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DOI: 10.1055/a-1671-6336
Endoscopic tissue sampling – Part 2: Lower gastrointestinal tract. European Society of Gastrointestinal Endoscopy (ESGE) Guideline
Recommendations
1 ESGE suggests performing segmental biopsies (at least two from each segment), which should be placed in different specimen containers (ileum, cecum, ascending, transverse, descending, and sigmoid colon, and rectum) in patients with clinical and endoscopic signs of colitis.
Weak recommendation, low quality of evidence.
2 ESGE recommends taking two biopsies from the right hemicolon (ascending and transverse colon) and, in a separate container, two biopsies from the left hemicolon (descending and sigmoid colon) when microscopic colitis is suspected.
Strong recommendation, low quality of evidence.
3 ESGE recommends pancolonic dye-based chromoendoscopy or virtual chromoendoscopy with targeted biopsies of any visible lesions during surveillance endoscopy in patients with inflammatory bowel disease.
Strong recommendation, moderate quality of evidence.
4 ESGE suggests that, in high risk patients with a history of colonic neoplasia, tubular-appearing colon, strictures, ongoing therapy-refractory inflammation, or primary sclerosing cholangitis, chromoendoscopy with targeted biopsies can be combined with four-quadrant non-targeted biopsies every 10 cm along the colon.
Weak recommendation, low quality of evidence.
5 ESGE recommends that, if pouch surveillance for dysplasia is performed, visible abnormalities should be biopsied, with at least two biopsies systematically taken from each of the afferent ileal loop, the efferent blind loop, the pouch, and the anorectal cuff.
Strong recommendation, low quality of evidence.
6 ESGE recommends that, in patients with known ulcerative colitis and endoscopic signs of inflammation, at least two biopsies be obtained from the worst affected areas for the assessment of activity or the presence of cytomegalovirus; for those with no evident endoscopic signs of inflammation, advanced imaging technologies may be useful in identifying areas for targeted biopsies to assess histologic remission if this would have therapeutic consequences.
Strong recommendation, low quality of evidence.
7 ESGE suggests not biopsying endoscopically visible inflammation or normal-appearing mucosa to assess disease activity in known Crohn’s disease.
Weak recommendation, low quality of evidence.
8 ESGE recommends that adequately assessed colorectal polyps that are judged to be premalignant should be fully excised rather than biopsied.
Strong recommendation, low quality of evidence.
9 ESGE recommends that, where endoscopically feasible, potentially malignant colorectal polyps should be excised en bloc rather than being biopsied. If the endoscopist cannot confidently perform en bloc excision at that time, careful representative images (rather than biopsies) should be taken of the potential focus of cancer, and the patient should be rescheduled or referred to an expert center.
Strong recommendation, low quality of evidence.
10 ESGE recommends that, in malignant lesions not amenable to endoscopic excision owing to deep invasion, six carefully targeted biopsies should be taken from the potential focus of cancer.
Strong recommendation, low quality of evidence.
Publication History
Received: 15 October 2021
Accepted after revision: 18 October 2021
Article published online:
29 October 2021
© 2021. European Society of Gastrointestinal Endoscopy. All rights reserved.
Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany
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References
- 1 Pouw RE, Barret M, Biermann K. et al. Endoscopic tissue sampling – Part 1: Upper gastrointestinal and hepatopancreatobiliary tracts. European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2021;
- 2 GRADE Working Group. Grading quality of evidence and strength of recommendations. BMJ 2004; 328: 1490
- 3 Dumonceau JM, Hassan C, Riphaus A. et al. European Society of Gastrointestinal Endoscopy (ESGE) Guideline Development Policy. Endoscopy 2012; 44: 626-629
- 4 Dejaco C, Oesterreicher C, Angelberger S. et al. Diagnosing colitis: a prospective study on essential parameters for reaching a diagnosis. Endoscopy 2003; 35: 1004-1008
- 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 Yantiss RK, Odze RD. Optimal approach to obtaining mucosal biopsies for assessment of inflammatory disorders of the gastrointestinal tract. Am J Gastroenterol 2009; 104; 774-783
