Looking beyond symptom relief: Evolution of mucosal healing in inflammatory bowel disease

Therapeutic Advances in Gastroenterology

Volumn 4, Issue 2, 2011, Pages 129-143

  Iacucci, Marietta ^a   Ghosh, Subrata ^b  

^a SAN CAMILLO FORLANINI HOSPITAL   (Italy)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

Anti tumour necrosis factor therapy; Crohn's disease; Healing; Immunosuppressive drugs; Long term disease course; Mucosal ulcers; Remission; Ulcerative colitis

Indexed keywords

ADALIMUMAB; AMINOSALICYLIC ACID; ANTIBIOTIC AGENT; AZATHIOPRINE; BUDESONIDE; C REACTIVE PROTEIN; CALGRANULIN; CORTICOSTEROID; ENEMA; HEMOGLOBIN; INFLIXIMAB; INTERLEUKIN 6; LACTOFERRIN; MERCAPTOPURINE; MESALAZINE; METHOTREXATE; PREDNISOLONE; SOLUBLE INTERLEUKIN 2 RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANUS FISTULA; CAPSULE ENDOSCOPY; CLINICAL ASSESSMENT; CLINICAL ASSESSMENT TOOL; COLONOSCOPY; COMPUTER ASSISTED TOMOGRAPHY; CONFOCAL MICROSCOPY; CONTRAST ENHANCEMENT; CORTICOSTEROID THERAPY; CROHN DISEASE; CROHN DISEASE ACTIVITY INDEX; CROHN DISEASE ENDOSCOPIC INDEX OF SEVERITY; DIFFERENTIAL DIAGNOSIS; DIGESTIVE TRACT ENDOSCOPY; DISEASE CONTROL; DISEASE COURSE; DISEASE SEVERITY; DOUBLE BALLOON ENTEROSCOPY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; DRUG MEGADOSE; DRUG RESPONSE; ELEMENTAL DIET; ENDOSCOPY; ENTERIC FEEDING; ENTERITIS; ERYTHROCYTE SEDIMENTATION RATE; FECES LEVEL; GASTROINTESTINAL BIOPSY; GASTROINTESTINAL MUCOSA; HARVEY BRADSHAW INDEX; HEALING; HEMOGLOBIN BLOOD LEVEL; HISTOPATHOLOGY; HOSPITALIZATION; HUMAN; INTERMETHOD COMPARISON; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; INTESTINE RADIOGRAPHY; IRRITABLE BOWEL DISEASE QUALITY OF LIFE INDEX; IRRITABLE COLON; LAMINA PROPRIA; LEUKOCYTE COUNT; LEUKOCYTOSIS; MAINTENANCE THERAPY; MONOTHERAPY; MUCOSAL HEALING; NUCLEAR MAGNETIC RESONANCE IMAGING; OUTCOME ASSESSMENT; POWELL TUCK INDEX; PREDICTION; PRIORITY JOURNAL; QUALITY OF LIFE INDEX; RANDOMIZED CONTROLLED TRIAL (TOPIC); REMISSION; REVIEW; SENSITIVITY AND SPECIFICITY; SIMPLE CLINICAL COLITIS ACTIVITY INDEX; SIMPLIFIED ENDOSCOPIC SEVERITY INDEX FOR CROHN DISEASE; TABLET FORMULATION; ULCERATIVE COLITIS; ULCERATIVE COLITIS DISEASE ACTIVITY INDEX; UNSPECIFIED SIDE EFFECT;

EID: 79953327694     PISSN: 1756283X     EISSN: 17562848     Source Type: Journal    
DOI: 10.1177/1756283X11398930     Document Type: Review

References (62)

