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The role of ‘no-touch’ automated room disinfection systems in infection prevention and control

  • J.A. Otter
    Correspondence
    Corresponding author. Address: Bioquell UK Ltd, 52 Royce Close, West Portway, Andover, Hampshire SP10 3TS, UK. Tel.: +44 (0) 1264 835835; fax: +44 (0) 1264 835917.
    Affiliations
    Centre for Clinical Infection and Diagnostics Research (CIDR), Department of Infectious Diseases, King's College London, School of Medicine and Guy's and St Thomas' NHS Foundation Trust, UK

    Bioquell UK Ltd, Andover, Hampshire, UK
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  • S. Yezli
    Affiliations
    Bioquell UK Ltd, Andover, Hampshire, UK
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  • T.M. Perl
    Affiliations
    Division of Infectious Diseases, Department of Medicine, Johns Hopkins University, School of Medicine, Baltimore, MD, USA

    Department of Hospital Epidemiology and Infection Control, The Johns Hopkins Hospital, Baltimore, MD, USA
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  • F. Barbut
    Affiliations
    Infection Control Unit, Hôpital Saint Antoine, Assistance Publique-Hôpitaux de Paris, France
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  • G.L. French
    Affiliations
    Centre for Clinical Infection and Diagnostics Research (CIDR), Department of Infectious Diseases, King's College London, School of Medicine and Guy's and St Thomas' NHS Foundation Trust, UK
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Published:November 29, 2012DOI:https://doi.org/10.1016/j.jhin.2012.10.002

      Summary

      Background

      Surface contamination in hospitals is involved in the transmission of pathogens in a proportion of healthcare-associated infections. Admission to a room previously occupied by a patient colonized or infected with certain nosocomial pathogens increases the risk of acquisition by subsequent occupants; thus, there is a need to improve terminal disinfection of these patient rooms. Conventional disinfection methods may be limited by reliance on the operator to ensure appropriate selection, formulation, distribution and contact time of the agent. These problems can be reduced by the use of ‘no-touch’ automated room disinfection (NTD) systems.

      Aim

      To summarize published data related to NTD systems.

      Methods

      Pubmed searches for relevant articles.

      Findings

      A number of NTD systems have emerged, which remove or reduce reliance on the operator to ensure distribution, contact time and process repeatability, and aim to improve the level of disinfection and thus mitigate the increased risk from the prior room occupant. Available NTD systems include hydrogen peroxide (H2O2) vapour systems, aerosolized hydrogen peroxide (aHP) and ultraviolet radiation. These systems have important differences in their active agent, delivery mechanism, efficacy, process time and ease of use. Typically, there is a trade-off between time and effectiveness among NTD systems. The choice of NTD system should be influenced by the intended application, the evidence base for effectiveness, practicalities of implementation and cost constraints.

      Conclusion

      NTD systems are gaining acceptance as a useful tool for infection prevention and control.

      Keywords

      Introduction

      Contaminated surfaces have been underestimated as a source from which nosocomial transmission can occur.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
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      • Alvarado C.J.
      • Hassemer C.A.
      • Zilz M.A.
      Relation of the inanimate hospital environment to endemic nosocomial infection.
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      • 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.
      Recent studies show that admission to a room previously occupied by a patient with Clostridium difficile, vancomycin-resistant enterococci (VRE), meticillin-resistant Staphylococcus aureus (MRSA), Acinetobacter baumannii and Pseudomonas aeruginosa increases the risk of acquiring these pathogens for subsequent occupants of the same room by a factor of two or more.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestel D.D.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      • Huang S.S.
      • Datta R.
      • Platt R.
      Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
      • Drees M.
      • Snydman D.
      • Schmid C.
      • et al.
      Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci.
      • Nseir S.
      • Blazejewski C.
      • Lubret R.
      • Wallet F.
      • Courcol R.
      • Durocher A.
      Risk of acquiring multidrug-resistant Gram-negative bacilli from prior room occupants in the ICU.
      In these circumstances, current terminal cleaning and disinfection following the discharge of patients with these pathogens is inadequate and needs to be improved. The emergence of the 027/NAP1 epidemic strain of C. difficile and potentially untreatable multidrug-resistant Gram-negative bacteria that can also survive on surfaces is a further reason to improve environmental decontamination.
      • Peleg A.Y.
      • Hooper D.C.
      Hospital-acquired infections due to gram-negative bacteria.
      • Dubberke E.R.
      • Reske K.A.
      • Noble-Wang J.
      • et al.
      Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities.
      Effective cleaning and disinfection using conventional methods relies on a human operator to correctly select and formulate an appropriate agent and distribute the agent to all target surfaces for the necessary contact time. Improvement of these conventional methods depends on modification of human behaviour, which is often difficult. The use of novel ‘no-touch’ automated room disinfection (NTD) systems provides an alternative approach, which removes or reduces reliance on the operator.
      • 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.
      • 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.
      • Byrns G.
      • Fuller T.P.
      The risks and benefits of chemical fumigation in the health care environment.
      Automated systems have been adopted widely in other areas of healthcare to remove human error. Examples include robotic surgery and many aspects of critical care such as ventilators. Indeed, commenting on the future of infection control in the late 1990s, Dr Robert Weinstein wrote: ‘Given the choice of improving technology or improving human behavior, technology is the better choice.
      • Weinstein R.A.
      Nosocomial infection update.
      Despite the relatively recent attention, the concept of NTD is not new. A paper was published in 1901 advising on how to disinfect a ‘sick-room’ through gaseous formaldehyde.
      • Riddle M.M.
      The disinfection of sick-rooms and their contents.
      In the 1960s, formaldehyde was replaced by aerosolized chemicals such as quaternary ammonium compounds and phenolics due to concerns over toxicity.
      • Friedman H.
      • Volin E.
      • Laumann D.
      Terminal disinfection in hospitals with quaternary ammonium compounds by use of a spray-fog technique.
      • Ostrander W.E.
      • Griffith L.J.
      Evaluation of disinfectants for hospital housekeeping use.
      • Munster A.M.
      • Ostrander W.E.
      Terminal disinfection of contaminated patient care areas: to fog or not to fog?.
      However, advice from the US Centers for Disease Control and Prevention (CDC) since the 1970s is that disinfectant fogging should not be performed routinely in patient-care areas.
      • Munster A.M.
      • Ostrander W.E.
      Terminal disinfection of contaminated patient care areas: to fog or not to fog?.

      Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee (HICPAC). Guideline for disinfection and sterilization in healthcare facilities. 2008.

      The emergence of several new NTD systems based on either H2O2 or ultraviolet (UV) radiation and the increasing recognition of the importance of environmental contamination in transmission suggests that this recommendation should be re-evaluated.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      This review presents evidence for the need to improve or augment conventional cleaning and disinfection; considers the targets for hospital disinfection and when use of an NTD system may be appropriate; summarizes and compares evidence relating to the various NTD systems; and discusses the role of regulators and professional societies in guiding evidence-based adoption.

      What level of surface contamination is a risk for transmission?

