Positionspapier zur Befunderstellung endoskopischer Untersuchungen bei Patienten mit chronisch-entzündlichen Darmerkrankungen

Carsten Schmidt; Oliver Bachmann; Daniel C. Baumgart; Martin Goetz; Oliver Drvarov; Torsten F. Kucharzik; Tanja Kühbacher; Jost Langhorst; Jochen Maul; Wolfgang Mohl; Jonas Mudter; Michael Repp; Andreas Sturm; Dieter Witzemann; Raja Atreya

doi:10.1055/a-1504-9782

Zeitschrift für Gastroenterologie, Inhaltsverzeichnis

Z Gastroenterol 2021; 59(10): 1091-1109
DOI: 10.1055/a-1504-9782

Übersicht

Positionspapier zur Befunderstellung endoskopischer Untersuchungen bei Patienten mit chronisch-entzündlichen Darmerkrankungen

Position paper on endoscopic reporting in IBD

Carsten Schmidt

¹Medizinische Klinik II, Klinikum Fulda gAG, Fulda, Germany

²Medizinische Fakultät der Friedrich-Schiller-Universität Jena, Germany,

,

Oliver Bachmann

³Klinik für Innere Medizin 1, Siloah St. Trudpert Klinikum, Pforzheim, Germany

,

Daniel C. Baumgart

⁴Division of Gastroenterology, University of Alberta, Edmonton, Canada

,

Martin Goetz

⁵Innere Medizin IV, Klinikverbund Südwest GmbH, Böblingen, Germany

,

Oliver Drvarov

⁶Gastroenterologie Rahlstedt, Hamburg, Germany

,

Torsten F. Kucharzik

⁷Allgemeine Innere Medizin, Städtisches Klinikum Lüneburg, Lüneburg, Germany

,

Tanja Kühbacher

⁸Klinik für Innere Medizin, Diabetologie, Gastroenterologie, Pulmonologie, Tumormedizin und Palliativmedizin, medius Klinik Nürtingen, Nürtingen, Germany

,

Jost Langhorst

⁹Klinik für Integrative Medizin und Naturheilkunde, Klinikum Bamberg, Bamberg, Germany

¹⁰Lehrstuhl für Integrative Medizin Schwerpunkt translationale Gastroenterologie, Universität Duisburg-Essen, Duisburg-Essen, Germany

,

Jochen Maul

¹¹Gastroenterology, Gastroenterologie am Bayerischen Platz, Berlin, Germany

¹²Medizinische Klinik für Gastroenterologie, Infektiologie und Rheumatologie, Campus Benjamin Franklin, Charité Universitätsmedizin Berlin, Berlin, Germany

,

Wolfgang Mohl

¹³Zentrum für Gastroenterologie Saar MVZ GmbH Saarbrücken, Saarbrücken, Germany

,

Jonas Mudter

¹⁴Klinik für Gastroenterologie und Infektiologie, HELIOS Kliniken Schwerin, Schwerin, Germany

¹⁵Medizinische Klinik 1, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany

,

Michael Repp

¹⁶Zentrum für Innere Medizin, Klinik für Gastroenterologie/Hepatologie, Klinikum Altenburger Land GmbH, Altenburg, Germany

,

Andreas Sturm

¹⁷Klinik für Innere Medizin mit Schwerpunkt Gastroenterologie, DRK Kliniken Berlin Westend, Berlin, Germany (Ringgold ID: RIN38179)

,

Dieter Witzemann

¹⁸Praxis für Gastroenterologie, Unterschleißheim, Germany

,

Raja Atreya

¹⁵Medizinische Klinik 1, Universitätsklinikum Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany

