Endoscopy 2022; 54(09): 904-915
DOI: 10.1055/a-1874-0946
Position Statement

Performance measures for colonoscopy in inflammatory bowel disease patients: European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative

Evelien Dekker*
 1   Department of Gastroenterology and Hepatology, Amsterdam University Medical Centers, Amsterdam, The Netherlands
,
Karlijn J. Nass*
 1   Department of Gastroenterology and Hepatology, Amsterdam University Medical Centers, Amsterdam, The Netherlands
,
Marietta Iacucci
 2   Institute of Immunology and Immunotherapy, NIHR Birmingham Biomedical Research Centre, University Hospitals NHS Foundation Trust, University of Birmingham, Birmingham, UK
,
Alberto Murino
 3   Royal Free Unit for Endoscopy, The Royal Free Hospital and University College London Institute for Liver and Digestive Health, London, UK
,
João Sabino
 4   Department of Gastroenterology and Hepatology, University Hospital Leuven, TARGID, KU Leuven, Leuven, Belgium
,
Marek Bugajski
 5   Department of Gastroenterology, Hepatology and Oncology, Medical Center for Postgraduate Education, Warsaw, Poland
 6   Department of Gastroenterological Oncology, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
 7   Department of Health Management and Health Economics, University of Oslo, Oslo, Norway
,
Cristina Carretero
 8   Department of Gastroenterology, University of Navarre Clinic, Healthcare Research Institute of Navarre, Pamplona, Spain
,
George Cortas
 9   University of Balamand Faculty of Medicine, St. George Hospital University Medical Center, Beirut, Lebanon
,
Edward J. Despott
 3   Royal Free Unit for Endoscopy, The Royal Free Hospital and University College London Institute for Liver and Digestive Health, London, UK
,
James E. East
10   Translational Gastroenterology Unit, Nuffield Department of Medicine, John Radcliffe Hospital, University of Oxford, Oxford, UK
11   Division of Gastroenterology and Hepatology, Mayo Clinic Healthcare, London, UK
,
Michal F. Kaminski
 5   Department of Gastroenterology, Hepatology and Oncology, Medical Center for Postgraduate Education, Warsaw, Poland
 6   Department of Gastroenterological Oncology, The Maria Sklodowska-Curie Memorial Cancer Center and Institute of Oncology, Warsaw, Poland
 7   Department of Health Management and Health Economics, University of Oslo, Oslo, Norway
,
12   Gastroenterology Unit, Copenhagen University Hospital – Amager and Hvidovre, Hvidovre, Denmark
13   Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark
,
Martin Keuchel
14   Clinic for Internal Medicine, Agaplesion Bethesda Krankenhaus Bergedorf, Hamburg, Germany
,
Mark Löwenberg
 1   Department of Gastroenterology and Hepatology, Amsterdam University Medical Centers, Amsterdam, The Netherlands
,
Ashraf Monged
15   Endoscopy Unit, Royal College of Surgeons of Ireland Hospitals Group, Dublin, Ireland
,
Olga M. Nardone
16   Institute of Translational Medicine and Institute of Immunology and Immunotherapy, University of Birmingham, Birmingham, UK
17   Gastroenterology, Department of Clinical Medicine and Surgery, University Federico II of Naples, Naples, Italy
,
18   Department of Medicine I, University Medical Center Mainz, Mainz, Germany
,
Mahmoud M. Omar
19   Department of Internal Medicine, Digestive Diseases and Endoscopy, New Mowasat Hospital, Salmiya, Kuwait
,
20   Gastroenterology Department, Endoscopy Unit, ICMDiM, Hospital Clinic, CIBEREHD, IDIBAPS, University of Barcelona, Catalonia, Spain
,
Laurent Peyrin-Biroulet
21   Department of Gastroenterology, University Hospital of Nancy, Nancy, France
,
22   Department of Gastroenterology, University Hospital of North Tees, Stockton-on-Tees, Cleveland, UK
,
 4   Department of Gastroenterology and Hepatology, University Hospital Leuven, TARGID, KU Leuven, Leuven, Belgium
› Author Affiliations

