Preventing colorectal cancer and cancer mortality with colonoscopy: what we know and what we don’t know

Introduction

The goal of most colonoscopies is the prevention of incident colorectal cancer and especially death from colorectal cancer. The effectiveness of colonoscopy is now justly under attack following the publication of studies showing that colonoscopy reduces the risk of distal colorectal cancer and advanced neoplasms but has no [1] [2] or limited [3] effect on the incidence of proximal neoplasms. The reasons for no or limited proximal colon protection by colonoscopy are uncertain, but there are two broad categories of possible explanations. One category is altered biology in the proximal colon. Interval cancers in the proximal colon are more likely to be microsatellite unstable (MSI) and to bear the CpG Island Methylator Phenotype (CIMP) [4]. MSI is known to push tumors through the adenoma–carcinoma sequence rapidly, and CIMP tumors are believed to be the end product of serrated polyps, a group of lesions that are endoscopically subtle and about which little is known compared with adenomas.

A second category of explanations is technical failure, including poor preparation (which preferentially affects the right colon), incomplete cecal intubation, incomplete polypectomy, and suboptimal examination techniques that fail to detect precancerous lesions and early cancers [5]. The two categories of problems could be related, in that nonpolypoid lesions and serrated lesions are more common in the proximal colon and because both types of lesions are endoscopically subtle, so that their detection may escape a larger fraction of colonoscopists and a wider range of examination techniques. Indeed, consistent detection of flat and serrated lesions may yet be shown to require special technology. A key piece of missing information that will suggest which group of explanations underlies poor right colon protection is whether interval cancers cluster among individual examiners [6]. If clustering is present, then we should be able to raise performance and correct the problem. If clustering is not present, it suggests that either we should give up on colonoscopy for screening and return to flexible sigmoidoscopy, or that we need new technology to enhance detection during colonoscopy.

This editorial will discuss the potential causes of interval cancers, with an emphasis on where existing data suggest we should change clinical practice, where data suggest we should change terminology, and areas where more data are needed to guide us to best practice.

