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Healthcare Infection Healthcare Infection Society
Official Journal of the Australasian College for Infection Prevention and Control
REVIEW (Open Access)

Role of the hospital environment in disease transmission, with a focus on Clostridium difficile

William A. Rutala A B C and David J. Weber A B
+ Author Affiliations
- Author Affiliations

A Hospital Epidemiology, University of North Carolina Health Care, Chapel Hill, NC 27514, USA.

B Division of Infectious Diseases, University of North Carolina School of Medicine, Chapel Hill, NC 27599-7030, USA.

C Corresponding author. Email: brutala@unch.unc.edu

Healthcare Infection 18(1) 14-22 https://doi.org/10.1071/HI12057
Submitted: 14 November 2012  Accepted: 20 December 2012   Published: 27 February 2013

Journal Compilation © Australasian College for Infection Prevention and Control 2013

Abstract

Contamination of the surface environment in hospital rooms plays an important role in the transmission of several key healthcare-associated pathogens including Clostridium difficile, methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus spp. (VRE), Acinetobacter spp. and norovirus. Clostridium difficile is especially important as it is now the most common healthcare-associated pathogen in the United States. It may cause serious disease, especially in older individuals, it may survive for long periods of time in the environment and it is relatively resistant to many commonly used antiseptics and disinfectants.

Evidence that the contaminated surface environment is important in the transmission of C. difficile includes the following: (1) environmental contamination is frequent in the rooms of patients with C. difficile infection (CDI), (2) the hands/gloves of healthcare personnel are as likely to become contaminated from contact with the environment as from direct contact with the patient, (3) the higher the frequency of environmental contamination, the more frequent the contamination of the hands/gloves of healthcare providers, (4) patients admitted to a room previously occupied by a patient with CDI have an increased risk of developing C. difficile infection, and (5) improved cleaning/disinfection of the environment has led to a decrease in the incidence of C. difficile transmission.

Key measures to prevent C. difficile transmission and infection include antibiotic stewardship (minimising antibiotic use), placing patients with CDI on contact precautions, and proper cleaning and disinfection of the surfaces in hospital rooms daily and at discharge using a sporicidal disinfectant or a ‘no-touch’ method (e.g. ultraviolet light).

Additional keywords: environmental surfaces, disinfection, noncritical items.


References

[1]  Weinstein RA. Epidemiology and control of nosocomial infections in adult intensive care units. Am J Med 1991; 91 S179–84.
Epidemiology and control of nosocomial infections in adult intensive care units.Crossref | GoogleScholarGoogle Scholar |

[2]  Huslage K, Rutala WA, Sickbert-Bennett E, Weber DJ. A quantitative approach to defining high-touch surfaces in hospitals. Infect Control Hosp Epidemiol 2010; 31 850–3.
A quantitative approach to defining high-touch surfaces in hospitals.Crossref | GoogleScholarGoogle Scholar |

[3]  Stiefel U, Cadnum JL, Eckstein BC, Guerrero DM, Tima MA, Donskey CJ. Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients. Infect Control Hosp Epidemiol 2011; 32 185–7.
Contamination of hands with methicillin-resistant Staphylococcus aureus after contact with environmental surfaces and after contact with the skin of colonized patients.Crossref | GoogleScholarGoogle Scholar |

[4]  Guerrero DM, Nerandzic MM, Jury LA, Jinno S, Chang S, Donskey CJ. Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms. Am J Infect Control 2012; 40 556–8.
Acquisition of spores on gloved hands after contact with the skin of patients with Clostridium difficile infection and with environmental surfaces in their rooms.Crossref | GoogleScholarGoogle Scholar |

[5]  Randle J, Arthur A, Vaughn N. Twenty-four hour observational study of hospital hand hygiene compliance. J Hosp Infect 2010; 76 252–5.
Twenty-four hour observational study of hospital hand hygiene compliance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfotlagsg%3D%3D&md5=221cf0603c522b013b10c9b419b5273cCAS |

[6]  Dancer SJ. The role of environmental cleaning in the control of hospital-acquired infection. J Hosp Infect 2009; 73 378–85.
The role of environmental cleaning in the control of hospital-acquired infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MjmsFOqsQ%3D%3D&md5=89acbc17a0be9228b386dd194d448998CAS |

