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Maneuvering Clinical Pathways for Ulcerative Colitis

  • Christopher M. Johnson
  • Catherine D. Linzay
  • Themistocles DassopoulosEmail author
Inflammatory Bowel Disease (S Hanauer, Section Editor)
  • 100 Downloads
Part of the following topical collections:
  1. Topical Collection on Inflammatory Bowel Disease

Abstract

Purpose of Review

Recent years have brought about several advances in the treatment of patients with ulcerative colitis (UC). Here, we discuss salient recommendations of recent treatment guidelines; review the efficacy, safety, and real-world data of vedolizumab and tofacitinib; appraise their place vis-à-vis established agents; and consider the newly proposed approaches of risk-stratified and treat-to-target therapy.

Recent Findings

Once daily oral mesalamine dosing is equivalent to split dosing in mild–moderate UC. Real-world data are accumulating on the effectiveness and safety of vedolizumab for moderate to severe UC, while there are few such data on the most recently approved agent, tofacitinib. High-dose infliximab is being investigated for severe UC. New approaches are challenging the established paradigm of selecting therapy based on current disease activity. The risk-stratified approach incorporates long-term risk as well as the current burden of inflammation. The treat-to-target approach aims at improved long-term outcomes by adjusting therapy to resolve intestinal inflammation.

Summary

The therapeutic options for UC are continually expanding. Risk-stratified therapy and the treat-to-target approach represent paradigm shifts in UC management. Optimal disease control requires an individualized approach that takes into consideration current inflammatory burden, long-term risk, patient preferences, and ongoing assessment of response to treatment.

