Skip to main content
Top
Published in: International Journal of Colorectal Disease 3/2020

01-03-2020 | Chronic Inflammatory Bowel Disease | Original Article

Clinical assessment of risk factors for infection in inflammatory bowel disease patients

Authors: Joan Tosca, Natalia Garcia, Isabel Pascual, Marta Maia Bosca-Watts, Rosario Anton, Ana Sanahuja, Pilar Mas, Francisco Mora, Miguel Minguez

Published in: International Journal of Colorectal Disease | Issue 3/2020

Login to get access

Abstract

Purpose

Recognizing patients with inflammatory bowel disease who are prone to infection would enable the adjustment of the type and intensity of immunosuppressive treatment. The aim of this study was to identify a clinical profile of risk for infections in IBD patients, based on the interaction of immunosuppressive treatment with factors inherent to the patient.

Methods

A case-control study was performed among patients older than 18 years. Patients with any significant infection (any kind of severe or recurrent infection according to standard clinical criteria or a critical enough infection according to the patient) were defined as cases. Both cases and controls were randomly selected in a 1:3 ratio. All the period from diagnosis to the end of recruitment (June 2016) was analyzed. Risk factors for infection were identified by logistic regression analysis; the strength of association was reported by odds ratio (OR) with 95% confidence interval (95%CI).

Results

A total of 112 cases and 270 controls were included. The independent risk factors for significant infection are the number of immunosuppressants (one drug: OR 1.28, 95% CI 0.53–3.11, two drugs: OR 2.37, 95% CI 1.01–5,56, and three drugs: OR 5.84, 95% CI 1.57–21.72), body mass index (OR 1.08; 95 %CI 1,01–1,16), the degree of comorbidity (OR 1.52; 95% CI 1.04–2.21), and the intensity of inflammatory activity (OR 1.43; 95% CI 1.19–1.71).

