Endoscopy 2009; 41(3): 218-226
DOI: 10.1055/s-0028-1119627
Original article

© Georg Thieme Verlag KG Stuttgart · New York

Appropriateness of colonoscopy in Europe (EPAGE II) – Chronic diarrhea and known inflammatory bowel disease

S.  Schusselé Filliettaz1 , P.  Juillerat2 , B.  Burnand1 , C.  Arditi1 , A.  Windsor3 , C.  Beglinger4 , R.  W.  Dubois5 , I.  Peytremann-Bridevaux1 , V.  Pittet1 , J.-J.  Gonvers2 , F.  Froehlich2,  4 , J.-P.  Vader1 , and the EPAGE II Study Group6
  • 1Healthcare Evaluation Unit, Institute of Social and Preventive Medicine, University of Lausanne and Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland
  • 2Department of Gastroenterology and Hepatology, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
  • 3Department of Surgery, University College London Hospitals, London, United Kingdom
  • 4Department of Gastroenterology, University of Basle, Basle, Switzerland
  • 5Cerner LifeSciences, Beverly Hills, USA
  • 6The EPAGE II Study Group[*]
Further Information

Publication History

submitted17 June 2008

accepted after revision5 December 2008

Publication Date:
11 March 2009 (online)

Background and study aims: To summarize the published literature on assessment of appropriateness of colonoscopy for investigation of chronic diarrhea, management of patients with known inflammatory bowel disease (IBD), and for colorectal cancer (CRC) surveillance in such patients, and to report report appropriateness criteria developed by an expert panel, the 2008 European Panel on the Appropriateness of Gastrointestinal Endoscopy, EPAGE II.

Methods: A systematic search of guidelines, systematic reviews, and primary studies regarding the evaluation of chronic diarrhea, the management of IBD, and colorectal cancer surveillance in IBD was performed. The RAND/UCLA Appropriateness Method was applied to develop appropriateness criteria for colonoscopy for these conditions.

Results: According to the literature, colonoscopic evaluation may be justified for patients aged > 50 years with recent-onset chronic diarrhea or with alarm symptoms. Surveillance colonoscopy for CRC should be offered to all patients with extensive ulcerative colitis or colonic Crohn’s disease of 8 years’ duration, and to all patients with less extensive disease of 15 years’ duration. Intervals for surveillance colonoscopy depend on duration of evolution, initial diagnosis, and histological findings. The EPAGE II criteria also confirmed the appropriateness of diagnostic colonoscopy for diarrhea of > 4 weeks’ duration. They also suggest that, in addition to assessing extent of IBD by colonoscopy, further colonoscopic examination is appropriate in the face of persistent or worsening symptoms. Surveillance colonoscopy in IBD patients was generally appropriate after a lapse of 2 years. In the presence of dysplasia at previous colonoscopy, it was not only appropriate but necessary.

Conclusions: Despite or perhaps because of the limitations of the available published studies, the panel-based EPAGE II (http://www.epage.ch) criteria can help guide appropriate colonoscopy use in the absence of strong evidence from the literature.

