Systematic literature review and pooled analyses of risk factors for finding adenomas at surveillance colonoscopy

Background and study aim: Colorectal cancer (CRC) screening guidelines recommend surveillance after polypectomy. There is variation in the surveillance intervals that are being advised. This variation also affects adherence. Surveillance intervals need to be based on risk factors at index. We therefore aimed to systematically review risk factors of adenoma findings at surveillance colonoscopy.

Methods: A systematic literature search was performed up to September 2009. Studies that reported on follow-up colonoscopy findings with stratification for index characteristics were included. Pooled relative risks (RR) were calculated using random effects models, and heterogeneity was determined by means of the I² -statistic.

Results: A total of 27 studies met the inclusion criteria. The most important risk factors for adenoma findings were the presence on index colonoscopy of the following: advanced adenomas (RR: 1.81), ≥ 3 adenomas (RR: 1.64), size ≥ 10 mm (RR: 1.66), and age ≥ 60 years (RR: 1.65). The presence of villous adenomas, high grade dysplasia, proximal adenomas, and male gender were associated with less profound increases in RR. Marked variation in study design and substantial heterogeneity between studies was observed.

Conclusions: Convincing evidence exists that patients with advanced adenomas, ≥ 3 adenomas, adenomas ≥ 10 mm, or age ≥ 60 years have an increased risk of adenoma recurrence. The evidence for other baseline findings for an increased risk of adenoma recurrence is inconclusive. Marked variation and consistently lower RRs in studies of medium or low quality emphasize the necessity for well performed and well reported studies. Given the high impact of surveillance on patients and service providers, there is need for further assessment of the risk(s) of adenoma recurrence.

