Histological healing: should it be considered as a new outcome for ulcerative colitis?

References

• Ungaro R, Mehandru S, Allen PB, et al. Ulcerative colitis. Lancet. 2017;389(10080):1756–1770.
   PubMed Web of Science ®Google Scholar
• Hindryckx P, Baert F, Hart A, et al. Clinical trials in ulcerative colitis: a historical perspective. J Crohns Colitis. 2015;9(7):580–588.
   PubMed Web of Science ®Google Scholar
• Ungaro R, Colombel JF, Lissoos T, et al. A treat-to-target update in ulcerative colitis: a systematic review. Am J Gastroenterol. 2019;114(6):874–883.
   PubMed Web of Science ®Google Scholar
• Marchal Bressenot A. Which evidence for a treat to target strategy in ulcerative colitis? Best Pract Res Clin Gastroenterol. 2018;32-33:3–8.
   PubMed Web of Science ®Google Scholar
• Peyrin-Biroulet L, Bressenot A, Kampman W, et al. Histologic remission: the ultimate therapeutic goal in ulcerative colitis? Clin Gastroenterol Hepatol. 2014;12(6):929–34e2.
   PubMed Web of Science ®Google Scholar
• Lopez A, Pouillon L, Beaugerie L, et al. Colorectal cancer prevention in patients with ulcerative colitis. Best Pract Res Clin Gastroenterol. 2018;32-33:103–109.
   PubMed Web of Science ®Google Scholar
• Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol. 2004;287:G7e17.
   Web of Science ®Google Scholar
• Zenlea T, Yee EU, Rosenberg L, et al. Histology grade is independently associated with relapse risk in patients with ulcerative colitis in clinical remission: a prospective study. Am J Gastroenterol. 2016;111(5):685–690.
   PubMed Web of Science ®Google Scholar
• Kanazawa M, Takahashi F, Tominaga K, et al. Relationship between endoscopic mucosal healing and histologic inflammation during remission maintenance phase in ulcerative colitis: a retrospective study. Endosc Int Open. 2019;7(4):E568–E575.
   PubMed Web of Science ®Google Scholar
• Danese S, Roda G, Peyrin-Biroulet L, et al. Evolving therapeutic goals in ulcerative colitis: towards disease clearance. Nat Rev Gastroenterol Hepatol. [updated 2019 Sept 13]. DOI:10.1038/s41575-019-0211-1
   Web of Science ®Google Scholar
• Colombel JF, D’haens G, Lee WJ, et al. Outcomes and strategies to support a treat-to-target approach in inflammatory bowel disease: a systematic review. J Crohns Colitis. [updated 2019 Aug 12]. DOI:10.1093/ecco-jcc/jjz131
   Google Scholar
• Sands BE, Sandborn WJ, Panaccione R, et al. Ustekinumab as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2019;381(13):1201–1214.
   PubMed Web of Science ®Google Scholar
• Sands BE, Peyrin-Biroulet L, Loftus EV Jr, et al. Vedolizumab versus adalimumab for moderate-to-severe ulcerative colitis. N Engl J Med. 2019;381(13):1215–1226.
   PubMed Web of Science ®Google Scholar
• Villanacci V, Baert F, Cornillie F, et al. Challenges faced by cross-sectional imaging and histological endpoints in clinical trials. J Crohns Colitis. 2017;11(suppl_2):S586–S592.
   PubMedGoogle Scholar
• Pai RK, Geboes K. Disease activity and mucosal healing in inflammatory bowel disease: a new role for histopathology? Virchows Arch. 2018;472(1):99–110.
   PubMed Web of Science ®Google Scholar
• Marchal-Bressenot A, Riddell RH, Boulagnon-Rombi C, et al. Review article: the histological assessment of disease activity in ulcerative colitis. Aliment Pharmacol Ther. 2015;42(8):957–967.
   PubMed Web of Science ®Google Scholar
• Marchal-Bressenot A, Salleron J, Bou-lagnon-Rombi C, et al. Development and validation of the Nancy histological index for UC. Gut. 2017;66:43–49.
   PubMed Web of Science ®Google Scholar
• Bryant RV, Burger DC, Delo J, et al. Beyond endoscopic mucosal healing in UC: histological remission better predicts corticosteroid use and hospitalization over 6 years of follow-up. Gut. 2016;65:408–414.
   PubMed Web of Science ®Google Scholar
• Magro F, Lopes J, Borralho P, et al. Comparison of different histological indexes in the assessment of UC activity and their accuracy regarding endoscopic outcomes and faecal calprotectin levels. Gut. 2019;68(4):594–603.
   PubMed Web of Science ®Google Scholar
• Magro F, Lopes J, Borralho P, et al. Comparing the continuous geboes score with the robarts histopathology index: definitions of histological remission and response and their relation to faecal calprotectin levels. J Crohn’s Colitis. [updated 2019 Sept 4]. DOI:10.1093/ecco-jcc/jjz123
   Google Scholar
• Ozaki R, Kobayashi T, Okabayashi S, et al. Histological risk factors to predict clinical relapse in ulcerative colitis with endoscopically normal mucosa. J Crohns Colitis. 2018;12(11):1288–1294.
   PubMed Web of Science ®Google Scholar
• Meucci G, Fasoli R, Saibeni S, et al. Prognostic significance of endoscopic remission in patients with active ulcerative colitis treated with oral and topical mesalazine: a prospective, multicenter study. Inflamm Bowel Dis. 2012;18:1006–1010.