› Institutsangaben

Abstract

Zusammenfassung

Die vollständige und reproduzierbare Erfassung und Dokumentation endoskopischer Befunde ist als Grundlage der Behandlung von Patienten mit chronisch entzündlichen Darmerkrankungen wie Morbus Crohn und Colitis ulcerosa von entscheidender Bedeutung. Diese Befunde sind zum einen Grundlage therapeutischer Entscheidungen und zum anderen ein unverzichtbarer Parameter der Bewertung des Ansprechens auf eine Behandlung. Endoskopische Befunde sollten daher nach standardisierten Kriterien erstellt werden, um eine Vergleichbarkeit der Befunde unterschiedlicher Untersucher wie auch die valide Erfassung von Veränderungen im zeitlichen Verlauf der Erkrankung zu gewährleisten. Vor diesem Hintergrund haben 15 Mitglieder der AG Bildgebung des Kompetenznetzes Darmerkrankungen ein Positionspapier erarbeitet, in dem eine Befundstruktur für die Dokumentation endoskopischer Untersuchungen entworfen wird. Die Empfehlungen adressieren neben den formalen Angaben zu jeder Untersuchung insbesondere eine Vielzahl von Attributen akuter und chronisch entzündlicher mukosaler Veränderungen sowie endoskopisch detektierbarer Komplikationen, die detailliert erläutert und anhand charakteristischer Abbildungen illustriert werden. Zudem werden häufiger verwendete endoskopische Aktivitätsindizes vorgestellt, und ihre Nutzung im klinischen Alltag wird diskutiert.

Abstract

The complete and reliable documentation of endoscopic findings make up the crucial foundation for the treatment of patients with inflammatory bowel diseases such as Crohn´s disease and ulcerative colitis. These findings are, on the one hand, a prerequisite for therapeutic decisions and, on the other hand, important as a tool for assessing the response to ongoing treatments. Endoscopic reports should, therefore, be recorded according to standardized criteria to ensure that the findings of different endoscopists can be adequately compared and that changes in the course of the disease can be traced back. In consideration of these necessities, fifteen members of the Imaging Working Group of the German Kompetenznetz Darmerkrankungen have created a position paper proposing a structure and specifications for the documentation of endoscopic exams. In addition to the formal report structure, the recommendations address a large number of attributes of acute and chronic inflammatory alterations as well as endoscopically detectable complications, which are explained in detail and illustrated using exemplary images. In addition, more frequently used endoscopic activity indices are presented and their use in everyday clinical practice is discussed.

Schlüsselwörter

Endoskopie - Gastroskopie - Koloskopie - Videokapselendoskopie - Enteroskopie - Terminologie - Morbus Crohn - Colitis ulcerosa - entzündliche Darmerkrankungen

Keywords

Endoscopy - gastroscopy - colonoscopy - video capsule endoscopy - enteroscopy - terminology - Crohn’s disease - ulcerative colitis - IBD