Keywords

Ulcerative colitis Inflammatory bowel disease Vedolizumab Tofacitinib 

Notes

Compliance with Ethical Standards

Conflict of Interest

Christopher M. Johnson, Catherine D. Linzay, and Themistocles Dassopoulos declare no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Rutgeerts P, Sandborn WJ, Feagan BG, Reinisch W, Olson A, Johanns J, et al. Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2005;353(23):2462–76.CrossRefPubMedGoogle Scholar
  2. 2.
    Shah SC, Colombel JF, Sands BE, Narula N. 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):1245–55.CrossRefPubMedGoogle Scholar
  3. 3.
    Harbord M, Eliakim R, Bettenworth D, Karmiris K, Katsanos K, Kopylov U, et al. Third European Evidence-based Consensus on Diagnosis and Management of Ulcerative Colitis. Part 2: current management. J Crohns Colitis. 2017;11(7):769–84.CrossRefPubMedGoogle Scholar
  4. 4.
    •• Rubin DT, Ananthakrishnan AN, Siegel CA, Sauer BG, Long MD. ACG clinical guideline: ulcerative colitis in adults. Am J Gastroenterol. 2019;114(3):384–413 ACG guidelines on the management of UC. CrossRefPubMedGoogle Scholar
  5. 5.
    •• Ko CW, Singh S, Feuerstein JD, et al. AGA clinical practice guidelines on the management of mild-to-moderate ulcerative colitis. Gastroenterology. 2019;156(3):748–64 AGA guidelines on induction therapy for mild-to-moderate UC. CrossRefPubMedGoogle Scholar
  6. 6.
    Singh S, Feuerstein JD, Binion DG, Tremaine WJ. AGA technical review on the management of mild-to-moderate ulcerative colitis. Gastroenterology. 2019;156(3):769–808.CrossRefPubMedGoogle Scholar
  7. 7.
    Dassopoulos T, Cohen RD, Scherl EJ, Schwartz RM, Kosinski L, Regueiro MD. Ulcerative colitis care pathway. Gastroenterology. 2015;149(1):238–45.CrossRefPubMedGoogle Scholar
  8. 8.
    Suzuki Y, Iida M, Ito H, Nishino H, Ohmori T, Arai T, et al. 2.4 g mesalamine (Asacol 400 mg tablet) once daily is as effective as three times daily in maintenance of remission in ulcerative colitis: a randomized, noninferiority, multi-center trial. Inflamm Bowel Dis. 2017;23(5):822–32.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Kane SV. Systematic review: adherence issues in the treatment of ulcerative colitis. Aliment Pharmacol Ther. 2006;23(5):577–85.CrossRefPubMedGoogle Scholar
  10. 10.
    Testa A, Castiglione F, Nardone OM, Colombo GL. Adherence in ulcerative colitis: an overview. Patient Prefer Adherence. 2017;11:297–303.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Sandborn WJ, Travis S, Moro L, Jones R, Gautille T, Bagin R, et al. Once-daily budesonide MMX® extended-release tablets induce remission in patients with mild to moderate ulcerative colitis: results from the CORE I study. Gastroenterology. 2012;143(5):1218–26.CrossRefPubMedGoogle Scholar
  12. 12.
    Travis SP, Danese S, Kupcinskas L, Alexeeva O, D’Haens G, Gibson PR, et al. Once-daily budesonide MMX in active, mild-to-moderate ulcerative colitis: results from the randomised CORE II study. Gut. 2014;63(3):433–41.CrossRefPubMedGoogle Scholar
  13. 13.
    Rubin DT, Cohen RD, Sandborn WJ, Lichtenstein GR, Axler J, Riddell RH, et al. Budesonide multimatrix is efficacious for mesalamine-refractory, mild to moderate ulcerative colitis: a randomised, placebo-controlled trial. J Crohns Colitis. 2017;11(7):785–91.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Magro F, Gionchetti P, Eliakim R, Ardizzone S, Armuzzi A, Barreiro-de Acosta M, et al. 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. 2017;11(6):649–70.CrossRefGoogle Scholar
  15. 15.
    D’Albasio G, Pacini F, Camarri E, et al. Combined therapy with 5-aminosalicylic acid tablets and enemas for maintaining remission in ulcerative colitis: a randomized double-blind study. Am J Gastroenterol. 1997;92(7):1143–7.PubMedGoogle Scholar
  16. 16.
    Yokoyama H, Takagi S, Kuriyama S, Takahashi S, Takahashi H, Iwabuchi M, et al. Effect of weekend 5-aminosalicylic acid (mesalazine) enema as maintenance therapy for ulcerative colitis: results from a randomized controlled study. Inflamm Bowel Dis. 2007;13(9):1115–20.CrossRefPubMedGoogle Scholar
  17. 17.