Abstract

The European Society of Gastrointestinal Endoscopy (ESGE) presents a short list of performance measures for colonoscopy in inflammatory bowel disease (IBD) patients. Current performance measures for colonoscopy mainly focus on detecting (pre)malignant lesions. However, these performance measures are not relevant for all colonoscopy indications in IBD patients. Therefore, our aim was to provide endoscopy services across Europe and other interested countries with a tool for quality monitoring and improvement in IBD colonoscopy. Eight key performance measures and one minor performance measure were recommended for measurement and evaluation in daily endoscopy practice.

* Equal first authors


Supplementary material



Publication History

Article published online:
29 July 2022

© 2022. European Society of Gastrointestinal Endoscopy. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 
  • References

  • 1 Rutter MD, Senore C, Bisschops R. et al. The European Society of Gastrointestinal Endoscopy Quality Improvement Initiative: developing performance measures. Endoscopy 2016; 48: 81-89
  • 2 Bisschops R, Areia M, Coron E. et al. Performance measures for upper gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2016; 48: 843-864
  • 3 Domagk D, Oppong KW, Aabakken L. et al. Performance measures for ERCP and endoscopic ultrasound: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2018; 50: 1116-1127
  • 4 Kaminski MF, Thomas-Gibson S, Bugajski M. et al. Performance measures for lower gastrointestinal endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2017; 49: 378-397
  • 5 Spada C, McNamara D, Despott EJ. et al. Performance measures for small-bowel endoscopy: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2019; 51: 574-598
  • 6 Valori R, Cortas G, de Lange T. et al. Performance measures for endoscopy services: a European Society of Gastrointestinal Endoscopy (ESGE) Quality Improvement Initiative. Endoscopy 2018; 50: 1186-1204
  • 7 Iacucci M, Cannatelli R, Tontini GE. et al. Improving the quality of surveillance colonoscopy in inflammatory bowel disease. Lancet Gastroenterol Hepatol 2019; 4: 971-983
  • 8 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
  • 9 Smith SCL, Cannatelli R, Bazarova A. et al. Performance measures in inflammatory bowel disease surveillance colonoscopy: Implementing changes to practice improves performance. Dig Endosc 2020; 32: 592-599
  • 10 Singh K, Al Khoury A, Kurti Z. et al. High adherence to surveillance guidelines in inflammatory bowel disease patients results in low colorectal cancer and dysplasia rates, while rates of dysplasia are low before the suggested onset of surveillance. J Crohns Colitis 2019; 13: 1343-1350
  • 11 Guyatt GH, Oxman AD, Vist GE. et al. GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008; 336: 924-926
  • 12 Frazzoni L, La Marca M, Radaelli F. et al. Systematic review with meta-analysis: the appropriateness of colonoscopy increases the probability of relevant findings and cancer while reducing unnecessary exams. Aliment Pharmacol Ther 2021; 53: 22-32
  • 13 Manes G, Imbesi V, Ardizzone S. et al. Appropriateness and diagnostic yield of colonoscopy in the management of patients with ulcerative colitis: a prospective study in an open access endoscopy service. Inflamm Bowel Dis 2008; 14: 1133-1138
  • 14 Hassan C, East J, Radaelli F. et al. Bowel preparation for colonoscopy: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – Update 2019. Endoscopy 2019; 51: 775-794
  • 15 Rutter MD. Importance of nonpolypoid (flat and depressed) colorectal neoplasms in screening for CRC in patients with IBD. Gastrointest Endosc Clin N Am 2014; 24: 327-335
