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Role of the environment in the transmission of Clostridium difficile in health care facilities

      Recent data demonstrate that the contaminated hospital surface environment plays a key role in the transmission of Clostridium difficile. Enhanced environmental cleaning of rooms housing Clostridium difficile-infected patients is warranted, and, if additional studies demonstrate a benefit of “no-touch” methods (eg, ultraviolet irradiation, hydrogen peroxide systems), their routine use should be considered.

      Key Words

      Clostridium difficile, a gram-positive, anaerobic bacteria, was first isolated from stool in 1935. It is now recognized as the major cause of antibiotic-associated colitis.
      • Kelly C.
      • LaMont J.T.
      Clostridium difficile: more difficult than ever.
      Over the past decade, an increasing incidence has been recognized both for C difficile infection (CDI) and severe or fatal CDI.
      • Freeman J.
      • Bauer M.P.
      • Baines S.D.
      • Corver J.
      • Fawley W.N.
      • Goorhuis B.
      • et al.
      The changing epidemiology of Clostridium difficile infections.
      • Carroll K.C.
      • Bartlett J.G.
      Biology of Clostridium difficile: implications for epidemiology and diagnosis.
      • Lo Vecchio A.
      • Zacur G.M.
      Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options.
      • Moudgal V.
      • Sobel J.D.
      Clostridium difficile colitis: a review.
      • Badger V.O.
      • Ledeboer N.A.
      • Graham M.B.
      • Edmiston C.E.
      Clostridium difficile: epidemiology, pathogenesis, management, and prevention of a recalcitrant healthcare-associated pathogen.
      USA Today reported that C difficile caused 346,800 hospitalizations and more than 30,000 deaths in the United States in 2010, which represented a greater than 4-fold increase in hospitalizations from 1993.

      Eisler P. Far more could be done to stop the deadly bacteria C diff. USA Today August 20, 2012. Available from: http://www.usatoday.com/news/health/story/2012-08-16/deadly-bacteria-hospital-infections/57079514/1. Accessed November 15, 2012.

      A recent study conducted among 30 community hospitals in the southeastern United States reported that health care-associated CDI was 21% more common than methicillin-resistant Staphylococcus aureus infection.
      • Miller B.A.
      • Chen L.F.
      • Sexton D.J.
      • Anderson D.J.
      Comparison of the burdens of hospital-onset, healthcare facility-associated Clostridium difficile infection and of healthcare-associated infections due to methicillin-resistant Staphylococcus aureus in community hospitals.
      Associated with the increase in CDI has been the spread of a new C difficile strain throughout the United States that is characterized as restriction endonuclease analysis group B1, North American pulsed-field gel electrophoresis type 1 (NAP 1), also described as ribotype 027 and toxinotype III. This strain is also characterized by increased production of toxins A and B, production of a binary toxin, and fluoroquinolone resistance and particularly impacts patients >65 years of age with health care exposure such as nursing home resident.
      The major mechanism of transmission of health care-associated pathogens among patients has been thought to be patient-to-patient transmission via the hands of health care providers.
      • Weinstein R.A.
      Epidemiology and control of nosocomial infections in adult intensive care units.
      Over the past decade, there has been a growing appreciation that environmental contamination of the surfaces and equipment in patient’s rooms makes an important contribution to hospital-acquired infection with methicillin-resistant Staphylococcus aureus, vancomycin-resistant Enterococcus species, norovirus, Acinetobacter species, and C difficile.
      • Boyce J.M.
      Environmental contamination makes an important contribution to hospital infection.
      • Weber D.J.
      • Rutala W.A.
      • Miller M.B.
      • Huslage K.
      • Sickbert-Bennett E.
      Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.
      • Otter J.A.
      • Yezli S.
      • French G.L.
      The role played by contaminated surfaces in the transmission of nosocomial pathogens.
      This paper will review the scientific evidence demonstrating that the contaminated environment plays an important role in the transmission of C difficile. We will also review currently recommended methods to reduce the risk of environmental-mediated transmission of C difficile and discuss potential future technologies under development to disinfect hospital room surfaces and equipment. This paper will expand and update recent publications on this same topic.
      • Weber D.J.
      • Rutala W.A.
      The role of the environment in transmission of Clostridium difficile infection in healthcare facilities.
      • Rutala W.A.
      • Weber D.J.
      Role of the hospital environment in disease transmission, with a focus on Clostridium difficile.

      Evidence that the contaminated environment plays a role in transmission of C difficile

      A number of microbiologic features of C difficile promote environmental survival and transmission of this pathogen (Table 1). These include prolonged environmental survival of spores, low inoculating dose (based on animal studies), frequent environmental contamination, continued environmental contamination despite treatment of symptomatic patients, and relative resistance to germicides. In recent years, there has been growing evidence that contamination of room surfaces and equipment plays an important role in the transmission of C difficile between patients (Table 2).
      Table 1Microbiologic features of Clostridium difficile that favor a role for environmental transmission
      • Stable in the environment for prolonged periods of time (spore forming bacillus)
      • Low inoculating dose (based on animal studies)
      • Relative resistance to germicides (antiseptics and disinfectants)
      • Fecal-oral transmission
      Table 2Evidence of the role of environmental contamination in patient-to-patient transmission
      • Frequent contamination of surfaces in rooms of patients with CDI
      • Frequent contamination of equipment in rooms of patients with CDI
      • Contamination may be found in hospital rooms of patients without CDI
      • Frequent contamination of hands or gloves of HCP caring for patients with CDI
      • Frequency of hand contamination of HCP correlated with frequency of environmental contamination
      • Frequency of CDI correlates with frequency of environmental contamination
      • Person-to-person transmission of C difficile demonstrated using molecular typing in clusters and outbreaks
      • Being admitted to room whose previous occupant had CDI is a risk factor for development of CDI
      • Enhanced environmental disinfection (with hypochlorites) has been part of interventions that control C difficile outbreaks
      • Improved room disinfection had been demonstrated to lead to decreased rates of CDI

      Environmental survival

      Vegetative C difficile bacilli survive for only a short time on hospital surfaces. Whereas vegetative bacilli survive for only 15 minutes on surfaces exposed to room air, they remain viable for up to 6 hours on moist surfaces at room temperature.
      • Buggy B.P.
      • Wilson K.H.
      • Fekety R.
      Comparison of methods for recovery of Clostridium difficile from an environmental surface.
      • Jump R.L.P.
      • Pultz M.J.
      • Donskey C.J.
      Vegetative Clostridium difficile survives in room air on moist surfaces and in gastric contents with reduced acidity: a potential mechanism to explain the association between proton pumps inhibitors and C difficile-associated diarrhea.
      On the other hand, bacterial spores are highly resistant to drying, heat, and chemical agents.
      • Russell A.D.
      Bacterial spores and chemical sporicidal agents.
      Kim et al reported that C difficile inoculated onto a floor persisted for 5 months.
      • Kim K.H.
      • Fekety R.
      • Batts D.H.
      • Brown D.
      • Cudmore M.
      • Silva Jr., J.
      • et al.
      Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated diarrhea.
      Neither storage temperature (4°C, −20°F) nor multiple cycles of refrigeration/freezing and thawing have been found to affect the viability of C difficile vegetative cells or spores.
      • Freeman J.
      • Wilcox M.H.
      The effects of storage conditions on viability of Clostridium difficile vegetative cells and spores and toxin activity in human faeces.

