Clostridium difficile infection and inflammatory bowel disease

Scandinavian Journal of Gastroenterology

Volumn 45, Issue 3, 2010, Pages 261-272

  Musa, Saif ^a   Thomson, Sam ^a   Cowan, Matthew ^a   Rahman, Tony ^a  

^a ST GEORGE S HOSPITAL   (United Kingdom)

Author keywords

Clostridium difficile; Crohn's disease; Epidemiology; Inflammatory bowel diseases; Pseudomembranous enterocolitis; Risk factors; Treatment; Ulcerative colitis

Indexed keywords

ADALIMUMAB; ALPHA DEFENSIN; AMINOSALICYLIC ACID; AZATHIOPRINE; CORTICOSTEROID; CYCLOSPORIN; IMMUNOGLOBULIN; INFLIXIMAB; MERCAPTOPURINE; METHOTREXATE; METRONIDAZOLE; NITAZOXANIDE; PROBIOTIC AGENT; PROTON PUMP INHIBITOR; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIFALAZIL; RIFAMPICIN; RIFAXIMIN; TACROLIMUS; TIGECYCLINE; TIZOXANIDE; TOLEVAMER; VANCOMYCIN;

ABDOMINAL CRAMP; ANTIBIOTIC THERAPY; BLOODY DIARRHEA; CLINICAL FEATURE; CLINICAL TRIAL; CLOSTRIDIUM DIFFICILE INFECTION; COLON RESECTION; CORTICOSTEROID THERAPY; CROHN DISEASE; DRUG COST; DRUG MEGADOSE; DRUG SUBSTITUTION; DRUG TREATMENT FAILURE; DRUG WITHDRAWAL; ENTERITIS; FECES ANALYSIS; HUMAN; INTESTINE FLORA; NAUSEA; PATHOGENESIS; PRIORITY JOURNAL; RECURRENT INFECTION; REVIEW; RISK FACTOR; SACCHAROMYCES BOULARDII; TREATMENT OUTCOME; ULCERATIVE COLITIS;

CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM INFECTIONS; HUMANS; INFLAMMATORY BOWEL DISEASES; RISK FACTORS; SEVERITY OF ILLNESS INDEX; TREATMENT OUTCOME;

EID: 77149140102     PISSN: 00365521     EISSN: 15027708     Source Type: Journal    
DOI: 10.3109/00365520903497098     Document Type: Review

References (103)

