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Evidence that contaminated surfaces contribute to the transmission of hospital pathogens and an overview of strategies to address contaminated surfaces in hospital settings

      Evidence that contaminated surfaces contribute to the transmission of hospital pathogens comes from studies modeling transmission routes, microbiologic studies, observational epidemiologic studies, intervention studies, and outbreak reports. This review presents evidence that contaminated surfaces contribute to transmission and discusses the various strategies currently available to address environmental contamination in hospitals.

      Key Words

      Environmental surfaces were once thought to play a negligible role in the endemic transmission of nosocomial pathogens.
      • Rhame F.S.
      The inanimate environment.
      However, recent data indicate that contaminated surfaces play an important role in the endemic and epidemic transmission of certain pathogens that cause health care-associated infections.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      Clostridium difficile, methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE), norovirus, and multidrug-resistant (MDR) gram-negative rods including Acinetobacter baumannii share the ability to be shed from infected or colonized patients, survive on dry surfaces for extend periods, and are difficult to eradicate by cleaning and disinfection.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      Whereas the role of contaminated surfaces in the transmission of some pathogens such as the spore-forming C difficile has been recognized for some time,
      • Samore M.H.
      • Venkataraman L.
      • DeGirolami P.C.
      • Arbeit R.D.
      • Karchmer A.W.
      Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.
      the importance of contaminated surfaces in the transmission of other pathogens such as MDR A baumannii has come to light only in recent years.
      • 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.
      The continued emergence of antimicrobial resistance in gram-negative bacteria in particular means that effective prevention and control strategies are required urgently.
      • Peleg A.Y.
      • Hooper D.C.
      Hospital-acquired infections due to gram-negative bacteria.
      The transmission routes of pathogens are complicated and difficult to investigate, so studies focused on the role of surfaces in transmission have been rare until relatively recently.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      Data suggesting that contaminated surfaces play a role in transmission come from studies modeling transmission,
      • Lee B.Y.
      • Wettstein Z.S.
      • McGlone S.M.
      • Bailey R.R.
      • Umscheid C.A.
      • Smith K.J.
      • et al.
      Economic value of norovirus outbreak control measures in healthcare settings.
      • Lawley T.D.
      • Clare S.
      • Deakin L.J.
      • Goulding D.
      • Yen J.L.
      • Raisen C.
      • et al.
      Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.
      • Oelberg D.G.
      • Joyner S.E.
      • Jiang X.
      • Laborde D.
      • Islam M.P.
      • Pickering L.K.
      Detection of pathogen transmission in neonatal nurseries using DNA markers as surrogate indicators.
      microbiologic studies in vitro and in situ,
      • Boyce J.M.
      Are the epidemiology and microbiology of methicillin-resistant Staphylococcus aureus changing?.
      • 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.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • Setzer J.M.
      • Doll S.A.
      • Perry A.M.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      • Otter J.A.
      • French G.L.
      Survival of nosocomial bacteria and spores on surfaces and inactivation by hydrogen peroxide vapor.
      observational epidemiologic studies,
      • Samore M.H.
      • Venkataraman L.
      • DeGirolami P.C.
      • Arbeit R.D.
      • Karchmer A.W.
      Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.
      • 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.
      • Drees M.
      • Snydman D.
      • Schmid C.
      • Barefoot L.
      • Hansjosten K.
      • Vue P.
      • et al.
      Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci.
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestel D.D.
      • Arndt J.
      • Strachan C.L.
      • Welch K.B.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.
      • Huang S.S.
      • Datta R.
      • Platt R.
      Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
      • Hardy K.J.
      • Oppenheim B.A.
      • Gossain S.
      • Gao F.
      • Hawkey P.M.
      A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients’ acquisition of MRSA.
      intervention studies aimed at improving the efficacy of cleaning and disinfection,
      • Passaretti C.L.
      • Otter J.A.
      • Reich N.G.
      • Myers J.
      • Shepard J.
      • Ross T.
      • et al.
      An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • McDonald L.C.
      • Adams N.M.
      • Cooper T.
      • et al.
      Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      • 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.
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      • 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.
      and outbreak reports.
      • Denton M.
      • Wilcox M.H.
      • Parnell P.
      • Green D.
      • Keer V.
      • Hawkey P.M.
      • et al.
      Role of environmental cleaning in controlling an outbreak of Acinetobacter baumannii on a neurosurgical intensive care unit.
      • Zanetti G.
      • Blanc D.S.
      • Federli I.
      • Raffoul W.
      • Petignat C.
      • Maravic P.
      • et al.
      Importation of Acinetobacter baumannii into a burn unit: a recurrent outbreak of infection associated with widespread environmental contamination.
      • Thornley C.N.
      • Emslie N.A.
      • Sprott T.W.
      • Greening G.E.
      • Rapana J.P.
      Recurring norovirus transmission on an airplane.
      The role played by contaminated environmental surfaces in the transmission of nosocomial pathogens was recently reviewed.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      Here, we present the latest data evaluating the role of contaminated surfaces in transmission and discuss the various strategies available to address environmental contamination in hospitals.

