Hostname: page-component-745bb68f8f-5r2nc Total loading time: 0 Render date: 2025-01-20T18:17:36.605Z Has data issue: false hasContentIssue false
  • English
  • Français

Strategies to Prevent Clostridium difficile Infections in Acute Care Hospitals: 2014 Update

Published online by Cambridge University Press:  10 May 2016

Erik R. Dubberke ,
Philip Carling ,
Ruth Carrico ,
Curtis J. Donskey ,
Vivian G. Loo ,
L. Clifford McDonald ,
Lisa L. Maragakis ,
Thomas J. Sandora ,
David J. Weber  and
Deborah S. Yokoe
...Show all authors
Erik R. Dubberke*
Affiliation:
Washington University School of Medicine, St. Louis, Missouri
Philip Carling
Affiliation:
Boston University School of Medicine, Boston, Massachusetts
Ruth Carrico
Affiliation:
Division of Infectious Diseases, University of Louisville School of Medicine, Louisville, Kentucky
Curtis J. Donskey
Affiliation:
Case Western Reserve University, Louis Stokes Cleveland Veterans Affairs Medical Center, Cleveland, Ohio
Vivian G. Loo
Affiliation:
McGill University Health Centre, McGill University, Montreal, Quebec, Canada
L. Clifford McDonald
Affiliation:
Division of Healthcare Quality Promotion, Centers for Disease Control and Prevention, Atlanta, Georgia
Lisa L. Maragakis
Affiliation:
Johns Hopkins University School of Medicine, Baltimore, Maryland
Thomas J. Sandora
Affiliation:
Boston Children’s Hospital, Harvard Medical School, Boston, Massachusetts
David J. Weber
Affiliation:
School of Medicine, University of North Carolina, Chapel Hill, North Carolina
Deborah S. Yokoe
Affiliation:
Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts
Dale N. Gerding
Affiliation:
Edward Hines Jr. Veterans Affairs Hospital, Hines, Illinois; and Loyola University Chicago Stritch School of Medicine, Chicago, Illinois
*
Washington University School of Medicine, 660 South Euclid Avenue, Box 8051, St. Louis, MO 63110 ([email protected]).
Get access Rights & Permissions [Opens in a new window]

Abstract

An abstract is not available for this content so a preview has been provided. Please use the Get access link above for information on how to access this content.
Image of the first page of this content. For PDF version, please use the ‘Save PDF’ preceeding this image.'
Type
SHEA/IDSA Practice Recommendation
Information
Infection Control & Hospital Epidemiology , Volume 35 , Issue 6 , 01 June 2014 , pp. 628 - 645
Copyright
© 2014 by The Society for Healthcare Epidemiology of America. All rights reserved.

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Infect Control Hosp Epidemiol 2014;35(6):628-645

References

1. Dubberke, ER, Gerding, DN, Classen, D, et al. Strategies to prevent Clostridium difficile infections in acute care hospitals. Infect Control Hosp Epidemiol 2008;29(suppl 1):S81–S92.Google Scholar
2. Yokoe, DS, Anderson, DJ, Berenholtz, SM, et al. Introduction to “A Compendium of Strategies to Prevent Healthcare-Associated Infections in Acute Care Hospitals: 2014 Updates.” Infect Control Hosp Epidemiol 2014;35(5):455–459.Google Scholar
3. McDonald, LC, Owings, M, Jernigan, DB. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996–2003. Emerg Infect Dis 2006;12(3):409–415.CrossRefGoogle ScholarPubMed
4. 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 infection due to methicillin-resistant Staphylococcus aureus in community hospitals. Infect Control Hosp Epidemiol 2011;32(4):387–390.Google Scholar
5. Zilberberg, MD, Shorr, AF, Kollef, MH. Growth and geographic variation in hospitalizations with resistant infections, United States, 2000–2005. Emerg Infect Dis 2008;14(11):1756–1758.Google Scholar
6. Lucado, J, Gould, C, Elixhauser, A. Clostridium difficile Infection (CDI) Hospital Stays, 2009. HCUP Statistical Brief 124. Rockville, MD: Agency for Healthcare Research and Quality, 2012. http://www.hcup-us.ahrq.gov/reports/statbriefs/sb124.pdf.Google Scholar