References

  • 1 Thomas P D, Forbes A, Green J. et al . Guidelines for the investigation of chronic diarrhoea, 2nd edition.  Gut. 2003;  52 Suppl 5 v1-v15
  • 2 Fine K D, Schiller L R. AGA technical review on the evaluation and management of chronic diarrhea.  Gastroenterology. 1999;  116 1464-1486
  • 3 Bolin T D, Davis A E, Duncombe V M. A prospective study of persistent diarrhoea.  Aust NZ J Med. 1982;  12 22-26
  • 4 Bytzer P, Stokholm M, Andersen I. et al . Aetiology, medical history, and faecal weight in adult patients referred for diarrhoea. A prospective survey.  Scand J Gastroenterol. 1990;  25 572-578
  • 5 Carter M J, Lobo A J, Travis S P. Guidelines for the management of inflammatory bowel disease in adults.  Gut. 2004;  53 Suppl 5 V1-V16
  • 6 Kornbluth A, Sachar D B. Ulcerative colitis practice guidelines in adults (update): American College of Gastroenterology, Practice Parameters Committee.  Am J Gastroenterol. 2004;  99 1371-1385
  • 7 D’Haens G, Sandborn W J, Feagan B G. et al . A review of activity indices and efficacy end points for clinical trials of medical therapy in adults with ulcerative colitis.  Gastroenterology. 2007;  132 763-786
  • 8 Henriksen M, Jahnsen J, Lygren I. et al . Ulcerative colitis and clinical course: results of a 5-year population-based follow-up study (the IBSEN study).  Inflamm Bowel Dis. 2006;  12 543-550
  • 9 Stange E F, Travis S PL, Vermeire S. et al . European evidence based consensus on the diagnosis and management of Crohn’s disease: definitions and diagnosis.  Gut. 2006;  55 Suppl 1 i1-i15
  • 10 Hanauer S B, Sandborn W. Management of Crohn’s disease in adults.  Am J Gastroenterol. 2001;  96 635-643
  • 11 Gasche C, Scholmerich J, Brynskov J. et al . A simple classification of Crohn’s disease: report of the Working Party for the World Congresses of Gastroenterology, Vienna 1998.  Inflamm Bowel Dis. 2000;  6 8-15
  • 12 Satsangi J, Silverberg M S, Vermeire S. et al . The Montreal classification of inflammatory bowel disease: controversies, consensus, and implications.  Gut. 2006;  55 749-753
  • 13 Silverberg M S, Satsangi J, Ahmad T. et al . Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: Report of a Working Party of the 2005 Montreal World Congress of Gastroenterology.  Can J Gastroenterol. 2005;  19 Suppl A 5-36
  • 14 Best W R, Becktel J M, Singleton J W. Rederived values of the eight coefficients of the Crohn’s Disease Activity Index (CDAI).  Gastroenterology. 1979;  77 843-846
  • 15 Henriksen M, Jahnsen J, Lygren I. et al . Clinical course in Crohn’s disease: results of a five-year population-based follow-up study (the IBSEN study).  Scand J Gastroenterol. 2007;  42 602-610
  • 16 Silverstein M D, Loftus E V, Sandborn W J. et al . Clinical course and costs of care for Crohn’s disease: Markov model analysis of a population-based cohort.  Gastroenterology. 1999;  117 49-57
  • 17 Konikoff M R, Denson L A. Role of fecal calprotectin as a biomarker of intestinal inflammation in inflammatory bowel disease.  Inflamm Bowel Dis. 2006;  12 524-534
  • 18 Leighton J A, Shen B, Baron T H. et al . ASGE guideline: endoscopy in the diagnosis and treatment of inflammatory bowel disease.  Gastrointest Endosc. 2006;  63 558-565
  • 19 Vader J P, Froehlich F, Juillerat P. et al . Appropriate treatment for Crohn’s disease: methodology and summary results of a multidisciplinary international expert panel approach – EPACT.  Digestion. 2006;  73 237-248
  • 20 Bernstein C N, Blanchard J F, Kliewer E. et al . Cancer risk in patients with inflammatory bowel disease: a population-based study.  Cancer. 2001;  91 854-862
