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Disinfectants used for environmental disinfection and new room decontamination technology

  • William A. Rutala
    Correspondence
    Address correspondence to William A. Rutala, PhD, MPH, Division of Infectious Diseases, 130 Mason Farm Road, Bioinformatics, UNC at Chapel Hill, Chapel Hill, NC 27599-7030.
    Affiliations
    Hospital Epidemiology, University of North Carolina Health Care System, Chapel Hill, NC

    Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, NC
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  • David J. Weber
    Affiliations
    Hospital Epidemiology, University of North Carolina Health Care System, Chapel Hill, NC

    Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, NC
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      Environmental contamination plays an important role in the transmission of several key health care-associated pathogens. Effective and thorough cleaning/disinfecting of the patient environment is essential. Room decontamination units (such as ultraviolet-C and hydrogen peroxide systems) aid in reducing environmental contamination after terminal room cleaning and disinfection.

      Key Words

      Health care-associated infections remain an important source of morbidity and mortality with an estimated 1.7 million infections and 99,000 deaths annually.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      The major source of nosocomial pathogens is thought to be the patient’s endogenous flora, but an estimated 20% to 40% of health care-associated infections have been attributed to cross infection via the hands of health care personnel.
      • Weinstein R.A.
      Epidemiology and control of nosocomial infections in adult intensive care units.
      Contamination of the hands of health care personnel could in turn result from either direct patient contact or indirectly from touching contaminated environmental surfaces. Health care personnel have frequent contact with the environmental surfaces in patient’s rooms, providing ample opportunity for contamination of gloves and/or hands.
      • Huslage K.
      • Rutala W.A.
      • Sickbert-Bennett E.
      • Weber D.J.
      A quantitative approach to defining high-touch surfaces in hospitals.
      Two recent studies demonstrated that contact with the environment was just as likely to contaminate the hands of health care workers as was direct contact with the patient.
      • Stiefel 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.
      • Guerrero 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.
      Furthermore, it has been observed that there is lower compliance with hand hygiene by health care personnel following contact with the patient’s environment than directly with the patient.
      • Randle J.
      • Arthur A.
      • Vaughn N.
      Twenty-four hour observational study of hospital hand hygiene compliance.
      There is excellent evidence in the scientific literature that environmental contamination plays an important role in the transmission of several key health care-associated pathogens including methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus (VRE), Acinetobacter, norovirus, and Clostridium difficile.
      • Dancer S.J.
      The role of environmental cleaning in the control of hospital-acquired infection.
      • Boyce J.M.
      Environmental contamination makes an important contribution to hospital infection.
      • Weber 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination by ultraviolet radiation.
      All these pathogens have been demonstrated to persist in the environment for hours to days (in some cases months),
      • Kramer A.
      • Schwebke I.
      • Kampf G.
      How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
      to frequently contaminate the environmental surfaces in rooms of colonized or infected patients, to transiently colonize the hands of health care personnel, to be transmitted by health care personnel, and to cause outbreaks in which environmental transmission was deemed to play a role. Furthermore, admission to a room in which the previous patient had been colonized or infected with MRSA, VRE, Acinetobacter, or C difficile has been shown to be a risk factor for the newly admitted patient to develop colonization or infection.
      • Huang S.S.
      • Datta R.
      • Platt R.
      Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestal D.D.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.
      • Otter J.A.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.

      Adequacy of room cleaning and disinfection using chemical germicides

      It has long been recommended in the United States that environmental surfaces in patient rooms be cleaned/disinfected on a regular basis (eg, daily, 3 times per week), when surfaces are visibly soiled, and following patient discharge (terminal cleaning).

      Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.