1. Agrawal A. Durrani S. Leiper K. Ellis A. Morris A.I. Rhodes J.M. (2005) Effect of systemic corticosteroid therapy on risk for intra-abdominal or pelvic abscess in non-operated Crohn's disease. Clin Gastroenterol Hepatol 3: 1215–1220.
2. Albert J.G. Martiny F. Krummenerl A. Stock K. Leßke J. Göbel C.M. et al (2005) Diagnosis of small bowel Crohn's disease: A prospective comparison of capsule endoscopy with magnetic resonance imaging and fluoroscopic enteroclysis. Gut 54: 1721–1727.
3. Baert F. Moortgat L. van Assche G. Caenepeel P. Vergauwe P. de Vos M. et al (2010) Mucosal healing predicts sustained clinical remission in patients with early-stage Crohn's disease. Gastroenterology 138: 463–468.
4. Bassi A. Dodd S. Williamson P. Bodger K. (2004) Cost of illness of inflammatory bowel disease in the UK: A single centre retrospective study. Gut 53: 1471–1478.
5. Best W.R. Becktel J.M. Singleton J.W. Kerm F. (1976) Development of Crohn's disease activity index. Gastroenterology 70: 439–444.
6. Caprilli R. Viscido A. Latella G. (2007) Current management of severe ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 4: 92–101.
7. Cellier C. Sahmoud T. Froguel E. Adenis A. Belaiche J. Bretagne J.F. et al (1994) Correlation between clinical activity, endoscopy, severity, and biological parameters in colonic and ileocolonic Crohn's disease. A prospective multicentre study of 121 cases. Groupe d'Etudes Therapeutiques des Affections Inflammatoires Digestives. Gut 35: 231–235.
8. Colombel J.F. Rutgeerts P. Sandborn W.J. Camez A. Pollack P. Chen N. et al (2010 a) Deep remission for adalimumab-treated patients with moderate to severe ileocolonic Crohn's disease: Results from EXTEND. J Crohn's Colitis 4: S10–S10.
9. Colombel J.F. Sandborn W.J. Reinisch W. Mantzaris G.J. Kornbluth A. Rachmilewitz D. et al (2010 b) Infliximab, azathioprine or combination therapy for Crohn's disease. N Engl J Med 362: 1383–1395.
10. Colombel J.F. Sandborn W.J. Rutgeerts P. Enns R. Hanauer S.B. Panaccione R. et al (2007) Adalimumab for maintenance of clinical response and remission in patients with Crohn's disease: The Charm Trial. Gastroenterology 132: 52–65.
11. Cosnes J. Cattan S. Blain A. Beaugerie L. Carbonnel F. Parc R. et al (2002) Long-term evolution of disease behavior of Crohn's disease. Inflamm Bowel Dis 8: 244–250.
12. Daperno M. D'Haens G. van Assche G. Baert F. Bulois P. Maunoury V. et al (2004) Development and validation of a new, simplified endoscopic activity score for Crohn's disease: The Ses-Cd. Gastrointest Endosc 60: 505–512.
13. Desmond A.N. O'Regan K. Curran C. McWilliams S. Fitzgerald T. Maher M.M. et al (2008) Crohn's disease: Factors associated with exposure to high levels of diagnostic radiation. Gut 57: 1524–1529.
14. D'Haens G. (1996.) Clinical and immunopathological characteristics of early recurrent Crohn's disease: In search of pathogenesis. Thesis, K.U. Leuven.
15. D'Haens G. Baert F. van Assche G. Caenepeel P. Vergauwe P. Tuynman H. et al (2008) Early combined immunosuppression or conventional management in patients with newly diagnosed Crohn's disease: An open randomized trial. Lancet 371: 660–667.
16. D'Haens G. Geboes K. Rutgeerts P. (1999) Endoscopic and histologic healing of Crohn's (ileo-) colitis with azathioprine. Gastrointest Endosc 50: 667–671.
17. Dignass, A.U., Bokemeyer, B., Adamek, H., Mross, M., Vinter-Jensen, L., Börner, N. et al. (2009) Mesalamine once daily is more effective than twice daily in patients with quiescent ulcerative colitis. Clin Gastroenterol Hepatol 7 (7): 762–769.
18. Floren C.H. Benoni C. William R. (1987) Histological and colonoscopy assessment of disease extension in ulcerative colitis. Scand J Gastroenterol 22: 459–462.
19. Froslie K.F. Jahnsen J. Moum B.A. Vatn M.H. (2007) Mucosal healing in inflammatory bowel disease: Results from a Norwegian population-based cohort. Gastroenterology 133: 412–422.
20. Geboes K. Riddell R. Ost A. Jensfelt B. Persson T. Lofberg R. (2000) A reproducible grading scale for histological assessment of inflammation in ulcerative colitis. Gut 47: 404–409.
21. Gomes P. Du Boulay C. Smith C.L. Holdstock G. (1986) Relationship between disease activity indices and colonoscopic findings in patients with colonic inflammatory bowel disease. Gut 27: 92–95.