7. Bauer, MP, Notermans, DW, van Benthem, BH, et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet 2011;377(9759):63–73.CrossRefGoogle ScholarPubMed
8. Loo, VG, Poirier, L, Miller, MA, et al. A predominantly clonal multi-institutional outbreak of Clostridium difficile–associated diarrhea with high morbidity and mortality. N Engl J Med 2005;353(23):2442–2449.Google Scholar
9. Miller, M, Gravel, D, Mulvey, M, et al. Health care–associated Clostridium difficile infection in Canada: patient age and infecting strain type are highly predictive of severe outcome and mortality. Clin Infect Dis 2010;50(2):194–201.Google Scholar
10. Denno, DM, Shaikh, N, Stapp, JR, et al. Diarrhea etiology in a pediatric emergency department: a case control study. Clin Infect Dis 2012;55(7):897–904.CrossRefGoogle Scholar
11. Feghaly, RE, Stauber, JL, Tarr, PI, Haslam, DB. Viral co-infections are common and are associated with higher bacterial burden in children with Clostridium difficile infection. J Pediatr Gastroenterol Nutr 2013;57(6):813–816.Google Scholar
12. Rousseau, C, Poilane, I, De Pontual, L, Maherault, AC, Le Monnier, A, Collignon, A. Clostridium difficile carriage in healthy infants in the community: a potential reservoir for pathogenic strains. Clin Infect Dis 2012;55(9):1209–1215.Google Scholar
13. Vital signs: preventing Clostridium difficile infections. MMWR Morb Mortal Wkly Rep 2012;61:157–162.Google Scholar
14. Campbell, RJ, Giljahn, L, Machesky, K, et al. Clostridium difficile infection in Ohio hospitals and nursing homes during 2006. Infect Control Hosp Epidemiol 2009;30(6):526–533.CrossRefGoogle ScholarPubMed
15. Dubberke, ER, Reske, KA, Yan, Y, Olsen, MA, McDonald, LC, Fraser, VJ. Clostridium difficile–associated disease in a setting of endemicity: identification of novel risk factors. Clin Infect Dis 2007;45(12):1543–1549.Google Scholar
16. Dubberke, ER, Butler, AM, Yokoe, DS, et al. Multicenter study of Clostridium difficile infection rates from 2000 to 2006. Infect Control Hosp Epidemiol 2010;31(10):1030–1037.Google Scholar
17. Kim, J, Shaklee, JF, Smathers, S, et al. Risk factors and outcomes associated with severe Clostridium difficile infection in children. Pediatr Infect Dis J 2012;31(2):134–138.Google Scholar
18. Kuijper, EJ, Barbut, F, Brazier, JS, et al. Update of Clostridium difficile infection due to PCR ribotype 027 in Europe, 2008. Euro Surveill 2008;13(31).Google Scholar
19. McDonald, LC, Killgore, GE, Thompson, A, et al. An epidemic, toxin gene–variant strain of Clostridium difficile . N Engl J Med 2005;353(23):2433–2441.CrossRefGoogle ScholarPubMed
20. Burns, DA, Heeg, D, Cartman, ST, Minton, NP. Reconsidering the sporulation characteristics of hypervirulent Clostridium difficile BI/NAP1/027. PLoS ONE 2011;6(9):e24894.CrossRefGoogle ScholarPubMed
21. Merrigan, M, Venugopal, A, Mallozzi, M, et al. Human hypervirulent Clostridium difficile strains exhibit increased sporulation as well as robust toxin production. J Bacteriol 2010;192(19):4904–4911.Google Scholar
22. Warny, M, Pepin, J, Fang, A, et al. Toxin production by an emerging strain of Clostridium difficile associated with outbreaks of severe disease in North America and Europe. Lancet 2005;366(9491):1079–1084.Google Scholar
23. Walker, AS, Eyre, DW, Wyllie, DH, et al. Relationship between bacterial strain type, host biomarkers, and mortality in Clostridium difficile infection. Clin Infect Dis 2013;56(11):1589–1600.Google Scholar
24. Black, SR, Weaver, KN, Jones, RC, et al. Clostridium difficile outbreak strain BI is highly endemic in Chicago area hospitals. Infect Control Hosp Epidemiol 2011;32(9):897–902.Google Scholar
25. Cheknis, AK, Sambol, SP, Davidson, DM, et al. Distribution of Clostridium difficile strains from a North American, European and Australian trial of treatment for C. difficile infections: 2005–2007. Anaerobe 2009;15(6):230–233.Google Scholar