Volltext

Referenzen

Literatur
1 Bhangu A, Bowley DM, Horner R. et al. Volume and accreditation, but not specialty, affect quality standards in colonoscopy. Br J Surg 2012; 99: 1436-1444
2 Rogart JN, Siddiqui UD, Jamidar PA. et al. Fellow involvement may increase adenoma detection rates during colonoscopy. Am J Gastroenterol 2008; 103: 2841-2846
3 Adler A, Wegscheider K, Lieberman D. et al. Factors determining the quality of screening colonoscopy: a prospective study on adenoma detection rates, from 12,134 examinations (Berlin colonoscopy project 3, BECOP-3). Gut 2013; 62: 236-241
4 Diamond SJ, Enestvedt BK, Jiang Z. et al. Adenoma detection rate increases with each decade of life after 50 years of age. Gastrointest Endosc 2011; 74: 135-140
5 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
6 Bourreille A, Ignjatovic A, Aabakken L. et al. Role of small-bowel endoscopy in the management of patients with inflammatory bowel disease: an international OMED-ECCO consensus. Endoscopy 2009; 41: 618-637
7 Farraye FA, Waye JD, Moscandrew M. et al. Variability in the diagnosis and management of adenoma-like and non-adenoma-like dysplasia-associated lesions or masses in inflammatory bowel disease: an Internet-based study. Gastrointest Endosc 2007; 66: 519-529
8 Nett A, Velayos F, McQuaid K. Quality bowel preparation for surveillance colonoscopy in patients with inflammatory bowel disease is a must. Gastrointest Endosc Clin N Am 2014; 24: 379-392
9 Sint Nicolaas J, de Jonge V, van Baalen O. et al. Optimal resource allocation in colonoscopy: timing of follow-up colonoscopies in relation to adenoma detection rates. Endoscopy 2013; 45: 545-552
10 Williams JE, Faigel DO. Colonoscopy reports and current state of performance measures. Gastrointest Endosc Clin N Am 2010; 20: 685-697
11 Lai EJ, Calderwood AH, Doros G. et al. The Boston bowel preparation scale: a valid and reliable instrument for colonoscopy-oriented research. Gastrointest Endosc 2009; 69: 620-625
12 Serper M, Gawron AJ, Smith SG. et al. Patient factors that affect quality of colonoscopy preparation. Clin Gastroenterol Hepatol 2014; 12: 451-457
13 Barclay RL, Vicari JJ, Doughty AS. et al. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy. N Engl J Med 2006; 355: 2533-2541
14 Boroff ES, Gurudu SR, Hentz JG. et al. Polyp and adenoma detection rates in the proximal and distal colon. Am J Gastroenterol 2013; 108: 993-999
15 Francis DL, Rodriguez-Correa DT, Buchner A. et al. Application of a conversion factor to estimate the adenoma detection rate from the polyp detection rate. Gastrointest Endosc 2011; 73: 493-497
16 Kaminski MF, Regula J, Kraszewska E. et al. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med 2010; 362: 1795-1803
17 Leung FW. PDR or ADR as a quality indicator for colonoscopy. Am J Gastroenterol 2013; 108: 1000-1002
18 Jover R, Zapater P, Polania E. et al. Modifiable endoscopic factors that influence the adenoma detection rate in colorectal cancer screening colonoscopies. Gastrointest Endosc 2013; 77: 381-389 e381
19 Meining A, Schmidbaur W, Schumacher B. et al. The revised version of standard terminology in gastroenterological endoscopy – result of a consensus project of the german society for gastroenterology, digestive and metabolic diseases. Z Gastroenterol 2018; 56: e1
20 Devlin SM, Melmed GY, Irving PM. et al. Recommendations for Quality Colonoscopy Reporting for Patients with Inflammatory Bowel Disease: Results from a RAND Appropriateness Panel. Inflamm Bowel Dis 2016; 22: 1418-1424
21 Carman N, Tomalty D, Church PC. et al. Clinical disease activity and endoscopic severity correlate poorly in children newly diagnosed with Crohn’s disease. Gastrointest Endosc 2019; 89: 364-372
22 Preiß JC, Bokemeyer B, Buhr HJ. et al. Updated German clinical practice guideline on "Diagnosis and treatment of Crohn’s disease" 2014. Z Gastroenterol 2014; 52: 1431-1484
