Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline

Michał F. Kamiński; Cesare Hassan; Raf Bisschops; Jürgen Pohl; Maria Pellisé; Evelien Dekker; Ana Ignjatovic-Wilson; Arthur Hoffman; Gaius Longcroft-Wheaton; Denis Heresbach; Jean-Marc Dumonceau; James E. East

doi:10.1055/s-0034-1365348

Endoscopy, Table of Contents

Endoscopy 2014; 46(05): 435-457
DOI: 10.1055/s-0034-1365348

Guideline

Advanced imaging for detection and differentiation of colorectal neoplasia: European Society of Gastrointestinal Endoscopy (ESGE) Guideline

Michał F. Kamiński

¹Department of Gastroenterology and Hepatology, Medical Centre for Postgraduate Education, Maria Sklodowska-Curie Memorial Cancer Centre and Institute of Oncology, Warsaw, Poland

,

Cesare Hassan

²Digestive Endoscopy Unit, Nuovo Regina Margherita Hospital, Rome, Italy

,

Raf Bisschops

³Department of Gastroenterology, University Hospital Leuven, Leuven, Belgium

,

Jürgen Pohl

⁴Department of Gastroenterology and Interventional Endoscopy, Klinikum im Friedrichshain, Berlin, Germany

,

Maria Pellisé

⁵Department of Gastroenterology, Institut de Malaties Digestives i Metabòliques, Hospital Clinic, Barcelona, Spain

,

Evelien Dekker

⁶Department of Gastroenterology and Hepatology, Academic Medical Centre, Amsterdam, The Netherlands

,

Ana Ignjatovic-Wilson

⁷Wolfson Unit for Endoscopy, St Mark's Hospital, Imperial College London, UK

,

Arthur Hoffman

⁸Medizinische Klinik, St. Mary Hospital, Frankfurt, Germany

,

Gaius Longcroft-Wheaton

⁹Department of Gastroenterology, Queen Alexandra Hospital, Portsmouth Hospitals NHS Trust, Portsmouth, United Kingdom

,

Denis Heresbach

¹⁰Department of Gastroenterology, University Hospital, CHU Rennes, France

,

Jean-Marc Dumonceau

¹¹Gedyt Endoscopy Center, Buenos Aires, Argentina

,

James E. East

¹²Translational Gastroenterology Unit, John Radcliffe Hospital, Oxford University, Oxford, United Kingdom.

› Author Affiliations

Abstract

This Guideline is an official statement of the European Society of Gastrointestinal Endoscopy (ESGE). It addresses the role of advanced endoscopic imaging for the detection and differentiation of colorectal neoplasia.

Main recommendations

1 ESGE suggests the routine use of high definition white-light endoscopy systems for detecting colorectal neoplasia in average risk populations (weak recommendation, moderate quality evidence).

2 ESGE recommends the routine use of high definition systems and pancolonic conventional or virtual (narrow band imaging [NBI], i-SCAN) chromoendoscopy in patients with known or suspected Lynch syndrome (strong recommendation, low quality evidence).

2b ESGE recommends the routine use of high definition systems and pancolonic conventional or virtual (NBI) chromoendoscopy in patients with known or suspected serrated polyposis syndrome (strong recommendation, low quality evidence).

3 ESGE recommends the routine use of 0.1 % methylene blue or 0.1 % – 0.5 % indigo carmine pancolonic chromoendoscopy with targeted biopsies for neoplasia surveillance in patients with long-standing colitis. In appropriately trained hands, in the situation of quiescent disease activity and adequate bowel preparation, nontargeted, four-quadrant biopsies can be abandoned (strong recommendation, high quality evidence).

4 ESGE suggests that virtual chromoendoscopy (NBI, FICE, i-SCAN) and conventional chromoendoscopy can be used, under strictly controlled conditions, for real-time optical diagnosis of diminutive (≤ 5 mm) colorectal polyps to replace histopathological diagnosis. The optical diagnosis has to be reported using validated scales, must be adequately photodocumented, and can be performed only by experienced endoscopists who are adequately trained and audited (weak recommendation, high quality evidence).

5 ESGE suggests the use of conventional or virtual (NBI) magnified chromoendoscopy to predict the risk of invasive cancer and deep submucosal invasion in lesions such as those with a depressed component (0-IIc according to the Paris classification) or nongranular or mixed-type laterally spreading tumors (weak recommendation, moderate quality evidence).

Conclusion

Advanced imaging techniques will need to be applied in specific patient groups in routine clinical practice and to be taught in endoscopic training programs.

