Skip to main content
    • Aa
    • Aa

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

  • Erik R. Dubberke (a1), Philip Carling (a2), Ruth Carrico (a3), Curtis J. Donskey (a4), Vivian G. Loo (a5), L. Clifford McDonald (a6), Lisa L. Maragakis (a7), Thomas J. Sandora (a8), David J. Weber (a9), Deborah S. Yokoe (a10) and Dale N. Gerding (a11)...

Previously published guidelines are available that provide comprehensive recommendations for detecting and preventing healthcare-associated infections (HAIs). The intent of this document is to highlight practical recommendations in a concise format designed to assist acute care hospitals in implementing and prioritizing their Clostridium difficile infection (CDI) prevention efforts. This document updates “Strategies to Prevent Clostridium difficile Infections in Acute Care Hospitals,” published in 2008. This expert guidance document is sponsored by the Society for Healthcare Epidemiology of America (SHEA) and is the product of a collaborative effort led by SHEA, the Infectious Diseases Society of America (IDSA), the American Hospital Association (AHA), the Association for Professionals in Infection Control and Epidemiology (APIC), and The Joint Commission, with major contributions from representatives of a number of organizations and societies with content expertise. The list of endorsing and supporting organizations is presented in the introduction to the 2014 updates.

    • Send article to Kindle

      To send this article to your Kindle, first ensure is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle.

      Note you can select to send to either the or variations. ‘’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Strategies to Prevent Clostridium difficile Infections in Acute Care Hospitals: 2014 Update
      Available formats
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Dropbox account. Find out more about sending content to Dropbox.

      Strategies to Prevent Clostridium difficile Infections in Acute Care Hospitals: 2014 Update
      Available formats
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your Google Drive account. Find out more about sending content to Google Drive.

      Strategies to Prevent Clostridium difficile Infections in Acute Care Hospitals: 2014 Update
      Available formats
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

3. LC McDonald , M Owings , DB Jernigan . Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996-2003. Emerg Infect Dis 2006;12(3):409415.

5. MD Zilberberg , AF Shorr , MH Kollef . Growth and geographic variation in hospitalizations with resistant infections, United States, 2000-2005. Emerg Infect Dis 2008;14(11):17561758.

7. MP Bauer , DW Notermans , BH van Benthem , et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet 2011;377(9759):6373.

8. VG Loo , L Poirier , MA Miller , 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):24422449.

9. M Miller , D Gravel , M Mulvey , 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):194201.

10. DM Denno , N Shaikh , JR Stapp , et al. Diarrhea etiology in a pediatric emergency department: a case control study. Clin Infect Dis 2012;55(7):897904.

11. RE Feghaly , JL Stauber , PI Tarr , DB Hasiam . 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):813816.

12. C Rousseau , I Poilane , De L Pontual , AC Maherault , A Le Monnier , A Collignon . Clostridium difficile carriage in healthy infants in the community: a potential reservoir for pathogenic strains. Clin Infect Dis 2012;55(9):12091215.

15. ER Dubberke , KA Reske , Y Yan , MA Olsen , LC McDonald , VJ Fraser . Clostridium difficile-associated disease in a setting of endemicity: identification of novel risk factors. Clin Infect Dis 2007;45(12):15431549.

17. J Kim , JF Shaklee , S Smathers , et al. Risk factors and outcomes associated with severe Clostridium difficile infection in children. Pediatr Infect Dis J 2012;31(2):134138.

19. LC McDonald , GE Killgore , A Thompson , et al. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl f Med 2005;353(23):24332441.

20. DA Burns , D Heeg , ST Cartman , NP Minton . Reconsidering the sporulation characteristics of hypervirulent Clostridium difficile BI/NAP1/027. PLoS ONE 2011;6(9):e24894.

21. M Merrigan , A Venugopal , M Mallozzi , et al. Human hyper-virulent Clostridium difficile strains exhibit increased sporulation as well as robust toxin production, J Bacteriol 2010; 192(19):49044911.

22. M Warny , J Pepin , A Fang , 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):10791084.

23. AS Walker , DW Eyre , DH Wyllie , et al. Relationship between bacterial strain type, host biomarkers, and mortality in Clostridium difficile infection. Clin Infect Dis 2013;56(11):15891600.

25. AK Cheknis , SP Sambol , DM Davidson , 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):230233.

27. ER Dubberke , AM Butler , KA Reske , et al. Attributable outcomes of endemic Clostridium difficile-associated disease in nonsurgical patients. Emerg Infect Dis 2008;14(7):10311038.

28. ER Dubberke , MA Olsen . Burden of Clostridium difficile on the healthcare system. Clin Infect Dis 2012;55(suppl 2):S88S92.

29. AJ Hall , AT Curns , LC McDonald , UD Parashar , BA Lopman . The roles of Clostridium difficile and norovirus among gastroenteritis-associated deaths in the United States, 1999-2007. Clin Infect Dis 2012;55(2):216223.