      Evidence that contaminated surfaces contribute to transmission

      Modeling transmission

      Modeling transmission routes can provide “proof of principle” that contaminated surfaces are involved in transmission: for example, monitoring the spread of nonmicrobial markers,
      • Oelberg D.G.
      • Joyner S.E.
      • Jiang X.
      • Laborde D.
      • Islam M.P.
      • Pickering L.K.
      Detection of pathogen transmission in neonatal nurseries using DNA markers as surrogate indicators.
      the use of animal models,
      • Lawley T.D.
      • Clare S.
      • Deakin L.J.
      • Goulding D.
      • Yen J.L.
      • Raisen C.
      • et al.
      Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.
      and mathematical modelling.
      • Lee B.Y.
      • Wettstein Z.S.
      • McGlone S.M.
      • Bailey R.R.
      • Umscheid C.A.
      • Smith K.J.
      • et al.
      Economic value of norovirus outbreak control measures in healthcare settings.
      One study evaluated the spread of a nonmicrobial marker (plant DNA) designed to model the spread of pathogens from hospitals surfaces. The marker was inoculated onto a single telephone handle in one of six 8-cot “pods” in a neonatal intensive care unit (ICU). The spread of the marker was remarkable: within 4 hours, it was identified from environmental surfaces and staff hands across the unit including all 6 pods. Whereas the spread of plant DNA does not necessarily accurately represent the spread of a pathogenic micro-organism, it does present a picture of dynamic and rapid transmission involving both environmental surfaces and staff hands.
      Another approach to modeling transmission is the use of animal models. For example, Lawley et al used a murine model to evaluate the transmission of C difficile.
      • Lawley T.D.
      • Clare S.
      • Deakin L.J.
      • Goulding D.
      • Yen J.L.
      • Raisen C.
      • et al.
      Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.
      The model established that C difficile could be spread through experimentally contaminated cages in a dose-dependent manner. Furthermore, the model also demonstrated that disinfection of the cages using a range of disinfectants interrupted transmission proportionally to the level of spore reduction achieved.
      Mathematical modeling can also provide some insight into transmission routes. Mathematical models including the role of contaminated surfaces are rare, but one study evaluated the likely economic impact of various control strategies for norovirus including improved disinfection.
      • Lee B.Y.
      • Wettstein Z.S.
      • McGlone S.M.
      • Bailey R.R.
      • Umscheid C.A.
      • Smith K.J.
      • et al.
      Economic value of norovirus outbreak control measures in healthcare settings.
      The model found that increased disinfection alone or in combination with increased hand hygiene and using protective apparel were most useful for the control and containment of norovirus outbreaks.

