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Gastroenterology

Endoscopic mucosal healing and histologic remission in ulcerative colitis: a systematic literature review of clinical, quality-of-life and economic outcomes

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Pages 1531-1541 | Received 09 Feb 2022, Accepted 20 May 2022, Published online: 11 Jun 2022

References

  • Ordas I, Eckmann L, Talamini M, et al. Ulcerative colitis. Lancet. 2012;380(9853):1606–1619.
  • Rubin DT, Ananthakrishnan AN, Siegel CA, et al. ACG clinical guideline: ulcerative colitis in adults. Am J Gastroenterol. 2019;114(3):384–413.
  • Harbord M, Eliakim R, Bettenworth D, et al. Third European evidence-based consensus on diagnosis and management of ulcerative colitis. Part 2: current management. J Crohns Colitis. 2017;11(7):769–784.
  • Bressler B, Marshall JK, Bernstein CN, et al. Clinical practice guidelines for the medical management of nonhospitalized ulcerative colitis: the Toronto consensus. Gastroenterology. 2015;148(5):1035–1058.e3.
  • Daperno M, Castiglione F, de Ridder L, et al. Results of the 2nd part scientific workshop of the ECCO. II: measures and markers of prediction to achieve, detect, and monitor intestinal healing in inflammatory bowel disease. J Crohns Colitis. 2011;5(5):484–498.
  • Peyrin-Biroulet L, Ferrante M, Magro F, et al. Results from the 2nd scientific workshop of the ECCO. I: impact of mucosal healing on the course of inflammatory bowel disease. J Crohns Colitis. 2011;5(5):477–483.
  • Peyrin-Biroulet L, Sandborn W, Sands BE, et al. Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE): determining therapeutic goals for treat-to-target. Am J Gastroenterol. 2015;110(9):1324–1338.
  • 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.
  • Falvey JD, Hoskin T, Meijer B, et al. Disease activity assessment in IBD: clinical indices and biomarkers fail to predict endoscopic remission. Inflamm Bowel Dis. 2015;21(4):824–831.
  • Regueiro M, Rodemann J, Kip KE, et al. Physician assessment of ulcerative colitis activity correlates poorly with endoscopic disease activity. Inflamm Bowel Dis. 2011;17(4):1008–1014.
  • Feagan BG, Reinisch W, Rutgeerts P, et al. The effects of infliximab therapy on health-related quality of life in ulcerative colitis patients. Am J Gastroenterology. 2007;102(4):794–802.
  • Motoya S, Watanabe K, Ogata H, et al. Vedolizumab in Japanese patients with ulcerative colitis: a phase 3, randomized, double-blind, placebo-controlled study. PLoS One. 2019;14(2):e0212989.
  • Ryan C, Sobell JM, Leonardi CL, et al. Safety of adalimumab dosed every week and every other week: focus on patients with hidradenitis suppurativa or psoriasis. Am J Clin Dermatol. 2018;19(3):437–447.
  • Sandborn WJ, Feagan BG, Marano C, et al. Subcutaneous golimumab induces clinical response and remission in patients with moderate-to-severe ulcerative colitis. Gastroenterology. 2014;146(1):85–95.
  • U.S. National Library of Medicine. Safety and efficacy trial of RPC1063 for moderate to severe ulcerative colitis [NCT02435992]. [cited 2022 May 3]. Available at: https://clinicaltrials.gov/ct2/show/NCT02435992?term=ozanimod&type=Intr&cond=Ulcerative+Colitis&intr=Ozanimod&phase=2&draw=2&rank=2.
  • 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.
  • D'Haens G, Sandborn WJ, Feagan BG, et al. A review of activity indices and efficacy end points for clinical trials of medical therapy in adults with ulcerative colitis. Gastroenterology. 2007;132(2):763–786.
  • Turner D, Ricciuto A, Lewis A, et al. STRIDE-II: an update on the Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE) initiative of the International Organization for the Study of IBD (IOIBD): determining therapeutic goals for treat-to-target strategies in IBD. Gastroenterology. 2021;160(5):1570–1583.
  • Shah SC, Colombel JF, Sands BE, et al. Mucosal healing is associated with improved long-term outcomes of patients with ulcerative colitis: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2016;14(9):1245–1255.e8.
  • Pai RK, Hartman DJ, Rivers CR, et al. Complete resolution of mucosal neutrophils associates with improved long-term clinical outcomes of patients with ulcerative colitis. Clin Gastroenterol Hepatol. 2020;18(11):2510–2517.e5.
  • Bryant RV, Burger DC, Delo J, et al. Beyond endoscopic mucosal healing in UC: histological remission better predicts corticosteroid use and hospitalisation over 6 years of follow-up. Gut. 2016;65(3):408–414.
  • Mazzuoli S, Guglielmi FW, Antonelli E, et al. Definition and evaluation of mucosal healing in clinical practice. Dig Liver Dis. 2013;45(12):969–977.
  • Boal Carvalho P, Cotter J. Mucosal healing in ulcerative colitis: a comprehensive review. Drugs. 2017;77(2):159–173.
  • Aniwan S, Bruining DH, Park SH, et al. The combination of patient-reported clinical symptoms and an endoscopic score correlates well with health-related quality of life in patients with ulcerative colitis. J Clin Med. 2019;8(8):1171.