      Studies have demonstrated that adequate environment cleaning is frequently lacking. For example, Carling et al assessed the thoroughness of terminal cleaning in the patient’s immediate environment in 23 acute care hospitals (1,119 patient rooms) by using a transparent, easily cleaned, stable solution that fluoresces when exposed to hand-held ultraviolet (UV) light.
      • Carling P.C.
      • Parry M.F.
      • Von Beheren S.M.
      Healthcare Environmental Hygiene Study Group
      Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.
      The overall thoroughness of cleaning, expressed as a percent of surfaces evaluated, was 49% (range for all hospitals, 35%-81%). Using a similar design, Carling et al assessed the environmental cleaning in intensive care unit rooms in 16 hospitals (2,320 objects) and demonstrated that only 57.1% of sites were cleaned following discharge of the room’s occupant.
      • Carling P.C.
      • von Bheren S.
      • Kim P.
      • Woods C.
      Intensive care unit environmental cleaning: an evaluation in sixteen hospitals using a novel assessment tool.
      A study by Havill et al using adenosine triphosphate (ATP) bioluminescence assays and aerobic cultures demonstrated that medical equipment frequently had not been disinfected as per protocol.
      • Havill N.L.
      • Havill H.L.
      • Mangione E.
      • Dumigan D.G.
      • Boyce J.M.
      Cleanliness of portable medical equipment disinfected by nursing staff.
      Disinfection is generally performed using an US Environmental Protection Agency (EPA)-registered hospital disinfectant such as quaternary ammonium compounds, chlorine-containing compound, phenolics, or improved hydrogen peroxide (HP) (Table 1). The improved HP-based environmental surface disinfectants have proved to be more effective (>6-log10 reduction) and fast-acting (30-60 seconds) microbicides in the presence of a soil load (to simulate the presence of body fluids) than commercially available HP.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Efficacy of improved hydrogen peroxide against important healthcare-associated pathogens.
      Table 1Summary of advantages and disadvantages of disinfectants used as low-level disinfectants

      Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.

      Low-level disinfectantAdvantagesDisadvantages
      Alcohol
      • Bactericidal, tuberculocidal, fungicidal, virucidal
      • Fast acting
      • Easy to use
      • Used to disinfect small surfaces such as rubber stoppers on medication vials
      • No toxic residue
      • Not sporicidal
      • Affected by organic matter
      • No detergent or cleaning properties
      • Not EPA registered
      • Damage some instruments (eg, harden rubber, deteriorate glue)
      • Flammable (large amounts require special storage)
      • Evaporates rapidly
      • Do not use alcohol for large surfaces
      Chlorine
      • Broad-spectrum bactericidal, tuberculocidal, fungicidal, virucidal, sporicidal
      • No toxic residue
      • Fast acting
      • Inexpensive
      • Unaffected by water hardness
      • Low incidence of serious toxicity
      • Reduces biofilms of surfaces
      • Relatively stable (eg, 50% reduction in chlorine concentration in 30 days)
      • Used as the disinfectant in water treatment
      • EPA registered
      • At 5% can cause eye irritation, oropharyngeal, esophageal, and gastric burns
      • Corrosiveness to metals in high concentrations (>500 ppm)
      • Inactivated by organic matter
      • Discoloring of fabrics
      • Release of toxic chlorine gas when mixed with acid or ammonia
      • Potential hazard is production of trihalomethane
      Improved hydrogen peroxide
      • 30 second-1 min bactericidal and virucidal claim
      • 5 min mycobactericidal claim
      • Safe for workers (lowest EPA toxicity category, IV)
      • Benign for the environment
      • Unaffected by organic matter
      • Surface compatible
      • Noncorrosive
      • EPA registered
      • Non-staining
      • More expensive than some low-level disinfectants
      Iodophors
      • Bactericidal, mycobactericidal, virucidal
      • Used for disinfecting blood culture bottles
      • Require prolonged contact to kill fungi
      • Not sporicidal
      • Damage silicone catheters
      • More commonly used as a antiseptic than disinfectant
      Phenolics
      • Bactericidal, tuberculocidal, fungicidal, virucidal
      • Inexpensive
      • EPA registered
      • Absorbed by porous materials and irritate tissue
      • Depigmentation of skin caused by certain phenolics
      • Not sporicidal
      • Hyperbilirubinemia in infants when phenolic is not prepared as recommended
      Quaternary ammonium compounds
      • Bactericidal, fungicidal, virucidal against enveloped viruses (eg, HIV)
      • Good cleaning agents
      • EPA registered
      • Surface compatible
      • Persistent antimicrobial activity when undisturbed
      • Not sporicidal, generally not tuberculocidal, and virucidal against nonenveloped viruses
      • High water hardness and cotton/gauze can make less microbicidal
      • A few reports documented asthma as result of exposure to benzalkonium chloride
      • Affected by organic matter
      Effective cleaning/disinfecting of the patient environment is essential; however, there have been few studies that have assessed various cleaning methods. A recent study comparing several cleaning/disinfecting methods against C difficile (eg, saturated cloth; spray [let sit 10 seconds] and wipe; spray, wipe, spray [let sit 1 minute] and wipe; use of disposable pop-up wipes) demonstrated no difference in the effectiveness of various wiping procedures. Wiping with a sporicidal agent eliminated ≥3.90 log10 C difficile by both physical removal and inactivation.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Efficacy of different “cleaning/disinfection” methods against Clostridium difficile spores: importance of physical removal versus sporicidal inactivation.