  • 21 Collins P D, Mpofu C, Watson A J. et al . Strategies for detecting colon cancer and/or dysplasia in patients with inflammatory bowel disease.  Cochrane Database Syst Rev. 2006;  2 CD000279
  • 22 Eaden J A, Abrams K R, Mayberry J F. The risk of colorectal cancer in ulcerative colitis: a meta-analysis.  Gut. 2001;  48 526-535
  • 23 Gupta R B, Harpaz N, Itzkowitz S. et al . Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study.  Gastroenterology. 2007;  133 1099-1105
  • 24 Jess T, Gamborg M, Matzen P. et al . Increased risk of intestinal cancer in Crohn’s disease: a meta-analysis of population-based cohort studies.  Am J Gastroenterol. 2005;  100 2724-2729
  • 25 Jess T, Loftus jr. E V, Velayos F S. et al . Risk of intestinal cancer in inflammatory bowel disease: a population-based study from Olmsted County, Minnesota.  Gastroenterology. 2006;  130 1039-1046
  • 26 Jess T, Loftus E V, Velayos F S. et al . Risk factors for colorectal neoplasia in inflammatory bowel disease: a nested case–control study from Copenhagen county, Denmark and Olmsted county, Minnesota.  Am J Gastroenterol. 2007;  102 829-836
  • 27 Karvellas C J, Fedorak R N, Hanson J. et al . Increased risk of colorectal cancer in ulcerative colitis patients diagnosed after 40 years of age.  Can J Gastroenterol. 2007;  21 443-446
  • 28 Lakatos L, Mester G, Erdelyi Z. et al . Risk factors for ulcerative colitis-associated colorectal cancer in a Hungarian cohort of patients with ulcerative colitis: results of a population-based study.  Inflamm Bowel Dis. 2006;  12 205-211
  • 29 Siegel C A, Sands B E. Risk factors for colorectal cancer in Crohn’s colitis: a case-control study.  Inflamm Bowel Dis. 2006;  12 491-496
  • 30 Soetikno R M, Lin O S, Heidenreich P A. et al . Increased risk of colorectal neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis: a meta-analysis.  Gastrointest Endosc. 2002;  56 48-54
  • 31 Thomas T, Abrams K A, Robinson R J. et al . Meta-analysis: cancer risk of low-grade dysplasia in chronic ulcerative colitis.  Aliment Pharmacol Ther. 2007;  25 657-668
  • 32 von Roon A C, Reese G, Teare J. et al . The risk of cancer in patients with Crohn’s disease.  Dis Colon Rectum. 2007;  50 839-855
  • 33 Hookman P, Barkin J S. What should be the standard care for cancer surveillance, diagnosis of dysplasia, and the decision for colectomy in chronic inflammatory bowel disease?.  Am J Gastroenterol. 2002;  97 1249-1255
  • 34 Rubin D T. The changing face of colorectal cancer in inflammatory bowel disease: progress at last!.  Gastroenterology. 2006;  130 1350-1352
  • 35 Itzkowitz S H, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation.  Am J Physiol Gastrointest Liver Physiol. 2004;  287 G7-G17
  • 36 Itzkowitz S H, Harpaz N. Diagnosis and management of dysplasia in patients with inflammatory bowel diseases.  Gastroenterology. 2004;  126 1634-1648
  • 37 Askling J, Dickman P W, Karlen P. et al . Family history as a risk factor for colorectal cancer in inflammatory bowel disease.  Gastroenterology. 2001;  120 1356-1362
  • 38 Geboes K. Review article: what are the important endoscopic lesions for detection of dysplasia in inflammatory bowel disease?.  Aliment Pharmacol Ther. 2006;  24 Suppl 3 50-55
  • 39 Rubin D T, Rothe J A, Hetzel J T. et al . Are dysplasia and colorectal cancer endoscopically visible in patients with ulcerative colitis?.  Gastrointest Endosc. 2007;  65 998-1004