      Microbiologic studies

      Environmental sampling of the surfaces surrounding patients in hospitals has established that certain pathogens are shed into the hospital environment. Wide variation in the reported frequency of environmental contamination can be explained by several factors, including the culturability of the organism, the degree of shedding by the patient, the sampling methodology, the ease of contamination (or difficulty of cleaning) of the particular environment, and whether there is an ongoing outbreak at the time of sampling.
      Surfaces in the vicinity of patients have a higher frequency of contamination than other sites.
      • 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.
      • Huslage K.
      • Rutala W.A.
      • Sickbert-Bennett E.
      • Weber D.J.
      A quantitative approach to defining “high-touch” surfaces in hospitals.
      Infected patients shed more pathogens than those who are only colonized, and diarrhea results in widespread contamination.
      • Boyce J.M.
      • Potter-Bynoe G.
      • Chenevert C.
      • King T.
      Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications.
      • Boyce J.M.
      • Opal S.M.
      • Chow J.W.
      • Zervos M.J.
      • Potter-Bynoe G.
      • Sherman C.B.
      • et al.
      Outbreak of multidrug-resistant Enterococcus faecium with transferable vanB class vancomycin resistance.
      Although the presence of a pathogen on a surface does not necessarily represent a risk for transmission,
      • Rhame F.S.
      The inanimate environment.
      studies have demonstrated that the infectious dose of some pathogens is low. For example, a small number of C difficile spores or norovirus particles are sufficient to initiate an infection.
      • Lawley T.D.
      • Clare S.
      • Deakin L.J.
      • Goulding D.
      • Yen J.L.
      • Raisen C.
      • et al.
      Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens.
      • Yezli S.
      • Otter J.A.
      Minimum infective dose of the major human respiratory and enteric viruses transmitted through food and the environment.
      • Larson H.E.
      • Borriello S.P.
      Quantitative study of antibiotic-induced susceptibility to Clostridium difficile enterocecitis in hamsters.
      Microbiologic studies have established that certain hospital pathogens can survive on dry hospital surfaces for extend periods (Table 1).
      • Kramer A.
      • Schwebke I.
      • Kampf G.
      How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
      The survival of hospital pathogens on dry hospital surfaces in vitro varies according to experimental conditions, but some strains of vegetative bacteria have the capacity to survive for months on dry hospital surfaces. VRE in particular seems to have remarkable survival properties, with a recent study showing that VRE can remain viable on dry surfaces for almost 4 years.
      • Wagenvoort J.H.
      • De Brauwer E.I.
      • Penders R.J.
      • Willems R.J.
      • Top J.
      • Bonten M.J.
      Environmental survival of vancomycin-resistant Enterococcus faecium.
      The mechanisms underlying this surprising survival capacity of certain vegetative bacteria are unknown, but the recent discovery of biofilms on dry hospital surfaces may provide a mechanism through which vegetative bacteria could survive on dry surfaces for such extend periods without a nutrient source.
      • Vickery K.
      • Deva A.
      • Jacombs A.
      • Allan J.
      • Valente P.
      • Gosbell I.B.
      Presence of biofilm containing viable multiresistant organisms despite terminal cleaning on clinical surfaces in an intensive care unit.
      • Yezli S.
      • Otter J.A.
      Does the discovery of biofilms on dry hospital environmental surfaces change the way we think about hospital disinfection?.
      Table 1Survival of hospital pathogens on dry hospital surfaces
      NOTE. Adapted from Kramer et al.
      • Kramer A.
      • Schwebke I.
      • Kampf G.
      How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.
      OrganismSurvival time
      Clostridium difficile (spores)>5 Months
      Acinetobacter spp3 Days to 11 months
      • Wagenvoort J.H.
      • Joosten E.J.
      An outbreak Acinetobacter baumannii that mimics MRSA in its environmental longevity.
      Enterococcus spp including VRE5 Days to >46 months
      • Wagenvoort J.H.
      • De Brauwer E.I.
      • Penders R.J.
      • Willems R.J.
      • Top J.
      • Bonten M.J.
      Environmental survival of vancomycin-resistant Enterococcus faecium.
      Pseudomonas aeruginosa6 Hours to 16 months
      Klebsiella spp2 Hours to >30 months
      Staphylococcus aureus, including MRSA7 Days to >12 months
      • Wagenvoort J.H.
      • Sluijsmans W.
      • Penders R.J.
      Better environmental survival of outbreak vs. sporadic MRSA isolates.
      Norovirus (and feline calicivirus)8 Hours to >2 weeks
      • Doultree J.C.
      • Druce J.D.
      • Birch C.J.
      • Bowden D.S.
      • Marshall J.A.
      Inactivation of feline calicivirus, a Norwalk virus surrogate.
      In vitro studies of the spread of DNA or other markers, model organisms, or pathogens show that transfer can occur from environmental surfaces to hands and vice versa.
      • Winther B.
      • McCue K.
      • Ashe K.
      • Rubino J.
      • Hendley J.O.
      Rhinovirus contamination of surfaces in homes of adults with natural colds: transfer of virus to fingertips during normal daily activities.
      • Rusin P.
      • Maxwell S.
      • Gerba C.
      Comparative surface-to-hand and fingertip-to-mouth transfer efficiency of gram-positive bacteria, gram-negative bacteria, and phage.
      • Barker J.
      • Vipond I.B.
      • Bloomfield S.F.
      Effects of cleaning and disinfection in reducing the spread of Norovirus contamination via environmental surfaces.
      • Rheinbaben F.
      • Schunemann S.
      • Gross T.
      • Wolff M.H.