      The relationship between the level of residual surface contamination after disinfection and the risk of transmission has not been studied in detail. It depends on various factors, including the characteristics of the organism involved, patient susceptibility and staff compliance with infection control policies (for example hand hygiene following contact with environmental surfaces).
      • Hayden 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.
      • 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.
      • Kramer A.
      • Schwebke I.
      • Kampf G.
      How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
      The fact that subsequent occupants of a room vacated by a previously colonized or infected patient are at an increased risk of infection indicates that conventional terminal disinfection does not reduce contamination sufficiently to prevent all transmission in these cases.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestel D.D.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.
      • Huang S.S.
      • Datta R.
      • Platt R.
      Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
      • Drees M.
      • Snydman D.
      • Schmid C.
      • et al.
      Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci.
      • Nseir S.
      • Blazejewski C.
      • Lubret R.
      • Wallet F.
      • Courcol R.
      • Durocher A.
      Risk of acquiring multidrug-resistant Gram-negative bacilli from prior room occupants in the ICU.
      There is some evidence that the extent to which transmission is interrupted is proportional to the level of surface contamination. For example, Lawley et al. used an in vitro mouse model to show that the degree to which transmission of C. difficile was blocked correlated with the log10 reduction of the various disinfectants tested.
      • Lawley T.D.
      • Clare S.
      • Deakin L.J.
      • et al.
      Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.
      The degree of shedding and the infective dose can be used to guide the appropriate target for hospital cleaning and disinfection. Certain pathogens such as C. difficile and norovirus can be shed into the environment in high numbers and have a low infectious dose.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      • Larson H.E.
      • Borriello S.P.
      Quantitative study of antibiotic-induced susceptibility to Clostridium difficile enterocecitis in hamsters.
      • Yezli S.
      • Otter J.A.
      Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment.
      For example, stool concentrations of norovirus can reach >1 × 1012 particles per gram and up to 105 virus norovirus particles per 30 cm2 have been identified on hospital surfaces, whereas the infectious dose is 1–100 particles.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      • Yezli S.
      • Otter J.A.
      Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment.
      • Morter S.
      • Bennet G.
      • Fish J.
      • et al.
      Norovirus in the hospital setting: virus introduction and spread within the hospital environment.
      Therefore, the presence of a pathogen on a surface at any concentration may be a risk for transmission. This is reflected in proposed guidelines for microbiological hygiene standards and recent discussion surrounding the intended target for hospital disinfection.
      • Dancer S.J.
      How do we assess hospital cleaning? A proposal for microbiological standards for surface hygiene in hospitals.
      • Walder M.
      • Holmdahl T.
      Reply to Roberts.
      • Roberts C.G.
      Hydrogen peroxide vapor and aerosol room decontamination systems.
      However, in practice, a risk-based approach must be used when setting a target for an acceptable level of residual contamination, balancing patient safety with practicality and cost, as is the case when selecting liquid disinfectants. More stringent targets should be set when the risk and/or consequences of infection are high, for example, for virulent, resistant and/or highly infectious pathogens, especially in high-risk settings with immunocompromised patients; a lower standard may be acceptable in lower-risk settings.
      • Dancer S.J.
      How do we assess hospital cleaning? A proposal for microbiological standards for surface hygiene in hospitals.
      • Walder M.
      • Holmdahl T.
      Reply to Roberts.
      • Roberts C.G.
      Hydrogen peroxide vapor and aerosol room decontamination systems.

      Limitations of conventional cleaning and disinfection

      Conventional cleaning and disinfection is performed by a human operator with liquid detergents or disinfectants. Microbiological studies indicate that conventional cleaning and disinfection without programmes of targeted improvement rarely eradicate pathogens from surfaces.
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.
      • 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.
      • Byers K.E.
      • Durbin L.J.
      • Simonton B.M.
      • Anglim A.M.
      • Adal K.A.
      • Farr B.M.
      Disinfection of hospital rooms contaminated with vancomycin-resistant Enterococcus faecium.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      • 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.
      Problems associated with both ‘product’ and ‘procedure’ contribute to this (Box 1), in particular, the reliance on the operator to repeatedly ensure adequate selection, formulation, distribution and contact time of the agent. For example, a large assessment of conventional cleaning in 36 acute hospitals using fluorescent markers revealed that less than 50% of high-risk objects in hospital rooms were cleaned at patient discharge.
      • Carling P.C.
      • Parry M.M.
      • Rupp M.E.
      • Po J.L.
      • Dick B.
      • Von Beheren S.
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
      Modifying human behaviour is difficult but several different approaches can be taken, including routine microbiological analysis of surface hygiene, the use of fluorescent markers or ATP assays to assess the thoroughness of cleaning, feedback of cleaning performance and educational campaigns.
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      • Dancer S.J.
      How do we assess hospital cleaning? A proposal for microbiological standards for surface hygiene in hospitals.
      • Carling P.C.
      • Parry M.M.
      • Rupp M.E.
      • Po J.L.
      • Dick B.
      • Von Beheren S.
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
      • Mulvey D.
      • Redding P.
      • Robertson C.
      • et al.
      Finding a benchmark for monitoring hospital cleanliness.
      • Boyce J.M.
      • Havill N.L.
      • Dumigan D.G.
      • Golebiewski M.
      • Balogun O.
      • Rizvani R.
      Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay.
      Monitoring and feedback can improve the frequency of surfaces that are cleaned and reduce the level of environmental contamination and there is some evidence that improving the efficacy of conventional cleaning/disinfection can reduce the acquisition of pathogens.
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      • Carling P.C.
      • Parry M.M.
      • Rupp M.E.
      • Po J.L.
      • Dick B.
      • Von Beheren S.
      Improving cleaning of the environment surrounding patients in 36 acute care hospitals.
      • Carling P.C.
      • Briggs J.L.
      • Perkins J.
      • Highlander D.
      Improved cleaning of patient rooms using a new targeting method.
      • 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.
      • et al.
      Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
      • Dancer S.J.
      • White L.F.
      • Lamb J.
      • Girvan E.K.
      • Robertson C.
      Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
      • Hayden 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.
      However, no studies have evaluated the sustainability of such systematic improvements. Indeed, recent evidence indicates that altering the location of fluorescent dye spots reduced the proportion of objects that were cleaned from 90% to approximately 60%.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      In situations where the elimination of pathogens is required, even systematic improvement of conventional cleaning and disinfection may not be sufficient. Multiple rounds of disinfection with sodium hypochlorite (bleach) taking many hours, risking damage to materials and presenting health risks for operators may have limited success in removing environmental reservoirs of pathogens.
      • Morter S.
      • Bennet G.
      • Fish J.
      • et al.
      Norovirus in the hospital setting: virus introduction and spread within the hospital environment.
      • Byers K.E.
      • Durbin L.J.
      • Simonton B.M.
      • Anglim A.M.
      • Adal K.A.
      • Farr B.M.
      Disinfection of hospital rooms contaminated with vancomycin-resistant Enterococcus faecium.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      • Dettenkofer M.
      • Block C.
      Hospital disinfection: efficacy and safety issues.
      • McGowan M.J.
      • Shimoda L.M.
      • Woolsey G.D.
      Effects of sodium hypochlorite on denture base metals during immersion for short-term sterilization.
      • Mirabelli M.C.
      • Zock J.P.
      • Plana E.
      • et al.
      Occupational risk factors for asthma among nurses and related healthcare professionals in an international study.
      NTD systems offer the potential to overcome some of these problems.
      • Davies A.
      • Pottage T.
      • Bennett A.
      • Walker J.
      Gaseous and air decontamination technologies for Clostridium difficile in the healthcare environment.
      • 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.
      • Byrns G.
      • Fuller T.P.
      The risks and benefits of chemical fumigation in the health care environment.

      When to consider an NTD system

      Notwithstanding current CDC guidelines recommending against routine ‘disinfectant fogging’ in patient-care areas, the use of an NTD system may be warranted in some circumstances based on current data.

      Rutala WA, Weber DJ, Healthcare Infection Control Practices Advisory Committee (HICPAC). Guideline for disinfection and sterilization in healthcare facilities. 2008.

      Figure 1 outlines a hierarchical approach to hospital disinfection, identifying areas where NTD systems may be appropriate, and Table I highlights specific scenarios where various NTD systems may be considered. The strongest reason for considering an NTD system is to prevent environment-borne transmission by improving terminal disinfection of clinical areas after infected or colonized patients have been discharged (Figure 1).
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      This has been performed in endemic settings or during outbreaks (Table I).
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      • 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.
      • 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.
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward.

      Kaiser M, Elemendorf S, Kent D, Evans A, Harrington SM, McKenna D. Management of a multi-year MDR Acinetobacter baumannii outbreak in the ICU setting. Infectious Diseases Society of America (IDSA) Annual Meeting. Abstract 394. 2011.