22. Hanauer S.B. Sandborn W.J. Kornbluth A. Katz S. Safdi M. Woogen S. et al (2005) Delayed-release oral mesalamine at 4.8 g/day (800 mg tablet) for the treatment of moderately active ulcerative colitis: The Ascend II Trial. Am J Gastroenterol 100: 2478–2485.
23. Harvey R.F. Bradshaw J.M. (1980) A simple index of Crohn's-disease activity. Lancet 1: 514–514.
24. Hyams J. Crandall W. Kugathasan S. Griffiths A. Olson A. Johanns J. et al (2007) Induction and maintenance infliximab therapy for the treatment of moderate-to-severe Crohn's disease in children. Gastroenterology 132: 863–873, quiz 1165–1166.
25. Jones J. Loftus E.V. Jr Panaccione R. Chen L.S. Peterson S. McConnell J. et al (2008) Relationships between disease activity and serum and fecal biomarkers in patients with Crohn's disease. Clin Gastroenterol Hepatol 6: 1218–1224.
26. Kamm M.A. Sandborn W.J. Gassull M. Schreiber S. Jackowski L. Butler T. et al (2007) Once-daily, high-concentration MMX mesalamine in active ulcerative colitis. Gastroenterology 132: 66–75.
27. Kiesslich R. Goetz M. Angus E.M. Hu Q. Guan Y. Potten C. et al (2007) Identification of epithelial gaps in human small and large intestine by confocal endomicroscopy. Gastroenterology 133: 1769–1778.
28. Langhorst J. Elsenbruch S. Koelzer J. Rueffer A. Michalsen A. Dobos G.J. (2008) Noninvasive markers in the assessment of intestinal inflammation in inflammatory bowel diseases: Performance of fecal lactoferrin, calprotectin, and PMN-elastase, CRP, and clinical indices. Am J Gastroenterol 103: 162–169.
29. Lichtenstein G.R. Kamm M.A. Boddu P. Gubergrits N. Lyne A. Butler T. et al (2007) Effect of once- or twice-daily MMX mesalamine (Spd476) for the induction of remission of mild to moderately active ulcerative colitis. Clin Gastroenterol Hepatol 5: 95–102.
30. Makins, R. and Blanshard, C. (2006) Guidelines for capsule endoscopy: diagnoses will be missed. Aliment Pharmacol Ther 24 (2): 293–297.
31. Malchow H. Ewe K. Brandes J.W. Goebell H. Ehms H. Sommer H. et al (1984) European Cooperative Crohn's Disease Study (ECCDS): Results of drug treatment. Gastroenterology 86: 249–266.
32. Mary J.Y. Modigliani R. (1989) 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 30: 983–989.
33. Modigliani R. Mary J.Y. Simon J.F. Cortot A. Soule J.C. Gendre J.P. et al (1990) Clinical, biological, and endoscopic picture of attacks of Crohn's disease. Evolution on prednisolone. Groupe D'Etude Therapeutique Des Affections Inflammatoires Digestives. Gastroenterology 98: 811–818.
34. Moussata D. Goetz M. Watson A.J. Kerner M. Gloeckner A. Hoffman A. et al. (2009) Confocal laser endomicroscopy for the in vivo identification, localization and quantification of tissue based bacteria in patients with different types of colitis. Gastrointest Endosc 69: 131–131, abstract no.
35. Munkholm P. Langholz E. Davidsen M. Binder V. (1995) Disease activity courses in a regional cohort of Crohn's disease patients. Scand J Gastroenterol 30: 699–706.
36. Odze R. Antonioli D. Peppercorn M. Goldman H. (1993) Effect of topical 5-aminosalicylic acid (5-ASA) therapy on rectal mucosal biopsy morphology in chronic ulcerative colitis. Am J Surg Pathol 17: 869–875.
37. Powell-Tuck J. Bown R.L. Lennard-Jones J. (1978) A comparison of oral prednisolone given a single or multiple daily doses for active proctocolitis. Scand J Gastroenterol 13: 833–837.
38. Rutgeerts P.J. (2001) Review article: The limitations of corticosteroid therapy in Crohn's disease. Aliment Pharmacol Ther 15: 1515–1525.
39. Rutgeerts P. Feagan B.G. Lichtenstein G.R. Mayer L.F. Schreiber S. Colombel J.F. et al. (2004) Comparison of scheduled and episodic treatment strategies of infliximab in Crohn's disease. Gastroenterology 126: 402–413.
40. Rutgeerts P. Geboes K. Vantrappen G. Beyls J. Kerremans R. Hiele M. (1990) Predictability of the postoperative course of Crohn's disease. Gastroenterology 99: 956–963.
41. Rutgeerts P. Sandborn W.J. Feagan B.G. Reinisch W. Olson A. Johanns J. et al. (2005) Infliximab for induction and maintenance therapy for ulcerative colitis. N Engl J Med 353: 2462–2476.