      Transmission of viruses via contact in a household setting: experiments using bacteriophage straight phiX174 as a model virus.
      Several microbiologic studies have investigated the transfer of pathogens from surfaces to the hands or gloves of health care personnel in the absence of direct patient contact (Table 2). Contact with an environmental surface carries approximately the same risk of acquiring MRSA,
      • 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.
      VRE,
      • 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.
      and C difficile
      • Guerrero D.M.
      • Nerandzic M.M.
      • Jury L.A.
      • Jinno S.
      • Chang S.
      • Donskey C.J.
      Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.
      hand or glove contamination as touching an infected or colonized patient. One study estimated that VRE hand contamination was acquired through approximately 10% of contacts with either the patient or the surfaces surrounding the patient.
      • 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.
      Importantly, hand hygiene compliance was significantly more likely following direct patient contact compared with contact with the patient environment, meaning that contamination acquired from the environment is likely to persist for longer and hence could be relatively more important for onward transmission.
      • Randle J.
      • Arthur A.
      • Vaughan N.
      Twenty-four-hour observational study of hospital hand hygiene compliance.
      Table 2Transfer of pathogens from surfaces to the hands of health care personnel
      Direct patient contactContact with environmental surfaces only
      52% of 44 HCP acquired VRE on their hands or gloves
      • 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.
      45% of 50 HCP acquired MRSA on their gloved hands
      • 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.
      40% of 50 HCP acquired MRSA on their gloved hands
      • 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.
      50% of 30 HCP acquired Clostridium difficile on their gloved hands
      • Guerrero D.M.
      • Nerandzic M.M.
      • Jury L.A.
      • Jinno S.
      • Chang S.
      • Donskey C.J.
      Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.
      50% of 30 HCP acquired C difficile on their gloved hands
      • Guerrero D.M.
      • Nerandzic M.M.
      • Jury L.A.
      • Jinno S.
      • Chang S.
      • Donskey C.J.
      Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.
      Compliance with hand hygiene: 80%
      • Randle J.
      • Arthur A.
      • Vaughan N.
      Twenty-four-hour observational study of hospital hand hygiene compliance.
      Compliance with hand hygiene: 50%
      • Randle J.
      • Arthur A.
      • Vaughan N.
      Twenty-four-hour observational study of hospital hand hygiene compliance.
      HCP, Health care personnel.
      Cleaning and/or disinfection is usually performed daily (or several times daily) to reduce the environmental burden and ensure that the patient environment remains visibly clean. More stringent cleaning and/or disinfection is performed at patient discharge (sometimes called “terminal” cleaning/disinfection) to ensure that the clinical area is properly disinfected and safe for the next occupant. Many studies have been performed to investigate the efficacy of cleaning and disinfection, and most focus on the efficacy of terminal cleaning/disinfection. Environmental sampling performed after terminal disinfection often identifies surfaces contaminated with the pathogen that the process is aiming to eliminate.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • McDonald L.C.
      • Adams N.M.
      • Cooper T.
      • et al.
      Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      • 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.
      • Verity P.
      • Wilcox M.H.
      • Fawley W.
      • Parnell P.
      Prospective evaluation of environmental contamination by Clostridium difficile in isolation side rooms.
      • 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.
      • 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.
      • Morter S.
      • Bennet G.
      • Fish J.
      • Richards J.
      • Allen D.J.
      • Nawaz S.
      • et al.
      Norovirus in the hospital setting: virus introduction and spread within the hospital environment.
      • Goldenberg S.D.
      • Patel A.
      • Tucker D.
      • French G.L.
      Lack of enhanced effect of a chlorine dioxide-based cleaning regimen on environmental contamination with Clostridium difficile spores.
      Even multiple “rounds” of bleach disinfection may not be sufficient to eliminate some pathogens.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • Setzer J.M.
      • Doll S.A.
      • Perry A.M.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      • 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.
      • Morter S.
      • Bennet G.
      • Fish J.
      • Richards J.
      • Allen D.J.
      • Nawaz S.
      • et al.
      Norovirus in the hospital setting: virus introduction and spread within the hospital environment.
      For example, a recent study found that 27% of rooms remained contaminated with A baumannii or MRSA following 4 rounds of bleach disinfection.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • Setzer J.M.
      • Doll S.A.
      • Perry A.M.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      Similarly, 43% of surfaces were contaminated with norovirus RNA after 1 round of bleach disinfection, and 16% of surfaces were contaminated after 2 rounds of bleach disinfection. Bleach and other disinfectants are effective against these and other pathogens in vitro, and, in theory, cleaning using a detergent alone would remove contamination with these pathogens. Thus, the failure of cleaning and disinfection to consistently eliminate surface contamination with pathogens is most likely explained by the challenge of repeatedly achieving adequate distribution and contact time of the agent.