      • Otter J.A.
      • Yezli S.
      • Schouten M.A.
      • van Zanten A.R.
      • Houmes-Zielman G.
      • Nohlmans-Paulssen M.K.
      Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.
      • Ray A.
      • Perez F.
      • Beltramini A.M.
      • et al.
      Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital.
      • Bates C.J.
      • Pearse R.
      Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit.
      Whereas the disinfection of single rooms is more common, NTD systems have been used to disinfect multi-occupancy areas.
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      • 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.
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward.
      • Otter J.A.
      • Yezli S.
      • Schouten M.A.
      • van Zanten A.R.
      • Houmes-Zielman G.
      • Nohlmans-Paulssen M.K.
      Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.
      • Bates C.J.
      • Pearse R.
      Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit.
      Figure thumbnail gr1
      Figure 1Proposed approach for a disinfection decision diagram. aKey pathogens associated with contamination of the environment include C. difficile, vancomycin-resistant enterococcus, meticillin-resistant S. aureus, A. baumannii, P. aeruginosa and norovirus. bFor detailed scenarios when a ‘no-touch’ automated room disinfection (NTD) system may be considered (). All NTD systems are applied after a cleaning step to ensure that surfaces are free from visible contamination, which is unacceptable to subsequent patients and will reduce the efficacy of the NTD disinfection. cThere is limited equivocal evidence that enhanced cleaning/disinfection in a low-risk general ward setting can reduce the spread of pathogens.
      • 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.
      • Dancer S.J.
      • White L.F.
      • Lamb J.
      • Girvan E.K.
      • Robertson C.
      Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
      • Mayfield J.L.
      • Leet T.
      • Miller J.
      • Mundy L.M.
      Environmental control to reduce transmission of Clostridium difficile.
      ICU, intensive care unit.
      Table IDetailed scenarios for when to consider a ‘no-touch’ automated room disinfection (NTD) system for terminal disinfection of clinical areas used by patients infected or colonized with pathogens associated with transmission from the environment
      ScenarioDisinfection method
      Single roomMulti-occupancy areaLow-risk settings (e.g. general ward)High-risk setting (e.g. ICU)Low-risk environmental–pathogenic characteristics (e.g. VRE/MRSA)
      The risk associated with individual pathogens in the context of disinfection will depend on a number of factors, including the importance of environmental contamination in transmission, clinical implications, local epidemiology and financial outcomes. For example, a multidrug-resistant Gram-negative rod causing an outbreak would be considered a ‘high-risk’ pathogen, whereas VRE colonization would be considered lower risk.
      High-risk environmental–pathogenic characteristics (e.g. C. difficile)
      The risk associated with individual pathogens in the context of disinfection will depend on a number of factors, including the importance of environmental contamination in transmission, clinical implications, local epidemiology and financial outcomes. For example, a multidrug-resistant Gram-negative rod causing an outbreak would be considered a ‘high-risk’ pathogen, whereas VRE colonization would be considered lower risk.
      Standard cleaning and disinfectionEnhanced cleaning and disinfectionNTD
      A cleaning step to ensure that surfaces are free from visible contamination is required before all NTD systems to make the area aesthetically acceptable to the next occupant, and increase the efficacy of NTD disinfection.
      No
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.
      • 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.
      • 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.
      Yes
      • Dancer S.J.
      • White L.F.
      • Lamb J.
      • Girvan E.K.
      • Robertson C.
      Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
      • Mahamat A.
      • MacKenzie F.M.
      • Brooker K.
      • Monnet D.L.
      • Daures J.P.
      • Gould I.M.
      Impact of infection control interventions and antibiotic use on hospital MRSA: a multivariate interrupted time-series analysis.
      UVC
      • 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      No
      • 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.
      • Verity P.
      • Wilcox M.H.
      • Fawley W.
      • Parnell P.
      Prospective evaluation of environmental contamination by Clostridium difficile in isolation side rooms.
      Yes
      • 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.
      • Mayfield J.L.
      • Leet T.
      • Miller J.
      • Mundy L.M.
      Environmental control to reduce transmission of Clostridium difficile.
      UVC
      • 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.
      /aHP
      • 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.
      /H2O2 vapour
      • 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.
      No
      • 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.
      • Hayden 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.
      Yes
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      • Hayden 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.
      UVC
      • 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.
      /aHP
      • Bartels M.D.
      • Kristoffersen K.
      • Slotsbjerg T.
      • Rohde S.M.
      • Lundgren B.
      • Westh H.
      Environmental meticillin-resistant Staphylococcus aureus (MRSA) disinfection using dry-mist-generated hydrogen peroxide.
      /H2O2 vapour
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.
      • 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.
      No
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestel D.D.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      No
      • Morter S.
      • Bennet G.
      • Fish J.
      • et al.
      Norovirus in the hospital setting: virus introduction and spread within the hospital environment.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      H2O2 vapour
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      • 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.
      No
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.
      • 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.
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward.
      Yes
      • Dancer S.J.
      • White L.F.
      • Lamb J.
      • Girvan E.K.
      • Robertson C.
      Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study.
      • Mahamat A.
      • MacKenzie F.M.
      • Brooker K.
      • Monnet D.L.
      • Daures J.P.
      • Gould I.M.
      Impact of infection control interventions and antibiotic use on hospital MRSA: a multivariate interrupted time-series analysis.
      No
      The use of an NTD system to disinfect multi-occupancy areas may not be warranted in a low-risk setting due to the requirement to block beds.
      ,
      • Otter J.A.
      • Puchowicz M.
      • Ryan D.
      • et al.
      Feasibility of routinely using hydrogen peroxide vapor to decontaminate rooms in a busy United States hospital.
      No
      • 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.
      • Hayden 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.
      Yes
      • 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.
      • Mayfield J.L.
      • Leet T.
      • Miller J.
      • Mundy L.M.
      Environmental control to reduce transmission of Clostridium difficile.
      aHP/H2O2 vapour
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward.
      No
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestel D.D.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      Unclear
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      • 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.
      H2O2 vapour
      • Otter J.A.
      • Yezli S.
      • Schouten M.A.
      • van Zanten A.R.
      • Houmes-Zielman G.
      • Nohlmans-Paulssen M.K.
      Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.
      ICU, intensive care unit; VRE, vancomycin-resistant enterococcus; MRSA, meticillin-resistant Staphylococcus aureus; UVC, ultraviolet C spectrum; aHP, aerosolized hydrogen peroxide.
      ‘Yes’, method is appropriate based on current data; ‘No’, method is inappropriate based on current data.
      a The risk associated with individual pathogens in the context of disinfection will depend on a number of factors, including the importance of environmental contamination in transmission, clinical implications, local epidemiology and financial outcomes. For example, a multidrug-resistant Gram-negative rod causing an outbreak would be considered a ‘high-risk’ pathogen, whereas VRE colonization would be considered lower risk.
      b A cleaning step to ensure that surfaces are free from visible contamination is required before all NTD systems to make the area aesthetically acceptable to the next occupant, and increase the efficacy of NTD disinfection.
      c The use of an NTD system to disinfect multi-occupancy areas may not be warranted in a low-risk setting due to the requirement to block beds.
      Conversely, NTD systems are not suitable for performing daily disinfection before patients are discharged due to the need for temporary relocation of the patient. Thus, concerns about recontamination by the room occupant after the NTD intervention are not well placed when considering terminal disinfection because although this recontamination may lead to some indirect infection, it does not prevent the chain of infection between consecutive occupants of the same room being broken.
      • Drees M.
      • Snydman D.
      • Schmid C.
      • et al.
      Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci.
      • Hayden 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.
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.
      • 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.
      • Hardy K.J.
      • Gossain S.
      • Henderson N.
      • et al.
      Rapid recontamination with MRSA of the environment of an intensive care unit after decontamination with hydrogen peroxide vapour.
      • 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.
      • 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.
      Other potential applications of NTD systems include the removal of environmental pathogens disturbed during building works such as Aspergillus fumigatus, as part of emergency preparedness planning, the disinfection of mobile medical equipment in a dedicated facility, and decontamination of emergency vehicles or operating theatres.
      • Vonberg R.P.
      • Gastmeier P.
      Nosocomial aspergillosis in outbreak settings.
      • 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.
      • van't Veen A.
      • van der Zee A.
      • Nelson J.
      • Speelberg B.
      • Kluytmans J.A.
      • Buiting A.G.
      Outbreak of infection with a multiresistant Klebsiella pneumoniae strain associated with contaminated roll boards in operating rooms.
      Due to the potential for mobile medical equipment, such as blood pressure cuffs and mobile computers to become contaminated, combined with the challenge of disinfecting them effectively, the feasibility and effectiveness of NTD systems for disinfecting these items should be prioritized for evaluation.
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward.
      • Boyce J.M.
      • Potter-Bynoe G.
      • Chenevert C.
      • King T.
      Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications.
      • Dumford III, D.M.
      • Nerandzic M.M.
      • Eckstein B.C.
      • Donskey C.J.
      What is on that keyboard? Detecting hidden environmental reservoirs of Clostridium difficile during an outbreak associated with North American pulsed-field gel electrophoresis type 1 strains.

