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Published in: BMC Gastroenterology 1/2019

Open Access 01-12-2019 | Ulcerative Colitis | Research article

Retrospective analysis of Clostridium difficile infection in patients with ulcerative colitis in a tertiary hospital in China

Authors: Hui Xu, Hao Tang, Tao Xu, Meng Xiao, Ji Li, Bei Tan, Hong Yang, Hong Lv, Yue Li, Jiaming Qian

Published in: BMC Gastroenterology | Issue 1/2019

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Abstract

Background

Many reports have documented the increasing impact of Clostridium difficile infection (CDI) in patients with ulcerative colitis (UC). We conducted a retrospective study to determine the incidence, clinical characteristics, risk factors and prognosis of CDI in patients with UC.

Methods

We studied patients with UC, hospitalized between January 2010 and December 2015 in a tertiary hospital in China. Stool samples were tested for C. difficile toxins A and B (CDAB) by enzyme immunoassays in UC patients with disease flare. CDI in UC patients was diagnosed by clinical symptoms and positive CDAB test, and each case was matched with CDAB-negative patients in a 1:2 ratio. Univariate and binary logistic regression analyses were used to measure the differences between patients with and without CDI.

Results

Thirty-four (8.92%) of 381 patients with UC were CDAB positive. Antibiotic exposure within 3 months prior to the study (P = 0.004), hospitalization within 1 month prior to the study (P = 0.025), systemic use of steroids (P = 0.002) and active cytomegalovirus (CMV) infection (P = 0.001) were higher in CDI than non-CDI patients. Binary logistic regression analysis revealed that CMV infection was associated with CDI (odds ratio = 13.502, 95% confidence interval 1.307–139.512, P = 0.029). UC patients with C. difficile and CMV co-infection had more severe colonoscopic features.