26. Lessa, FC. Incidence and insights into C. difficile infection epidemiology. ID Week. October 18, 2012.Google Scholar
27. Dubberke, ER, Butler, AM, Reske, KA, et al. Attributable outcomes of endemic Clostridium difficile–associated disease in nonsurgical patients. Emerg Infect Dis 2008;14(7):1031–1038.Google Scholar
28. Dubberke, ER, Olsen, MA. Burden of Clostridium difficile on the healthcare system. Clin Infect Dis 2012;55(suppl 2):S88–S92.CrossRefGoogle ScholarPubMed
29. Hall, AJ, Curns, AT, McDonald, LC, Parashar, UD, Lopman, BA. The roles of Clostridium difficile and norovirus among gastroenteritis-associated deaths in the United States, 1999–2007. Clin Infect Dis 2012;55(2):216–223.CrossRefGoogle ScholarPubMed
30. Sammons, JS, Localio, R, Xiao, R, Coffin, SE, Zaoutis, T. Clostridium difficile infection is associated with increased risk of death and prolonged hospitalization in children. Clin Infect Dis 2013;57(1):1–8.Google Scholar
31. Pepin, J, Saheb, N, Coulombe, MA, et al. Emergence of fluoroquinolones as the predominant risk factor for Clostridium difficile–associated diarrhea: a cohort study during an epidemic in Quebec. Clin Infect Dis 2005;41(9):1254–1260.Google Scholar
32. Dial, S, Delaney, JA, Barkun, AN, Suissa, S. Use of gastric acid–suppressive agents and the risk of community-acquired Clostridium difficile–associated disease. JAMA 2005;294(23):2989–2995.Google Scholar
33. Belmares, J, Gerding, DN, Parada, JP, Miskevics, S, Weaver, F, Johnson, S. Outcome of metronidazole therapy for Clostridium difficile disease and correlation with a scoring system. J Infect 2007;55(6):495–501.Google Scholar
34. Musher, DM, Aslam, S, Logan, N, et al. Relatively poor outcome after treatment of Clostridium difficile colitis with metronidazole. Clin Infect Dis 2005;40(11):1586–1590.Google Scholar
35. Zar, FA, Bakkanagari, SR, Moorthi, KM, Davis, MB. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile–associated diarrhea, stratified by disease severity. Clin Infect Dis 2007;45(3):302–307.Google Scholar
36. Kuijper, EJ, Coignard, B, Tull, P. Emergence of Clostridium difficile–associated disease in North America and Europe. Clin Microbiol Infect 2006;12(suppl 6):2–18.Google Scholar
37. McDonald, LC, Coignard, B, Dubberke, E, Song, X, Horan, T, Kutty, PK. Recommendations for surveillance of Clostridium difficile–associated disease. Infect Control Hosp Epidemiol 2007;28(2):140–145.Google Scholar
38. Dubberke, ER, Han, Z, Bobo, L, et al. Impact of clinical symptoms on interpretation of diagnostic assays for Clostridium difficile infections. J Clin Microbiol 2011;49(8):2887–2893.Google Scholar
39. Pepin, J, Valiquette, L, Cossette, B. Mortality attributable to nosocomial Clostridium difficile–associated disease during an epidemic caused by a hypervirulent strain in Quebec. CMAJ 2005;173(9):1037–1042.Google Scholar
40. Dubberke, ER, Butler, AM, Hota, B, et al. Multicenter study of the impact of community-onset Clostridium difficile infection on surveillance for C. difficile infection. Infect Control Hosp Epidemiol 2009;30(6):518–525.Google Scholar
41. Longtin, Y, Trottier, S, Brochu, G, et al. Impact of the type of diagnostic assay on Clostridium difficile infection and complication rates in a mandatory reporting program. Clin Infect Dis 2013;56(1):67–73.Google Scholar
42. Planche, TD, Davies, KA, Coen, PG, et al. Differences in outcome according to Clostridium difficile testing method: a prospective multicentre diagnostic validation study of C difficile infection. Lancet Infect Dis 2013;13(11):936–945.Google Scholar
43. Dubberke, ER, Reske, KA, McDonald, LC, Fraser, VJ. ICD-9 codes and surveillance for Clostridium difficile–associated disease. Emerg Infect Dis 2006;12(10):1576–1579.Google Scholar
44. Cohen, SH, Gerding, DN, Johnson, S, 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(5):431–455.CrossRefGoogle Scholar