      Frequency and level of environmental contamination

      In 1989 McFarland et al reported that 49% of rooms occupied by symptomatic patients with C difficile were contaminated and that 29% of rooms occupied by asymptomatic patients were contaminated.
      • Freeman J.
      • Wilcox M.H.
      The effects of storage conditions on viability of Clostridium difficile vegetative cells and spores and toxin activity in human faeces.
      Since that study, numerous other studies have demonstrated widespread and frequent contamination on hospital surfaces and equipment in the rooms of patients with CDI.
      • Russell A.D.
      Bacterial spores and chemical sporicidal agents.
      • Kaatz G.W.
      • Gitlin S.D.
      • Schaberg D.R.
      • et al.
      Acquisition of Clostridium difficile from the hospital environment.
      • 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.
      • Pulvirenti J.J.
      • Gerding D.N.
      • Nathan C.
      • et al.
      Differences in the incidence of Clostridium difficile among patients infected with human immunodeficiency virus admitted to a public hospital and a private hospital.
      • McCoubrey J.
      • Starr J.
      • Martin H.
      • Poxton I.R.
      Clostridium difficile in a geriatric unit: a prospective epidemiologic study employing a novel S-layer typing method.
      • Martirosian G.
      • Szczesny A.
      • Cohen S.H.
      • Silva J.
      Analysis of Clostridium difficile-associated diarrhea among patients hospitalized in tertiary care academic hospital.
      • Dubberke E.R.
      • Reske K.A.
      • Yan Y.
      • Olsen M.A.
      • McDonald L.C.
      • Fraser V.J.
      Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities.
      In these reports, the frequency of C difficile recovered from environmental surfaces in the rooms of patients with C difficile was as follows: Kim et al, 9.3%
      • Kim K.H.
      • Fekety R.
      • Batts D.H.
      • Brown D.
      • Cudmore M.
      • Silva Jr., J.
      • et al.
      Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated diarrhea.
      ; Kaatz et al, 31.4%
      • Kaatz G.W.
      • Gitlin S.D.
      • Schaberg D.R.
      • et al.
      Acquisition of Clostridium difficile from the hospital environment.
      ; Samore et al, 58%
      • 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.
      ; Pulvirenti et al, 14.7%, 2.9%
      • Pulvirenti J.J.
      • Gerding D.N.
      • Nathan C.
      • et al.
      Differences in the incidence of Clostridium difficile among patients infected with human immunodeficiency virus admitted to a public hospital and a private hospital.
      ; McCourbrey et al, 14%
      • McCoubrey J.
      • Starr J.
      • Martin H.
      • Poxton I.R.
      Clostridium difficile in a geriatric unit: a prospective epidemiologic study employing a novel S-layer typing method.
      ; Martirosian et al, 12.2%
      • Martirosian G.
      • Szczesny A.
      • Cohen S.H.
      • Silva J.
      Analysis of Clostridium difficile-associated diarrhea among patients hospitalized in tertiary care academic hospital.
      ; and Dubberke et al, 27%.
      • Dubberke E.R.
      • Reske K.A.
      • Yan Y.
      • Olsen M.A.
      • McDonald L.C.
      • Fraser V.J.
      Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities.
      Moreover, C difficile has been isolated from surfaces in rooms of patients not colonized or infected with C difficile, although with a lower frequency.
      • Kim K.H.
      • Fekety R.
      • Batts D.H.
      • Brown D.
      • Cudmore M.
      • Silva Jr., J.
      • et al.
      Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated diarrhea.
      • Dubberke E.R.
      • Reske K.A.
      • Yan Y.
      • Olsen M.A.
      • McDonald L.C.
      • Fraser V.J.
      Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities.
      • Fekety R.
      • Kim K.-H.
      • Brown D.
      • Batts D.H.
      • Cudmore M.
      • Silva J.
      Epidemiology of antibiotic-associated colitis: isolation of Clostridium difficile from the hospital environment.
      • Mutters R.
      • Nonnenmacher C.
      • Susin C.
      • Albrecht U.
      • Kropatsch R.
      • Schumacher S.
      Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction.
      Other studies have also demonstrated a high frequency of environmental contamination but did not specify whether samples were collected from rooms of colonized or infected patients.
      • Malamou-Ladas H.
      • O’Farrell S.
      • Nash J.Q.
      • Tabaqchali S.
      Isolation of Clostridium difficile from patients and the environment of hospital wards.
      • Delmee M.
      • Verellen G.
      • Avesani V.
      • Francois G.
      Clostridium difficile in neonates: serogrouping and epidemiology.
      • Cartmill T.D.I.
      • Panigrahi H.
      • Worsley D.
      • McCann D.C.
      • Nice C.N.
      • Keith E.
      Management and control of a large outbreak of diarrhoea due to Clostridium difficile.
      • Nath S.K.
      • Thornley J.H.
      • Kelly M.
      • Kucera B.
      • On S.L.
      • Holmes B.
      • et al.
      A sustained outbreak of Clostridium difficile in a general hospital: persistence of a toxigenic clone in four units.
      • Saif N.A.
      • Brazier J.S.
      The distribution of Clostridium difficile in the environment of South Wales.
      • Cohen S.H.
      • Yajarayma J.
      • Tang J.
      • Meunzer J.
      • Gumerlock P.H.
      • Silva J.
      Isolation of various genotypes of Clostridium difficile from patients and the environment in an oncology ward.
      • Settle C.D.
      • Wilcox M.H.
      • Fawley W.N.
      • Corrado O.J.
      • Hawkey P.M.
      Prospective study of the risk of Clostridium difficile diarrhoea in elderly patients following treatment with cefotaxime or piperacillin-tazobactam.
      • Titov L.
      • Lebedkova N.
      • Shabanov A.
      • Tang V.J.
      • Cohen S.H.
      • Silva J.
      Isolation and molecular characterization of Clostridium difficile strains from patients and the hospital environment in Belarus.
      • 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.
      The frequency of environmental contamination has been associated with the time-course and treatment status of patients with CDI. Sethi et al demonstrated that the frequency of environmental contamination was highest prior to treatment, remained high at the time of resolution of diarrhea (37%), was lower at the end of treatment (14%), but again increased 1 to 4 weeks after treatment (50%).
      • Sethi A.K.
      • Al-Nassar W.N.
      • Nerandzic M.M.
      • Bobulsky G.S.
      • Donskey C.J.
      Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C difficile infection.
      Contamination of such rooms is likely a reflection of both the prolonged survival of C difficile spores and inadequate terminal room cleaning and disinfection. In addition to hospital rooms, C difficile has been recovered from physician and nurse work areas including telephones and computer keyboards.
      • Dumford 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 get electrophoresis type l strains.
      Because C difficile spores have been isolated from the air, aerial disseminating of spores, may in part, account for widespread environmental contamination in work areas and rooms not occupied by colonized or infected patients.
      • Robert K.
      • Smith C.F.
      • Snelling A.M.
      • Kerr K.G.
      • Banfield K.R.
      • Sleigh P.A.
      • et al.
      Aerial dissemination of Clostridium difficile spores.
      • Best E.L.
      • Fawley W.N.
      • Parnell P.
      • Wilcox M.H.
      The potential for airborne dispersal of Clostridium difficile from symptomatic patients.
      Most studies that evaluated the level of microbial contamination of the environment reported that surfaces were contaminated with <1- to 2-log10 C difficile.
      • Kim K.H.
      • Fekety R.
      • Batts D.H.
      • Brown D.
      • Cudmore M.
      • Silva Jr., J.
      • et al.
      Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated diarrhea.
      • Kaatz G.W.
      • Gitlin S.D.
      • Schaberg D.R.
      • et al.
      Acquisition of Clostridium difficile from the hospital environment.
      • 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.
      • Fekety R.
      • Kim K.-H.
      • Brown D.
      • Batts D.H.
      • Cudmore M.
      • Silva J.
      Epidemiology of antibiotic-associated colitis: isolation of Clostridium difficile from the hospital environment.
      • Eckstein B.C.
      • Adams D.A.
      • Eckstein E.C.
      • Rao A.
      • Sethi A.K.
      • Yadavalli G.K.
      • et al.
      Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
      However, some studies have reported somewhat higher levels of contamination.
      • Mulligan M.E.
      • George W.L.
      • Rolfe R.D.
      • Finegold S.M.
      Epidemiology aspects of Clostridium difficile induced diarrhea and colitis.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • et al.
      Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      Two studies reported >2-log10 C difficile on surfaces; one reported “1 to >200” colonies,
      • Mulligan M.E.
      • George W.L.
      • Rolfe R.D.
      • Finegold S.M.
      Epidemiology aspects of Clostridium difficile induced diarrhea and colitis.
      and a second study that sampled several sites with a sponge found up to 1,300 colonies.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • et al.
      Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      Importantly, the frequency of acquisition of C difficile has been linked with the level of environmental contamination.
      • 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.
      • 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.
      • Fawley W.N.
      • Parnell P.
      • Verity P.
      • Freeman J.
      • Wilcox M.H.
      Molecular epidemiology of endemic Clostridium difficile infection and the significance of subtypes of the United Kingdom epidemic strain (PCR ribotype 1).
      For example, Fawley et al reported that, in a ward with endemic C difficile, the incidence of CDI correlated significantly with the prevalence of environmental C difficile in ward areas closely associated with patients and health care personnel (HCP).
      • Fawley W.N.
      • Parnell P.
      • Verity P.
      • Freeman J.
      • Wilcox M.H.
      Molecular epidemiology of endemic Clostridium difficile infection and the significance of subtypes of the United Kingdom epidemic strain (PCR ribotype 1).
      C difficile has also been isolated from medical devices such as ultrasound machines, electrocardiogram machine’s blood, pulse oximeters, blood pressure cuffs,
      • Pulvirenti J.J.
      • Gerding D.N.
      • Nathan C.
      • et al.
      Differences in the incidence of Clostridium difficile among patients infected with human immunodeficiency virus admitted to a public hospital and a private hospital.
      • Dumford 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 get electrophoresis type l strains.
      • Walker N.
      • Gupta R.
      • Cheesbrough J.
      Blood pressure cuffs: friend or foe?.
      and personal equipment such as stethoscopes and flashlights.
      • Fekety R.
      • Kim K.-H.
      • Brown D.
      • Batts D.H.
      • Cudmore M.
      • Silva J.
      Epidemiology of antibiotic-associated colitis: isolation of Clostridium difficile from the hospital environment.
      • Alleyne S.A.
      • Hussain A.M.
      • Clokie M.
      • Jenkins D.R.
      Stethoscopes: potential vectors of Clostridium difficile.
      McFarland et al demonstrated in 1981 that a contaminated portable commode chair was responsible for secondary spread to 8 other patients on the ward within the span of 1 week.
      • McFarland L.V.
      • Mulligan M.E.
      • Kwok R.Y.
      • Stamm W.E.
      Nosocomial acquisition of Clostridium difficile infection.
      A before-and-after study
      • Brooks S.
      • Khan A.
      • Stoica D.
      • et al.
      Reduction in vancomycin-resistant Enterococcus and Clostridium difficile infections following change to tympanic thermometers.
      and a cross-over study
      • Jernigan J.A.
      • Siegman-Igra Y.
      • Guerrant R.C.
      • Farr B.M.
      A randomized cross-over study of disposable thermometers for prevention of Clostridium difficile and other nosocomial infections.
      have demonstrated that switching from electronic rectal thermometers to either tympanic or disposable thermometers, respectively, resulted in a decreased incidence of CDI.

