Diagnosis, management, and prevention of clostridium difficile infection in long-term care facilities: A review

Journal of the American Geriatrics Society

Volumn 58, Issue 8, 2010, Pages 1556-1564

  Simor, Andrew E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

antibiotic associated diarrhea; Clostridium difficile; nosocomial diarrhea; pseudomembranous colitis

Indexed keywords

ANTIBIOTIC AGENT; CEPHALOSPORIN; CLINDAMYCIN; CLOSTRIDIUM DIFFICILE TOXIN A; CLOSTRIDIUM DIFFICILE TOXIN B; ENEMA; GLUTAMATE DEHYDROGENASE; IMMUNOGLOBULIN; METRONIDAZOLE; MONOCLONAL ANTIBODY; NITAZOXANIDE; PROBIOTIC AGENT; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RAMOPLANIN; RIFAMPICIN; TIACUMICIN B; VANCOMYCIN;

BACTERIAL VIRULENCE; CLINICAL FEATURE; CLINICAL TRIAL; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; COLONOSCOPE; DIARRHEA; DISEASE SEVERITY; DISEASE TRANSMISSION; DISINFECTION; ENVIRONMENTAL SANITATION; ENZYME ASSAY; ENZYME IMMUNOASSAY; EPIDEMIC; EUROPE; FECES ANALYSIS; FLUID RESUSCITATION; HAND WASHING; HEALTH CARE FACILITY; HUMAN; HYGIENE; HYPOALBUMINEMIA; INFECTION CONTROL; INFECTION RISK; INTENSIVE CARE UNIT; LACTOBACILLUS; LEUKOCYTOSIS; MORBIDITY; MORTALITY; NASOGASTRIC TUBE; NORTH AMERICA; PATHOGENESIS; POLYMERASE CHAIN REACTION; PREVALENCE; REVIEW; SACCHAROMYCES BOULARDII; SENSITIVITY AND SPECIFICITY; STREPTOCOCCUS THERMOPHILUS;

AGED; ANTI-INFECTIVE AGENTS; CLOSTRIDIUM DIFFICILE; CROSS INFECTION; DIARRHEA; ENTEROCOLITIS, PSEUDOMEMBRANOUS; EQUIPMENT CONTAMINATION; HUMANS; INFECTION CONTROL; LONG-TERM CARE; METRONIDAZOLE; RISK FACTORS; SEVERITY OF ILLNESS INDEX; VANCOMYCIN;

EID: 77955233611     PISSN: 00028614     EISSN: 15325415     Source Type: Journal    
DOI: 10.1111/j.1532-5415.2010.02958.x     Document Type: Review

References (83)