  • 16 Megna B, Weiss J, Ley D. et al. Clear liquid diet before bowel preparation predicts successful chromoendoscopy in patients with inflammatory bowel disease. Gastrointest Endosc 2019; 89: 373-379 e2
  • 17 Negreanu L, Voiosu T, State M. et al. Quality of colonoscopy preparation in patients with inflammatory bowel disease: retrospective analysis of 348 colonoscopies. J Int Med Res 2020; 48: 300060520903654
  • 18 Aabakken L, Barkun AN, Cotton PB. et al. Standardized endoscopic reporting. J Gastroenterol Hepatol 2014; 29: 234-240
  • 19 Daperno M, Comberlato M, Bossa F. et al. Inter-observer agreement in endoscopic scoring systems: preliminary report of an ongoing study from the Italian Group for Inflammatory Bowel Disease (IG-IBD). Dig Liver Dis 2014; 46: 969-973
  • 20 Hart L, Chavannes M, Lakatos PL. et al. Do you see what I see? An assessment of endoscopic lesions recognition and description by gastroenterology trainees and staff physicians. . J Can Assoc Gastroenterol 2020; 3: 216-221
  • 21 Marques S, Bispo M, Pimentel-Nunes P. et al. Image documentation in gastrointestinal endoscopy: review of recommendations. GE Port J Gastroenterol 2017; 24: 269-274
  • 22 Neilson LJ, Bevan R, Panter S. et al. Terminal ileal intubation and biopsy in routine colonoscopy practice. Expert Rev Gastroenterol Hepatol 2015; 9: 567-574
  • 23 Ansari A, Soon SY, Saunders BP. et al. A prospective study of the technical feasibility of ileoscopy at colonoscopy. Scand J Gastroenterol 2003; 38: 1184-1186
  • 24 Makkar R, Lopez R, Shen B. Clinical utility of retrograde terminal ileum intubation in the evaluation of chronic non-bloody diarrhea. J Dig Dis 2013; 14: 536-542
  • 25 Morini S, Lorenzetti R, Stella F. et al. Retrograde ileoscopy in chronic nonbloody diarrhea: a prospective, case-control study. Am J Gastroenterol 2003; 98: 1512-1515
  • 26 Yusoff IF, Ormonde DG, Hoffman NE. Routine colonic mucosal biopsy and ileoscopy increases diagnostic yield in patients undergoing colonoscopy for diarrhea. J Gastroenterol Hepatol 2002; 17: 276-280
  • 27 Shergill AK, Lightdale JR. ASGE Standards of Practice Committee. et al. The role of endoscopy in inflammatory bowel disease. Gastrointest Endosc 2015; 81: 1101-1121
  • 28 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
  • 29 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
  • 30 Pouw RE, Bisschops R, Gecse KB. et al. Endoscopic tissue sampling – Part 2: Lower gastrointestinal tract. European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2021; 53: 1261-1273
  • 31 Bernstein CN, Eliakim A, Fedail S. et al. World Gastroenterology Organisation Global Guidelines Inflammatory Bowel Disease: Update August 2015. J Clin Gastroenterol 2016; 50: 803-818
  • 32 Hokama A, Kishimoto K, Nakamoto M. et al. Endoscopic and histopathological features of gastrointestinal amyloidosis. World J Gastrointest Endosc 2011; 3: 157-161
  • 33 Minematsu H, Hokama A, Makishi T. et al. Colonoscopic findings and pathologic characteristics of Strongyloides colitis: a case series. Digestion 2011; 83: 210-214
  • 34 Singh R, Balekuduru A, Simon EG. et al. The differentiation of amebic colitis from inflammatory bowel disease on endoscopic mucosal biopsies. Indian J Pathol Microbiol 2015; 58: 427-432
  • 35 Ye Z, Lin Y, Cao Q. et al. Granulomas as the most useful histopathological feature in distinguishing between Crohn's disease and intestinal tuberculosis in endoscopic biopsy specimens. Medicine (Baltimore) 2015; 94: e2157
  • 36 Abu Baker F, Z'Cruz De La Garza JA, Nafrin S. et al. Can microscopic ileitis in patients with clinically suspected inflammatory bowel disease predict the future?. BMC Gastroenterol 2020; 20: 52