30. JS Sammons , R Localio , R Xiao , SE Coffin , T. Zaoutis Clostridium difficile infection is associated with increased risk of death and prolonged hospitalization in children. Clin Infect Dis 2013;57(1):18.

31. J Pepin , N Saheb , MA Coulombe , et al. Emergence of fluo-roquinolones as the predominant risk factor for Clostridium difficile-associated diarrhea: a cohort study during an epidemic in Quebec. Clin Infect Dis 2005;41(9):12541260.

32. S Dial , JA Delaney , AN Barkun , S. Suissa Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficile-associated disease. JAMA 2005;294(23):29892995.

33. J Belmares , DN Gerding , JP Parada , S Miskevics , F Weaver , S. Johnson Outcome of metronidazole therapy for Clostridium difficile disease and correlation with a scoring system. J Infect 2007;55(6):495501.

34. DM Musher , S Aslam , N Logan , et al. Relatively poor outcome after treatment of Clostridium difficile colitis with metronidazole. Clin Infect Dis 2005;40(11):15861590.

35. FA Zar , SR Bakkanagari , KM Moorthi , MB Davis . A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin Infect Dis 2007;45(3):302307.

36. EJ Kuijper , B Coignard , P. Tull Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 2006;12(suppl 6):218.

38. ER Dubberke , Z Han , L Bobo , et al. Impact of clinical symptoms on interpretation of diagnostic assays for Clostridium difficile infections, J Clin Microbiol 2011;49(8):28872893.

39. J Pepin , L Valiquette , B. Cossette Mortality attributable to nosocomial Clostridium difficile-associated disease during an epidemic caused by a hypervirulent strain in Quebec. CMA/2005; 173(9):10371042.

41. Y Longtin , S Trottier , G Brochu , 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):6773.

42. TD Planche , KA Davies , PG Coen , 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):936945.

43. ER Dubberke , KA Reske , LC McDonald , VJ Fraser . ICD-9 codes and surveillance for Clostridium difficile-associated disease. Emerg Infect Dis 2006;12(10):15761579.

46. CR Polage , DL Chin , JL Leslie , J Tang , SH Cohen , JV Solnick . Outcomes in patients tested for Clostridium difficile toxins. Diagn Microbiol Infect Dis 2012;74(4):369373.

49. MP Bauer , EJ Kuijper , JT van Dissel . European Society of Clinical Microbiology and Infectious Diseases (ESCMID): treatment guidance document for Clostridium difficile infection (CDI). Clin Microbiol Infect 2009;15(12):10671079.

51. CM Surawicz , LJ Brandt , DG Binion , et al. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol 2013;108(4):478498.

53. SP Stone , BS Cooper , CC Kibbler , et al. The ORION statement: guidelines for transparent reporting of outbreak reports and intervention studies of nosocomial infection. Lancet Infect Dis 2007;7(4):282288.

54. S Fowler , A Webber , BS Cooper , et al. Successful use of feedback to improve antibiotic prescribing and reduce Clostridium difficile infection: a controlled interrupted time series. J Anti-microb Chemother 2007;59(5):990995.

55. L Valiquette , B Cossette , MP Garant , H Diab , J. Pepin 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 NAPI/027 strain. Clin Infect Dis 2007; 45(suppl 2):S112S121.

56. MA Aldeyab , MP Kearney , MG Scott , 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. JAnúmicrob Chemother 2012;67(12):29882996.

57. MJ Talpaert , RG Gopal , BS Cooper , P. Wade 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): 21682174.

58. DM Guerrero , MM Nerandzic , LA Jury , S Jinno , S Chang , CJ Donskey . 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):556558.

59. LV McFarland , ME Mulligan , RY Kwok , WE Stamm . Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320(4):204210.

63. RG Gopal , A Jeanes , M Osman , C Aylott , J. Green Marketing hand hygiene in hospitals—a case study, J Hosp Infect 2002; 50(1):4247.

66. N Knight , T Strait , N Anthony , 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):523528.

68. N Vernaz , H Sax , D Pittet , P Bonnabry , J Schrenzel , S. Harbarth Temporal effects of antibiotic use and hand rub consumption on the incidence of MRSA and Clostridium difficile. Antimicrob Chemother 2008;62(3):601607.

70. VT Chang , K. Nelson The role of physical proximity in nosocomial diarrhea. Clin Infect Dis 2000;31(3):717722.

71. CR Clabots , S Johnson , MM Olson , LR Peterson , DN Gerding . Acquisition of Clostridium difficileby hospitalized patients: evidence for colonized new admissions as a source of infection. J Infect Dis 1992;166(3):561567.

72. MH Samore , L Venkataraman , PC DeGirolami , RD Arbeit , AW Karchmer . Clinical and molecular epidemiology of sporadic and clustered cases of nosocomial Clostridium difficile diarrhea. Am J Med 1996;100(1):3240.

74. JL Mayfield , T Leet , J Miller , LM Mundy . Environmental control to reduce transmission of Clostridium difficile. Clin Infect Dis 2000;31(4):9951000.

