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Endoscopic activity in inflammatory bowel disease: clinical significance and application in practice

  • Kyeong Ok Kim (Division of Gastroenterology and Hepatology, Department of Internal Medicine, Yeungnam University College of Medicine)
  • Received : 2022.03.27
  • Accepted : 2022.04.26
  • Published : 2022.07.30

Abstract

Endoscopy is vital for diagnosis, assessing treatment response, monitoring and surveillance in patients with inflammatory bowel disease (IBD). With the growing importance of mucosal healing as a treatment target, the assessment of disease activity by endoscopy has been accepted as the standard of care for IBD. There are many endoscopic activity indices for facilitating standardized reporting of the gastrointestinal mucosal appearance in IBD, and each index has its strengths and weaknesses. Although most endoscopic indices do not have a clear-cut validated definition, endoscopic remission or mucosal healing is associated with favorable outcomes, such as a decreased risk of relapse. Therefore, experts suggest utilizing endoscopic indices for monitoring disease activity and optimizing treatment to achieve remission. However, the regular monitoring of endoscopic activity is limited in practice owing to several factors, such as the complexity of the procedure, time consumption, inter-observer variability, and lack of a clear-cut, validated definition of endoscopic response or remission. Although experts have recently suggested consensus-based definitions, further studies are needed to define the values that can predict long-term outcomes.