  • 37 Novak G, Stevens T, van Viegen T. et al. Evaluation of optimal biopsy location for assessment of histological activity, transcriptomic and immunohistochemical analyses in patients with active Crohn's disease. Aliment Pharmacol Ther 2019; 49: 1401-1409
  • 38 Fiehn AK, Miehlke S, Aust D. et al. Distribution of histopathological features along the colon in microscopic colitis. Int J Colorectal Dis 2021; 36: 151-159
  • 39 Tontini GE, Bisschops R, Neumann H. Endoscopic scoring systems for inflammatory bowel disease: pros and cons. Expert Rev Gastroenterol Hepatol 2014; 8: 543-554
  • 40 Mohammed Vashist N, Samaan M, Mosli MH. et al. Endoscopic scoring indices for evaluation of disease activity in ulcerative colitis. Cochrane Database Syst Rev 2018; 1: Cd011450
  • 41 de Jong DC, Löwenberg M, Koumoutsos I. et al. Validation and investigation of the operating characteristics of the Ulcerative Colitis Endoscopic Index of Severity. Inflamm Bowel Dis 2019; 25: 937-944
  • 42 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
  • 43 Khanna R, Ma C, Jairath V. et al. Endoscopic assessment of inflammatory bowel disease activity in clinical trials. Clin Gastroenterol Hepatol 2022; 20: 727-736
  • 44 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
  • 45 Iacucci M, Smith SCL, Bazarova A. et al. An international multicenter real-life prospective study of electronic chromoendoscopy score PICaSSO in ulcerative colitis. Gastroenterology 2021; 160: 1558-1569
  • 46 Daperno M, D'Haens G, van Assche G. et al. Development and validation of a new, simplified endoscopic activity score for Crohnʼs disease: the SES-CD. Gastrointest Endosc 2004; 60: 505-512
  • 47 Friedman S, Rubin PH, Bodian C. et al. Screening and surveillance colonoscopy in chronic Crohn's colitis: results of a surveillance program spanning 25 years. Clin Gastroenterol Hepatol 2008; 6: 993-998
  • 48 Gillen CD, Walmsley RS, Prior P. et al. Ulcerative colitis and Crohn's disease: a comparison of the colorectal cancer risk in extensive colitis. Gut 1994; 35: 1590-1592
  • 49 Subramanian V, Ramappa V, Telakis E. et al. Comparison of high definition with standard white light endoscopy for detection of dysplastic lesions during surveillance colonoscopy in patients with colonic inflammatory bowel disease. Inflamm Bowel Dis 2013; 19: 350-355
  • 50 Blonski W, Kundu R, Lewis J. et al. Is dysplasia visible during surveillance colonoscopy in patients with ulcerative colitis?. Scand J Gastroenterol 2008; 43: 698-703
  • 51 Rubin DT, Rothe JA, Hetzel JT. et al. Are dysplasia and colorectal cancer endoscopically visible in patients with ulcerative colitis?. Gastrointest Endosc 2007; 65: 998-1004
  • 52 Bisschops R, East JE, Hassan C. et al. Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline – Update 2019. Endoscopy 2019; 51: 1155-1179
  • 53 Bisschops R, Bessissow T, Joseph JA. et al. Chromoendoscopy versus narrow band imaging in UC: a prospective randomised controlled trial. Gut 2018; 67: 1087-1094
  • 54 Iacucci M, Kaplan GG, Panaccione R. et al. A randomized trial comparing high definition colonoscopy alone with high definition dye spraying and electronic virtual chromoendoscopy for detection of colonic neoplastic lesions during IBD surveillance colonoscopy. Am J Gastroenterol 2018; 113: 225-234
  • 55 López-Serrano A, Suárez MJ, Besó P. et al. Virtual chromoendoscopy with iSCAN as an alternative method to dye-spray chromoendoscopy for dysplasia detection in long-standing colonic inflammatory bowel disease: a case-control study. Scand J Gastroenterol 2021; 56: 820-828
  • 56 Gasia MF, Ghosh S, Panaccione R. et al. Targeted biopsies identify larger proportions of patients with colonic neoplasia undergoing high-definition colonoscopy, dye chromoendoscopy, or electronic virtual chromoendoscopy. Clin Gastroenterol Hepatol 2016; 14: 704-712
