Skip to main content
Top
Published in: Digestive Diseases and Sciences 8/2022

23-09-2021 | Chronic Inflammatory Bowel Disease | Original Article

Association Between Immunosuppressive Therapy and Outcome of Clostridioides difficile Infection: Systematic Review and Meta-Analysis

Authors: Yiting Li, Haifeng Cai, Daniel A. Sussman, Jean Donet, Kevin Dholaria, Jiajia Yang, Ami Panara, Ryan Croteau, Jamie S. Barkin

Published in: Digestive Diseases and Sciences | Issue 8/2022

Login to get access

Abstract

Background

Patients with Clostridioides difficile infection (CDI) often have coexisting medical problems requiring immunosuppressive therapy. However, limited data are available on the association between immunosuppressive therapy and CDI outcomes.

Aim

To determine the association between immunosuppressive therapy and CDI outcomes.

Methods

PubMed, Embase, and Cochrane Library were searched through February 2021. Two reviewers independently reviewed and included studies that compared adult CDI patients who received immunosuppressive therapy to those who did not. The primary outcome was complicated CDl, including death, surgery, shock, or ICU admission. Raw data or unadjusted odds ratios (ORs) were used to calculate pooled ORs with 95% confidence intervals (CIs).

Results

Twenty-two studies with a total of 5759 CDI patients were selected. Immunosuppressive therapy was significantly associated with both primary outcome and death, with pooled ORs of 1.61 (95% CI 1.33–1.96) and 1.73 (95% CI 1.39–2.15) separately. The association between corticosteroids and primary outcome was also significant with OR of 1.73 (95% CI 1.41, 2.12). In subgroup analysis, the factors explaining differences in study results included study quality, patient age, and whether individual studies had adjusted for potential confounders. In a systematic review, most studies suggested a positive association between immunosuppressive therapy and complicated outcomes of CDI in patients comorbid for IBD.