      Improving room cleaning/disinfection and demonstrating the effectiveness of surface decontamination in reducing health care-associated infections

      Several investigators have reported that intervention programs aimed at environmental services workers resulted in significant improvement in cleaning practices.
      • Carling P.C.
      • Parry M.F.
      • Bruno-Murtha A.L.
      • Dick B.
      Improving environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission.
      • Carling P.C.
      • Parry M.F.
      • Rupp M.E.
      • Po J.L.
      • Dick B.
      • Von Beheren S.M.
      Healthcare Environmental Hygiene Study Group
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
      • Lewis T.
      • Griffith C.
      • Gallo M.
      • Weinbren M.
      A modified ATP benchmark for evaluating the cleaning of some hospital environmental surfaces.
      Such interventions have generally included multiple activities: improved education, monitoring the thoroughness of cleaning (eg, by use of ATP assays or fluorescent dyes) with feedback of performance to the environmental service workers, and/or use of cleaning checklists. We have found that a specific assignment of cleaning responsibility for each hospital unit (eg, medical equipment to be cleaned by nursing; environmental surfaces to be cleaned by environmental service) is also important to ensure all objects and surfaces are decontaminated, especially the surfaces of medical equipment (eg, cardiac monitors). Improved environmental cleaning has been demonstrated to reduce the environmental contamination with VRE,
      • Hota B.
      • Blom D.W.
      • Lyle E.A.
      • Weinstein R.A.
      • Hayden M.K.
      Intervention evaluation of environmental contamination by vancomycin-resistant enterococci: failure of personnel, product, or procedure?.
      • Goodman E.R.
      • Platt R.
      • Bass R.
      • Onderdonk A.B.
      • Yokoe D.S.
      • Huang S.S.
      Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
      • Eckstein B.C.
      • Adams D.A.
      • Eckstein E.C.
      • Rao A.
      • Sethi A.K.
      • Yadavalli G.K.
      • et al.
      Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
      MRSA,
      • Goodman E.R.
      • Platt R.
      • Bass R.
      • Onderdonk A.B.
      • Yokoe D.S.
      • Huang S.S.
      Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
      and C difficile.
      • Eckstein B.C.
      • Adams D.A.
      • Eckstein E.C.
      • Rao A.
      • Sethi A.K.
      • Yadavalli G.K.
      • et al.
      Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
      Importantly, no study has reported, in the postintervention period, proper cleaning of more than 85% of objects. A concern of published studies is that they have only demonstrated improved cleaning of a limited number of “high risk” objects (or “targeted” objects) and not an improvement in the overall thoroughness of room decontamination. The focus of disinfection efforts should be directed at thorough, room disinfection
      • Hota B.
      • Blom D.W.
      • Lyle E.A.
      • Weinstein R.A.
      • Hayden M.K.
      Intervention evaluation of environmental contamination by vancomycin-resistant enterococci: failure of personnel, product, or procedure?.
      and not focused on “high risk” surfaces because they have not been demonstrated to be associated with an increased risk of contamination of health care personnel hands/gloves or increased risk for patient-to-patient transmission of pathogens. Nor should the disinfection efforts be focused on “high-touch” surfaces because the level of contamination is similar to that of lower, less frequently contacted surfaces (eg, high touch surface 71.9 colony-forming units [CFU]/Rodac vs low touch surface 56.7 CFU/Rodac before cleaning).
      • Huslage K.
      • Rutala W.A.
      • Gergen M.F.
      • Sickbert-Bennett E.E.
      • Weber D.J.
      Microbial assessment of high, medium, and low-touch hospital room surfaces.
      More emphasis should be placed on adequately training environmental service workers and providing timely feedback on the thoroughness of cleaning using fluorescent marking or ATP-based methods and surface disinfection of all “touchable” surfaces.