75. MH Wilcox , WN Fawley , N Wigglesworth , P Parnell , P Verity , J. Freeman Comparison of the effect of detergent versus hy-pochlorite cleaning on environmental contamination and incidence of Clostridium difficile infection. J Hosp Infect 2003; 54(2):109114.

76. AE Simor . Diagnosis, management, and prevention of Clostridium difficile infection in long-term care facilities: a review. J Am Geriatr Soc 2010;58(8):15561564.

78. VG Loo , AM Bourgault , L Poirier , et al. Host and pathogen factors for Clostridium difficile infection and colonization. N Engl J Med 2011;365(18):16931703.

79. SB Doernberg , LG Winston , DH Deck , HE Chambers Does doxycycline protect against development of Clostridium difficile infection? Clin Infect Dis 2012;55(5):615620.

80. F Le , V Arora , DN Shah , M Salazar , HR Palmer , KW Garey . A real-world evaluation of oral vancomycin for severe Clostridium difficile infection: implications for antibiotic stewardship programs. Pharmacotherapy 2012;32(2):129134.

81. SE Harpe , TJ Inocencio , AL Pakyz , MJ Oinonen , RE Polk . Characterization of continued antibacterial therapy after diagnosis of hospital-onset Clostridium difficile infection: implications for antimicrobial stewardship. Pharmacotherapy 2012; 32(8):744754.

84. ER Dubberke , KA Reske , J Noble-Wang , et al. Prevalence of Clostridium difficile environmental contamination and strain variability in multiple health care facilities. Am J Infect Control 2007;35(5):315318.

85. DM Dumford III, MM Nerandzic , BC Eckstein , CJ Donskey . 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):1519.

86. AM Lewis , J Gammon , I Hosein . The pros and cons of isolation and containment, J Hosp Infect 1999;43(1):1923.

91. PC Carling , MF Parry , SM Von Beheren . Identifying opportunities to enhance environmental cleaning in 23 acute care hospitals. Infect Control Hosp Epidemiol 2008;29(1):17.

93. MH Wilcox , WN Fawley , P. Parnell Value of lysozyme agar incorporation and alkaline thioglycollate exposure for the environmental recovery of Clostridium difficile. Hosp Infect 2000; 44(1):6569.

100. C McNulty , M Logan , IP Donald , 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):707711.

101. SM Pear , TH Williamson , KM Bettin , DN Gerding , JN Galgiani . Decrease in nosocomial Clostridium difficile-associated diarrhea by restricting clindamycin use. Ann Intern Med 1994; 120(4):272277.

102. S Johnson , SR Homann , KM Bettin , et al. Treatment of asymptomatic Clostridium difficile carriers (fecal excretors) with van-comycin or metronidazole: a randomized, placebo-controlled trial. Ann Intern Med 1992;117(4):297302.

103. KB Kirkland , JM Weinstein . Adverse effects of contact isolation. Lancet 1999;354(9185):11771178.

104. DJ Morgan , DJ Diekema , K Sepkowitz , EN Perencevich . Adverse outcomes associated with contact precautions: a review of the literature. Am J Infect Control 2009;37(2):8593.

105. S Saint , LA Higgins , BK Nallamothu , C. Chenoweth Do physicians examine patients in contact isolation less frequently? a brief report. Am J Infect Control 2003;31(6):354356.

106. HT Stelfox , DW Bates , DA Redelmeier . Safety of patients isolated for infection control. JAMA 2003;290(14):18991905.

107. LV McFarland , GW Elmer , CM Surawicz . Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol 2002;97(7):17691775.

108. JD Siegel , E Rhinehart , M Jackson , L. Chiarello 2007 Guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control 2007;35(10 suppl 2):S65S164.

109. JZ Goldenberg , SS Ma , JD Saxton , et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea in adults and children. Cochmne Database Syst Rev 2013;5:CD006095.

110. BC Johnston , SS Ma , JZ Goldenberg , et al. Probiotics for the prevention of Clostridium difficile-associated diarrhea: a systematic review and meta-analysis. Ann Intern Med 2012; 157(12):878888.

113. SJ Allen , K Wareham , D Wang , et al. Lactobacilli and bifido-bacteria 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):12491257.

114. P Munoz , E Bouza , M Cuenca-Estrella , et al. Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin Infect Dis 2005;40(11):16251634.

116. SK Wong , A Kneebone , M Morgan , CJ Henderson , A Morgan , B. Jalaludin 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):776782.

119. JE Farley , D Doughman , R Jeeva , P Jeffries , JM Stanley . 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):258259.

120. T Landers , S Abusalem , MB Coty , J. Bingham Patient-centered hand hygiene: the next step in infection prevention. Am J Infect Control 2012;40(4 suppl 1):S11S17.

122. GH Guyatt , AD Oxman , GE Vist , et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008;336(7650):924926.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Infection Control & Hospital Epidemiology
  • ISSN: 0899-823X
  • EISSN: 1559-6834
  • URL: /core/journals/infection-control-and-hospital-epidemiology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 4358 *
Loading metrics...

Abstract views

Total abstract views: 9172 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 23rd June 2017. This data will be updated every 24 hours.