- 7 Langner C, Aust D, Ensari A. et al. Histology of microscopic colitis – review with a practical approach for pathologists. Histopathology 2015; 66: 613-626
- 8 Nguyen GC, Smalley WE, Vege SS. et al. American Gastroenterological Association Institute Guideline on the medical management of microscopic colitis. Gastroenterol 2016; 150: 242-246
- 9 Arasaradnam RP, Brown S, Forbes A. et al. Guidelines for the investigation of chronic diarrhoea in adults: British Society of Gastroenterology, 3rd edition. Gut 2018; 67: 1380-1399
- 10 Münch A, Sanders DS, Molloy-Bland M. et al. Undiagnosed microscopic colitis: a hidden cause of chronic diarrhea and a frequently missed treatment opportunity. Frontline Gastroenterol 2019; 11: 228-234
- 11 Kanstrup Fiehn AM, Heiberg Engel PJ, Lanzarotto F. et al. Topographical distribution of microscopic colitis and the importance of orientation of paraffin-embedded biopsies. Human Pathol 2020; 103: 63-71
- 12 Kanstrup Fiehn AM, Miehlke S, Aust D. et al. Distribution of histopathological features along the colon in microscopic colitis. Int J Colorectal Dis 2021; 36: 151-159
- 13 Seenarain V, Idrees M, Mogridge J. et al. Random colonic biopsies in macroscopically normal colonoscopies: is there any benefit? A two-centre audit of current practice.. ANZ J Surg 2020; 90: E163-E167
- 14 Miehlke S, Guagnozzi D, Zabana Y. et al. European guidelines on microscopic colitis: United European Gastroenterology and European Microscopic Colitis Group statements and recommendations. United European Gastroenterol J 2021; 9: 13-37
- 15 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
- 16 Jess T, Rungoe C, Peyrin-Biroulet L. Risk of colorectal cancer in patients with ulcerative colitis: a meta-analysis of population-based cohort studies. Clin Gastroenterol Hepatol 2012; 10: 639-645
- 17 Rutter MD, Saunders BP, Wilkinson KH. et al. Cancer surveillance in longstanding ulcerative colitis: endoscopic appearances help predict cancer risk. Gut 2004; 53: 1813-1816
- 18 Rutter MD, Saunders BP, Wilkinson KH. et al. Thirty-year analysis of a colonoscopic surveillance program for neoplasia in ulcerative colitis. Gastroenterol 2006; 130: 1030-1038
- 19 Mahmoud R, Shah SC, Ten Hove JR. et al. No association between pseudopolyps and colorectal neoplasia in patients with inflammatory bowel diseases. Gastroenterol 2019; 156: 1333-1344
- 20 Barclay RL, Vicari JJ, Doughty AS. et al. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy. NEJM 2006; 355: 2533-2541
- 21 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
- 22 Subramanian V, Mannath J, Ragunath K. et al. Meta-analysis: the diagnostic yield of chromoendoscopy for detecting dysplasia in patients with colonic inflammatory bowel disease. Aliment Pharmacol Ther 2011; 33: 304-312
- 23 van den Broek FJ, Stokkers PC, Reitsma JB. et al. Random biopsies taken during colonoscopic surveillance of patients with longstanding ulcerative colitis: low yield and absence of clinical consequences. Am J Gastroenterol 2014; 109: 715-722
- 24 Imperatore N, Castiglione F, Testa A. et al. Augmented endoscopy for surveillance of colonic inflammatory bowel disease: systematic review with network meta-analysis. J Crohns Colitis 2019; 13: 714-724
- 25 Yang DH, Park SJ, Kim HS. et al. High-definition chromoendoscopy versus high-definition white light colonoscopy for neoplasia surveillance in ulcerative colitis: a randomized controlled trial. Am J Gastroenterol 2019; 114: 1642-1648
- 26 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
- 27 Feuerstein JD, Rakowsky S, Sattler L. et al. Meta-analysis of dye-based chromoendoscopy compared with standard- and high-definition white-light endoscopy in patients with inflammatory bowel disease at increased risk of colon cancer. Gastrointest Endosc 2019; 90: 186-195
- 28 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
- 29 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
- 30 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
- 31 Torres C, Antonioli D, Odze RD. Polypoid dysplasia and adenomas in inflammatory bowel disease: a clinical, pathologic, and follow-up study of 89 polyps from 59 patients. Am J Surg Pathol 1998; 22: 275-284
- 32 Krugliak Cleveland N, Huo D, Sadiq F. et al. Assessment of peri-polyp biopsy specimens of flat mucosa in patients with inflammatory bowel disease. Gastrointest Endosc 2018; 87: 1304-1309
