Clostridium difficile infection: Epidemiology, risk factors and management

Nature Reviews Gastroenterology and Hepatology

Volumn 8, Issue 1, 2011, Pages 17-26

  Ananthakrishnan, Ashwin N ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; ANTIBIOTIC AGENT; CEPHALOSPORIN; CLINDAMYCIN; IMMUNOGLOBULIN; MACROLIDE; METRONIDAZOLE; PIPERACILLIN PLUS TAZOBACTAM; PROBIOTIC AGENT; QUINOLONE DERIVATIVE; RIFAXIMIN; TEICOPLANIN; TIGECYCLINE; VANCOMYCIN;

AGE DISTRIBUTION; BACTERIAL COLONIZATION; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; CLINICAL FEATURE; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM DIFFICILE INFECTION; COLON RESECTION; CYTOTOXICITY TEST; DRUG COST; DRUG DOSE COMPARISON; DRUG DOSE REDUCTION; DRUG EFFICACY; DRUG MEGADOSE; DRUG TREATMENT FAILURE; DRUG USE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDEMIOLOGICAL DATA; HEALTH CARE COST; HUMAN; INFECTION CONTROL; INFECTION RISK; INTESTINE LAVAGE; PATHOGENESIS; PRIORITY JOURNAL; RECURRENT INFECTION; REVIEW; RISK ASSESSMENT; RISK FACTOR; TREATMENT DURATION; TREATMENT INDICATION; TREATMENT RESPONSE;

CLOSTRIDIUM DIFFICILE; COLITIS; ENTEROCOLITIS, PSEUDOMEMBRANOUS; HUMANS; METRONIDAZOLE; PREVALENCE; RISK FACTORS; VANCOMYCIN;

EID: 78651111353     PISSN: 17595045     EISSN: 17595053     Source Type: Journal    
DOI: 10.1038/nrgastro.2010.190     Document Type: Review

References (91)