Keywords

References

  1. Lee JS, Kim ES, Moon W. Chronological review of endoscopic indices in inflammatory bowel disease. Clin Endosc 2019;52:129-136. https://doi.org/10.5946/ce.2018.042
  2. Kim KO, Chiorean MV. Advanced neoplasia detection using chromoendoscopy and white light colonoscopy for surveillance in patients with inflammatory bowel disease. Intest Res 2020;18:438-446. https://doi.org/10.5217/ir.2019.00090
  3. Ham NS, Myung SJ. Endoscopic molecular imaging in inflammatory bowel disease. Intest Res 2021;19:33-44. https://doi.org/10.5217/ir.2019.09175
  4. Pokala A, Shen B. Update of endoscopic management of Crohn's disease strictures. Intest Res 2020;18:1-10. https://doi.org/10.5217/ir.2019.09158
  5. Colombel JF, 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. https://doi.org/10.1053/j.gastro.2011.06.054
  6. Modigliani R, Mary JY, Simon JF, et al. Clinical, biological, and endoscopic picture of attacks of Crohn's disease. Evolution on prednisolone. Groupe d'Etude Therapeutique des Affections Inflammatoires Digestives. Gastroenterology 1990;98:811-818. https://doi.org/10.1016/0016-5085(90)90002-I
  7. Rutgeerts P, Sandborn WJ, Feagan BG, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med 2005;353:2462-2476. https://doi.org/10.1056/NEJMoa050516
  8. Baars JE, Nuij VJ, Oldenburg B, et al. Majority of patients with inflammatory bowel disease in clinical remission have mucosal inflammation. Inflamm Bowel Dis 2012;18:1634-1640. https://doi.org/10.1002/ibd.21925
  9. Gomes P, du Boulay C, Smith CL, et al. Relationship between disease activity indices and colonoscopic findings in patients with colonic inflammatory bowel disease. Gut 1986;27:92-95. https://doi.org/10.1136/gut.27.1.92
  10. 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;5:477-483. https://doi.org/10.1016/j.crohns.2011.06.009
  11. Neurath MF, Travis SP. Mucosal healing in inflammatory bowel diseases: a systematic review. Gut 2012;61:1619-1635. https://doi.org/10.1136/gutjnl-2012-302830
  12. 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;160:1570-1583. https://doi.org/10.1053/j.gastro.2020.12.031
  13. Truelove SC, Witts LJ. Cortisone in ulcerative colitis; final report on a therapeutic trial. Br Med J 1955;2:1041-1048. https://doi.org/10.1136/bmj.2.4947.1041
  14. Fefferman DS, Farrell RJ. Endoscopy in inflammatory bowel disease: indications, surveillance, and use in clinical practice. Clin Gastroenterol Hepatol 2005;3:11-24.
  15. Schroeder KW, Tremaine WJ, Ilstrup DM. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. N Engl J Med 1987;317:1625-1629. https://doi.org/10.1056/NEJM198712243172603
  16. Christensen B, Rubin DT. Understanding endoscopic disease activity in IBD: how to incorporate it into practice. Curr Gastroenterol Rep 2016;18:5.
  17. Walsh A, Palmer R, Travis S. Mucosal healing as a target of therapy for colonic inflammatory bowel disease and methods to score disease activity. Gastrointest Endosc Clin N Am 2014;24:367-378. https://doi.org/10.1016/j.giec.2014.03.005
  18. D'Haens G, Feagan B, Colombel JF, et al. Challenges to the design, execution, and analysis of randomized controlled trials for inflammatory bowel disease. Gastroenterology 2012;143:1461-1469. https://doi.org/10.1053/j.gastro.2012.09.031
  19. Kamm MA, Sandborn WJ, Gassull M, et al. Once-daily, high-concentration MMX mesalamine in active ulcerative colitis. Gastroenterology 2007;132:66-75. https://doi.org/10.1053/j.gastro.2006.10.011
  20. Feagan BG, Sandborn WJ, D'Haens G, et al. The role of centralized reading of endoscopy in a randomized controlled trial of mesalamine for ulcerative colitis. Gastroenterology 2013;145:149-157. https://doi.org/10.1053/j.gastro.2013.03.025
  21. Lobaton T, Bessissow T, De Hertogh G, et al. The modified Mayo endoscopic score (MMES): a new index for the assessment of extension and severity of endoscopic activity in ulcerative colitis patients. J Crohns Colitis 2015;9:846-852. https://doi.org/10.1093/ecco-jcc/jjv111
  22. Travis SP, Schnell D, Krzeski P, et al. Developing an instrument to assess the endoscopic severity of ulcerative colitis: the Ulcerative Colitis Endoscopic Index of Severity (UCEIS). Gut 2012;61:535-542. https://doi.org/10.1136/gutjnl-2011-300486
  23. Travis SP, Schnell D, Krzeski P, et al. Reliability and initial validation of the ulcerative colitis endoscopic index of severity. Gastroenterology 2013;145:987-995. https://doi.org/10.1053/j.gastro.2013.07.024
  24. Tontini GE, Bisschops R, Neumann H. Endoscopic scoring systems for inflammatory bowel disease: pros and cons. Expert Rev Gastroenterol Hepatol 2014;8:543-554. https://doi.org/10.1586/17474124.2014.899899
  25. Cicero G, Mazziotti S. Crohn's disease at radiological imaging: focus on techniques and intestinal tract. Intest Res 2021;19:365-378. https://doi.org/10.5217/ir.2020.00097
  26. Hart L, Bessissow T. Endoscopic scoring systems for the evaluation and monitoring of disease activity in Crohn's disease. Best Pract Res Clin Gastroenterol 2019;38-39:101616.
  27. Mary JY, Modigliani R. Development and validation of an endoscopic index of the severity for Crohn's disease: a prospective multicentre study. Groupe d'Etudes Therapeutiques des Affections Inflammatoires du Tube Digestif (GETAID). Gut 1989;30:983-989. https://doi.org/10.1136/gut.30.7.983
  28. Annese V, Daperno M, Rutter MD, et al. European evidence based consensus for endoscopy in inflammatory bowel disease. J Crohns Colitis 2013;7:982-1018. https://doi.org/10.1016/j.crohns.2013.09.016
  29. 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;5:484-498. https://doi.org/10.1016/j.crohns.2011.07.003