      Frequency of hand contamination of patients and health care personnel

      Clostridium difficile has commonly been isolated from the skin and hands of infected patients.
      • Mutters R.
      • Nonnenmacher C.
      • Susin C.
      • Albrecht U.
      • Kropatsch R.
      • Schumacher S.
      Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction.
      • Sethi A.K.
      • Al-Nassar W.N.
      • Nerandzic M.M.
      • Bobulsky G.S.
      • Donskey C.J.
      Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C difficile infection.
      • Bobulsky G.S.
      • Al-Nassir W.N.
      • Riggs M.M.
      • Sethi A.K.
      • Donskey C.J.
      Clostridium difficile skin contamination in patients with C difficile-associated disease.
      Sethi et al demonstrated that the frequency of skin contamination of patients with CDI was similar to the frequency of stool detection.
      • Sethi A.K.
      • Al-Nassar W.N.
      • Nerandzic M.M.
      • Bobulsky G.S.
      • Donskey C.J.
      Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C difficile infection.
      C difficile has also been frequently isolated from the hands of health care personnel providing care to patients with CDI.
      • Miller B.A.
      • Chen L.F.
      • Sexton D.J.
      • Anderson D.J.
      Comparison of the burdens of hospital-onset, healthcare facility-associated Clostridium difficile infection and of healthcare-associated infections due to methicillin-resistant Staphylococcus aureus in community hospitals.
      • 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.
      • Mutters R.
      • Nonnenmacher C.
      • Susin C.
      • Albrecht U.
      • Kropatsch R.
      • Schumacher S.
      Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction.
      • Malamou-Ladas H.
      • O’Farrell S.
      • Nash J.Q.
      • Tabaqchali S.
      Isolation of Clostridium difficile from patients and the environment of hospital wards.
      The frequency of positive hand cultures for health care personnel has been shown to be strongly correlated with the intensity of environmental contamination.
      • 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.
      • Mutters R.
      • Nonnenmacher C.
      • Susin C.
      • Albrecht U.
      • Kropatsch R.
      • Schumacher S.
      Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction.
      • 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.
      For example, hand contamination was 0% when environmental contamination was 0% to 25%, 8% when environmental contamination was 26% to 50%, and 36% when environmental contamination was greater than 50%.
      • Samore M.H.
      • Venkataraman L.
      • DeGirolami P.C.
      • Arbeit R.D.
      • Karchmer A.W.
      Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.
      Bobulsky et al demonstrated that contact with the skin of a patient with CDI would lead to 1 to >100 colonies on the gloves of an investigator; contact with the skin yielded the highest number of colonies.
      • Bobulsky G.S.
      • Al-Nassir W.N.
      • Riggs M.M.
      • Sethi A.K.
      • Donskey C.J.
      Clostridium difficile skin contamination in patients with C difficile-associated disease.
      In a recent study, Guerrero et al reported that acquisition of C difficile spores on gloved hands was as likely after contact with commonly touched environmental surfaces (eg, bed rails, bedside table) as after contact with commonly examined skin sites (ie, chest, arm, hand).
      • Guerrero D.M.
      • Nerandzic M.M.
      • Jury L.A.
      • Jinno S.
      • Chang S.
      • Donskey C.J.
      Acquisition of spores on gloves hands after contact with skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.
      Importantly, C difficile has been isolated from the hands of health care personnel on wards without any known infected patients.
      • Mutters R.
      • Nonnenmacher C.
      • Susin C.
      • Albrecht U.
      • Kropatsch R.
      • Schumacher S.
      Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction.

      Evidence of person-to-person transmission using molecular typing

      Patient-to-patient transmission of C difficile has been demonstrated by time-space clustering of incident cases using molecular typing.
      • McFarland L.V.
      • Mulligan M.E.
      • Kwok R.Y.
      • Stamm W.E.
      Nosocomial acquisition of Clostridium difficile infection.
      • Kaatz G.W.
      • Gitlin S.D.
      • Schaberg D.R.
      • et al.
      Acquisition of Clostridium difficile from the hospital environment.
      • Pulvirenti J.J.
      • Gerding D.N.
      • Nathan C.
      • et al.
      Differences in the incidence of Clostridium difficile among patients infected with human immunodeficiency virus admitted to a public hospital and a private hospital.
      • Fawley W.N.
      • Parnell P.
      • Verity P.
      • Freeman J.
      • Wilcox M.H.
      Molecular epidemiology of endemic Clostridium difficile infection and the significance of subtypes of the United Kingdom epidemic strain (PCR ribotype 1).
      • Fawley W.N.
      • Freeman J.
      • Smith C.
      • Harmanus C.
      • van den Berg E.J.
      • Kuijper E.J.
      • et al.
      Use of highly discriminatory fingerprinting to analyze clusters of Clostridium difficile infection cases due to epidemic ribotype 027 strains.
      • Rexach C.E.
      • Tang-Feldman Y.J.
      • Cohen S.H.
      Spatial and temporal analysis of Clostridium difficile infections in patients at a pediatric hospital in California.
      Over time, increasingly sophisticated methods of molecular typing have been used to demonstrate person-to-person transmission of C difficile.

      Other evidence of the role of environmental contamination

      Being admitted to a room previous occupied by a patient with CDI has been demonstrated to be a risk factor for the development of CDI.
      • Silva J.
      • Iezzi C.
      Clostridium difficile as a nosocomial pathogen.
      • Monsieur I.
      • Mets T.
      • Lauwers S.
      • De Bock V.
      • Delmee M.
      Clostridium difficile infection in a geriatric ward.
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestel D.D.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium diffiicile infection.
      In a multivariate analysis of risk factors for acquisition of CDI, Shaughnessy et al reported that the hazard ratio for admission to a room whose previous occupant had CDI was 2.35 (strongest risk factor in the analysis).
      • Shaughnessy M.K.
      • Micielli R.L.
      • DePestel D.D.
      • et al.
      Evaluation of hospital room assignment and acquisition of Clostridium diffiicile infection.
      Monsieur et al described 9 patients who developed C difficile during their hospitalization; 4 of these patients stayed in rooms where the previous patients had CDI, and all acquired a type of C difficile that was isolated from a previous patient.
      • Monsieur I.
      • Mets T.
      • Lauwers S.
      • De Bock V.
      • Delmee M.
      Clostridium difficile infection in a geriatric ward.
      Improved room disinfection has led to decreased rates of CDI.
      • Kaatz G.W.
      • Gitlin S.D.
      • Schaberg D.R.
      • et al.
      Acquisition of Clostridium difficile from the hospital environment.
      • 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.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • et al.
      Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      • Salgado C.D.
      • Mauldin P.D.
      • Fogle P.J.
      • Bosso J.A.
      Analysis of an outbreak of Clostridium difficilecontrolled with enhanced control measures.
      • Orenstein R.
      • Aronhalt K.C.
      • McManus J.E.
      • Fedraw L.A.
      A targeted strategy to wipe out Clostridium difficile.

      Prevention of C difficile transmission because of contaminated environment

      Several guidelines are available from professional organizations that detail methods to prevent CDI in health care facilities.
      • Dubberke E.R.
      • Gerding D.N.
      • Classen D.
      • Arias K.M.
      • Podgorny K.
      • Anderson D.J.
      • et al.
      Strategies to prevent Clostridium difficileinfection in acute care hospitals.
      • Cohen S.H.
      • Gerding D.N.
      • Johnson S.
      • Kelly C.P.
      • Loo V.G.
      • McDonald L.C.
      • et al.
      Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA).
      • Rebmann T.
      • Carrico R.M.
      Preventing Clostridium difficile infections: an executive summary of the Association for Professionals in Infection Control and Epidemiology’s elimination guide.
      Association for Professionals in Infection Control and Epidemiology
      Guide to the elimination of Clostridium difficile in healthcare settings.
      In addition, several excellent reviews have summarized the method to prevent CDI.
      • Badger V.O.
      • Ledeboer N.A.
      • Graham M.B.
      • Edmiston C.E.
      Clostridium difficile: epidemiology, pathogenesis, management, and prevention of a recalcitrant healthcare-associated pathogen.
      • Hsu J.
      • Abad C.
      • Dinh M.
      • Safdar N.
      Prevention of endemic healthcare-associated Clostridium difficile infection: reviewing the evidence.
      • Simor A.E.
      Diagnosis, management and prevention of Clostridium difficile infection in long-term care facilities: a review.
      Key preventive measures include reducing the use of medications that are known to precipitate CDI, placing patients with CDI on Contact Precautions with use of gloves and appropriate hand hygiene, and improved room disinfection with sporicidal agents. New technologies for room disinfection are being investigated including “no-touch” methods and self-disinfecting surfaces.