      Contact time for disinfection of noncritical surfaces and patient care equipment

      The US Centers for Disease and Prevention (CDC) guideline discusses a 1-minute contact time (ie, wet time) for low-level disinfection of noncritical environmental surfaces and patient care equipment. To get EPA clearance of the CDC Guideline, it was necessary to insert the sentences “By law, all applicable label instructions on EPA-registered products must be followed. If the user selects exposure conditions that differ from those on the EPA-registered product label, the user assumes liability from any injuries resulting from off-label use and is potentially subject to enforcement action under FIFRA.”

      Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.

      There are several points that should be made about this apparent disconnect between label instructions and what scientific studies demonstrate to include: (1) multiple scientific studies have demonstrated the efficacy of hospital disinfectants against pathogens causing health care-associated infections with a contact time of at least 1 minute

      Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee. Guideline for disinfection and sterilization in healthcare facilities, 2008. Available from: cdcgov/ncidod/dhqp/pdf/guidelines/Disinfection_Nov_2008pdf. Accessed February 12, 2013.

      ; (2) there are no data that demonstrate improved infection prevention by a 10-minute contact time versus a 1-minute contact time; and (3) we are not aware of an enforcement action by the EPA against health care facilities for “off label” use of a surface disinfectant. Furthermore, the only way an institution can achieve a contact time of 10 minutes is to reapply the surface disinfectant multiple times to the surface (which is unlikely) because the typical dry time for a water-based disinfectant is 1.5 to 2 minutes. Last, as important as disinfectant contact time is to surface disinfection, nothing is more important than the thoroughness of cleaning/disinfecting all hand contact surfaces (eg, environmental surfaces or patient care equipment) because current studies demonstrate that less than 50% of high-risk objects are cleaned/disinfected at terminal cleaning.
      • Carling P.C.
      • Parry M.F.
      • Bruno-Murtha A.L.
      • Dick B.
      Improving environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission.
      • Carling P.C.
      • Parry M.F.
      • Rupp M.E.
      • Po J.L.
      • Dick B.
      • Von Beheren S.M.
      Healthcare Environmental Hygiene Study Group
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
      Wiping all “hand contact” or “touchable” surfaces/equipment, and not just perceived “high risk” surfaces/equipment, is essential because “high risk” surfaces/equipment have not been epidemiologically defined. In addition, “high touch” surfaces have only recently been defined but there was no significant difference in microbial contamination of “high,” “medium,” and “low” touch surfaces.
      • Huslage K.
      • Rutala W.A.
      • Sickbert-Bennett E.
      • Weber D.J.
      A quantitative approach to defining high-touch surfaces in hospitals.
      If an institution chooses to use a product with a nonachievable label claim (eg, 10 minutes), it should prepare a formal risk assessment (see http://www.unc.edu/depts/spice/dis/SurfDisRiskAssess2011.pdf) to be presented to surveyors (eg, The Joint Commission) when challenged. Alternatively, the hospital could purchase and use for low-level disinfection of noncritical surfaces and patient care equipment an EPA-registered disinfectant with an achievable contact time such as a disinfectant with a 30 second to 2 minute bactericidal claim (see http://www.epa.gov/oppad001/chemregindex.htm).
      Another issue is which pathogen on the disinfectant label should be used to identify contact time (eg, bacteria, Candida, mycobacteria, spores) for surfaces in health care facilities. The CDC Guideline based the 1-minute contact time on demonstration of bactericidal activity for vegetative bacteria such as S aureus, Enterococcus, Eschericihia coli, coagulase-negative Staphylococcus, Pseudomonas aeruginosa, Klebsiella spp, Enterobacter spp, and others. These vegetative bacteria are the pathogens that cause the vast majority of health care-associated infections (85%-90%).
      • Kang J.
      • Sickbert-Bennett E.E.
      • Brown V.M.
      • Weber D.J.
      • Rutala W.A.
      Relative frequency of healthcare-associated pathogens by infection site at a university hospital from 1980-2008.
      • Hidron A.I.
      • Edwards J.R.
      • Patel J.
      • Horan T.C.
      • Sievert D.M.
      • Pollock D.A.
      • et al.
      Antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007.
      Furthermore, contaminated surfaces with organisms such as Candida, nontuberculous mycobacteria, and other fungi have rarely, if ever, been shown to be a risk factor for health care-associated infections. The only exception to this principle is the use of EPA-registered disinfectant effective against C difficile spores or norovirus for disinfecting the rooms of patients with one of these pathogens (see http://www.epa.gov/oppad001/chemregindex.htm).

