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Review Article| Volume 51, ISSUE 5, P613-620, May 2019

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Risk factors and timing for colectomy in chronically active refractory ulcerative colitis: A systematic review

Published:February 06, 2019DOI:https://doi.org/10.1016/j.dld.2019.01.018

      Abstract

      Background

      In patients with chronic refractory ulcerative colitis (UC) the precise timing for indication to colectomy is unclear.

      Aims

      We performed a systematic review of the literature on the risk factors for colectomy in patients with chronic refractory UC in the biologic era.

      Methods

      PubMed Central/Medline and Embase were systemically searched for records published between January 2000 and December 2017. Current evidence was summarized and filtered by expert opinion.

      Results

      70 studies were included in the qualitative synthesis. Several factors were found to be associated with a higher or reduced risk for colectomy, including variables at baseline – such as progression from proctitis/left-sided to extensive colitis, extensive colitis at diagnosis, high baseline C Reactive Protein or erythrocyte sedimentation rate, male gender, and younger age at diagnosis – previous medical history, and factors arising during therapy with biologics, including the absence of clinical response after induction with infliximab or adalimumab, and the lack of mucosal healing during therapy with anti-TNFs.

      Conclusions

      Two main points may help physicians to decide when the surgical option may be considered in patients with chronic refractory UC: (1) a first risk stratification can be obtained by analyzing factors at baseline and medical history, including the previous exposure to anti-TNFs; (2) during therapy with biologics, the early assessment (after 12–16 weeks of treatment) of clinical and endoscopic response is a strong predictor of the subsequent risk of colectomy.