[7]  Boyce JM. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 2007; 65 50–4.
Environmental contamination makes an important contribution to hospital infection.Crossref | GoogleScholarGoogle Scholar |

[8]  Weber DJ, Rutala WA, Miller MB, 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 S25–33.
Role of hospital surfaces in the transmission of emerging health care-associated pathogens: Norovirus, Clostridium difficile, and Acinetobacter species.Crossref | GoogleScholarGoogle Scholar |

[9]  Rutala WA, Weber DJ. Are room decontamination units needed to prevent transmission of environmental pathogens? Infect Control Hosp Epidemiol 2011; 32 743–7.
Are room decontamination units needed to prevent transmission of environmental pathogens?Crossref | GoogleScholarGoogle Scholar |

[10]  Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis 2006; 6 130
How long do nosocomial pathogens persist on inanimate surfaces? A systematic review.Crossref | GoogleScholarGoogle Scholar |

[11]  Huang SS, Datta R, Platt R. Risk of acquiring antibiotic-resistant bacteria from prior room occupants. Arch Intern Med 2006; 166 1945–51.
Risk of acquiring antibiotic-resistant bacteria from prior room occupants.Crossref | GoogleScholarGoogle Scholar |

[12]  Shaughnessy MK, Micielli RL, DePestel DD, Arndt J, Strachan CL, Welch KB, et al Evaluation of hospital room assignment and acquisition of Clostridium difficile infection. Infect Control Hosp Epidemiol 2011; 32 201–6.
Evaluation of hospital room assignment and acquisition of Clostridium difficile infection.Crossref | GoogleScholarGoogle Scholar |

[13]  Otter JA. The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect Control Hosp Epidemiol 2011; 32 687–99.
The role played by contaminated surfaces in the transmission of nosocomial pathogens.Crossref | GoogleScholarGoogle Scholar |

[14]  Weber DJ, Anderson D, Sexton D, Rutala WA. Importance of the environment in the transmission of Clostridium difficile in healthcare facilities. Am J Infect Control 2013in press.;

[15]  Kelly C, LaMont JT. Clostridium difficile – more difficult than ever. N Engl J Med 2008; 359 1932–40.
Clostridium difficile – more difficult than ever.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlaitbfN&md5=dc40184944e5f2b43d808c05c2aa445fCAS |

[16]  Freeman J, Bauer MP, Baines SD, Corver J, Fawley WN, Goorhuis B, et al The changing epidemiology of Clostridium difficile infections. Clin Microbiol Rev 2010; 23 529–49.
The changing epidemiology of Clostridium difficile infections.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFWgtLjI&md5=8c7e952bc52552730dc7535c72f331b7CAS |

[17]  Carroll KC, Bartlett JG. Biology of Clostridium difficile: implications for epidemiology and diagnosis. Annu Rev Microbiol 2011; 65 501–21.
Biology of Clostridium difficile: implications for epidemiology and diagnosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVSrtLbK&md5=f700d685e36dd5ca6e5e661ee7ef79cfCAS |

[18]  Lo Vecchio A, Zacur GM. Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options. Curr Opin Gastroenterol 2012; 28 1–9.
Clostridium difficile infection: an update on epidemiology, risk factors, and therapeutic options.Crossref | GoogleScholarGoogle Scholar |

[19]  Moudgal V, Sobel JD. Clostridium difficile colitis: a review. Hosp Prac 2012; 40 139–48.
Clostridium difficile colitis: a review.Crossref | GoogleScholarGoogle Scholar |

[20]  Badger VO, Ledeboer NA, Graham MB, Edmiston CE. Clostridium difficile: epidemiology, pathogenesis, management, and prevention of a recalcitrant healthcare-associated pathogen. JPEN J Parenter Enteral Nutr 2012; 36 645–662.
Clostridium difficile: epidemiology, pathogenesis, management, and prevention of a recalcitrant healthcare-associated pathogen.Crossref | GoogleScholarGoogle Scholar |

[21]  Eisler P. Far more could be done to stop the deadly bacteria C. diff. McLean, VA: USA Today; 2012. Available online at: http://www.usatoday.com/news/health/story/2012-08-16/deadly-bacteria-hospital-infections/57079514/1 [verified 24 January 2013].