Full Text

References

References
1 Stock C, Brenner H. Utilization of lower gastrointestinal endoscopy and fecal occult blood test in 11 European countries: evidence from the Survey of Health, Aging and Retirement in Europe (SHARE). Endoscopy 2010; 42: 546-556
2 Sonnenberg A, Amorosi SL, Lacey MJ et al. Patterns of endoscopy in the United States: analysis of data from the Centers for Medicare and Medicaid Services and the National Endoscopic Database. Gastrointest Endosc 2008; 67: 489-496
3 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
4 Meester RG, Corley DA, Doubeni CA et al. Impact of variation in screening colonoscopy quality on the prevention of colorectal cancer deaths. A modelling study. Gastroenterology 2013; 144: 190
5 Rex DK. Maximizing detection of adenomas and cancers during colonoscopy. Am J Gastroenterol 2006; 101: 2866-2877
6 Spiegel BM, Ho W, Esrailian E et al. Controversies in ulcerative colitis: a survey comparing decision making of experts versus community gastroenterologists. Clin Gastroenterol Hepatol 2009; 7: 168-174 , 174 e1
7 Richardson WWM, Nishikawa J, Hayward R. The well-built clinical question: A key to evidence-based decisions. ACP Journal Club 1995; 123: A12-A13
8 Atkins D, Best D, Briss PA et al. Grading quality of evidence and strength of recommendations. BMJ 2004; 328: 1490
9 Wanders LK, East JE, Uitentuis SE et al. Diagnostic performance of narrowed spectrum endoscopy, autofluorescence imaging, and confocal laser endomicroscopy for optical diagnosis of colonic polyps: a meta-analysis. Lancet Oncol 2013; 14: 1337-1347 [Epub 2013 Nov 13]
10 Dumonceau JM, Hassan C, Riphaus A et al. European Society of Gastrointestinal Endoscopy (ESGE) Guideline Development Policy. Endoscopy 2012; 44: 626-629
11 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
12 von Karsa L, Patnick J. European Colorectal Cancer Screening Guidelines Working Group et al. European guidelines for quality assurance in colorectal cancer screening and diagnosis: overview and introduction to the full supplement publication. Endoscopy 2013; 45: 51-59
13 Lieberman DA, Holub J, Eisen G et al. Utilization of colonoscopy in the United States: results from a national consortium. Gastrointest Endosc 2005; 62: 875-883
14 Subramanian V, Mannath J, Hawkey CJ et al. High definition colonoscopy vs. standard video endoscopy for the detection of colonic polyps: a meta-analysis. Endoscopy 2011; 43: 499-505
15 Deenadayalu VP, Chadalawada V, Rex DK. 170 degrees wide-angle colonoscope: effect on efficiency and miss rates. Am J Gastroenterol 2004; 99: 2138-2142
16 Fatima H, Rex DK, Rothstein R et al. Cecal insertion and withdrawal times with wide-angle versus standard colonoscopes: a randomized controlled trial. Clin Gastroenterol Hepatol 2008; 6: 109-114
17 Rex DK, Chadalawada V, Helper DJ. Wide angle colonoscopy with a prototype instrument: impact on miss rates and efficiency as determined by back-to-back colonoscopies. Am J Gastroenterol 2003; 98: 2000-2005
18 Rastogi A, Early DS, Gupta N et al. Randomized, controlled trial of standard-definition white-light, high-definition white-light, and narrow-band imaging colonoscopy for the detection of colon polyps and prediction of polyp histology. Gastrointest Endosc 2011; 74: 593-602
19 Brown SR, Baraza W. Chromoscopy versus conventional endoscopy for the detection of polyps in the colon and rectum. Cochrane Database Syst Rev 2010; CD006439
20 Pohl J, Schneider A, Vogell H et al. Pancolonic chromoendoscopy with indigo carmine versus standard colonoscopy for detection of neoplastic lesions: a randomised two-centre trial. Gut 2011; 60: 485-490
21 Togashi K, Hewett DG, Radford-Smith GL et al. The use of indigocarmine spray increases the colonoscopic detection rate of adenomas. J Gastroenterol 2009; 44: 826-833
22 Hashimoto K, Higaki S, Nishiahi M et al. Does chromoendoscopy improve the colonoscopic adenoma detection rate?. Hepatogastroenterology 2010; 57: 1399-1404
23 Kahi CJ, Anderson JC, Waxman I et al. High-definition chromocolonoscopy vs. high-definition white light colonoscopy for average-risk colorectal cancer screening. Am J Gastroenterol 2010; 105: 1301-1307
24 Dinesen L, Chua TJ, Kaffes AJ. Meta-analysis of narrow-band imaging versus conventional colonoscopy for adenoma detection. Gastrointest Endosc 2012; 75: 604-611
25 Pasha SF, Leighton JA, Das A et al. Comparison of the yield and miss rate of narrow band imaging and white light endoscopy in patients undergoing screening or surveillance colonoscopy: a meta-analysis. Am J Gastroenterol 2012; 107: 363-370
26 Kaltenbach T, Friedland S, Soetikno R. A randomised tandem colonoscopy trial of narrow band imaging versus white light examination to compare neoplasia miss rates. Gut 2008; 57: 1406-1412
27 Rex DK, Helbig CC. High yields of small and flat adenomas with high-definition colonoscopes using either white light or narrow band imaging. Gastroenterology 2007; 133: 42-47
28 Inoue T, Murano M, Murano N et al. Comparative study of conventional colonoscopy and pan-colonic narrow-band imaging system in the detection of neoplastic colonic polyps: a randomized, controlled trial. J Gastroenterol 2008; 43: 45-50
29 Adler A, Aschenbeck J, Yenerim T et al. Narrow-band versus white-light high definition television endoscopic imaging for screening colonoscopy: a prospective randomized trial. Gastroenterology 2009; 136: 410-416 e1 ; quiz 715
30 Paggi S, Radaelli F, Amato A et al. The impact of narrow band imaging in screening colonoscopy: a randomized controlled trial. Clin Gastroenterol Hepatol 2009; 7: 1049-1054