      Keywords

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      References

        • Ungaro R.
        • Mehandru S.
        • Allen P.B.
        • Peyrin-Biroulet L.
        • Colombel J.F.
        Ulcerative colitis.
        Lancet. 2017; 389: 1756-1770
        • Øresland T.
        • Bemelman W.A.
        • Sampietro G.M.
        • Spinelli A.
        • Windsor A.
        • Ferrante M.
        • et al.
        European evidence based consensus on surgery for ulcerative colitis.
        J Crohns Colitis. 2015; 9: 4-25
        • Dayan B.
        • Turner D.
        Role of surgery in severe ulcerative colitis in the era of medical rescue therapy.
        World J Gastroenterol. 2012; 18: 3833-3838
        • Annese V.
        • Duricova D.
        • Gower-Rousseau C.
        • Jess T.
        • Langholz E.
        Impact of new treatments on hospitalisation, surgery, infection, and mortality in IBD: a focus paper by the epidemiology committee of ECCO.
        Crohns Colitis. 2016; 10: 216-225
        • Jakobsen C.
        • Paerregaard A.
        • Munkholm P.
        • Wewer V.
        Pediatric inflammatory bowel disease: increasing incidence, decreasing surgery rate, and compromised nutritional status: a prospective population based cohort study 2007-2009.
        Inflamm Bowel Dis. 2011; 17: 2541-2550
        • Vind I.
        • Riis L.
        • Jess T.
        • et al.
        Increasing incidences of inflammatory bowel disease and decreasing surgery rates in Copenhagen City and County, 2003–2005: a population-based study from the Danish Crohn colitis database.
        Am J Gastroenterol. 2006; 101: 1274-1282
        • Vester-Andersen M.K.
        • Prosberg M.V.
        • Jess T.
        • Andersson M.
        • Bengtsson B.G.
        • Blixt T.
        • et al.
        Disease course and surgery rates in inflammatory bowel disease: a population-based, 7-year follow-up study in the era of immunomodulating therapy.
        Am J Gastroenterol. 2014; 109: 705-714
        • Singh S.
        • Al-Darmaki A.
        • Frolkis A.D.
        • Seow C.H.
        • Leung Y.
        • Novak K.L.
        • et al.
        Postoperative mortality among patients with inflammatory bowel diseases: a systematic review and meta-analysis of population-based studies.
        Gastroenterology. 2015; 149: 928-937
        • Burisch J.
        • Pedersen N.
        • Čuković-Čavka S.
        • Brinar M.
        • Kaimakliotis I.
        • Duricova D.
        • et al.
        Eastwest gradient in the incidence of inflammatory bowel disease in Europe: the ECCO-EpiCom inception cohort.
        Gut. 2014; 63: 588-597
        • Laine L.
        • Kaltenbach T.
        • Barkun A.
        • McQuaid K.
        • Subramanian V.
        • Soetikno R.
        SCENIC international consensus statement on surveillance and management of dysplasia in inflammatory bowel disease.
        Gastroenterology. 2015; 148 (e28): 639-651
        • Shamseer L.
        • Moher D.
        • Clarke M.
        • Ghersi D.
        • Liberati A.
        • Petticrew M.
        • et al.
        Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation.
        BMJ. 2015; 349: 7647
        • Ardizzone S.
        • Cassinotti A.
        • Duca P.
        • et al.
        Mucosal healing predicts late outcomes after the first course of corticosteroids for newly diagnosed ulcerative colitis.
        Clin Gastroenterol Hepatol. 2011; 9: 483-–489
        • Charpentier C.
        • Salleron J.
        • Savoye G.
        • et al.
        Natural history of elderly-onset inflammatory bowel disease: a population-based cohort study.
        Gut. 2014; 63: 423-432
        • Colombel J.F.
        • Rutgeerts P.
        • Reinisch W.
        • et al.
        Early mucosal healing with infliximab is associated with improved long-term clinical outcomes in ulcerative colitis.
        Gastroenterology. 2011; 141: 1194-1201
        • Cosnes J.
        • Carbonnel F.
        • Beaugerie L.
        • et al.
        Effects of appendicectomy on the course of ulcerative colitis.
        Gut. 2002; 51: 803-807
        • Fernández-Salazar L.
        • Muñoz F.
        • Barrio J.
        • et al.
        Infliximab in ulcerative colitis: real-life analysis of factors predicting treatment discontinuation due to lack of response or colectomy: ECIA (ACAD Colitis and Infliximab Study).