      Overview of NTD systems

      Several different types of NTD system are currently used in clinical healthcare settings, the most common being aerosolized hydrogen peroxide (aHP) systems (such as ASP Glosair, previously Sterinis, Steris Biogienie and Oxypharm Nocospray), H2O2 vapour systems (such as the Bioquell and Steris systems), and ultraviolet C radiation (UVC) systems (such as Lumalier Tru-D).
      • 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.
      • 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.
      • Boyce J.M.
      New approaches to decontamination of rooms after patients are discharged.
      • Orlando P.
      • Cristina M.L.
      • Dallera M.
      • Ottria G.
      • Vitale A.
      • Badolati G.
      Surface disinfection: evaluation of the efficacy of a nebulization system spraying hydrogen peroxide.
      The different characteristics of these three system types are summarized in Table II. A fourth class of NTD system based on pulsed-xenon UV (PX-UV) radiation has emerged relatively recently and with a limited literature so far.
      • Stibich M.
      • Stachowiak J.
      • Tanner B.
      • et al.
      Evaluation of a pulsed-xenon ultraviolet room disinfection device for impact on hospital operations and microbial reduction.
      Table IISummary of frequently used ‘no-touch’ automated room disinfection (NTD) systems
      Aerosolized hydrogen peroxide (aHP)H2O2 vapourUltraviolet C (UVC) radiation
      ProductsASP Glosair (previously Sterinis)
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.


      Oxypharm Nocospray
      • Chan H.T.
      • White P.
      • Sheorey H.
      • Cocks J.
      • Waters M.J.
      Evaluation of the biological efficacy of hydrogen peroxide vapour decontamination in wards of an Australian hospital.
      Bioquell HPV systems
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.


      Steris VHP systems
      • Ray A.
      • Perez F.
      • Beltramini A.M.
      • et al.
      Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital.
      Lumalier Tru-D
      • 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.
      AbbreviationaHP/‘dry mist’ HP (DMHP)
      • Otter J.A.
      • Yezli S.
      A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.
      • Andersen B.M.
      • Syversen G.
      • Thoresen H.
      • et al.
      Failure of dry mist of hydrogen peroxide 5% to kill Mycobacterium tuberculosis.
      HPV
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      /VHP
      • Ray A.
      • Perez F.
      • Beltramini A.M.
      • et al.
      Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital.
      UVC
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      Active solution5–6% H2O2, <50 ppm Ag cations
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      30–35% H2O2UVC, 254 nm
      ApplicationAerosol of active solutionVapour, either condensing (Bioquell HPV) or non-condensing (Steris VHP)Radiation
      DistributionNon-homogeneous distribution
      • Orlando P.
      • Cristina M.L.
      • Dallera M.
      • Ottria G.
      • Vitale A.
      • Badolati G.
      Surface disinfection: evaluation of the efficacy of a nebulization system spraying hydrogen peroxide.
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      Homogeneous
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      Affected by line of sight
      • 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      Particle size8–10 μm (ASP Glosair)
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      • Andersen B.M.
      • Rasch M.
      • Hochlin K.
      • Jensen F.H.
      • Wismar P.
      • Fredriksen J.E.
      Decontamination of rooms, medical equipment and ambulances using an aerosol of hydrogen peroxide disinfectant.


      0.5 μm (Oxypharm Nocospray)
      • Orlando P.
      • Cristina M.L.
      • Dallera M.
      • Ottria G.
      • Vitale A.
      • Badolati G.
      Surface disinfection: evaluation of the efficacy of a nebulization system spraying hydrogen peroxide.
      Vapour phaseN/A
      Process time (single occupancy room)2–3 h
      • 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.
      • Andersen B.M.
      • Rasch M.
      • Hochlin K.
      • Jensen F.H.
      • Wismar P.
      • Fredriksen J.E.
      Decontamination of rooms, medical equipment and ambulances using an aerosol of hydrogen peroxide disinfectant.
      1.5–2.5 h (HPV)
      • 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.
      • Barbut F.
      • Yezli S.
      • Otter J.A.
      Activity in vitro of hydrogen peroxide vapour against Clostridium difficile spores.

      Department of Health, NHS Purchasing and Supply Agency (UK). HCAI Technology Innovation Programme. Showcase Hospitals Report Number 3. The Bioquell Hydrogen Peroxide Vapour (HPV) Disinfection System. 2009.

      • Otter J.A.
      • Yezli S.
      Cycle times for hydrogen peroxide vapour decontamination.


      8 h (VHP)
      • Ray A.
      • Perez F.
      • Beltramini A.M.
      • et al.
      Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital.
      15 min (vegetative setting)
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.


      1–1.5 h (spore setting)
      • Boyce J.M.
      • Havill N.L.
      • Moore B.A.
      Terminal decontamination of patient rooms using an automated mobile UV light unit.
      • 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.
      Required health and safety measuresAir vents and doors isolated; active monitoring with a hand-held sensor necessary to check for leaks and ensure room is safe to re-enter.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      • Beswick A.J.
      • Farrant J.
      • Makison C.
      • et al.
      Comparison of multiple systems for laboratory whole room fumigation.
      Air vents and doors isolated; active monitoring with a hand-held sensor necessary to check for leaks and ensure room is safe to re-enter.
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.
      • 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.
      • 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.
      Air vents and doors not isolated. No requirement for active monitoring or testing to ensure room is safe to re-enter.
      Aeration (removal of active solution from enclosure)Passive decompositionActive catalytic conversionNot required
      Sporicidal efficacyIncomplete inactivation in situ
      • 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.
      • 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.
      ; ∼4-log10 reduction of C. difficile in vitro; limited ability to inactivate 6-log10 BIs
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      • Andersen B.M.
      • Rasch M.
      • Hochlin K.
      • Jensen F.H.
      • Wismar P.
      • Fredriksen J.E.
      Decontamination of rooms, medical equipment and ambulances using an aerosol of hydrogen peroxide disinfectant.
      Complete inactivation in situ
      • 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.
      ; >6-log10 reduction of C. difficile in vitro
      • Otter J.A.
      • French G.L.
      Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor.
      ; routinely validated using 6-log10 BIs
      • 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.
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      No studies in situ. 1–4-log10 reduction in vitro depending on line of sight
      • 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      ; does not inactivate 6-log10 BIs
      • 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.
      Tuberculocidal efficacyUnclear
      • Beswick A.J.
      • Farrant J.
      • Makison C.
      • et al.
      Comparison of multiple systems for laboratory whole room fumigation.
      • Andersen B.M.
      • Syversen G.
      • Thoresen H.
      • et al.
      Failure of dry mist of hydrogen peroxide 5% to kill Mycobacterium tuberculosis.
      • Andersen B.M.
      Does ‘airborne’ hydrogen peroxide kill Mycobacterium tuberculosis?.
      • Grare M.
      • Dailloux M.
      • Simon L.
      • Dimajo P.
      • Laurain C.
      Efficacy of dry mist of hydrogen peroxide (DMHP) against Mycobacterium tuberculosis and use of DMHP for routine decontamination of biosafety level 3 laboratories.
      Yes
      • Beswick A.J.
      • Farrant J.
      • Makison C.
      • et al.
      Comparison of multiple systems for laboratory whole room fumigation.
      • 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.
      • Kahnert A.
      • Seiler P.
      • Stein M.
      • Aze B.
      • McDonnell G.
      • Kaufmann S.H.
      Decontamination with vaporized hydrogen peroxide is effective against Mycobacterium tuberculosis.
      Unclear
      UK Rapid Review Panel Recommendation3: ‘A potentially useful new concept but insufficiently validated; more research and development is required before it is ready for evaluation in practice.’1: ‘Basic research and development, validation and recent in-use evaluations have shown benefits that should be available to NHS bodies to include as appropriate in their cleaning, hygiene or infection control protocols.’ (HPV)None
      EPA registrationUnknownSterilantUnknown
      Evidence of clinical impactNone publishedSignificant reduction in the incidence of C. difficile and VRE. (HPV)
      • 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.