31 East JE, Ignjatovic A, Suzuki N et al. A randomized, controlled trial of narrow-band imaging vs high-definition white light for adenoma detection in patients at high risk of adenomas. Colorectal Dis 2012; 14: e771-e778
32 Stipho S, Gilani N, Ramirez F. The clinical utilty of high-definition magnification endoscopy with and without narrow band imaging for detection of colonic neoplasia. Gastrointest Endosc 2008; 67: AB130
33 Glenn T, Hoffmann BJ, Romagnuolo J et al. Does narrow band imaging (NBI) enhance colon polyp detection?. Gastrointest Endosc 2005; 61: AB227
34 Inaba Y, Watari J, Okamoto K et al. Usefulness of narrow band imaging as a digital chromoendoscopy in screening colonoscopy: a prospective pilot study. Gastrointest Endosc 2005; 61: AB228
35 Sabbagh LC, Reveiz L, Aponte D et al. Narrow-band imaging does not improve detection of colorectal polyps when compared to conventional colonoscopy: a randomized controlled trial and meta-analysis of published studies. BMC Gastroenterol 2011; 11: 100
36 Pohl J, Lotterer E, Balzer C et al. Computed virtual chromoendoscopy versus standard colonoscopy with targeted indigocarmine chromoscopy: a randomised multicentre trial. Gut 2009; 58: 73-78
37 Chung SJ, Kim D, Song JH et al. Efficacy of computed virtual chromoendoscopy on colorectal cancer screening: a prospective, randomized, back-to-back trial of Fuji Intelligent Color Enhancement versus conventional colonoscopy to compare adenoma miss rates. Gastrointest Endosc 2010; 72: 136-142
38 Hong SN, Choe WH, Lee JH et al. Prospective, randomized, back-to-back trial evaluating the usefulness of i-SCAN in screening colonoscopy. Gastrointest Endosc 2012; 75: 1011-1021.e2
39 Kuiper T, van den Broek FJ, Naber AH et al. Endoscopic trimodal imaging detects colonic neoplasia as well as standard video endoscopy. Gastroenterology 2011; 140: 1887-1894
40 van den Broek FJ, Fockens P, Van Eeden S et al. Clinical evaluation of endoscopic trimodal imaging for the detection and differentiation of colonic polyps. Clin Gastroenterol Hepatol 2009; 7: 288-295
41 Matsuda T, Saito Y, Fu KI et al. Does autofluorescence imaging videoendoscopy system improve the colonoscopic polyp detection rate? –a pilot study. Am J Gastroenterol 2008; 103: 1926-1932
42 Takeuchi Y, Inoue T, Hanaoka N et al. Autofluorescence imaging with a transparent hood for detection of colorectal neoplasms: a prospective, randomized trial. Gastrointest Endosc 2010; 72: 1006-1013
43 Rotondano G, Bianco MA, Sansone S et al. Trimodal endoscopic imaging for the detection and differentiation of colorectal adenomas: a prospective single-centre clinical evaluation. Int J Colorectal Dis 2012; 27: 331-336
44 He Q, Li JD, An SL et al. Cap-assisted colonoscopy versus conventional colonoscopy: systematic review and meta-analysis. Int J Colorectal Dis 2013; 28: 279-281
45 Ng SC, Tsoi KKF, Hirai HW et al. The efficacy of cap-assisted colonoscopy in polyp detection and cecal intubation: a meta-analysis of randomized controlled trials. Am J Gastroenterol 2012; 107: 1165-1173
46 Westwood DA, Alexakis N, Connor SJ. Transparent cap-assisted colonoscopy versus standard adult colonoscopy: a systematic review and meta-analysis. Dis Colon Rectum 2012; 55: 218-225
47 Morgan J, Thomas K, Lee-Robichaud H et al. Transparent cap colonoscopy versus standard colonoscopy for investigation of gastrointestinal tract conditions. Cochrane Database Syst Rev 16.02.2011; 2
48 Leufkens AM, DeMarco DC, Rastogi A. Effect of a retrograde-viewing device on adenoma detection rate during colonoscopy: the TERRACE study. Gastrointest Endosc 2011; 73: 480-489
49 Mamula P, Tierney WM, Banerjee S et al. Devices to improve colon polyp detection. Gastrointest Endosc 2011; 73: 1092-1097
50 Wallace MH, Frayling IM, Clark SK et al. Attenuated adenomatous polyposis coli: the role of ascertainment bias through failure to dye-spray at colonoscopy. Dis Colon Rectum 1999; 42: 1078-1080
51 East JE, Saunders BP, Jass JR. Sporadic and syndromic hyperplastic polyps and serrated adenomas of the colon: classification, molecular genetics, natural history, and clinical management. Gastroenterol Clin North Am 2008; 37: 25-46
52 Jarvinen HJ, Aarnio M, Mustonen H et al. Controlled 15-year trial on screening for colorectal cancer in families with hereditary nonpolyposis colorectal cancer. Gastroenterology 2000; 118: 829-834
53 Cairns SR, Scholefield JH, Steele RJ et al. Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 2010; 59: 666-689
54 Rex DK, Ahnen DJ, Baron JA et al. Serrated lesions of the colorectum: review and recommendations from an expert panel. Am J Gastroenterol 2012; 107: 1315-1329 ; quiz 1314, 1330
55 Boparai KS, Mathus-Vliegen EM, Koornstra JJ et al. Increased colorectal cancer risk during follow-up in patients with hyperplastic polyposis syndrome: a multicentre cohort study. Gut 2010; 59: 1094-1100
56 Vasen HF, Abdirahman M, Brohet R et al. One to 2-year surveillance intervals reduce risk of colorectal cancer in families with Lynch syndrome. Gastroenterology 2010; 138: 2300-2306
57 Rondagh EJ, Gulikers S, Gomez-Garcia EB et al. Nonpolypoid colorectal neoplasms: a challenge in endoscopic surveillance of patients with Lynch syndrome. Endoscopy 2013; 45: 257-264
58 Hazewinkel Y, Lopez-Ceron M, East JE et al. Endoscopic features of sessile serrated adenomas: validation by international experts using high-resolution white-light endoscopy and narrow-band imaging. Gastrointest Endosc 2013; 77: 916-924
59 Hurlstone DP, Karajeh M, Cross SS et al. The role of high-magnification-chromoscopic colonoscopy in hereditary nonpolyposis colorectal cancer screening: a prospective “back-to-back” endoscopic study. Am J Gastroenterol 2005; 100: 2167-2173