  30. Daperno M, D'Haens G, Van Assche G, et al. Development and validation of a new, simplified endoscopic activity score for Crohn's disease: the SES-CD. Gastrointest Endosc 2004;60:505-512. https://doi.org/10.1016/S0016-5107(04)01878-4
  31. Rutgeerts P, Geboes K, Vantrappen G, et al. Natural history of recurrent Crohn's disease at the ileocolonic anastomosis after curative surgery. Gut 1984;25:665-672. https://doi.org/10.1136/gut.25.6.665
  32. Rutgeerts P, Geboes K, Vantrappen G, et al. Predictability of the postoperative course of Crohn's disease. Gastroenterology 1990;99:956-963. https://doi.org/10.1016/0016-5085(90)90613-6
  33. Sandborn WJ, Feagan BG, Hanauer SB, et al. A review of activity indices and efficacy endpoints for clinical trials of medical therapy in adults with Crohn's disease. Gastroenterology 2002;122:512-530. https://doi.org/10.1053/gast.2002.31072
  34. Domenech E, Manosa M, Bernal I, et al. Impact of azathioprine on the prevention of postoperative Crohn's disease recurrence: results of a prospective, observational, long-term follow-up study. Inflamm Bowel Dis 2008;14:508-513. https://doi.org/10.1002/ibd.20359
  35. Ollech JE, Aharoni-Golan M, Weisshof R, et al. Differential risk of disease progression between isolated anastomotic ulcers and mild ileal recurrence after ileocolonic resection in patients with Crohn's disease. Gastrointest Endosc 2019;90:269-275. https://doi.org/10.1016/j.gie.2019.01.029
  36. Corte C, Fernandopulle N, Catuneanu AM, et al. Association between the ulcerative colitis endoscopic index of severity (UCEIS) and outcomes in acute severe ulcerative colitis. J Crohns Colitis 2015;9:376-381. https://doi.org/10.1093/ecco-jcc/jjv047
  37. Allez M, Lemann M, Bonnet J, et al. Long term outcome of patients with active Crohn's disease exhibiting extensive and deep ulcerations at colonoscopy. Am J Gastroenterol 2002;97:947-953. https://doi.org/10.1016/S0002-9270(02)03970-9
  38. 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;14:1245-1255. https://doi.org/10.1016/j.cgh.2016.01.015
  39. Froslie KF, Jahnsen J, Moum BA, et al. Mucosal healing in inflammatory bowel disease: results from a Norwegian population-based cohort. Gastroenterology 2007;133:412-422. https://doi.org/10.1053/j.gastro.2007.05.051
  40. 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 Gastroenterol 2007;102:794-802. https://doi.org/10.1111/j.1572-0241.2007.01094.x
  41. 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. https://doi.org/10.1002/ibd.21838
  42. 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. https://doi.org/10.1016/j.cgh.2010.12.028
  43. Shah SC, Colombel JF, Sands BE, et al. Systematic review with meta- analysis: mucosal healing is associated with improved long-term outcomes in Crohn's disease. Aliment Pharmacol Ther 2016;43:317-333. https://doi.org/10.1111/apt.13475
  44. Baert F, Moortgat L, Van Assche G, et al. Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn's disease. Gastroenterology 2010;138:463-468. https://doi.org/10.1053/j.gastro.2009.09.056
  45. Rutgeerts P, Diamond RH, Bala M, et al. Scheduled maintenance treatment with infliximab is superior to episodic treatment for the healing of mucosal ulceration associated with Crohn's disease. Gastrointest Endosc 2006;63:433-442. https://doi.org/10.1016/j.gie.2005.08.011
  46. Rutgeerts P, Feagan BG, Lichtenstein GR, et al. Comparison of scheduled and episodic treatment strategies of infliximab in Crohn's disease. Gastroenterology 2004;126:402-413. https://doi.org/10.1053/j.gastro.2003.11.014
  47. Solberg IC, Lygren I, Jahnsen J, et al. Clinical course during the first 10 years of ulcerative colitis: results from a population-based inception cohort (IBSEN Study). Scand J Gastroenterol 2009;44:431-440. https://doi.org/10.1080/00365520802600961
  48. Rutter M, Saunders B, Wilkinson K, et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology 2004;126:451-459. https://doi.org/10.1053/j.gastro.2003.11.010
  49. Rutter MD, Saunders BP, Wilkinson KH, et al. Thirty-year analysis of a colonoscopic surveillance program for neoplasia in ulcerative colitis. Gastroenterology 2006;130:1030-1038. https://doi.org/10.1053/j.gastro.2005.12.035
  50. Ikeya K, Hanai H, Sugimoto K, et al. The ulcerative colitis endoscopic index of severity more accurately reflects clinical outcomes and longterm prognosis than the Mayo endoscopic score. J Crohns Colitis 2016;10:286-295. https://doi.org/10.1093/ecco-jcc/jjv210
  51. Vuitton L, Peyrin-Biroulet L, Colombel JF, et al. Defining endoscopic response and remission in ulcerative colitis clinical trials: an international consensus. Aliment Pharmacol Ther 2017;45:801-813. https://doi.org/10.1111/apt.13948
  52. Vuitton L, Marteau P, Sandborn WJ, et al. IOIBD technical review on endoscopic indices for Crohn's disease clinical trials. Gut 2016;65:1447-1455. https://doi.org/10.1136/gutjnl-2015-309903
  53. Ferrante M, Colombel JF, Sandborn WJ, et al. Validation of endoscopic activity scores in patients with Crohn's disease based on a post hoc analysis of data from SONIC. Gastroenterology 2013;145:978-986. https://doi.org/10.1053/j.gastro.2013.08.010
  54. Bouguen G, Levesque BG, Pola S, et al. Feasibility of endoscopic assessment and treating to target to achieve mucosal healing in ulcerative colitis. Inflamm Bowel Dis 2014;20:231-239. https://doi.org/10.1097/01.MIB.0000437985.00190.aa
  55. 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;10:13-19. https://doi.org/10.1093/ecco-jcc/jjv158
  56. Bouguen G, Levesque BG, Pola S, et al. Endoscopic assessment and treating to target increase the likelihood of mucosal healing in patients with Crohn's disease. Clin Gastroenterol Hepatol 2014;12:978-985. https://doi.org/10.1016/j.cgh.2013.11.005
  57. 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;25:782-788.  https://doi.org/10.1093/ibd/izy300