References

• 1 Baxter N N, Goldwasser M A, Paszat L F. et al . Association of colonoscopy and death from colorectal cancer.  Ann Intern Med. 2009;  150 1-8
• 2 Brenner H, Hoffmeister M, Arndt V. et al . Protection from right- and left-sided colorectal neoplasms after colonoscopy: population-based study.  J Natl Cancer Inst. 2010;  102 89-95
• 3 Singh G, Gerson L B, Wang H. et al . Screening colonoscopy, colorectal cancer and gender: an unfair deal for the fair sex?.  Gastrointest Endosc. 2007;  65 AB100
• 4 Arain M A, Sawhney M, Sheikh S. et al . CIMP status of interval colon cancers: another piece to the puzzle.  Am J Gastroenterol. 2009;  DOI:10.1038/ajg.2009.699
• 5 Rex D K. Maximizing detection of adenomas and cancers during colonoscopy.  Am J Gastroenterol. 2006;  101 2866-2877
• 6 de Groen P, Szarka L, Francis D. et al . Random video file peer review to assess quality of colonoscopy.  Am J Gastroenterol. 2008;  103 S551-0
• 7 Froehlich F, Wietlisbach V, Gonvers J J. et al . Impact of colonic cleansing on quality and diagnostic yield of colonoscopy: the European Panel of Appropriateness of Gastrointestinal Endoscopy European multicenter study.  Gastrointest Endosc. 2005;  61 378-384
• 8 Harewood G C, Sharma V K, de Garmo P. Impact of colonoscopy preparation quality on detection of suspected colonic neoplasia.  Gastrointest Endosc. 2003;  58 76-79
• 9 Parra-Blanco A, Nicolas-Perez D, Gimeno-Garcia A. et al . The timing of bowel preparation before colonoscopy determines the quality of cleansing, and is a significant factor contributing to the detection of flat lesions: a randomized study.  World J Gastroenterol. 2006;  12 6161-6166
• 10 Bianco M, Cipolletta L, Rotondano G, Buffoli F. The cooperative Flat Lesions Italian Network (FLIN). Prevalence of nonpolypoid colorectal neoplasia: a multicenter observational study.  Endoscopy. 2010;  42 279-285
• 11 Rostom A, Jolicoeur E, Dube C. et al . A randomized prospective trial comparing different regimens of oral sodium phosphate and polyethylene glycol-based lavage solution in the preparation of patients for colonoscopy.  Gastrointest Endosc. 2006;  64 544-552
• 12 Aoun E, Abdul-Baki H, Azar C. et al . A randomized single-blind trial of split-dose PEG-electrolyte solution without dietary restriction compared with whole dose PEG-electrolyte solution with dietary restriction for colonoscopy preparation.  Gastrointest Endosc. 2005;  62 213-218
• 13 Park J S, Sohn C I, Hwang S J. et al . Quality and effect of single dose versus split dose of polyethylene glycol bowel preparation for early-morning colonoscopy.  Endoscopy. 2007;  39 616-619
• 14 Church J M. Effectiveness of polyethylene glycol antegrade gut lavage bowel preparation for colonoscopy - timing is the key!.  Dis Colon Rectum. 1998;  41 1223-1225
• 15 El Sayed A M, Kanafani Z A, Mourad F H. et al . A randomized single-blind trial of whole versus split-dose polyethylene glycol-electrolyte solution for colonoscopy preparation.  Gastrointest Endosc. 2003;  58 36-40
• 16 Frommer D. Cleansing ability and tolerance of three bowel preparations for colonoscopy.  Dis Colon Rectum. 1997;  40 100-104
• 17 Abdul-Baki H, Hashash J G, Elhajj I I. et al . A randomized, controlled, double-blind trial of the adjunct use of tegaserod in whole-dose or split-dose polyethylene glycol electrolyte solution for colonoscopy preparation.  Gastrointest Endosc. 2008;  68 294-300
• 18 Chiu H M, Lin J T, Wang H P. et al . The impact of colon preparation timing on colonoscopic detection of colorectal neoplasms – a prospective endoscopist-blinded randomized trial.  Am J Gastroenterol. 2006;  101 2719-2725
• 19 Gupta T, Mandot A, Desai D. et al . Comparison of two schedules (previous evening versus same morning) of bowel preparation for colonoscopy.  Endoscopy. 2007;  39 706-709
• 20 Rex D K, Ulbright T M. Step section histology of proximal colon polyps that appear hyperplastic by endoscopy.  Am J Gastroenterol. 2002;  97 1530-1534
• 21 Rex D K, Rahmani E Y. New endoscopic finding associated with hyperplastic polyps.  Gastrointest Endosc. 1999;  50 704-706
• 22 Pabby A, Schoen R E, Weissfeld J L. et al . Analysis of colorectal cancer occurrence during surveillance colonoscopy in the Dietary Polyp Prevention Trial.  Gastrointest Endosc. 2005;  61 385-391
• 23 Farrar W D, Sawhney M S, Nelson D B. et al . Colorectal cancers found after a complete colonoscopy.  Clin Gastroenterol Hepatol. 2006;  4 1259-1264
• 24 Rex D K. Have we defined best colonoscopic polypectomy practice in the United States?.  Clin Gastroenterol Hepatol. 2007;  5 674-677
• 25 Ellis K, Shiel M, Marquis S, Katon R. Efficacy of hot biopsy foreceps, cold micro-snare and microsnare with cautery techniques in the removal of diminutive colonic polyps [abstract].  Gastrointest Endosc. 1997;  45 AB107
