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

Healthcare Infection

Volumn 18, Issue 1, 2013, Pages 14-22

  Rutala, William A ^a,b   Weber, David J ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

disinfection; environmental surfaces; noncritical items

Indexed keywords

ANTIBIOTIC AGENT; DISINFECTANT AGENT;

ANTIBIOTIC THERAPY; ARTICLE; CLEANING; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; DISEASE TRANSMISSION; DISINFECTION; HAND WASHING; HEALTH CARE PERSONNEL; HOSPITAL ADMISSION; HOSPITAL INFECTION; HUMAN; INFECTION CONTROL; MOLECULAR TYPING; NONHUMAN; PROTECTIVE CLOTHING; ULTRAVIOLET RADIATION; WASTE MANAGEMENT;

EID: 84874877347     PISSN: 18355617     EISSN: 18355625     Source Type: Journal    
DOI: 10.1071/HI12057     Document Type: Article

References (105)

1. Weinstein RA. Epidemiology and control of nosocomial infections in adult intensive care units. Am J Med 1991; 91(Suppl. 3B): S179-84. doi:10.1016/0002-9343(91)90366-6
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. doi:10.1086/655016
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. doi:10.1086/657944
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. doi:10.1016/j.ajic.2011.08.002
5. Randle J, Arthur A, Vaughn N. Twenty-four hour observational study of hospital hand hygiene compliance. J Hosp Infect 2010; 76: 252-5. doi:10.1016/j.jhin.2010.06.027
6. Dancer SJ. The role of environmental cleaning in the control of hospital-acquired infection. J Hosp Infect 2009; 73: 378-85. doi:10.1016/j.jhin.2009.03.030
7. Boyce JM. Environmental contamination makes an important contribution to hospital infection. J Hosp Infect 2007; 65: 50-4. doi:10.1016/S0195-6701(07) 60015-2
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. doi:10.1016/j.ajic.2010.04.196
9. Rutala WA, Weber DJ. Are room decontamination units needed to prevent transmission of environmental pathogens? Infect Control Hosp Epidemiol 2011; 32: 743-7. doi:10.1086/661226
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. doi:10.1186/1471-2334-6-130
11. Huang SS, Datta R, Platt R. Risk of acquiring antibioticresistant bacteria from prior room occupants. Arch Intern Med 2006; 166: 1945-51. doi:10.1001/archinte.166.18.1945
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. doi:10.1086/658669
13. Otter JA. The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect Control Hosp Epidemiol 2011; 32: 687-99. doi:10.1086/660363
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 2013; in press.
15. Kelly C, LaMont JT. Clostridium difficile - more difficult than ever. N Engl J Med 2008; 359: 1932-40. doi:10.1056/NEJMra0707500
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. doi:10.1128/CMR.00082-09
17. Carroll KC, Bartlett JG. Biology of Clostridium difficile: implications for epidemiology and diagnosis. Annu Rev Microbiol 2011; 65: 501 doi:10.1146/annurev-micro-090110-102824
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. doi:10.1097/MOG.0b013e32834bc9a9
19. MoudgalV, Sobel JD. Clostridium difficile colitis: a review. HospPrac 2012; 40: 139-48. doi:10.3810/hp.2012.02.954
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. doi:10.1177/0148607112446703
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-bacteriahospital- 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 ControlHospEpidemiol 2011; 32: 387-90. doi:10.1086/659156
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. doi:10.1086/ 320736
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. doi:10.1128/ AAC.01443-06
25. Russell AD. Bacterial spores and chemical sporicidal agents. Clin Microbiol Rev 1990; 3: 99-119.
26. Kim KH, Fekety R, Batts DH, Brown D, Cudmore M, Silva J Jr, et al. Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated diarrhea. J Infect Dis 1981; 143: 42-50. doi:10.1093/infdis/143.1.42
27. McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989; 320: 204-10. doi:10.1056/NEJM198901263200402
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. doi:10.1016/S0002-9343(96)90008-X
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. doi:10.1086/501987
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. JMedMicrobiol 2003; 52: 573-8. doi:10.1099/ jmm.0.05179-0
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. doi:10.1016/j.diagmicrobio.2004.12.015
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. doi:10.1016/j.ajic.2006.12.006
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. doi:10.1016/0002-9343(81)90553-2
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. doi:10.1016/j.jhin.2008.10.021
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. doi:10.1136/jcp.36.1.88
37. Delmée M, Verellen G, Avesani V, Francois G. Clostridium difficile in neonates: serogrouping and epidemiology. Eur J Pediatr 1988; 147: 36-40. doi:10.1007/BF00442608
38. Cartmill TDI, Panigrahi H, WorsleyMA,McCannDC, Nice CN, Keith E. Management and control of a large outbreak of diarrhoea due to Clostridium difficile. J Hosp Infect 1994; 27: 1-15. doi:10.1016/0195- 6701(94)90063-9
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. doi:10.1086/646935
40. Al Saif N, Brazier JS. The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 1996; 45: 133-7. doi:10.1099/00222615-45-2-133
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. doi:10.1093/clinids/24.5.889
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. doi:10.1046/j.1365-2036.1998.00428.x
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.
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. doi:10.1016/S0195-6701(02)00400-0
45. Sethi AK, Al-NassarWN,NerandzicMM,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. doi:10.1086/649016