1. Bartlett, J. G. et al. Antibiotic-associated pseudomembranous colitis due to toxinproducing clostridia. N. Engl. J. Med. 298, 531-534 (1978).
2. Pituch, H. Clostridium difficile is no longer just a nosocomial infection or an infection of adults. Int. J. Antimicrob. Agents 33 (Suppl. 1), S42-S45 (2009).
3. Freeman, J. et al. The changing epidemiology of Clostridium difficile infections. Clin. Microbiol. Rev. 23, 529-549 (2010).
4. Kim, J. et al. epidemiological features of Clostridium difficile-associated disease among inpatients at childrens hospitals in the United States, 2001-2006. Pediatrics 122, 1266-1270 (2008).
5. Ananthakrishnan, A. N., Issa, M. & Binion, D. G. Clostridium difficile and inflammatory bowel disease. Gastroenterol. Clin. North Am. 38, 711-728 (2009).
6. Bartlett, J. G. The case for vancomycin as the preferred drug for treatment of Clostridium difficile infection. Clin. Infect. Dis. 46, 1489-1492 (2008).
7. Bartlett, J. G. & Gerding, D. N. Clinical recognition and diagnosis of Clostridium difficile infection. Clin. Infect. Dis. 46 (Suppl. 1), S12-S18 (2008).
8. McDonald, l. C., Owings, M. & Jernigan, D. B. Clostridium difficile infection in patients discharged from US short-stay hospitals, 1996- 2003. Emerg. Infect. Dis. 12, 409-415 (2006).
9. US Department of Health and Human Services. HCUPnet [online], (2010).
10. Pepin, J. et al. Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 171, 466-472 (2004).
11. Kuijper, e. J., Coignard, B. & Tull, P. emergence of Clostridium difficile-associated disease in North America and europe. Clin. Microbiol. Infect. 12 (Suppl. 6), 2-18 (2006).
12. rupnik, M., wilcox, M. H. & Gerding, D. N. Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7, 526-536 (2009).
13. Bauer, M. P. et al. Clinical and microbiological characteristics of community-onset Clostridium difficile infection in The Netherlands. Clin. Microbiol. Infect. 15, 1087-1092 (2009).
14. wilcox, M. H. et al. A case-control study of community-associated Clostridium difficile infection. J. Antimicrob. Chemother. 62, 388-396 (2008).
15. Kyne, l., Hamel, M. B., Polavaram, r. & Kelly, C. P. Health care costs and mortality associated with nosocomial diarrhea due to Clostridium difficile. Clin. Infect. Dis. 34, 346-353 (2002).
16. Dubberke, e. r. & wertheimer, A. I. review of current literature on the economic burden of Clostridium difficile infection. Infect. Control Hosp. Epidemiol. 30, 57-66 (2009).
17. Bartlett, J. G. Historical perspectives on studies of Clostridium difficile and C. difficile infection. Clin. Infect. Dis. 46 (Suppl. 1), S4-S11 (2008).
18. voth, D. e. & Ballard, J. D. Clostridium difficile toxins: mechanism of action and role in disease. Clin. Microbiol. Rev. 18, 247-263 (2005).
19. Giesemann, T., egerer, M., Jank, T. & Aktories, K. Processing of Clostridium difficile toxins. J. Med. Microbiol. 57, 690-696 (2008).
20. Drudy, D. et al. Isolation and characterisation of toxin A-negative, toxin B-positive Clostridium difficile in Dublin, Ireland. Clin. Microbiol. Infect. 13, 298-304 (2007).
21. Barbut, F. et al. Clinical features of Clostridium difficile-associated diarrhoea due to binary toxin (actin-specific ADP-ribosyltransferase)-producing strains. J. Med. Microbiol. 54, 181-185 (2005).
22. Mcellistrem, M. C. et al. A hospital outbreak of Clostridium difficile disease associated with isolates carrying binary toxin genes. Clin. Infect. Dis. 40, 265-272 (2005).
23. Geric, B. et al. Binary toxin-producing, large clostridial toxin-negative Clostridium difficile strains are enterotoxic but do not cause disease in hamsters. J. Infect. Dis. 193, 1143-1150 (2006).
24. Schwan, C. et al. Clostridium difficile toxin CDT induces formation of microtubule-based protrusions and increases adherence of bacteria. PLoS Pathog. 5, e1000626 (2009).
25. Pepin, J., valiquette, l. & Cossette, B. Mortality attributable to nosocomial Clostridium difficileassociated disease during an epidemic caused by a hypervirulent strain in Quebec. CMAJ 173, 1037-1042 (2005).
26. Clements, A. C. et al. Clostridium difficile PCr ribotype 027: assessing the risks of further worldwide spread. Lancet Infect. Dis. 10, 395-404 (2010).
27. loo, v. G. et al. A predominantly clonal multiinstitutional outbreak of Clostridium difficileassociated diarrhea with high morbidity and mortality. N. Engl. J. Med. 353, 2442-2449 (2005).
28. McDonald, l. C. et al. An epidemic, toxin genevariant strain of Clostridium difficile. N. Engl. J. Med. 353, 2433-2441 (2005).
29. Bauer, M. P. et al. Final results of the first paneuropean Clostridium difficile infection survey. Presented at the 20th european Congress of Clinical Microbiology and Infectious Diseases (eCCMID), vienna, Austria, 2010.
30. Pepin, J. 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. 41, 1254-1260 (2005).
31. Goorhuis, A. et al. emergence of Clostridium difficile infection due to a new hypervirulent strain, polymerase chain reaction ribotype 078. Clin. Infect. Dis. 47, 1162-1170 (2008).