      Hand hygiene

      The Guideline for Hand Hygiene in Health-Care Settings states that “none of the agents (including alcohols, chlorhexidine, hexachlorophene, iodophores, PCMX, and triclosan) used in antiseptic handwash or antiseptic hand-rub preparations are reliably sporicidal.”
      Centers for Disease Control and Prevention
      Guideline for hand hygiene in health-care settings; recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.
      Human challenge studies with Bacillus atrophaeus (surrogate for C difficile), a spore-forming bacteria, revealed that a waterless rub containing 61% ethanol was ineffective in eliminating spores but that handwashing with soap and water or water and 2% chlorhexidine gluconate eliminated 1.5-to 2.0-log10 spores with a 10-, 30-, or 60-second wash.
      • Weber D.J.
      • Sickbert-Bennett E.
      • Gergen M.F.
      • Rutala W.A.
      Efficacy of selected hand hygiene agents used to remove Bacillus atrophaeus (a surrogate of Bacillus anthracis) from contaminated hands.
      Human challenge studies with C difficile have revealed that handwashing with soap and water (or water and an antiseptic) is significantly more effective at removing C difficile spores from the hands of volunteers than are alcohol-based hand rubs.
      • Oughton M.T.
      • Loo V.G.
      • Dendukuri N.
      • Feen S.
      • Libman M.D.
      Hand hygiene with soap and water is superior to alcohol rub and antiseptic wipes for removal of Clostridium difficile.
      • Jabbar U.
      • Leischner J.
      • Kasper D.
      • et al.
      Effectiveness of alcohol-based hand rubs for removal of Clostridium difficile spores from hands.
      In general, alcohol-based hand rubs were equivalent to no intervention. Water and soap or water and chlorhexidine have similar efficacy on bare hands
      • Bettin K.
      • Clabots C.
      • Mathie P.
      • Willard K.
      • Gerding D.N.
      Effectiveness of liquid soap vs. chlorhexidine gluconate for the removal of Clostridium difficile from bare hands and gloved hands.
      likely because of emulsification of spores and physical removal from the hands via rinsing. Importantly, one study demonstrated that handshaking transferred a mean of 30% of the residual C difficile spores to the hands of recipients.
      • Jabbar U.
      • Leischner J.
      • Kasper D.
      • et al.
      Effectiveness of alcohol-based hand rubs for removal of Clostridium difficile spores from hands.
      Hospitalized patients with CDI should be placed on Contact Precautions: private room, use of gloves and gowns by both HCP and visitors when entering the room, limiting patient movement throughout the hospital, preferential use of dedicated patient care equipment, and disinfection of all shared patient care equipment between patients. Despite the evidence that handwashing with soap and water (or an antiseptic soap) is superior to the use of waterless alcohol-based hand rubs for removing C difficile in human challenge studies, current guidelines continue to recommend the widespread use of alcohol-based hand rubs to reduce the overall incidence of health care-associated infections. Multiple studies have reported that increased use of alcohol-based hand rubs was not associated with an increase in CDI and was often associated with a reduction of health care-associated infections.
      • Gordin F.M.
      • Schultz M.E.
      • Huber R.A.
      • Gill J.A.
      Reduction in nosocomial transmission of drug-resistant bacteria after introduction of an alcohol-based handrub.
      • Boyce J.M.
      • Ligi C.
      • Kohan C.
      • Dumigan D.
      • Havill N.L.
      Lack of association between the increased incidence of Clostridium difficile-associated disease and the increased use of alcohol-based hand rubs.
      • Vernaz N.
      • Sax H.
      • Pittet D.
      • Bonnabry P.
      • Schrenzel J.
      • Harbarth S.
      Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile.
      • Rupp M.E.
      • Fitzgerald T.
      • Puumala S.
      • Anderson J.R.
      • Craig R.
      • Iwen P.C.
      • et al.
      Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units.
      • Kaier K.
      • Hagist C.
      • Frank U.
      • Conrad A.
      • Meyer E.
      Two time-series analyses of the impact of antibiotic consumption and alcohol-based hand disinfection on the incidence of nosocomial methicillin-resistant Staphylococcus aureus infection and Clostridium difficile infection.
      • Knight N.
      • Strait T.
      • Anthony N.
      • et al.
      Clostridium difficile colitis: a retrospective study of incidence and severity before and after institution of an alcohol-based hand rub policy.
      • Kirkland K.B.
      • Homa K.A.
      • Lasky R.A.
      • Ptak J.A.
      • Taylor E.A.
      • Splaine M.E.
      Impact of a hospital-wide hand hygiene initiative on healthcare-associated infections: results of an interrupted time series.
      The current Centers for Disease Control and Prevention (CDC)/Healthcare Infection Control Practices Advisory Committee Guideline on Isolation recommends that HCP caring for patients with CDI use soap and water for hand hygiene rather than waterless antiseptic hand rubs.

      Siegel JD, Rhinehart E, Jackson M, Chiarello L. 2007 Guideline for isolation precautions: preventing transmission of infectious agents in healthcare. Available from: http://www.cdCgov/ncidod/dhqp/pdf/isolation2007.pdf. Accessed September 10, 2012.

      However, the most recent Infectious Diseases Society of America (IDSA)/Society for Healthcare Epidemiology of America (SHEA) Guideline recommends the use of soap (or antimicrobial soap) and water after caring for or contacting patients with CDI only in a “setting in which there is an outbreak or an increased CDI rate.”
      • Cohen S.H.
      • Gerding D.N.
      • Johnson S.
      • Kelly C.P.
      • Loo V.G.
      • McDonald L.C.
      • et al.
      Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA).

      Improved cleaning with sporicidal agents

      Multiple studies have demonstrated that surfaces in hospital rooms are poorly cleaned during terminal cleaning. Although methods of assessing the adequate cleaning varied (ie, visibly clean, ATPase, fluorescent dye, aerobic plate counts), several studies have demonstrated that less than 50% of many surfaces are cleaned.
      • Blue J.
      • O’Neill C.
      • Speziale P.
      • Revill J.
      • Ramage L.
      • Ballantyne L.
      Use of a fluorescent chemical as a quality indicator for hospital cleaning program.
      • Carling P.C.
      • Parry M.F.
      • Von Beheren S.M.
      Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.
      • Carling P.C.
      • Parry M.M.
      • Rupp M.E.
      • Po J.L.
      • Dick B.
      • Von Beheren S.
      Improving cleaning on the environment surrounding patients in 36 acute care hospitals.
      • Carling P.C.
      • Parry M.F.
      • Bruno-Murtha L.A.
      • Dick B.
      Improved environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission.
      Similar deficiencies have been reported for cleaning of portable medical equipment.
      • Havill N.L.
      • Havill H.L.
      • Mangione E.
      • Dumigan D.G.
      • Boyce J.M.
      Cleanliness of portable medical equipment disinfected by nursing staff.
      Despite terminal cleaning of hospital rooms, many surfaces remain contaminated with C difficile spores.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • et al.
      Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      This occurs most likely because many rooms are inadequately cleaned by environmental service workers and because C difficile is not susceptible to most commonly used surface disinfectants (ie, phenolics and quaternary ammonium compounds).
      Surface disinfectants such as 70% isopropanol,
      • Russell A.D.
      Bacterial spores and chemical sporicidal agents.
      phenols,
      • Russell A.D.
      Bacterial spores and chemical sporicidal agents.
      and quaternary ammonium compounds
      • Russell A.D.
      Bacterial spores and chemical sporicidal agents.
      • Vohra P.
      • Poxton I.R.
      Efficacy of decontaminants and disinfectants against Clostridium difficile.
      are not sporicidal. Furthermore, exposure to a cleaning agent or disinfectant has been shown to increase the sporulation rate of C difficile.
      • Fawley W.N.
      • Underwood S.
      • Freeman J.
      • Baines S.D.
      • Saxton K.
      • Stephenson K.
      • et al.
      Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains.
      • Wilcox M.H.
      • Fawley W.N.
      Hospital disinfectants and spore formation by Clostridium difficile.
      In a comprehensive study of 32 disinfectants using a suspension test and only 1- and 60-minute exposure times, only chlorine dioxide products achieved a >4-log10 reduction in C difficile spores under both clean (0.3% albumin) and dirty (3% albumen) conditions.
      • Speight S.
      • Moy A.
      • Macken S.
      • Chitnis R.
      • Hoffman P.N.
      • Davies A.
      • et al.
      Evaluation of the sporicidal activity of different chemical disinfectants used in hospitals against Clostridium difficile.
      Products based on hypochlorites, triamine, or a hypochlorite-based mixture only achieved a >4-log10 reduction after 60 minutes in clean and dirty conditions. Sodium hypochlorite has been demonstrated to be effective in kill C difficile spores.
      • Fawley W.N.
      • Underwood S.
      • Freeman J.
      • Baines S.D.
      • Saxton K.
      • Stephenson K.
      • et al.
      Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains.
      • Perez J.
      • Springthorpe S.
      • Sattar S.A.
      Activity of selected oxidizing microbicides against the spores of Clostridium difficile: relevance to environmental control.
      • 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.
      • Omidbakhsh N.
      Evaluation of sporicidal activities of selected environmental surface disinfectants: carrier tests with the spores of Clostridium difficile and its surrogates.
      • Alfa M.J.
      • Lo E.
      • Wald A.
      • Ducek C.
      • DeGagne P.
      • Harding G.K.M.
      Improved eradication of Clostridium difficile spores from toilets of hospitalized patients using an accelerated hydrogen peroxide as the cleaning agent.
      However, the killing is both time and concentration dependent and up to 5 to 10 minutes may be required to achieve a greater than 3-log10 reduction, especially with concentrations of less than 1,000 to 3,000 ppm.
      • Perez J.
      • Springthorpe S.
      • Sattar S.A.
      Activity of selected oxidizing microbicides against the spores of Clostridium difficile: relevance to environmental control.
      • 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.
      • Alfa M.J.
      • Lo E.
      • Wald A.
      • Ducek C.
      • DeGagne P.
      • Harding G.K.M.
      Improved eradication of Clostridium difficile spores from toilets of hospitalized patients using an accelerated hydrogen peroxide as the cleaning agent.
      Rutala et al found that wiping with a 1:10 dilution of bleach (6,000 ppm chlorine) eliminated >3.90-log10 C difficile by a combination of inactivation and physical removal.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Efficacy of different cleaning and disinfection methods against Clostridium difficilespores: importance of physical removal versus sporicidal inactivation.
      In a suspension test, an improved hydrogen peroxide product (0.5% hydrogen peroxide) demonstrated a ∼2-log10 reduction of C difficile spores compared with the >5-log10 decrease achieved with 5,000-ppm sodium hypochlorite at 1 minute.
      • Alfa M.J.
      • Lo E.
      • Wald A.
      • Ducek C.
      • DeGagne P.
      • Harding G.K.M.
      Improved eradication of Clostridium difficile spores from toilets of hospitalized patients using an accelerated hydrogen peroxide as the cleaning agent.
      The use of 1:10 diluted household bleach (hypochlorite) solutions for surface disinfection have been demonstrated to reduce CDI rates when used either in outbreak settings or when hyperendemic rates of CDI have been document.
      • Kaatz G.W.
      • Gitlin S.D.
      • Schaberg D.R.
      • et al.
      Acquisition of Clostridium difficile from the hospital environment.
      • Orenstein R.
      • Aronhalt K.C.
      • McManus J.E.
      • Fedraw L.A.
      A targeted strategy to wipe out Clostridium difficile.
      • Mayfield J.L.
      • Leet T.
      • Miller J.
      • Mundy L.M.
      Environmental control to reduce transmission of Clostridium difficile.
      • McMullen K.M.
      • Zack J.
      • Coopersmith C.M.
      • Kollef M.
      • Dubberke E.
      • Warren D.K.
      Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea.
      • Whitaker J.
      • Brown B.S.
      • Vidal S.
      • Calcaterra M.
      Designing a protocol that eliminates Clostridium difficile: a collaborative venture.
      • Hacek D.M.
      • Ogle A.M.
      • Fisher A.
      • Robicsek A.
      • Peterson L.R.
      Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile.
      For example, Mayfield et al demonstrated that initiation of room disinfection with 1:10 hypochlorite led to a decrease in CDI from 8.6 to 3.3 cases per 1,000 days (P < .05) in a bone marrow transplant unit.
      • Mayfield J.L.
      • Leet T.
      • Miller J.
      • Mundy L.M.
      Environmental control to reduce transmission of Clostridium difficile.
      Reverting back to a quaternary ammonium compound resulted in an increase in CDI to 8.1 cases per 1,000 patient-days. In a before-and-after study using bleach wipes (0.55% active chlorine) for both daily and terminal cleaning, Orenstein et al demonstrated a reduction of C difficile on 2 wards for which C difficile was hyperendemic (ward A dropped from 24.2 cases per 10,000 hospital-days to 3.5 cases, and ward B dropped from 24.1 cases per 10,000 hospital-days to 3.7 cases).
      • Orenstein R.
      • Aronhalt K.C.
      • McManus J.E.
      • Fedraw L.A.
      A targeted strategy to wipe out Clostridium difficile.
      Whereas cleaning by environmental service workers has been shown to be effective in reducing C difficile contamination in hospital rooms, surface disinfection with diluted bleach applied by research staff was even more effective.
      • Best E.L.
      • Fawley W.N.
      • Parnell P.
      • Wilcox M.H.
      The potential for airborne dispersal of Clostridium difficile from symptomatic patients.
      The CDC and Healthcare Infection Control Practices Advisory Committee recommend consistent environmental cleaning and disinfection be used as one of the control measures for C difficile and that “hypochlorite solutions (5,000 ppm) may be required if transmission continues.