60 Lecomte T, Cellier C, Meatchi T et al. Chromoendoscopic colonoscopy for detecting preneoplastic lesions in hereditary nonpolyposis colorectal cancer syndrome. Clin Gastroenterol Hepatol 2005; 3: 897-902
61 Huneburg R, Lammert F, Rabe C et al. Chromocolonoscopy detects more adenomas than white light colonoscopy or narrow band imaging colonoscopy in hereditary nonpolyposis colorectal cancer screening. Endoscopy 2009; 41: 316-322
62 Stoffel EM, Turgeon DK, Stockwell DH et al. Missed adenomas during colonoscopic surveillance in individuals with Lynch syndrome (hereditary nonpolyposis colorectal cancer). Cancer Prev Res (Phila) 2008; 1: 470-475
63 East JE, Suzuki N, Stavrinidis M et al. Narrow band imaging for colonoscopic surveillance in hereditary non-polyposis colorectal cancer. Gut 2008; 57: 65-70
64 Bisschops R, Tejpar S, Willekens H et al. I-scan detects more polyps in Lynch Syndrome (HNPCC) patients: a prospective controlled randomized back-to-back study. Gastrointest Endosc 2012; 75: AB330
65 Ramsoekh D, Haringsma J, Poley JW et al. A back-to-back comparison of white light video endoscopy with autofluorescence endoscopy for adenoma detection in high-risk subjects. Gut 2010; 59: 785-793
66 Boparai KS, van den Broek FJ, van Eeden S et al. Increased polyp detection using narrow band imaging compared with high resolution endoscopy in patients with hyperplastic polyposis syndrome. Endoscopy 2011; 43: 676-682
67 Boparai KS, van den Broek FJ, van Eeden S et al. Hyperplastic polyposis syndrome: a pilot study for the differentiation of polyps by using high-resolution endoscopy, autofluorescence imaging, and narrow-band imaging. Gastrointest Endosc 2009; 70: 947-955
68 Soravia C, Berk T, Madlensky L et al. Genotype-phenotype correlations in attenuated adenomatous polyposis coli. Am J Hum Genet 1998; 62: 1290-1301
69 Heiskanen I, Luostarinen T, Jarvinen HJ. Impact of screening examinations on survival in familial adenomatous polyposis. Scand J Gastroenterol 2000; 35: 1284-1287
70 Matsumoto T, Esaki M, Fujisawa R et al. Chromoendoscopy, narrow-band imaging colonoscopy, and autofluorescence colonoscopy for detection of diminutive colorectal neoplasia in familial adenomatous polyposis. Dis Colon Rectum 2009; 52: 1160-1165
71 Friederich P, de Jong AE, Mathus-Vliegen LM et al. Risk of developing adenomas and carcinomas in the ileal pouch in patients with familial adenomatous polyposis. Clin Gastroenterol Hepatol 2008; 6: 1237-1242
72 Tajika M, Nakamura T, Nakahara O et al. Prevalence of adenomas and carcinomas in the ileal pouch after proctocolectomy in patients with familial adenomatous polyposis. J Gastrointest Surg 2009; 13: 1266-1273
73 Van Assche G, Dignass A, Bokemeyer B et al. Second European evidence-based consensus on the diagnosis and management of ulcerative colitis part 3: special situations. J Crohns Colitis 2013; 7: 1-33
74 Rutter MD, Saunders BP, Wilkinson KH et al. Thirty-year analysis of a colonoscopic surveillance program for neoplasia in ulcerative colitis. Gastroenterology 2006; 130: 1030-1038
75 Watanabe K, Sogawa M, Yamagami H et al. Endoscopic differential diagnosis between ulcerative colitis-associated neoplasia and sporadic neoplasia in surveillance colonoscopy using narrow band imaging. Dig Endosc 2011; 23 (Suppl. 01) 143-149
76 Hurlstone DP, Sanders DS, Atkinson R et al. Endoscopic mucosal resection for flat neoplasia in chronic ulcerative colitis: can we change the endoscopic management paradigm?. Gut 2007; 56: 838-846
77 Kiesslich R, Fritsch J, Holtmann M et al. Methylene blue-aided chromoendoscopy for the detection of intraepithelial neoplasia and colon cancer in ulcerative colitis. Gastroenterology 2003; 124: 880-888
78 Kiesslich R, Goetz M, Lammersdorf K et al. Chromoscopy-guided endomicroscopy increases the diagnostic yield of intraepithelial neoplasia in ulcerative colitis. Gastroenterology 2007; 132: 874-882
79 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
80 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
81 Gunther U, Kusch D, Heller F et al. Surveillance colonoscopy in patients with inflammatory bowel disease: comparison of random biopsy vs. targeted biopsy protocols. Int J Colorectal Dis 2011; 26: 667-672
82 Hurlstone DP, Sanders DS, Lobo AJ et al. Indigo carmine-assisted high-magnification chromoscopic colonoscopy for the detection and characterisation of intraepithelial neoplasia in ulcerative colitis: a prospective evaluation. Endoscopy 2005; 37: 1186-1192
83 Matsumoto T, Nakamura S, Jo Y et al. Chromoscopy might improve diagnostic accuracy in cancer surveillance for ulcerative colitis. Am J Gastroenterol 2003; 98: 1827-1833
84 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
85 Marion JF, Waye JD, Present DH et al. Chromoendoscopy-targeted biopsies are superior to standard colonoscopic surveillance for detecting dysplasia in inflammatory bowel disease patients: a prospective endoscopic trial. Am J Gastroenterol 2008; 103: 2342-2349
86 Eaden JA, Ward BA, Mayberry JF. How gastroenterologists screen for colonic cancer in ulcerative colitis: an analysis of performance. Gastrointest Endosc 2000; 51: 123-128
87 Olliver JR, Wild CP, Sahay P et al. Chromoendoscopy with methylene blue and associated DNA damage in Barrett’s oesophagus. Lancet 2003; 362: 373-374
88 Elsadani NN, East JE, Walters JR. New 2010 British Society of Gastroenterology colitis surveillance guidelines: costs and surveillance intervals. Gut 2011; 60: 282-283
89 Kiesslich R, Neurath MF. Surveillance colonoscopy in ulcerative colitis: magnifying chromoendoscopy in the spotlight. Gut 2004; 53: 165-167