1. Gerding DN, Johnson S, Peterson LR et al. Clostridium difficile-associated diarrhea and colitis. Infect Control Hosp Epidemiol 1995 16 : 459 477.
2. McDonald LC, Owings M, Jernigan DB. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996-2003. Emerg Infect Dis 2006 12 : 409 415.
3. Kelly CP, LaMont JT. Clostridium difficile - more difficult than ever. N Engl J Med 2008 359 : 1932 1940.
4. Simor AE, Bradley SF, Strausbaugh LJ et al. Clostridium difficile in long-term-care facilities for the elderly. Infect Control Hosp Epidemiol 2002 23 : 696 703.
5. Jarvis WR, Schlosser J, Jarvis AA et al. National point prevalence of Clostridium difficile in US health care facility inpatients, 2008. Am J Infect Control 2009 37 : 263 270.
6. 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 : 526 533.
7. Zilberberg MD, Shorr AF, Kollef MH. Increase in adult Clostridium difficile-related hospitalizations and case-fatality rate, United States, 2000-2005. Emerg Infect Dis 2008 14 : 929 931.
8. Redelings MD, Sorvillo F, Mascola L. Increase in Clostridium difficile-related mortality rates, United States, 1999-2004. Emerg Infect Dis 2007 13 : 1417 1419.
9. Kyne L, Hamel MB, Polavaram R et al. Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin Infect Dis 2002 34 : 346 353.
10. Dubberke ER, Butler AM, Reske KA et al. Attributable outcomes of endemic Clostridium difficile-associated disease in nonsurgical patients. Emerg Infect Dis 2008 14 : 1031 1038.
11. Pépin J, Valiquette L, Alary ME et al. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: A changing pattern of disease severity. Can Med Assoc J 2004 171 : 466 472.
12. 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 : 2442 2449.
13. McDonald LC, Killgore GE, Thompson A et al. An epidemic, toxin gene-variant strain of Clostridium difficile. N Engl J Med 2005 353 : 2433 2441.
14. 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 : 1079 1084.
15. Pépin J, Valiquette L, Cossette B. Mortality attributable to nosocomial Clostridium difficile-associated disease during an epidemic caused by a hypervirulent strain in Quebec. Can Med Assoc J 2005 173 : 1037 1041.
16. Geric B, Carman RJ, Rupnik M et al. Binary toxin-producing, large clostridial toxin-negative Clostridium difficile strains are enterotoxic but do not cause disease in hamsters. J Infect Dis 2006 193 : 1143 1150.
17. Fawley WN, Underwood S, Freeman J et al. Efficacy of hospital cleaning agents and germicides against epidemic Clostridium difficile strains. Infect Control Hosp Epidemiol 2007 28 : 920 925.
18. Reineke J, Tenzer S, Rupnik M et al. Autocatalytic cleavage of Clostridium difficile toxin B. Nature 2007 446 : 415 419.
19. Lyras D, O'Connor JR, Howarth PM et al. Toxin B is essential for virulence of Clostridium difficile. Nature 2009 458 : 1176 1179.
20. Johnson S, Clabots CR, Linn FV et al. Nosocomial Clostridium difficile colonisation and disease. Lancet 1990 336 : 97 100.
21. Shim JK, Johnson S, Samore MH et al. Primary symptomless colonisation by Clostridium difficile and decreased risk of subsequent diarrhoea. Lancet 1998 351 : 633 636. (Pubitemid 28098446)
22. Kyne L, Warny M, Qamar A et al. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N Engl J Med 2000 342 : 390 397.
23. McFarland LV, Mulligan ME, Kwok RYY et al. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989 320 : 204 210.
24. Kim K-H, Fekety R, Batts D et al. Isolation of Clostridium difficile from the environment and contacts of patients with antibiotic-associated colitis. J Infect Dis 1981 143 : 42 50. (Pubitemid 11152596)
25. Brooks SE, Veal RO, Kramer M et al. Reduction in the incidence of Clostridium difficile-associated diarrhea in an acute care hospital and a skilled nursing facility following replacement of electronic thermometers with single-use disposables. Infect Control Hosp Epidemiol 1992 13 : 98 103.
26. Chang VT, Nelson K. The role of physical proximity in nosocomial diarrhea. Clin Infect Dis 2000 31 : 717 722.
27. Johnson S, Gerding DN, Olson MM et al. Prospective, controlled study of vinyl glove use to interrupt Clostridium difficile nosocomial transmission. Am J Med 1990 88 : 137 140.
28. Bignardi GE. Risk factors for Clostridium difficile infection. J Hosp Infect 1998 40 : 1 15.