      Manian FA, Griesenauer S, Senkel D. Impact of an intensive terminal cleaning and disinfection (C/D) protocol involving selected hospital rooms on endemic nosocomial infection (NI) rates of common pathogens at a tertiary care medical center. 5th Decennial Meeting of the Society for Healthcare Epidemiology of America (SHEA), Atlanta, GA, USA. Abstract LB6. 2010.

      • 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.


      Removal of environmental reservoirs during outbreaks.
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward.
      • Otter J.A.
      • Yezli S.
      • Schouten M.A.
      • van Zanten A.R.
      • Houmes-Zielman G.
      • Nohlmans-Paulssen M.K.
      Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.
      • Bates C.J.
      • Pearse R.
      Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit.

      Otter JA, Davies B, Klein J, Watts TL, Kearns AM, French GL. Identification and control of an outbreak of gentamicin-resistant, methicillin-susceptible Staphylococcus aureus on a neonatal unit. 13th International Symposium on Staphylococci and Staphylococcal Infection (ISSSI), Cairns, Australia, 2008.

      Short duration study indicating a reduction in CDI associated with UVC.
      • Pettis A.M.
      Elimination of Clostridium difficile infections (CDI) by illumination? Surface disinfection by ultraviolet light treatment.
      N/A, not applicable; BI, biological indicator; NHS, National Health Service (UK); EPA, Environmental Protection Agency (USA); VRE, vancomycin-resistant enterococcus; CDI, Clostridium difficile infection.

      Aerosolized hydrogen peroxide

      Technology description

      Aerosolized H2O2 systems deliver a pressure-generated aerosol. The systems employed most frequently in healthcare use a solution containing 5–6% H2O2 and <50 ppm silver.
      • Orlando P.
      • Cristina M.L.
      • Dallera M.
      • Ottria G.
      • Vitale A.
      • Badolati G.
      Surface disinfection: evaluation of the efficacy of a nebulization system spraying hydrogen peroxide.
      • Otter J.A.
      • Havill N.L.
      • Boyce J.M.
      Hydrogen peroxide vapor is not the same as aerosolized hydrogen peroxide.
      • Otter J.A.
      • Yezli S.
      A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.
      • 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.
      • Chan H.T.
      • White P.
      • Sheorey H.
      • Cocks J.
      • Waters M.J.
      Evaluation of the biological efficacy of hydrogen peroxide vapour decontamination in wards of an Australian hospital.
      Aerosolized droplets are introduced into an enclosure via a unidirectional nozzle.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      • Boyce J.M.
      New approaches to decontamination of rooms after patients are discharged.
      One manufacturer (ASP Glosair) states a particle size of 8–10 μm whereas another manufacturer (Oxypharm Nocospray) states a smaller particle size of 0.5 μm.
      • Orlando P.
      • Cristina M.L.
      • Dallera M.
      • Ottria G.
      • Vitale A.
      • Badolati G.
      Surface disinfection: evaluation of the efficacy of a nebulization system spraying hydrogen peroxide.
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      The dose typically recommended for hospital rooms is 6 mL/m3, although multiple cycles of this dose have been used in several studies.
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      • Andersen B.M.
      • Rasch M.
      • Hochlin K.
      • Jensen F.H.
      • Wismar P.
      • Fredriksen J.E.
      Decontamination of rooms, medical equipment and ambulances using an aerosol of hydrogen peroxide disinfectant.
      Following exposure, the aerosol is left to decompose naturally without any active aeration system.

      Microbiological efficacy

      Aerosolized H2O2 systems have been shown to reduce contamination with C. difficile and MRSA on hospital surfaces.
      • Orlando P.
      • Cristina M.L.
      • Dallera M.
      • Ottria G.
      • Vitale A.
      • Badolati G.
      Surface disinfection: evaluation of the efficacy of a nebulization system spraying hydrogen peroxide.
      • 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.
      • Chan H.T.
      • White P.
      • Sheorey H.
      • Cocks J.
      • Waters M.J.
      Evaluation of the biological efficacy of hydrogen peroxide vapour decontamination in wards of an Australian hospital.
      • Bartels M.D.
      • Kristoffersen K.
      • Slotsbjerg T.
      • Rohde S.M.
      • Lundgren B.
      • Westh H.
      Environmental meticillin-resistant Staphylococcus aureus (MRSA) disinfection using dry-mist-generated hydrogen peroxide.
      • 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.
      However, aHP systems have not been shown to eradicate pathogens in clinical practice. For example, one or more positive C. difficile culture was collected from 20% of 15 and 50% of 10 rooms studied after an aHP process.
      • 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.
      • 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.
      One aHP system (ASP Glosair) achieves an ∼4-log10 reduction on C. difficile spores in vitro and has limited capacity to inactivate commercially produced 6-log10 spore biological indicators (BIs).
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      • Andersen B.M.
      • Rasch M.
      • Hochlin K.
      • Jensen F.H.
      • Wismar P.
      • Fredriksen J.E.
      Decontamination of rooms, medical equipment and ambulances using an aerosol of hydrogen peroxide disinfectant.
      • 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.
      The efficacy of aHP systems against catalase-positive bacteria remains to be firmly established, with conflicting published data on the level of inactivation of MRSA and A. baumannii and the tuberculocidal activity of aHP.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      • Piskin N.
      • Celebi G.
      • Kulah C.
      • Mengeloglu Z.
      • Yumusak M.
      Activity of a dry mist-generated hydrogen peroxide disinfection system against methicillin-resistant Staphylococcus aureus and Acinetobacter baumannii.
      • Beswick A.J.
      • Farrant J.
      • Makison C.
      • et al.
      Comparison of multiple systems for laboratory whole room fumigation.
      • Andersen B.M.
      • Syversen G.
      • Thoresen H.
      • et al.
      Failure of dry mist of hydrogen peroxide 5% to kill Mycobacterium tuberculosis.
      • Andersen B.M.
      Does ‘airborne’ hydrogen peroxide kill Mycobacterium tuberculosis?.
      • Grare M.
      • Dailloux M.
      • Simon L.
      • Dimajo P.
      • Laurain C.
      Efficacy of dry mist of hydrogen peroxide (DMHP) against Mycobacterium tuberculosis and use of DMHP for routine decontamination of biosafety level 3 laboratories.
      This is likely because catalase-positive bacteria are considerably less susceptible to the 5–6% H2O2 aerosol used by aHP systems than catalase-negative bacteria or metabolically inert spores.
      • Pottage T.
      • Macken S.
      • Walker J.T.
      • Bennett A.M.
      Meticillin-resistant Staphylococcus aureus is more resistant to vaporized hydrogen peroxide than commercial Geobacillus stearothermophilus biological indicators.
      • Otter J.A.
      • French G.L.
      Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor.