[22]  Miller BA, Chen LF, Sexton DJ, Anderson DJ. 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; 32 387–90.
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.Crossref | GoogleScholarGoogle Scholar |

[23]  Sambol SP, Tang JK, Merrigan MM, Johnson S, Gerding DN. Infection of hamsters with epidemiologically important strains of Clostridium difficile. J Infect Dis 2001; 183 1760–6.
Infection of hamsters with epidemiologically important strains of Clostridium difficile.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M3nslymtw%3D%3D&md5=fb78978a90cfaa251d9ab79fbefcce17CAS |

[24]  Jump RLP, Pultz MJ, Donskey CJ. 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 2883–7.
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.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXoslOjurc%3D&md5=629165013fa1c090f2a4e4edfc14d997CAS |

[25]  Russell AD. Bacterial spores and chemical sporicidal agents. Clin Microbiol Rev 1990; 3 99–119.
| 1:STN:280:DyaK3c3lsVGrsA%3D%3D&md5=1e6dc6dee543aacfe48581dc05fb5827CAS |

[26]  Kim KH, Fekety R, Batts DH, Brown D, Cudmore M, Silva 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.
Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated diarrhea.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7mvFeltQ%3D%3D&md5=54ccad6048069a67c05e3673de9e8e4cCAS |

[27]  McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989; 320 204–10.
Nosocomial acquisition of Clostridium difficile infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M%2FpslWhtw%3D%3D&md5=bdd9338f8033515df17935d482f8b965CAS |

[28]  Kaatz GW, Gitlin SD, Schaberg DR, Wilson KH, Kauffman CA, Seo SM, et al Acquisition of Clostridium difficile from the hospital environment. Am J Epidemiol 1988; 27 1289–94.

[29]  Samore MH, Venkataraman L, DeGirolami PC, Arbeit RD, Karchmer AW. Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea. Am J Med 1996; 100 32–40.
Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK287msVyjug%3D%3D&md5=ca9883d0d85e19ee45db08e6fdd62454CAS |

[30]  Pulvirenti JJ, Gerding DN, Nathan C, Hafiz I, Mehra T, Marsh D, 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; 23 641–7.
Differences in the incidence of Clostridium difficile among patients infected with human immunodeficiency virus admitted to a public hospital and a private hospital.Crossref | GoogleScholarGoogle Scholar |

[31]  McCoubrey J, Starr J, Martin H, Poxton IR. Clostridium difficile in a geriatric unit: a prospective epidemiologic study employing a novel S-layer typing method. J Med Microbiol 2003; 52 573–8.
Clostridium difficile in a geriatric unit: a prospective epidemiologic study employing a novel S-layer typing method.Crossref | GoogleScholarGoogle Scholar |

[32]  Martirosian G, Szczesny A, Cohen SH, Silva J. Analysis of Clostridium difficile-associated diarrhea among patients hospitalized in tertiary care academic hospital. Diagn Microbiol Infect Dis 2005; 52 153–5.
Analysis of Clostridium difficile-associated diarrhea among patients hospitalized in tertiary care academic hospital.Crossref | GoogleScholarGoogle Scholar |

[33]  Dubberke ER, Reske KA, Noble-Wang J, Thompson A, Killgore G, Mayfield J, et al Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities. Am J Infect Control 2007; 35 315–8.
Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities.Crossref | GoogleScholarGoogle Scholar |

[34]  Fekety R, Kim K-H, Brown D, Batts DH, Cudmore M, Silva J. Epidemiology of antibiotic-associated colitis: Isolation of Clostridium difficile from the hospital environment. Am J Med 1981; 70 906–8.
Epidemiology of antibiotic-associated colitis: Isolation of Clostridium difficile from the hospital environment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7lslemuw%3D%3D&md5=81265d18b284268bb7a32a289a0d900fCAS |

[35]  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 43–8.
Quantitative detection of Clostridium difficile in hospital environmental samples by real-time polymerase chain reaction.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M%2Fit1ynsw%3D%3D&md5=48dbf0d19ec9b1c1e387adbcb16dd145CAS |

[36]  Malamou-Ladas H, O’Farrell S, Nash JQ, Tabaqchali S. Isolation of Clostridium difficile from patients and the environment of hospital wards. J Clin Pathol 1983; 36 88–92.
Isolation of Clostridium difficile from patients and the environment of hospital wards.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s7gvFOjtg%3D%3D&md5=cc88f4af72d3be28e6e3e62a14845b15CAS |