  • 40 Rutter M D, Saunders B P, Wilkinson K H. et al . Cancer surveillance in longstanding ulcerative colitis: endoscopic appearances help predict cancer risk.  Gut. 2004;  53 1813-1816
  • 41 Bronner M P, Goldblum J R, Kimmey M B. et al . Low-grade dysplasia in ulcerative colitis: natural history data still unknown.  Gastroenterology. 2004;  127 362-363
  • 42 Lim C H, Dixon M F, Vail A. et al . Ten year follow up of ulcerative colitis patients with and without low grade dysplasia.  Gut. 2003;  52 1127-1132
  • 43 Rubio C A, Befrits R. Low-grade dysplasia in flat mucosa in ulcerative colitis.  Gastroenterology. 2004;  126 1494-1495
  • 44 Ullman T, Croog V, Harpaz N. et al . Progression of flat low-grade dysplasia to advanced neoplasia in patients with ulcerative colitis.  Gastroenterology. 2003;  125 1311-1319
  • 45 Campbell S, Ghosh S. Ulcerative colitis and colon cancer: strategies for cancer prevention.  Dig Dis. 2002;  20 38-48
  • 46 Delco F, Sonnenberg A. The unsolved problem of surveillance for colorectal cancer in ulcerative colitis.  Can J Gastroenterol. 1999;  13 655-660
  • 47 Froehlich F, Larequi-Lauber T, Gonvers J J. et al . 11. Appropriateness of colonoscopy: inflammatory bowel disease.  Endoscopy. 1999;  31 647-653
  • 48 Gonvers J J, Bochud M, Burnand B. et al . 10. Appropriateness of colonoscopy: diarrhea.  Endoscopy. 1999;  31 641-646
  • 49 Longstreth G F, Thompson W G, Chey W D. et al . Functional bowel disorders.  Gastroenterology. 2006;  130 1480-1491
  • 50 Juillerat P, Peytremann-Bridevaux I, Vader J P. et al . Appropriateness of Colonoscopy in Europe (EPAGE II). Presentation of methodology, general results, and analysis of complications.  Endoscopy. 2008;  41 240-246
  • 51 Adler A, Roll S, Marowski B. et al . Appropriateness of colonoscopy in the era of colorectal cancer screening: a prospective, multicenter study in a private-practice setting (Berlin Colonoscopy Project 1, BECOP 1).  Dis Colon Rectum. 2007;  50 1628-1638
  • 52 Agnarsdottir M, Gunnlaugsson O, Orvar K B. et al . Collagenous and lymphocytic colitis in Iceland.  Dig Dis Sci. 2002;  47 1122-1128
  • 53 DeBosset V, Froehlich F, Rey J P. et al . Do explicit appropriateness criteria enhance the diagnostic yield of colonoscopy?.  Endoscopy. 2002;  34 360-368
  • 54 Duncan J E, Sweeney W B, Trudel J L. et al . Colonoscopy in the elderly: low risk, low yield in asymptomatic patients.  Dis Colon Rectum. 2006;  49 646-651
  • 55 Fernandez-Banares F, Salas A, Forne M. et al . Incidence of collagenous and lymphocytic colitis: a 5-year population-based study.  Am J Gastroenterol. 1999;  94 418-423
  • 56 Fine K D, Seidel R H, Do K. The prevalence, anatomic distribution, and diagnosis of colonic causes of chronic diarrhea.  Gastrointest Endosc. 2000;  51 318-326
  • 57 Gonvers J J, Harris J K, Wietlisbach V. et al . A European view of diagnostic yield and appropriateness of colonoscopy.  Hepatogastroenterology. 2007;  54 729-735
  • 58 Lasson A, Kilander A, Stotzer P O. Diagnostic yield of colonoscopy based on symptoms.  Scand J Gastroenterol. 2008;  43 356-362
  • 59 Lieberman D A, de Garmo P L, Fleischer D E. et al . Colonic neoplasia in patients with nonspecific GI symptoms.  Gastrointest Endosc. 2000;  51 647-651
  • 60 Matteoni C A, Wang N, Goldblum J R. et al . Flexible sigmoidoscopy for the detection of microscopic colitis.  Am J Med. 2000;  108 416-418
  • 61 Morini S, Hassan C, Meucci G. et al . Diagnostic yield of open access colonoscopy according to appropriateness.  Gastrointest Endosc. 2001;  54 175-179