32. Clayton, e. M. et al. The vexed relationship between Clostridium difficile and inflammatory bowel disease: an assessment of carriage in an outpatient setting among patients in remission. Am. J. Gastroenterol. 104, 1162-1169 (2009).
33. Kyne, l., warny, M., Qamar, A. & Kelly, C. P. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N. Engl. J. Med. 342, 390-397 (2000).
34. Kyne, l., warny, M., Qamar, A. & Kelly, C. P. Association between antibody response to toxin A and protection against recurrent Clostridium difficile diarrhoea. Lancet 357, 189-193 (2001).
35. Bartlett, J. G. Clinical practice. Antibioticassociated diarrhea. N. Engl. J. Med. 346, 334-339 (2002).
36. Bignardi, G. e. risk factors for Clostridium difficile infection. J. Hosp. Infect. 40, 1-15 (1998).
37. Gerding, D. N. Clostridium difficile 30 years on: what has, or has not, changed and why? Int. J. Antimicrob. Agents 33 (Suppl. 1), S2-S8 (2009).
38. Gerding, D. N. et al. Clostridium difficileassociated diarrhea and colitis. Infect. Control Hosp. Epidemiol. 16, 459-477 (1995).
39. Kelly, C. P. A 76-year-old man with recurrent Clostridium difficile-associated diarrhea: review of C. difficile infection. JAMA 301, 954-962 (2009).
40. Kelly, C. P. & laMont, J. T. Clostridium difficile infection. Annu. Rev. Med. 49, 375-390 (1998).
41. Diggs, N. G. & Surawicz, C. M. evolving concepts in Clostridium difficile colitis. Curr. Gastroenterol. Rep. 11, 400-405 (2009).
42. rupnik, M., Grabnar, M. & Geric, B. Binary toxin producing Clostridium difficile strains. Anaerobe 9, 289-294 (2003).
43. Gerding, D. N., Muto, C. A. & Owens, r. C. Jr. Measures to control and prevent Clostridium difficile infection. Clin. Infect. Dis. 46 (Suppl. 1), S43-S49 (2008).
44. Owens, r. C. Jr et al. Antimicrobial-associated risk factors for Clostridium difficile infection. Clin. Infect. Dis. 46 (Suppl. 1), S19-S31 (2008).
45. McFarland, l. v. renewed interest in a difficult disease: Clostridium difficile infections- epidemiology and current treatment strategies. Curr. Opin. Gastroenterol. 25, 24-35 (2009).
46. Debast, S. B. et al. Successful combat of an outbreak due to Clostridium difficile PCr ribotype 027 and recognition of specific risk factors. Clin. Microbiol. Infect. 15, 427-434 (2009).
47. Cohen, S. H. 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. 31, 431-455 (2010).
48. Ananthakrishnan, A. N., McGinley, e. l. & Binion, D. G. excess hospitalisation burden associated with Clostridium difficile in patients with inflammatory bowel disease. Gut 57, 205-210 (2008).
49. Issa, M. et al. Impact of Clostridium difficile on inflammatory bowel disease. Clin. Gastroenterol. Hepatol. 5, 345-351 (2007).
50. Dial, S. et al. risk of Clostridium difficile diarrhea among hospital inpatients prescribed proton pump inhibitors: cohort and case-control studies. CMAJ 171, 33-38 (2004).
51. Dial, S., Delaney, J. A., Barkun, A. N. & Suissa, S. Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficileassociated disease. JAMA 294, 2989-2995 (2005).
52. Greenstein, A. J. et al. risk factors for the development of fulminant Clostridium difficile colitis. Surgery 143, 623-629 (2008).
53. Butala, P. & Divino, C. M. Surgical aspects of fulminant Clostridium difficile colitis. Am. J. Surg. 200, 131-135 (2010).
54. Henrich, T. J., Krakower, D., Bitton, A. & Yokoe, D. S. Clinical risk factors for severe Clostridium difficile-associated disease. Emerg. Infect. Dis. 15, 415-422 (2009).
55. Fekety, r. N. & Shah, A. B. Diagnosis and treatment of Clostridium difficile colitis. JAMA 269, 71-75 (1993).
56. lundeen, S. J. Clostridium difficile enteritis: an early postoperative complication in inflammatory bowel disease patients after colectomy. J. Gastrointest. Surg. 11, 138-142 (2007).
57. Shen, B. O. et al. Clostridium difficile infection in patients with ileal pouch-anal anastomosis. Clin. Gastroenterol. Hepatol. 6, 782-788 (2008).
58. Crobach, M. J., Dekkers, O. M., wilcox, M. H. & Kuijper, e. J. european Society of Clinical Microbiology and Infectious Diseases (eSCMID): data review and recommendations for diagnosing Clostridium difficile-infection (CDI). Clin. Microbiol. Infect. 15, 1053-1066 (2009).
59. Fekety, r. Guidelines for the diagnosis and management of Clostridium difficile-associated diarrhea and colitis. American College of Gastroenterology, Practice Parameters Committee. Am. J. Gastroenterol. 92, 739-750 (1997).
60. Kononen, e. Diagnostic trends in Clostridium difficile detection in Finnish microbiology laboratories. Anaerobe 15, 261-265 (2009).
61. Gerding, D. N., Muto, C. A. & Owens, r. C. Jr. Treatment of Clostridium difficile infection. Clin. Infect. Dis. 46 (Suppl. 1), S32-S42 (2008).
62. leffler, D. A. & lamont, J. T. Treatment of Clostridium difficile-associated disease. Gastroenterology 136, 1899-1912 (2009).
63. Teasley, D. G. et al. Prospective randomised trial of metronidazole versus vancomycin for Clostridium difficile-associated diarrhoea and colitis. Lancet 8358, 1043-1046 (1983).