Conclusions

Our systematic review and meta-analysis demonstrate that immunosuppressive therapy is a risk factor for complicated outcomes of CDI.
Literature
1.
go back to reference Ananthakrishnan AN. Clostridium difficile infection: epidemiology, risk factors and management. Nat Rev Gastroenterol Hepatol. 2011;8:17–26.PubMedCrossRef Ananthakrishnan AN. Clostridium difficile infection: epidemiology, risk factors and management. Nat Rev Gastroenterol Hepatol. 2011;8:17–26.PubMedCrossRef
2.
go back to reference Stranges PM, Hutton DW, Collins CD. Cost-effectiveness analysis evaluating fidaxomicin versus oral vancomycin for the treatment of Clostridium difficile infection in the United States. Value Health. 2013;16:297–304.PubMedCrossRef Stranges PM, Hutton DW, Collins CD. Cost-effectiveness analysis evaluating fidaxomicin versus oral vancomycin for the treatment of Clostridium difficile infection in the United States. Value Health. 2013;16:297–304.PubMedCrossRef
3.
go back to reference Surawicz CM, Brandt LJ, Binion DG et al. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol. 2013;108:478–498.PubMedCrossRef Surawicz CM, Brandt LJ, Binion DG et al. Guidelines for diagnosis, treatment, and prevention of Clostridium difficile infections. Am J Gastroenterol. 2013;108:478–498.PubMedCrossRef
4.
go back to reference van Werkhoven CH, van der Tempel J, Jajou R et al. Identification of patients at high risk for Clostridium difficile infection: development and validation of a risk prediction model in hospitalized patients treated with antibiotics. Clin Microbiol Infect Official Public Eur Soc Clin Microbiol Infect Dis. 2015;21:e781-788. van Werkhoven CH, van der Tempel J, Jajou R et al. Identification of patients at high risk for Clostridium difficile infection: development and validation of a risk prediction model in hospitalized patients treated with antibiotics. Clin Microbiol Infect Official Public Eur Soc Clin Microbiol Infect Dis. 2015;21:e781-788.
5.
go back to reference Kuntz JL, Johnson ES, Raebel MA et al. Predicting the risk of Clostridium difficile infection following an outpatient visit: development and external validation of a pragmatic, prognostic risk score. Clin Microbiol Infect Official Public Eur Soc Clin Microbiol Infect Dis. 2015;21:256–262. Kuntz JL, Johnson ES, Raebel MA et al. Predicting the risk of Clostridium difficile infection following an outpatient visit: development and external validation of a pragmatic, prognostic risk score. Clin Microbiol Infect Official Public Eur Soc Clin Microbiol Infect Dis. 2015;21:256–262.
6.
go back to reference Linsky A, Gupta K, Lawler EV, Fonda JR, Hermos JA. Proton pump inhibitors and risk for recurrent Clostridium difficile infection. Arch Internal Med. 2010;170:772–778.CrossRef Linsky A, Gupta K, Lawler EV, Fonda JR, Hermos JA. Proton pump inhibitors and risk for recurrent Clostridium difficile infection. Arch Internal Med. 2010;170:772–778.CrossRef
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;103:1443–1450.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;103:1443–1450.PubMedCrossRef
8.
go back to reference Berg AM, Kelly CP, Farraye FA. Clostridium difficile infection in the inflammatory bowel disease patient. Inflamm Bowel Dis. 2013;19:194–204.PubMedCrossRef Berg AM, Kelly CP, Farraye FA. Clostridium difficile infection in the inflammatory bowel disease patient. Inflamm Bowel Dis. 2013;19:194–204.PubMedCrossRef
9.
go back to reference Chopra T, Alangaden GJ, Chandrasekar P. Clostridium difficile infection in cancer patients and hematopoietic stem cell transplant recipients. Exp Rev Anti-Infect Therapy. 2010;8:1113–1119.CrossRef Chopra T, Alangaden GJ, Chandrasekar P. Clostridium difficile infection in cancer patients and hematopoietic stem cell transplant recipients. Exp Rev Anti-Infect Therapy. 2010;8:1113–1119.CrossRef
10.
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;105:2040–2049.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;105:2040–2049.PubMedCrossRef
11.
go back to reference Ben-Horin S, Margalit M, Bossuyt P et al. Combination immunomodulator and antibiotic treatment in patients with inflammatory bowel disease and Clostridium difficile infection. Clin Gastroenterol Hepatol Official Clin Pract J Am Gastroenterol Assoc. 2009;7:981–987. Ben-Horin S, Margalit M, Bossuyt P et al. Combination immunomodulator and antibiotic treatment in patients with inflammatory bowel disease and Clostridium difficile infection. Clin Gastroenterol Hepatol Official Clin Pract J Am Gastroenterol Assoc. 2009;7:981–987.