Conclusions

Recent use of antibiotics, prior hospitalization and systemic use of steroids increased the risk of CDI. CMV infection was an independent risk factor of CDI in patients with UC.
Literature
1.
go back to reference Bartlett JG, Chang TW, Gurwith M, Gorbach SL, Onderdonk AB. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med. 1978;298(10):531–4.PubMedCrossRef Bartlett JG, Chang TW, Gurwith M, Gorbach SL, Onderdonk AB. Antibiotic-associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med. 1978;298(10):531–4.PubMedCrossRef
2.
go back to reference Trifan A, Stanciu C, Stoica O, Girleanu I, Cojocariu C. Impact of Clostridium difficile infection on inflammatory bowel disease outcome: a review. World J Gastroenterol. 2014;20(33):11736–42.PubMedPubMedCentralCrossRef Trifan A, Stanciu C, Stoica O, Girleanu I, Cojocariu C. Impact of Clostridium difficile infection on inflammatory bowel disease outcome: a review. World J Gastroenterol. 2014;20(33):11736–42.PubMedPubMedCentralCrossRef
3.
go back to reference Czepiel J, Biesiada G, Perucki W, Mach T. Clostridium difficile infection in patients with inflammatory bowel disease. Przeglad gastroenterologiczny. 2014;9(3):125–9.PubMedPubMedCentral Czepiel J, Biesiada G, Perucki W, Mach T. Clostridium difficile infection in patients with inflammatory bowel disease. Przeglad gastroenterologiczny. 2014;9(3):125–9.PubMedPubMedCentral
4.
go back to reference Leffler DA, Lamont JT. Clostridium difficile Infection. N Engl J Med. 2015;373(3):287–8.PubMed Leffler DA, Lamont JT. Clostridium difficile Infection. N Engl J Med. 2015;373(3):287–8.PubMed
5.
go back to reference 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(3):345–51.PubMedCrossRef 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(3):345–51.PubMedCrossRef
6.
go back to reference Rodemann JF, Dubberke ER, Reske KA, Seo DH, Stone CD. Incidence of Clostridium difficile infection in inflammatory bowel disease. Clin Gastroenterol Hepatol. 2007;5(3):339–44.PubMedCrossRef Rodemann JF, Dubberke ER, Reske KA, Seo DH, Stone CD. Incidence of Clostridium difficile infection in inflammatory bowel disease. Clin Gastroenterol Hepatol. 2007;5(3):339–44.PubMedCrossRef
7.
go back to reference 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(6):1443–50.PubMedCrossRef 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(6):1443–50.PubMedCrossRef
8.
go back to reference Yang H, Li Y, Wu W, Sun Q, Zhang Y, Zhao W, et al. The incidence of inflammatory bowel disease in northern China: a prospective population-based study. PLoS One. 2014;9(7):e101296.PubMedPubMedCentralCrossRef Yang H, Li Y, Wu W, Sun Q, Zhang Y, Zhao W, et al. The incidence of inflammatory bowel disease in northern China: a prospective population-based study. PLoS One. 2014;9(7):e101296.PubMedPubMedCentralCrossRef
9.
go back to reference Zhao J, Ng SC, Lei Y, Yi F, Li J, Yu L, et al. First prospective, population-based inflammatory bowel disease incidence study in mainland of China: the emergence of "western" disease. Inflamm Bowel Dis. 2013;19(9):1839–45.PubMed Zhao J, Ng SC, Lei Y, Yi F, Li J, Yu L, et al. First prospective, population-based inflammatory bowel disease incidence study in mainland of China: the emergence of "western" disease. Inflamm Bowel Dis. 2013;19(9):1839–45.PubMed
10.
go back to reference disease Csoib. Concensus on diagnosis and treatment of inflammatory bowel disease. Chin J Gastroenterol. 2012;17(12):763–81. disease Csoib. Concensus on diagnosis and treatment of inflammatory bowel disease. Chin J Gastroenterol. 2012;17(12):763–81.
11.
go back to reference Silverberg MS, Satsangi J, Ahmad T, Arnott ID, Bernstein CN, Brant SR, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19(Suppl A):5a–36a.PubMedCrossRef Silverberg MS, Satsangi J, Ahmad T, Arnott ID, Bernstein CN, Brant SR, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19(Suppl A):5a–36a.PubMedCrossRef
12.
go back to reference Schroeder KW, Tremaine WJ, Ilstrup DM. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. N Engl J Med. 1987;317(26):1625–9.PubMedCrossRef Schroeder KW, Tremaine WJ, Ilstrup DM. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. N Engl J Med. 1987;317(26):1625–9.PubMedCrossRef
13.
go back to reference Herrera-Cáceres JO, Camacho-Ortiz A, Galindo-Fraga A, Hernández-Durán M, Cordero-Rangel A, Hernández-Cruz A, et al. Concordance between two enzyme immunoassays for the detection of Clostridium difficile toxins. Arch Med Res. 2010;41(2):92–6.PubMedCrossRef Herrera-Cáceres JO, Camacho-Ortiz A, Galindo-Fraga A, Hernández-Durán M, Cordero-Rangel A, Hernández-Cruz A, et al. Concordance between two enzyme immunoassays for the detection of Clostridium difficile toxins. Arch Med Res. 2010;41(2):92–6.PubMedCrossRef
14.