      Siegel JD, Rhinehart E, Jackson M, Chiarello L. 2007 Guideline for isolation precautions: preventing transmission of infectious agents in healthcare. Available from: http://www.cdCgov/ncidod/dhqp/pdf/isolation2007.pdf. Accessed September 10, 2012.

      The 2008 IDSA/SHEA Clostridium difficile Guideline recommended that “facilities should consider using a 1:10 dilution of sodium hypochlorite (household beach) for environmental disinfection in outbreak settings and settings of hyperendemicity in conjunction with other infection prevention and control measures . . . the beach solution should have a contact time of at least 10 minutes.”
      • Dubberke E.R.
      • Gerding D.N.
      • Classen D.
      • Arias K.M.
      • Podgorny K.
      • Anderson D.J.
      • et al.
      Strategies to prevent Clostridium difficileinfection in acute care hospitals.
      The 2010 IDSA/SHEA Clostridium difficile Guideline recommends using a “chlorine-containing cleaning agent or other sporicidal agent to address environmental contamination in areas with increased rates of CDI.”
      • Cohen S.H.
      • Gerding D.N.
      • Johnson S.
      • Kelly C.P.
      • Loo V.G.
      • McDonald L.C.
      • et al.
      Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA).
      The Association for Professionals in Infection Control and Epidemiology also recommends a 1:10 dilution of hypochlorite for use when there is ongoing transmission, but they recommend a contact time of 1 minute for nonporous surfaces.
      Association for Professionals in Infection Control and Epidemiology
      Guide to the elimination of Clostridium difficile in healthcare settings.
      Multiple surface disinfectants are now Environmental Protection Agency-registered as effective against Clostridium difficile; most contain sodium hypochlorite, but several other germicides have also been registered (ethaneperoxoic acid/hydrogen peroxide, silver, terraacetylethylenediamine).

      Environmental Protection Agency. Selected EPA-registered disinfectants. Available from: http://www.epa.gov/oppad001/chemregindex.htm. Accessed September 20, 2012.

      Current evidence suggests that the Association for Professionals in Infection Control and Epidemiology recommendation for contact time is adequate to inactive C difficile spores based on the relatively low numbers of C difficile contaminating specific environmental surfaces. All the guidelines emphasize the need to provide adequate cleaning of all surfaces in the room. Ideally, noncritical patient care items, such as blood pressure cuffs, stethoscopes, and thermometers, should be dedicated to a single patient with CDI. When this is not possible, adequate cleaning and disinfection of shared items between patients should be ensured.

      “No Touch” methods for room disinfection

      New “no touch” methods have recently been introduced that provide room disinfection. The most promising of these methods uses either ultraviolet (UV) light
      • Davies A.
      • Pottage T.
      • Bennett A.
      • Walker J.
      Gaseous and air decontamination technologies for Clostridium difficile in the healthcare environment.
      • Rutala W.A.
      • Weber D.J.
      Are room decontamination units needed to prevent transmission of environmental pathogens?.
      or gaseous hydrogen peroxide.
      • 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.
      • Otter J.A.
      • Yezli S.
      A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.
      There are currently at least 3 devices available for room disinfection that use UV-C light: (1) a device (Tru-D Smart UVC; TRU-D, Memphis, TN) that emits UV-C (254 nm) and uses a computer and sensors to monitor the amount of energy delivered, (2) a second device (IRiS; Medline Industries, Inc, Mundelein, IL) that also uses UV-C irradiation, and (3) a device (Xenex Health care Services; San Antonio, TX) that uses pulsed-xenon UV radiation (200-320 nm) and a UV sensor for dose assurance. In study using Formica sheets contaminated with C difficile spores, one UV-C device was shown to eliminate > 4-log10 spores in direct line of sight and 2.43-log10 spores using indirect UV reflection within 50 minutes.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      Other investigators using the same device and similar study designs have demonstrated similar findings. Boyce et al reported log10 reductions in C difficile spores of 1.7 for the toilet to 2.9 for the floor under the bed with a mean exposure time of 67.8 minutes (range, 34.2-100.1 minutes).
      • Boyce J.M.
      • Havill N.L.
      • Moore B.A.
      Terminal decontamination of patient room using an automated mobile UV light unit.
      Nerandzic et al reported a reduction of C difficile spores at a reflected dose of 22,000 μWs/cm2 (spore-killing dose) for ∼45 minutes by >2- to 3-log10.
      • 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.
      Several different devices for the generation of hydrogen peroxide have been evaluated
      • Otter J.A.
      • Yezli S.
      A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.
      including those produced by Glosair (formerly Sterinis), which produces a dry mist (5% hydrogen peroxide, <50-ppm silver cations, <50-ppm ortho-phosporic acid); Steris, which produces vaporized hydrogen peroxide (35% hydrogen peroxide); and Bioquell, which produces hydrogen peroxide vapor (35% hydrogen peroxide).
      • Otter J.A.
      • Yezli S.
      A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.
      Both the Bioquell and Steris systems are highly sporicidal (>6-log10 reduction), whereas the Glosair system results in a ∼4-log10 reduction.
      • 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.
      In a hyperendemic setting, Boyce et al demonstrated that terminal disinfection with a device that produces hydrogen peroxide reduced the incidence of CDI on high-incidence wards and significantly reduced the incidence of the epidemic strain hospital wide.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • et al.
      Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      Few comparative trials of the different “no touch” methods have been published. A comparison of the Bioquell hydrogen peroxide system with the Tru-D UV-C system demonstrated that hydrogen peroxide achieved a 6-log10 reduction in C difficile spores inoculated onto carriers and placed in a patient room, whereas the UV-C system achieved an average log10 reduction of 2.2.
      • 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.
      The mean times to complete the hydrogen peroxide decontamination process was 153 minutes (range, 140-177 minutes), whereas UV-C decontamination required a mean length of time of 73 minutes (range, 39-100 minutes) during the study.
      To date, only a single study discussed above of a “no touch” method of room decontamination used health care-associated infections as an outcome.
      • Boyce J.M.
      • Havill N.L.
      • Otter J.A.
      • et al.
      Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
      Thus, the effectiveness of these devices to reduce health care-associated infections have not been demonstrated. Furthermore, no cost benefit studies of these devices have been published. Major limitations of all current devices include the fact that they are only able to be used for terminal disinfection because patients and staff must be removed from the room; they are costly; and their use is associated with substantial “down time” for the room decreasing room turnover. The advantages and limitations of UV light and hydrogen peroxide devices have been reviewed.
      • Rutala W.A.
      • Gergen M.F.
      • Weber D.J.
      Room decontamination with UV radiation.
      Because the different UV room disinfection devices and hydrogen peroxide methods differ in important aspects, each device should be validated as a method to prevent health care-associated infection prior to being accepted for routine use.