      “No Touch” methods for room disinfection

      As noted above, multiple studies have demonstrated that environmental surfaces and objects in rooms are frequently not properly cleaned. Furthermore, whereas interventions aimed at improving cleaning thoroughness have demonstrated effectiveness, many surfaces remain inadequately cleaned and therefore potentially contaminated. For this reason, several manufacturers have developed room disinfection units that can decontaminate environmental surfaces and objects. These systems use 1 of 2 methods: either UV light or HP (Table 2, Table 3, Table 4).
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      • Davies A.
      • Pottage T.
      • Bennett A.
      • Walker J.
      Gaseous and air decontamination technologies for Clostridium difficile in the healthcare environment.
      These technologies supplement, but do not replace, standard cleaning and disinfection because surfaces must be physically cleaned of dirt and debris. Additionally, these methods can only be used for terminal or discharge room decontamination (ie, cannot be used for daily room decontamination) because the room must be emptied of people. This paper will update and expand on a recent publication of this topic.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      Table 2Comparison of room decontamination systems using hydrogen peroxide and ultraviolet irradiation
      NOTE. Adapted from Rutala and Weber
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      Otter and Yezli.
      • Otter J.A.
      • Yezli S.
      A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.
      Glosair (formerly Sterinis)SterisBioquellTru-D
      AbbreviationDMHP (dry mist HP)VHP (vaporized HP)HPV (HP vapor)UV-C
      Active agent5% hydrogen peroxide, <50 ppm silver cations, <50 ppm ortho-phosphoric acidVaprox (35% hydrogen peroxide)35% hydrogen peroxideUV-C irradiation at 254 nm
      ApplicationAerosol of active solutionVapor, noncondensingVapor, condensingUV irradiation; direct and reflected
      Aeration (removal of active agent from enclosure)Passive decompositionActive catalytic conversionActive catalytic conversionNot necessary
      Sporicidal efficacySingle cycle does not inactivate Bacillus atrophaeus BIs; ∼4-log10 reduction of C difficile and incomplete inactivation in situInactivation of Geobacillus stearothermophilus BIsInactivation of Geobacillus stearothermophilus BIs; >6-log10 reduction of C difficile in vitro and complete inactivation in situ1.8- to 4-log10 reduction of C difficile in situ
      Evidence of clinical impactNone publishedNone publishedSignificant reduction in the incidence of C difficileNone published
      BIs, Biologic indicators; UV-C, ultraviolet-C light; VRE, vancomycin-resistant Enterococcus.
      Glosair (Advanced Sterilization Products, Irvine, CA); Steris (Mentor, OH); Bioquell (Horsham, PA); Tru-D (Lumalier Conporation, Memphis, TN).
      Table 3Efficacy of hydrogen peroxide systems for decontamination of the hospital environment, by health care-associated pathogen
      NOTE. Modified from Falagas et al.
      • Falagas M.E.
      • Thomaidis P.C.
      • Kotsantis I.K.
      • Sgouros K.
      • Samonis G.
      • Karageorgopoulos D.E.
      Airborne hydrogen peroxide for disinfection of the hospital environment and infection control: a systematic review.
      Lead author, yearHP systemPathogenSites revealing contamination before HPVSites revealing contamination after HPV% Reduction
      French, 2004
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.T.
      • Watling D.
      • Parks M.J.
      Tackling contamination of the hospital environment by methicillin-resistant Staphylococcus aureus (MRSA): a comparison between conventional terminal cleaning and hydrogen peroxide vapour decontamination.
      HPVMRSA61/85-72%1/85-1%98
      Bates, 2005
      • Bates C.J.
      • Pearse R.
      Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit.
      HPVSerratia2/42-5%0/24-0%100
      Jeanes, 2005
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      HPVMRSA10/28-36%0/50-0%100
      Otter, 2007
      • Otter J.A.
      • Cummins M.
      • Ahmad F.
      • van Tonder C.
      • Drabu Y.J.
      Assessing the biological efficacy and rate of recontamination following hydrogen peroxide vapour decontamination.
      HPVMRSA18/30-60%1/30-3%95
      Dryden, 2008
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • Lewis T.