12.
go back to reference Cavagnaro C, Berezin S, Medow MS. Corticosteroid treatment of severe, non-responsive Clostridium difficile induced colitis. Arch Dis Childhood. 2003;88:342–344.CrossRef Cavagnaro C, Berezin S, Medow MS. Corticosteroid treatment of severe, non-responsive Clostridium difficile induced colitis. Arch Dis Childhood. 2003;88:342–344.CrossRef
13.
go back to reference Sailhamer EA, Carson K, Chang Y, et al. Fulminant Clostridium difficile colitis: patterns of care and predictors of mortality. Arch Surg (Chicago, IL: 1960). 2009;144:433–439 Sailhamer EA, Carson K, Chang Y, et al. Fulminant Clostridium difficile colitis: patterns of care and predictors of mortality. Arch Surg (Chicago, IL: 1960). 2009;144:433–439
14.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
15.
go back to reference Yanai H, Nguyen GC, Yun L et al. Practice of gastroenterologists in treating flaring inflammatory bowel disease patients with Clostridium difficile: antibiotics alone or combined antibiotics/immunomodulators? Inflam Bowel Dis. 2011;17:1540–1546.CrossRef Yanai H, Nguyen GC, Yun L et al. Practice of gastroenterologists in treating flaring inflammatory bowel disease patients with Clostridium difficile: antibiotics alone or combined antibiotics/immunomodulators? Inflam Bowel Dis. 2011;17:1540–1546.CrossRef
16.
go back to reference Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.PubMedPubMedCentralCrossRef Moher D, Liberati A, Tetzlaff J, Altman DG, Group P. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6:e1000097.PubMedPubMedCentralCrossRef
17.
go back to reference Kelly CR, Ihunnah C, Fischer M et al. Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol. 2014;109:1065–1071.PubMedPubMedCentralCrossRef Kelly CR, Ihunnah C, Fischer M et al. Fecal microbiota transplant for treatment of Clostridium difficile infection in immunocompromised patients. Am J Gastroenterol. 2014;109:1065–1071.PubMedPubMedCentralCrossRef
18.
go back to reference Ott SJ, Waetzig GH, Rehman A et al. Efficacy of Sterile fecal filtrate transfer for treating patients with Clostridium difficile infection. Gastroenterology. 2017;152:799–811.PubMedCrossRef Ott SJ, Waetzig GH, Rehman A et al. Efficacy of Sterile fecal filtrate transfer for treating patients with Clostridium difficile infection. Gastroenterology. 2017;152:799–811.PubMedCrossRef
19.
go back to reference Webb BJ, Brunner A, Ford CD et al. Fecal microbiota transplantation for recurrent Clostridium difficile infection in hematopoietic stem cell transplant recipients. Transp Infect Dis. 2016;18:628–633.CrossRef Webb BJ, Brunner A, Ford CD et al. Fecal microbiota transplantation for recurrent Clostridium difficile infection in hematopoietic stem cell transplant recipients. Transp Infect Dis. 2016;18:628–633.CrossRef
20.
go back to reference Vermeire S, Joossens M, Verbeke K et al. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J Crohn’s Colitis. 2016;10:387–394.CrossRef Vermeire S, Joossens M, Verbeke K et al. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J Crohn’s Colitis. 2016;10:387–394.CrossRef
22.
go back to reference Paul M, Shani V, Muchtar E et al. Systematic review and meta-analysis of the efficacy of appropriate empiric antibiotic therapy for sepsis. Antimicrob Agents Chemother. 2010;54:4851–4863.PubMedPubMedCentralCrossRef Paul M, Shani V, Muchtar E et al. Systematic review and meta-analysis of the efficacy of appropriate empiric antibiotic therapy for sepsis. Antimicrob Agents Chemother. 2010;54:4851–4863.PubMedPubMedCentralCrossRef
23.
go back to reference Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions. New York: Wiley; 2011. Higgins JP, Green S. Cochrane handbook for systematic reviews of interventions. New York: Wiley; 2011.
24.
go back to reference Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ (Clin Res Ed). 1997;315:629–634.CrossRef Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ (Clin Res Ed). 1997;315:629–634.CrossRef
25.
go back to reference Laza R, Jurac R, Crisan A et al. Clostridium difficile in western Romania: unfavourable outcome predictors in a hospital for infectious diseases. BMC Infect Dis. 2015;15:141.PubMedPubMedCentralCrossRef Laza R, Jurac R, Crisan A et al. Clostridium difficile in western Romania: unfavourable outcome predictors in a hospital for infectious diseases. BMC Infect Dis. 2015;15:141.PubMedPubMedCentralCrossRef