1. Bartlett JG, Moon N, Chang TW, Taylor N, Onderdonk AB. Role of Clostridium difficile in antibiotic-associated pseudomembranous colitis. Gastroenterology 1978;75:778-782
2. Larson HE, Parry JV, Price AB, Davies DR, Dolby J, Tyrrell DA. Un-described toxin in pseudomembranous colitis. Br Med J 1977;1:1246-1248
3. LaMont JT, Trnka YM. Therapeutic implications of Clostridium difficile toxin during relapse of chronic inflammatory bowel disease. Lancet 1980;1:381-383
4. Bolton RP, Sherriff RJ, Read AE. Clostridium difficile associated diarrhoea: a role in inflammatory bowel disease? Lancet 1980;1:383-384
5. Trnka YM, LaMont JT. Association of Clostridium difficile toxin with symptomatic relapse of chronic inflammatory bowel disease. Gastroenterology 1980;80:693-696
6. Keighley MR, Youngs D, Johnson M, Allan RN, Burdon DW. Clostridium difficile toxin in acute diarrhoea complicating inflammatory bowel disease. Gut 1982;23: 410-414
7. Rolny P, Järnerot G, Möllby R. Occurrence of Clostridium difficile toxin in inflammatory bowel disease. Scand J Gastroenterol 1983;18:61-64
8. Gurian L, Klein K, Ward TT. Role of Clostridium difficile and Campylobacter jejuni in relapses of inflammatory bowel disease. West J Med 1983;138:359-360
9. Burke DA, Axon AT. Clostridium difficile, sulphasalazine, and ulcerative colitis. Postgrad Med J 1987;63:955-957
10. Weber P, Koch M, Heizmann WR, Scheurlen M, Jenss H, Hartmann F. Microbic superinfection in relapse of inflammatory bowel disease. J Clin Gastroenterol 1992;14:302-308
11. Mylonaki M, Langmead L, Pantes A, Johnson F, Rampton DS. Enteric infection in relapse of inflammatory bowel disease: importance of microbiological examination of stool. Eur J Gastroenterol Hepatol 2004;16:775-778
12. Meyer AM, Ramzan NN, Loftus EV, Heigh RI, Leighton JA. The diagnostic yield of stool pathogen studies during relapses of inflammatory bowel disease. J Clin Gastroenterol 2004;38:772-775
13. Rodemann, JF, Dubberke ER, Reske KA, Seo da H, Stone CD. Incidence of Clostridium difficile infection in inflammatory bowel disease. Clin Gastroenterol Hepatol 2007;5:339-344
14. Issa M, Vijayapal A, Graham MB, Beaulieu DB, Otterson MF, Lundeen S, et al. Impact of Clostridium difficile on inflammatory bowel disease. Clin Gastroenterol Hepatol 2007;5:345-351
15. Nguyen GC, Kaplan GG, Harris ML, Brant SR. A national survey of the prevalence and impact of Clostridium difficile infection among hospitalized inflammatory bowel disease patients. Am J Gastroenterol 2008;103:1443-1450
16. Greenstein AJ, Byrn JC, Zhang LP, Swedish KA, Jahn AE, Divino CM. Risk factors for the development of fulminant Clostridium difficile colitis. Surgery 2008;143:623-629
17. Ricciardi R, Ogilvie Jr JW, Roberts PL, Marcello PW, Concannon TW, Baxter NN. Epidemiology of Clostridium difficile colitis in hospitalized patients with inflammatory bowel diseases. Dis Colon Rectum 2009;52:40-45
18. Ananthakrishnan AN, McGinley EL, Binion DG. Excess hospitalisation burden associated with Clostridium difficile in patients with inflammatory bowel disease. Gut 2008;57:205-210
19. Jodorkovsky D, Young Y, Abreu MT. Clinical outcomes of patients with ulcerative colitis and co-existing Clostridium difficile Infection. Dig Dis Sci 2009;Mar 3 [Epub ahead of print].
20. UK IBD Audit: Second round: full national report and appendices, 2009. Available from: http://www.rcplondon. ac.uk/clinical-standards/ceeu/Current- work/Pages/UK-IBDAudit. aspx#background.
21. Caprilli R, Gassull MA, Escher JC, Moser G, Munkholm P, Forbes A, et al. European Crohn's and Colitis Organisation. European evidence based consensus on the diagnosis and management of Crohn's disease: special situations. Gut 2006;55 Suppl 1:36-58.