      Self-disinfecting surfaces

      The potential use of self-disinfecting surfaces has been reviewed.
      • Weber D.J.
      • Rutala W.A.
      Self-disinfecting surfaces.
      To date, only copper coating of room surfaces has been assessed for its effectiveness in reducing C difficile. Copper has been shown to kill greater than 6-log10 of vegetative C difficile cells within 30 minutes.
      • Wheeldon L.J.
      • Worthington T.
      • Lambert P.A.
      • Hilton A.C.
      • Lowden C.J.
      • Eilliot T.S.J.
      Antimicrobial efficacy of copper surfaces against spores and vegetative cells of Clostridium difficile: the germination theory.
      However, the same authors demonstrated no reduction in viability of dormant C difficile spores within 3 hours. Greater than 3-log10 of C difficile spores have been shown to be completely inactivated by copper surfaces in 24 to 48 hours.
      • Weaver L.
      • Michels H.T.
      • Keevil C.W.
      Survival of Clostridium difficile on copper and steel.: futuristic options for hospital hygiene.
      Copper-coated surfaces have not been demonstrated to reduce C difficile in trials using coated surfaces in patient rooms. The application of copper to prevent and control infection has been reviewed.
      • O’Gorman J.
      • Humphreys H.
      Application of copper to prevent and control infection. Where are we now?.

      Conclusion

      The incidence of health care-associated infections continues to increase. Preventing these infections will require improved antibiotic stewardship, rapid identification, and use of contact precautions for patients with CDI and enhanced environmental disinfection.

      References

        • Kelly C.
        • LaMont J.T.
        Clostridium difficile: more difficult than ever.
        New Engl J Med. 2008; 359: 1932-1940
        • Freeman J.
        • Bauer M.P.
        • Baines S.D.
        • Corver J.
        • Fawley W.N.
        • Goorhuis B.
        • et al.
        The changing epidemiology of Clostridium difficile infections.
        Clin Microbiol Rev. 2010; 23: 529-549
        • Carroll K.C.
        • Bartlett J.G.
        Biology of Clostridium difficile: implications for epidemiology and diagnosis.
        Annu Rev Microbiol. 2011; 65: 501-521
        • Lo Vecchio A.
        • Zacur G.M.
        Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options.
        Curr Opin Gastroenterol. 2012; 28: 1-9
        • Moudgal V.
        • Sobel J.D.
        Clostridium difficile colitis: a review.
        Hosp Pract (Minneap). 2012; 40: 139-148
        • Badger V.O.
        • Ledeboer N.A.
        • Graham M.B.
        • Edmiston C.E.
        Clostridium difficile: epidemiology, pathogenesis, management, and prevention of a recalcitrant healthcare-associated pathogen.
        J Parenter Enteral Nutr. 2012; 36: 645-662
      1. Eisler P. Far more could be done to stop the deadly bacteria C diff. USA Today August 20, 2012. Available from: http://www.usatoday.com/news/health/story/2012-08-16/deadly-bacteria-hospital-infections/57079514/1. Accessed November 15, 2012.