      • Davis-Blues K.
      • Otter J.A.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal methicillin-resistant Staphylococcus aureus outbreak on a surgical ward.
      HPVMRSA8/29-28%1/29-3%88
      Boyce, 2008
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • McDonald L.C.
      • Adams N.M.T.
      • Cooper T.
      • et al.
      Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      HPVC difficile11/43-26%0/37-0%100
      Bartels, 2008
      • Bartels M.D.
      • Kristofferson K.
      • Slotsbjerg T.
      • Rohde S.M.
      • Lunfgren B.
      • Westh H.
      Environmental methicillin-resistant Staphylococcus aureus (MRSA) disinfection using dry-mist-generated hydrogen peroxide.
      HP dry mistMRSA4/14-29%0/14-0%100
      Shapey, 2008
      • 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.
      HP dry mistC difficile48/203-24%7/203-3%88
      Barbut, 2009
      • 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.
      HP dry mistC difficile34/180-19%4/180-2%88
      Otter, 2010
      • Otter J.A.
      • Yezli S.
      • Schouten M.A.
      • van Zanten A.R.H.
      • Houmes-Zielman G.
      • Nohlmans-Paulssen M.K.E.
      Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.
      HPVGNR10/21-48%0/63-0%100
      HPV, Hydrogen peroxide vapor.
      Table 4Advantages and disadvantages of room decontamination by ultraviolet irradiation and hydrogen peroxide
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      Ultraviolet irradiation
      Advantages
      • Reliable biocidal activity against a wide range of health care-associated pathogens
      • Room surfaces and equipment decontaminated
      • Room decontamination is rapid (∼15 minutes) for vegetative bacteria
      • Effective against Clostridium difficile, although requires longer exposure (∼50 minutes)
      • HVAC (heating, ventilation and air conditioning) system does not need to be disabled and the room does not need to be sealed
      • UV is residual free and does not give rise to health or safety concerns
      • No consumable products so costs include only capital equipment and staff time
      • Good distribution in the room of UV energy via an automated monitoring system
      Disadvantages
      • All patients and staff must be removed from the room prior to decontamination
      • Decontamination can only be accomplished at terminal disinfection (ie, cannot be used for daily disinfection) as room must be emptied of people
      • Capital equipment costs are substantial
      • Does not remove dust and stains, which is important to patients and visitors, and, hence, cleaning must precede UV decontamination
      • Sensitive to use parameters (eg, wavelength, UV dose delivered)
      • Requires that equipment and furniture be moved away from the walls
      • Studies have not been conducted to demonstrate whether use of UV room decontamination decreases the incidence of health care-associated infections
      Decontamination by hydrogen peroxide systems
      Advantages
      • Reliable biocidal activity against a wide range of health care-associated pathogens
      • Room surfaces and equipment decontaminated
      • Effective against Clostridium difficile
      • Useful for disinfecting complex equipment and furniture
      • Does not require that furniture and equipment be moved away from the walls
      • HP is residual free and does not give rise to health or safety concerns (aeration unit converts HP into oxygen and water)
      • Uniform distribution in the room via an automated dispersal system
      • Demonstrated to reduce health care-associated infections (ie, Clostridium difficile)
      Disadvantages
      • All patients and staff must be removed from the room prior to decontamination
      • HVAC system must be disabled to prevent unwanted dilution of HP during use and the doors must be closed with gaps sealed by tape
      • Decontamination can only be accomplished as terminal disinfection (ie, cannot be used for daily disinfection) as room must be emptied of people
      • Capital equipment costs are substantial
      • Decontamination requires ∼2.5 to 5 hours
      • Does not remove dust and stains which are important to patients and visitors, and hence cleaning must precede UV decontamination
      • Sensitive to use parameters (eg, HP concentration)
      HVAC, Heating, ventilation, and air conditioning.

