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Recommendations for Surveillance of Clostridium difficile–Associated Disease

  • L. Clifford McDonald (a1), Bruno Coignard (a2), Erik Dubberke (a3), Xiaoyan Song (a4), Teresa Horan (a1), Preeta K. Kutty (a1) and the Ad Hoc Clostridium difficile Surveillance Working Group...

The epidemiology of Clostridium difficile-associated disease (CDAD) is changing, with evidence of increased incidence and severity. However, the understanding of the magnitude of and reasons for this change is currently hampered by the lack of standardized surveillance methods.

Objective and Methods.

An ad hoc C. difficile surveillance working group was formed to develop interim surveillance definitions and recommendations based on existing literature and expert opinion that can help to improve CDAD surveillance and prevention efforts.

Definitions and Recommendations.

A CDAD case patient was defined as a patient with symptoms of diarrhea or toxic megacolon combined with a positive result of a laboratory assay and/or endoscopic or histopathologic evidence of pseudomembranous colitis. Recurrent CDAD was defined as repeated episodes within 8 weeks of each other. Severe CDAD was defined by CDAD-associated admission to an intensive care unit, colectomy, or death within 30 days after onset. Case patients were categorized by the setting in which C. difficile was likely acquired, to account for recent evidence that suggests that healthcare facility-associated CDAD may have its onset in the community up to 4 weeks after discharge. Tracking of healthcare facility–onset, healthcare facility–associated CDAD is the minimum surveillance required for healthcare settings; tracking of community–onset, healthcare facility–associated CDAD should be performed only in conjunction with tracking of healthcare facility–onset, healthcare facility–associated CDAD. Community–associated CDAD was defined by symptom onset more than 12 weeks after the last discharge from a healthcare facility. Rates of both healthcare facility–onset, healthcare facility–associated CDAD and community–onset, healthcare facility–associated CDAD should be expressed as case patients per 10,000 patient–days; rates of community-associated CDAD should be expressed as case patients per 100,000 person-years.