      Observational epidemiologic studies

      Carefully performed observational epidemiologic studies have established that contaminated surfaces are involved in the transmission of certain pathogens.
      • Samore M.H.
      • Venkataraman L.
      • DeGirolami P.C.
      • Arbeit R.D.
      • Karchmer A.W.
      Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.
      • Hardy K.J.
      • Oppenheim B.A.
      • Gossain S.
      • Gao F.
      • Hawkey P.M.
      A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients’ acquisition of MRSA.
      • Bonten M.J.
      • Hayden M.K.
      • Nathan C.
      • van Voorhis J.
      • Matushek M.
      • Slaughter S.
      • et al.
      Epidemiology of colonisation of patients and environment with vancomycin-resistant enterococci.
      For example, one study concluded that at least 3 of 26 patients acquired MRSA directly from contaminated environmental surfaces.
      • Hardy K.J.
      • Oppenheim B.A.
      • Gossain S.
      • Gao F.
      • Hawkey P.M.
      A study of the relationship between environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and patients’ acquisition of MRSA.
      However, it is difficult to determine the independent role of contaminated surfaces in these studies.
      A useful way to elucidate the role of contaminated surfaces in transmission is to evaluate the risk of acquiring certain pathogens in patients admitted to rooms where the prior occupant was known to be infected or colonized with the pathogen. If environmental surfaces are an important factor in transmission because of inadequate disinfection after discharge of an infected or colonized patient, there will be an increased risk of acquisition of the same pathogen in the subsequent room occupant. This has been shown to be the case for a range of organisms, including C difficile, MRSA, VRE, and MDR gram-negative rods, including A baumannii (Fig 1).
      • 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.
      • Drees M.
      • Snydman D.
      • Schmid C.
      • Barefoot L.
      • Hansjosten K.
      • Vue P.
      • et al.
      Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci.
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestel D.D.
      • Arndt J.
      • Strachan C.L.
      • Welch K.B.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.
      • Huang S.S.
      • Datta R.
      • Platt R.
      Risk of acquiring antibiotic-resistant bacteria from prior room occupants.
      For example, during a 14-month study performed on 2 ICUs in the United States, all patients were screened for VRE on admission and twice weekly, and the environment was screened weekly
      • Drees M.
      • Snydman D.
      • Schmid C.
      • Barefoot L.
      • Hansjosten K.
      • Vue P.
      • et al.
      Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci.
      ; the 50 patients who acquired VRE were compared with the 588 who did not. Admission to a room from which a previous positive VRE culture had been obtained had the greatest increased risk of acquisition (hazard ratio [HR], 4.3); admission to a room where the immediate room occupant was infected or colonized with VRE had intermediate increased risk (HR, 3.8); and admission to a room that had been occupied by a VRE-infected or -colonized patient in the prior 2 weeks had the lowest increased risk (HR, 2.7).
      Figure thumbnail gr1
      Fig 1Chart showing the increased risk associated with the prior room occupant. The figures of difference in risk are unadjusted based on raw data. Several of the studies included adjusted measures of risk, but these were not included because of differences in study design. ∗ Any patient infected or colonized with VRE in the two weeks prior to admission. The immediate prior room occupant was known to be infected or colonized with VRE.
      The fact that terminal cleaning and disinfection does not reliably eliminate pathogens supports the findings of these “prior room occupancy” studies. Inadequate terminal disinfection may also result in a room becoming contaminated with more than 1 strain of a particular pathogen because of a “build up” over time. For example, MRSA with an average of 2.3 antibiograms were found in each patient room in one study where there was suboptimal terminal cleaning.
      • 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.
      Similarly, in other studies, approximately 30% of MRSA environmental types were not closely related to the MRSA type affecting the patient in the room.
      • Sexton T.
      • Clarke P.
      • O’Neill E.
      • Dillane T.
      • Humphreys H.
      Environmental reservoirs of methicillin-resistant Staphylococcus aureus in isolation rooms: correlation with patient isolates and implications for hospital hygiene.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • Adams N.M.
      Widespread environmental contamination associated with patients with diarrhea and methicillin-resistant Staphylococcus aureus colonization of the gastrointestinal tract.
      Also, pathogens can be identified in empty rooms
      • Drees M.
      • Snydman D.
      • Schmid C.
      • Barefoot L.
      • Hansjosten K.
      • Vue P.
      • et al.
      Prior environmental contamination increases the risk of acquisition of vancomycin-resistant enterococci.
      • Passaretti C.L.
      • Otter J.A.
      • Reich N.G.
      • Myers J.
      • Shepard J.
      • Ross T.
      • et al.
      An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.
      and can be transferred to the hands of health care personnel from surfaces in empty rooms.
      • Bhalla A.
      • Pultz N.J.
      • Gries D.M.
      • Ray A.J.
      • Eckstein E.C.
      • Aron D.C.
      • et al.
      Acquisition of nosocomial pathogens on hands after contact with environmental surfaces near hospitalized patients.
      These “prior room occupancy” studies allow the assessment of the risks associated with environmental contamination independent of common confounding variables of hospital infection, such as patient age, comorbidities, and length of stay. In addition, because the source patients were already discharged, in these studies patient acquisition directly from surfaces or via hand transfer from health care personnel is most likely to have come from contaminated surfaces.

      Intervention studies

      The findings of the prior room occupancy studies are supported by evidence that improved terminal cleaning and disinfection can reduce the risk of infection for the next occupant.
      • Passaretti C.L.
      • Otter J.A.
      • Reich N.G.
      • Myers J.
      • Shepard J.
      • Ross T.
      • et al.
      An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      Datta et al performed a retrospective cohort intervention study on 10 ICUs at a US hospital to evaluate the impact of improved cleaning and disinfection.
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      The intervention consisted of targeted feedback using a black-light marker, the introduction of a “bucket method” for wetting cleaning cloths, and increased education of housekeeping staff. Patient acquisition was compared during 20-month baseline and intervention periods separated by 16 months. The acquisition of both MRSA and VRE fell significantly during the intervention periods, by 50% and 27%, respectively. The risk associated with the prior room occupant was successfully mitigated for MRSA but not for VRE.
      Passaretti et al performed a prospective 30-month cohort intervention study on 6 high-risk units in a US hospital to evaluate the impact of introducing hydrogen peroxide vapor (HPV) for the terminal disinfection of select patient rooms. HPV was introduced to disinfect the rooms of patients known to be infected or colonized with multidrug-resistant organisms (MDROs) on 3 units following a 12-month preintervention phase. Patients admitted to rooms decontaminated using HPV were significantly less likely to acquire any MDRO (64% reduction) and VRE (80% reduction). HPV decontamination significantly reduced the proportion of rooms environmentally contaminated with MDROs by 35%. In particular, rooms contaminated with multiple MDROs, MDROs cultured from a room that differed from the room occupant’s known MDRO, and MDROs cultured from empty rooms were less frequent on HPV units during the intervention phase. These environmental findings can be explained by the improved terminal disinfection by HPV.
      Several prospective studies have demonstrated that interventions aimed at reducing surface contamination reduce the transmission of hospital pathogens. These can be broadly divided into studies of a change in disinfection agent
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • McDonald L.C.
      • Adams N.M.
      • Cooper T.
      • et al.
      Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      • Mayfield J.L.
      • Leet T.
      • Miller J.
      • Mundy L.M.
      Environmental control to reduce transmission of Clostridium difficile.
      • 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.
      • 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.
      or educational improvements using existing agents.
      • 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.
      • 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.
      These studies have been reviewed in detail by Otter et al.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      Since the publication of that review, a 4-year before-and-after Brazilian study evaluated the impact of an intervention aimed at reducing VRE environmental contamination.
      • Perugini M.R.
      • Nomi S.M.
      • Lopes G.K.
      • Belei R.A.
      • van der Heijden I.M.
      • Mostachio A.K.
      • et al.
      Impact of the reduction of environmental and equipment contamination on vancomycin-resistant enterococcus rates.
      The intervention comprised an educational program for housekeepers and health care personnel and observation of compliance with several infection prevention and control procedures. Following the intervention, there was a significant reduction in the frequency of VRE contamination of equipment and surfaces from 23% to 8.2% and an associated reduction in VRE prevalence from 7.7 to 1.9 cases per 1,000 patient-days. Although the multifaceted intervention makes it difficult to be certain that the reduction in environmental contamination is wholly responsible for the reduction in VRE cases, it provides further evidence that reducing the environmental burden can help to reduce the transmission of VRE.