      Clinical impact

      There is no published evidence that disinfection with aHP systems reduces epidemic or endemic infection rates.

      Practical considerations

      Aerosolized H2O2 is straightforward to use compared with H2O2 vapour systems and relatively inexpensive compared with H2O2 vapour and UVC systems. The capacity of single units to decontaminate areas larger than single rooms is limited, so multiple generators may be necessary.
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      Doors and air vents should be sealed and hand-held health and safety monitors are required to ensure that no leakage occurs during cycles and to verify that the concentration of H2O2 inside the enclosure is below health and safety exposure limits before permitting patients or staff to enter the room.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      Reported cycle times are 3–4 h for multiple cycles and 2 h for single cycles.
      • 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.
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      • Bartels M.D.
      • Kristoffersen K.
      • Slotsbjerg T.
      • Rohde S.M.
      • Lundgren B.
      • Westh H.
      Environmental meticillin-resistant Staphylococcus aureus (MRSA) disinfection using dry-mist-generated hydrogen peroxide.
      However, cycle times for single rooms may be considerably longer when hand-held sensors are used to ensure that H2O2 concentrations are below health and safety limits prior to room re-entry.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      Some studies suggest that homogeneous distribution of the active agent is not achieved, perhaps because aHP is introduced via a unidirectional nozzle and the particles are affected by gravity, thus being more effective on lower horizontal surfaces.
      • 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.
      • Holmdahl T.
      • Lanbeck P.
      • Wullt M.
      • Walder M.H.
      A head-to-head comparison of hydrogen peroxide vapor and aerosol room decontamination systems.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      Sublethal exposure to H2O2 or silver could result in the development of tolerance or resistance.
      • McDonnell G.
      • Russell A.D.
      Antiseptics and disinfectants: activity, action, and resistance.
      • Meyer B.
      • Cookson B.
      Does microbial resistance or adaptation to biocides create a hazard in infection prevention and control?.
      • Chopra I.
      The increasing use of silver-based products as antimicrobial agents: a useful development or a cause for concern?.
      The potential for transferable resistance to silver is greater than for H2O2 due to plasmid-mediated silver resistance genes.
      • McDonnell G.
      • Russell A.D.
      Antiseptics and disinfectants: activity, action, and resistance.
      • Chopra I.
      The increasing use of silver-based products as antimicrobial agents: a useful development or a cause for concern?.
      Data are awaited confirming the compatibility of aHP systems with common hospital materials, including sensitive electronics. Finally, several studies have noted equipment reliability problems, which was a feature of older foggers.
      • Munster A.M.
      • Ostrander W.E.
      Terminal disinfection of contaminated patient care areas: to fog or not to fog?.
      • 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.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      • Beswick A.J.
      • Farrant J.
      • Makison C.
      • et al.
      Comparison of multiple systems for laboratory whole room fumigation.

      H2O2 vapour

      Technology description

      H2O2 vapour systems deliver a heat-generated vapour of 30–35% w/w aqueous H2O2 through a high velocity air stream to achieve homogeneous distribution throughout an enclosed area (enclosure).
      • Boyce J.M.
      New approaches to decontamination of rooms after patients are discharged.
      • Otter J.A.
      • Yezli S.
      A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.
      Two systems using H2O2 vapour are available commercially: Bioquell and Steris (Table II). Bioquell systems are usually termed hydrogen peroxide vapour (HPV) and Steris systems vaporized hydrogen peroxide (VHP). Bioquell HPV includes a generator to produce HPV, modules to measure the concentration of HPV, temperature and relative humidity in the enclosure and an aeration unit to catalyse the breakdown of HPV to oxygen and water vapour after HPV exposure. A control pedestal is situated outside the enclosure to provide remote control. Bioquell HPV is delivered until the air in the enclosure becomes saturated and H2O2 begins to condense on surfaces.
      • Ray A.
      • Perez F.
      • Beltramini A.M.
      • et al.
      Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital.
      • 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.
      Steris VHP systems have a generator inside the room with an integral aeration unit and dehumidifier required to achieve a set humidity level prior to the cycle commencement. The system is controlled remotely from outside the enclosure. Steris VHP systems deliver ‘non-condensing’ VHP by drying the vapour stream as it is returned to the generator. Bioquell systems do not control the H2O2 air concentration throughout the exposure period whereas the Steris systems hold a steady H2O2 air concentration throughout the exposure period.

      Microbiological efficacy

      Both Bioquell HPV and Steris VHP systems are US Environmental Protection Agency (EPA)-registered sterilants, which means that they have passed the AOAC sporicide test on porous and non-porous surfaces.
      • Humphreys P.N.
      Testing standards for sporicides.
      Both systems are associated with the eradication of pathogens from surfaces in situ and cycles are validated by >6-log10 reduction of Geobacillus stearothermophilus BI spores.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      • 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.
      • Otter J.A.
      • Yezli S.
      • Schouten M.A.
      • van Zanten A.R.
      • Houmes-Zielman G.
      • Nohlmans-Paulssen M.K.
      Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.
      • Ray A.
      • Perez F.
      • Beltramini A.M.
      • et al.
      Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital.
      • Bates C.J.
      • Pearse R.
      Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit.
      • Hardy K.J.
      • Gossain S.
      • Henderson N.
      • et al.
      Rapid recontamination with MRSA of the environment of an intensive care unit after decontamination with hydrogen peroxide vapour.

      Otter JA, Davies B, Klein J, Watts TL, Kearns AM, French GL. Identification and control of an outbreak of gentamicin-resistant, methicillin-susceptible Staphylococcus aureus on a neonatal unit. 13th International Symposium on Staphylococci and Staphylococcal Infection (ISSSI), Cairns, Australia, 2008.

      HPV and VHP are sporicidal, bactericidal, mycobactericidal and virucidal, achieving >6-log10 reduction against a wide range of nosocomial pathogens including C. difficile spores, MRSA, VRE, A. baumannii and norovirus surrogates, though efficacy may be reduced by high loading and the presence of organic soil.
      • Fu T.Y.
      • Gent P.
      • Kumar V.
      Efficacy, efficiency and safety aspects of hydrogen peroxide vapour and aerosolized hydrogen peroxide room disinfection systems.
      • Otter J.A.
      • French G.L.
      Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor.
      • 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.
      • Berrie E.
      • Andrews L.
      • Yezli S.
      • Otter J.A.
      Hydrogen peroxide vapour (HPV) inactivation of adenovirus.

      Goyal SM, Chander Y, Yezli S, Otter JA. Hydrogen peroxide vapor (HPV) inactivation of feline calicivirus, a surrogate for norovirus – an update. Infection Prevention Society Annual Meeting. 2011.

      • Pottage T.
      • Richardson C.
      • Parks S.
      • Walker J.T.
      • Bennett A.M.
      Evaluation of hydrogen peroxide gaseous disinfection systems to decontaminate viruses.
      • Barbut F.
      • Yezli S.
      • Otter J.A.
      Activity in vitro of hydrogen peroxide vapour against Clostridium difficile spores.
      • Bentley K.
      • Dove B.K.
      • Parks S.R.
      • Walker J.T.
      • Bennett A.M.
      Hydrogen peroxide vapour decontamination of surfaces artificially contaminated with norovirus surrogate feline calicivirus.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      Impact of the suspending medium on susceptibility of meticillin-resistant Staphylococcus aureus to hydrogen peroxide vapour decontamination.

      Clinical impact

      HPV has been used to remove environmental reservoirs during outbreaks of C. difficile, MRSA and meticillin-susceptible S. aureus (MSSA), resistant Gram-negatives and other pathogens.
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      • 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.
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward.

      Kaiser M, Elemendorf S, Kent D, Evans A, Harrington SM, McKenna D. Management of a multi-year MDR Acinetobacter baumannii outbreak in the ICU setting. Infectious Diseases Society of America (IDSA) Annual Meeting. Abstract 394. 2011.