Conclusions

Regardless of immunosuppression, several patient factors such as comorbidity, body mass index, or the inflammatory activity of the disease determine the individual risk of infectious complications and should be considered for an adequate risk assessment.
Appendix
Available only for authorised users
Literature
1.
go back to reference Rahier JF, Magro F, Abreu C, Armuzzi A, Ben-Horin S, Chowers Y, Cottone M, de Ridder L, Doherty G, Ehehalt R, Esteve M, Katsanos K, Lees CW, Macmahon E, Moreels T, Reinisch W, Tilg H, Tremblay L, Veereman-Wauters G, Viget N, Yazdanpanah Y, Eliakim R, Colombel JF, European Crohn's and Colitis Organisation (ECCO) (2014) European Crohn’s and Colitis Organisation (ECCO). Second European evidence-based consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohns Colitis 8:443–468CrossRef Rahier JF, Magro F, Abreu C, Armuzzi A, Ben-Horin S, Chowers Y, Cottone M, de Ridder L, Doherty G, Ehehalt R, Esteve M, Katsanos K, Lees CW, Macmahon E, Moreels T, Reinisch W, Tilg H, Tremblay L, Veereman-Wauters G, Viget N, Yazdanpanah Y, Eliakim R, Colombel JF, European Crohn's and Colitis Organisation (ECCO) (2014) European Crohn’s and Colitis Organisation (ECCO). Second European evidence-based consensus on the prevention, diagnosis and management of opportunistic infections in inflammatory bowel disease. J Crohns Colitis 8:443–468CrossRef
2.
go back to reference Toruner M, Loftus EV Jr, Harmsen WS et al (2008) Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology 134:929–936CrossRef Toruner M, Loftus EV Jr, Harmsen WS et al (2008) Risk factors for opportunistic infections in patients with inflammatory bowel disease. Gastroenterology 134:929–936CrossRef
3.
go back to reference Stuck AE, Minder CE, Frey FJ (1989) Risk of infectious complications in patients taking glucocorticosteroids. Rev Infect Dis 11(6):954–963CrossRef Stuck AE, Minder CE, Frey FJ (1989) Risk of infectious complications in patients taking glucocorticosteroids. Rev Infect Dis 11(6):954–963CrossRef
4.
go back to reference Lichtenstein GR, Feagan BG, Cohen RD et al (2006) Serious infections and mortality in association with therapies for Crohn’s disease: TREAT registry. Clin Gastroenterol Hepatol 4:621–630 Erratum in: Clin Gastroenterol Hepatol 2006;4:931CrossRef Lichtenstein GR, Feagan BG, Cohen RD et al (2006) Serious infections and mortality in association with therapies for Crohn’s disease: TREAT registry. Clin Gastroenterol Hepatol 4:621–630 Erratum in: Clin Gastroenterol Hepatol 2006;4:931CrossRef
5.
go back to reference Peyrin-Biroulet L, Deltenre P, de Suray N, Branche J, Sandborn WJ, Colombel JF (2008) Efficacy and safety of tumor necrosis factor antagonists in Crohn’s disease: meta-analysis of placebo-controlled trials. Clin Gastroenterol Hepatol 6:644–653CrossRef Peyrin-Biroulet L, Deltenre P, de Suray N, Branche J, Sandborn WJ, Colombel JF (2008) Efficacy and safety of tumor necrosis factor antagonists in Crohn’s disease: meta-analysis of placebo-controlled trials. Clin Gastroenterol Hepatol 6:644–653CrossRef
6.
go back to reference Lichtenstein GR, Cohen RD, Feagan BG et al (2008) Safety of infliximab and other Crohn’s disease therapies; TREAT™ registry data with 24,575 patient-years of follow-up. Am J Gatroenterol 103:S–436 Lichtenstein GR, Cohen RD, Feagan BG et al (2008) Safety of infliximab and other Crohn’s disease therapies; TREAT™ registry data with 24,575 patient-years of follow-up. Am J Gatroenterol 103:S–436
7.
go back to reference Lichtenstein GR, Feagan BG, Cohen RD, Salzberg BA, Diamond RH, Price S, Langholff W, Londhe A, Sandborn WJ (2012) Serious infection and mortality in patients with Crohn’s disease: more than 5 years of follow-up in the TREAT™ registry. Am J Gastroenterol 107:1409–1422CrossRef Lichtenstein GR, Feagan BG, Cohen RD, Salzberg BA, Diamond RH, Price S, Langholff W, Londhe A, Sandborn WJ (2012) Serious infection and mortality in patients with Crohn’s disease: more than 5 years of follow-up in the TREAT™ registry. Am J Gastroenterol 107:1409–1422CrossRef
8.
go back to reference Fidder H, Schnitzler F, Ferrante M, Noman M, Katsanos K, Segaert S, Henckaerts L, van Assche G, Vermeire S, Rutgeerts P (2009) Long-term safety of infliximab for the treatment of inflammatory bowel disease: a single-centre cohort study. Gut 58:501–508CrossRef Fidder H, Schnitzler F, Ferrante M, Noman M, Katsanos K, Segaert S, Henckaerts L, van Assche G, Vermeire S, Rutgeerts P (2009) Long-term safety of infliximab for the treatment of inflammatory bowel disease: a single-centre cohort study. Gut 58:501–508CrossRef