23 Crocco S, Martelossi S, Giurici N. et al. Upper gastrointestinal involvement in paediatric onset Crohn’s disease: prevalence and clinical implications. J Crohns Colitis 2012; 6: 51-55
24 Annunziata ML, Caviglia R, Papparella LG. et al. Upper gastrointestinal involvement of Crohn’s disease: a prospective study on the role of upper endoscopy in the diagnostic work-up. Dig Dis Sci 2012; 57: 1618-1623
25 Diaz L, Hernandez-Oquet RE, Deshpande AR. et al. Upper Gastrointestinal Involvement in Crohn Disease: Histopathologic and Endoscopic Findings. South Med J 2015; 108: 695-700
26 Magro F, Langner C, Driessen A. et al. European consensus on the histopathology of inflammatory bowel disease. J Crohns Colitis 2013; 7: 827-851
27 Thia KT, Sandborn WJ, Harmsen WS. et al. Risk factors associated with progression to intestinal complications of Crohn’s disease in a population-based cohort. Gastroenterology 2010; 139: 1147-1155
28 Jensen MD, Nathan T, Rafaelsen SR. et al. Diagnostic accuracy of capsule endoscopy for small bowel Crohn’s disease is superior to that of MR enterography or CT enterography. Clin Gastroenterol Hepatol 2011; 9: 124-129
29 Yadav A, Heigh RI, Hara AK. et al. Performance of the patency capsule compared with nonenteroclysis radiologic examinations in patients with known or suspected intestinal strictures. Gastrointest Endosc 2011; 74: 834-839
30 Levesque BG. Yield to diagnostic accuracy: capsule endoscopy in Crohn’s disease. Gastrointest Endosc 2010; 71: 128-130
31 Magro F, Gionchetti P, Eliakim R. 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: 649-670
32 Despott EJ, Gupta A, Burling D. et al. Effective dilation of small-bowel strictures by double-balloon enteroscopy in patients with symptomatic Crohn’s disease (with video). Gastrointest Endosc 2009; 70: 1030-1036
33 Peyrin-Biroulet L, Loftus EV, Colombel JF. et al. The natural history of adult Crohn’s disease in population-based cohorts. Am J Gastroenterol 2010; 105: 289-297
34 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
35 De Cruz P, Kamm MA, Hamilton AL. et al. Crohn’s disease management after intestinal resection: a randomised trial. Lancet 2015; 385: 1406-1417
36 Gomollon F, Dignass A, Annese V. et al. 3rd European Evidence-based Consensus on the Diagnosis and Management of Crohn’s Disease 2016: Part 1: Diagnosis and Medical Management. J Crohns Colitis 2017; 11: 3-25
37 Hernandez JD, Jimenez-Huyke C, Rosado K. et al. Surveillance for dysplasia in patients with ileal pouch-anal anastomosis for ulcerative colitis: an interim analysis. Dig Dis Sci 2010; 55: 2332-2336
38 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
39 Kudo T, Matsumoto T, Esaki M. et al. Mucosal vascular pattern in ulcerative colitis: observations using narrow band imaging colonoscopy with special reference to histologic inflammation. International journal of colorectal disease 2009; 24: 495-501
40 Iacucci M, Uraoka T, Fort Gasia M. et al. Novel diagnostic and therapeutic techniques for surveillance of dysplasia in patients with inflammatory bowel disease. Canadian journal of gastroenterology & hepatology 2014; 28: 361-370
41 Nishiyama S, Oka S, Tanaka S. et al. Clinical usefulness of narrow band imaging magnifying colonoscopy for assessing ulcerative colitis-associated cancer/dysplasia. Endoscopy international open 2016; 4: E1183-e1187
42 Paine ER. Colonoscopic evaluation in ulcerative colitis. Gastroenterol Rep (Oxf) 2014; 2: 161-168
43 Bailey JR, Whiting CV, Tarlton JF. et al. New insights on fibrosis in Crohn’s disease. Expert Rev Gastroenterol Hepatol 2013; 7: 497-499
44 Chan WPW, Mourad F, Leong RW. Crohn’s disease associated strictures. J Gastroenterol Hepatol 2018; 33: 998-1008
45 Gordon IO, Agrawal N, Willis E. et al. Fibrosis in ulcerative colitis is directly linked to severity and chronicity of mucosal inflammation. Aliment Pharmacol Ther 2018; 47: 922-939