26.
go back to reference Hensgens MP, Dekkers OM, Goorhuis A, LeCessie S, Kuijper EJ. Predicting a complicated course of Clostridium difficile infection at the bedside. Clin Microbiol Infect Official Public Eur Soc Clin Microbiol Infect Dis. 2014;20:O301-308. Hensgens MP, Dekkers OM, Goorhuis A, LeCessie S, Kuijper EJ. Predicting a complicated course of Clostridium difficile infection at the bedside. Clin Microbiol Infect Official Public Eur Soc Clin Microbiol Infect Dis. 2014;20:O301-308.
27.
go back to reference Honda H, Yamazaki A, Sato Y, Dubberke ER. Incidence and mortality associated with Clostridium difficile infection at a Japanese tertiary care center. Anaerobe. 2014;25:5–10.PubMedCrossRef Honda H, Yamazaki A, Sato Y, Dubberke ER. Incidence and mortality associated with Clostridium difficile infection at a Japanese tertiary care center. Anaerobe. 2014;25:5–10.PubMedCrossRef
28.
go back to reference Rodriguez-Pardo D, Almirante B, Bartolome RM et al. Epidemiology of Clostridium difficile infection and risk factors for unfavorable clinical outcomes: results of a hospital-based study in Barcelona, Spain. J Clin Microbiol. 2013;51:1465–1473.PubMedPubMedCentralCrossRef Rodriguez-Pardo D, Almirante B, Bartolome RM et al. Epidemiology of Clostridium difficile infection and risk factors for unfavorable clinical outcomes: results of a hospital-based study in Barcelona, Spain. J Clin Microbiol. 2013;51:1465–1473.PubMedPubMedCentralCrossRef
29.
go back to reference Morrison RH, Hall NS, Said M et al. Risk factors associated with complications and mortality in patients with Clostridium difficile infection. Clin Infect Dis Official Public Infect Dis Soc Am. 2011;53:1173–1178.CrossRef Morrison RH, Hall NS, Said M et al. Risk factors associated with complications and mortality in patients with Clostridium difficile infection. Clin Infect Dis Official Public Infect Dis Soc Am. 2011;53:1173–1178.CrossRef
30.
go back to reference Dudukgian H, Sie E, Gonzalez-Ruiz C, Etzioni DA, Kaiser AMC. difficile colitis: predictors of fatal outcome. J Gastrointest Surg Official J Soc Surg Aliment Tract. 2010;14:315–322.CrossRef Dudukgian H, Sie E, Gonzalez-Ruiz C, Etzioni DA, Kaiser AMC. difficile colitis: predictors of fatal outcome. J Gastrointest Surg Official J Soc Surg Aliment Tract. 2010;14:315–322.CrossRef
31.
go back to reference Hardt C, Berns T, Treder W, Dumoulin FL. Univariate and multivariate analysis of risk factors for severe Clostridium difficile-associated diarrhoea: importance of co-morbidity and serum C-reactive protein. World J Gastroenterol. 2008;14:4338–4341.PubMedPubMedCentralCrossRef Hardt C, Berns T, Treder W, Dumoulin FL. Univariate and multivariate analysis of risk factors for severe Clostridium difficile-associated diarrhoea: importance of co-morbidity and serum C-reactive protein. World J Gastroenterol. 2008;14:4338–4341.PubMedPubMedCentralCrossRef
32.
go back to reference Greenstein AJ, Byrn JC, Zhang LP et al. Risk factors for the development of fulminant Clostridium difficile colitis. Surgery. 2008;143:623–629.PubMedCrossRef Greenstein AJ, Byrn JC, Zhang LP et al. Risk factors for the development of fulminant Clostridium difficile colitis. Surgery. 2008;143:623–629.PubMedCrossRef
33.
go back to reference Rubin MS, Bodenstein LE, Kent KC. Severe Clostridium difficile colitis. Dis Colon Rectum. 1995;38:350–354.PubMedCrossRef Rubin MS, Bodenstein LE, Kent KC. Severe Clostridium difficile colitis. Dis Colon Rectum. 1995;38:350–354.PubMedCrossRef
34.
go back to reference Bielakova K, Fernandova E, Matejovska-Kubesova H et al. Can we improve the therapy of Clostridium difficile infection in elderly patients? Wiener Klinische Wochenschrift. 2016;128:592–598.PubMedCrossRef Bielakova K, Fernandova E, Matejovska-Kubesova H et al. Can we improve the therapy of Clostridium difficile infection in elderly patients? Wiener Klinische Wochenschrift. 2016;128:592–598.PubMedCrossRef
35.
go back to reference Berdichevski T, Keller N, Rahav G et al. The impact of pseudomembrane formation on the outcome of Clostridium difficile-associated disease. Infection. 2013;41:969–977.PubMedCrossRef Berdichevski T, Keller N, Rahav G et al. The impact of pseudomembrane formation on the outcome of Clostridium difficile-associated disease. Infection. 2013;41:969–977.PubMedCrossRef
36.