[37]  Delmée M, Verellen G, Avesani V, Francois G. Clostridium difficile in neonates: serogrouping and epidemiology. Eur J Pediatr 1988; 147 36–40.
Clostridium difficile in neonates: serogrouping and epidemiology.Crossref | GoogleScholarGoogle Scholar |

[38]  Cartmill TDI, Panigrahi H, Worsley MA, McCann DC, Nice CN, Keith E. Management and control of a large outbreak of diarrhoea due to Clostridium difficile. J Hosp Infect 1994; 27 1–15.
Management and control of a large outbreak of diarrhoea due to Clostridium difficile.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2cznsFynsw%3D%3D&md5=672c2eda98e7542908df3f4d2303f3d9CAS |

[39]  Nath SK, Thornley JH, Kelly M, Kucera B, On SLW, 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; 15 382–9.
A sustained outbreak of Clostridium difficile in a general hospital: persistence of a toxigenic clone in four units.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2czmsFerug%3D%3D&md5=21b9484ded8a18e37297ced2f165dbf9CAS |

[40]  Al Saif N, Brazier JS. The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 1996; 45 133–7.
The distribution of Clostridium difficile in the environment of South Wales.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK28zhs12mtw%3D%3D&md5=cb60801e3265acc76822714106bb91d7CAS |

[41]  Cohen SH, Yajarayma J, Tang J, Meunzer J, Gumerlock PH, Silva J. Isolation of various genotypes of Clostridium difficile from patients and the environment in an oncology ward. Clin Infect Dis 1997; 24 889–93.
Isolation of various genotypes of Clostridium difficile from patients and the environment in an oncology ward.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3oslKlsg%3D%3D&md5=60a303614d82bb02b82da72ddc8ada75CAS |

[42]  Settle CD, Wilcox MH, Fawley WN, Corrado OJ, Hawkey PM. Prospective study of the risk of Clostridium difficile diarrhoea in elderly patients following treatment with cefotaxime or piperacillin-tazobactam. Aliment Pharmacol Ther 1998; 12 1217–23.
Prospective study of the risk of Clostridium difficile diarrhoea in elderly patients following treatment with cefotaxime or piperacillin-tazobactam.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlvV2ksw%3D%3D&md5=e780a59be1e7cb369aefd1f1c4833cb5CAS |

[43]  Titov L, Lebedkova N, Shabanov A, Tang VJ, Cohen SH, Silva J. Isolation and molecular characterization of Clostridium difficile strains from patients and the hospital environment in Belarus. J Clin Microbiol 2000; 38 1200–2.
| 1:CAS:528:DC%2BD3cXitVels7g%3D&md5=67bb7aa190970f30e2030abedf048182CAS |

[44]  Wilcox MH, Fawley WN, 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; 54 109–14.
Comparison of the effect of detergent versus hypochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s3pt1ahtw%3D%3D&md5=769a781e9ff8398f4e28c8ffd8e76ab1CAS |

[45]  Sethi AK, Al-Nassar WN, Nerandzic MM, Bobulsky GS, Donskey CJ. Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection. Infect Control Hosp Epidemiol 2010; 31 21–7.
Persistence of skin contamination and environmental shedding of Clostridium difficile during and after treatment of C. difficile infection.Crossref | GoogleScholarGoogle Scholar |

[46]  Dumford DM, Nerandzic MM, Eckstein BC, Donskey CJ. 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 15–9.
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.Crossref | GoogleScholarGoogle Scholar |

[47]  Roberts K, Smith CF, Snelling AM, Kerr KG, Banfield KR, Sleigh A, et al Aerial dissemination of Clostridium difficile spores. BMC Infect Dis 2008; 8 7
Aerial dissemination of Clostridium difficile spores.Crossref | GoogleScholarGoogle Scholar |

[48]  Best EL, Fawley WN, Parnell P, Wilcox MH. The potential for airborne dispersal of Clostridium difficile from symptomatic patients. Clin Infect Dis 2010; 50 1450–7.
The potential for airborne dispersal of Clostridium difficile from symptomatic patients.Crossref | GoogleScholarGoogle Scholar |

[49]  Eckstein BC, Adams DA, Eckstein EC, Rao A, Sethi AK, Yadavalli GK, 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
Reduction of Clostridium difficile and vancomycin-resistant Enterococcus contamination of environmental surfaces after an intervention to improve cleaning methods.Crossref | GoogleScholarGoogle Scholar |