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1.Bartlett JG. Clinical practice: antibiotic-associated diarrhea. N Engl J Med 2002;346:334339.
2.Bauer TM, Lalvani A, Fehrenbach J, et al. Derivation and validation of guidelines for stool cultures for enteropathogenic bacteria other than Clostridium difficile in hospitalized adults. JAMA 2001;285:313319.
3.Johnson S, Samore MH, Farrow KA, et al. Epidemics of diarrhea caused by a clindamycin-resistant strain of Clostridium difficile in four hospitals. N Engl J Med 1999;341:16451651.
4.Dallai RM, Harbrecht BG, Boujoukas AJ, et al. Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg 2002;235:363372.
5.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;173:10371042.
6.Muto CA, Pokrywka M, Shutt K, et al. A large outbreak of Clostridium difficile-associated disease with an unexpected proportion of deaths and colectomies at a teaching hospital following increased fluoroquinolone use. Infect Control Hosp Epidemiol 2005;26:273280.
7.McDonald LC, Killgore GE, Thompson A, et al. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 2005;353:24332441.
8.McDonald LC. Clostridium difficile, responding to a new threat from an old enemy. Infect Control Hosp Epidemiol 2005;26:672675.
9.Palmore TN, Sohn S, Malak SF, Eagan J, Sepkowitz KA. Risk factors for acquisition of Clostridium difficile-associated diarrhea among outpatients at a cancer hospital. Infect Control Hosp Epidemiol 2005;26:680684.
10.Sohn S, Climo M, Diekema D, et al. Varying rates of Clostridium difficile-associated diarrhea at prevention epicenter hospitals. Infect Control Hosp Epidemiol 2005;26:676679.
11.Olson MM, Shanholtzer CJ, Lee JT Jr, Gerding DN. Ten years of prospective Clostridium difficile-associated disease surveillance and treatment at the Minneapolis VA Medical Center, 1982-1991. Infect Control Hosp Epidemiol 1994;15:371381.
12.Johal SS, Hammond J, Solomon K, James PD, Mahida YR. Clostridium difficile associated diarrhoea in hospitalised patients: onset in the community and hospital and role of flexible sigmoidoscopy. Gut 2004;53:673677.
13.Archibald LK, Banerjee SN, Jarvis WR. Secular trends in hospital-acquired Clostridium difficile disease in the United States, 1987-2001. Infect Dis 2004;189:15851589.
14.Miller MA, Hyland M, Ofner-Agostini M, Gourdeau M, Ishak M. Morbidity, mortality, and healthcare burden of nosocomial Clostridium difficile-associated diarrhea in Canadian hospitals. Infect Control Hosp Epidemiol 2002;23:137140.
15.Miller MA, Gravel D, Mulvey M, et al. Surveillance for nosocomial Clostridium difficile associated diarrhea (N-CDAD) within acute-care hospitals in Canada: results of the 2005 nosocomial infections surveillance program (CNISP) study shows escalating mortality. In: Program and abstracts of the 16th Annual Scientific Meeting of the Society for Healthcare Epidemiology of America;March 18-21, 2006;Chicago, IL. Abstract 151.
16.Hirschhorn LR, Trnka Y, Onderdonk A, Lee ML, Platt R. Epidemiology of community-acquired Clostridium difficile-associated diarrhea. J Infect Dis 1994;169:127133.
17.Levy DG, Stergachis A, McFarland LV, et al. Antibiotics and Clostridium difficile diarrhea in the ambulatory care setting. Clin Ther 2000;22:91102.
18.Karlstrom O, Fryklund B, Tullus K, Burman LG. A prospective nationwide study of Clostridium difficile-associated diarrhea in Sweden. The Swedish C. difficile Study Group. Clin Infect Dis 1998;26:141145.
19.Noren T, Akerlund T, Back E, et al. Molecular epidemiology of hospital-associated and community-acquired Clostridium difficile infection in a Swedish county. J Clin Microbiol 2004;42:36353643.
20.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;294:29892995.
21.Severe Clostridium difficile-associated disease in populations previously at low risk—four states, 2005. MMWR Morb Mortal Wkly Rep 2005;54:12011205.
22.Chang H, Parada J, Evans C, Johnson S, Gerding DN. Onset of symptoms and time to diagnosis of Clostridium difficile diarrhea among outpatients discharged from an acute care hospital. In: Program and abstracts of the 16th Annual Scientific Meeting of the Society for Healthcare Epidemiology of America;March 18-21, 2006; Chicago, IL. Abstract 154.
23.McDonald J, Naggie S, Kuhn L, et al. Community-onset Clostridium difficile-associated diarrhea: a tale of two medical centers. In: Program and abstracts of the 16th Annual Scientific Meeting of the Society for Healthcare Epidemiology of America;March 18-21, 2006; Chicago, IL. Abstract 181.
24.Mayfield J, McMullen K, Dubberke E. Comparison of Clostridium difficile-associated disease rates using a traditional vs. expanded definition. In: Program and abstracts of the 16th Annual Scientific Meeting of the Society for Healthcare Epidemiology of America;March 18-21, 2006;Chicago, IL. Abstract 180.
25.McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320:204210.
26.Samore MH, DeGirolami PC, Tlucko A, Lichtenberg DA, Melvin ZA, Karchmer AW. Clostridium difficile colonization and diarrhea at a tertiary care hospital. Clin Infect Dis 1994;18:181187.
27.Walker KJ, Gilliland SS, Vance-Bryan K, et al. Clostridium difficile colonization in residents of long-term care facilities: prevalence and risk factors. J Am Geriatr Soc 1993;41:940946.
28.Rivera EV, Woods S. Prevalence of asymptomatic Clostridium difficile colonization in a nursing home population: a cross-sectional study. J Gend Specif Med 2003;6:2730.
29.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: 561-567.
30.Ozaki E, Kato H, Kita H, et al. Clostridium difficile colonization in healthy adults: transient colonization and correlation with enterococcal colonization. J Med Microbiol 2004;53:167172.
31.Iizuka M, Konno S, Itou H, et al. Novel evidence suggesting Clostridium difficile is present in human gut microbiota more frequently than previously suspected. Microbiol Immunol 2004;48:889892.
32.Viscidi R, Willey S, Bartlett JG. Isolation rates and toxigenic potential of Clostridium difficile isolates from various patient populations. Gastroenterology 1981;81:59.
33.Aronsson B, Mollby R, Nord CE. Antimicrobial agents and Clostridium difficile in acute enteric disease: epidemiological data from Sweden, 1980-1982. J Infect Dis 1985;151:476481.
34.Matsuki S, Ozaki E, Shozu M, et al. Colonization by Clostridium difficile of neonates in a hospital, and infants and children in three day-care facilities of Kanazawa, Japan. Int Microbiol 2005;8:4348.
35.Kyne L, Warny M, Qamar A, Kelly CP. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N Engl J Med 2000;342:390397.
36.Kyne L, Warny M, Qamar A, Kelly CP. Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. Lancet 2001;357:189193.
37.Shim JK, Johnson S, Samore MH, Bliss DZ, Gerding DN. Primary symptomless colonisation by Clostridium difficile and decreased risk of subsequent diarrhoea. Lancet 1998;351:633636.
38.Sambol SP, Merrigan MM, Tang JK, Johnson S, Gerding DN. Colonization for the prevention of Clostridium difficile disease in hamsters. J Infect Dis 2002;186:17811789.
39.Johnson S, Clabots CR, Linn FV, Olson MM, Peterson LR, Gerding DN. Nosocomial Clostridium difficile colonisation and disease. Lancet 1990;336:97100.
40.Anand A, Bashey B, Mir T, Glatt AE. Epidemiology, clinical manifestations, and outcome of Clostridium difficile-associated diarrhea. Am J Gastroenterol 1994;89:519523.
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Infection Control & Hospital Epidemiology
  • ISSN: 0899-823X
  • EISSN: 1559-6834
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