        Scand J Gastroenterol. 2016; 51: 186-195
        • Freire P.
        • Cardoso R.
        • Figueiredo P.
        • et al.
        NOD2 gene mutations in ulcerative colitis: useless or misunderstood?.
        Int J Colorectal Dis. 2014; 29: 653-661
        • Hefti M.M.
        • Chessin D.B.
        • Harpaz N.H.
        • et al.
        Severity of inflammation as a predictor of colectomy in patients with chronic ulcerative colitis.
        Dis Colon Rectum. 2009; 52: 193-197
        • Henriksen M.
        • Jahnsen J.
        • Lygren I.
        • et al.
        C-reactive protein: a predictive factor and marker of inflammation in inflammatory bowel disease. Results from a prospective population-based study.
        Gut. 2008; 57: 1518-1523
        • Herzog D.
        • Fournier N.
        • Buehr P.
        • et al.
        Prevalence of intestinal complications in inflammatory bowel disease: a comparison between paediatric-onset and adult-onset patients.
        Eur J Gastroenterol Hepatol. 2017; 29: 926-931
        • Ho G.T.
        • Chiam P.
        • Drummond H.
        • et al.
        The efficacy of corticosteroid therapy in inflammatory bowel disease: analysis of a 5-year UK inception cohort.
        Aliment Pharmacol Ther. 2006; 24: 319-330
        • Hoie O.
        • Wolters F.L.
        • Riis L.
        • et al.
        Low colectomy rates in ulcerative colitis in an unselected European cohort followed for 10 years.
        Gastroenterology. 2007; 132: 507-515
        • Jodorkovsky D.
        • Young Y.
        • Abreu M.T.
        Clinical outcomes of patients with ulcerative colitis and co-existing Clostridium difficile infection.
        Dig Dis Sci. 2010; 55: 415-420
        • Park S.H.
        • Yang S.K.
        • Hong S.M.
        • et al.
        Severe disease activity and cytomegalovirus colitis are predictive of a nonresponse to infliximab in patients with ulcerative colitis.
        Dig Dis Sci. 2013; 58: 3592-3599
        • Christensen K.R.
        • Steenholdt C.
        • Brynskov J.
        Clinical outcome of adalimumab therapy in patients with ulcerative colitis previously treated with infliximab: a Danish single-center cohort study.
        Scand J Gastroenterol. 2015; 50: 1018-1024
        • Rönnblom A.
        • Holmström T.
        • Tanghöj H.
        • et al.
        Low colectomy rate five years after diagnosis of ulcerative colitis. Results from a prospective population-based cohort in Sweden (ICURE) diagnosed during 2005-2009.
        Scand J Gastroenterol. 2016; 51: 1339-1344
        • Italian Group for the Study of Inflammatory Bowel Disease
        • Armuzzi A.
        • Biancone L.
        • Daperno M.
        • et al.
        Adalimumab in active ulcerative colitis: a “real-life” observational study.
        Dig Liver Dis. 2013; 45: 738-743
        • Angelison L.
        • Almer S.
        • Eriksson A.
        • et al.
        Long-term outcome of infliximab treatment in chronic active ulcerative colitis: a Swedish multicentre study of 250 patients.
        Aliment Pharmacol Ther. 2017; 45: 519-532
        • Radford-Smith G.L.
        • Edwards J.E.
        • Purdie D.M.
        • et al.
        Protective role of appendicectomy on onset and severity of ulcerative colitis and Crohn’s disease.
        Gut. 2002; 51: 808-813
        • Taxonera C.
        • Estellés J.
        • Fernández-Blanco I.
        • et al.
        Adalimumab induction and maintenance therapy for patients with ulcerative colitis previously treated with infliximab.
        Aliment Pharmacol Ther. 2011; 33: 340-348
        • Abou Khalil M.
        • Boutros M.
        • Nedjar H.
        • et al.
        Incidence rates and predictors of colectomy for ulcerative colitis in the era of biologics: results from a provincial database.
        J Gastrointest Surg. 2018; 22: 124-132
        • Manser C.N.
        • Borovicka J.
        • Seibold F.
        • et al.
        Risk factors for complications in patients with ulcerative colitis.
        United Eur Gastroenterol J. 2016; 4: 281-287
        • Buhl S.
        • Steenholdt C.
        • Rasmussen M.
        • et al.
        Outcomes After Primary Infliximab Treatment Failure in Inflammatory Bowel Disease.