[50]  Mulligan ME, George WL, Rolfe RD, Finegold SM. Epidemiology aspects of Clostridium difficile induced diarrhea and colitis. Am J Clin Nutr 1980; 33 2533–8.
| 1:STN:280:DyaL3M%2FlvFCktg%3D%3D&md5=0f1f8e2ccb09471d7aeacf2678de9c71CAS |

[51]  Boyce JM, Havill NL, Otter JA, McDonald LC, Adams NMT, Cooper T, et al Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting. Infect Control Hosp Epidemiol 2008; 29 723–9.
Impact of hydrogen peroxide room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting.Crossref | GoogleScholarGoogle Scholar |

[52]  Fawley WN, Parnell P, Verity P, Freeman J, Wilcox MH. 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 2685–96.
Molecular epidemiology of endemic Clostridium difficile infection and the significance of subtypes of the United Kingdom epidemic strain (PCR ribotype 1).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFOiu70%3D&md5=ca773346504a7479c6c383ff6eacd4f7CAS |

[53]  Walker N, Gupta R, Cheesbrough J. Blood pressure cuffs: friend or foe? J Hosp Infect 2006; 63 167–9.
Blood pressure cuffs: friend or foe?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283mvFWgtg%3D%3D&md5=b4471e93b3637c30a75b7d9408c6a853CAS |

[54]  Alleyne SA, Hussain AM, Clokie M, Jenkins DR. Stethoscopes: potential vectors of Clostridium difficile. J Hosp Infect 2009; 73 187–9.
Stethoscopes: potential vectors of Clostridium difficile.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnhvVGktw%3D%3D&md5=23709540ace440e05c554c511b36a1f0CAS |

[55]  Brooks S, Khan A, Stoica D, Griffith J, Friedman L, Mukherji R, et al Reduction in vancomycin-resistant Enterococcus and Clostridium difficile infections following change to tympanic thermometers. Infect Control Hosp Epidemiol 1998; 19 333–6.
Reduction in vancomycin-resistant Enterococcus and Clostridium difficile infections following change to tympanic thermometers.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3ntlOmsg%3D%3D&md5=d85e5bbb41611ab29ae6fbcb3ec6ef82CAS |

[56]  Jernigan JA, Siegman-Igra Y, Guerrant RC, Farr BM. A randomized cross-over study of disposable thermometers for prevention of Clostridium difficile and other nosocomial infections. Infect Control Hosp Epidemiol 1998; 19 494–9.
A randomized cross-over study of disposable thermometers for prevention of Clostridium difficile and other nosocomial infections.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czmsl2msQ%3D%3D&md5=4802f3e98aa6da57c282da4782b0f93bCAS |

[57]  Bobulsky GS, Al-Nassir WN, Riggs MM, Sethi AK, Donskey CJ. Clostridium difficile skin contamination in patients with C. difficile-associated disease. Infect Control Hosp Epidemiol 2008; 46 447–50.

[58]  Fawley WN, Freeman J, Smith C, Harmanus C, van den Berg RJ, Kuijper EJ, 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; 46 954–60.
Use of highly discriminatory fingerprinting to analyze clusters of Clostridium difficile infection cases due to epidemic ribotype 027 strains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksVeiu7s%3D&md5=6d70570e04b668c7213126f9a5bea9e0CAS |

[59]  Rexach CE, Tang-Feldman YJ, Cohen SH. Spatial and temporal analysis of Clostridium difficile infections in patients at a pediatric hospital in California. Infect Control Hosp Epidemiol 2005; 26 691–6.
Spatial and temporal analysis of Clostridium difficile infections in patients at a pediatric hospital in California.Crossref | GoogleScholarGoogle Scholar |

[60]  Silva J, Iezzi C. Clostridium difficile as a nosocomial pathogen. J Hosp Infect 1988; 11 378–85.
Clostridium difficile as a nosocomial pathogen.Crossref | GoogleScholarGoogle Scholar |

[61]  Monsieur I, Mets T, Lauwers S, De Bock V, Delmee M. Clostridium difficile infection in a geriatric ward. Arch Gerontol Geriatr 1991; 13 255–61.
Clostridium difficile infection in a geriatric ward.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2cvmsVSjtA%3D%3D&md5=def51e9df4dad560928b29307f6fb43aCAS |