90 Cairns SR, Scholefield JH, Steele RJ et al. Guidelines for colorectal cancer screening and surveillance in moderate and high risk groups (update from 2002). Gut 2010; 59: 666-689
91 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
92 Ignjatovic A, East JE, Subramanian V et al. Narrow band imaging for detection of dysplasia in colitis: a randomized controlled trial. Am J Gastroenterol 2012; 107: 885-890
93 Dekker E, van den Broek FJ, Reitsma JB et al. Narrow-band imaging compared with conventional colonoscopy for the detection of dysplasia in patients with longstanding ulcerative colitis. Endoscopy 2007; 39: 216-221
94 van den Broek FJ, Fockens P, van Eeden S et al. Endoscopic tri-modal imaging for surveillance in ulcerative colitis: randomised comparison of high-resolution endoscopy and autofluorescence imaging for neoplasia detection; and evaluation of narrow-band imaging for classification of lesions. Gut 2008; 57: 1083-1089
95 Pellise M, Lopez-Ceron M, Rodriguez de Miguel C et al. Narrow-band imaging as an alternative to chromoendoscopy for the detection of dysplasia in long-standing inflammatory bowel disease: a prospective, randomized, crossover study. Gastrointest Endosc 2011; 74: 840-848
96 Bisschops R, Bessissow T, Baert FJ et al. Chromoendoscopy versus narrow band imaging in ulcerative colitis: a prospective randomized controlled trial. Gastrointest Endosc 2012; 75: AB148
97 Matsumoto T, Nakamura S, Moriyama T et al. Autofluorescence imaging colonoscopy for the detection of dysplastic lesions in ulcerative colitis: a pilot study. Colorectal Dis 2010; 12: e291-e297
98 van den Broek FJ, Fockens P, van Eeden S et al. Narrow-band imaging versus high-definition endoscopy for the diagnosis of neoplasia in ulcerative colitis. Endoscopy 2011; 43: 108-115
99 Matsumoto T, Kudo T, Jo Y et al. Magnifying colonoscopy with narrow band imaging system for the diagnosis of dysplasia in ulcerative colitis: a pilot study. Gastrointest Endosc 2007; 66: 957-965
100 East JE, Suzuki N, von Herbay A et al. Narrow band imaging with magnification for dysplasia detection and pit pattern assessment in ulcerative colitis surveillance: a case with multiple dysplasia associated lesions or masses. Gut 2006; 55: 1432-1435
101 Regula J, Rupinski M, Kraszewska E et al. Colonoscopy in colorectal-cancer screening for detection of advanced neoplasia. N Engl J Med 2006; 355: 1863-1872
102 Gschwantler M, Kriwanek S, Langner E et al. High-grade dysplasia and invasive carcinoma in colorectal adenomas: a multivariate analysis of the impact of adenoma and patient characteristics. Eur J Gastroenterol Hepatol 2002; 14: 183-188
103 Ignjatovic A, East JE, Suzuki N et al. Optical diagnosis of small colorectal polyps at routine colonoscopy (Detect InSpect ChAracterise Resect and Discard; DISCARD trial): a prospective cohort study. Lancet Oncol 2009; 10: 1171-1178
104 Kiesslich R, von Bergh M, Hahn M et al. Chromoendoscopy with indigocarmine improves the detection of adenomatous and nonadenomatous lesions in the colon. Endoscopy 2001; 33: 1001-1006
105 Ignjatovic A, East JE, Guenther T et al. What is the most reliable imaging modality for small colonic polyp characterization? Study of white-light, autofluorescence, and narrow-band imaging. Endoscopy 2011; 43: 94-99
106 Rex DK, Kahi C, O’Brien M et al. The American Society for Gastrointestinal Endoscopy PIVI (Preservation and Incorporation of Valuable Endoscopic Innovations) on real-time endoscopic assessment of the histology of diminutive colorectal polyps. Gastrointest Endosc 2011; 73: 419-422
107 Granqvist S, Gabrielsson N, Sundelin P. Diminutive colonic polyps – clinical significance and management. Endoscopy 1979; 11: 36-42
108 Church JM, Fazio VW, Jones IT. Small colorectal polyps. Are they worth treating?. Dis Colon Rectum 1988; 31: 50-53
109 O‘Brien MJ, Winawer SJ, Zauber AG et al. The National Polyp Study. Patient and polyp characteristics associated with high-grade dysplasia in colorectal adenomas. Gastroenterology 1990; 98: 371-379
110 Weston AP, Campbell DR. Diminutive colonic polyps: histopathology, spatial distribution, concomitant significant lesions, and treatment complications. Am J Gastroenterol 1995; 90: 24-28
111 Read TE, Read JD, Butterly LF. Importance of adenomas 5 mm or less in diameter that are detected by sigmoidoscopy. NEJM 1997; 336: 8-12
112 Nusko G, Mansmann U, Altendorf-Hofmann A et al. Risk of invasive carcinoma in colorectal adenomas assessed by size and site. Int J Colorect Dis 1997; 12: 267-271
113 Aldridge AJ, Simson JN. Histological assessment of colorectal adenomas by size. Are polyps less than 10 mm in size clinically important?. Eur J Surg 2001; 167: 777-781
114 Pickhardt PJ, Choi JR, Hwang I et al. Computed tomographic virtual colonoscopy to screen for colorectal neoplasia in asymptomatic adults. NEJM 2003; 349: 2191-2200
115 Church JM. Clinical significance of small colorectal polyps. Dis Colon Rectum 2004; 47: 481-485
116 O’Brien MJ, Winawer SJ, Zauber AG et al. Flat adenomas in the National Polyp Study: is there increased risk for high-grade dysplasia initially or during surveillance?. Clin Gastroenterol Hepatol 2004; 2: 905-911
117 Souques M, Lassalle M, Guldner L et al. Colorectal polyps and cancers diagnosed by pathologists in Ile de France region. Crisapif-Petri Study. Gastroenterol Clin Biol 2006; 30: 587-593
118 Chen SC, Mouchli A, Chadalawada V et al. Histopathology of small polyps removed in the videoendoscopic era. Gastrointest Endosc 2006; 63: AB199
119 Butterly LF, Chase MP, Pohl H et al. Prevalence of clinically important histology in small adenomas. Clin Gastroenterol Hepatol 2006; 4: 343-348