9.
go back to reference Naganuma M, Kunisaki R, Yoshimura N, Takeuchi Y, Watanabe M (2013) A prospective analysis of the incidence of and risk factors for opportunistic infections in patients with inflammmatory bowel disease. J Gastroenterol 48:595–600CrossRef Naganuma M, Kunisaki R, Yoshimura N, Takeuchi Y, Watanabe M (2013) A prospective analysis of the incidence of and risk factors for opportunistic infections in patients with inflammmatory bowel disease. J Gastroenterol 48:595–600CrossRef
10.
go back to reference Osterman MT, Sandborn WJ, Colombel JF, Peyrin-Biroulet L, Robinson AM, Zhou Q, Lewis JD (2016) Crohn’s disease activity and concomitant immunosuppressants affect the risk of serious and opportunistic infections in patients treated with adalimumab. Am J Gastroenterol 111:1806–1815CrossRef Osterman MT, Sandborn WJ, Colombel JF, Peyrin-Biroulet L, Robinson AM, Zhou Q, Lewis JD (2016) Crohn’s disease activity and concomitant immunosuppressants affect the risk of serious and opportunistic infections in patients treated with adalimumab. Am J Gastroenterol 111:1806–1815CrossRef
11.
go back to reference Nyboe Andersen N, Pasternak B, Friis-Moller N et al (2015) Association between tumour necrosis factor- inhibitors and risk of serious infections in people with inflammatory bowel disease: nationwide Danish cohort study. BMJ 350:h2809CrossRef Nyboe Andersen N, Pasternak B, Friis-Moller N et al (2015) Association between tumour necrosis factor- inhibitors and risk of serious infections in people with inflammatory bowel disease: nationwide Danish cohort study. BMJ 350:h2809CrossRef
12.
go back to reference Kirchgesner J, Lemaitre M, Carrat F et al (2018) Risk of serious and opportunistic infections associated with treatment of inflammatory bowel diseases. Gastroenterology 155:337–346CrossRef Kirchgesner J, Lemaitre M, Carrat F et al (2018) Risk of serious and opportunistic infections associated with treatment of inflammatory bowel diseases. Gastroenterology 155:337–346CrossRef
13.
go back to reference Magro F, Gionchetti P, Eliakim R, Ardizzone S, Armuzzi A, Barreiro-de Acosta M, Burisch J, Gecse KB, Hart AL, Hindryckx P, Langner C, Limdi JK, Pellino G, Zagórowicz E, Raine T, Harbord M, Rieder F, European Crohn’s and Colitis Organisation [ECCO] (2017) Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1: definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and Ileo-anal pouch disorders. J Crohns Colitis 11:649–670CrossRef Magro F, Gionchetti P, Eliakim R, Ardizzone S, Armuzzi A, Barreiro-de Acosta M, Burisch J, Gecse KB, Hart AL, Hindryckx P, Langner C, Limdi JK, Pellino G, Zagórowicz E, Raine T, Harbord M, Rieder F, European Crohn’s and Colitis Organisation [ECCO] (2017) Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 1: definitions, diagnosis, extra-intestinal manifestations, pregnancy, cancer surveillance, surgery, and Ileo-anal pouch disorders. J Crohns Colitis 11:649–670CrossRef
14.
go back to reference Gomollón F, Dignass A, Annese V, Tilg H, van Assche G, Lindsay JO, Peyrin-Biroulet L, Cullen GJ, Daperno M, Kucharzik T, Rieder F, Almer S, Armuzzi A, Harbord M, Langhorst J, Sans M, Chowers Y, Fiorino G, Juillerat P, Mantzaris GJ, Rizzello F, Vavricka S, Gionchetti P, ECCO (2017) 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: part 1: diagnosis and medical management. J Crohns Colitis 11:3–25CrossRef Gomollón F, Dignass A, Annese V, Tilg H, van Assche G, Lindsay JO, Peyrin-Biroulet L, Cullen GJ, Daperno M, Kucharzik T, Rieder F, Almer S, Armuzzi A, Harbord M, Langhorst J, Sans M, Chowers Y, Fiorino G, Juillerat P, Mantzaris GJ, Rizzello F, Vavricka S, Gionchetti P, ECCO (2017) 3rd European evidence-based consensus on the diagnosis and management of Crohn’s disease 2016: part 1: diagnosis and medical management. J Crohns Colitis 11:3–25CrossRef
15.
go back to reference WHO (1995) Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. WHO Technical Report Series 854. Geneva: World Health Organization WHO (1995) Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. WHO Technical Report Series 854. Geneva: World Health Organization
16.
go back to reference (1993) Recommendations of the Advisory Committee on Immunization Practices (ACIP): use of vaccines and immune globulins for persons with altered immunocompetence. MMWR Recomm Rep 42:1–18 (1993) Recommendations of the Advisory Committee on Immunization Practices (ACIP): use of vaccines and immune globulins for persons with altered immunocompetence. MMWR Recomm Rep 42:1–18