        Inflamm Bowel Dis. 2017; 23: 1210-1217
        • Arias M.T.
        • Vande Casteele N.
        • Vermeire S.
        • et al.
        A panel to predict long-term outcome of infliximab therapy for patients with ulcerative colitis.
        Clin Gastroenterol Hepatol. 2015; 13: 531-538
        • Subramaniam K.
        • Richardson A.
        • Dodd J.
        • et al.
        Early predictors of colectomy and long-term maintenance of remission in ulcerative colitis patients treated using anti-tumour necrosis factor therapy.
        Intern Med J. 2014; 44: 464-470
        • Colombel J.F.
        • Rutgeerts P.
        • Reinisch W.
        • et al.
        Early mucosal healing with infliximab is associated with improved long-term clinical outcomes in ulcerative colitis.
        Gastroenterology. 2011; 141: 1194-1201
        • Williet N.
        • Pillot C.
        • Oussalah A.
        • et al.
        Incidence of and impact of medications on colectomy in newly diagnosed ulcerative colitis in the era of biologics.
        Inflamm Bowel Dis. 2012; 18: 1641-1646
        • Safroneeva E.
        • Vavricka S.R.
        • Fournier N.
        • et al.
        Prevalence and risk factors for therapy escalation in ulcerative Colitis in the Swiss IBD Cohort Study.
        Inflamm Bowel Dis. 2015; 21: 1348-1358
        • Taxonera C.
        • Barreiro-de Acosta M.
        • Calvo M.
        • et al.
        Infliximab dose escalation as an effective strategy for managing secondary loss of response in ulcerative colitis.
        Dig Dis Sci. 2015; 60: 3075-3084
        • Etchevers M.J.
        • Aceituno M.
        • García-Bosch O.
        • et al.
        Risk factors and characteristics of extent progression in ulcerative colitis.
        Inflamm Bowel Dis. 2009; 15: 1320-1325
        • García-Bosch O.
        • Gisbert J.P.
        • Cañas-Ventura A.
        • et al.
        Observational study on the efficacy of adalimumab for the treatment of ulcerative colitis and predictors of outcome.
        J Crohns Colitis. 2013; 7: 717-722
        • Ferrante M.
        • Vermeire S.
        • Fidder H.
        • et al.
        Long-term outcome after infliximab for refractory ulcerative colitis.
        J Crohns Colitis. 2008; 2: 219-225
        • Jakobovits S.L.
        • Jewell D.P.
        • Travis S.P.
        Infliximab for the treatment of ulcerative colitis: outcomes in Oxfordfrom 2000 to 2006.
        Aliment Pharmacol Ther. 2007; 25: 1055-1060
        • Kalkan İ.H.
        • Dağlı Ü.
        • Kekilli M.
        • et al.
        Clinical course and predictors of total colectomy in ulcerative colitis; a referral center experience from Turkey.
        Turk J Gastroenterol. 2015; 26: 25-30
        • Khan N.H.
        • Almukhtar R.M.
        • Cole E.B.
        • et al.
        Early corticosteroids requirement after the diagnosis of ulcerative colitis diagnosis can predict a more severe long-term course of the disease — a nationwide study of 1035 patients.
        Aliment Pharmacol Ther. 2014; 40: 374-381
        • Lakatos P.L.
        • Vegh Z.
        • Lovasz B.D.
        • et al.
        Is current smoking still an important environmental factor in inflammatory bowel diseases? Results from a population-based incident cohort.
        Inflamm Bowel Dis. 2013; 19: 1010-1017
        • Li D.
        • Collins B.
        • Velayos F.S.
        • et al.
        Racial and ethnic differences in health care utilization and outcomes among ulcerative colitis patients in an integrated health-care organization.
        Dig Dis Sci. 2014; 59: 287-294
        • Manetti N.
        • Bagnoli S.
        • Rogai F.
        • et al.
        Disease course and colectomy rate of ulcerative colitis: a follow-up cohort study of a referral center in Tuscany.
        Inflamm Bowel Dis. 2016; 22: 1945-1953
        • Miyahara K.
        • Nouso K.
        • Saito S.
        • et al.
        Serum glycan markers for evaluation of disease activity and prediction of clinical course in patients with ulcerative colitis.
        PLoS One. 2013; 8e74861
        • Oussalah A.
        • Evesque L.
        • Laharie D.
        • et al.
        A multicenter experience with infliximab for ulcerative colitis: outcomes and predictors of response, optimization, colectomy, and hospitalization.