  • 62 Offner F A, Jao R V, Lewin K J. et al . Collagenous colitis: a study of the distribution of morphological abnormalities and their histological detection.  Hum Pathol. 1999;  30 451-457
  • 63 Olesen M, Eriksson S, Bohr J. et al . Microscopic colitis: a common diarrhoeal disease: an epidemiological study in Orebro, Sweden, 1993–1998.  Gut. 2004;  53 346-350
  • 64 Pardi D S, Loftus jr. E V, Smyrk T C. et al . The epidemiology of microscopic colitis: a population based study in Olmsted County, Minnesota.  Gut. 2007;  56 504-508
  • 65 Patel Y, Pettigrew N M, Grahame G R. et al . The diagnostic yield of lower endoscopy plus biopsy in nonbloody diarrhea.  Gastrointest Endosc. 1997;  46 338-343
  • 66 Shah R J, Fenoglio-Preiser C, Bleau B L. et al . Usefulness of colonoscopy with biopsy in the evaluation of patients with chronic diarrhea.  Am J Gastroenterol. 2001;  96 1091-1095
  • 67 Yusoff I F, Ormonde D G, Hoffman N E. Routine colonic mucosal biopsy and ileoscopy increases diagnostic yield in patients undergoing colonoscopy for diarrhea.  J Gastroenterol Hepatol. 2002;  17 276-280
  • 68 Froehlich F, Gonvers JJ Diagnostic yield of colonoscopy by indication. In: Waye JD, Rex DK, Williams CB, (eds) Colonoscopy: principles and practice. London; Blackwell Science 2003: 111-130
  • 69 Pardi D S, Smyrk T C, Tremaine W J. et al . Microscopic colitis: a review.  Am J Gastroenterol. 2002;  97 794-802
  • 70 Agence Nationale d’Accréditation et d’Evaluation en Santé .[Endoscopie digestive basse: indications en dehors du dépistage en population – Argumentaire]. Saint-Denis La Plaine; Haute Autorité de Santé 2004: 138p. http://Available from: http://www.has-sante.fr/portail/display.jsp?id=c_272348 [Accessed: 28–5–2007]
  • 71 Australian Cancer Network Colorectal Cancer Guidelines Revision Committee .Guidelines for the prevention, early detection and management of colorectal cancer. Sydney; The Cancer Council Australia and Australian Cancer Network 2005: 368p. http://ISSN 0-9775060-1-0. Available from: http://www.nhmrc.gov.au/publications/synopses/cp106/_files/cp106.pdf* [Accessed: 1 – 6-2007]
  • 72 Eisen G M, Dominitz J A, Faigel D O. et al . Use of endoscopy in diarrheal illnesses.  Gastrointest Endosc. 2001;  54 821-823
  • 73 Rex D K, Petrini J L, Baron T H. et al . Quality indicators for colonoscopy.  Gastrointest Endosc. 2006;  63 S16-S28
  • 74 Singapore Ministry of Health .Colorectal cancer. Report nr 2/2004. Singapore; 2004: 98p. http://Available from: http://www.hpp.moh.gov.sg/HPP/MungoBlobs/145/831/2004%20colorectalcancer_0.pdf [Accessed: 13–8–2007]
  • 75 Beaugerie L. Place de l’endoscopie dans les colites microscopiques. 2003: 6p. http://Available from: http://www.sfed.org/documents_sfed/files/recommandations/Endoscopie_colitesmicro.pdf [Accessed: 1 – 6-2007]
  • 76 Kojima M, Wakai K, Tokudome S. et al . Bowel movement frequency and risk of colorectal cancer in a large cohort study of Japanese men and women.  Br J Cancer. 2004;  90 1397-1401
  • 77 Kune G A, Kune S, Field B. et al . The role of chronic constipation, diarrhea, and laxative use in the etiology of large-bowel cancer. Data from the Melbourne Colorectal Cancer Study.  Dis Colon Rectum. 1988;  31 507-512
  • 78 Otani T, Iwasaki M, Inoue M. et al . Bowel movement, state of stool, and subsequent risk for colorectal cancer: the Japan public health center-based prospective study.  Ann Epidemiol. 2006;  16 888-894
  • 79 American Cancer Society .Cancer facts and figures 2007. 2007: 56p. http://Available from: http://www.cancer.org/downloads/STT/CAFF2007PWSecured.pdf [Accessed: 8 – 11 – 2007]