      UV light for room decontamination

      UV irradiation has been used for the control of pathogenic microorganisms in a variety of applications, such as control of legionellosis, as well as disinfection of air, surfaces, and instruments.
      • Rutala W.A.
      • Weber D.J.
      Sterilization, high-level disinfection, and environmental cleaning.
      • Memarzadeh F.
      • Olmsted R.N.
      • Bartley J.M.
      Applications of ultraviolet germicidal irradiation disinfection in health care facilities: effective adjunct, but not stand-alone technology.
      At certain wavelengths, UV light will break the molecular bonds in DNA, thereby destroying the organism. UV-C has a characteristic wavelength of 200 to 270 nm (eg, 254 nm), which lies in the germicidal active portion of the electromagnetic spectrum of 200 to 320 nm. The efficacy of UV irradiation is a function of many different parameters such as intensity, exposure time, lamp placement, and air movement patterns.
      An automated mobile UV-C unit (Tru-D; Lumalier Corporation; Memphis, TN) has been shown to eliminate > 3-log10 vegetative bacteria (MRSA, VRE, Acinetobacter baumannii) and > 2.4-log10 C difficile seeded onto formica surfaces in patients’ rooms experimentally contaminated.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination by ultraviolet radiation.
      There are 3 studies that have demonstrated that this UV-C system is capable of reducing vegetative bacteria inoculated on a carrier by >3- to 4-log10 in 15 to 20 minutes and C difficile by >1.7- to 4-log10 in 35 to 100 minutes.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination by ultraviolet radiation.
      • Boyce J.M.
      • Havill N.L.
      • Moore B.A.
      Terminal decontamination of patient rooms using an automated mobile UV light unit.
      • 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.
      The studies also demonstrate reduced effectiveness when surfaces were not in direct line-of-sight.

      HP systems for room decontamination

      Several systems that produce HP (eg, HP vapor, aerosolized dry mist HP, vaporized HP) have been studied for their ability to decontaminate environmental surfaces and objects in hospital rooms (Tables 2 and 3). A system using HP vapor has been demonstrated to completely inactivate >106 Bacillus stearothermophilus spores contained in biologic indicators hung in patient rooms and almost eliminate all MRSA surface contamination.
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.T.
      • Watling D.
      • Parks M.J.
      Tackling contamination of the hospital environment by methicillin-resistant Staphylococcus aureus (MRSA): a comparison between conventional terminal cleaning and hydrogen peroxide vapour decontamination.
      Other studies have also demonstrated the ability of HP systems to almost eliminate MRSA, VRE, M tuberculosis, spores, viruses, and multidrug-resistant gram-negative bacilli.
      • Falagas M.E.
      • Thomaidis P.C.
      • Kotsantis I.K.
      • Sgouros K.
      • Samonis G.
      • Karageorgopoulos D.E.
      Airborne hydrogen peroxide for disinfection of the hospital environment and infection control: a systematic review.
      • 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.
      • Bentley K.
      • Dove B.K.
      • Parks S.R.
      • Walker J.T.
      • Bennett A.M.
      Hydrogen peroxide vapour decontamination of surfaces artifically contaminated with norovirus surrogate feline calicivirus.
      Importantly, using a before-after design, Boyce et al have previously shown that use of the HP systems was associated with a significant reduction in the incidence of C difficile infection on 5 high-incidence wards.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • McDonald L.C.
      • Adams N.M.T.
      • Cooper T.
      • et al.
      Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      A recent paper by Passaretti et al demonstrated that environmental decontamination with HP vapor reduced the risk of a patient admitted to a room previously occupied by a colonized or infected patient with a multidrug-resistant organism from acquiring an multidrug-resistant organism by 64% compared with using standard disinfection methods.
      • Passaretti C.L.
      • Otter J.A.
      • Reich N.G.
      • Myers J.
      • Shepard J.
      • Ross T.
      • et al.
      An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.
      However, HP system decontamination was shown to require more than 4-times longer to complete than conventional cleaning, thus resulting in prolonged bed turn-over time.
      • Otter J.A.
      • Puchowicz M.
      • Ryan D.
      • Salkeld J.A.
      • Copper T.A.
      • Havill N.L.
      • et al.
      Feasibility of routinely using hydrogen peroxide vapor to decontaminate rooms in a busy United States hospital.