go back to reference Alavi K, Servin JAC, Sturrock P et al. Predicting post-operative mortality for Clostridium difficile-associated colitis. Gastroenterology. 2010;138:S884.CrossRef Alavi K, Servin JAC, Sturrock P et al. Predicting post-operative mortality for Clostridium difficile-associated colitis. Gastroenterology. 2010;138:S884.CrossRef
37.
go back to reference Dejan M, Paul C, Shail G et al. Initial treatment decisions and outcomes in patients with inflammatory bowel disease and Clostridium difficile infection. Inflam Bowel Dis. 2014;20:S47.CrossRef Dejan M, Paul C, Shail G et al. Initial treatment decisions and outcomes in patients with inflammatory bowel disease and Clostridium difficile infection. Inflam Bowel Dis. 2014;20:S47.CrossRef
38.
go back to reference Yang Y, Liu HH, Poore A et al. Glucocorticoid use within 3 months may be associated with a lower bowel perforation rate in patients hospitalized with Clostridium difficile infection (CDI). Gastroenterology. 2016;150:S747.CrossRef Yang Y, Liu HH, Poore A et al. Glucocorticoid use within 3 months may be associated with a lower bowel perforation rate in patients hospitalized with Clostridium difficile infection (CDI). Gastroenterology. 2016;150:S747.CrossRef
39.
go back to reference Archbald-Pannone L, Pinkerton R, Guerrant R. Predicting mortality following Clostridium difficile infection. J Am Geriat Soc. 2012;60:S120. Archbald-Pannone L, Pinkerton R, Guerrant R. Predicting mortality following Clostridium difficile infection. J Am Geriat Soc. 2012;60:S120.
40.
go back to reference Ananthakrishnan AN, Guzman-Perez R, Gainer V et al. Predictors of severe outcomes associated with Clostridium difficile infection in patients with inflammatory bowel disease. Aliment Pharmacol Therap. 2012;35:789–795.CrossRef Ananthakrishnan AN, Guzman-Perez R, Gainer V et al. Predictors of severe outcomes associated with Clostridium difficile infection in patients with inflammatory bowel disease. Aliment Pharmacol Therap. 2012;35:789–795.CrossRef
41.
go back to reference Kenneally C, Rosini JM, Skrupky LP et al. Analysis of 30-day mortality for Clostridium difficile-associated disease in the ICU setting. Chest. 2007;132:418–424.PubMedCrossRef Kenneally C, Rosini JM, Skrupky LP et al. Analysis of 30-day mortality for Clostridium difficile-associated disease in the ICU setting. Chest. 2007;132:418–424.PubMedCrossRef
42.
go back to reference Avni T, Babitch T, Ben-Zvi H et al. Clostridioides difficile infection in immunocompromised hospitalized patients is associated with a high recurrence rate. Int J Infect Dis IJID Official Public Int Soc Infect Dis. 2020;90:237–242. Avni T, Babitch T, Ben-Zvi H et al. Clostridioides difficile infection in immunocompromised hospitalized patients is associated with a high recurrence rate. Int J Infect Dis IJID Official Public Int Soc Infect Dis. 2020;90:237–242.
43.
go back to reference Lei JH, Liu LR, Wei Q et al. Systematic review and meta-analysis of the survival outcomes of first-line treatment options in high-risk prostate cancer. Sci Rep. 2015;5:7713.PubMedPubMedCentralCrossRef Lei JH, Liu LR, Wei Q et al. Systematic review and meta-analysis of the survival outcomes of first-line treatment options in high-risk prostate cancer. Sci Rep. 2015;5:7713.PubMedPubMedCentralCrossRef
44.
go back to reference Dallal RM, Harbrecht BG, Boujoukas AJ et al. Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg. 2002;235:363–372.PubMedPubMedCentralCrossRef Dallal RM, Harbrecht BG, Boujoukas AJ et al. Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg. 2002;235:363–372.PubMedPubMedCentralCrossRef
45.
go back to reference Bignardi GE. Risk factors for Clostridium difficile infection. J Hospital Infect. 1998;40:1–15.CrossRef Bignardi GE. Risk factors for Clostridium difficile infection. J Hospital Infect. 1998;40:1–15.CrossRef
46.
go back to reference 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;342:390–397.PubMedCrossRef 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;342:390–397.PubMedCrossRef
47.
go back to reference Kelly CP. Immune response to Clostridium difficile infection. Eur J Gastroenterol Hepatol. 1996;8:1048–1053.PubMedCrossRef Kelly CP. Immune response to Clostridium difficile infection. Eur J Gastroenterol Hepatol. 1996;8:1048–1053.PubMedCrossRef
48.
49.