45. Litvin, M, Reske, KA, Mayfield, J, et al. Identification of a pseudo-outbreak of Clostridium difficile infection (CDI) and the effect of repeated testing, sensitivity, and specificity on perceived prevalence of CDI. Infect Control Hosp Epidemiol 2009;30(12):1166–1171.Google Scholar
46. Polage, CR, Chin, DL, Leslie, JL, Tang, J, Cohen, SH, Solnick, JV. Outcomes in patients tested for Clostridium difficile toxins. Diagn Microbiol Infect Dis 2012;74(4):369–373.Google Scholar
47. Dubberke, ER Jr, Nyazee, HA, Yokoe, DS, et al. Implementing automated surveillance for tracking Clostridium difficile infection at multiple healthcare facilities. Infect Control Hosp Epidemiol 2012;33(3):305–308.Google Scholar
48. Gase, KA, Haley, VB, Xiong, K, Van Antwerpen, C, Stricof, RL. Comparison of 2 Clostridium difficile surveillance methods: National Healthcare Safety Network’s laboratory-identified event reporting module versus clinical infection surveillance. Infect Control Hosp Epidemiol 2013;34(3):284–290.Google Scholar
49. Bauer, MP, Kuijper, EJ, van Dissel, JT. European Society of Clinical Microbiology and Infectious Diseases (ESCMID): treatment guidance document for Clostridium difficile infection (CDI). Clin Microbiol Infect 2009;15(12):1067–1079.Google Scholar
50. Simor, AE, Bradley, SF, Strausbaugh, LJ, Crossley, K, Nicolle, LE. Clostridium difficile in long-term-care facilities for the elderly. Infect Control Hosp Epidemiol 2002;23(11):696–703.Google Scholar
51. Surawicz, CM, Brandt, LJ, Binion, DG, et al. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol 2013;108(4):478–498.Google Scholar
52. Harris, AD, Bradham, DD, Baumgarten, M, Zuckerman, IH, Fink, JC, Perencevich, EN. The use and interpretation of quasi-experimental studies in infectious diseases. Clin Infect Dis 2004;38(11):1586–1591.Google Scholar
53. Stone, SP, Cooper, BS, Kibbler, CC, et al. The ORION statement: guidelines for transparent reporting of outbreak reports and intervention studies of nosocomial infection. Lancet Infect Dis 2007;7(4):282–288.Google Scholar
54. Fowler, S, Webber, A, Cooper, BS, et al. Successful use of feedback to improve antibiotic prescribing and reduce Clostridium difficile infection: a controlled interrupted time series. J Antimicrob Chemother 2007;59(5):990–995.Google Scholar
55. Valiquette, L, Cossette, B, Garant, MP, Diab, H, Pepin, J. Impact of a reduction in the use of high-risk antibiotics on the course of an epidemic of Clostridium difficile–associated disease caused by the hypervirulent NAP1/027 strain. Clin Infect Dis 2007;45(suppl 2):S112–S121.Google Scholar
56. Aldeyab, MA, Kearney, MP, Scott, MG, et al. An evaluation of the impact of antibiotic stewardship on reducing the use of high-risk antibiotics and its effect on the incidence of Clostridium difficile infection in hospital settings. J Antimicrob Chemother 2012;67(12):2988–2996.Google Scholar
57. Talpaert, MJ, Gopal, RG, Cooper, BS, Wade, P. Impact of guidelines and enhanced antibiotic stewardship on reducing broad-spectrum antibiotic usage and its effect on incidence of Clostridium difficile infection. J Antimicrob Chemother 2011;66(9):2168–2174.Google Scholar
58. 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(6):556–558.Google Scholar
59. McFarland, LV, Mulligan, ME, Kwok, RY, Stamm, WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320(4):204–210.Google Scholar
60. 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(2):185–187.CrossRefGoogle ScholarPubMed
61. Hayden, MK, Blom, DW, Lyle, EA, Moore, CG, Weinstein, RA. Risk of hand or glove contamination after contact with patients colonized with vancomycin-resistant Enterococcus or the colonized patients’ environment. Infect Control Hosp Epidemiol 2008;29(2):149–154.Google Scholar