17.
go back to reference Doran MF, Crowson CS, Pond GR, O'Fallon WM, Gabriel SE (2002) Predictors of infection in rheumatoid arthritis. Arthritis Rheum 46:2294–2300CrossRef Doran MF, Crowson CS, Pond GR, O'Fallon WM, Gabriel SE (2002) Predictors of infection in rheumatoid arthritis. Arthritis Rheum 46:2294–2300CrossRef
18.
go back to reference Ananthakrishnan AN, McGinley EL (2013) Infection-related hospitalizations are associated with increased mortality in patients with inflammatory bowel diseases. J Crohns Colitis 7:107–112CrossRef Ananthakrishnan AN, McGinley EL (2013) Infection-related hospitalizations are associated with increased mortality in patients with inflammatory bowel diseases. J Crohns Colitis 7:107–112CrossRef
19.
go back to reference Viget N, Vernier-Massouille G, Salmon-Ceron D, Yazdanpanah Y, Colombel JF (2008) Opportunistic infections in patients with inflammatory bowel disease: prevention and diagnosis. Gut 57:549–558CrossRef Viget N, Vernier-Massouille G, Salmon-Ceron D, Yazdanpanah Y, Colombel JF (2008) Opportunistic infections in patients with inflammatory bowel disease: prevention and diagnosis. Gut 57:549–558CrossRef
20.
go back to reference Cottone M, Kohn A, Daperno M, Armuzzi A, Guidi L, D'Inca R, Bossa F, Angelucci E, Biancone L, Gionchetti P, Ardizzone S, Papi C, Fries W, Danese S, Riegler G, Cappello M, Castiglione F, Annese V, Orlando A (2011) Advanced age is an independent risk factor for severe infections and mortality in patients given anti-tumor necrosis factor therapy for inflammatory bowel disease. Clin Gastroenterol Hepatol 9:30–35CrossRef Cottone M, Kohn A, Daperno M, Armuzzi A, Guidi L, D'Inca R, Bossa F, Angelucci E, Biancone L, Gionchetti P, Ardizzone S, Papi C, Fries W, Danese S, Riegler G, Cappello M, Castiglione F, Annese V, Orlando A (2011) Advanced age is an independent risk factor for severe infections and mortality in patients given anti-tumor necrosis factor therapy for inflammatory bowel disease. Clin Gastroenterol Hepatol 9:30–35CrossRef
21.
go back to reference Gavazzi G, Krause KH (2002) Ageing and infection. Lancet Infect Dis 2:659–666CrossRef Gavazzi G, Krause KH (2002) Ageing and infection. Lancet Infect Dis 2:659–666CrossRef
22.
go back to reference Lord JM, Butcher S, Killampali V, Lascelles D, Salmon M (2001) Neutrophil ageing and immunesenescence. Mech Ageing Dev 122:1521–1535CrossRef Lord JM, Butcher S, Killampali V, Lascelles D, Salmon M (2001) Neutrophil ageing and immunesenescence. Mech Ageing Dev 122:1521–1535CrossRef
23.
go back to reference Castle SC (2000) Clinical relevance of age-related immune dysfunction. Clin Infect Dis 31:578–585CrossRef Castle SC (2000) Clinical relevance of age-related immune dysfunction. Clin Infect Dis 31:578–585CrossRef
24.
go back to reference Borren NZ, Ananthakrishnan AN (2019) Safety of biologic therapy in older patients with immune-mediated diseases: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 17:1736–1743CrossRef Borren NZ, Ananthakrishnan AN (2019) Safety of biologic therapy in older patients with immune-mediated diseases: a systematic review and meta-analysis. Clin Gastroenterol Hepatol 17:1736–1743CrossRef
25.
go back to reference Gershwin ME, Borchers AT, Keen CL (2000) Phenotypic and functional considerations in the evaluation of immunity in nutritionally compromised hosts. J Infect Dis 182(Suppl 1):S108–S114CrossRef Gershwin ME, Borchers AT, Keen CL (2000) Phenotypic and functional considerations in the evaluation of immunity in nutritionally compromised hosts. J Infect Dis 182(Suppl 1):S108–S114CrossRef
26.
go back to reference Büning C, von Kraft C, Hermsdorf M, Gentz E, Wirth EK, Valentini L, Haas V (2015) Visceral adipose tissue in patients with Crohn’s disease correlates with disease activity, inflammatory markers, and outcome. Inflamm Bowel Dis 21:2590–2597CrossRef Büning C, von Kraft C, Hermsdorf M, Gentz E, Wirth EK, Valentini L, Haas V (2015) Visceral adipose tissue in patients with Crohn’s disease correlates with disease activity, inflammatory markers, and outcome. Inflamm Bowel Dis 21:2590–2597CrossRef
27.
go back to reference Karmiris K, Koutroubakis IE, Xidakis C et al (2006) Circulating levels of leptin, adiponectin, resistin, and ghrelin in inflammatory bowel disease. Inflamm Bowel Dis 2:100–105CrossRef Karmiris K, Koutroubakis IE, Xidakis C et al (2006) Circulating levels of leptin, adiponectin, resistin, and ghrelin in inflammatory bowel disease. Inflamm Bowel Dis 2:100–105CrossRef