46 Latella G, Di Gregorio J, Flati V. et al. Mechanisms of initiation and progression of intestinal fibrosis in IBD. Scand J Gastroenterol 2015; 50: 53-65
47 Lenti MV, Di Sabatino A. Intestinal fibrosis. Mol Aspects Med 2019; 65: 100-109
48 Maaser C, Sturm A, Vavricka SR. et al. ECCO-ESGAR Guideline for Diagnostic Assessment in IBD Part 1: Initial diagnosis, monitoring of known IBD, detection of complications. J Crohns Colitis 2019; 13: 144-164
49 Myren J, Eie H, Serck-Hanssen A. The diagnosis of colitis by colonoscopy with biopsy and X-ray examination. A blind comparative study. Scand J Gastroenterol 1976; 11: 141-144
50 Pera A, Bellando P, Caldera D. et al. Colonoscopy in inflammatory bowel disease. Diagnostic accuracy and proposal of an endoscopic score. Gastroenterology 1987; 92: 181-185
51 Yao T, Matsui T, Hiwatashi N. Crohn’s disease in Japan: diagnostic criteria and epidemiology. Diseases of the colon and rectum 2000; 43: S85-93
52 Bousvaros A, Antonioli DA, Colletti RB. et al. Differentiating ulcerative colitis from Crohn disease in children and young adults: report of a working group of the North American Society for Pediatric Gastroenterology, Hepatology, and Nutrition and the Crohn’s and Colitis Foundation of America. Journal of pediatric gastroenterology and nutrition 2007; 44: 653-674
53 Politis DS, Katsanos KH, Tsianos EV. et al. Pseudopolyps in inflammatory bowel diseases: Have we learned enough?. World J Gastroenterol 2017; 23: 1541-1551
54 Rezapour M, Quintero MA, Khakoo NS. et al. Reclassifying Pseudopolyps in Inflammatory Bowel Disease: Histologic and Endoscopic Description in the New Era of Mucosal Healing. Crohn’s & colitis 360 2019; 1: otz033
55 Mahmoud R, Shah SC, Ten Hove JR. et al. No Association Between Pseudopolyps and Colorectal Neoplasia in Patients With Inflammatory Bowel Diseases. Gastroenterology 2019; 156: 1333-1344.e1333
56 Goldgraber MB. Pseudopolyps in ulcerative colitis. Diseases of the colon and rectum 1965; 8: 355-363
57 Fort Gasia M, Ghosh S, Iacucci M. Colorectal polyps in ulcerative colitis and Crohn’s colitis. Minerva gastroenterologica e dietologica 2015; 61: 215-222
58 Laine L, Kaltenbach T, Barkun A. et al. SCENIC international consensus statement on surveillance and management of dysplasia in inflammatory bowel disease. Gastroenterology 2015; 148: 639-651.e628
59 Updated S3-Guideline Ulcerative Colitis. German Society for Digestive and Metabolic Diseases (DGVS). Z Gastroenterol [Anonym]. 2019; 57: 162-241
60 Louis E, Collard A, Oger AF. et al. Behaviour of Crohn’s disease according to the Vienna classification: changing pattern over the course of the disease. Gut 2001; 49: 777-782
61 Update on the paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy [Anonym]. 2005; 37: 570-578
62 Kamiński MF, Hassan C, Bisschops R. et al. Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2014; 46: 435-449
63 Kucharzik T, Dignaß A, Siegmund B. Not Available. Z Gastroenterol 2019; 57: 1279-1280
64 Blonski W, Kundu R, Furth EF. et al. High-grade dysplastic adenoma-like mass lesions are not an indication for colectomy in patients with ulcerative colitis. Scand J Gastroenterol 2008; 43: 817-820
65 Vieth M, Behrens H, Stolte M. Sporadic adenoma in ulcerative colitis: endoscopic resection is an adequate treatment. Gut 2006; 55: 1151-1155
66 Odze RD, Farraye FA, Hecht JL. et al. Long-term follow-up after polypectomy treatment for adenoma-like dysplastic lesions in ulcerative colitis. Clin Gastroenterol Hepatol 2004; 2: 534-541
67 Kudo S, Tamura S, Nakajima T. et al. Diagnosis of colorectal tumorous lesions by magnifying endoscopy. Gastrointest Endosc 1996; 44: 8-14
68 Hewett DG, Kaltenbach T, Sano Y. et al. Validation of a simple classification system for endoscopic diagnosis of small colorectal polyps using narrow-band imaging. Gastroenterology 2012; 143: 599-607 e591