29. Debast SB, Vaessen N, Choudry A et al. Successful combat of an outbreak due to Clostridium difficile PCR ribotype 027 and recognition of specific risk factors. Clin Microbiol Infect 2009 15 : 427 434.
30. Bliss DZ, Johnson S, Savik K et al. Acquisition of Clostridium difficile and Clostridium difficile-associated diarrhea in hospitalized patients receiving tube feeding. Ann Intern Med 1998 129 : 1012 1019.
31. Dubberke ER, Reske KA, Yan Y et al. Clostridium difficile-associated disease in a setting of endemicity: Identification of novel risk factors. Clin Infect Dis 2007 45 : 1543 1549.
32. Henrich TJ, Krakower D, Bitton A et al. Clinical risk factors for severe Clostridium difficile-associated disease. Emerg Infect Dis 2009 15 : 415 422.
33. Gravel D, Miller M, Simor A et al. Health care-associated Clostridium difficile infection in adults admitted to acute care hospitals in Canada: A Canadian Nosocomial Infection Surveillance Program study. Clin Infect Dis 2009 48 : 568 576.
34. Bender BS, Bennett R, Laughon BE et al. Is Clostridium difficile endemic in chronic-care facilities? Lancet 1986 2 : 11 13.
35. Cefai C, Elliott TSJ, Woodhouse KW. Gastrointestinal carriage rate of Clostridium difficile in elderly, chronic care hospital patients. J Hosp Infect 1988 11 : 335 339.
36. Simor AE, Yake SL, Tsimidis K. Infection due to Clostridium difficile among elderly residents of a long-term-care facility. Clin Infect Dis 1993 17 : 672 678.
37. 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 : 940 946.
38. Laffan AM, Bellantoni MF, Greenough III. WB et al. Burden of Clostridium difficile-associated diarrhea in a long-term care facility. J Am Geriatr Soc 2006 54 : 1068 1073.
39. Thomas DR, Bennett RG, Laughon BE et al. Postantibiotic colonization with Clostridium difficile in nursing home patients. J Am Geriatr Soc 1990 38 : 415 420.
40. Cartmill TDI, Shrimpton SB, Panigrahi H et al. Nosocomial diarrhoea due to a single strain of Clostridium difficile: A prolonged outbreak in elderly patients. Age Ageing 1992 21 : 245 249.
41. 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 : 707 711.
42. Gaynes R, Rimland D, Killum E et al. Outbreak of Clostridium difficile infection in a long-term care facility: Association with gatifloxacin use. Clin Infect Dis 2004 38 : 640 645. (Pubitemid 38333858)
43. Cherifi S, Delmee M, Van Broeck J et al. Management of an outbreak of Clostridium difficile-associated disease among geriatric patients. Infect Control Hosp Epidemiol 2006 27 : 1200 1205.
44. Riggs MM, Sethi AK, Zabarsky TF et al. Asymptomatic carriers are a potential source for transmission of epidemic and nonepidemic Clostridium difficile strains among long-term care facility residents. Clin Infect Dis 2007 45 : 992 998.
45. Kyne L, Merry C, O'Connell B et al. Factors associated with prolonged symptoms and severe disease due to Clostridium difficile. Age Ageing 1999 28 : 107 113.
46. Al-Tureihi FIJ, Hassoun A, Wolf-Klein G et al. Albumin, length of stay, and proton pump inhibitors: Key factors in Clostridium difficile-associated disease in nursing home patients. J Am Med Dir Assoc 2005 6 : 105 108.
47. Mylotte JM. Antimicrobial prescribing in long-term care facilities: Prospective evaluation of potential antimicrobial use and cost indicators. Am J Infect Control 1999 27 : 10 19.
48. Viscidi R, Laughon BE, Yolken R et al. Serum antibody response to toxins A and B of Clostridium difficile. J Infect Dis 1983 148 : 93 100.
49. Bassaris HP, Lianou PE, Legakis NJ et al. Interaction between Clostridium difficile and polymorphonuclear leucocytes from the elderly and post-operative cancer patients: Phagocytosis and bactericidal function. Med Microbiol Immunol 1984 173 : 49 55.
50. Quinn LK, Chen Y, Herwaldt LA. Infection control policies and practices for Iowa long-term care facility residents with Clostridium difficile infection. Infect Control Hosp Epidemiol 2007 28 : 1228 1232.
51. Miller MA, Hyland M, Ofner-Agostini M et al. Morbidity, mortality, and healthcare burden of nosocomial Clostridium difficile-associated diarrhea in Canadian hospitals. Infect Control Hosp Epidemiol 2002 23 : 137 140.
52. Kyne L, Warny M, Qamar A et al. Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. Lancet 2001 357 : 189 193.
53. Johnson S. Recurrent Clostridium difficile infection: A review of risk factors, treatment, and outcomes. J Infect 2009 58 : 403 410.