  • Barreiro-de Acosta M, Vallejo N, de la Iglesia D, et al. Evaluation of the risk of relapse in ulcerative colitis according to the degree of mucosal healing (Mayo 0 vs 1): a longitudinal cohort study. J Crohns Colitis. 2016;10(1):13–19.
  • Boal Carvalho P, Dias de Castro F, Rosa B, et al. Mucosal healing in ulcerative colitis—when zero is better. J Crohns Colitis. 2016;10(1):20–25.
  • Cushing KC, Tan W, Alpers DH, et al. Complete histologic normalisation is associated with reduced risk of relapse among patients with ulcerative colitis in complete endoscopic remission. Aliment Pharmacol Ther. 2020;51(3):347–355.
  • Fukuda T, Naganuma M, Sugimoto S, et al. Efficacy of therapeutic intervention for patients with an ulcerative colitis Mayo endoscopic score of 1. Inflamm Bowel Dis. 2019;25(4):782–788.
  • 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.
  • Kim JH, Cheon JH, Park Y, et al. Effect of mucosal healing (Mayo 0) on clinical relapse in patients with ulcerative colitis in clinical remission. Scand J Gastroenterol. 2016;51(9):1069–1074.
  • 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(10):998–1004.
  • Leung CM, Tang W, Kyaw M, et al. Endoscopic and histological mucosal healing in ulcerative colitis in the first year of diagnosis: results from a population-based inception cohort from six countries in Asia. J Crohns Colitis. 2017;11(12):1440–1448.
  • Lobatón T, Bessissow T, Ruiz-Cerulla A, et al. Prognostic value of histological activity in patients with ulcerative colitis in deep remission: a prospective multicenter study. United European Gastroenterol J. 2018;6(5):765–772.
  • Osterman MT, Scott FI, Fogt FF, et al. Endoscopic and histological assessment, correlation, and relapse in clinically quiescent ulcerative colitis (MARQUEE). Inflamm Bowel Dis. 2021;27(2):207–214.
  • 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.
  • Ramos L, De La Barreda R, Carrillo-Palau M, et al. Risk of relapse according to endoscopic score of mucosal healing (Mayo score 0 vs 1): clinical evaluation is still necessary [abstract P256]. J Crohns Colitis. 2018;12(supplement_1):S229–S230.
  • Muñoz Villafranca C, Rodríguez MTB, de Zárate JO, et al. Clinical outcome after discontinuation of infliximab in patients with ulcerative colitis in deep remission. Gastroenterol Hepatol. 2016;39(7):442–448.
  • Yamamoto T, Shimoyama T, Umegae S. Impacts of mucosal healing on clinical outcomes in patients with refractory ulcerative colitis on tacrolimus or biologics. Presented at the 12th Congress of ECCO-Inflammatory Bowel Diseases 2017. Barcelona, Spain.
  • Yamamoto T, Shimoyama T, Umegae S, et al. Endoscopic score vs. fecal biomarkers for predicting relapse in patients with ulcerative colitis after clinical remission and mucosal healing. Clin Transl Gastroenterol. 2018;9(3):136.
  • Kevans D, Kirsch R, Dargavel C, et al. Histological markers of clinical relapse in endoscopically quiescent ulcerative colitis. Inflamm Bowel Dis. 2020;26(11):1722–1729.
  • Nakarai A, Kato J, Hiraoka S, et al. An elevated platelet count increases the risk of relapse in ulcerative colitis patients with mucosal healing. Gut Liver. 2018;12(4):420–425.
  • Yokoyama K, Kobayashi K, Mukae M, et al. Clinical study of the relation between mucosal healing and long-term outcomes in ulcerative colitis. Gastroenterol Res Pract. 2013;2013:192794.
  • Frieri G, Galletti B, Di Ruscio M, et al. The prognostic value of histology in ulcerative colitis in clinical remission with mesalazine. Therap Adv Gastroenterol. 2017;10(10):749–759.
  • Theede K, Kiszka-Kanowitz M, Nordgaard-Lassen I, et al. The impact of endoscopic inflammation and mucosal healing on health-related quality of life in ulcerative colitis patients. J Crohns Colitis. 2015;9(8):625–632.
  • Bessissow T, Lemmens B, Ferrante M, et al. Prognostic value of serologic and histologic markers on clinical relapse in ulcerative colitis patients with mucosal healing. Am J Gastroenterol. 2012;107(11):1684–1692.
  • 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(6):483–489.e3.
  • Naganuma M, Hirai F, Kobayashi K, et al. Middle-term prognosis in patients with ulcerative colitis who achieved clinical and endoscopic remission by budesonide rectal foam. PLoS One. 2019;14(8):e0220413.
  • 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.
  • Mosli MH, Feagan BG, Zou G, et al. Development and validation of a histological index for UC. Gut. 2017;66(1):50–58.
  • Stark RG, Reitmeir P, Leidl R, et al. Validity, reliability, and responsiveness of the EQ-5D in inflammatory bowel disease in Germany. Inflamm Bowel Dis. 2010;16(1):42–51.
  • Travis S, Feagan BG, Peyrin-Biroulet L, et al. Effect of adalimumab on clinical outcomes and health-related quality of life among patients with ulcerative colitis in a clinical practice setting: results from InspirADA. J Crohns Colitis. 2017;11(11):1317–1325.

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