42. Sandborn W.J. Kamm M.A. Lichtenstein G.R. Lyne A. Butler T. Joseph R.E. (2007) MMX Multi matrix system mesalazine for the induction of remission in patients with mild-to-moderate ulcerative colitis: A combined analysis of two randomized, double-blind, placebo-controlled trials. Aliment Pharmacol Ther 26: 205–215.
43. Sandborn W.J. Lofberg R. Feagan B.G. Hanauer S.B. Campieri M. Greenberg G.R. (2005) Budesonide for maintenance of remission in patients with Crohn's disease in medically induced remission: A predetermined pooled analysis of four randomized, double-blind, placebo-controlled trials. Am J Gastroenterol 100: 1780–1788.
44. Schmidt S. Lepori D. Meuwly J.Y. Duvoisin B. Meuli R. Michetti P. et al. (2003) Prospective comparison of MR enteroclysis with multidetector spiral-CT enteroclysis: Interobserver agreement and sensitivity by means of ‘sign-by-sign’ correlation. Eur Radiol 13: 1303–1311.
45. Schreiber S. Renisch W. Colombel J.F. Sandborn W.J. Hommes D.W. Li J. et al. (2007) Early Crohn's disease shows high levels of remission to therapy with adalimumab: Sub-analysis of CHARM. Gastroenterology 132(Suppl 1): A147 (abstract 985).
46. Schreiber S. Rosenstiel P. Albrecht M. Hampe J. Krawczak M. (2005) Genetics of Crohn disease, an archetypal inflammatory barrier disease. Nat Rev Genet 6: 376–388.
47. Schroeder K.W. Tremaine W.J. Ilstrup D.M. (1987) Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. N Engl J Med 317: 1625–1629.
48. Seo M. Okada M. Yao T. Ueki M. Arima S. Okumura M. (1992) An index of disease activity in patients with ulcerative colitis. Am J Gastroenterol 87: 971–976.
49. Siddiki H.A. Fidler J.L. Fletcher J.G. Burton S.S. Huprich J.E. Hough D.M. et al. (2009) Prospective comparison of state-of-the-art MR enterography and CT enterography in small-bowel Crohn's disease. AJR Am J Roentgenol 193: 113–121.
50. Solem C.A. Loftus E.V. Jr Tremaine W.J. Harmsen W.S. Zinsmeister A.R. Sandborn W.J. (2005) Correlation of C-reactive protein with clinical, endoscopic, histologic, and radiographic activity in inflammatory bowel disease. Inflamm Bowel Dis 11: 707–712.
51. Sutherland L. Singleton J. Sessions J. Hanauer S. Krawitt E. Rankin G. et al. (1991) Double blind, placebo controlled trial of metronidazole in Crohn's disease. Gut 32: 1071–1075.
52. Travis S.P. Stange E.F. Lemann M. Oresland T. Chowers Y. Forbes A. et al. (2006) European evidence based consensus on the diagnosis and management of Crohn's disease: Current management. Gut 55(Suppl 1): i16–i35.
53. Triester S.L. Leighton J.A. Leontiadis G.I. Gurudu S.R. Fleischer D.E. Hara A.K. et al. (2006) A meta-analysis of the yield of capsule endoscopy compared to other diagnostic modalities in patients with non-stricturing small bowel Crohn's disease. Am J Gastroenterol 101(5): 954–964.
54. Truelove S.C. Witts L.J. (1955) Cortisone in ulcerative colitis: Final report on a therapeutic trial. Br Med J 2: 1041–1048.
55. Turner J.R. (2006) Molecular basis of epithelial barrier regulation: From basic mechanisms to clinical application. Am J Pathol 169: 1901–1909.
56. Vermeire S. van Assche G. Rutgeers P. (2006) Laboratory markers in IBD: Useful, magic, or unnecessary toys? Gut 55: 426–431.
57. Vermeire S. van Assche G. Rutgeerts P. (2007) Review article: Altering the natural history of Crohn's disease – evidence for and against current therapies. Aliment Pharmacol Ther 25: 3–12.
58. Walmsley R.S. Ayres R.C. Pounder R.E. Allan R.N. (1998) A simple clinical colitis activity index. Gut 43: 29–32.
59. Watson A.J. Chu S. Sieck L. Gerasimenko O. Bullen T. Campbell F. et al. (2005) Epithelial barrier function in vivo is sustained despite gaps in epithelial layers. Gastroenterology 129: 902–912.
60. Wold P.B. Fletcher J.C. Johnson C.D. Sandborn W.J. (2003) Assessment of small bowel Crohn disease non invasive peroral CT enterography compared with other imaging methods and endoscopy – feasibility study. Radiology 229: 275–281.
61. Yamamoto T. Nakahigashi M. Umegae S. Kitagawa T. Matsumoto K. (2005) Impact of elemental diet on mucosal inflammation in patients with active Crohn's disease: Cytokine production and endoscopic and histological findings. Inflamm Bowel Dis 11: 580–588.
62. Zachos M. Tondeur M. Griffiths A.M. (2005) Enteral nutritional therapy for induction of remission in Crohn's disease. Inflamm Bowel Dis 11: 580–588.