   PubMed Web of Science ®Google Scholar
• Le Berre C, Roda G, Nedeljkovic Protic M, et al. Modern use of 5-aminosalicylic acid compounds for ulcerative colitis. Expert Opin Biol Ther. 1–16. [updated 2019 Sept 18]. DOI:10.1080/14712598.2019.1666101
   Web of Science ®Google Scholar
• Römkens TEH, Kampschreur MT, Drenth JPH, et al. High mucosal healing rates in 5-ASA-treated ulcerative colitis patients: results of a meta-analysis of clinical trials. Inflamm Bowel Dis. 2012;18:2190–2198.
   PubMed Web of Science ®Google Scholar
• Rubin DT, Bradette M, Gabalec L, et al. Ulcerative colitis remission status after induction with Mesalazine predicts maintenance outcomes: the MOMENTUM Trial. J Crohns Colitis. 2016;10(8):925–933.
   PubMed Web of Science ®Google Scholar
• Bajpai M, Seril DN, Van Gurp J, et al. Effect of long-term mesalamine therapy on cancer-associated gene expression in colonic mucosa of patients with ulcerative colitis. Dig Dis Sci. 2019;64(3):740–750.
   PubMed Web of Science ®Google Scholar
• Prieux-Klotz C, Nahon S, Amiot A, et al. Rate and predictors of mucosal healing in ulcerative colitis treated with thiopurines: results of a multicentric cohort study. Dig Dis Sci. 2017;62(2):473–480.
   PubMed Web of Science ®Google Scholar
• Giugliano FP, Strisciuglio C, Martinelli M, et al. Does Azathioprine induce endoscopic and histologic healing in pediatric inflammatory bowel disease? A prospective, observational study. Dig Liver Dis. 2018;50(3):240–246.
   PubMedGoogle Scholar
• Molander P, Sipponen T, Kemppainen H, et al. Achievement of deep remission during scheduled maintenance therapy with TNFa-blocking agents in IBD. J Crohn’s Colitis. 2013;7:730–735.
   Google Scholar
• Magro F, Lopes SI, Lopes J, et al. Histological outcomes and predictive value of fecal markers in moderately to severely active ulcerative colitis patients receiving infliximab. J Crohn’s Colitis. 2016;10:1407–1416.
   Google Scholar
• Papamichael K, Rakowsky S, Rivera C, et al. Infliximab trough concentrations during maintenance therapy are associated with endoscopic and histologic healing in ulcerative colitis. Aliment Pharmacol Ther. 2018;47:478–484.
   PubMed Web of Science ®Google Scholar
• Fernández-Blanco JI, Fernández-Díaz G, Cara C, et al. Adalimumab for induction of histological remission in moderately to severely active ulcerative colitis. Dig Dis Sci. 2018;63(3):731–737.
   PubMed Web of Science ®Google Scholar
• Arijs I, De Hertogh G, Lemmens B, et al. Effect of vedolizumab (anti-a4ß7-integrin) therapy on histological healing and mucosal gene expression in patients with UC. Gut. 2018;67(1):43–52.
   PubMed Web of Science ®Google Scholar
• Pouillon L, Rousseau H, Busby-Venner H, et al. Vedolizumab trough levels and histological healing during maintenance therapy in ulcerative colitis. J Crohns Colitis. 2019;13(8):970–975.
   PubMed Web of Science ®Google Scholar
• Peyrin-Biroulet L, Feagan B, Pai RK, et al. Association between histological indices and ulcerative colitis activity measures among patients in the HICKORY (etrolizumab) open-label induction cohort. ECCO 2019 P136. [updated 2019 Oct 10]. Available from: https://www.ecco-ibd.eu/publications/congress-abstract-s/abstracts-2019/item/p136-association-between-histological-indices-and-ulcerative-colitis-activity-measures-among-patients-in-the-hickory-etrolizumab-open-label-induction-cohort.html
   Google Scholar
• Peyrin-Biroulet L, Panés J, Chiorean M, et al. Histological remission and mucosal healing in a randomised, placebo-controlled, Phase 2 study of etrasimod in patients with moderately to severely active ulcerative colitis. ECCO 2019 OP09. [updated 2019 Oct 10]. Available from https://www.ecco-ibd.eu/publications/congress-abstract-s/abstracts-2019/item/op09-histological-remission-and-mucosal-healing-in-a-randomised-placebo-controlled-phase-2-study-of-etrasimod-in-patients-with-moderately-to-severely-active-ulcerative-colitis.html
   Google Scholar
• Sandborn WJ, Feagan BG, Wolf DC, et al. Ozanimod induction and maintenance treatment for ulcerative colitis. N Engl J Med. 2016;374(18):1754–1762.
   PubMed Web of Science ®Google Scholar
• Jairath V, Peyrin-Biroulet L, Zou G, et al. Responsiveness of histological disease activity indices in ulcerative colitis: a post hoc analysis using data from the TOUCHSTONE randomised controlled trial. Gut. 2019;68(7):1162–1168.
   PubMed Web of Science ®Google Scholar
• Colombel JF, Panaccione R, Bossuyt P, et al. Effect of tight control management on Crohn’s disease (CALM): a multicentre, randomised, controlled phase 3 trial. Lancet. 2018;390(10114):2779–2789.
   PubMed Web of Science ®Google Scholar
• Römkens TEH, Kranenburg P, van Tilburg A, et al. Assessment of histological remission in ulcerative colitis: discrepancies between daily practice and expert opinion. J Crohn’s Colitis. 2018;12:425–431.
   Google Scholar
• Bryant RV, Costello SP, Schoeman S, et al. Limited uptake of ulcerative colitis “treat-to-target” recommendations in real-world practice. J Gastroenterol Hepatol. 2018;33(3):599–607.
   PubMed Web of Science ®Google Scholar