120 Kim DH, Pickhardt PJ, Taylor AJ et al. CT colonography versus colonoscopy for the detection of advanced neoplasia. NEJM 2007; 357: 1403-1412
121 Yoo TW, Park DI, Kim YH et al. Clinical significance of small colorectal adenoma less than 10 mm: the KASID study. Hepatogastroenterology 2007; 54: 418-421
122 Lieberman D, Moravec M, Holub J et al. Polyp size and advanced histology in patients undergoing colonoscopy screening: implications for CT colonography. Gastroenterology 2008; 135: 1100-1105
123 Rex DK, Overhiser AJ, Chen SC et al. Estimation of impact of American College of Radiology recommendations on CT colonography reporting for resection of high-risk adenoma findings. American J Gastroenterol 2009; 104: 149-153
124 Graser A, Stieber P, Nagel D et al. Comparison of CT colonography, colonoscopy, sigmoidoscopy and faecal occult blood tests for the detection of advanced adenoma in an average risk population. Gut 2009; 58: 241-248
125 Bretagne JF, Manfredi S, Piette C et al. Yield of high-grade dysplasia based on polyp size detected at colonoscopy: a series of 2295 examinations following a positive fecal occult blood test in a population-based study. Dis Colon Rectum 2010; 53: 339-345
126 Denis B, Bottlaender J, Weiss AM et al. Some diminutive colorectal polyps can be removed and discarded without pathological examination. Endoscopy 2011; 43: 81-86
127 Chaput U, Alberto SF, Terris B et al. Risk factors for advanced adenomas amongst small and diminutive colorectal polyps: a prospective monocenter study. Dig Liver Dis 2011; 43: 609-612
128 Repici A, Hassan C, Vitetta E et al. Safety of cold polypectomy for <10 mm polyps at colonoscopy: a prospective multicenter study. Endoscopy 2012; 44: 27-31
129 Tsai FC, Strum WB. Prevalence of advanced adenomas in small and diminutive colon polyps using direct measurement of size. Dig Dis Sci 2011; 56: 2384-2388
130 Shapiro R, Ben-Horin S, Bar-Meir S et al. The risk of advanced histology in small-sized colonic polyps: are non-invasive colonic imaging modalities good enough?. Int J Colorect Dis 2012; 27: 1071-1075
131 Kolligs FT, Crispin A, Graser A et al. Risk factors for advanced neoplasia within subcentimetric polyps: implications for diagnostic imaging. Gut 2012; 62: 863-870 doi: Epub 2012 Apr 23
132 Gupta N, Bansal A, Rao D et al. Prevalence of advanced histological features in diminutive and small colon polyps. Gastrointest Endosc 2012; 75: 1022-1030
133 Terry MB, Neugut AI, Bostick RM et al. Reliability in the classification of advanced colorectal adenomas. Cancer Epidemiol Biomarkers Prev 2002; 11: 660-663
134 Costantini M, Sciallero S, Giannini A et al. Interobserver agreement in the histologic diagnosis of colorectal polyps. the experience of the multicenter adenoma colorectal study (SMAC). J Clin Epidemiol 2003; 56: 209-214
135 Lasisi F, Mouchli A, Riddell R et al. Agreement in interpreting villous elements and dysplasia in adenomas less than one centimetre in size. Dig Liver Dis 2013; 45: 1049-1055
136 Atkin WS, Valori R, Kuipers EJ et al. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First Edition--Colonoscopic surveillance following adenoma removal. Endoscopy 2012; 44: E151-163
137 Lieberman DA, Rex DK, Winawer SJ et al. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology 2012; 143: 844-857
138 Hassan C, Quintero E, Dumonceau JM et al. Post-polypectomy colonoscopy surveillance: European Society of Gastrointestinal Endoscopy (ESGE) Guideline. Endoscopy 2013; 45: 842-864
139 Endoscopic Classification Review Group. Update on the Paris classification of superficial neoplastic lesions in the digestive tract. Endoscopy 2005; 37: 570-578
140 Longcroft-Wheaton G, Brown J, Cowlishaw D et al. High-definition vs. standard-definition colonoscopy in the characterization of small colonic polyps: results from a randomized trial. Endoscopy 2012; 44: 905-910
141 McGill SK, Evangelou E, Ioannidis JP et al. Narrow band imaging to differentiate neoplastic and non-neoplastic colorectal polyps in real time: a meta-analysis of diagnostic operating characteristics. Gut 2013; 62: 1704-1713
142 Togashi K, Osawa H, Koinuma K et al. A comparison of conventional endoscopy, chromoendoscopy, and the optimal-band imaging system for the differentiation of neoplastic and non-neoplastic colonic polyps. Gastrointest Endosc 2009; 69: 734-741
143 Ladabaum U, Fioritto A, Mitani A et al. Real-time optical biopsy of colon polyps with narrow band imaging in community practice does not yet meet key thresholds for clinical decisions. Gastroenterology 2013; 144: 81-91
144 Paggi S, Rondonotti E, Amato A et al. Resect and discard strategy in clinical practice: a prospective cohort study. Endoscopy 2012; 44: 899-904
145 Schachschal G, Mayr M, Treszl A et al. Endoscopic versus histological characterisation of polyps during screening colonoscopy. Gut 28.06.2013;
146 Masci E, Mangiavillano B, Crosta C et al. Interobserver agreement among endoscopists on evaluation of polypoid colorectal lesions visualized with the Pentax i-Scan technique. Dig Liver Dis 2013; 45: 207-210
147 Pigo F, Bertani H, Manno M et al. i-Scan high-definition white light endoscopy and colorectal polyps: prediction of histology, interobserver and intraobserver agreement. Int J Colorectal Dis 2013; 28: 399-406
148 van den Broek FJ, van Soest EJ, Naber AH et al. Combining autofluorescence imaging and narrow-band imaging for the differentiation of adenomas from non-neoplastic colonic polyps among experienced and non-experienced endoscopists. Am J Gastroenterol 2009; 104: 1498-1507