go back to reference Issa M, Ananthakrishnan AN, Binion DG. Clostridium difficile and inflammatory bowel disease. Inflamm Bowel Dis. 2008;14(10):1432–42.PubMedCrossRef Issa M, Ananthakrishnan AN, Binion DG. Clostridium difficile and inflammatory bowel disease. Inflamm Bowel Dis. 2008;14(10):1432–42.PubMedCrossRef
15.
go back to reference Zhang T, Lin QY, Fei JX, Zhang Y, Lin MY, Jiang SH, et al. Clostridium difficile infection worsen outcome of hospitalized patients with inflammatory bowel disease. Sci Rep. 2016;6:29791.PubMedPubMedCentralCrossRef Zhang T, Lin QY, Fei JX, Zhang Y, Lin MY, Jiang SH, et al. Clostridium difficile infection worsen outcome of hospitalized patients with inflammatory bowel disease. Sci Rep. 2016;6:29791.PubMedPubMedCentralCrossRef
16.
go back to reference Gu Y, Zhang MC, Sun J, Lv K, Zhong J. Risk factors and clinical outcome of clostridium difficile infection in patients with IBD:a Chinese single-center retrospective study of 260 cases. J Dig Dis. 2017;18(4):207–11. Gu Y, Zhang MC, Sun J, Lv K, Zhong J. Risk factors and clinical outcome of clostridium difficile infection in patients with IBD:a Chinese single-center retrospective study of 260 cases. J Dig Dis. 2017;18(4):207–11.
17.
go back to reference Goodhand JR, Alazawi W, Rampton DS. Systematic review: Clostridium difficile and inflammatory bowel disease. Aliment Pharmacol Ther. 2011;33(4):428–41.PubMedCrossRef Goodhand JR, Alazawi W, Rampton DS. Systematic review: Clostridium difficile and inflammatory bowel disease. Aliment Pharmacol Ther. 2011;33(4):428–41.PubMedCrossRef
18.
go back to reference Kaneko T, Matsuda R, Taguri M, Inamori M, Ogura A, Miyajima E, et al. Clostridium difficile infection in patients with ulcerative colitis: investigations of risk factors and efficacy of antibiotics for steroid refractory patients. Clin Res Hepatol Gastroenterol. 2011;35(4):315–20.PubMedCrossRef Kaneko T, Matsuda R, Taguri M, Inamori M, Ogura A, Miyajima E, et al. Clostridium difficile infection in patients with ulcerative colitis: investigations of risk factors and efficacy of antibiotics for steroid refractory patients. Clin Res Hepatol Gastroenterol. 2011;35(4):315–20.PubMedCrossRef
19.
go back to reference Ramos-Martinez A, Ortiz-Balbuena J, Curto-Garcia I, Asensio-Vegas A, Martinez-Ruiz R, Munez-Rubio E, et al. Risk factors for Clostridium difficile diarrhea in patients with inflammatory bowel disease. Span J Dig Dis. 2015;107(1):4–8. Ramos-Martinez A, Ortiz-Balbuena J, Curto-Garcia I, Asensio-Vegas A, Martinez-Ruiz R, Munez-Rubio E, et al. Risk factors for Clostridium difficile diarrhea in patients with inflammatory bowel disease. Span J Dig Dis. 2015;107(1):4–8.
20.
go back to reference Hensgens MP, Goorhuis A, Dekkers OM, Kuijper EJ. Time interval of increased risk for Clostridium difficile infection after exposure to antibiotics. J Antimicrob Chemother. 2012;67(3):742–8.PubMedCrossRef Hensgens MP, Goorhuis A, Dekkers OM, Kuijper EJ. Time interval of increased risk for Clostridium difficile infection after exposure to antibiotics. J Antimicrob Chemother. 2012;67(3):742–8.PubMedCrossRef
21.
go back to reference Bossuyt P, Verhaegen J, Van Assche G, Rutgeerts P, Vermeire S. Increasing incidence of Clostridium difficile-associated diarrhea in inflammatory bowel disease. J Crohns Colitis. 2009;3(1):4–7.PubMedCrossRef Bossuyt P, Verhaegen J, Van Assche G, Rutgeerts P, Vermeire S. Increasing incidence of Clostridium difficile-associated diarrhea in inflammatory bowel disease. J Crohns Colitis. 2009;3(1):4–7.PubMedCrossRef
22.
go back to reference Regnault H, Bourrier A, Lalande V, Nion-Larmurier I, Sokol H, Seksik P, et al. Prevalence and risk factors of Clostridium difficile infection in patients hospitalized for flare of inflammatory bowel disease: a retrospective assessment. Dig Liver Dis. 2014;46(12):1086–92.PubMedCrossRef Regnault H, Bourrier A, Lalande V, Nion-Larmurier I, Sokol H, Seksik P, et al. Prevalence and risk factors of Clostridium difficile infection in patients hospitalized for flare of inflammatory bowel disease: a retrospective assessment. Dig Liver Dis. 2014;46(12):1086–92.PubMedCrossRef
23.
go back to reference Das R, Feuerstadt P, Brandt LJ. Glucocorticoids are associated with increased risk of short-term mortality in hospitalized patients with clostridium difficile-associated disease. Am J Gastroenterol. 2010;105(9):2040–9.PubMedCrossRef Das R, Feuerstadt P, Brandt LJ. Glucocorticoids are associated with increased risk of short-term mortality in hospitalized patients with clostridium difficile-associated disease. Am J Gastroenterol. 2010;105(9):2040–9.PubMedCrossRef
24.
go back to reference 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(3):253–64.PubMedCrossRef 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(3):253–64.PubMedCrossRef
25.