      Outbreak reports

      Findings derived from outbreaks are often limited by lack of controls, multiple interventions and the potential for regression to the mean. However, many outbreak reports implicate contaminated surfaces in the transmission of C difficile,
      • Walters B.A.
      • Stafford R.
      • Roberts R.K.
      • Seneviratne E.
      Contamination and crossinfection with Clostridium difficile in an intensive care unit.
      • Kaatz G.W.
      • Gitlin S.D.
      • Schaberg D.R.
      • Wilson K.H.
      • Kauffman C.A.
      • Seo S.M.
      • et al.
      Acquisition of Clostridium difficile from the hospital environment.
      MRSA,
      • Layton M.C.
      • Perez M.
      • Heald P.
      • Patterson J.E.
      An outbreak of mupirocin-resistant Staphylococcus aureus on a dermatology ward associated with an environmental reservoir.
      • Rampling A.
      • Wiseman S.
      • Davis L.
      • Hyett A.P.
      • Walbridge A.N.
      • Payne G.C.
      • et al.
      Evidence that hospital hygiene is important in the control of methicillin-resistant Staphylococcus aureus.
      VRE,
      • Nourse C.
      • Murphy H.
      • Byrne C.
      • O'Meara A.
      • Breatnach F.
      • Kaufmann M.
      • et al.
      Control of a nosocomial outbreak of vancomycin resistant Enterococcus faecium in a paediatric oncology unit: risk factors for colonisation.
      • Falk P.S.
      • Winnike J.
      • Woodmansee C.
      • Desai M.
      • Mayhall C.G.
      Outbreak of vancomycin-resistant enterococci in a burn unit.
      MDR gram-negative rods
      • Denton M.
      • Wilcox M.H.
      • Parnell P.
      • Green D.
      • Keer V.
      • Hawkey P.M.
      • et al.
      Role of environmental cleaning in controlling an outbreak of Acinetobacter baumannii on a neurosurgical intensive care unit.
      • Zanetti G.
      • Blanc D.S.
      • Federli I.
      • Raffoul W.
      • Petignat C.
      • Maravic P.
      • et al.
      Importation of Acinetobacter baumannii into a burn unit: a recurrent outbreak of infection associated with widespread environmental contamination.
      and norovirus.
      • Thornley C.N.
      • Emslie N.A.
      • Sprott T.W.
      • Greening G.E.
      • Rapana J.P.
      Recurring norovirus transmission on an airplane.
      • Green J.
      • Wright P.A.
      • Gallimore C.I.
      • Mitchell O.
      • Morgan-Capner P.
      • Brown D.W.
      The role of environmental contamination with small round structured viruses in a hospital outbreak investigated by reverse-transcriptase polymerase chain reaction assay.
      Data supporting the role of contaminated surfaces in the transmission of norovirus come from outbreak reports, mostly in community settings. For example, a recent study from New Zealand provides compelling data that environmental contamination contributes to the transmission of norovirus through a remarkable outbreak of norovirus affecting successive flights of the same plane with distinct crews and passengers, associated with an episode of vomiting.
      • Thornley C.N.
      • Emslie N.A.
      • Sprott T.W.
      • Greening G.E.
      • Rapana J.P.
      Recurring norovirus transmission on an airplane.
      The attack rate among staff decreased sequentially with subsequent flights, presumably as the environmental reservoir diminished. The attack rate in passengers could not be determined because follow-up of each passenger was not feasible. The outbreak only ceased once the plane was refitted with new carpet in the affected area. Health care facilities do not have epidemiologically distinct cohorts of patients and staff, so it is more difficult to establish the role of contaminated surfaces in the transmission of norovirus. However, the finding of norovirus RNA contamination on surfaces in the immediate vicinity of patients and the general association between improved disinfection and the containment of outbreaks provides convincing evidence that contaminated surfaces are an important factor in the transmission of norovirus.
      • Lee B.Y.
      • Wettstein Z.S.
      • McGlone S.M.
      • Bailey R.R.
      • Umscheid C.A.
      • Smith K.J.
      • et al.
      Economic value of norovirus outbreak control measures in healthcare settings.
      • Morter S.
      • Bennet G.
      • Fish J.
      • Richards J.
      • Allen D.J.
      • Nawaz S.
      • et al.
      Norovirus in the hospital setting: virus introduction and spread within the hospital environment.
      • Wu H.M.
      • Fornek M.
      • Schwab K.J.
      • Chapin A.R.
      • Gibson K.
      • Schwab E.
      • et al.
      A norovirus outbreak at a long-term-care facility: the role of environmental surface contamination.