- 33 Ten Hove JR, Mooiweer E, Dekker E. et al. Low rate of dysplasia detection in mucosa surrounding dysplastic lesions in patients undergoing surveillance for inflammatory bowel diseases. Clin Gastroenterol Hepatol 2017; 15: 222-228
- 34 Lahiff C, Wang LM, Travis SPL. et al. Diagnostic yield of dysplasia in polyp-adjacent biopsies for patients with inflammatory bowel disease: a cross-sectional study. J Crohns Colitis 2018; 12: 670-676
- 35 Lamb CA, Kennedy NA, Raine T. et al. British Society of Gastroenterology consensus guidelines on the management of inflammatory bowel disease in adults. Gut 2019; 68: s1-s106
- 36 Annese V, Beaugerie L, Egan L. et al. European evidence-based consensus: inflammatory bowel disease and malignancies. J Crohns Colitis 2015; 9: 945-965
- 37 Kariv R, Remzi FH, Lian L. et al. Preoperative colorectal neoplasia increases risk for pouch neoplasia in patients with restorative proctocolectomy. Gastroenterol 2010; 139: 806-812
- 38 Derikx LAAP, Kievit W, Drenth JPH. et al. Prior colorectal neoplasia is associated with increased risk of ileoanal pouch neoplasia in patients with inflammatory bowel disease. Gastroenterol 2014; 146: 119-128
- 39 Scarpa M, van Koperen PJ, Ubbink DT. et al. Systematic review of dysplasia after restorative proctocolectomy for ulcerative colitis. Br J Surg 2007; 94: 534-545
- 40 Kuiper T, Vlug MS, van den Broek FJ. et al. The prevalence of dysplasia in the ileoanal pouch following restorative proctocolectomy for ulcerative colitis with associated dysplasia. Colorectal Dis 2012; 14: 469-473
- 41 Zhao-Xiu L, Ming-Bing X, Xian-Rui W. et al. Chronic pouchitis is associated with pouch polyp formation in patients with underlying ulcerative colitis. J Crohns Colitis 2014; 8: 363-369
- 42 Vento P, Lepistö A, Kärkkäinen P. et al. Risk of cancer in patients with chronic pouchitis after restorative proctocolectomy for ulcerative colitis. Colorectal Dis 2011; 13: 58-66
- 43 Zhu H, Wu XR, Queener E. et al. Chronic pouchitis is associated with pouch polyp formation in patients with underlying ulcerative colitis. J Crohns Colitis 2014; 8: 363-369
- 44 Herline AJ, Meisinger LL, Rusin LC. et al. Is routine pouch surveillance for dysplasia indicated for ileoanal pouches?. Dis Colon Rectum 2003; 46: 156-159
- 45 Nilubol N, Scherl E, Bub DS. et al. Mucosal dysplasia in ileal pelvic pouches after restorative proctocolectomy. Dis Colon Rectum 2007; 50: 825-831
- 46 Bryant RV, Burger DC, Delo J. et al. Beyond endoscopic mucosal healing in UC: histological remission better predicts corticosteroid use and hospitalisation over 6 years of follow-up. Gut 2016; 65: 408-414
- 47 Lemmens B, Arijs I, van Assche G. et al. Correlation between the endoscopic and histologic score in assessing the activity of ulcerative colitis. Inflamm Bowel Dis 2013; 19: 1194-1201
- 48 Simsek HD, Basyigit S, Aktas B. et al. Assessment of the correlation between endoscopic activity and histological activity in ulcerative colitis patients. Med Princ Pract 2016; 25: 378-384
- 49 Iacucci M, Fort Gasia M, Hassan C. et al. Complete mucosal healing defined by endoscopic Mayo subscore still demonstrates abnormalities by novel high definition colonoscopy and refined histological gradings. Endoscopy 2015; 47: 726-734
- 50 Iacucci M, Kiesslich R, Gui X. et al. Beyond white light: optical enhancement in conjunction with magnification colonoscopy for the assessment of mucosal healing in ulcerative colitis. Endoscopy 2017; 49: 553-559
- 51 Marchal-Bressenot A, Salleron J, Boulagnon-Rombi C. et al. Development and validation of the Nancy histological index for UC. Gut 2017; 66: 43-49
- 52 Mosli MH, Feagan BG, Zou G. et al. Development and validation of a histological index for UC. Gut 2017; 66: 50-58
- 53 Schroeder KW, Tremaine WJ, Ilstrup DM. Coated oral 5-aminosalicylic acid therapy for mildly to moderately active ulcerative colitis. A randomized study. NEJM 1987; 317: 1625-1629
- 54 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
- 55 Osterman MT, Scott FI, Fogt FF. et al. Endoscopic and histological assessment, correlation, and relapse in clinically quiescent ulcerative colitis (MARQUEE). Inflamm Bowel Dis 2021; 27: 207-214
- 56 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
- 57 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.e8
- 58 Novak G, Parker CE, Pai RK. et al. Histologic scoring indices for evaluation of disease activity in Crohn's disease. Cochrane Database Syst Rev 2017; 7: CD012351
- 59 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
