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.