64. wenisch, C. et al. Comparison of vancomycin, teicoplanin, metronidazole, and fusidic acid for the treatment of Clostridium difficile-associated diarrhea. Clin. Infect. Dis. 22, 813-818 (1996).
65. Bolton, r. P. & Culshaw, M. A. Faecal metronidazole concentrations during oral and intravenous therapy for antibiotic associated colitis due to Clostridium difficile. Gut 27, 1169-1172 (1986).
66. Pepin, J. et al. Increasing risk of relapse after treatment of Clostridium difficile colitis in Quebec, Canada. Clin. Infect. Dis. 40, 1591-1597 (2005).
67. Zar, F. A., Bakkanagari, S. r., Moorthi, K. M. & Davis, M. B. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin. Infect. Dis. 45, 302-307 (2007).
68. Aslam, S., Hamill, r. J. & Musher, D. M. Treatment of Clostridium difficile-associated disease: old therapies and new strategies. Lancet Infect. Dis. 5, 549-557 (2005).
69. Musher, D. M. et al. relatively poor outcome after treatment of Clostridium difficile colitis with metronidazole. Clin. Infect. Dis. 40, 1586-1590 (2005).
70. Hu, M. Y. et al. A prospective study of risk factors and historical trends in metronidazole failure for Clostridium difficile infection. Clin. Gastroenterol. Hepatol. 6, 1354-1360 (2008).
71. Fekety, r. et al. Treatment of antibioticassociated Clostridium difficile colitis with oral vancomycin: comparison of two dosage regimens. Am. J. Med. 86, 15-19 (1989).
72. Pepin, J. vancomycin for the treatment of Clostridium difficile infection: for whom is this expensive bullet really magic? Clin. Infect. Dis. 46, 1493-1498 (2008).
73. louie, T. results of a phase III trial comparing tolveamer, vancomycin and metronidazole in Clostridium difficile-associated diarrhea (CDAD). Presented at the Interscience Conference on Antimicrobial Agents and Chemotherapy (washington DC), 2007.
74. Jiang, Z. D., Dupont, H. l., la rocco, M. & Garey, K. w. In vitro activity of rifaximin and rifampin against clinical isolates of Clostridium difficile in Houston, Texas. Anaerobe doi:10.1016/j.anaerobe.2008.12.008.
75. Johnson, S. recurrent Clostridium difficile infection: a review of risk factors, treatments, and outcomes. J. Infect. 58, 403-410 (2009).
76. Garey, K. w., Sethi, S., Yadav, Y. & DuPont, H. l. Meta-analysis to assess risk factors for recurrent Clostridium difficile infection. J. Hosp. Infect. 70, 298-304 (2008).
77. McFarland, l. v., elmer, G. w. & Surawicz, C. M. Breaking the cycle: treatment strategies for 163 cases of recurrent Clostridium difficile disease. Am. J. Gastroenterol. 97, 1769-1775 (2002).
78. Johnson, S. et al. Interruption of recurrent Clostridium difficile-associated diarrhea episodes by serial therapy with vancomycin and rifaximin. Clin. Infect. Dis. 44, 846-848 (2007).
79. Johnson, S. et al. rifaximin redux: treatment of recurrent Clostridium difficile infections with rifaximin immediately post-vancomycin treatment. Anaerobe 15, 290-291 (2009).
80. McFarland, l. v. Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. Am. J. Gastroenterol. 101, 812-822 (2006).
81. Miller, M. Fidaxomicin (OPT-80) for the treatment of Clostridium difficile infection. Expert Opin. Pharmacother. 11, 1569-1578 (2010).
82. Cornely, O. A. et al. randomized controlled trial (rCT) of fidaxomicin (FDX) versus vancomycin (vAN) in treatment of recurrent Clostridium difficile infection (CDI). Presented at the Interscience Conference on Antimicrobial Agents and Chemotherapy, 2010.
83. wilcox, M. H. Descriptive study of intravenous immunoglobulin for the treatment of recurrent Clostridium difficile diarrhoea. J. Antimicrob. Chemother. 53, 882-884 (2004).
84. lowy, I. et al. Treatment with monoclonal antibodies against Clostridium difficile toxins. N. Engl. J. Med. 362, 197-205 (2010).
85. Safdar, A. Treatment with monoclonal antibodies against Clostridium difficile toxins. N. Engl. J. Med. 362, 1444-1446 (2010).
86. van Nood, e., Speelman, P., Kuijper, e. J. & Keller, J. J. Struggling with recurrent Clostridium difficile infections: is donor faeces the solution? Euro. Surveill. 14, 19316 (2009).
87. Bauer, M. P., van Dissel, J. T. & Kuijper, e. J. Clostridium difficile: controversies and approaches to management. Curr. Opin. Infect. Dis. 22, 517-524 (2009).
88. McPherson, S. et al. Intravenous immunoglobulin for the treatment of severe, refractory, and recurrent Clostridium difficile diarrhea. Dis. Colon Rectum 49, 640-645 (2006).
89. Abougergi, M. S., Broor, A., Cui, w. & Jaar, B. G. Intravenous immunoglobulin for the treatment of severe Clostridium difficile colitis: an observational study and review of the literature. J. Hosp. Med. 5, e1-e9 (2010).
90. Herpers, B. l. et al. Intravenous tigecycline as adjunctive or alternative therapy for severe refractory Clostridium difficile infection. Clin. Infect. Dis. 48, 1732-1735 (2009).
91. vonberg, r. P. et al. Infection control measures to limit the spread of Clostridium difficile. Clin. Microbiol. Infect. 14 (Suppl. 5), 2-20 (2008).