- 60 Dragasevic S, Sokic-Milutinovic A, Stojkovic Lalosevic M. et al. Correlation of patient-reported outcome (PRO-2) with endoscopic and histological features in ulcerative colitis and Crohn's disease patients. Gastroenterol Res Pract 2020; 2020: 2065383
- 61 Molander P, Sipponen T, Kemppainen H. et al. Achievement of deep remission during scheduled maintenance therapy with TNFα-blocking agents in IBD. J Crohns Colitis 2013; 7: 730-735
- 62 Tajra JB, Calegaro JU, de Paula AP. et al. Correlation and concordance measures between clinical, endoscopic and histological scores activity in Crohn's disease under treatment. Gastroenterol 2019; 54: 441-445
- 63 Gong W, Guo K, Zheng T. et al. Correlation between endoscopic and histological validated scoring indices in Crohn's disease. Dig Liver Dis 2019; 51: 812-817
- 64 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
- 65 Sipponen T, Kärkkäinen P, Savilahti E. et al. Correlation of faecal calprotectin and lactoferrin with an endoscopic score for Crohn's disease and histological findings. Aliment Pharmacol Ther 2008; 28: 1221-1229
- 66 Lang-Schwarz C, Angeloni M, Agaimy A. et al. Validation of the ‘Inflammatory Bowel Disease–Distribution, Chronicity, Activity (IBD-DCA) Score’ for ulcerative colitis and Crohn’s disease. J Crohns Colitis 2021; 15: 1621-1630
- 67 Brennan GT, Melton SD, Spechler SJ. et al. Clinical implications of histologic abnormalities in ileocolonic biopsies of patients with Crohn's disease in remission. J Clin Gastroenterol 2017; 51: 43-48
- 68 Bateman AC, Patel P. Lower gastrointestinal endoscopy: guidance on indications for biopsy. Frontline Gastroenterol 2014; 5: 96-102
- 69 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
- 70 Komeda Y, Kashida H, Sakurai T. et al. Magnifying narrow band imaging (NBI) for the diagnosis of localized colorectal lesions using the Japan NBI Expert Team (JNET) classification. Oncology 2017; 93: 49-54
- 71 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. Gastroenterol 2012; 143: 599-607
- 72 Rutter MD, Chattree A, Barbour JA. et al. British Society of Gastroenterology/Association of Coloproctologists of Great Britain and Ireland guidelines for the management of large non-pedunculated colorectal polyps. Gut 2015; 64: 1847-1873
- 73 Cho SB, Park SY, Yoon KW. et al. [The effect of post-biopsy scar on the submucosal elevation for endoscopic resection of rectal carcinoids]. Korean J Gastroenterol 2009; 53: 36-42
- 74 Han KS, Sohn DK, Choi DH. et al. Prolongation of the period between biopsy and EMR can influence the nonlifting sign in endoscopically resectable colorectal cancers. Gastrointest Endosc 2008; 67: 97-102
- 75 Chen CH, Wu KL, Hu ML. et al. Is a biopsy necessary for colon polyps suitable for polypectomy when performing a colonoscopy?. Chang Gung Med J 2011; 34: 506-511
- 76 Absar MS, Haboubi NY. Colonic neoplastic polyps: biopsy is not efficient to exclude malignancy. The Trafford experience. Tech Coloproctol 2004; 8: s257-s260
- 77 Gondal G, Grotmol T, Hofstad B. et al. Biopsy of colorectal polyps is not adequate for grading of neoplasia. Endoscopy 2005; 37: 1193-1197
- 78 Sung HY, Cheung DY, Cho SH. et al. Polyps in the gastrointestinal tract: discrepancy between endoscopic forceps biopsies and resected specimens. Eur J Gastroenterol Hepatol 2009; 21: 190-195
- 79 Blumberg D. Laparoscopic colon resection of benign polyps: high grade dysplasia on endoscopic biopsy and polyp location predict risk of cancer. Surg Laparosc Endosc Percutan Tech 2009; 19: 255-257
- 80 Marshall JB, Diaz-Arias AA, Barthel JS. et al. Prospective evaluation of optimal number of biopsy specimens and brush cytology in the diagnosis of cancer of the colorectum. Am J Gastroenterol 1993; 88: 1352-1354
- 81 Choi Y, Choi HS, Jeon WK. et al. Optimal number of endoscopic biopsies in diagnosis of advanced gastric and colorectal cancer. J Korean Med Sci 2012; 27: 36-39
- 82 Gado A, Ebeid B, Abdelmohsen A. et al. Improving the yield of histological sampling in patients with suspected colorectal cancer during colonoscopy by introducing a colonoscopy quality assurance program. Gastroenterology Res 2011; 4: 157-161
- 83 Backes Y, Seerden TCJ, van Gestel R. et al. Tumor seeding during colonoscopy as a possible cause for metachronous colorectal cancer. Gastroenterol 2019; 157: 1222-1232
- 84 Hassan C, Ponchon T, Bisschops R. et al. European Society of Gastrointestinal Endoscopy (ESGE) Publications Policy – Update 2020. Endoscopy 2020; 52: 123-126