[62]  Salgado CD, Mauldin PD, Fogle PJ, Bosso JA. Analysis of an outbreak of Clostridium difficile controlled with enhanced control measures. Am J Infect Control 2009; 37 458–64.
Analysis of an outbreak of Clostridium difficile controlled with enhanced control measures.Crossref | GoogleScholarGoogle Scholar |

[63]  Orenstein R, Aronhalt KC, McManus JE, Fedraw LA. A targeted strategy to wipe out Clostridium difficile. Infect Control Hosp Epidemiol 2011; 32 1137–9.
A targeted strategy to wipe out Clostridium difficile.Crossref | GoogleScholarGoogle Scholar |

[64]  Dubberke ER, Gerding DN, Classen D, Arias KM, Podgorny K, Anderson DJ, et al Strategies to prevent Clostridium difficile infection in acute care hospitals. Infect Control Hosp Epidemiol 2008; 29 S81–S92.
Strategies to prevent Clostridium difficile infection in acute care hospitals.Crossref | GoogleScholarGoogle Scholar |

[65]  Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, McDonald LC, 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; 31 431–55.
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).Crossref | GoogleScholarGoogle Scholar |

[66]  Rebmann T, Carrico RM. 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; 39 239–42.
Preventing Clostridium difficile infections: an executive summary of the Association for Professionals in Infection Control and Epidemiology’s elimination guide.Crossref | GoogleScholarGoogle Scholar |

[67]  Association for Professionals in Infection Control and Epidemiology. Guide to the elimination of Clostridium difficile in healthcare settings. Washington DC: APIC; 2008.

[68]  Hsu J, Abad C, Dinh M, Safdar N. Prevention of endemic healthcare-associated Clostridium difficile infection: reviewing the evidence. Am J Gastroenterol 2010; 105 2327–39.
Prevention of endemic healthcare-associated Clostridium difficile infection: reviewing the evidence.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cbktlKqtg%3D%3D&md5=e22e8024ae83f35cfad8d2707b3417fbCAS |

[69]  Simor AE. Diagnosis, management and prevention of Clostridium difficile infection in long-term care facilities: a review. J Am Geriatr Soc 2010; 58 1556–64.
Diagnosis, management and prevention of Clostridium difficile infection in long-term care facilities: a review.Crossref | GoogleScholarGoogle Scholar |

[70]  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 Recomm Rep 2002; 51 1–45.

[71]  Weber DJ, Sickbert-Bennett E, Gergen MF, Rutala WA. Efficacy of selected hand hygiene agents used to remove Bacillus atrophaeus (a surrogate of Bacillus anthracis) from contaminated hands. JAMA 2003; 289 1274–7.
Efficacy of selected hand hygiene agents used to remove Bacillus atrophaeus (a surrogate of Bacillus anthracis) from contaminated hands.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFyntLs%3D&md5=6e29b5d5801ce4d0908db1ad575fe1a3CAS |

[72]  Oughton MT, Loo VG, Dendukuri N, Fenen S, Libman MD. Hand hygiene with soap and water is superior to alcohol rub and antiseptic wipes for removal of Clostridium difficile. Infect Control Hosp Epidemiol 2009; 30 939–44.
Hand hygiene with soap and water is superior to alcohol rub and antiseptic wipes for removal of Clostridium difficile.Crossref | GoogleScholarGoogle Scholar |

[73]  Jabbar U, Leischner J, Kasper D, Gerber R, Sambol SP, Parada JP, et al Effectiveness of alcohol-based hand rubs for removal of Clostridium difficile spores from hands. Infect Control Hosp Epidemiol 2010; 31 565–70.
Effectiveness of alcohol-based hand rubs for removal of Clostridium difficile spores from hands.Crossref | GoogleScholarGoogle Scholar |

[74]  Bettin K, Clabots C, Mathie P, Willard K, Gerding DN. 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.
Effectiveness of liquid soap vs. chlorhexidine gluconate for the removal of Clostridium difficile from bare hands and gloved hands.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7lsFOltA%3D%3D&md5=cc189c718d15f060eee06457aeea9c69CAS |

[75]  Stuart RL, Marshall C, McLaws M-L, Boardman C, Russo PL, Harrington G, et al ASID/AICA position statement-infection control guidelines for patients with Clostridium difficile infection in healthcare settings. Healthc Infect 2011; 16 33–9.