References

• 1 Jemal A, Siegel R, Ward E et al. Cancer statistics, 2009.  CA Cancer J Clin. 2009;  59 225-249
• 2 Ferlay J, Parkin D M, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008.  Eur J Cancer. 2010;  46 765-781
• 3 Lieberman D A, Weiss D G, Bond J H et al. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380.  N Engl J Med. 2000;  343 162-168
• 4 Schoenfeld P, Cash B, Flood A et al. Colonoscopic screening of average-risk women for colorectal neoplasia.  N Engl J Med. 2005;  352 2061-2068
• 5 Imperiale T F, Wagner D R, Lin C Y et al. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings.  N Engl J Med. 2000;  343 169-174
• 6 Winawer S J, Zauber A G, Ho M N et al. Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup.  N Engl J Med. 1993;  329 1977-1981
• 7 Thiis-Evensen E, Hoff G S, Sauar J et al. Population-based surveillance by colonoscopy: effect on the incidence of colorectal cancer. Telemark Polyp Study I.  Scand J Gastroenterol. 1999;  34 414-420
• 8 Citarda F, Tomaselli G, Capocaccia R et al. Efficacy in standard clinical practice of colonoscopic polypectomy in reducing colorectal cancer incidence.  Gut. 2001;  48 812-815
• 9 Meagher A P, Stuart M. Does colonoscopic polypectomy reduce the incidence of colorectal carcinoma?.  Aust N Z J Surg. 1994;  64 400-404
• 10 Jorgensen O D, Kronborg O, Fenger C, Rasmussen M. Influence of long-term colonoscopic surveillance on incidence of colorectal cancer and death from the disease in patients with precursors (adenomas).  Acta Oncol. 2007;  46 355-360
• 11 Hardcastle J D, Chamberlain J O, Robinson M H et al. Randomised controlled trial of faecal-occult-blood screening for colorectal cancer.  Lancet. 1996;  348 1472-1477
• 12 Kronborg O, Fenger C, Olsen J et al. Randomised study of screening for colorectal cancer with faecal-occult-blood test.  Lancet. 1996;  348 1467-1471
• 13 Mandel J S, Bond J H, Church T R et al. Reducing mortality from colorectal cancer by screening for fecal occult blood. Minnesota Colon Cancer Control Study.  N Engl J Med. 1993;  328 1365-1371
• 14 Levin B, Lieberman D A, McFarland B et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology.  Gastroenterology. 2008;  134 1570-1595
• 15 Leddin D, Hunt R, Champion M et al. Canadian Association of Gastroenterology and the Canadian Digestive Health Foundation: Guidelines on colon cancer screening.  Can J Gastroenterol. 2004;  18 93-99
• 16 West N J, Boustiere C, Fischbach W et al. Colorectal cancer screening in Europe: differences in approach; similar barriers to overcome.  Int J Colorectal Dis. 2009;  24 731-740
• 17 Atkin W S, Edwards R, Kralj-Hans I et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial.  Lancet. 2010;  375 1624-1633
• 18 Muto T, Bussey H J, Morson B C. The evolution of cancer of the colon and rectum.  Cancer. 1975;  36 2251-2270
• 19 Nusko G, Mansmann U, Kirchner T, Hahn E G. Risk related surveillance following colorectal polypectomy.  Gut. 2002;  51 424-428
• 20 Noshirwani K C, van Stolk R U, Rybicki L A, Beck G J. Adenoma size and number are predictive of adenoma recurrence: implications for surveillance colonoscopy.  Gastrointest Endosc. 2000;  51 433-437
• 21 van Stolk R U, Beck G J, Baron J A et al. Adenoma characteristics at first colonoscopy as predictors of adenoma recurrence and characteristics at follow-up. The Polyp Prevention Study Group.  Gastroenterology. 1998;  115 13-18
• 22 Martinez M E, Sampliner R, Marshall J R et al. Adenoma characteristics as risk factors for recurrence of advanced adenomas.  Gastroenterology. 2001;  120 1077-1083
• 23 Martinez M E, Baron J A, Lieberman D A et al. A pooled analysis of advanced colorectal neoplasia diagnoses after colonoscopic polypectomy.  Gastroenterology. 2009;  136 832-841
• 24 van Rijn J C, Reitsma J B, Stoker J et al. Polyp miss rate determined by tandem colonoscopy: a systematic review.  Am J Gastroenterol. 2006;  101 343-350
• 25 Schoen R E. Surveillance after positive and negative colonoscopy examinations: issues, yields, and use.  Am J Gastroenterol. 2003;  98 1237-1246
• 26 Arditi C, Gonvers J J, Burnand B et al. Appropriateness of colonoscopy in Europe (EPAGE II). Surveillance after polypectomy and after resection of colorectal cancer.  Endoscopy. 2009;  41 209-217
• 27 Harewood G C, Lieberman D A. Colonoscopy practice patterns since introduction of medicare coverage for average-risk screening.  Clin Gastroenterol Hepatol. 2004;  2 72-77
• 28 Saini S D, Kim H M, Schoenfeld P. Incidence of advanced adenomas at surveillance colonoscopy in patients with a personal history of colon adenomas: a meta-analysis and systematic review.  Gastrointest Endosc. 2006;  64 614-626
• 29 Hamilton S R, Aaltonen L A. eds. World Health Organization Classification of Tumours. Pathology and genetics of tumours of the digestive system.. Lyon: IARC Press; 2000
• 30 Wells G, Shea B, O'Connell D. The Newcastle-Ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa Health Research Institute Web site.. Available at URL: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp Last accessed: 27 January 2011
• 31 Sint Nicolaas J, de Jonge V, Steyerberg E W et al. Risk of colorectal carcinoma in post-liver transplant patients: a systematic review and meta-analysis.  Am J Transplant. 2010;  10 868-876
• 32 DerSimonian R, Kacker R. Random-effects model for meta-analysis of clinical trials: an update.  Contemp Clin Trials. 2007;  28 105-114
• 33 Hatala R, Keitz S, Wyer P, Guyatt G. Tips for learners of evidence-based medicine: 4. Assessing heterogeneity of primary studies in systematic reviews and whether to combine their results.  CMAJ. 2005;  172 661-665