62. Boyce, JM, Ligi, C, Kohan, C, Dumigan, D, Havill, NL. Lack of association between the increased incidence of Clostridium difficile–associated disease and the increasing use of alcohol-based hand rubs. Infect Control Hosp Epidemiol 2006;27(5):479–483.CrossRefGoogle ScholarPubMed
63. Gopal, RG, Jeanes, A, Osman, M, Aylott, C, Green, J. Marketing hand hygiene in hospitals—a case study. J Hosp Infect 2002;50(1):42–47.Google Scholar
64. Gordin, FM, Schultz, ME, Huber, RA, Gill, JA. Reduction in nosocomial transmission of drug-resistant bacteria after introduction of an alcohol-based handrub. Infect Control Hosp Epidemiol 2005;26(7):650–653.Google Scholar
65. 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 incidences of nosocomial methicillin-resistant Staphylococcus aureus infection and Clostridium difficile infection. Infect Control Hosp Epidemiol 2009;30(4):346–353.Google Scholar
66. 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(7):523–528.Google Scholar
67. Rupp, ME, Fitzgerald, T, Puumala, S, et al. Prospective, controlled, cross-over trial of alcohol-based hand gel in critical care units. Infect Control Hosp Epidemiol 2008;29(1):8–15.Google Scholar
68. 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(3):601–607.Google Scholar
69. Shaughnessy, MK, Micielli, RL, Depestel, DD, et al. Evaluation of hospital room assignment and acquisition of Clostridium difficile infection. Infect Control Hosp Epidemiol 2011;32(3):201–206.Google Scholar
70. Chang, VT, Nelson, K. The role of physical proximity in nosocomial diarrhea. Clin Infect Dis 2000;31(3):717–722.Google Scholar
71. Clabots, CR, Johnson, S, Olson, MM, Peterson, LR, Gerding, DN. Acquisition of Clostridium difficile by hospitalized patients: evidence for colonized new admissions as a source of infection. J Infect Dis 1992;166(3):561–567.Google Scholar
72. 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(1):32–40.CrossRefGoogle ScholarPubMed
73. Boyce, JM, Havill, NL, Otter, JA, et al. Impact of hydrogen peroxide vapor room decontamination on Clostridium difficile environmental contamination and transmission in a healthcare setting. Infect Control Hosp Epidemiol 2008;29(8):723–729.Google Scholar
74. Mayfield, JL, Leet, T, Miller, J, Mundy, LM. Environmental control to reduce transmission of Clostridium difficile . Clin Infect Dis 2000;31(4):995–1000.Google Scholar
75. 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(2):109–114.Google Scholar
76. Simor, AE. Diagnosis, management, and prevention of Clostridium difficile infection in long-term care facilities: a review. J Am Geriatr Soc 2010;58(8):1556–1564.Google Scholar
77. Boyce, JM, Pittet, D; Society for Healthcare Epidemiology of America, Association for Professionals in Infection Control, and Infectious Diseases Society of America. 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.Google Scholar
78. Loo, VG, Bourgault, AM, Poirier, L, et al. Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med 2011;365(18):1693–1703.Google Scholar
79. Doernberg, SB, Winston, LG, Deck, DH, Chambers, HF. Does doxycycline protect against development of Clostridium difficile infection? Clin Infect Dis 2012;55(5):615–620.Google Scholar
80. Le, F, Arora, V, Shah, DN, Salazar, M, Palmer, HR, Garey, KW. A real-world evaluation of oral vancomycin for severe Clostridium difficile infection: implications for antibiotic stewardship programs. Pharmacotherapy 2012;32(2):129–134.Google Scholar
81. Harpe, SE, Inocencio, TJ, Pakyz, AL, Oinonen, MJ, Polk, RE. Characterization of continued antibacterial therapy after diagnosis of hospital-onset Clostridium difficile infection: implications for antimicrobial stewardship. Pharmacotherapy 2012;32(8):744–754.Google Scholar
82. Frequently asked questions about Clostridium difficile for healthcare providers. Centers for Disease Control and Prevention website. 2005. http://www.cdc.gov/HAI/organisms/cdiff/Cdiff_faqs_HCP.html.Google Scholar
83. Sethi, AK, Al Nassir, 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(1):21–27.Google Scholar