[76]  Boyce JM, Ligi C, Kohan C, Dumigan D, Havill NL. 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; 27 479–83.
Lack of association between the increased incidence of Clostridium difficile-associated disease and the increased use of alcohol-based hand rubs.Crossref | GoogleScholarGoogle Scholar |

[77]  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; 62 601–7.
Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVShsr3O&md5=6f2051872b79b7808bf90593018832d5CAS |

[78]  Rupp ME, Fitzgerald T, Puumala S, Anderson JR, Craig RC, Iwen PC, et al Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units. Infect Control Hosp Epidemiol 2008; 29 8–15.
Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units.Crossref | GoogleScholarGoogle Scholar |

[79]  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; 30 346–53.
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.Crossref | GoogleScholarGoogle Scholar |

[80]  Knight N, Strait T, Anthony N, Lovell R, Norton HJ, Sautter R, 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; 38 523–8.
Clostridium difficile colitis: a retrospective study of incidence and severity before and after institution of an alcohol-based hand rub policy.Crossref | GoogleScholarGoogle Scholar |

[81]  Kirkland KB, Homa KA, Lasky RA, Ptak JA, Taylor EA, Splaine ME. Impact of a hospital-wide hand hygiene initiative on healthcare-associated infections: results of an interrupted time series. BMJ Qual Saf. 2012(Epub ahead of print);
Impact of a hospital-wide hand hygiene initiative on healthcare-associated infections: results of an interrupted time series.Crossref | GoogleScholarGoogle Scholar |

[82]  Siegel JD, Rhinehart E, Jackson M, Chiarello L. Guideline for isolation precautions: preventing transmission of infectious agents in healthcare. Atlanta, GA: Centers for Disease Prevention and Control; 2007 Available online at: http://www.cdc.gov/hicpac/pdf/isolation/Isolation2007.pdf [verified 24 January 2013].

[83]  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; 23 216–9.

[84]  Carling PC, Parry MF, Von Beheren SM. Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals. Infect Control Hosp Epidemiol 2008; 29 1–7.
Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1c%2FmvFOkug%3D%3D&md5=f5618d8e93a1c5167726eb4c747d52c2CAS |

[85]  Carling PC, Parry MM, Rupp ME, Po JL, Dick B, Von Beheren S. Improving cleaning on the environment surrounding patients in 36 acute care hospitals. Infect Control Hosp Epidemiol 2008; 29 1035–41.
Improving cleaning on the environment surrounding patients in 36 acute care hospitals.Crossref | GoogleScholarGoogle Scholar |

[86]  Carling PC, Parry MF, Bruno-Murtha LA, Dick B. Improved environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission. Crit Care Med 2010; 38 1054–9.
Improved environmental hygiene in 27 intensive care units to decrease multidrug-resistant bacterial transmission.Crossref | GoogleScholarGoogle Scholar |

[87]  Havill NL, Havill HL, Mangione E, Dumigan DG, Boyce JM. Cleanliness of portable medical equipment disinfected by nursing staff. Am J Infect Control 2011; 39 602–604.
Cleanliness of portable medical equipment disinfected by nursing staff.Crossref | GoogleScholarGoogle Scholar |

[88]  Vohra P, Poxton IR. Efficacy of decontaminants and disinfectants against Clostridium difficile. J Med Microbiol 2011; 60 1218–24.
Efficacy of decontaminants and disinfectants against Clostridium difficile.Crossref | GoogleScholarGoogle Scholar |

[89]  Fawley WN, Underwood S, Freeman J, Baines SD, Saxton K, Stephenson K, et al Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains. Infect Control Hosp Epidemiol 2007; 28 920–5.
Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains.Crossref | GoogleScholarGoogle Scholar |

[90]  Wilcox MH, Fawley WN. Hospital disinfectants and spore formation by Clostridium difficile. Lancet 2000; 356 1324
Hospital disinfectants and spore formation by Clostridium difficile.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3crhsVSksA%3D%3D&md5=faf33cd1c3dd4aa1212ce03c46c694b5CAS |

[91]  Speight S, Moy A, Macken S, Chitnis R, Hoffman PN, 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.
Evaluation of the sporicidal activity of different chemical disinfectants used in hospitals against Clostridium difficile.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MjmtFCntw%3D%3D&md5=2004c901921c934897925c46d7fa9bd7CAS |