• 34 Keku T O, Amin A, Galanko J et al. Apoptosis in normal rectal mucosa, baseline adenoma characteristics, and risk of future adenomas.  Cancer Epidemiol Biomarkers Prev. 2008;  17 306-310
• 35 Matsuda T, Fujii T, Sano Y et al. Five-year incidence of advanced neoplasia after initial colonoscopy in Japan: a multicenter retrospective cohort study.  Jpn J Clin Oncol. 2009;  39 435-442
• 36 Avidan B, Sonnenberg A, Schnell T G et al. New occurrence and recurrence of neoplasms within 5 years of a screening colonoscopy.  Am J Gastroenterol. 2002;  97 1524-1529
• 37 Bertario L, Russo A, Sala P et al. Predictors of metachronous colorectal neoplasms in sporadic adenoma patients.  Int J Cancer. 2003;  105 82-87
• 38 Blumberg D, Opelka F G, Hicks T C et al. Significance of a normal surveillance colonoscopy in patients with a history of adenomatous polyps.  Dis Colon Rectum. 2000;  43 1084-1091 [Discussion in 1091 – 1092]
• 39 Fornasarig M, Valentini M, Poletti M et al. Evaluation of the risk for metachronous colorectal neoplasms following intestinal polypectomy: a clinical, endoscopic and pathological study.  Hepatogastroenterology. 1998;  45 1565-1572
• 40 Fossi S, Bazzoli F, Ricciardiello L et al. Incidence and recurrence rates of colorectal adenomas in first-degree asymptomatic relatives of patients with colon cancer.  Am J Gastroenterol. 2001;  96 1601-1604
• 41 Hixson L J, Fennerty M B, Sampliner R E et al. Two-year incidence of colon adenomas developing after tandem colonoscopy.  Am J Gastroenterol. 1994;  89 687-691
• 42 Holtzman R, Poulard J B, Bank S et al. Repeat colonoscopy after endoscopic polypectomy.  Dis Colon Rectum. 1987;  30 185-188
• 43 Imperiale T F, Glowinski E A, Lin-Cooper C et al. Five-year risk of colorectal neoplasia after negative screening colonoscopy.  N Engl J Med. 2008;  359 1218-1224
• 44 Laiyemo A O, Murphy G, Albert P S et al. Postpolypectomy colonoscopy surveillance guidelines: predictive accuracy for advanced adenoma at 4 years.  Ann Intern Med. 2008;  148 419-426
• 45 Lieberman D A, Weiss D G, Harford W V et al. Five-year colon surveillance after screening colonoscopy.  Gastroenterology. 2007;  133 1077-1085
• 46 Neugut A I, Jacobson J S, Ahsan H et al. Incidence and recurrence rates of colorectal adenomas: a prospective study.  Gastroenterology. 1995;  108 402-408
• 47 Nusko G, Hahn E G, Mansmann U. Risk of advanced metachronous colorectal adenoma during long-term follow-up.  Int J Colorectal Dis. 2008;  23 1065-1071
• 48 Rex D K, Cummings O W, Helper D J et al. 5-year incidence of adenomas after negative colonoscopy in asymptomatic average-risk persons.  Gastroenterology. 1996;  111 1178-1181 [Comment in Gastroenterology 1996; 111: 1385 – 1387 and Gastroenterology 2002; 122: 839 – 840]
• 49 Waye J D, Braunfeld S. Surveillance intervals after colonoscopic polypectomy.  Endoscopy. 1982;  14 79-81
• 50 Winawer S J, Zauber A G, O'Brien M J et al. Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps. The National Polyp Study Workgroup.  N Engl J Med. 1993;  328 901-906
• 51 Woolfson I K, Eckholdt G J, Wetzel C R et al. Usefulness of performing colonoscopy one year after endoscopic polypectomy.  Dis Colon Rectum. 1990;  33 389-393
• 52 Yamaji Y, Mitsushima T, Ikuma H et al. Incidence and recurrence rates of colorectal adenomas estimated by annually repeated colonoscopies on asymptomatic Japanese.  Gut. 2004;  53 568-572
• 53 Ji J S, Choi K Y, Lee W C et al. Endoscopic and histopathologic predictors of recurrence of colorectal adenoma on lowering the miss rate.  Korean J Intern Med. 2009;  24 196-202
• 54 Leung W K, Lau J Y, Suen B Y et al. Repeat-screening colonoscopy 5 years after normal baseline-screening colonoscopy in average-risk Chinese: a prospective study.  Am J Gastroenterol. 2009;  104 2028-2034
• 55 Triantafyllou K, Papatheodoridis G V, Paspatis G A et al. Predictors of the early development of advanced metachronous colon adenomas.  Hepatogastroenterology. 1997;  44 533-538
• 56 Jorgensen O D, Kronborg O, Fenger C. A randomized surveillance study of patients with pedunculated and small sessile tubular and tubulovillous adenomas. The Funen Adenoma Follow-up Study.  Scand J Gastroenterol. 1995;  30 686-692
• 57 Nava H, Carlsson G, Petrelli N J et al. Follow-up colonoscopy in patients with colorectal adenomatous polyps.  Dis Colon Rectum. 1987;  30 465-468
• 58 Terry M B, Neugut A I, Bostick R M et al. Reliability in the classification of advanced colorectal adenomas.  Cancer Epidemiol Biomarkers Prev. 2002;  11 660-663
• 59 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
• 60 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
• 61 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
• 62 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
• 63 Bressler B, Paszat L F, Chen Z et al. Rates of new or missed colorectal cancers after colonoscopy and their risk factors: a population-based analysis.  Gastroenterology. 2007;  132 96-102
• 64 Kaminski M F, Regula J, Kraszewska E et al. Quality indicators for colonoscopy and the risk of interval cancer.  N Engl J Med. 2010;  362 1795-1803
• 65 Lin O S, Kozarek R A, Schembre D B et al. Screening colonoscopy in very elderly patients: prevalence of neoplasia and estimated impact on life expectancy.  JAMA. 2006;  295 2357-2365
• 66 Benson K, Hartz A J. A comparison of observational studies and randomized, controlled trials.  N Engl J Med. 2000;  342 1878-1886
• 67 Concato J, Shah N, Horwitz R I. Randomized, controlled trials, observational studies, and the hierarchy of research designs.  N Engl J Med. 2000;  342 1887-1892
• 68 Lansdorp-Vogelaar I, van Ballegooijen M, Zauber A G et al. Effect of rising chemotherapy costs on the cost savings of colorectal cancer screening.  J Natl Cancer Inst. 2009;  101 1412-1422