        • Miller B.A.
        • Chen L.F.
        • Sexton D.J.
        • Anderson D.J.
        Comparison of the burdens of hospital-onset, healthcare facility-associated Clostridium difficile infection and of healthcare-associated infections due to methicillin-resistant Staphylococcus aureus in community hospitals.
        Infect Control Hosp Epidemiol. 2011; 32: 387-390
        • Weinstein R.A.
        Epidemiology and control of nosocomial infections in adult intensive care units.
        Am J Med. 1991; 91: S179-S184
        • Boyce J.M.
        Environmental contamination makes an important contribution to hospital infection.
        J Hosp Infect. 2007; 65: 50-54
        • Weber D.J.
        • Rutala W.A.
        • Miller M.B.
        • Huslage K.
        • Sickbert-Bennett E.
        Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.
        Am J Infect Control. 2010; 38: S25-S33
        • Otter J.A.
        • Yezli S.
        • French G.L.
        The role played by contaminated surfaces in the transmission of nosocomial pathogens.
        Infect Control Hosp Epidemiol. 2011; 32: 687-699
        • Weber D.J.
        • Rutala W.A.
        The role of the environment in transmission of Clostridium difficile infection in healthcare facilities.
        Infect Control Hosp Epidemiol. 2011; 32: 207-209
        • Rutala W.A.
        • Weber D.J.
        Role of the hospital environment in disease transmission, with a focus on Clostridium difficile.
        Healthcare Infect. 2013; 18: 14-22
        • Buggy B.P.
        • Wilson K.H.
        • Fekety R.
        Comparison of methods for recovery of Clostridium difficile from an environmental surface.
        J Clin Microbiol. 1983; 18: 348-352
        • Jump R.L.P.
        • Pultz M.J.
        • Donskey C.J.
        Vegetative Clostridium difficile survives in room air on moist surfaces and in gastric contents with reduced acidity: a potential mechanism to explain the association between proton pumps inhibitors and C difficile-associated diarrhea.
        Antimicrob Agents Chemother. 2007; 51: 2883-2887
        • Russell A.D.
        Bacterial spores and chemical sporicidal agents.
        Clin Microbiol Rev. 1990; 3: 99-119
        • Kim K.H.
        • Fekety R.
        • Batts D.H.
        • Brown D.
        • Cudmore M.
        • Silva Jr., J.
        • et al.
        Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated diarrhea.
        J Infect Dis. 1981; 143: 42-50
        • Freeman J.
        • Wilcox M.H.
        The effects of storage conditions on viability of Clostridium difficile vegetative cells and spores and toxin activity in human faeces.
        J Clin Pathhol. 2003; 56: 126-128
        • McFarland L.V.
        • Mulligan M.E.
        • Kwok R.Y.
        • Stamm W.E.
        Nosocomial acquisition of Clostridium difficile infection.
        N Engl J Med. 1989; 320: 204-210
        • Kaatz G.W.
        • Gitlin S.D.
        • Schaberg D.R.
        • et al.
        Acquisition of Clostridium difficile from the hospital environment.
        Am J Epidemiol. 1988; 27: 1289-1294
        • Samore M.H.
        • Venkataraman L.
        • DeGirolami P.C.
        • Arbeit R.D.
        • Karchmer A.W.
        Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.
        Am J Med. 1996; 100: 32-40
        • Pulvirenti J.J.
        • Gerding D.N.
        • Nathan C.
        • et al.
        Differences in the incidence of Clostridium difficile among patients infected with human immunodeficiency virus admitted to a public hospital and a private hospital.
        Infect Control Hosp Epidemiol. 2002; 23: 641-647
        • McCoubrey J.
        • Starr J.
        • Martin H.
        • Poxton I.R.
        Clostridium difficile in a geriatric unit: a prospective epidemiologic study employing a novel S-layer typing method.
        J Med Microbiol. 2003; 52: 573-578
        • Martirosian G.
        • Szczesny A.
        • Cohen S.H.
        • Silva J.
        Analysis of Clostridium difficile-associated diarrhea among patients hospitalized in tertiary care academic hospital.
        Diag Microbiol Infect Dis. 2005; 52: 153-155
        • Dubberke E.R.
        • Reske K.A.
        • Yan Y.
        • Olsen M.A.
        • McDonald L.C.
        • Fraser V.J.
        Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities.
        Am J Infect Control. 2007; 35: 315-318
        • Fekety R.
        • Kim K.-H.
        • Brown D.
        • Batts D.H.
        • Cudmore M.
        • Silva J.
        Epidemiology of antibiotic-associated colitis: isolation of Clostridium difficile from the hospital environment.
        Am J Med. 1981; 70: 906-908
        • Mutters R.
        • Nonnenmacher C.
        • Susin C.
        • Albrecht U.
        • Kropatsch R.
        • Schumacher S.
        Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction.
        J Hosp Infect. 2009; 71: 43-48
        • Malamou-Ladas H.
        • O’Farrell S.
        • Nash J.Q.
        • Tabaqchali S.
        Isolation of Clostridium difficile from patients and the environment of hospital wards.
        J Clin Pathol. 1983; 36: 88-92
        • Delmee M.
        • Verellen G.
        • Avesani V.
        • Francois G.
        Clostridium difficile in neonates: serogrouping and epidemiology.
        Eur J Pediatr. 1988; 147: 36-40
        • Cartmill T.D.I.
        • Panigrahi H.
        • Worsley D.
        • McCann D.C.
        • Nice C.N.
        • Keith E.
        Management and control of a large outbreak of diarrhoea due to Clostridium difficile.
        J Hosp Infect. 1994; 27: 1-15
        • Nath S.K.
        • Thornley J.H.
        • Kelly M.
        • Kucera B.
        • On S.L.
        • Holmes B.
        • et al.
        A sustained outbreak of Clostridium difficile in a general hospital: persistence of a toxigenic clone in four units.
        Infect Control Hosp Epidemiol. 1994; 15: 382-389
        • Saif N.A.
        • Brazier J.S.
        The distribution of Clostridium difficile in the environment of South Wales.
        J Med Microbiol. 1996; 45: 133-137
        • Cohen S.H.
        • Yajarayma J.
        • Tang J.
        • Meunzer J.
        • Gumerlock P.H.
        • Silva J.
        Isolation of various genotypes of Clostridium difficile from patients and the environment in an oncology ward.
        Clin Infect Dis. 1997; 24: 889-893
        • Settle C.D.
        • Wilcox M.H.
        • Fawley W.N.
        • Corrado O.J.
        • Hawkey P.M.
        Prospective study of the risk of Clostridium difficile diarrhoea in elderly patients following treatment with cefotaxime or piperacillin-tazobactam.
        Aliment Pharmacol Ther. 1998; 12: 1217-1223
        • Titov L.
        • Lebedkova N.
        • Shabanov A.
        • Tang V.J.
        • Cohen S.H.
        • Silva J.
        Isolation and molecular characterization of Clostridium difficile strains from patients and the hospital environment in Belarus.
        J Clin Microbiol. 2000; 38: 1200-1202
        • Wilcox M.H.
        • Fawley W.N.
        • Wigglesworth N.
        • Parnell P.
        • Verity P.
        • Freeman J.
        Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection.
        J Hosp Infect. 2003; 54: 109-114
        • Sethi A.K.
        • Al-Nassar W.N.
        • Nerandzic M.M.
        • Bobulsky G.S.
        • Donskey C.J.
        Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C difficile infection.
        Infect Control Hosp Epidemiol. 2010; 31: 21-27
        • Dumford 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 get electrophoresis type l strains.
        Am J Infect Control. 2009; 37: 15-19
        • Robert K.
        • Smith C.F.
        • Snelling A.M.
        • Kerr K.G.
        • Banfield K.R.
        • Sleigh P.A.
        • et al.
        Aerial dissemination of Clostridium difficile spores.
        BMC Infect Dis. 2008; 8: 7
        • Best E.L.
        • Fawley W.N.
        • Parnell P.
        • Wilcox M.H.
        The potential for airborne dispersal of Clostridium difficile from symptomatic patients.
        Clin Infect Dis. 2010; 50: 1450-1457
        • Eckstein B.C.
        • Adams D.A.
        • Eckstein E.C.
        • Rao A.
        • Sethi A.K.
        • Yadavalli G.K.
        • et al.
        Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.
        BMC Infect Dis. 2007; 7: 61
        • Mulligan M.E.
        • George W.L.
        • Rolfe R.D.
        • Finegold S.M.
        Epidemiology aspects of Clostridium difficile induced diarrhea and colitis.
        Am J Clin Nutr. 1980; 33: 2533-2538
        • Boyce J.M.
        • Havill N.L.
        • Otter J.A.
        • et al.
        Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.
        Infect Control Hosp Epidemiol. 2008; 29: 723-729
        • Fawley W.N.
        • Parnell P.
        • Verity P.
        • Freeman J.
        • Wilcox M.H.
        Molecular epidemiology of endemic Clostridium difficile infection and the significance of subtypes of the United Kingdom epidemic strain (PCR ribotype 1).
        J Clin Microbiol. 2005; 43: 2685-2696
        • Walker N.
        • Gupta R.
        • Cheesbrough J.
        Blood pressure cuffs: friend or foe?.
        J Hosp Infect. 2006; 63: 167-169
        • Alleyne S.A.
        • Hussain A.M.
        • Clokie M.
        • Jenkins D.R.
        Stethoscopes: potential vectors of Clostridium difficile.
        J Hosp Infect. 2009; 73: 187-193
        • Brooks S.
        • Khan A.
        • Stoica D.
        • et al.
        Reduction in vancomycin-resistant Enterococcus and Clostridium difficile infections following change to tympanic thermometers.
        Infect Control Hosp Epidemiol. 1998; 19: 333-336
        • Jernigan J.A.
        • Siegman-Igra Y.
        • Guerrant R.C.
        • Farr B.M.
        A randomized cross-over study of disposable thermometers for prevention of Clostridium difficile and other nosocomial infections.
        Infect Control Hosp Epidemiol. 1998; 19: 494-499
        • Bobulsky G.S.
        • Al-Nassir W.N.
        • Riggs M.M.
        • Sethi A.K.
        • Donskey C.J.
        Clostridium difficile skin contamination in patients with C difficile-associated disease.
        Infect Control Hosp Epidemiol. 2008; 46: 447-450
        • Guerrero D.M.
        • Nerandzic M.M.
        • Jury L.A.
        • Jinno S.
        • Chang S.
        • Donskey C.J.
        Acquisition of spores on gloves hands after contact with skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.
        Am J Infect Control. 2012; 40: 556-558
        • Fawley W.N.
        • Freeman J.
        • Smith C.
        • Harmanus C.
        • van den Berg E.J.
        • Kuijper E.J.
        • et al.
        Use of highly discriminatory fingerprinting to analyze clusters of Clostridium difficile infection cases due to epidemic ribotype 027 strains.
        J Clin Microbiol. 2008; 46: 954-960
        • Rexach C.E.
        • Tang-Feldman Y.J.
        • Cohen S.H.
        Spatial and temporal analysis of Clostridium difficile infections in patients at a pediatric hospital in California.
        Infect Control Hosp Epidemiol. 2005; 26: 691-696
        • Silva J.
        • Iezzi C.
        Clostridium difficile as a nosocomial pathogen.
        J Hosp Infect. 1988; 11: 378-385
        • Monsieur I.
        • Mets T.
        • Lauwers S.
        • De Bock V.
        • Delmee M.
        Clostridium difficile infection in a geriatric ward.
        Arch Gerontol Geriatr. 1991; 13: 255-262
        • Shaughnessy M.K.
        • Micielli R.L.
        • DePestel D.D.
        • et al.
        Evaluation of hospital room assignment and acquisition of Clostridium diffiicile infection.
        Infect Control Hosp Epidemiol. 2011; 32: 201-206
        • Salgado C.D.
        • Mauldin P.D.
        • Fogle P.J.
        • Bosso J.A.
        Analysis of an outbreak of Clostridium difficilecontrolled with enhanced control measures.
        Am J Infect Control. 2009; 37: 458-464
        • Orenstein R.
        • Aronhalt K.C.
        • McManus J.E.
        • Fedraw L.A.
        A targeted strategy to wipe out Clostridium difficile.
        Infect Control Hosp Epidemiol. 2011; 32: 1137-1139
        • Dubberke E.R.
        • Gerding D.N.
        • Classen D.
        • Arias K.M.
        • Podgorny K.
        • Anderson D.J.
        • et al.
        Strategies to prevent Clostridium difficileinfection in acute care hospitals.
        Infect Control Hosp Epidemiol. 2008; 29: S81-S92
        • Cohen S.H.
        • Gerding D.N.
        • Johnson S.
        • Kelly C.P.
        • Loo V.G.
        • McDonald L.C.
        • et al.
        Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the Society for Healthcare Epidemiology of America (SHEA) and the Infectious Diseases Society of America (IDSA).
        Infect Control Hosp Epidemiol. 2010; 31: 431-455
        • Rebmann T.
        • Carrico R.M.
        Preventing Clostridium difficile infections: an executive summary of the Association for Professionals in Infection Control and Epidemiology’s elimination guide.
        Am J Infect Control. 2011; 39: 239-242
        • Association for Professionals in Infection Control and Epidemiology
        Guide to the elimination of Clostridium difficile in healthcare settings.
        APIC, Washington [DC]2008
        • Hsu J.
        • Abad C.
        • Dinh M.
        • Safdar N.
        Prevention of endemic healthcare-associated Clostridium difficile infection: reviewing the evidence.
        Am J Gastroenterol. 2010; 105: 2327-2339
        • Simor A.E.
        Diagnosis, management and prevention of Clostridium difficile infection in long-term care facilities: a review.
        J Am Geriatr Soc. 2010; 58: 1556-1564
        • Centers for Disease Control and Prevention
        Guideline for hand hygiene in health-care settings; recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force.
        MMWR. 2002; 51: 1-45
        • Weber D.J.
        • Sickbert-Bennett E.
        • Gergen M.F.
        • Rutala W.A.
        Efficacy of selected hand hygiene agents used to remove Bacillus atrophaeus (a surrogate of Bacillus anthracis) from contaminated hands.
        JAMA. 2003; 289: 1274-1277
        • Oughton M.T.
        • Loo V.G.
        • Dendukuri N.
        • Feen S.
        • Libman M.D.
        Hand hygiene with soap and water is superior to alcohol rub and antiseptic wipes for removal of Clostridium difficile.
        Infect Control Hosp Epidemiol. 2009; 30: 939-944
        • Jabbar U.
        • Leischner J.
        • Kasper D.
        • et al.
        Effectiveness of alcohol-based hand rubs for removal of Clostridium difficile spores from hands.
        Infect Control Hosp Epidemiol. 2010; 31: 565-570
        • Bettin K.
        • Clabots C.
        • Mathie P.
        • Willard K.
        • Gerding D.N.
        Effectiveness of liquid soap vs. chlorhexidine gluconate for the removal of Clostridium difficile from bare hands and gloved hands.
        Infect Control Hosp Epidemiol. 1994; 15: 697-702
        • Gordin F.M.
        • Schultz M.E.
        • Huber R.A.
        • Gill J.A.
        Reduction in nosocomial transmission of drug-resistant bacteria after introduction of an alcohol-based handrub.
        Infect Control Hosp Epidemiol. 2005; 26: 650-653
        • Boyce J.M.
        • Ligi C.
        • Kohan C.
        • Dumigan D.
        • Havill N.L.
        Lack of association between the increased incidence of Clostridium difficile-associated disease and the increased use of alcohol-based hand rubs.
        Infect Control Hosp Epidemiol. 2006; 27: 479-483
        • Vernaz N.
        • Sax H.
        • Pittet D.
        • Bonnabry P.
        • Schrenzel J.
        • Harbarth S.
        Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile.
        J Antimicrob Chemother. 2008; 62: 601-607
        • Rupp M.E.
        • Fitzgerald T.
        • Puumala S.
        • Anderson J.R.
        • Craig R.
        • Iwen P.C.
        • et al.
        Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units.
        Infect Control Hosp Epidemiol. 2008; 29: 8-15
        • Kaier K.
        • Hagist C.
        • Frank U.
        • Conrad A.
        • Meyer E.
        Two time-series analyses of the impact of antibiotic consumption and alcohol-based hand disinfection on the incidence of nosocomial methicillin-resistant Staphylococcus aureus infection and Clostridium difficile infection.
        Infect Control Hosp Epidemiol. 2009; 30: 346-353
        • Knight N.
        • Strait T.
        • Anthony N.
        • et al.
        Clostridium difficile colitis: a retrospective study of incidence and severity before and after institution of an alcohol-based hand rub policy.
        Am J Infect Control. 2010; 38: 523-528
        • Kirkland K.B.
        • Homa K.A.
        • Lasky R.A.
        • Ptak J.A.
        • Taylor E.A.
        • Splaine M.E.
        Impact of a hospital-wide hand hygiene initiative on healthcare-associated infections: results of an interrupted time series.
        BMJ Qual Saf. 2012; 21: 1019-1026
      2. Siegel JD, Rhinehart E, Jackson M, Chiarello L. 2007 Guideline for isolation precautions: preventing transmission of infectious agents in healthcare. Available from: http://www.cdCgov/ncidod/dhqp/pdf/isolation2007.pdf. Accessed September 10, 2012.