        Am J Gastroenterol. 2010; 105: 2617-2625
        • Romberg-Camps M.J.
        • Dagnelie P.C.
        • Kester A.D.
        • et al.
        Influence of phenotype at diagnosis and of other potential prognostic factors on the course of inflammatory bowel disease.
        Am J Gastroenterol. 2009; 104: 371-383
        • Rungoe C.
        • Langholz E.
        • Andersson M.
        • et al.
        Changes in medical treatment and surgery rates in inflammatory bowel disease: a nationwide cohort study 1979-2011.
        Gut. 2014; 63: 1607-1616
        • Sahami S.
        • Konté K.
        • Buskens C.J.
        • et al.
        Risk factors for proximal disease extension and colectomy in left-sided ulcerative colitis.
        United Eur Gastroenterol J. 2017; 5: 554-562
        • Shiga H.
        • Takagi S.
        • Inoue R.
        • et al.
        What determines the later clinical course of patients who do not undergo colectomy at the first attack? A Japanese cohort study on ulcerative colitis.
        Digestion. 2010; 81: 104-112
        • Taxonera C.
        • Iglesias E.
        • Muñoz F.
        • et al.
        Adalimumab maintenance treatment in ulcerative colitis: outcomes by prior anti-TNF use and efficacy of dose escalation.
        Dig Dis Sci. 2017; 62: 481-490
        • Iborra M.
        • Pérez-Gisbert J.
        • Bosca-Watts M.M.
        • et al.
        Effectiveness of adalimumab for the treatment of ulcerative colitis in clinical practice: comparison between anti-tumour necrosis factor-naéve and non-naéve patients.
        J Gastroenterol. 2017; 52: 788-799
        • Ananthakrishnan A.N.
        • Issa M.
        • Beaulieu D.B.
        • et al.
        History of medical hospitalization predicts future need for colectomy in patients with ulcerative colitis.
        Inflamm Bowel Dis. 2009; 15: 176-181
        • van der Heide F.
        • Dijkstra A.
        • Weersma R.K.
        • et al.
        Effects of active and passive smoking on disease course of Crohn’s disease and ulcerative colitis.
        Inflamm Bowel Dis. 2009; 15: 1199-1207
        • Al-Darmaki A.
        • Hubbard J.
        • Seow C.H.
        • et al.
        Clinical predictors of the risk of early colectomy in ulcerative colitis: a population-based study.
        Inflamm Bowel Dis. 2017; 23: 1272-1277
        • Taxonera C.
        • Rodríguez C.
        • Bertoletti F.
        • et al.
        Clinical outcomes of golimumab as first, second or third anti-TNF agent in patients with moderate-to-severe ulcerative colitis.
        Inflamm Bowel Dis. 2017; 23: 1394-1402
        • Portela F.
        • Magro F.
        • Lago P.
        • et al.
        Ulcerative colitis in a Southern European country: a national perspective.
        Inflamm Bowel Dis. 2010; 16: 822-829
        • Niewiadomski O.
        • Studd C.
        • Hair C.
        • et al.
        Prospective population-based cohort of inflammatory bowel disease in the biologics era: disease course and predictors of severity.
        J Gastroenterol Hepatol. 2015; 30: 1346-1353
        • Kevans D.
        • Waterman M.
        • Milgrom R.
        • et al.
        Serological markers associated with disease behavior and response to anti-tumor necrosis factor therapy in ulcerative colitis.
        J Gastroenterol Hepatol. 2015; 30: 64-70
        • Burisch J.
        • Ungaro R.
        • Vind I.
        • et al.
        Proximal disease extension in patients with limited ulcerative colitis: a Danish population-based inception cohort.
        J Crohns Colitis. 2017; 11: 1200-1204
        • Armuzzi A.
        • Pugliese D.
        • Danese S.
        • et al.
        Long-term combination therapy with infliximab plus azathioprine predicts sustained steroid-free clinical benefit in steroid-dependent ulcerative colitis.
        Inflamm Bowel Dis. 2014; 20: 1368-1374
        • Cañas-Ventura A.
        • Márquez L.
        • Ricart E.
        • et al.
        Risk of colectomy in patients with ulcerative colitis under thiopurine treatment.
        J Crohns Colitis. 2014; 8: 1287-1293
        • Armuzzi A.
        • Pugliese D.
        • Danese S.
        • et al.
        Infliximab in steroid-dependent ulcerative colitis: effectiveness and predictors of clinical and endoscopic remission.