[92]  Perez J, Springthorpe S, Sattar SA. Activity of selected oxidizing microbicides against the spores of Clostridium difficile: relevance to environmental control. Am J Infect Control 2005; 33 320–5.
Activity of selected oxidizing microbicides against the spores of Clostridium difficile: relevance to environmental control.Crossref | GoogleScholarGoogle Scholar |

[93]  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; 30 507–14.
Comparison of the efficacy of a hydrogen peroxide dry-mist disinfection system and sodium hypochlorite solution for eradication of Clostridium difficile spores.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MzjvFajtw%3D%3D&md5=91e4eacb79acd555a3cfc3de67a8d8cfCAS |

[94]  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; 38 718–22.
Evaluation of sporicidal activities of selected environmental surface disinfectants: carrier tests with the spores of Clostridium difficile and its surrogates.Crossref | GoogleScholarGoogle Scholar |

[95]  Alfa MJ, Lo E, Wald A, Ducek C, DeGagne P, Harding GKM. 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
Improved eradication of Clostridium difficile spores from toilets of hospitalized patients using an accelerated hydrogen peroxide as the cleaning agent.Crossref | GoogleScholarGoogle Scholar |

[96]  Rutala WA, Gergen MF, Weber DJ. Efficacy of different “cleaning/disinfection” methods against Clostridium difficile spores: Importance of physical removal versus sporicidal inactivation. Infect Control Hosp Epidemiol 2012; 33 1255–8.

[97]  Mayfield JL, Leet T, Miller J, Mundy LM. Environmental control to reduce transmission of Clostridium difficile. Clin Infect Dis 2000; 31 995–1000.
Environmental control to reduce transmission of Clostridium difficile.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7htValtw%3D%3D&md5=e6a0244d4f4534cd1dc5ea1e32dd6614CAS |

[98]  McMullen KM, Zack J, Coopersmith CM, Kollef M, Dubberke E, Warren DK. Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea. Infect Control Hosp Epidemiol 2007; 28 205–7.
Use of hypochlorite solution to decrease rates of Clostridium difficile-associated diarrhea.Crossref | GoogleScholarGoogle Scholar |

[99]  Whitaker J, Brown BS, Vidal S, Calcaterra M. Designing a protocol that eliminates Clostridium difficile: a collaborative venture. Am J Infect Control 2007; 35 310–4.
Designing a protocol that eliminates Clostridium difficile: a collaborative venture.Crossref | GoogleScholarGoogle Scholar |

[100]  Hacek DM, Ogle AM, Fisher A, Robicsek A, Peterson LR. Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile. Am J Infect Control 2010; 38 350–3.
Significant impact of terminal room cleaning with bleach on reducing nosocomial Clostridium difficile.Crossref | GoogleScholarGoogle Scholar |

[101]  Environmental Protection Agency. Selected EPA-registered disinfectants. Available online at: http://www.epa.gov/oppad001/chemregindex.htm [verified 24 January 2013].

[102]  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.
Gaseous and air decontamination technologies for Clostridium difficile in the healthcare environment.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M3hvFOhsQ%3D%3D&md5=d888a66fb250aa25880912908110a9ffCAS |

[103]  Rutala WA, Gergen MF, Weber DJ. Room decontamination by ultraviolet radiation. Infect Control Hosp Epidemiol 2010; 31 1025–9.
Room decontamination by ultraviolet radiation.Crossref | GoogleScholarGoogle Scholar |

[104]  Falagas ME, Thomaidis PC, Kotsantis IK, Sgouros K, Samonis G, Karageorgopoulos DE. Airborne hydrogen peroxide for disinfection of the hospital environment and infection control: a systematic review. J Hosp Infect 2011; 78 171–7.
Airborne hydrogen peroxide for disinfection of the hospital environment and infection control: a systematic review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MrptlKjsA%3D%3D&md5=2df3199c64074a37652c62f5f6ef8d65CAS |

[105]  Otter JA, Yezli S. A call for clarity when discussing hydrogen peroxide vapour and aerosol systems. J Hosp Infect 2011; 77 83–4.
A call for clarity when discussing hydrogen peroxide vapour and aerosol systems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M%2FmslCkuw%3D%3D&md5=89adc455ad2ab33253676c2c3fb7ec57CAS |