  • 80 Davila R E, Rajan E, Adler D. et al . ASGE guideline: the role of endoscopy in the diagnosis, staging, and management of colorectal cancer.  Gastrointest Endosc. 2005;  61 1-7
  • 81 Davila R E, Rajan E, Baron T H. et al . ASGE guideline: colorectal cancer screening and surveillance.  Gastrointest Endosc. 2006;  63 546-557
  • 82 Institute for Clinical Systems Improvement (ICSI) .Colorectal cancer screening. 11th Edition . Bloomington (MN); 2006: 51p. http://Available from: http://www.icsi.org/colorectal_cancer_screening/colorectal_cancer_screening_5.html [Accessed: 13–8–2007]
  • 83 Levin B, Barthel J, Burt R. et al .Practice guidelines in Oncology: Colorectal cancer screening. National Comprehensive Cancer Network 2007 http://Available from: http://www.nccn.org/professionals/physician_gls/PDF/colorectal_screening.pdf [Accessed: 8–11–2007
  • 84 McLeod R. Canadian Task Force on Preventive Health Care .Screening strategies for colorectal cancer: systematic review and recommendations. Technical review. CTFPHC Technical Report nr 01–2. London, Ontario; Canadian Task Force on Preventive Health Care 2001: 37p. http://Available from: http://www.ctfphc.org/ [Accessed: 8-11 – 2007]
  • 85 National Guideline Clearinghouse .Colorectal cancer screening clinical practice guideline – NGC summary. Oakland (USA); Kaiser Permanente Care Management Institute 2006: 16p. http://Available from: http://www.guidelines.gov/summary/summary.aspx?doc_id=10847&nbr=005662&string=colon [Accessed: 9 – 11 – 2007]
  • 86 Pignone M P, Rich M, Teutsch S. et al .Screening for colorectal cancer in adults. Rockville; Agency for Healthcare Research and Quality (AHRQ) 2002: 48p. http://Available from: http://www.ahrq.gov/downloads/pub/prevent/pdfser/colocanser.pdf [Accessed: 18 – 5-2007]
  • 87 Rex D K, Johnson D A, Lieberman D A. et al . Colorectal cancer prevention 2000: screening recommendations of the American College of Gastroenterology. American College of Gastroenterology.  Am J Gastroenterol. 2000;  95 868-877
  • 88 Winawer S, Fletcher R, Rex D. et al . Colorectal cancer screening and surveillance: clinical guidelines and rationale – Update based on new evidence.  Gastroenterology. 2003;  124 544-560
  • 89 Beau P, Gay G, Arput J. et al .Place de l’endocopie dans le bilan de la maladie de Crohn. Société Française d’Endoscopie Digestive 2004: 6p. http://Available from: http://www.sfed.org/documents_sfed/files/recommandations/Endoscopie_Crohn.pdf [Accessed: 1 – 6-2007]
  • 90 Hoffmann J C, Zeitz M, Bischoff S C. et al . Diagnostik und Therapie der Colitis ulcerosa: Ergebnisse einer evidenzbasierten Konsensuskonferenz der Deutschen Gesellschaft fuer Verdauungs- und Stoffwechselerkrankungen zusammen mit dem Kompetenznetz chronisch entzuendliche Darmerkrankungen [Diagnosis and therapy of ulcerative colitis: results of an evidence based consensus conference by the German society of Digestive and Metabolic Diseases and the competence network on inflammatory bowel disease].  Z Gastroenterol. 2004;  42 979-1032
  • 91 Hoffmann R M, Kruis W. Chronisch-entzuendliche Darmerkrankungen. 3rd ed. Stuttgart; Demeter 2002 ISBN/ISSN 3–13–1 155 930. Available from: http://www.dgvs.de/media/3.3.CED.pdf [Accessed: 24 – 9-2007]
  • 92 Schreiber S, Folsch U R. Klinische Diagnostik, Klassification [Clinical diagnostics, classification].  Z Gastroenterol. 2003;  41 21-23