      Strategies to address environmental contamination

      It is now clear that contaminated surfaces contribute to the transmission of some pathogens in some settings. However, the importance of contaminated surfaces relative to other transmission routes is not well understood. Indeed, when 6 experts speaking at an environmental session at APIC 2012 were asked to estimate the “percentage of all C difficile transmission in hospitals that is mediated, directly or indirectly, by contamination of the inanimate environment,” the responses ranged from 25% to 75% (unpublished data). Modeling, prior room occupancy studies, and intervention studies give a general indication of the contribution of contaminated surfaces to transmission, but carefully designed studies are required to provide more definitive data.
      Despite the limitations of the evidence base, more needs to be done to address environmental contamination in hospitals to deliver the safest possible health care. Strategies to address environmental contamination can be divided into reducing and containing the shedding of pathogens and improved cleaning and disinfection.

      Reducing and containing shedding

      Improving compliance with hand hygiene following contact with a patient’s surroundings will reduce the chances of indirect spread of pathogens acquired on the hands of health care personnel following contact with their surroundings (Table 2).
      • Randle J.
      • Arthur A.
      • Vaughan N.
      Twenty-four-hour observational study of hospital hand hygiene compliance.
      Also, improved compliance with hand hygiene before and after direct contact with patients will reduce the spread of contamination into the health care environment on the hands of health care personnel.
      The rapid identification and isolation of infected or colonized patients is crucial for containing contamination. There is uncertainty surrounding the length of time patients should be isolated, and further work is required on this. Whereas hospitals in the United States generally have a high proportion of single rooms, hospitals in other countries typically have a much lower proportion of single rooms.
      • Moore G.
      • Ali S.
      • FitzGerald G.
      • Muzslay M.
      • Atkinson S.
      • Smith S.
      • et al.
      Ward assessment of SmartIdeas Project: bringing source isolation to the patient.
      The lack of single rooms hampers effective isolation of patients known to be infected or colonized with pathogens. Where single rooms are not available, cohorting of patients affected with the same pathogen within a multioccupancy area is often practiced.
      • Yokoe D.S.
      • Mermel L.A.
      • Anderson D.J.
      • Arias K.M.
      • Burstin H.
      • Calfee D.P.
      • et al.
      A compendium of strategies to prevent healthcare-associated infections in acute care hospitals.
      • MacCannell T.
      • Umscheid C.A.
      • Agarwal R.K.
      • Lee I.
      • Kuntz G.
      • Stevenson K.B.
      Guideline for the prevention and control of norovirus gastroenteritis outbreaks in healthcare settings.
      However, increasing the number of single rooms has been associated with reduced transmission.
      • Teltsch D.Y.
      • Hanley J.
      • Loo V.
      • Goldberg P.
      • Gursahaney A.
      • Buckeridge D.L.
      Infection acquisition following intensive care unit room privatization.
      Thus, hospitals and health care administrators should ensure the adequate provision of isolation facilities through building hospitals with a high proportion of single occupancy rooms or modifying existing facilities to increase the proportion of single occupancy rooms.
      • Moore G.
      • Ali S.
      • FitzGerald G.
      • Muzslay M.
      • Atkinson S.
      • Smith S.
      • et al.
      Ward assessment of SmartIdeas Project: bringing source isolation to the patient.
      • MacCannell T.
      • Umscheid C.A.
      • Agarwal R.K.
      • Lee I.
      • Kuntz G.
      • Stevenson K.B.
      Guideline for the prevention and control of norovirus gastroenteritis outbreaks in healthcare settings.
      • Teltsch D.Y.
      • Hanley J.
      • Loo V.
      • Goldberg P.
      • Gursahaney A.
      • Buckeridge D.L.
      Infection acquisition following intensive care unit room privatization.
      • Illingworth E.
      • Taborn E.
      • Fielding D.
      • Cheesbrough J.
      • Diggle P.J.
      • Orr D.
      Is closure of entire wards necessary to control norovirus outbreaks in hospital? Comparing the effectiveness of two infection control strategies.
      “Source control” through daily bathing with chlorhexidine is another approach to reducing the shedding of pathogens, and this has been shown to reduce the transmission of MRSA and VRE.
      • Vernon M.O.
      • Hayden M.K.
      • Trick W.E.
      • Hayes R.A.
      • Blom D.W.
      • Weinstein R.A.
      • et al.
      Chlorhexidine gluconate to cleanse patients in a medical intensive care unit: the effectiveness of source control to reduce the bioburden of vancomycin-resistant enterococci.
      • Climo M.W.
      • Sepkowitz K.A.
      • Zuccotti G.
      • Fraser V.J.
      • Warren D.K.
      • Perl T.M.
      • et al.
      The effect of daily bathing with chlorhexidine on the acquisition of methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus, and healthcare-associated bloodstream infections: results of a quasi-experimental multicenter trial.
      However, most studies of the effectiveness of this intervention have been performed in ICU settings, so studies are required outside of the ICU.