        • Blue J.
        • O’Neill C.
        • Speziale P.
        • Revill J.
        • Ramage L.
        • Ballantyne L.
        Use of a fluorescent chemical as a quality indicator for hospital cleaning program.
        Can J Infect Control. 2008; 23: 216-219
        • Carling P.C.
        • Parry M.F.
        • Von Beheren S.M.
        Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.
        Infect Control Hosp Epidemiol. 2008; 29: 1-7
        • Carling P.C.
        • Parry M.M.
        • Rupp M.E.
        • Po J.L.
        • Dick B.
        • Von Beheren S.
        Improving cleaning on the environment surrounding patients in 36 acute care hospitals.
        Infect Control Hosp Epidemiol. 2008; 29: 1035-1041
        • Carling P.C.
        • Parry M.F.
        • Bruno-Murtha L.A.
        • Dick B.
        Improved environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission.
        Crit Care Med. 2010; 38: 1054-1059
        • Havill N.L.
        • Havill H.L.
        • Mangione E.
        • Dumigan D.G.
        • Boyce J.M.
        Cleanliness of portable medical equipment disinfected by nursing staff.
        Am J Infect Control. 2011; 39: 602-604
        • Vohra P.
        • Poxton I.R.
        Efficacy of decontaminants and disinfectants against Clostridium difficile.
        J Med Microbiol. 2011; 60: 1218-1224
        • Fawley W.N.
        • Underwood S.
        • Freeman J.
        • Baines S.D.
        • Saxton K.
        • Stephenson K.
        • et al.
        Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains.
        Infect Control Hosp Epidemiol. 2007; 28: 920-925
        • Wilcox M.H.
        • Fawley W.N.
        Hospital disinfectants and spore formation by Clostridium difficile.
        Lancet. 2000; 356: 1324
        • Speight S.
        • Moy A.
        • Macken S.
        • Chitnis R.
        • Hoffman P.N.
        • Davies A.
        • et al.
        Evaluation of the sporicidal activity of different chemical disinfectants used in hospitals against Clostridium difficile.
        J Hosp Infect. 2011; 79: 18-22
        • Perez J.
        • Springthorpe S.
        • Sattar S.A.
        Activity of selected oxidizing microbicides against the spores of Clostridium difficile: relevance to environmental control.
        Am J Infect Control. 2005; 33: 320-325
        • Barbut F.
        • Menuet D.
        • Verachten M.
        • Girou E.
        Comparison of the efficacy of a hydrogen peroxide dry-mist disinfection system and sodium hypochlorite solution for eradication of Clostridium difficile spores.
        Infect Control Hosp Epidemiol. 2009; 30: 507-514
        • Omidbakhsh N.
        Evaluation of sporicidal activities of selected environmental surface disinfectants: carrier tests with the spores of Clostridium difficile and its surrogates.
        Am J Infect Control. 2010; 38: 718-722
        • Alfa M.J.
        • Lo E.
        • Wald A.
        • Ducek C.
        • DeGagne P.
        • Harding G.K.M.
        Improved eradication of Clostridium difficile spores from toilets of hospitalized patients using an accelerated hydrogen peroxide as the cleaning agent.
        BMC Infect Dis. 2010; 10: 268
        • Rutala W.A.
        • Gergen M.F.
        • Weber D.J.
        Efficacy of different cleaning and disinfection methods against Clostridium difficilespores: importance of physical removal versus sporicidal inactivation.
        Infect Control Hosp Epidemiol. 2012; 33: 1255-1258
        • Mayfield J.L.
        • Leet T.
        • Miller J.
        • Mundy L.M.
        Environmental control to reduce transmission of Clostridium difficile.
        Clin Infect Dis. 2000; 31: 995-1000
        • McMullen K.M.
        • Zack J.
        • Coopersmith C.M.
        • Kollef M.
        • Dubberke E.
        • Warren D.K.
        Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea.
        Infect Control Hosp Epidemiol. 2007; 28: 205-207
        • Whitaker J.
        • Brown B.S.
        • Vidal S.
        • Calcaterra M.
        Designing a protocol that eliminates Clostridium difficile: a collaborative venture.
        Am J Infect Control. 2007; 35: 310-314
        • Hacek D.M.
        • Ogle A.M.
        • Fisher A.
        • Robicsek A.
        • Peterson L.R.
        Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile.
        Am J Infect Control. 2010; 38: 350-353
      3. Environmental Protection Agency. Selected EPA-registered disinfectants. Available from: http://www.epa.gov/oppad001/chemregindex.htm. Accessed September 20, 2012.

        • Davies A.
        • Pottage T.
        • Bennett A.
        • Walker J.
        Gaseous and air decontamination technologies for Clostridium difficile in the healthcare environment.
        J Hosp Infect. 2011; 77: 199-203
        • Rutala W.A.
        • Weber D.J.
        Are room decontamination units needed to prevent transmission of environmental pathogens?.
        Infect Control Hosp Epidemiol. 2011; 32: 743-746
        • 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.
        J Hosp Infect. 2011; 78: 171-177
        • Otter J.A.
        • Yezli S.
        A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.
        J Hosp Infect. 2011; 77: 83-84
        • Rutala W.A.
        • Gergen M.F.
        • Weber D.J.
        Room decontamination with UV radiation.
        Infect Control Hosp Epidemiol. 2010; 31: 1025-1029
        • Boyce J.M.
        • Havill N.L.
        • Moore B.A.
        Terminal decontamination of patient room using an automated mobile UV light unit.
        Infect Control Hosp Epidemiol. 2011; 32: 737-742
        • Nerandzic M.M.
        • Cadnum J.L.
        • Pultz M.J.
        • Donskey C.J.
        Evaluation of an automated ultraviolet radiation device for decontamination of Clostridium difficile and other healthcare-associated pathogens in hospital rooms.
        BMC Infect Dis. 2010; 10: 197
        • Havill N.L.
        • Moore B.A.
        • Boyce J.M.
        Comparison of the microbiological efficacy of hydrogen peroxide vapor and ultraviolet light processes for room decontamination.
        Infect Control Hosp Epidemiol. 2012; 33: 507-512
        • Weber D.J.
        • Rutala W.A.
        Self-disinfecting surfaces.
        Infect Control Hosp Epidemiol. 2012; 33: 10-13
        • Wheeldon L.J.
        • Worthington T.
        • Lambert P.A.
        • Hilton A.C.
        • Lowden C.J.
        • Eilliot T.S.J.
        Antimicrobial efficacy of copper surfaces against spores and vegetative cells of Clostridium difficile: the germination theory.
        J Antimicrob Chemother. 2008; 62: 522-535
        • Weaver L.
        • Michels H.T.
        • Keevil C.W.
        Survival of Clostridium difficile on copper and steel.: futuristic options for hospital hygiene.
        J Hosp Infect. 2008; 68: 145-151
        • O’Gorman J.
        • Humphreys H.
        Application of copper to prevent and control infection. Where are we now?.
        J Hosp Infect. 2012; 81: 217-223