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. doi:10.1016/j.ajic.2008.07.009
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. doi:10.1186/1471-2334-8-7
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. doi:10.1086/652648
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.BMCInfect Dis 2007; 7: 61. doi:10.1186/1471-2334-7-61
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.
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. doi:10.1086/589906
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. doi:10.1128/ JCM.43.6.2685-2696.2005
53. Walker N, Gupta R, Cheesbrough J. Blood pressure cuffs: friend or foe? J Hosp Infect 2006; 63: 167-9. doi:10.1016/j.jhin.2005.10.019
54. Alleyne SA, Hussain AM, Clokie M, Jenkins DR. Stethoscopes: potential vectors of Clostridium difficile. J Hosp Infect 2009; 73: 187-9. doi:10.1016/j.jhin.2009.05.014
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. doi:10.1086/647824
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. doi:10.1086/647855
57. Bobulsky GS, Al-Nassir WN, Riggs MM, Sethi AK, Donskey CJ. Clostridium difficile skin contamination in patients with C. difficileassociated 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. doi:10.1128/ JCM.01764-07
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. doi:10.1086/502604
60. Silva J, Iezzi C. Clostridium difficile as a nosocomial pathogen. J Hosp Infect 1988; 11(Suppl. A): 378-85. doi:10.1016/0195-6701(88) 90214-9
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. doi:10.1016/0167-4943(91)90047-T
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. doi:10.1016/ j.ajic.2008.11.010
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. doi:10.1086/662586
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(Suppl. 1): S81-S92. doi:10.1086/591065
65. CohenSH,GerdingDN,Johnson S, Kelly CP,LooVG,McDonaldLC, 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. doi:10.1086/651706
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. doi:10.1016/j.ajic.2010.10.011
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 healthcareassociated Clostridium difficile infection: reviewing the evidence. Am J Gastroenterol 2010; 105: 2327-39. doi:10.1038/ajg.2010.254
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. doi:10.1111/j.1532-5415.2010.02958.x
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(RR-16): 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. doi:10.1001/jama. 289.10.1274
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. doi:10.1086/605322
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. doi:10.1086/652772
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. doi:10.1086/646840
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 Clostridiumdifficile 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 difficileassociated disease and the increased use of alcohol-based hand rubs. Infect ControlHosp Epidemiol 2006; 27: 479-83. doi:10.1086/504362
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 ofMRSAand Clostridium difficile. J Antimicrob Chemother 2008; 62: 601-7. doi:10.1093/jac/dkn199
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. doi:10.1086/524333
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 ControlHospEpidemiol 2009; 30: 346-53. doi:10.1086/596605
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. doi:10.1016/j.ajic.2009. 12.008
81. Kirkland KB, Homa KA, Lasky RA, Ptak JA, Taylor EA, Splaine ME. Impact of a hospital-wide hand hygiene initiative on healthcareassociated infections: results of an interrupted time series. BMJ Qual Saf. 2012 (Epub ahead of print) doi:10.1136/bmjqs-2012-000800
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. doi:10.1086/524329
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. doi:10.1086/591940
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. doi:10.1097/CCM.0b013e3181cdf705
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. doi:10.1016/j.ajic. 2010.10.030
88. Vohra P, Poxton IR. Efficacy of decontaminants and disinfectants against Clostridium difficile. J Med Microbiol 2011; 60: 1218-24. doi:10.1099/jmm.0. 030288-0
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. doi:10.1086/519201
90. Wilcox MH, Fawley WN. Hospital disinfectants and spore formation by Clostridium difficile. Lancet 2000; 356: 1324. doi:10.1016/S0140- 6736(00)02819-1
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. doi:10.1016/j.jhin.2011.05.016
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. doi:10.1016/j.ajic. 2005.04.240
93. Barbut F, Menuet D, VerachtenM,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 ControlHospEpidemiol 2009; 30: 507-14. doi:10.1086/597232
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. doi:10.1016/j.ajic.2010.02.009
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. doi:10.1186/1471- 2334-10-268
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. doi:10.1086/318149
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. doi:10.1086/511791
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. doi:10.1016/j.ajic.2006.08.010
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. doi:10.1016/j.ajic.2009.11.003
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. doi:10.1016/j.jhin.2010.08.012
103. Rutala WA, Gergen MF, Weber DJ. Room decontamination by ultraviolet radiation. Infect Control Hosp Epidemiol 2010; 31: 1025-9. doi:10.1086/656244
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. doi:10.1016/j.jhin.2010.12.006
105. Otter JA, Yezli S. A call for clarity when discussing hydrogen peroxide vapour and aerosol systems. J Hosp Infect 2011; 77: 83-4. doi:10.1016/j.jhin. 2010.07.023