22. Travis SPL, Stange EF, Lémann M, Øresland T, Bemelman WA, Chowers Y, et al. European Crohn's and Colitis Organisation. European evidence-based Consensus on the management of ulcerative colitis: Current management. J Crohn's Colitis 2008;2:24-62.
23. McLaren L, Bartlett J, Gitnick G, and the IBD Research Group. Infectious agents in inflammatory bowel disease (IBD): collaborative studies. Gastroenterology 1981;80:1228.
24. Meyers S, Mayer L, Bottone E, Desmond E, Janowitz HD. Occurrence of Clostridium difficile toxin during the course of inflammatory bowel disease. Gastroenterology 1981;80:697-700.
25. Dorman SA, Liggoria E, Winn WC, Beeken WL. Isolation of Clostridium difficile from patients with inactive Crohn's disease. Gastroenterology 1982;82:1348-1351
26. Tvede M, Willumsen, L. Clostridium difficile in patients with irritable bowel syndrome and ulcerative colitis. Lancet 1982;1:1124.
27. Tremaine WJ, Billie J, Huizenga KA, Washington JA, Ilstrup DM. Factors which influence the occurrence of Clostridium dfficile infections in inflammatory bowel disease. Gastroenterology 1983;84:1337.
28. Kochhar R, Ayyagari A, Goenka MK, Dhali GK, Aggarwal R, Mehta SK. Role of infectious agents in exacerbations of ulcerative colitis in India. A study of Clostridium difficile. J Clin Gastroenterol 1993;16:26-30.
29. Clayton EM, Rea MC, Shanahan F, Quigley EM, Kiely B, Hill C, 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 2009;104:1162-1169
30. Wang Y, Shen B. Clostridium difficile-associated diarrhea in Crohn's disease patients with Ostomy. Inflamm Bowel Dis 2009;Apr 30 [Epub ahead of print].
31. Shen BO, Jiang ZD, Fazio VW, Remzi FH, Rodriguez L, Bennett AE, et al. Clostridium difficile infection in patients with ileal pouch-anal anastomosis. Clin Gastroenterol Hepatol 2008;6:782-788
32. Health Protection Agency. Clostridium difficile infection: How to deal with the problem, 2009. Available from: http://www.hpa.org.uk/web/HPAwebFile/ HPAweb-C/ 1232006607827.
33. Kuijper EJ, Coignard B, Tüll P. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect 2006;12(Suppl 6):2-18.
34. McDonald LV, Coignard B, Dubberbeke E, Song X, Horan T, Kutty PK. The Centre for Disease Control and Prevention. Surveillance definitions for Clostridium difficile-associated disease, 2007. Available from: http:// www.cdc.gov/ncidod/dhqp/pdf/surveillance/Surveillance-c- diff.pdf.
35. Stange EF, Travis SP, Vermeire S, Beglinger C, Kupcinkas L, Geboes K, et al. European Crohn's and Colitis Organisation (ECCO). European evidence based consensus on the diagnosis and management of Crohn's disease: definitions and diagnosis. Gut 2006;55(Suppl 1):1-15.
36. D'Haens G, Sandborn WJ, Feagan BG, Geboes K, Hanauer SB, Irvine EJ, et al. A review of activity indices and efficacy end points for clinical trials of medical therapy in adults with ulcerative colitis. Gastroenterology 2007;132:763-786
37. Stange EF, Travis SP, Vermeire S, Beglinger C, Kupcinkas L, Geboes K, et al., for the European Crohn's and Colitis Organisation (ECCO). European evidencebased consensus on the diagnosis and management of ulcerative colitis: Definitions and diagnosis, 2007. Available from: http://www.ecco-ibd.eu/ publications/guidelines.php? navId=30.
38. McFarland LV. Update on the changing epidemiology of Clostridium difficile-associated disease. Nat Clin Pract Gastroenterol Hepatol 2008;5:40-48
39. Powell N, Jung SE, Krishnan B. Clostridium difficile infection and inflammatory bowel disease: a marker for disease extent? Gut 2008;57:1183-1184