149 Rastogi A, Pondugula K, Bansal A et al. Recognition of surface mucosal and vascular patterns of colon polyps by using narrow-band imaging: interobserver and intraobserver agreement and prediction of polyp histology. Gastrointest Endosc 2009; 69: 716-22
150 Huang Q, Fukami N, Kashida H et al. Interobserver and intra-observer consistency in the endoscopic assessment of colonic pit patterns. Gastrointest Endosc 2004; 60: 520-526
151 East JE, Suzuki N, Saunders BP. Comparison of magnified pit pattern interpretation with narrow band imaging versus chromoendoscopy for diminutive colonic polyps: a pilot study. Gastrointest Endosc 2007; 66: 310-316
152 Sato R, Fujiya M, Watari J et al. The diagnostic accuracy of high-resolution endoscopy, autofluorescence imaging and narrow-band imaging for differentially diagnosing colon adenoma. Endoscopy 2011; 43: 862-868
153 Rogart JN, Jain D, Siddiqui UD et al. Narrow-band imaging without high magnification to differentiate polyps during real-time colonoscopy: improvement with experience. Gastrointest Endosc 2008; 68: 1136-1145
154 East JE, Suzuki N, Bassett P et al. Narrow band imaging with magnification for the characterization of small and diminutive colonic polyps: pit pattern and vascular pattern intensity. Endoscopy 2008; 40: 811-817
155 Ignjatovic A, Thomas-Gibson S, East JE et al. Development and validation of a training module on the use of narrow-band imaging in differentiation of small adenomas from hyperplastic colorectal polyps. Gastrointest Endosc 2011; 73: 128-133
156 Raghavendra M, Hewett DG, Rex DK. Differentiating adenomas from hyperplastic colorectal polyps: narrow-band imaging can be learned in 20 minutes. Gastrointest Endosc 2010; 72: 572-576
157 Rastogi A, Rao DS, Gupta N et al. Impact of a computer-based teaching module on characterization of diminutive colon polyps by using narrow-band imaging by non-experts in academic and community practice: a video-based study. Gastrointest Endosc 07.09.2013; [Epub ahead of print]
158 Higashi R, Uraoka T, Kato J et al. Diagnostic accuracy of narrow-band imaging and pit pattern analysis significantly improved for less-experienced endoscopists after an expanded training program. Gastrointest Endosc 2010; 72: 127-135
159 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.e1
160 Kumar S, Fioritto A, Mitani A et al. Optical biopsy of sessile serrated adenomas: do these lesions resemble hyperplastic polyps under narrow-band imaging?. Gastrointest Endosc 2013; 78: 902-909
161 Varnavas A, Ignjatovic A, Bharath A et al. Classification of colon images using the magnitude of orientation dominance. Proceedings of the 5th UKRI PG Conference in Biomedical Engineering and Medical Physics. 2009 1. 13-14
162 Tischendorf JJ, Gross S, Winograd R et al. Computer-aided classification of colorectal polyps based on vascular patterns: a pilot study. Endoscopy 2010; 42: 203-207
163 Takemura Y, Yoshida S, Tanaka S et al. Computer-aided system for predicting the histology of colorectal tumors by using narrow-band imaging magnifying colonoscopy (with video). Gastrointest Endosc 2012; 75: 179-185
164 Gross S, Trautwein C, Behrens A et al. Computer-based classification of small colorectal polyps by using narrow-band imaging with optical magnification. Gastrointest Endosc 2011; 74: 1354-1359
165 Gupta N, Bansal A, Rao D et al. Accuracy of in vivo optical diagnosis of colon polyp histology by narrow-band imaging in predicting colonoscopy surveillance intervals. Gastrointest Endosc 2012; 75: 494-502
166 Longcroft-Wheaton GR, Higgins B, Bhandari P. Flexible spectral imaging color enhancement and indigo carmine in neoplasia diagnosis during colonoscopy: a large prospective UK series. Eur J Gastroenterol Hepatol 2011; 23: 903-911
167 Hassan C, Pickhardt PJ, Rex DK. A resect and discard strategy would improve cost-effectiveness of colorectal cancer screening. Clin Gastroenterol Hepatol 2010; 8: 865-869 , 869e1–e3
168 Valori R, Rey JF, Atkin WS et al. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition–Quality assurance in endoscopy in colorectal cancer screening and diagnosis. Endoscopy 2012; 44: E88-105
169 Steele RJ, Pox C, Kuipers EJ et al. European guidelines for quality assurance in colorectal cancer screening and diagnosis. First edition–Management of lesions detected in colorectal cancer screening. Endoscopy 2012; 44: E140-50
170 Watanabe T, Itabashi M, Shimada Y et al. Japanese Society for Cancer of the Colon and Rectum (JSCCR) guidelines 2010 for the treatment of colorectal cancer. Int J Clin Oncol 2012; 17: 1-29
171 Nakadoi K, Tanaka S, Kanao H et al. Management of T1 colorectal carcinoma with special reference to criteria for curative endoscopic resection. J Gastroenterol Hepatol 2012; 27: 1057-1062
172 Kudo S, Rubio CA, Teixeira CR et al. Pit pattern in colorectal neoplasia: endoscopic magnifying view. Endoscopy 2001; 33: 367-373
173 Hirata M, Tanaka S, Oka S et al. Evaluation of microvessels in colorectal tumors by narrow band imaging magnification. Gastrointest Endosc 2007; 66: 945-952
174 Fujii T, Hasegawa RT, Saitoh Y et al. Chromoscopy during colonoscopy. Endoscopy 2001; 33: 1036-1041
175 Nagata S, Tanaka S, Haruma K et al. Pit pattern diagnosis of early colorectal carcinoma by magnifying colonoscopy: clinical and histological implications. Int J Oncol 2000; 16: 927-934
176 Kudo S, Lambert R, Allen JI et al. Nonpolypoid neoplastic lesions of the colorectal mucosa. Gastrointest Endosc 2008; 68: 3-S47
177 Bianco MA, Rotondano G, Marmo R et al. Predictive value of magnification chromoendoscopy for diagnosing invasive neoplasia in nonpolypoid colorectal lesions and stratifying patients for endoscopic resection or surgery. Endoscopy 2006; 38: 470-476