      Comparison of UV irradiation versus HP for room decontamination

      The UV-C system and the systems that use HP have their own advantages and disadvantages (Table 4). The main advantage of both units is their ability to achieve substantial reductions in vegetative bacteria. As noted above, manual cleaning has been demonstrated to be suboptimal because many environmental surfaces are not cleaned. Another advantage is their ability to substantially reduce C difficile spores as low-level disinfectants (such as quaternary ammonium compounds) have only limited or no measurable activity against spore-forming bacteria. Both systems are residual free, and they decontaminate all exposed surfaces and equipment in the room.
      The major disadvantages of both decontamination systems are the substantial capital equipment costs; the need to remove personnel and patients from the room, thus limiting their use to terminal room disinfection (must prevent/minimize exposure to UV and HP); the staff time needed to transport the system to rooms to be decontaminated and monitor its use; and the need to physically clean the room of dust and debris. There are several important differences between the 2 systems. The UV-C system offers faster decontamination, which reduces the “down” time of the room before another patient can be admitted. A UV reflective wall coating reduced the time necessary to decontaminate a room using a UV-C emitting device from 25 minutes to 5 minutes for MRSA and from 44 minutes to 9 minutes for C difficile spores (Unpublished results, Rutala, Gergen, Tande, Weber, 2012). The HP systems have been demonstrated to be more effective in eliminating spore-forming organisms. Whether this improved sporicidal activity is clinically important is unclear because studies have demonstrated that, although environmental contamination is common in the rooms of patients with C difficile infection, the level of contamination is relatively low (also true for MRSA, VRE). Finally, the HP system was demonstrated to reduce C difficile incidence in a clinical study, whereas similar studies with the UV-C system have not been published.

      Conclusion

      Ample evidence exists that environmental contamination with important health care-associated pathogens (MRSA, VRE, Acinetobacter, norovirus, and Clostridium difficile) poses a risk for patient-to-patient transmission of these organisms. Multiple studies have demonstrated that environmental service workers frequently fail to decontaminate “high-risk” objects. Importantly, recent studies demonstrated that contact with the environment was just as likely to contaminate the hands of health care workers as was direct contact with the patient.
      • Stiefel 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.
      • Guerrero 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.
      Whereas an intervention bundle can improve cleaning by environmental service workers, it still remains suboptimal with many objects and surfaces not cleaned. Furthermore, the ability to achieve high rates of cleaning long-term has not been demonstrated. Although “no touch” room decontamination systems might aid in reducing/eliminating environmental contamination after terminal room disinfection, we still need to develop new practices or technologies to improve the thoroughness of daily room cleaning (eg, tinted germicides that color surfaces when applied, but the color disappears once it dries). Finally, cost-effectiveness analysis of these no-touch methods should be performed.
      There is now ample evidence that “no touch” systems such as UV-C or HP can reduce environmental contamination with health care-associated pathogens. However, each specific system should be studied and their efficacy demonstrated (similar to systems in Table 2) before introduction into health care facilities. Importantly, only a single study that used a before-after design has been published, which demonstrates that such a system can reduce health care-associated infections. Additional studies assessing the effectiveness of “no touch” room decontamination systems are needed to further assess the benefits of these technologies. In addition, cost-effectiveness studies would be useful in aiding selection among the different room decontamination technologies and specific systems. Last, if additional studies continue to demonstrate benefit, widespread adoption of these technologies (eg, a supplemental intervention during outbreaks, after discharge of patients on Contact Precautions, on a regular basis in special rooms [eg, operating rooms]) should be considered for terminal room disinfection in health care facilities.

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