40. Ben-Horin S, Margalit M, Bossuyt P, Maul J, Shapira Y, Bojic D, et al. European Crohn's and Colitis Organization (ECCO). Combination immunomodulator and antibiotic treatment in patients with inflammatory bowel disease and clostridium difficile infection. Clin Gastroenterol Hepatol 2009;7:981-987
41. Schneeweiss S, Korzenik J, Solomon DH, Canning C, Lee J, Bressler B. Infliximab and other immunomodulating drugs in patients with inflammatory bowel disease and the risk of serious bacterial infections. Aliment Pharmacol Ther 2009;30:253-264
42. Greenfield C, Aguilar Ramirez JR, Pounder RE, Williams T, Danvers M, Marper SR, et al. Clostridium difficile and inflammatory bowel disease. Gut 1983;24:713-717
43. Toruner M, Loftus EV Jr, Harmsen WS, Zinsmeister AR, Orenstein R, Sandborn WJ, et al. Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology 2008;134:929-936
44. Tremaine WJ. Inflammatory bowel disease and Clostridium difficile-associated diarrhea: a growing problem. Clin Gastroenterol Hepatol 2007;5:310-311
45. Sunenshine RH, McDonald LC, for the Centre for Disease Control and PreventionSurveillance Clostridium difficileassociated disease: New challenges from an established pathogen, 2006. Available from: http://www.cdc.gov/ncidod/ dhqp/id-Cdiff.html.
46. Issa M, Ananthakrishnan AN, Binion DG. Clostridium difficile and inflammatory bowel disease. Inflamm Bowel Dis 2008;14:1432-1442
47. Navaneethan U, Giannella RA. Thinking beyond the colon- small bowel involvement in Clostridium difficile infection. Gut Pathog 2009;1:7.
48. Poutanen SM, Simor AE. Clostridium difficile-associated diarrhea in adults. CMAJ 2004;171:51-58
49. Bartlett JG. Clinical practice. Antibiotic-associated diarrhea. N Engl J Med 2002;346:334-339
50. Owens RC, Donskey CJ, Gaynes RP, Loo VG, Muto CA. Antimicrobial- associated risk factors for Clostridium difficile infection. Clin Infect Dis 2008;46(Suppl 1):19-31.
51. Warny M, Vaerman JP, Avesani V, Delmée M. Human antibody response to Clostridium difficile toxin A in relation to clinical course of infection. Infect Immun 1994;62:384-389
52. Kelly CP, Pothoulakis C, LaMont, JT. Clostridium difficile colitis. N Engl J Med 1994;330:257-262
53. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007;448:427-434
54. Sonnenberg A. Similar geographic variations of mortality and hospitalization associated with IBD and Clostridium difficile colitis. Inflamm Bowel Dis 2009;Jul 27 [Epub ahead of print].
55. Nomura K, Fujimoto Y, Yamashita M, Morimoto Y, Ohshiro M, Sato K, et al. Absence of pseudomembranes in Clostridium difficile-associated diarrhea in patients using immunosuppression agents. Scand J Gastroenterol 2009;44:74-78
56. Wang A, Takeshima F, Ikeda M, Ohnita K, Furusu H, Isomoto H, et al. Ulcerative colitis complicating pseudomembranous colitis of the right colon. J Gastroenterol 2002;37:309-312
57. García-Osogobio S, Takahashi T, Gamboa-Domínguez A, Medina H, Arch J, Mass W, et al. Toxic pseudomembranous colitis in a patient with ulcerative colitis. Inflamm Bowel Dis 2000;6:188-190
58. Chen FC, Woods R. Pseudomembranous panenteritis and septicaemia in a patient with ulcerative colitis. Aust N Z J Surg 1996;66:565-567
59. Giesemann T, Guttenberg G, Aktories K. Human alphadefensins inhibit Clostridium difficile toxin B. Gastroenterology 2008;134:2049-2058
60. Salzman NH. Defensins versus bacteria: not just antibiotics anymore. Gastroenterology 2008;134:2174-2177
61. Ramasundara M, Leach ST, Lemberg DA, Day AS. Defensins and inflammation: the role of defensins in inflammatory bowel disease. J Gastroenterol Hepatol 2009;24:202-208