• 26 ASGE Standards of Practice Committee . Hot biopsy forceps.  Gastrointest Endosc. 1992;  38 753-756
• 27 Brooker J C, Saunders B P, Shah S G. et al . Treatment with argon plasma coagulation reduces recurrence after piecemeal resection of large sessile colonic polyps: a randomized trial and recommendations.  Gastrointest Endosc. 2002;  55 371-375
• 28 Mattar W, Rex D K. Large sessile adenomas are associated with a high prevalence of synchronous advanced adenomas.  Clin Gastroenterol Hepatol. 2008;  6 877-879
• 29 Rex D K, Lieberman D. ACG colorectal cancer prevention action plan: update on CT-colonography.  Am J Gastroenterol. 2006;  101 1410-1413
• 30 Rex D K. Narrow-band imaging without optical magnification for histologic analysis of colorectal polyps.  Gastroenterology. 2009;  136 1174-1181
• 31 Ignjatovic A, East J, 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 Oncology. 2009;  10 1171-1178
• 32 Rex D K, Fennerty M B, Sharma P. et al . Bringing new endoscopic imaging technology into everyday practice: what is the role of professional GI societies? Polyp imaging as a template for moving endoscopic innovation forward to answer key clinical questions.  Gastrointest Endosc. 2010;  71 142-146
• 33 The Paris endoscopic classification of superficial neoplastic lesions: esophagus, stomach, and colon: November 30 to December 1, 2002.  Gastrointest Endosc. 2003;  58 (6 Suppl) S3-S43
• 34 Jaramillo E, Watanabe M, Slezak P, Rubio C. Flat neoplastic lesions of the colon and rectum detected by high-resolution video endoscopy and chromoscopy.  Gastrointest Endosc. 1995;  42 114-122
• 35 Tsuda S, Veress B, Toth E, Fork F. Flat and depressed colorectal tumours in southern Swedish population: a prospective chromoendoscopic and histopathological study.  Gut. 2002;  51 550-555
• 36 Hurlstone D, Cross S, 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
• 37 Rembacken B, 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
• 38 Kudo S, Lambert R, Allen J I. et al . Nonpolypoid neoplastic lesions of the colorectal mucosa.  Gastrointest Endosc. 2008;  68 (4 Suppl) S3-47
• 39 Soetikno R M, Kaltenbach T, Rouse R V. et al . Prevalence of nonpolypoid (flat and depressed) colorectal neoplasms in asymptomatic and symptomatic adults.  Jama. 2008;  299 1027-1035
• 40 Brooker J, Saunders B, Shah S. et al . Total colonic dye-spray increases the detection of diminutive adenomas during routine colonoscopy: a randomized controlled trial.  Gastrointest Endosc. 2002;  56 333-338
• 41 Hurlstone D P, Cross S S, Slater R. et al . Detecting diminutive colorectal lesions at colonoscopy: a randomised controlled trial of pan-colonic versus targeted chromoscopy.  Gut. 2004;  53 376-380
• 42 Le Rhun M, Coron E, Parlier D. et al . High resolution colonoscopy with chromoscopy versus standard colonoscopy for the detection of colonic neoplasia: a randomized study.  Clin Gastroenterol Hepatol. 2006;  4 349-354
• 43 Adler A, Pohl H, Papanikolaou I S. et al . A prospective randomised study on narrow-band imaging versus conventional colonoscopy for adenoma detection: does narrow-band imaging induce a learning effect?.  Gut. 2008;  57 59-64
• 44 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
• 45 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
• 46 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
• 47 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
• 48 Rex D K, Helbig C C. High yields of small and flat adenomas with high-definition colonoscopes using either white light or narrow band imaging.  Gastroenterology. 2007;  133 42-47
• 49 Kahi C, Anderson J, Waxman I. et al . The American College of Gastroenterology high definition chromocolonoscopy study: findings and implications of colorectal cancer screening.  Am J Gastroenterol. 2009;  104 S559
• 50 East J E, Stavrindis M, Thomas-Gibson S. et al . A comparative study of standard vs. high definition colonoscopy for adenoma and hyperplastic polyp detection with optimized withdrawal technique.  Aliment Pharmacol Ther. 2008;  28 768-776
• 51 Spring K J, Zhao Z Z, Karamatic R. et al . High prevalence of sessile serrated adenomas with BRAF mutations: a prospective study of patients undergoing colonoscopy.  Gastroenterology. 2006;  131 1400-1407
• 52 Winawer S J, Zauber A G, Fletcher R H. et al . Guidelines for colonoscopy surveillance after polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer and the American Cancer Society.  Gastroenterology. 2006;  130 1872-1885
• 53 Khalid O, Radaideh S, Cummings O W. et al . Reinterpretation of histology of proximal colon polyps called hyperplastic in 2001.  World J Gastroenterol. 2009;  15 3767-3770