  • 57 Hlavaty T, Huorka M, Koller T. et al. Colorectal cancer screening in patients with ulcerative and Crohn's colitis with use of colonoscopy, chromoendoscopy and confocal endomicroscopy. Eur J Gastroenterol Hepatol 2011; 23: 680-689
  • 58 Kandiah K, Subramaniam S, Thayalasekaran S. et al. Multicentre randomised controlled trial on virtual chromoendoscopy in the detection of neoplasia during colitis surveillance high-definition colonoscopy (the VIRTUOSO trial). Gut 2021; 70: 1684-1690
  • 59 Rutter MD, Saunders BP, Schofield G. et al. Pancolonic indigo carmine dye spraying for the detection of dysplasia in ulcerative colitis. Gut 2004; 53: 256-260
  • 60 Hu AB, Burke KE, Kochar B. et al. Yield of random biopsies during colonoscopies in inflammatory bowel disease patients undergoing dysplasia surveillance. Inflamm Bowel Dis 2021; 27: 779-786
  • 61 Moussata D, Allez M, Cazals-Hatem D. et al. Are random biopsies still useful for the detection of neoplasia in patients with IBD undergoing surveillance colonoscopy with chromoendoscopy?. Gut 2018; 67: 616-624
  • 62 Carballal S, Maisterra S, López-Serrano A. et al. Real-life chromoendoscopy for neoplasia detection and characterisation in long-standing IBD. Gut 2018; 67: 70-78
  • 63 Dekker E, Houwen B, Puig I. et al. Curriculum for optical diagnosis training in Europe: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy 2020; 52: 899-923
  • 64 Sanduleanu S, Rutter MD. Interval colorectal cancers in inflammatory bowel disease: the grim statistics and true stories. Gastrointest Endosc Clin N Am 2014; 24: 337-348
  • 65 Wintjens DSJ, Bogie RMM, van den Heuvel TRA. et al. Incidence and classification of postcolonoscopy colorectal cancers in inflammatory bowel disease: a Dutch population-based cohort study. J Crohns Colitis 2018; 12: 777-783
  • 66 Corley DA, Jensen CD, Marks AR. et al. Adenoma detection rate and risk of colorectal cancer and death. NEJM 2014; 370: 1298-1306
  • 67 Kaminski MF, Regula J, Kraszewska E. et al. Quality indicators for colonoscopy and the risk of interval cancer. NEJM 2010; 362: 1795-1803
  • 68 Mooiweer E, van der Meulen-de Jong AE, Ponsioen CY. et al. Chromoendoscopy for surveillance in inflammatory bowel disease does not increase neoplasia detection compared with conventional colonoscopy with random biopsies: results from a large retrospective study. Am J Gastroenterol 2015; 110: 1014-1021
  • 69 Lutgens MW, van Oijen MG, van der Heijden GJ. et al. Declining risk of colorectal cancer in inflammatory bowel disease: an updated meta-analysis of population-based cohort studies. Inflamm Bowel Dis 2013; 19: 789-799
  • 70 Weimers P, Ankersen DV, Løkkegaard ECL. et al. Occurrence of colorectal cancer and the influence of medical treatment in patients with inflammatory bowel disease: a Danish nationwide cohort study, 1997 to 2015. Inflamm Bowel Dis 2021; 27: 1795-1803
  • 71 Bisschops R, Rutter MD, Areia M. et al. Overcoming the barriers to dissemination and implementation of quality measures for gastrointestinal endoscopy: European Society of Gastrointestinal Endoscopy (ESGE) and United European Gastroenterology (UEG) position statement. Endoscopy 2021; 53: 196-202
  • 72 Bretthauer M, Aabakken L, Dekker E. et al. Requirements and standards facilitating quality improvement for reporting systems in gastrointestinal endoscopy: European Society of Gastrointestinal Endoscopy (ESGE) Position Statement. Endoscopy 2016; 48: 291-294
  • 73 Ivers N, Jamtvedt G, Flottorp S. et al. Audit and feedback: effects on professional practice and healthcare outcomes. Cochrane Database Syst Rev 2012;