84. Dubberke, ER, Reske, KA, Noble-Wang, J, et al. Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities. Am J Infect Control 2007;35(5):315–318.Google Scholar
85. Dumford, DM III, 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 gel electrophoresis type 1 strains. Am J Infect Control 2009;37(1):15–19.Google Scholar
86. Lewis, AM, Gammon, J, Hosein, I. The pros and cons of isolation and containment. J Hosp Infect 1999;43(1):19–23.Google Scholar
87. 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(6):565–570.Google Scholar
88. Oughton, MT, Loo, VG, Dendukuri, N, Fenn, 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(10):939–944.Google Scholar
89. Edmonds, SL, Zapka, C, Kasper, D, et al. Effectiveness of hand hygiene for removal of Clostridium difficile spores from hands. Infect Control Hosp Epidemiol 2013;34(3):302–305.Google Scholar
90. Boyce, JM, Havill, NL, Dumigan, DG, Golebiewski, M, Balogun, O, Rizvani, R. Monitoring the effectiveness of hospital cleaning practices by use of an adenosine triphosphate bioluminescence assay. Infect Control Hosp Epidemiol 2009;30(7):678–684.Google Scholar
91. 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):1–7.Google Scholar
92. Sitzlar, B, Deshpande, A, Fertelli, D, Kundrapu, S, Sethi, AK, Donskey, CJ. An environmental disinfection odyssey: evaluation of sequential interventions to improve disinfection of Clostridium difficile isolation rooms. Infect Control Hosp Epidemiol 2013;34(5):459–465.Google Scholar
93. Wilcox, MH, Fawley, WN, Parnell, P. Value of lysozyme agar incorporation and alkaline thioglycollate exposure for the environmental recovery of Clostridium difficile . J Hosp Infect 2000;44(1):65–69.Google Scholar
94. Abbett, SK, Yokoe, DS, Lipsitz, SR, et al. Proposed checklist of hospital interventions to decrease the incidence of healthcare-associated Clostridium difficile infection. Infect Control Hosp Epidemiol 2009;30(11):1062–1069.Google Scholar
95. 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(2):205–207.Google Scholar
96. Mermel, LA, Jefferson, J, Blanchard, K, et al. Reducing Clostridium difficile incidence, colectomies, and mortality in the hospital setting: a successful multidisciplinary approach. Jt Comm J Qual Patient Saf 2013;39(7):298–305.Google Scholar
97. Orenstein, R, Aronhalt, KC, McManus JE Jr, Fedraw, LA. A targeted strategy to wipe out Clostridium difficile . Infect Control Hosp Epidemiol 2011;32(11):1137–1139.Google Scholar
98. Kundrapu, S, Sunkesula, V, Jury, LA, Sitzlar, BM, Donskey, CJ. Daily disinfection of high-touch surfaces in isolation rooms to reduce contamination of healthcare workers’ hands. Infect Control Hosp Epidemiol 2012;33(10):1039–1042.Google Scholar
99. Kallen, AJ, Thompson, A, Ristaino, P, et al. Complete restriction of fluoroquinolone use to control an outbreak of Clostridium difficile infection at a community hospital. Infect Control Hosp Epidemiol 2009;30(3):264–272.Google Scholar
100. McNulty, C, Logan, M, Donald, IP, et al. Successful control of Clostridium difficile infection in an elderly care unit through use of a restrictive antibiotic policy. J Antimicrob Chemother 1997;40(5):707–711.Google Scholar
101. Pear, SM, Williamson, TH, Bettin, KM, Gerding, DN, Galgiani, JN. Decrease in nosocomial Clostridium difficile–associated diarrhea by restricting clindamycin use. Ann Intern Med 1994;120(4):272–277.Google Scholar
102. Johnson, S, Homann, SR, Bettin, KM, et al. Treatment of asymptomatic Clostridium difficile carriers (fecal excretors) with vancomycin or metronidazole: a randomized, placebo-controlled trial. Ann Intern Med 1992;117(4):297–302.Google Scholar
103. Kirkland, KB, Weinstein, JM. Adverse effects of contact isolation. Lancet 1999;354(9185):1177–1178.Google Scholar