69 Narula N, Alshahrani AA, Yuan Y. et al. Patient-Reported Outcomes and Endoscopic Appearance of Ulcerative Colitis-a Systematic Review and Meta-Analysis. Clin Gastroenterol Hepatol 2018;
70 Rogler G, Vavricka S, Schoepfer A. et al. Mucosal healing and deep remission: what does it mean?. World journal of gastroenterology : WJG 2013; 19: 7552-7560
71 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
72 Fernandes SR, Pinto J, Marques da Costa P. et al. Disagreement Among Gastroenterologists Using the Mayo and Rutgeerts Endoscopic Scores. Inflammatory bowel diseases 2018; 24: 254-260
73 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 e142
74 Mohammed Vashist N, Samaan M, Mosli MH. et al. Endoscopic scoring indices for evaluation of disease activity in ulcerative colitis. The Cochrane database of systematic reviews 2018; 1: CD011450
75 Mohammed Vashist N, Samaan M, Mosli MH. et al. Endoscopic scoring indices for evaluation of disease activity in ulcerative colitis. The Cochrane database of systematic reviews 2018; 1: Cd011450
76 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
77 Vuitton L, Peyrin-Biroulet L, Colombel JF. et al. Defining endoscopic response and remission in ulcerative colitis clinical trials: an international consensus. Alimentary pharmacology & therapeutics 2017; 45: 801-813
78 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
79 Travis SP, Schnell D, Feagan BG. et al. The Impact of Clinical Information on the Assessment of Endoscopic Activity: Characteristics of the Ulcerative Colitis Endoscopic Index Of Severity [UCEIS]. J Crohns Colitis 2015; 9: 607-616
80 Ikeya K, Hanai H, Sugimoto K. et al. The Ulcerative Colitis Endoscopic Index of Severity More Accurately Reflects Clinical Outcomes and Long-term Prognosis than the Mayo Endoscopic Score. J Crohns Colitis 2016; 10: 286-295
81 Thia KT, Loftus EV, Pardi DS. et al. Measurement of disease activity in ulcerative colitis: interobserver agreement and predictors of severity. Inflamm Bowel Dis 2011; 17: 1257-1264
82 Samuel S, Bruining DH, Loftus EV. et al. Validation of the ulcerative colitis colonoscopic index of severity and its correlation with disease activity measures. Clin Gastroenterol Hepatol 2013; 11: 49-54 e41
83 Iacucci M, Daperno M, Lazarev M. et al. Development and reliability of the new endoscopic virtual chromoendoscopy score: the PICaSSO (Paddington International Virtual ChromoendoScopy ScOre) in ulcerative colitis. Gastrointest Endosc 2017; 86: 1118-1127.e1115
84 Iacucci M, Smith SC, Bazarova A. et al. An international multicenter real-life prospective study of electronic chromoendoscopy score PICaSSO in Ulcerative Colitis. Gastroenterology 2020;
85 Feagan BG, Greenberg GR, Wild G. et al. Treatment of ulcerative colitis with a humanized antibody to the alpha4beta7 integrin. N Engl J Med 2005; 352: 2499-2507
86 Rachmilewitz D. Coated mesalazine (5-aminosalicylic acid) versus sulphasalazine in the treatment of active ulcerative colitis: a randomised trial. BMJ 1989; 298: 82-86
87 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
88 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
89 Sipponen T, Nuutinen H, Turunen U. et al. Endoscopic evaluation of Crohn’s disease activity: comparison of the CDEIS and the SES-CD. Inflammatory bowel diseases 2010; 16: 2131-2136
90 Jones J, Loftus EV, Panaccione R. et al. Relationships between disease activity and serum and fecal biomarkers in patients with Crohn’s disease. ClinGastroenterolHepatol 2008; 6: 1218-1224
91 Dignass A, Stoynov S, Dorofeyev AE. et al. Once versus three times daily dosing of oral budesonide for active Crohn’s disease: a double-blind, double-dummy, randomised trial. Journal of Crohn’s & colitis 2014; 8: 970-980