178 Kanao H, Tanaka S, Oka S et al. Narrow-band imaging magnification predicts the histology and invasion depth of colorectal tumors. Gastrointest Endosc 2009; 69: 631-636
179 Wada Y, Kudo SE, Kashida H et al. Diagnosis of colorectal lesions with the magnifying narrow-band imaging system. Gastrointest Endosc 2009; 70: 522-531
180 Matsumoto K, Nagahara A, Terai T et al. Evaluation of new subclassification of type V(I) pit pattern for determining the depth and type of invasion of colorectal neoplasm. J Gastroenterol 2011; 46: 31-38
181 Kanao H, Tanaka S, Oka S et al. Clinical significance of type V(I) pit pattern subclassification in determining the depth of invasion of colorectal neoplasms. World J Gastroenterol 2008; 14: 211-217
182 Kobayashi N, Saito Y, Sano Y et al. Determining the treatment strategy for colorectal neoplastic lesions: endoscopic assessment or the non-lifting sign for diagnosing invasion depth?. Endoscopy 2007; 39: 701-705
183 Saitoh Y, Obara T, Watari J et al. Invasion depth diagnosis of depressed type early colorectal cancers by combined use of videoendoscopy and chromoendoscopy. Gastrointest Endosc 1998; 48: 362-370
184 Matsuda T, Fujii T, Saito Y et al. Efficacy of the invasive/non-invasive pattern by magnifying chromoendoscopy to estimate the depth of invasion of early colorectal neoplasms. Am J Gastroenterol 2008; 103: 2700-2706
185 Hayashi N, Tanaka S, Hewett DG et al. Endoscopic prediction of deep submucosal invasive carcinoma: validation of the narrow-band imaging international colorectal endoscopic (NICE) classification. Gastrointest Endosc 2013; 78: 625-632 doi:
186 Tsuda S, Veress B, Toth E et al. Flat and depressed colorectal tumours in a southern Swedish population: a prospective chromoendoscopic and histopathological study. Gut 2002; 51: 550-555
187 Rembacken BJ, Fujii T, Cairns A et al. Flat and depressed colonic neoplasms: a prospective study of 1000 colonoscopies in the UK. Lancet 2000; 355: 1211-1214
188 Hurlstone DP, Cross SS, Adam I et al. A prospective clinicopathological and endoscopic evaluation of flat and depressed colorectal lesions in the United Kingdom. Am J Gastroenterol 2003; 98: 2543-2549
189 Soetikno RM, Kaltenbach T, Rouse RV et al. Prevalence of nonpolypoid (flat and depressed) colorectal neoplasms in asymptomatic and symptomatic adults. JAMA 2008; 299: 1027-1035
190 Diebold MD, Samalin E, Merle C et al. Colonic flat neoplasia: frequency and concordance between endoscopic appearance and histological diagnosis in a French prospective series. Am J Gastroenterol 2004; 99: 1795-1800
191 Rotondano G, Bianco MA, Buffoli F et al. The Cooperative Italian FLIN Study Group: prevalence and clinico-pathological features of colorectal laterally spreading tumors. Endoscopy 2011; 43: 856-861
192 Bianco MA, Cipolletta L, Rotondano G et al. Prevalence of nonpolypoid colorectal neoplasia: an Italian multicenter observational study. Endoscopy 2010; 42: 279-285
193 Robertson DJ, Greenberg ER, Beach M et al. Colorectal cancer in patients under close colonoscopic surveillance. Gastroenterology 2005; 129: 34-41
194 Pabby A, Schoen RE, Weissfeld JL et al. Analysis of colorectal cancer occurrence during surveillance colonoscopy in the dietary Polyp Prevention Trial. Gastrointest Endosc 2005; 61: 385-391
195 Pohl H, Srivastava A, Bensen SP et al. Incomplete polyp resection during colonoscopy – results of the complete adenoma resection (CARE) study. Gastroenterology 2013; 144: 74-80 e1
196 Hurlstone DP, Cross SS, Brown S et al. A prospective evaluation of high-magnification chromoscopic colonoscopy in predicting completeness of EMR. Gastrointest Endosc 2004; 59: 642-650
197 Hurlstone DP, Cross SS, Drew K. An evaluation of colorectal endoscopic mucosal resection using high-magnification chromoscopic colonoscopy: a prospective study of 1000 colonoscopies. Endoscopy 2004; 36: 491-498
198 Moss A, Bourke MJ, Williams SJ et al. Endoscopic mucosal resection outcomes and prediction of submucosal cancer from advanced colonic mucosal neoplasia. Gastroenterology 2011; 140: 1909-1918
199 Buchner AM, Guarner-Argente C, Ginsberg GG. Outcomes of EMR of defiant colorectal lesions directed to an endoscopy referral center. Gastrointest Endosc 2012; 76: 255-263
200 Cipolletta L, Bianco MA, Garofano ML et al. Can magnification endoscopy detect residual adenoma after piecemeal resection of large sessile colorectal lesions to guide subsequent treatment? A prospective single-center study. Dis Colon Rectum 2009; 52: 1774-1779
201 Munakata A, Uno Y. Colonoscopic polypectomy with local injection of methylene blue. Tohoku J Exp Med 1994; 173: 377-382
202 Khashab M, Eid E, Rusche M et al. Incidence and predictors of “late” recurrences after endoscopic piecemeal resection of large sessile adenomas. Gastrointest Endosc 2009; 70: 344-349
203 Shahid MW, Buchner AM, Coron E et al. Diagnostic accuracy of probe-based confocal laser endomicroscopy in detecting residual colorectal neoplasia after EMR: a prospective study. Gastrointest Endosc 2012; 75: 525-533
204 Rogart JN, Aslanian HR, Siddiqui UD. Narrow band imaging to detect residual or recurrent neoplastic tissue during surveillance endoscopy. Dig Dis Sci 2011; 56: 472-478
205 Higaki S, Hashimoto S, Harada K et al. Long-term follow-up of large flat colorectal tumors resected endoscopically. Endoscopy 2003; 35: 845-849
206 Hurlstone DP, Sanders DS, Cross SS et al. Colonoscopic resection of lateral spreading tumours: a prospective analysis of endoscopic mucosal resection. Gut 2004; 53: 1334-1339

Supplementary Material

Supplementary material