      • Otter J.A.
      • Yezli S.
      • Schouten M.A.
      • van Zanten A.R.
      • Houmes-Zielman G.
      • Nohlmans-Paulssen M.K.
      Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.
      • Bates C.J.
      • Pearse R.
      Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit.
      • 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.

      Otter JA, Davies B, Klein J, Watts TL, Kearns AM, French GL. Identification and control of an outbreak of gentamicin-resistant, methicillin-susceptible Staphylococcus aureus on a neonatal unit. 13th International Symposium on Staphylococci and Staphylococcal Infection (ISSSI), Cairns, Australia, 2008.

      VHP has been used for the removal of environmental reservoirs during outbreaks of A. baumannii in two studies.
      • Ray A.
      • Perez F.
      • Beltramini A.M.
      • et al.
      Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital.
      • Chmielarczyk A.
      • Higgins P.G.
      • Wojkowska-Mach J.
      • et al.
      Control of an outbreak of Acinetobacter baumannii infections using vaporized hydrogen peroxide.
      Two pre–post and one cohort study have evaluated the clinical impact of HPV; there are no data for the clinical impact of VHP aside from outbreak settings.
      • 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.

      Manian FA, Griesenauer S, Senkel D. Impact of an intensive terminal cleaning and disinfection (C/D) protocol involving selected hospital rooms on endemic nosocomial infection (NI) rates of common pathogens at a tertiary care medical center. 5th Decennial Meeting of the Society for Healthcare Epidemiology of America (SHEA), Atlanta, GA, USA. Abstract LB6. 2010.

      • 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.
      Boyce et al. performed a before–after study showing that HPV decontamination of rooms vacated by patients with C. difficile infection (CDI) significantly reduced the incidence of CDI on five focus wards and hospital-wide, when the analysis was restricted to the months when the epidemic strain was known to be present.
      • 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.
      A conference abstract by Manian et al. showed that HPV decontamination of rooms vacated by patients with a range of pathogens significantly reduced the rate of C. difficile and VRE infection, and substantially reduced the rate of MRSA and multidrug-resistant A. baumannii infection.

      Manian FA, Griesenauer S, Senkel D. Impact of an intensive terminal cleaning and disinfection (C/D) protocol involving selected hospital rooms on endemic nosocomial infection (NI) rates of common pathogens at a tertiary care medical center. 5th Decennial Meeting of the Society for Healthcare Epidemiology of America (SHEA), Atlanta, GA, USA. Abstract LB6. 2010.

      A cohort study by Passaretti et al. found that patients admitted to rooms vacated by patients with multidrug-resistant organisms (MDROs) and disinfected using HPV were 64% less likely to acquire MDROs than patients admitted to rooms vacated by patients with MDROs and disinfected using standard methods.
      • 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.
      Thus, HPV decontamination successfully mitigates the risk from the prior room occupant.
      • 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.

      Practical considerations

      H2O2 vapour systems have been used to decontaminate rooms, multi-bedded bays and entire units.
      • French G.L.
      • Otter J.A.
      • Shannon K.P.
      • Adams N.M.
      • 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.
      • Jeanes A.
      • Rao G.
      • Osman M.
      • Merrick P.
      Eradication of persistent environmental MRSA.
      • 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.
      • Dryden M.
      • Parnaby R.
      • Dailly S.
      • et al.
      Hydrogen peroxide vapour decontamination in the control of a polyclonal meticillin-resistant Staphylococcus aureus outbreak on a surgical ward.
      • Otter J.A.
      • Yezli S.
      • Schouten M.A.
      • van Zanten A.R.
      • Houmes-Zielman G.
      • Nohlmans-Paulssen M.K.
      Hydrogen peroxide vapor decontamination of an intensive care unit to remove environmental reservoirs of multidrug-resistant gram-negative rods during an outbreak.
      • Bates C.J.
      • Pearse R.
      Use of hydrogen peroxide vapour for environmental control during a Serratia outbreak in a neonatal intensive care unit.
      However, HPV is less straightforward than UVC and aHP systems because it requires two units (a generator and aeration unit) for a single room. Door and air vents need to be sealed. As with aHP, hand-held health and safety monitors are required to ensure that no leakage occurs during cycles and to verify that the concentration of H2O2 inside the enclosure is below health and safety exposure limits before permitting patients or staff to enter the room. Thus, staff training requirements for using H2O2 vapour systems are higher than for UV systems. The potential for selection of less susceptible strains is lower than for aHP or UV systems because the high-concentration H2O2 vapour systems typically eradicate pathogens so that few micro-organisms undergo sublethal exposure. Reported cycle times are currently 1.5–2.5 h for a single room for HPV and 8 h for VHP.
      • Ray A.
      • Perez F.
      • Beltramini A.M.
      • et al.
      Use of vaporized hydrogen peroxide decontamination during an outbreak of multidrug-resistant Acinetobacter baumannii infection at a long-term acute care hospital.
      • Barbut F.
      • Yezli S.
      • Otter J.A.
      Activity in vitro of hydrogen peroxide vapour against Clostridium difficile spores.

      Department of Health, NHS Purchasing and Supply Agency (UK). HCAI Technology Innovation Programme. Showcase Hospitals Report Number 3. The Bioquell Hydrogen Peroxide Vapour (HPV) Disinfection System. 2009.

      • Otter J.A.
      • Yezli S.
      Cycle times for hydrogen peroxide vapour decontamination.
      The compatibility of HPV with hospital materials, including sensitive electronics, is well established.

      Environmental Protection Agency (USA). Compatibility of material and electronic equipment with hydrogen peroxide and chlorine dioxide fumigation. Assessment and evaluation report. 2010.

      Ultraviolet C radiation (UVC)

      Technology description

      UVC systems for room decontamination deliver specific doses (for example, 12,000 μWs/cm2 for vegetative bacteria and 22,000–36,000 μWs/cm2 for spores) of UVC (254 nm range) to surfaces.
      • 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      The device is placed in the centre of the room and frequently touched mobile items are arranged close to the device for optimal exposure. UVC travels in straight lines and is less effective out of direct line of sight from the device. Some manufacturers therefore recommend multiple cycles from different locations.
      • Boyce J.M.
      • Havill N.L.
      • Moore B.A.
      Terminal decontamination of patient rooms using an automated mobile UV light unit.
      Some UVC systems contain sensors to measure the amount of UVC light reflected back to the device to confirm the delivery of a specified dose.

      Microbiological efficacy

      Several studies of one UVC system (Lumalier Tru-D) indicate a significant reduction of surface contamination.
      • 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      However, these reports indicate incomplete inactivation of C. difficile, VRE, Acinetobacter or MRSA from hospital surfaces.
      • 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      UVC produces a dose-dependent 2–4-log10 reduction on nosocomial pathogens experimentally dried on to surfaces.
      • 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      It may be possible to improve efficacy at the cost of extending cycles. Importantly, the microbiological reduction is significantly lower out of direct line of sight of the device.
      • 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.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      For example, in one study of a UVC device, a 1-log10 reduction was achieved on C. difficile spores inoculated on plastic carriers placed 10 feet away from the device out of direct line of sight, compared with 2.6-log10 reduction in direct line of sight.
      • 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.

      Clinical impact

      A recent conference abstract indicates an association between the use of UVC and a reduction in the incidence of CDI.
      • Pettis A.M.
      Elimination of Clostridium difficile infections (CDI) by illumination? Surface disinfection by ultraviolet light treatment.
      Further clinical studies on this and other pathogens are needed to assess the potential role of UVC systems in reducing nosocomial infection rates.