go back to reference Kim HB, Wang Y, Sun X. A detrimental role of immunosuppressive drug, dexamethasone, during Clostridium difficile infection in association with a gastrointestinal microbial shift. J Microbiol Biotechnol. 2016;26:567–571.PubMedPubMedCentralCrossRef Kim HB, Wang Y, Sun X. A detrimental role of immunosuppressive drug, dexamethasone, during Clostridium difficile infection in association with a gastrointestinal microbial shift. J Microbiol Biotechnol. 2016;26:567–571.PubMedPubMedCentralCrossRef
50.
go back to reference Tourret J, Willing BP, Dion S et al. Immunosuppressive treatment alters secretion of ileal antimicrobial peptides and gut microbiota, and favors subsequent colonization by uropathogenic Escherichia coli. Transplantation. 2017;101:74–82.PubMedCrossRef Tourret J, Willing BP, Dion S et al. Immunosuppressive treatment alters secretion of ileal antimicrobial peptides and gut microbiota, and favors subsequent colonization by uropathogenic Escherichia coli. Transplantation. 2017;101:74–82.PubMedCrossRef
51.
go back to reference Flannigan KL, Rajbar T, Moffat A et al. Changes in composition of the gut bacterial microbiome after fecal microbiota transplantation for recurrent Clostridium difficile infection in a pediatric heart transplant patient. Front Cardiovasc Med. 2017;4:17.PubMedPubMedCentralCrossRef Flannigan KL, Rajbar T, Moffat A et al. Changes in composition of the gut bacterial microbiome after fecal microbiota transplantation for recurrent Clostridium difficile infection in a pediatric heart transplant patient. Front Cardiovasc Med. 2017;4:17.PubMedPubMedCentralCrossRef
52.
53.
go back to reference Stuck AE, Minder CE, Frey FJ. Risk of infectious complications in patients taking glucocorticosteroids. Rev Infect Dis. 1989;11:954–963.PubMedCrossRef Stuck AE, Minder CE, Frey FJ. Risk of infectious complications in patients taking glucocorticosteroids. Rev Infect Dis. 1989;11:954–963.PubMedCrossRef
54.
go back to reference Schneeweiss S, Korzenik J, Solomon DH et al. Infliximab and other immunomodulating drugs in patients with inflammatory bowel disease and the risk of serious bacterial infections. Aliment Pharmacol Therap. 2009;30:253–264.CrossRef Schneeweiss S, Korzenik J, Solomon DH et al. Infliximab and other immunomodulating drugs in patients with inflammatory bowel disease and the risk of serious bacterial infections. Aliment Pharmacol Therap. 2009;30:253–264.CrossRef
55.
go back to reference Tang YM, Stone CD. Clostridium difficile infection in inflammatory bowel disease: challenges in diagnosis and treatment. Clin J Gastroenterol. 2017;10:112–123.PubMedCrossRef Tang YM, Stone CD. Clostridium difficile infection in inflammatory bowel disease: challenges in diagnosis and treatment. Clin J Gastroenterol. 2017;10:112–123.PubMedCrossRef
56.
go back to reference Binion DG. Clostridium difficile infection in patients with inflammatory bowel disease. Gastroenterol Hepatol (N Y). 2012;8:615–617. Binion DG. Clostridium difficile infection in patients with inflammatory bowel disease. Gastroenterol Hepatol (N Y). 2012;8:615–617.
57.
go back to reference Ananthakrishnan AN, McGinley EL, Binion DG, Saeian K. A nationwide analysis of changes in severity and outcomes of inflammatory bowel disease hospitalizations. J Gastrointest Surg Official J Soc Surg Aliment Tract. 2011;15:267–276.CrossRef Ananthakrishnan AN, McGinley EL, Binion DG, Saeian K. A nationwide analysis of changes in severity and outcomes of inflammatory bowel disease hospitalizations. J Gastrointest Surg Official J Soc Surg Aliment Tract. 2011;15:267–276.CrossRef
58.
go back to reference Ananthakrishnan AN, McGinley EL, Saeian K, Binion DG. Temporal trends in disease outcomes related to Clostridium difficile infection in patients with inflammatory bowel disease. Inflam Bowel Dis. 2011;17:976–983.CrossRef Ananthakrishnan AN, McGinley EL, Saeian K, Binion DG. Temporal trends in disease outcomes related to Clostridium difficile infection in patients with inflammatory bowel disease. Inflam Bowel Dis. 2011;17:976–983.CrossRef
59.
go back to reference Jen MH, Saxena S, Bottle A, Aylin P, Pollok RC. Increased health burden associated with Clostridium difficile diarrhoea in patients with inflammatory bowel disease. Aliment Pharmacol Therap. 2011;33:1322–1331.CrossRef Jen MH, Saxena S, Bottle A, Aylin P, Pollok RC. Increased health burden associated with Clostridium difficile diarrhoea in patients with inflammatory bowel disease. Aliment Pharmacol Therap. 2011;33:1322–1331.CrossRef
60.