62. Savoye G. Alpha-defensins and Clostridium difficile recent growing concerns in inflammatory bowel disease. Am J Gastroenterol 2008;103:3215.
63. Testore GP, Nardi F, Babudieri S, Giuliano M, Di Rosa R, Panichi G. Isolation of Clostridium difficile from human jejunum: identification of a reservoir for disease? J Clin Pathol 1986;39:861-862
64. Linskens RK, Huijsdens XW, Savelkoul PH, Vandenbroucke- Grauls CM, Meuwissen SG. The bacterial flora in inflammatory bowel disease: current insights in pathogenesis and the influence of antibiotics and probiotics. Scand J Gastroenterol 2001;234:29-40.
65. Ott SJ, Musfeldt M, Wenderoth DF, Hampe J, Brant O, Fölsch UR, et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 2004;53:685-693
66. Sorg JA, Sonenshein AL. Bile salts and glycine as cogerminants for Clostridium difficile spores. J Bacteriol 2008;190:2505-2512
67. Williams RN, Hemingway D, Miller AS. Enteral Clostridium difficile, an emerging cause for high-output ileostomy. J Clin Pathol 2009;62:951-953
68. Mann SD, Pitt J, Springall RG, Thillainayagam AV. Clostridium difficile infection - an unusual cause of refractory pouchitis: report of a case. Dis Colon Rectum 2003;46:267-270
69. Shen B, Goldblum JR, Hull TL, Remzi FH, Bennett AE, Fazio VW. Clostridium difficile-associated pouchitis. Dig Dis Sci 2006;51:2361-2364
70. Boland E, Thompson JS. Fulminant Clostridium difficile enteritis after proctocolectomy and ileal pouch-anal anastamosis. Gastroenterol Res Pract 2008;2008:985658.
71. Gerding DN, Muto CA, Owens RC Jr. Treatment of Clostridium difficile infection. Clin Infect Dis 2008;46(Suppl 1): S32-42.
72. Kuntz DP, Shortsleeve MJ, Kantrowitz PA, Gauvin GP. Clostridium difficile enteritis. A cause of intramural gas. Dig Dis Sci 1993;38:1942-1944
73. Vesoulis Z, Williams G, Matthews B. Pseudomembranous enteritis after proctocolectomy: report of a case. Dis Colon Rectum 2000;43:551-554
74. Freiler JF, Durning SJ, Ender PT. Clostridium difficile small bowel enteritis occurring after total colectomy. Clin Infect Dis 2001;33:1429-1431
75. Kim KA, Wry P, Hughes Jr E, Butcher J, Barbot D. Clostridium difficile small-bowel enteritis after total proctocolectomy: a rare but fatal, easily missed diagnosis. Report of a case. Dis Colon Rectum 2007;50:920-923
76. Lundeen SJ, Otterson MF, Binion DG, Carman ET, Peppard WJ. Clostridium difficile enteritis: an early postoperative complication in inflammatory bowel disease patients after colectomy. J Gastrointest Surg 2007;11: 138-142
77. Wood MJ, Hyman N, Hebert JC, Blaszyk H. Catastrophic Clostridium difficile enteritis in a pelvic pouch patient: report of a case. J Gastrointest Surg 2008;12:350-352
78. Follmar KE, Condron SA, Turner II, Nathan JD, Ludwig KA. Treatment of metronidazole-refractory Clostridium difficile enteritis with vancomycin. Surg Infect (Larchmt) 2008;9:195-200.
79. Yafi FA, Selvasekar CR, Cima RR. Clostridium difficile enteritis following total colectomy. Tech Coloproctol 2008;12:73-74
80. Fleming F, Khursigara N, O'Connell N, Darby S, Waldron D. Fulminant small bowel enteritis: a rare complication of Clostridium difficile-associated disease. Inflamm Bowel Dis 2009;15:801-802
81. Croagh DG, Bach SP, Keck J. A rare cause of acute abdomen after proctocolectomy. Am J Surg 2009;197:41-42
82. Shen B, Remzi FH, Fazio VW. Fulminant Clostridium difficile-associated pouchitis with a fatal outcome. Nat Rev Gastroenterol Hepatol 2009;6:492-495
83. Planche T, Aghaizu A, Holliman R, Riley P, Poloniecki J, Breathnach A, et al. Diagnosis of Clostridium difficile infection by toxin detection kits: a systematic review. Lancet Infect Dis 2008;8:777-784