    • Ungaro RC, Limketkai BN, Jensen CB, Allin KH, Agrawal M, Ullman T, et al. Stopping 5-aminosalicylates in patients with ulcerative colitis starting biologic therapy does not increase the risk of adverse clinical outcomes: analysis of two nationwide population-based cohorts. Gut. 2019;68(6):977–84 5-ASA therapy provides no benefits after patients have been escalated to biologic therapy. CrossRefPubMedGoogle Scholar
  18. 18.
    Singh S, Proudfoot JA, Dulai PS, Jairath V, Fumery M, Xu R, et al. No benefit of concomitant 5-aminosalicylates in patients with ulcerative colitis escalated to biologic therapy: pooled analysis of individual participant data from clinical trials. Am J Gastroenterol. 2018;113(8):1197–205.CrossRefPubMedGoogle Scholar
  19. 19.
    Ma C, Kotze PG, Almutairdi A, Jairath V, Panaccione R. Concomitant use of aminosalicylates is not associated with improved outcomes in patients with ulcerative colitis escalated to vedolizumab [published online ahead of print December 7, 2018]. Clin Gastroenterol Hepatol.Google Scholar
  20. 20.
    Hindryckx P, Novak G, Vande Casteele N, Laukens D, Parker C, Shackelton LM, et al. Review article: dose optimisation of infliximab for acute severe ulcerative colitis. Aliment Pharmacol Ther. 2017;45(5):617–30.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Choy MC, Seah D, Faleck DM, Shah SC, Chao CY, An YK, et al. Systematic review and meta-analysis: optimal salvage therapy in acute severe ulcerative colitis. Inflamm Bowel Dis. 2019 Jun 18;25(7):1169–86.CrossRefPubMedGoogle Scholar
  22. 22.
    Nalagatla N, Falloon K, Tran G, Borren NZ, Avalos D, Luther J, et al. Effect of accelerated infliximab induction on short- and long-term outcomes of acute severe ulcerative colitis: a retrospective multicenter study and meta-analysis. Clin Gastroenterol Hepatol. 2019;17(3):502–9.CrossRefPubMedGoogle Scholar
  23. 23.
    Zeissig S, Rosati E, Dowds CM, Aden K, Bethge J, Schulte B, et al. Vedolizumab is associated with changes in innate rather than adaptive immunity in patients with inflammatory bowel disease. Gut. 2019;68(1):25–39.CrossRefPubMedGoogle Scholar
  24. 24.
    Rosario M, Dirks NL, Milch C, Parikh A, Bargfrede M, Wyant T, et al. A review of the clinical pharmacokinetics, pharmacodynamics, and immunogenicity of vedolizumab. Clin Pharmacokinet. 2017;56(11):1287–301.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Rosario M, Dirks NL, Gastonguay MR, Fasanmade AA, Wyant T, Parikh A, et al. Population pharmacokinetics-pharmacodynamics of vedolizumab in patients with ulcerative colitis and Crohn’s disease. Aliment Pharmacol Ther. 2015;42(2):188–202.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Feagan BG, Rutgeerts P, Sands BE, Hanauer S, Colombel JF, Sandborn WJ, et al. Vedolizumab as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2013;369(8):699–710.CrossRefPubMedGoogle Scholar
  27. 27.
    • Colombel J, Sands B, Rutgeerts P, et al. The safety of vedolizumab for ulcerative colitis and Crohn’s disease. Gut. 2017;66(5):839–51 A large study demonstrating a low incidence of serious infections on vedolizumab. CrossRefPubMedGoogle Scholar
  28. 28.
    Meserve J, Aniwan S, Koliani-Pace JL, Shashi P, Weiss A, Faleck D, et al. Retrospective analysis of safety of vedolizumab in patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol. 2019;17(8):1533–40.CrossRefPubMedGoogle Scholar
  29. 29.
    Mahadevan U, Vermeire S, Lasch K, Abhyankar B, Bhayat F, Blake A, et al. Vedolizumab exposure in pregnancy: outcomes from clinical studies in inflammatory bowel disease. Aliment Pharmacol Ther. 2017;45(7):941–50.CrossRefPubMedGoogle Scholar
  30. 30.
    Moens A, Van Hoeve K, Humblet E, et al. Outcome of pregnancies in female patients with inflammatory bowel diseases treated with vedolizumab. J Crohns Colitis. 2019;13(1):12–8.CrossRefPubMedGoogle Scholar
  31. 31.
    Bar-Gil Shitrit A, Ben Ya’acov A, Livovsky DM, et al. Exposure to vedolizumab in IBD pregnant women appears of low risk for mother and neonate: a first prospective comparison study. Am J Gastroenterol. 2019;114(7):1172–5.CrossRefPubMedGoogle Scholar
  32. 32.
    Mahadevan U, Robinson C, Bernasko N, Boland B, Chambers C, Dubinsky M, et al. Inflammatory bowel disease in pregnancy clinical care pathway: a report from the American Gastroenterological Association IBD Parenthood Project Working Group. Gastroenterology. 2019;156(5):1508–24.CrossRefPubMedGoogle Scholar
