Management of inflammatory bowel disease with Clostridium difficile infection

Table 1 Epidemiology of Clostridium difficile infection in inflammatory bowel disease

Ref.	Patient population	Sampling time frame	Diagnosis method	Disease activity	Conclusions
Keighley[92] (1983)	IBD adult inpatients	1978-1980	Stool culture on selective medium + cytotoxicity assay	Active	CDI incidence (%) IBD: 5.7; UC 4.7; CD 6.3
Gurian et al[93] (1983)	IBD adult inpatients and outpatients	1980-1981	Stool culture on selective medium + cytotoxicity assay	Active	CDI incidence (%) IBD: 0
Rolny et al[26] (1983)	IBD adult inpatients	1980-1981	Stool culture on selective medium + cytotoxicity assay	Active	CDI incidence (%) UC: 5; CD: 7.7
Greenfield et al[21] (1983)	IBD adult inpatients and outpatients	1980-1981	Stool culture on selective medium + cytotoxicity assay	Mixed	CDI incidence (%) UC: 13.7; CD: 13.2
Burke et al[94] (1987)	IBD adult outpatients	1984-1986	Stool culture on selective medium + cytotoxicity assay	Active	CDI incidence (%) IBD 3.2
Gryboski[95] (1991)	IBD pediatric inpatients and outpatients	1986-1990	Stool culture on selective medium + cytotoxicity assay	Active	CDI incidence (%) IBD 16; UC: 18; CD 14
Meyer et al[22] (2004)	IBD adult inpatients and outpatients	2000-2001	Immunoassay for Toxin A until 2001 then EIA for Toxin A/B	Active	CDI incidence (%) IBD: 16.7; UC: 12.5; CD: 23.8; IC: 11.1
Mylonaki et al[23] (2004)	IBD adult inpatients and outpatients	1997-2001	ELISA for Toxins A/B	Active	CDI incidence (%) IBD: 5.5; CD: 13.2
Issa et al[24] (2007)	IBD adult inpatients and outpatients	2005	ELISA for Toxins A/B	Active	CDI incidence (%) UC: 6.1; CD: 4.1
					IBD patients accounted for 4% of the total CDI patient cohort in 2003, 7% in 2004, and 16% in 2005
Rodemann et al[16] (2007)	IBD pediatric and adult inpatients (United States)	1998-2004	Cell cytotoxic culture	Active	CDI incidence (%) UC: 3.9; CD: 1.6
			2002 onwards C. difficile Toxin A/B immunoassay		CDI incidence increase: UC > CD > non-IBD
					Non-IBD population: 8.5 to 15.9/1000 admissions
					CD: 9.5 to 22.3/1000 admissions
					UC: 18.4 to 57.6/1000 admissions
Shen et al[33] (2008)	UC adult outpatients with IPAA	2005-2006	ELISA for Toxin A/B	Mixed	CDI incidence (%) UC: 18.3
Bossuyt et al[20] (2009)	IBD and non-IBD CDI adult inpatients	2000-2008	EIA for Toxin A until 2005, then EIA for Toxins A/B	Active	All patients: 3.75-fold increase in CDI between 2000-2003 and 2004-2008
Balamurugan et al[96] (2008)	UC adult outpatients	2004-2005	PCR for C. difficile	Mixed	CDI incidence (%) UC: 92
			Toxin A/B ELISA
Ananthakrishnan et al[18] (2008)	IBD and non-IBD CDI adult inpatients	1998-2004	N/R	N/R	CDI incidence increase: UC: 24 to 39/1000 discharge ; CD: 8 to 12/1000 discharges
Nguyen et al[17] (2008)	IBD and non-IBD adult inpatients	1998-2004	N/R	N/R	CDI incidence increase: UC: 26.6 to 51.2/1000 discharges
Pascarella et al[35] (2009)	IBD pediatric inpatients	2005-2007	Enzyme immunoassay for toxins A/B	Mixed	CDI incidence (%) UC: 21.3; CD: 35
Ricciardi et al[27] (2009)	IBD adult inpatients	1993-2003	N/R	Active	CDI incidence (%) UC: 2.8; CD: 1.0
					CDI incidence increase: IBD: 12.2 to 21/1000 discharges; CD + colonic involvement: 12.2 to 23.1/1000 discharges
Wultańska et al[36] (2010)	IBD pediatric outpatients	2005-2007	EIA for Toxins A/B	Mixed	CDI incidence (%) IBD: 60; UC: 61; CD: 59
			or PCR