84. Johnson S, Homann SR, Bettin KM, Quick JN, Clabots CR, Peterson CL, 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.
85. Vonberg RP, Kuijper EJ, Wilcox MH, Barbut F, Tüll P, Gastmeier P, et al. Infection control measures to limit the spread of Clostridium difficile. Clin Microbiol Infect 2008;14 (Suppl 5):2-20.
86. Teasley DG, Gerding DN, Olson MM, Peterson LR, Gebhard RL, Schwartz MJ, et al. Prospective randomised trial of metronidazole versus vancomycin for Clostridium difficile-associated diarrhoea and colitis. Lancet 1983;2: 1043-1046
87. Wenisch C, Parschalk B, Hasenhundl M, Hirschl AM, Graninger W. Comparison of vancomycin, teicoplanin, metronidazole, and fusidic acid for the treatment of Clostridium difficile-associated diarrhea. Clin Infect Dis 1996; 22:813-818
88. Chang TW, Gorbach SL, Bartlett, JG. Inhibition of binding of Clostridium difficile toxin by steroids. J Infect Dis 2008;142:113.
89. Castagliuolo I, Karalis K, Valenick L, Pasha A, Nikulasson S, Wlk M, et al. Endogenous corticosteroids modulate Clostridium difficile toxin A-induced enteritis in rats. Am J Physiol Gastrointest Liver Physiol 2001;280:G539-45.
90. Binion DG. Management of Clostridium difficile infection in inflammatory bowel disease. Gastroenterol Hepatol 2009;5:253-256
91. Musher DM, Aslam S, Logan N, Nallacheru S, Bhaila I, Borchert F, et al. Relatively poor outcome after treatment of Clostridium difficile colitis with metronidazole. Clin Infect Dis 2006;40:1586-1590
92. Nair S, Yadav D, Corpuz M, Pitchumoni CS. Clostridium difficile colitis: factors influencing treatment failure and relapse-a prospective evaluation. Am J Gastroenterol 1998;93:1873-1876
93. Pepin J, Alary ME, Valiquette L, Raiche E, Ruel J, Fulop K, et al. Increasing risk of relapse after treatment of Clostridium difficile colitis in Quebec, Canada. Clin Infect Dis 2005;40:1591-1597
94. Hermsen JL, Dobrescu C, Kudsk KA. Clostridium difficile infection: a surgical disease in evolution. J Gastrointest Surg 2008;12:1512-1517
95. Synnott K, Mealy K, Merry C, Kyne L, Keane C, Quill R. Timing of surgery for fulminating pseudomembranous colitis. Br J Surg 1998;85:229-231
96. Chan S, Kelly M, Helme S, Gossage J, Modarai B, Forshaw M. Outcomes following colectomy for Clostridium difficile colitis. Int J Surg 2009;7:78-81.
97. Koss K, Clark MA, Sanders DS, Morton D, Keighley MR, Goh J. The outcome of surgery in fulminant Clostridium difficile colitis. Colorectal Dis 2006;8:149-154
98. Berman L, Carling T, Fitzgerald TN, Bell RL, Duffy AJ, Longo WE, et al. Defining surgical therapy for pseudomembranous colitis with toxic megacolon. J Clin Gastroenterol 2008;42:476-480
99. Jaber MR, Olafsson S, Fung WL, Reeves ME. Clinical review of the management of fulminant Clostridium difficile infection. Am J Gastroenterol 2008;103: 3195-3203
100. Pepin J, Vo TT, Boutros M, Marcotte E, Dial S, Dubé S, et al. Risk factors for mortality following emergency colectomy for fulminant Clostridium difficile infection. Dis Colon Rectum 2009;52:400-405
101. Issa M, Weber LR, Skaros S, Dawn M, Borromeo B, Emmons J, et al. Decreasing rates of colectomy despite high rates of hospitalization in Clostridium difficile infected IBD patients: a tertiary referral center experience. Gastroenterology 2007;132:A663.
102. Johnson S. Recurrent Clostridium difficile infection: causality and therapeutic approaches. Int J Antimicrob Agents 2009;33(Suppl 1):S33-6.
103. Bauer MP, van Dissel JT, Kuijper EJ. Clostridium difficile: controversies and approaches to management. Curr Opin Infect Dis 2009;22:517-524