-563
        • Li C.S.
        • Wang Y.C.
        Surface germicidal effects of ozone for microorganisms.
        AIHA J (Fairfax, VA). 2003; 64: 533-537