  33. 33.
    • Narula N, Peerani F, Meserve J, et al. Vedolizumab for ulcerative colitis: treatment outcomes from the VICTORY consortium. Am J Gastroenterol. 2018;113(9):1345 Real-world data on effectiveness and safety of vedolizumab in UC. CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Chaparro M, Garre A, Ricart E, Iborra M, Mesonero F, Vera I, et al. Short and long-term effectiveness and safety of vedolizumab in inflammatory bowel disease: results from the ENEIDA registry. Aliment Pharmacol Ther. 2018;48(8):839–51.CrossRefPubMedGoogle Scholar
  35. 35.
    Rosario M, French JL, Dirks NL, Sankoh S, Parikh A, Yang H, et al. Exposure-efficacy relationships for vedolizumab induction therapy in patients with ulcerative colitis or Crohn’s disease. J Crohns Colitis. 2017;11(8):921–9.CrossRefPubMedGoogle Scholar
  36. 36.
    Peyrin-biroulet L, Danese S, Argollo M, et al. Loss of response to vedolizumab and ability of dose intensification to restore response in patients with Crohn’s disease or ulcerative colitis: a systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2019;17(5):838–46.CrossRefPubMedGoogle Scholar
  37. 37.
    Kotze PG, Ma C, Almutairdi A, al-Darmaki A, Devlin SM, Kaplan GG, et al. Real-world clinical, endoscopic and radiographic efficacy of vedolizumab for the treatment of inflammatory bowel disease. Aliment Pharmacol Ther. 2018;48(6):626–37.CrossRefPubMedGoogle Scholar
  38. 38.
    Feagan BG, Lasch K, Lissoos T, Cao C, Wojtowicz AM, Khalid JM, et al. Rapid response to vedolizumab therapy in biologic-naive patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol. 2019;17(1):130–8.CrossRefPubMedGoogle Scholar
  39. 39.
    Dulai PS, Boland BS, Singh S, Chaudrey K, Koliani-Pace JL, Kochhar G, et al. Development and validation of a scoring system to predict outcomes of vedolizumab treatment in patients with Crohn’s disease. Gastroenterology. 2018;155(3):687–95.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Osterman MT, Rosario M, Lasch K, Barocas M, Wilbur JD, Dirks NL, et al. Vedolizumab exposure levels and clinical outcomes in ulcerative colitis: determining the potential for dose optimisation. Aliment Pharmacol Ther. 2019;49(4):408–18.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Dubinsky MC, Cross RK, Sandborn WJ, et al. Extraintestinal manifestations in vedolizumab and anti-TNF-treated patients with inflammatory bowel disease. Inflamm Bowel Dis. 2018.Google Scholar
  42. 42.
    Feagan BG, Sandborn WJ, Colombel JF, Byrne SO, Khalid JM, Kempf C, et al. Incidence of arthritis/arthralgia in inflammatory bowel disease with long-term vedolizumab treatment: post hoc analyses of the GEMINI trials. J Crohns Colitis. 2019;13(1):50–7.CrossRefPubMedGoogle Scholar
  43. 43.
    Ferrante M, de Buck van Overstraeten A, Schils N, et al. Perioperative use of vedolizumab is not associated with postoperative infectious complications in patients with ulcerative colitis undergoing colectomy. J Crohns Colitis. 2017;11(11):1353–61.CrossRefPubMedGoogle Scholar
  44. 44.
    Lightner AL, Mckenna NP, Moncrief S, Pemberton JH, Raffals LE, Mathis KL. Surgical outcomes in vedolizumab-treated patients with ulcerative colitis. Inflamm Bowel Dis. 2017;23(12):2197–201.CrossRefPubMedGoogle Scholar
  45. 45.
    Yamada A, Komaki Y, Patel N, Komaki F, Aelvoet AS, Tran AL, et al. Risk of postoperative complications among inflammatory bowel disease patients treated preoperatively with vedolizumab. Am J Gastroenterol. 2017;112(9):1423–9.CrossRefPubMedGoogle Scholar
  46. 46.
    Adar T, Faleck D, Sasidharan S, Cushing K, Borren NZ, Nalagatla N, et al. Comparative safety and effectiveness of tumor necrosis factor α antagonists and vedolizumab in elderly IBD patients: a multicentre study. Aliment Pharmacol Ther. 2019;49(7):873–9.CrossRefPubMedGoogle Scholar
  47. 47.
    Danese S, Grisham M, Hodge J, Telliez JB. JAK inhibition using tofacitinib for inflammatory bowel disease treatment: a hub for multiple inflammatory cytokines. Am J Physiol Gastrointest Liver Physiol. 2016;310(3):G155–62.CrossRefPubMedGoogle Scholar
  48. 48.
    Xeljanz highlights of prescribing information. Available at: http://labeling.pfizer.com/ShowLabeling.aspx?id=959. Accessed July 14, 2019.