54. Leav BA, Blair B, Leney M et al. Serum anti-toxin B antibody correlates with protection from recurrent Clostridium difficile infection (CDI). Vaccine 2010 28 : 965 969.
55. Peterson LR, Robicsek A. Does my patient have Clostridium difficile infection? Ann Intern Med 2009 151 : 176 179.
56. Eastwood K, Else P, Charlett A et al. Comparison of nine commercially available Clostridium difficile toxin detection assays, a real-time PCR assay for C. difficile tcdB, and a glutamate dehydrogenase detection assay to cytotoxin testing and cytotoxigenic culture methods. J Clin Microbiol 2009 47 : 3211 3217.
57. Gerding DN, Muto CA, Owens RC Jr. Treatment of Clostridium difficile infection. Clin Infect Dis 2008 46 : S32 S42.
58. Olson MM, Shanholtzer CJ, Lee JT Jr. et al. 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 : 371 381.
59. Zar FA, Bakkanagari SR, Moorthi KMLST et al. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin Infect Dis 2007 45 : 302 307.
60. Cohen DN, Gerding GW, 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 : 431 455.
61. McFarland LV, Elmer GW, Surawicz CM. Breaking the cycle: Treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am J Gastroenterol 2002 97 : 1769 1775.
62. Lowy I, Molrine DC, Leav B et al. Treatment with monoclonal antibodies against Clostridium difficile toxins. N Engl J Med 2010 362 : 197 205.
63. Miller M. The fascination with probiotics for Clostridium difficile infection: Lack of evidence for prophylactic or therapeutic efficacy. Anaerobe 2009 15 : 281 284.
64. McFarland LV. Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. Am J Gastroenterol 2006 101 : 812 822.
65. Pillai A, Nelson R. Probiotics for treatment of Clostridium difficile-associated colitis in adults. Cochrane Database Syst Rev 2008; doi :.
66. Hickson M, D'Souza AL, Muthu N et al. Use of probiotic Lactobacillus preparation to prevent diarrhoea associated with antibiotics: Randomised double-blind placebo controlled trial. BMJ 2007 335 : 80 83.
67. Aas J, Gessert CE, Bakken JS. Recurrent Clostridium difficile colitis: Case series involving 18 patients treated with donor stool administered via a nasogastric tube. Clin Infect Dis 2003 36 : 580 585.
68. MacConnachie AA, Fox R, Kennedy DR et al. Faecal transplant for recurrent Clostridium difficile-associated diarrhoea: A UK case series. Q J Med 2009 102 : 781 784.
69. National Clostridium difficile Standards Group: Report to the Department of Health. National Clostridium difficile Standards Group. J Hosp Infect 2004 56 (Suppl. 1) : 1 38.
70. 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.
71. Climo MW, Israel DS, Wong ES et al. Hospital-wide restriction of clindamycin: Effect on the incidence of Clostridium difficile-associated diarrhea and cost. Ann Intern Med 1998 128 : 989 995.
72. 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 : 264 272.
73. Valiquette L, Cossette B, Garant MP et al. 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 : S112 S121.
74. Nuila F, Cadle RM, Logan N et al. Antibiotic stewardship and Clostridium difficile-associated disease. Infect Control Hosp Epidemiol 2008 29 : 1096 1097.
75. Weiss K, Boisvert A, Chagnon M et al. Multipronged intervention strategy to control an outbreak of Clostridium difficile infection (CDI) and its impact on the rates of CDI from 2002 to 2007. Infect Control Hosp Epidemiol 2009 30 : 156 162.
76. Muto CA, Blank MK, Marsh JW et al. Control of an outbreak of infection with the hypervirulent Clostridium difficile BI strain in a university hospital using a comprehensive "bundle" approach. Clin Infect Dis 2007 45 : 1266 1273.
77. 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 : 1062 1069.
78. Mayfield JL, Leet T, Miller J et al. Environmental control to reduce transmission of Clostridium difficile. Clin Infect Dis 2000 31 : 995 1000.
79. Oughton MT, Loo VG, Dendukuri N et al. 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 : 939 944.
80. Boyce JM, Ligi C, Kohan C et al. 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 : 479 483.
81. 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 : 8 15.
82. 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 : 297 302.
83. 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 : 723 729.