go back to reference Kassam Z, Lee CH, Yuan Y, Hunt RH. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013;108:500–508.PubMedCrossRef Kassam Z, Lee CH, Yuan Y, Hunt RH. Fecal microbiota transplantation for Clostridium difficile infection: systematic review and meta-analysis. Am J Gastroenterol. 2013;108:500–508.PubMedCrossRef
61.
go back to reference Li YT, Cai HF, Wang ZH, Xu J, Fang JY. Systematic review with meta-analysis: long-term outcomes of faecal microbiota transplantation for Clostridium difficile infection. Aliment Pharmacol Therap. 2016;43:445–457.CrossRef Li YT, Cai HF, Wang ZH, Xu J, Fang JY. Systematic review with meta-analysis: long-term outcomes of faecal microbiota transplantation for Clostridium difficile infection. Aliment Pharmacol Therap. 2016;43:445–457.CrossRef
62.
go back to reference Quraishi MN, Widlak M, Bhala N et al. Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment Pharmacol Therap. 2017;46:479–493.CrossRef Quraishi MN, Widlak M, Bhala N et al. Systematic review with meta-analysis: the efficacy of faecal microbiota transplantation for the treatment of recurrent and refractory Clostridium difficile infection. Aliment Pharmacol Therap. 2017;46:479–493.CrossRef
64.
go back to reference Dubberke ER, Burdette SD, Practice ASTIDCo. Clostridium difficile infections in solid organ transplantation. Am J Transp Official J Am Soc Transp Am Soc Transp Surg. 2013;13:42–49. Dubberke ER, Burdette SD, Practice ASTIDCo. Clostridium difficile infections in solid organ transplantation. Am J Transp Official J Am Soc Transp Am Soc Transp Surg. 2013;13:42–49.
65.
go back to reference Bakken JS, Borody T, Brandt LJ et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol Official Clin Pract J Am Gastroenterol Assoc. 2011;9:1044–1049. Bakken JS, Borody T, Brandt LJ et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol Official Clin Pract J Am Gastroenterol Assoc. 2011;9:1044–1049.
66.
go back to reference Dubberke ER, Gerding DN, Classen D et al. Strategies to prevent Clostridium difficile infections in acute care hospitals. Infect Control Hosp Epidemiol. 2008;29:S81-92.PubMedCrossRef Dubberke ER, Gerding DN, Classen D et al. Strategies to prevent Clostridium difficile infections in acute care hospitals. Infect Control Hosp Epidemiol. 2008;29:S81-92.PubMedCrossRef
67.
go back to reference Ray AJ, Deshpande A, Fertelli D et al. A multicenter randomized trial to determine the effect of an environmental disinfection intervention on the incidence of healthcare-associated Clostridium difficile infection. Infect Control Hosp Epidemiol. 2017;38:777–783.PubMedCrossRef Ray AJ, Deshpande A, Fertelli D et al. A multicenter randomized trial to determine the effect of an environmental disinfection intervention on the incidence of healthcare-associated Clostridium difficile infection. Infect Control Hosp Epidemiol. 2017;38:777–783.PubMedCrossRef
68.
go back to reference 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.PubMedCrossRef 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.PubMedCrossRef
69.
go back to reference Pear SM, Williamson TH, Bettin KM, Gerding DN, Galgiani JN. Decrease in nosocomial Clostridium difficile-associated diarrhea by restricting clindamycin use. Ann Internal Med. 1994;120:272–277.CrossRef Pear SM, Williamson TH, Bettin KM, Gerding DN, Galgiani JN. Decrease in nosocomial Clostridium difficile-associated diarrhea by restricting clindamycin use. Ann Internal Med. 1994;120:272–277.CrossRef
70.
go back to reference Shen NT, Maw A, Tmanova LL et al. Timely use of probiotics in hospitalized adults prevents Clostridium difficile infection: a systematic review with meta-regression analysis. Gastroenterology. 2017;152:1889–1900.PubMedCrossRef Shen NT, Maw A, Tmanova LL et al. Timely use of probiotics in hospitalized adults prevents Clostridium difficile infection: a systematic review with meta-regression analysis. Gastroenterology. 2017;152:1889–1900.PubMedCrossRef
Metadata
Title
Association Between Immunosuppressive Therapy and Outcome of Clostridioides difficile Infection: Systematic Review and Meta-Analysis
Authors
Yiting Li
Haifeng Cai
Daniel A. Sussman
Jean Donet
Kevin Dholaria
Jiajia Yang
Ami Panara
Ryan Croteau
Jamie S. Barkin
Publication date
23-09-2021
Publisher
Springer US
Published in
Digestive Diseases and Sciences / Issue 8/2022
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-021-07229-2

Other articles of this Issue 8/2022

Digestive Diseases and Sciences 8/2022 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.