  49. 49.
    •• Sandborn WJ, Su C, Sands BE, et al. Tofacitinib as induction and maintenance therapy for ulcerative colitis. N Engl J Med. 2017;376(18):1723–36 OCTAVE induction and maintenance trials. CrossRefPubMedGoogle Scholar
  50. 50.
    Hanauer S, Panaccione R, Danese S, Cheifetz A, Reinisch W, Higgins PDR, et al. Tofacitinib induction therapy reduces symptoms within 3 days for patients with ulcerative colitis. Clin Gastroenterol Hepatol. 2019;17(1):139–47.CrossRefPubMedGoogle Scholar
  51. 51.
    Sandborn WJ, Panés J, D’Haens GR, et al. Safety of tofacitinib for treatment of ulcerative colitis, based on 4.4 years of data from global clinical trials. Clin Gastroenterol Hepatol. 2019;17(8):1541–50.CrossRefPubMedGoogle Scholar
  52. 52.
    Colombel JF. Herpes zoster in patients receiving JAK inhibitors for ulcerative colitis: mechanism, epidemiology, management, and prevention. Inflamm Bowel Dis. 2018;24(10):2173–82.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Winthrop KL, Melmed GY, Vermeire S, Long MD, Chan G, Pedersen RD, et al. Herpes zoster infection in patients with ulcerative colitis receiving tofacitinib. Inflamm Bowel Dis. 2018;24(10):2258–65.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Sands BE, Taub PR, Armuzzi A, et al. Tofacitinib treatment is associated with modest and reversible increases in serum lipids in patients with ulcerative colitis. Clin Gastroenterol Hepatol. 2019.Google Scholar
  55. 55.
    Mahadevan U, Dubinsky MC, Su C, Lawendy N, Jones TV, Marren A, et al. Outcomes of pregnancies with maternal/paternal exposure in the tofacitinib safety databases for ulcerative colitis. Inflamm Bowel Dis. 2018;24(12):2494–500.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Verden A, Dimbil M, Kyle R, Overstreet B, Hoffman KB. Analysis of spontaneous postmarket case reports submitted to the FDA regarding thromboembolic adverse events and JAK inhibitors. Drug Saf. 2018;41(4):357–61.CrossRefPubMedGoogle Scholar
  57. 57.
  58. 58.
    Dooling KL, Guo A, Patel M, Lee GM, Moore K, Belongia EA, et al. Recommendations of the advisory committee on immunization practices for use of herpes zoster vaccines. MMWR Morb Mortal Wkly Rep. 2018;67(3):103–8.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Vink P, Ramon Torrell JM, Sanchez Fructuoso A, et al. Immunogenicity and safety of the adjuvanted recombinant zoster vaccine in chronically immunosuppressed adults following renal transplant: a phase III, randomized clinical trial. Clin Infect Dis. 2019.Google Scholar
  60. 60.
    Weisshof R, Aharoni Golan M, Sossenheimer PH, et al. Real-world experience with tofacitinib in IBD at a tertiary center. Dig Dis Sci. 2019;64(7):1945–51.CrossRefPubMedGoogle Scholar
  61. 61.
    Berinstein JA, Steiner CA, Regal RE, Allen JI, Kinnucan JAR, Stidham RW, et al. Efficacy of induction therapy with high-intensity tofacitinib in 4 patients with acute severe ulcerative colitis. Clin Gastroenterol Hepatol. 2019;17(5):988–90.CrossRefPubMedGoogle Scholar
  62. 62.
    Bauermann P, Heiligenhaus A, Heinz C. Effect of Janus kinase inhibitor treatment on anterior uveitis and associated macular edema in an adult patient with juvenile idiopathic arthritis. Ocul Immunol Inflamm. 2019:1–3.Google Scholar
  63. 63.
    Paley MA, Karacal H, Rao PK, Margolis TP, Miner JJ. Tofacitinib for refractory uveitis and scleritis. Am J Ophthalmol Case Rep. 2019;13:53–5.CrossRefPubMedGoogle Scholar
  64. 64.
    Kochar B, Herfarth N, Mamie C, Navarini AA, Scharl M, Herfarth HH. Tofacitinib for the treatment of pyoderma gangrenosum. Clin Gastroenterol Hepatol. 2019;17(5):991–3.CrossRefPubMedGoogle Scholar
  65. 65.
    Faleck D, Shashi P, Meserve J, et al. Comparative effectiveness of vedolizumab and TNF-antagonist therapy in ulcerative colitis: a multicentre consortium propensity score-matched analysis. J Crohns Colitis. 2018;12(Supplement_1):S019.CrossRefGoogle Scholar
  66. 66.
    Singh S, Fumery M, Sandborn WJ, Murad MH. Systematic review with network meta-analysis: first- and second-line pharmacotherapy for moderate-severe ulcerative colitis. Aliment Pharmacol Ther. 2018;47(2):162–75.CrossRefPubMedGoogle Scholar
  67. 67.