104. Morgan, DJ, Diekema, DJ, Sepkowitz, K, Perencevich, EN. Adverse outcomes associated with contact precautions: a review of the literature. Am J Infect Control 2009;37(2):85–93.Google Scholar
105. Saint, S, Higgins, LA, Nallamothu, BK, Chenoweth, C. Do physicians examine patients in contact isolation less frequently? a brief report. Am J Infect Control 2003;31(6):354–356.Google Scholar
106. Stelfox, HT, Bates, DW, Redelmeier, DA. Safety of patients isolated for infection control. JAMA 2003;290(14):1899–1905.Google Scholar
107. McFarland, LV, Elmer, GW, Surawicz, CM. Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol 2002;97(7):1769–1775.Google Scholar
108. Siegel, JD, Rhinehart, E, Jackson, M, Chiarello, L. 2007 Guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control 2007;35(10 suppl 2):S65–S164.Google Scholar
109. Goldenberg, JZ, Ma, SS, Saxton, JD, et al. Probiotics for the prevention of Clostridium difficile–associated diarrhea in adults and children. Cochrane Database Syst Rev 2013;5:CD006095.Google Scholar
110. Johnston, BC, Ma, SS, Goldenberg, JZ, et al. Probiotics for the prevention of Clostridium difficile–associated diarrhea: a systematic review and meta-analysis. Ann Intern Med 2012;157(12):878–888.Google Scholar
111. Dubberke, ER, Yan, Y, Reske, KA, et al. Development and validation of a Clostridium difficile infection risk prediction model. Infect Control Hosp Epidemiol 2011;32(4):360–366.Google Scholar
112. Gupta, S, Miller, M, Mehta, V, et al. A large prospective North American epidemiologic study of hospital-associated Clostridium difficile colonization and infection. International Clostridium difficile Symposium; Bled, Slovenia; abstract O20. September 22, 2012.Google Scholar
113. Allen, SJ, Wareham, K, Wang, D, et al. Lactobacilli and bifidobacteria in the prevention of antibiotic-associated diarrhoea and Clostridium difficile diarrhoea in older inpatients (PLACIDE): a randomised, double-blind, placebo-controlled, multicentre trial. Lancet 2013;382(9900):1249–1257.Google Scholar
114. Munoz, P, Bouza, E, Cuenca-Estrella, M, et al. Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin Infect Dis 2005;40(11):1625–1634.Google Scholar
115. 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(6):507–514.Google Scholar
116. Wong, SK, Kneebone, A, Morgan, M, Henderson, CJ, Morgan, A, Jalaludin, B. Surgical management of colorectal cancer in south-western Sydney 1997–2001: a prospective series of 1293 unselected cases from six public hospitals. ANZ J Surg 2005;75(9):776–782.Google Scholar
117. McKibben, L, Horan, TC, Tokars, JI, et al. Guidance on public reporting of healthcare-associated infections: recommendations of the Healthcare Infection Control Practices Advisory Committee. Infect Control Hosp Epidemiol 2005;26(6):580–587.Google Scholar
118. Berenholtz, SM, Pham, JC, Thompson, DA, et al. Collaborative cohort study of an intervention to reduce ventilator-associated pneumonia in the intensive care unit. Infect Control Hosp Epidemiol 2011;32(4):305–314.Google Scholar
119. Farley, JE, Doughman, D, Jeeva, R, Jeffries, P, Stanley, JM. Department of Health and Human Services releases new immersive simulation experience to improve infection control knowledge and practices among health care workers and students. Am J Infect Control 2012;40(3):258–259.Google Scholar
120. Landers, T, Abusalem, S, Coty, MB, Bingham, J. Patient-centered hand hygiene: the next step in infection prevention. Am J Infect Control 2012;40(4 suppl 1):S11–S17.Google Scholar
121. Dubberke, ER. Prevention of healthcare-associated Clostridium difficile infection: what works? Infect Control Hosp Epidemiol 2010;31(suppl 1):S38–S41.Google Scholar
122. Guyatt, GH, Oxman, AD, Vist, GE, et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008;336(7650):924–926.Google Scholar
123. GRADE. Canadian Task Force on Preventive Health Care website. http://canadiantaskforce.ca/methods/grade/. Accessed December 31, 2013.Google Scholar