Ananthakrishnan et al[58] (2011)	IBD adult inpatients	1998, 2004, 2007	N/R	N/R	CDI incidence increase: CD: 0.8 to 1.5% of hospitalizations; UC: 2.4 to 5.3% of hospitalizations
					Absolute mortality increase in CDI + IBD (5.9% to 7.2%)
Kaneko et al[46] (2011)	UC pediatric and adult inpatients and outpatients	2006-2009	ELISA for Toxin A	Active	CDI incidence (%) UC inpatient: 36.6; UC outpatient: 41.7
Mezoff et al[37] (2011)	IBD pediatric patients	2007-2008	EIA for Toxins A and B	Mixed	CDI incidence (%) UC: 5.8; CD: 7.8; IC: 11.1
Ott et al[28] (2011)	IBD adult inpatients	2001-2008	ELISA for Toxins A/B or characteristic histology	Active	CDI incidence (%) IBD: 4.0; CD: 13.2; UC: 4.7
Banaszkiewicz et al[38] (2012)	IBD pediatric inpatients	2007-2010	EIA for Toxins A and B	Mixed	CDI incidence (%) IBD: 47
Antonelli et al[29] (2012)	IBD adult inpatients	2007-2010	N/R	Active	CDI incidence (%) UC: 11.1; CD: 1.7
Murthy et al[31] (2012)	UC adult inpatients	2002-2008	N/R	Active	CDI incidence (%) UC: 9.0
Lamousé-Smith et al[97] (2013)	IBD pediatric inpatients and outpatients (United States)	2006-2012	PCR for Toxin B +/- ELISA for Toxin A/B	Mixed	CDI incidence (%) UC: 18.4; CD: 11.6
Masclee et al[47] (2013)	IBD adult outpatients	2009-2010	PCR for C. difficile and Toxin A/B	Active	CDI incidence (%) IBD: 4.9; UC: 3.4; CD: 5.9
Mir et al[39] (2013)	IBD pediatric patients	2010-2012	EIA or PCR for Toxin A/B	N/R	CDI incidence (%) IBD: 8.1; UC: 5.6; CD: 9.3 ; IBDU: 11.1
					No significant variation in IBD incidence over 3 yr
Pant et al[98] (2013)	IBD pediatric inpatients	2000, 2003, 2006, 2009	N/R	N/R	CDI incidence increase: IBD: 21.7 to 28 cases/1000 IBD cases per year; UC: 28.1 to 42.2/1000 cases per year; CD: 18.3 to 20.3/1000 cases per year
Li et al[34] (2013)	IBD adult outpatients with IPAA	2010-2011	PCR for Toxin B gene	Active	CDI incidence (%) IBD: 10.7; UC: 10.4; CD: 0; IC: 25.0
Martinelli et al[40] (2014)	IBD pediatric inpatients and outpatients	2010-2011	EIA for Toxins A/B	Mixed	CDI incidence (%): IBD: 10.0; UC: 7.5; CD: 11.9
Regnault et al[30] (2014)	IBD adult inpatients	2008-2010	Stool culture on selective medium + cytotoxicity assay +/- toxigenic culture	Active	CDI incidence (% hospitalizations): IBD: 7.0; UC: 6.8; CD: 7.2
Negrón et al[32] (2014)	UC adult inpatients	2000-2009	EIA for Toxins A/B	Active	CDI incidence (%) UC: 6.1
Hourigan et al[99] (2014)	IBD and non-IBD pediatric and adult inpatients	1993-2012	N/R	N/R	CDI incidence increase: IBD: 19.9 to 67/1000 admissions
					Rate of increase in CDI not significantly different between patients with or without IBD
Krishnarao et al[25] (2015)	IBD adult inpatients and outpatients	2008-2011	EIA and PCR	Mixed	CDI incidence (%) IBD: 5.1
Sandberg et al[19] (2015)	IBD pediatric inpatients	1997-2011	N/R	N/R	Hospitalization rate increase: CDI + IBD: 2.8 to 14.4 per million population per year
					Rate of increase for UC + CDI = CD + CDI
Simian et al[100] (2016)	IBD adult and pediatric inpatients and outpatients	2014-2015	PCR	N/R	CDI incidence (%) UC: 5.0; CD: 5.0
Roy et al[101] (2016)	CD adult outpatients on chronic antibiotic therapy > 6 mo	1992-2015	N/R	N/R	CDI incidence (%) CD: 2.0

IBD: Inflammatory bowel disease; UC: Ulcerative colitis; CD: Crohn’s Disease; IC: Indeterminate colitis; IBDU: Inflammatory bowel disease unclassified; IPAA: Ileal anal-pouch anastomosis; EIA: Enzyme immunoassay; ELISA: Enzyme linked immunosorbent assay; PCR: Polymerase chain reaction ; N/R: Not reported.