    •• Schreiber S, Peyrin-Biroulet L, Loftus EV, et al. VARSITY: a double-blind, double-dummy, randomised, controlled trial of vedolizumab versus adalimumab in patients with active ulcerative colitis. J Crohns Colitis. 2019;13(Supplement 1):S612–3 VARSITY trial demonstrated the superior efficacy of vedolizumab over adalimumab in UC. CrossRefGoogle Scholar
  68. 68.
    Wolf D, D’Haens G, Sandborn WJ, et al. Escalation to weekly dosing recaptures response in adalimumab-treated patients with moderately to severely active ulcerative colitis. Aliment Pharmacol Ther. 2014;40(5):486–97.PubMedGoogle Scholar
  69. 69.
    Black CM, Yu E, Mccann E, Kachroo S. Dose escalation and healthcare resource use among ulcerative colitis patients treated with adalimumab in English hospitals: an analysis of real-world data. PLoS One. 2016;11(2):e0149692.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Taxonera C, Iglesias E, Muñoz F, Calvo M, Barreiro-de Acosta M, Busquets D, et al. Adalimumab maintenance treatment in ulcerative colitis: outcomes by prior anti-TNF use and efficacy of dose escalation. Dig Dis Sci. 2017;62(2):481–90.CrossRefPubMedGoogle Scholar
  71. 71.
    Pöllinger B, Schmidt W, Seiffert A, Imhoff H, Emmert M. Costs of dose escalation among ulcerative colitis patients treated with adalimumab in Germany. Eur J Health Econ. 2019;20(2):195–203.CrossRefPubMedGoogle Scholar
  72. 72.
    Van de Vondel S, Baert F, Reenaers C, et al. Incidence and predictors of success of adalimumab dose escalation and de-escalation in ulcerative colitis: a real-world Belgian cohort study. Inflamm Bowel Dis. 2018;24(5):1099–105.CrossRefPubMedGoogle Scholar
  73. 73.
    •• 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):1324–38 Consensus statement on the treat-to-target paradigm. Google Scholar
  74. 74.
    Baars JE, Nuij VJ, Oldenburg B, Kuipers EJ, Van der Woude CJ. Majority of patients with inflammatory bowel disease in clinical remission have mucosal inflammation. Inflamm Bowel Dis. 2012;18(9):1634–40.CrossRefPubMedGoogle Scholar
  75. 75.
    Rosenberg L, Lawlor GO, Zenlea T, Goldsmith JD, Gifford A, Falchuk KR, et al. Predictors of endoscopic inflammation in patients with ulcerative colitis in clinical remission. Inflamm Bowel Dis. 2013;19(4):779–84.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Rutter M, Saunders B, Wilkinson K, Rumbles S, Schofield G, Kamm M, et al. Severity of inflammation is a risk factor for colorectal neoplasia in ulcerative colitis. Gastroenterology. 2004;126(2):451–9.CrossRefPubMedGoogle Scholar
  77. 77.
    Frøslie KF, Jahnsen J, Moum BA, Vatn MH. Mucosal healing in inflammatory bowel disease: results from a Norwegian population-based cohort. Gastroenterology. 2007;133(2):412–22.CrossRefPubMedGoogle Scholar
  78. 78.
    Ardizzone S, Cassinotti A, Duca P, Mazzali C, Penati C, Manes G, et al. Mucosal healing predicts late outcomes after the first course of corticosteroids for newly diagnosed ulcerative colitis. Clin Gastroenterol Hepatol. 2011;9(6):483–9.CrossRefPubMedGoogle Scholar
  79. 79.
    Colombel JF, Rutgeerts P, Reinisch W, Esser D, Wang Y, Lang Y, et al. Early mucosal healing with infliximab is associated with improved long-term clinical outcomes in ulcerative colitis. Gastroenterology. 2011;141(4):1194–201.CrossRefPubMedGoogle Scholar
  80. 80.
    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(3):367–78.CrossRefPubMedGoogle Scholar
  81. 81.
    Flores BM, O’Connor A, Moss AC. Impact of mucosal inflammation on risk of colorectal neoplasia in patients with ulcerative colitis: a systematic review and meta-analysis. Gastrointest Endosc. 2017;86(6):1006–11.CrossRefPubMedGoogle Scholar
  82. 82.
    Pai RK, Jairath V, Vande Casteele N, Rieder F, Parker CE, Lauwers GY. The emerging role of histologic disease activity assessment in ulcerative colitis. Gastrointest Endosc. 2018;88(6):887–98.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Christopher M. Johnson
    • 1
  • Catherine D. Linzay
    • 2
  • Themistocles Dassopoulos
    • 2
    • 3
    Email author
  1. 1.Baylor Scott and White Medical CenterBaylor Scott and White HealthTempleUSA
  2. 2.Baylor University Medical CenterBaylor Scott and White HealthDallasUSA
  3. 3.Baylor Scott and White Center for Inflammatory Bowel DiseasesDallasUSA

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