  • 93 Barthet M, Gay G, Sautereau D. et al .Surveillance endoscopique des maladies inflammatoires digestives. Société Française d’Endoscopie Digestive 2004: 6p http://Available from: http://www.sfed.org/documents_sfed/files/recommandations/Surveillendo_MICI.pdf [Accessed: 27 – 5-2007]
  • 94 Eaden J A, Mayberry J F. Guidelines for screening and surveillance of asymptomatic colorectal cancer in patients with inflammatory bowel disease.  Gut. 2002;  51 Suppl 5 V10-V12
  • 95 Heresbach D, Boyer J, Laugier R. et al .Techniques et indications des biopsies lors de la coloscopie. Société Française d’Endoscopie Digestive 2007: 8p. http://Available from: http://www.sfed.org/documents_sfed/files/recommandations/Biopsie_coloscopie.pdf [Accessed: 1–6–2007]
  • 96 Itzkowitz S H, Present D H. Consensus conference: Colorectal cancer screening and surveillance in inflammatory bowel disease.  Inflamm Bowel Dis. 2005;  11 314-321
  • 97 Stange E F, Schreiber S, Folsch U R. et al . Crohn-Ergebnisse einer evidenzbasierten Konsensuskonferenz der Deutschen Gesellschaft fuer Verdauungs- und Stoffwechselkrankheiten [Diagnostics and treatment of Crohn’s disease – results of an evidence-based consensus conference of the German Society for Digestive and Metabolic Diseases].  Z Gastroenterol. 2003;  41 19-20
  • 98 Ahmadi A A, Polyak S. Endoscopy/surveillance in inflammatory bowel disease.  Surg Clin N Am. 2007;  87 743-762
  • 99 Morson B C, Pang L S. Rectal biopsy as an aid to cancer control in ulcerative colitis.  Gut. 1967;  8 423-434
  • 100 Provenzale D, Onken J. Surveillance issues in inflammatory bowel disease: ulcerative colitis.  J Clin Gastroenterol. 2001;  32 99-105
  • 101 Delco F, Sonnenberg A. A decision analysis of surveillance for colorectal cancer in ulcerative colitis.  Gut. 2000;  46 500-506
  • 102 Vleggaar F P, Lutgens M W, Claessen M M. Review article: The relevance of surveillance endoscopy in long-lasting inflammatory bowel disease.  Aliment Pharmacol Ther. 2007;  26 Suppl 2 47-52
  • 103 Riegler G, Bossa F, Caserta L. et al . Colorectal cancer and high grade dysplasia complicating ulcerative colitis in Italy. A retrospective co-operative IG-IBD study.  Dig Liver Dis. 2003;  35 628-634
  • 104 Rex D K, Cutler C S, Lemmel G T. et al . Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies.  Gastroenterology. 1997;  112 24-28
  • 105 Toruner M, Harewood G C, Loftus jr. E V. et al . Endoscopic factors in the diagnosis of colorectal dysplasia in chronic inflammatory bowel disease.  Inflamm Bowel Dis. 2005;  11 428-434
  • 106 Geboes K, Rutgeerts P, Opdenakker G. et al . Endoscopic and histologic evidence of persistent mucosal healing and correlation with clinical improvement following sustained infliximab treatment for Crohn’s disease.  Curr Med Res Opin. 2005;  21 1741-1754
  • 107 Rutgeerts P, Vermeire S, VanAssche G. Mucosal healing in inflammatory bowel disease: impossible ideal or therapeutic target?.  Gut. 2007;  56 453-455
  • 108 Brown S, Baraza W, Hurlstone P. Chromoscopy versus conventional endoscopy for the detection of polyps in the colon and rectum.  Cochrane Database Syst Rev. 2007;  4 CD006439
  • 109 Thorlacius H, Toth E. Role of chromoendoscopy in colon cancer surveillance in inflammatory bowel disease.  Inflamm Bowel Dis. 2007;  13 911-917
  • 110 Hassan C, Zullo A, de Francesco V. et al . Systematic review: Endoscopic dilatation in Crohn’s disease.  Aliment Pharmacol Ther. 2007;  26 1457-1464

1 See Appendix: The EPAGE II Study Group

J.-P. VaderMD MPH 

Institute of Social and Preventive Medicine

Rue du Bugnon 17
CH-1005 Lausanne
Switzerland

Fax: +41-21-3144954

Email: john-paul.vader@chuv.ch