      Practical considerations

      UVC is easy to use, does not require sealing of door or air vents and has a relatively short cycle time. Many high-touch sites may be out of line of sight; some manufacturers recommended multiple cycles in different parts of the room to overcome this problem but this places reliance on the operator to choose appropriate equipment locations, has implications for cycle times and requires more hands-on operator time. A recent study indicates that a UVC spore cycle in rooms ranging from 46 to 86 m3 took a median of 84 min (range: 72–146) for a two-stage procedure (where the UVC unit is positioned at two locations during the cycle) and median of 68 min (range: 34–100) for a one-stage procedure.
      • Boyce J.M.
      • Havill N.L.
      • Moore B.A.
      Terminal decontamination of patient rooms using an automated mobile UV light unit.
      Since some UVC systems rely on measurement of reflected dose to determine the cycle, the presence of surfaces that do not reflect UVC, or reflect it inefficiently (such as glass), variations in temperature and humidity and the age of the bulbs will affect the reflected dose and may increase the cycle times.
      • Reeda N.G.
      The history of ultraviolet germicidal irradiation for air disinfection.
      • Memarzadeh F.
      • Olmsted R.N.
      • Bartley J.M.
      Applications of ultraviolet germicidal irradiation disinfection in healthcare facilities: effective adjunct, but not stand-alone technology.
      UVC is relatively expensive compared with other NTD systems.
      ECRI (Emergency Care Research Institute)
      Enhanced environmental disinfection systems.
      The intensity of the UV light dissipates with the square of the distance from the source, which limits the capacity of UVC devices to disinfect areas larger than single patient rooms.
      • Harrington B.J.
      • Valigosky M.
      Monitoring ultraviolet lamps in biological safety cabinets with cultures of standard bacterial strains on TSA blood agar.
      The long-term impact of UVC on hospital materials has not been described.
      • Tyan Y.C.
      • Liao J.D.
      • Klauser R.
      • IeD Wu
      • Weng C.C.
      Assessment and characterization of degradation effect for the varied degrees of ultra-violet radiation onto the collagen-bonded polypropylene non-woven fabric surfaces.
      Finally, UV radiation is a known mutagen.
      • Anderson P.
      Mutagenesis.
      Since UVC systems do not inactivate all microbes in the room, a proportion of those that have received a sublethal dose may undergo mutation.

      Pulsed-xenon ultraviolet (PX-UV)

      Technology description

      Pulsed-xenon ultraviolet systems emit broad spectrum UV in short pulses.
      • Stibich M.
      • Stachowiak J.
      • Tanner B.
      • et al.
      Evaluation of a pulsed-xenon ultraviolet room disinfection device for impact on hospital operations and microbial reduction.
      They are placed at multiple room locations and have a relatively short cycle time.

      Microbiological efficacy

      One PX-UV system (Xenex) achieved a significant reduction in VRE contamination in a room in a 12 min cycle.
      • Stibich M.
      • Stachowiak J.
      • Tanner B.
      • et al.
      Evaluation of a pulsed-xenon ultraviolet room disinfection device for impact on hospital operations and microbial reduction.
      Further efficacy data are awaited.

      Clinical impact

      A recent conference abstract indicates that the use of PX-UV may be associated with a reduction in the incidence of CDI.

      Levin J, Parrish C, Riley L, English D. The use of portable pulsed xenon ultraviolet light (PPX-UV) after terminal cleaning was associated with a dramatic decrease in the hospital-associated Clostridium difficile infection (HA-CDI) rate in a community hospital. Infectious Diseases Society of America (IDSA) Annual Meeting. Abstract 342. 2011.

      However, the study was performed for a short duration so further data are awaited.

      Practical considerations

      Pulsed-xenon ultraviolet systems have similar practical considerations to UVC systems, including the need to use multiple room locations to address line-of-sight issues, the age of the bulbs affecting intensity of the pulse, limited capacity to decontaminate areas larger than single rooms and the potential for mutagenesis. Also, the system operates using a series of bright ‘camera flashes’, which may be disruptive to patients. However, given the short cycles associated with PX-UV, it should be prioritized for further evaluation.

      Other systems

      Gaseous ozone can achieve a high level of microbial inactivation.
      • Sharma M.
      • Hudson J.B.
      Ozone gas is an effective and practical antibacterial agent.
      • Moat J.
      • Cargill J.
      • Shone J.
      • Upton M.
      Application of a novel decontamination process using gaseous ozone.
      However, the requirement for high humidity is a practical limitation.
      • Li C.S.
      • Wang Y.C.
      Surface germicidal effects of ozone for microorganisms.
      Furthermore, ozone is toxic to humans, with a safe exposure level in the UK and USA of <0.1 ppm (compared with 1 ppm for H2O2), so effective containment of the gas, monitoring for leakage and assessing safe levels for re-entry are necessary in healthcare settings.

      Occupational Safety and Health Administration (OSHA). Occupational safety and health guideline for hydrogen peroxide. Washington, DC: US Department of Labor; not dated.

      Executive and Safety Executive. EH40/2005 Workplace exposure limits. Bootle, UK: HSE; 2005.

      Data on the compatibility of this process with hospital materials are needed due to ozone's known corrosive properties.
      • Davies A.
      • Pottage T.
      • Bennett A.
      • Walker J.
      Gaseous and air decontamination technologies for Clostridium difficile in the healthcare environment.
      Chlorine dioxide has a high level of efficacy against a range of pathogens.
      • Beswick A.J.
      • Farrant J.
      • Makison C.
      • et al.
      Comparison of multiple systems for laboratory whole room fumigation.
      However, concerns about safety and material compatibility mean that it is unlikely to be used in healthcare settings.
      • Beswick A.J.
      • Farrant J.
      • Makison C.
      • et al.
      Comparison of multiple systems for laboratory whole room fumigation.

      Environmental Protection Agency (USA). Compatibility of material and electronic equipment with hydrogen peroxide and chlorine dioxide fumigation. Assessment and evaluation report. 2010.

      ‘Fogging’ with various chemicals, including super-oxidized water and solutions of H2O2 mixed with other chemicals, has been evaluated.
      • Friedman H.
      • Volin E.
      • Laumann D.
      Terminal disinfection in hospitals with quaternary ammonium compounds by use of a spray-fog technique.
      • Ostrander W.E.
      • Griffith L.J.
      Evaluation of disinfectants for hospital housekeeping use.
      • Galvin S.
      • Boyle M.
      • Russell R.J.
      • et al.
      Evaluation of vaporized hydrogen peroxide, Citrox and pH neutral Ecasol for decontamination of an enclosed area: a pilot study.
      • Clark J.
      • Barrett S.P.
      • Rogers M.
      • Stapleton R.
      Efficacy of super-oxidized water fogging in environmental decontamination.
      • Tuladhar E.
      • Terpstra P.
      • Koopmans M.
      • Duizer E.
      Virucidal efficacy of hydrogen peroxide vapour disinfection.
      • Taneja N.
      • Biswal M.
      • Kumar A.
      • et al.
      Hydrogen peroxide vapour for decontaminating air-conditioning ducts and rooms of an emergency complex in northern India: time to move on.
      • De Lorenzi S.
      • Romanini L.
      • Finzi G.
      • Barrai I.
      • Salvatorelli G.
      Reducing microbial contamination of surfaces using RelyOn Virkosept aerosol spray.
      • Callahan K.L.
      • Beck N.K.
      • Duffield E.A.
      • Shin G.
      • Meschke J.S.
      Inactivation of methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant Enterococcus faecium (VRE) on various environmental surfaces by mist application of a stabilized chlorine dioxide and quaternary ammonium compound-based disinfectant.
      These systems are limited by directional introduction of the active agent and consequent non-homogeneous distribution, and the potential for the accumulation of large volumes of chemicals that require post-process removal, with associated risks to operators.
      • Taneja N.
      • Biswal M.
      • Kumar A.
      • et al.
      Hydrogen peroxide vapour for decontaminating air-conditioning ducts and rooms of an emergency complex in northern India: time to move on.
      Data on compatibility with hospital materials are awaited.

      Selecting, validating and regulating NTD systems

      The need for pre-cleaning

      All NTD systems require cleaning prior to their application (‘pre-cleaning’) for two reasons: to make the room aesthetically acceptable to the next occupant and to remove organic matter that red