Impact of Clostridium difficile infection on inflammatory bowel disease outcome: A review

Table 1 Main short-term outcomes in inflammatory bowel disease patients with Clostridium difficile infection as compared to those with inflammatory bowel disease alone or Clostridium difficile infection alone

Ref.	Journal and year of publication	Study design and time frame	Outcome
Murthy et al[21] Canada	Aliment Pharmacol Ther 2012	In-patients, Ontario, Canada, 2002-2008	Increased LOS (11 d vs 6 d, P = 0.0001), similar rate of colectomy (12% vs 9.8%; P = 0.30), and higher mortality rate (3.3% vs 0.38%, P < 0.0001) as compared with UC patients without CDI
Navaneethan et al[24] United States	J Crohns Colitis 2012	Out-/in-patients; 2002-2007	No significant difference in the colectomy risk within 3 months of index admission between UC patients with CDI and those with UC alone
Ananthakrishnan et al[28] United States	Aliment Pharmacol Ther 2012	In-patients; 1998-2010	4.4% colectomy and 15.2% mortality rates
Jen et al[17] United Kingdom	Aliment Pharmacol Ther 2011	Case-control analysis of United Kingdom Hospital Episodes Statistics, out-/in-patients; 2002-2007	Increased mortality (OR = 6.32), higher risk for surgery (OR = 1.87), and 27.9 d longer LOS than patients with IBD alone
Ananthakrishnan et al[18] United States	Inflamm Bowel Dis 2011	Case-control analysis of NIS database, out-/in-patients; 1998, 2004, 2007	Increase in colectomy rate from 1998 (OR = 1.39, 95%CI: 0.81-2.37) to 2007 (OR = 2.51, 95%CI: 1.90-3.34) (P = 0.03), and in mortality risk (1998: OR = 2.38, 95%CI: 1.52-3.72) (2007, OR = 3.38, 95%CI: 2.66-4.29) (P = 0.15)
Kaneko et al[25] Japan	Clin Res Hepatol Gastroenterol 2011	Out-/in-patients; 2006-2009	No association between CDI and colectomy rate in UC patients
Kariv et al[20] United States	J Crohns Colitis 2011	Out-/in- patients with UC; 2000-2006	No difference in colectomy rates (48% vs 50.9%, P = 0.81) between infected and non-infected UC patients, no mortality in UC patients with or without CDI
Jodorkovsky et al[19] United States	Dig Dis Sci 2010	In-patients; 2004/06-2005/06	Similar mean LOS for IBD patients with CDI and those without CDI (11.7 d vs 11.0 d; P = 0.70); similar use of cyclosporine therapy (48% vs 47%); higher emergent colectomy rate (23% vs 13.4%, P = 0.17)
Bossuyt et al[14] Belgium	J Crohns Colitis 2009	In-patients; 2000-2008	LOS shorter as compared to non-IBD patients (15.2 d vs 27.7 d, P = 0.001); one patient with UC+ CDI had a semi-urgent colectomy; no mortality in IBD patients, 2 deaths in non-IBD patients
Ricciardi et al[15] United States	Dis Colon Rectum 2009	Case-control analysis of NIS database, out-/in-patients; 1993-2003	Increased case fatality in UC+CDI patients but not in those with CD+CDI; operative mortality for UC+CDI patients reached 25.7%
Ben-Horin et al[26] Israel and some European countries	Clin Gastroenterol Hepatol 2009	Multi-center, in-patients; 2000-2008	Low colectomy rate (6%) in IBD patients with CDI
Ananthakrishnan et al[13] United States	Gut 2008	Case-control analysis of NIS database, out-/in-patients; 2003	Four-fold higher mortality rate (OR = 4.7, 95%CI: 2.9-7.9) compared with IBD alone and twice higher than in those with CDI alone (OR = 2.21, 95%CI: 1.4-3.4); 3-d longer compared with IBD alone; six-fold greater risk of bowel surgery than those with CDI alone (OR = 6.6, 95%CI: 4.7-9.3); 11406 higher hospital adjusted charges
Nguyen et al[16] United States	Am J Gastroenterol 2008	Case-control analysis of NIS database, out-/in-patients; 1998-2004	Increased mortality in UC (OR = 3.79, 95%CI: 2.84-5.06) but not in CD patients (OR = 1.66, 95%CI: 0.75-3.66); increased LOS with 65% for CD and 46% for UC, and increased hospital charges compared with non-IBD patients
Rodemann et al[12] United States	Clin Gastroenterol Hepatol 2007	In-patients, 1998-2004	LOS similar to non-IBD patients
Issa et al[11] United States	Clin Gastroenterol Hepatol 2007	Observational study, out-/in-patients; 2004-2005	Increased LOS (13 d vs 6 d); the colectomy rate in UC+CDI decreased from 45% in 2004 to 25% in 2005

C. difficile: Clostridium difficile; CDI: Clostridium difficile infection; CD: Crohn's disease; IBD: Inflammatory bowel disease; LOS: Length of hospital stay; NIS: National Inpatient Sample; OR: Odds ratio; UC: Ulcerative colitis.

Table 2 Long-term outcomes in inflammatory bowel disease patients with Clostridium difficile infection compared to those with inflammatory bowel disease alone

Ref.	Journal and year of publication	Study design and time frame	Outcome
Murthy et al[21] Canada	Aliment Pharmacol Ther 2012	In-patients; 2002-2008	UC patients with CDI was associated with increased adjusted 5-yr risk of mortality, but not of colectomy, as compared with UC without CDI
Navaneethan et al[24] United States	J Crohns Colitis 2012	Out-/in-patients; 2002-2007	One year following CDI: increased rates of ERV (37.8% vs 4%, P = 0.001) and colectomy (35.6% vs 9.9%, P = 0.001); escalation in medical therapy in 58.8% as compared to the prior year (12.9%) (P = 0.0001)
Jodorkovsky et al[19] United States	Dig Dis Sci 2010	In-patients; 2004-2005	One year following CDI: UC patients with CDI had increased rate of ERV (8 vs 1, P = 0.012), higher number of UC– related hospitalizations (58 vs 27, P = 0.001), and two-fold higher rates of colectomy (44.6% vs 25%, P = 0.04) compared to UC alone
Chiplunker et al[27] United States	Gastroenterology 2009	Case-control, in-patients; 2005-2006	One year following CDI: over half required an escalation in their IBD medical therapy, 46% had more hospitalisations, colectomy occured in 10.3% , and no mortality

CDI: Clostridium difficile infection; ERV: Emergency room visits; IBD: Inflammatory bowel disease; OR: Odds ratio; UC: Ulcerative colitis.