92 Rutgeerts P, Van Assche G, Sandborn WJ. et al. Adalimumab induces and maintains mucosal healing in patients with Crohn’s disease: data from the EXTEND trial. Gastroenterology 2012; 142: 1102-1111 e1102
93 Colombel JF, Sandborn WJ, Reinisch W. et al. Infliximab, azathioprine, or combination therapy for Crohn’s disease. NEnglJMed 2010; 362: 1383-1395
94 Sipponen T, Karkkainen P, Savilahti E. et al. Correlation of faecal calprotectin and lactoferrin with an endoscopic score for Crohn’s disease and histological findings. AlimentPharmacolTher 2008; 28: 1221-1229
95 Rutgeerts P, Geboes K, Vantrappen G. et al. Predictability of the postoperative course of Crohn’s disease. Gastroenterology 1990; 99: 956-963
96 Fernandes SR, Pinto J, Marques da Costa P. et al. Disagreement Among Gastroenterologists Using the Mayo and Rutgeerts Endoscopic Scores. Inflamm Bowel Dis 2018; 24: 254-260
97 Ma C, Gecse KB, Duijvestein M. et al. Reliability of Endoscopic Evaluation of Postoperative Recurrent Crohn’s Disease. Clin Gastroenterol Hepatol 2020; 18: 2139-2141.e2132
98 Marteau P, Laharie D, Colombel JF. et al. Interobserver Variation Study of the Rutgeerts Score to Assess Endoscopic Recurrence after Surgery for Crohn’s Disease. J Crohns Colitis 2016; 10: 1001-1005
99 Gecse K LM, Bossuyt P. et al. Sa1198 Agreement among experts in the endoscopic evaluation of postoperative recurrence in Crohn’s disease using the Rutgeerts Score.. Gastroenterology 2014; 146: S-227
100 Bayart P, Duveau N, Nachury M. et al. Ileal or Anastomotic Location of Lesions Does Not Impact Rate of Postoperative Recurrence in Crohn’s Disease Patients Classified i2 on the Rutgeerts Score. Dig Dis Sci 2016; 61: 2986-2992
101 Rivière P, Vermeire S, Irles-Depe M. et al. No Change in Determining Crohn’s Disease Recurrence or Need for Endoscopic or Surgical Intervention With Modification of the Rutgeerts' Scoring System. Clin Gastroenterol Hepatol 2019; 17: 1643-1645
102 Peyrin-Biroulet L, Sandborn W, Sands BE. et al. Selecting Therapeutic Targets in Inflammatory Bowel Disease (STRIDE): Determining Therapeutic Goals for Treat-to-Target. The American journal of gastroenterology 2015; 110: 1324-1338
103 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
104 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
105 Ungaro RC, Yzet C, Bossuyt P. et al. Deep Remission at 1 Year Prevents Progression of Early Crohn’s Disease. Gastroenterology 2020; 159: 139-147
106 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: 1069-1074
107 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
108 Fukuda T, Naganuma M, Sugimoto S. et al. Efficacy of Therapeutic Intervention for Patients With an Ulcerative Colitis Mayo Endoscopic Score of 1. Inflammatory. bowel diseases 2018;
109 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
110 Frøslie 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
111 Lemann M, Mary JY, Colombel JF. et al. A randomized, double-blind, controlled withdrawal trial in Crohn’s disease patients in long-term remission on azathioprine. Gastroenterology 2005; 128: 1812-1818
112 Schnitzler F, Fidder H, Ferrante M. et al. Mucosal healing predicts long-term outcome of maintenance therapy with infliximab in Crohn’s disease. Inflamm Bowel Dis 2009; 15: 1295-1301
113 Osada T, Ohkusa T, Yokoyama T. et al. Comparison of several activity indices for the evaluation of endoscopic activity in UC: inter- and intraobserver consistency. Inflammatory bowel diseases 2010; 16: 192-197
114 Pagnini C, Menasci F, Desideri F. et al. Endoscopic scores for inflammatory bowel disease in the era of 'mucosal healing': Old problem, new perspectives. Dig Liver Dis 2016; 48: 703-708
115 Daperno M, Comberlato M, Bossa F. et al. Training Programs on Endoscopic Scoring Systems for Inflammatory Bowel Disease Lead to a Significant Increase in Interobserver Agreement Among Community Gastroenterologists. J Crohns Colitis 2017; 11: 556-561