        Inflamm Bowel Dis. 2013; 19: 1065-1072
        • Oussalah A.
        • Evesque L.
        • Laharie D.
        • et al.
        A multicenter experience with infliximab for ulcerative colitis: outcomes and predictors of response, optimization, colectomy, and hospitalization.
        Am J Gastroenterol. 2010; 105: 2617-2625
        • Kin C.
        • Kate Bundorf M.
        As infliximab use for ulcerative colitis has increased, so has the rate of surgical resection.
        J Gastrointest Surg. 2017; 21: 1159-1165
        • Szamosi T.
        • Banai J.
        • Lakatos L.
        • et al.
        Early azathioprine/biological therapy is associated with decreased risk for first surgery and delays time to surgery but not reoperation in both smokers and nonsmokers with Crohn’s disease, while smoking decreases the risk of colectomy in ulcerative colitis.
        Eur J Gastroenterol Hepatol. 2010; 22: 872-879
        • García-Bosch O.
        • Aceituno M.
        • Ordás I.
        • et al.
        Long-term follow-up of patients treated with infliximab for ulcerative colitis: predictive factors of response — an observational study.
        Dig Dis Sci. 2016; 61: 2051-2059
        • Chhaya V.
        • Saxena S.
        • Cecil E.
        • et al.
        The impact of timing and duration of thiopurine treatment on colectomy in ulcerative colitis: a national population-based study of incident cases between 1989 and 2009.
        Aliment Pharmacol Ther. 2015; 41: 87-98
        • Solberg I.C.
        • Høivik M.L.
        • Cvancarova M.
        • et al.
        Risk matrix model for prediction of colectomy in a population-based study of ulcerative colitis patients (the IBSEN study).
        Scand J Gastroenterol. 2015; 50: 1456-1462
        • Murthy S.K.
        • Greenberg G.R.
        • Croitoru K.
        • et al.
        Extent of early clinical response to infliximab predicts long-term treatment success in active ulcerative colitis.
        Inflamm Bowel Dis. 2015; 21: 2090-2096
        • Papamichael K.
        • Rivals-Lerebours O.
        • Billiet T.
        • et al.
        Long-term outcome of patients with ulcerative colitis and primary non-response to infliximab.
        J Crohns Colitis. 2016; 10: 1015-1023
        • Fernández-Salazar L.
        • Barrio J.
        • Muñoz F.
        • et al.
        Frequency, predictors, and consequences of maintenance infliximab therapy intensification in ulcerative colitis.
        Rev Esp Enferm Dig. 2015; 107: 527-533
        • Cesarini M.
        • Katsanos K.
        • Papamichael K.
        • et al.
        Dose optimization is effective in ulcerative colitis patients losing response to infliximab: a collaborative multicentre retrospective study.
        Dig Liver Dis. 2014; 46: 135-139
        • Rostholder E.
        • Ahmed A.
        • Cheifetz A.S.
        • et al.
        Outcomes after escalation of infliximab therapy in ambulatory patients with moderately active ulcerative colitis.
        Aliment Pharmacol Ther. 2012; 35: 562-567
        • Laharie D.
        • Filippi J.
        • Roblin X.
        • et al.
        Impact of mucosal healing on long-term outcomes in ulcerative colitis treated with infliximab: a multicenter experience.
        Aliment Pharmacol Ther. 2013; 37: 998-1004
        • Myrelid P.
        • Landerholm K.
        • Nordenvall C.
        • et al.
        Appendectomy and the risk of colectomy in ulcerative colitis: a national cohort study.
        Am J Gastroenterol. 2017; 112: 1311-1319
        • Parian A.
        • Limketkai B.
        • Koh J.
        • et al.
        Appendectomy does not decrease the risk of future colectomy in UC: results from a large cohort and meta-analysis.
        Gut. 2017; 66: 1390-1397
        • Gisbert J.P.
        • Marin A.C.
        • McNicholl A.G.
        • Chaparro M.
        Systematic review with meta-analysis: the efficacy of a second anti-TNF in patients with inflammatory bowel disease whose previous anti-TNF treatment has failed.
        Aliment Pharmacol Ther. 2015; 41: 613-623
        • Maida M.
        • Macaluso F.S.
        • Ianiro G.
        • et al.
        Screening of colorectal cancer: present and future.
        Expert Rev Anticancer Ther. 2017; 17: 1131-1146