go back to reference Chan KS, Lee WY, Yu WL. Coexisting cytomegalovirus infection in immunocompetent patients with Clostridium difficile colitis. J Microbiol Immunol Infect. 2016;49(6):829–36.PubMedCrossRef Chan KS, Lee WY, Yu WL. Coexisting cytomegalovirus infection in immunocompetent patients with Clostridium difficile colitis. J Microbiol Immunol Infect. 2016;49(6):829–36.PubMedCrossRef
26.
go back to reference Hung YP, Lee JC, Lin HJ, Liu HC, Wu YH, Tsai PJ, et al. Clinical impact of Clostridium difficile colonization. J Microbiol Immunol Infect. 2015;48(3):241–8.PubMedCrossRef Hung YP, Lee JC, Lin HJ, Liu HC, Wu YH, Tsai PJ, et al. Clinical impact of Clostridium difficile colonization. J Microbiol Immunol Infect. 2015;48(3):241–8.PubMedCrossRef
27.
go back to reference Hung Y-P, Lin H-J, Wu C-J, Chen P-L, Lee J-C, Liu H-C, et al. Vancomycin-resistant Clostridium innocuum bacteremia following oral vancomycin for Clostridium difficile infection. Anaerobe. 2014;30:24–6.PubMedCrossRef Hung Y-P, Lin H-J, Wu C-J, Chen P-L, Lee J-C, Liu H-C, et al. Vancomycin-resistant Clostridium innocuum bacteremia following oral vancomycin for Clostridium difficile infection. Anaerobe. 2014;30:24–6.PubMedCrossRef
28.
go back to reference Chen P-H, Lu IT, Lee B-J, Wang C-Y, Lee C-K. Age can be a problem: Clostridium difficile and cytomegalovirus colitis coinfection in an immunocompetent 90-year-old patient. Int J Gerontol. 2015;9(2):130–2.CrossRef Chen P-H, Lu IT, Lee B-J, Wang C-Y, Lee C-K. Age can be a problem: Clostridium difficile and cytomegalovirus colitis coinfection in an immunocompetent 90-year-old patient. Int J Gerontol. 2015;9(2):130–2.CrossRef
29.
go back to reference Stevens VW, Nelson RE, Schwab-Daugherty EM, Khader K, Jones MM, Brown KA, et al. Comparative effectiveness of vancomycin and metronidazole for the prevention of recurrence and death in patients with Clostridium difficile infection. JAMA Intern Med. 2017;177(4):546–53.PubMedCrossRef Stevens VW, Nelson RE, Schwab-Daugherty EM, Khader K, Jones MM, Brown KA, et al. Comparative effectiveness of vancomycin and metronidazole for the prevention of recurrence and death in patients with Clostridium difficile infection. JAMA Intern Med. 2017;177(4):546–53.PubMedCrossRef
30.
go back to reference Zar FA, Bakkanagari SR, Moorthi KM, Davis MB. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin Infect Dis. 2007;45(3):302–7.PubMedCrossRef Zar FA, Bakkanagari SR, Moorthi KM, Davis MB. A comparison of vancomycin and metronidazole for the treatment of Clostridium difficile-associated diarrhea, stratified by disease severity. Clin Infect Dis. 2007;45(3):302–7.PubMedCrossRef
31.
go back to reference Frolkis AD, Dykeman J, Negron ME, Debruyn J, Jette N, Fiest KM, et al. Risk of surgery for inflammatory bowel diseases has decreased over time: a systematic review and meta-analysis of population-based studies. Gastroenterology. 2013;145(5):996–1006.PubMedCrossRef Frolkis AD, Dykeman J, Negron ME, Debruyn J, Jette N, Fiest KM, et al. Risk of surgery for inflammatory bowel diseases has decreased over time: a systematic review and meta-analysis of population-based studies. Gastroenterology. 2013;145(5):996–1006.PubMedCrossRef
32.
go back to reference Negron ME, Rezaie A, Barkema HW, Rioux K, De Buck J, Checkley S, et al. Ulcerative colitis patients with Clostridium difficile are at increased risk of death, colectomy, and postoperative complications: a population-based inception cohort study. Am J Gastroenterol. 2016;111(5):691–704.PubMedCrossRef Negron ME, Rezaie A, Barkema HW, Rioux K, De Buck J, Checkley S, et al. Ulcerative colitis patients with Clostridium difficile are at increased risk of death, colectomy, and postoperative complications: a population-based inception cohort study. Am J Gastroenterol. 2016;111(5):691–704.PubMedCrossRef
33.
go back to reference Chen Y, Furuya-Kanamori L, Doi SA, Ananthakrishnan AN, Kirk M. Clostridium difficile infection and risk of colectomy in patients with inflammatory bowel disease: a Bias-adjusted meta-analysis. Inflamm Bowel Dis. 2017;23(2):200–7.PubMedCrossRef Chen Y, Furuya-Kanamori L, Doi SA, Ananthakrishnan AN, Kirk M. Clostridium difficile infection and risk of colectomy in patients with inflammatory bowel disease: a Bias-adjusted meta-analysis. Inflamm Bowel Dis. 2017;23(2):200–7.PubMedCrossRef
Metadata
Title
Retrospective analysis of Clostridium difficile infection in patients with ulcerative colitis in a tertiary hospital in China
Authors
Hui Xu
Hao Tang
Tao Xu
Meng Xiao
Ji Li
Bei Tan
Hong Yang
Hong Lv
Yue Li
Jiaming Qian
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Gastroenterology / Issue 1/2019
Electronic ISSN: 1471-230X
DOI
https://doi.org/10.1186/s12876-018-0920-x

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