28.
go back to reference Waluga M, Hartleb M, Boryczka G et al (2014) Serum adipokines in inflammatory bowel disease. World J Gastroenterol 14:6912–6917CrossRef Waluga M, Hartleb M, Boryczka G et al (2014) Serum adipokines in inflammatory bowel disease. World J Gastroenterol 14:6912–6917CrossRef
29.
go back to reference Vögelin M, Biedermann L, Frei P, Vavricka SR, Scharl S, Zeitz J, Sulz MC, Fried M, Rogler G, Scharl M (2016) The impact of azathioprine-associated lymphopenia on the onset of opportunistic infections in patients with inflammatory bowel disease. PLoS One 11(5):e0155218CrossRef Vögelin M, Biedermann L, Frei P, Vavricka SR, Scharl S, Zeitz J, Sulz MC, Fried M, Rogler G, Scharl M (2016) The impact of azathioprine-associated lymphopenia on the onset of opportunistic infections in patients with inflammatory bowel disease. PLoS One 11(5):e0155218CrossRef
30.
go back to reference Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD et al (2001) Tuberculosis associated with infliximab, a tumor necrosis factor α–neutralizing agent. N Engl J Med 345(15):1098–1104CrossRef Keane J, Gershon S, Wise RP, Mirabile-Levens E, Kasznica J, Schwieterman WD et al (2001) Tuberculosis associated with infliximab, a tumor necrosis factor α–neutralizing agent. N Engl J Med 345(15):1098–1104CrossRef
31.
go back to reference Nuño JLC, Mendoza MIV, Domènech E, de Acosta MB, Comas ME, Gisbert JP et al (2013) Recomendaciones del Grupo Español de Trabajo en Enfermedad de Crohn y Colitis Ulcerosa sobre el uso de fármacos antifactor de necrosis tumoral? en la enfermedad inflamatoria intestinal (2013). Gastroenterol Hepatol 36(3):127–146CrossRef Nuño JLC, Mendoza MIV, Domènech E, de Acosta MB, Comas ME, Gisbert JP et al (2013) Recomendaciones del Grupo Español de Trabajo en Enfermedad de Crohn y Colitis Ulcerosa sobre el uso de fármacos antifactor de necrosis tumoral? en la enfermedad inflamatoria intestinal (2013). Gastroenterol Hepatol 36(3):127–146CrossRef
32.
go back to reference Zabana Y, Rodríguez L, Lobatón T, Gordillo J, Montserrat A, Mena R et al (2019) Relevant infections in inflammatory bowel disease, and their relationship with immunosuppressive therapy and their effects on disease mortality. J Crohns Colitis Zabana Y, Rodríguez L, Lobatón T, Gordillo J, Montserrat A, Mena R et al (2019) Relevant infections in inflammatory bowel disease, and their relationship with immunosuppressive therapy and their effects on disease mortality. J Crohns Colitis
33.
go back to reference Lorenzetti R, Zullo A, Ridola L, Diamanti AP, Laganà B, Gatta L, Migliore A, Armuzzi A, Hassan C, Bruzzese V (2014) Higher risk of tuberculosis reactivation when anti-TNF is combined with immunosuppressive agents: a systematic review of randomized controlled trials. Ann Med 46(7):547–554CrossRef Lorenzetti R, Zullo A, Ridola L, Diamanti AP, Laganà B, Gatta L, Migliore A, Armuzzi A, Hassan C, Bruzzese V (2014) Higher risk of tuberculosis reactivation when anti-TNF is combined with immunosuppressive agents: a systematic review of randomized controlled trials. Ann Med 46(7):547–554CrossRef
34.
go back to reference Brassard P, Bitton A, Suissa A, Sinyavskaya L, Patenaude V, Suissa S (2014) Oral corticosteroids and the risk of serious infections in patients with elderly-onset inflammatory bowel diseases. Am J Gastroenterol 109(11):1795–1802 quiz 1803CrossRef Brassard P, Bitton A, Suissa A, Sinyavskaya L, Patenaude V, Suissa S (2014) Oral corticosteroids and the risk of serious infections in patients with elderly-onset inflammatory bowel diseases. Am J Gastroenterol 109(11):1795–1802 quiz 1803CrossRef
35.
go back to reference Baumgart D (2011) Crohn’s disease and ulcerative colitis. Springer Baumgart D (2011) Crohn’s disease and ulcerative colitis. Springer
Metadata
Title
Clinical assessment of risk factors for infection in inflammatory bowel disease patients
Authors
Joan Tosca
Natalia Garcia
Isabel Pascual
Marta Maia Bosca-Watts
Rosario Anton
Ana Sanahuja
Pilar Mas
Francisco Mora
Miguel Minguez
Publication date
01-03-2020
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Colorectal Disease / Issue 3/2020
Print ISSN: 0179-1958
Electronic ISSN: 1432-1262
DOI
https://doi.org/10.1007/s00384-019-03501-0

Other articles of this Issue 3/2020

International Journal of Colorectal Disease 3/2020 Go to the issue