      Improved cleaning and disinfection

      Effective cleaning and disinfection relies on the operator to repeatedly ensure adequate selection, formulation, distribution, and contact time of the agents used. Educational improvements designed to modify human behavior can be attempted with the support of various tools including fluorescent markers or adenosine triphosphate assays, and monitoring and feedback can improve the frequency of surface cleaning,
      • 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.
      reduce the level of environmental contamination,
      • Perugini M.R.
      • Nomi S.M.
      • Lopes G.K.
      • Belei R.A.
      • van der Heijden I.M.
      • Mostachio A.K.
      • et al.
      Impact of the reduction of environmental and equipment contamination on vancomycin-resistant enterococcus rates.
      • Goodman E.R.
      • Platt R.
      • Bass R.
      • Onderdonk A.B.
      • Yokoe D.S.
      • Huang S.S.
      Impact of an environmental cleaning intervention on the presence of methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci on surfaces in intensive care unit rooms.
      and reduce the acquisition of pathogens.
      • 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.
      • Datta R.
      • Platt R.
      • Yokoe D.S.
      • Huang S.S.
      Environmental cleaning intervention and risk of acquiring multidrug-resistant organisms from prior room occupants.
      However, no studies have evaluated the sustainability of such systematic improvements. Indeed, recent evidence indicates that altering the location of florescent 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?.
      Improvements in hospital design and materials, novel disinfectants, and cleaning/disinfection technologies should be evaluated to determine their effectiveness in improving cleaning and disinfection. For example, there has been recent discussion on “no-touch” automated room disinfection (NTD) systems, which remove or reduce the reliance on the operator to achieve adequate distribution and contact time of the active agents.
      • 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.
      HPV, aerosolized hydrogen peroxide, ultraviolet C, and pulsed-xenon ultraviolet radiation NTD systems have all shown promise and improved efficacy when compared with conventional methods.
      • Manian F.A.
      • Griesenauer S.
      • Senkel D.
      • Setzer J.M.
      • Doll S.A.
      • Perry A.M.
      • et al.
      Isolation of Acinetobacter baumannii complex and methicillin-resistant Staphylococcus aureus from hospital rooms following terminal cleaning and disinfection: can we do better?.
      • 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.
      • 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.
      • 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.
      • Stibich M.
      • Stachowiak J.
      • Tanner B.
      • Berkheiser M.
      • Moore L.
      • Raad I.
      • et al.
      Evaluation of a pulsed-xenon ultraviolet room disinfection device for impact on hospital operations and microbial reduction.
      HPV has been associated with reductions in patient acquisition and evaluations of other NTD systems with a clinical outcome are eagerly awaited.
      • Passaretti C.L.
      • Otter J.A.
      • Reich N.G.
      • Myers J.
      • Shepard J.
      • Ross T.
      • et al.
      An evaluation of environmental decontamination with hydrogen peroxide vapor for reducing the risk of patient acquisition of multidrug-resistant organisms.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • McDonald L.C.
      • Adams N.M.
      • Cooper T.
      • et al.
      Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      NTD systems are only appropriate for certain applications and should be introduced in parallel with an educational campaign to improve conventional methods.
      Antimicrobial or “self-disinfecting” surfaces and air disinfection units have shown some promise in reducing the environmental bioburden, but further evaluations with clinical outcomes are required.
      • Boswell T.C.
      • Fox P.C.
      Reduction in MRSA environmental contamination with a portable HEPA-filtration unit.
      • O’Gorman J.
      • Humphreys H.
      Application of copper to prevent and control infection. Where are we now?.
      The most appropriate strategies to address surface contamination will depend on the setting and on local epidemiology.

      Conclusion

      There is now compelling evidence from modeling of transmission routes, microbiologic studies, observational epidemiology studies, intervention studies, and outbreak reports that contaminated surfaces contribute to the transmission of hospital pathogens. The finding that admission to a room previously occupied by a patient with a hospital pathogen increases the risk of acquiring that pathogen, combined with intervention studies showing that this increased risk can be mitigated by improved environmental decontamination, provides the most powerful evidence that contaminated surfaces contribute to transmission and that more needs to be done to improve surface decontamination. Improvement strategies include interventions to reduce and contain the shedding of pathogens into the environment and interventions to improve the efficacy of cleaning and disinfection. The most appropriate strategies to address surface contamination will depend on the setting and on local epidemiology.

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