The Relationship Between Distal and Proximal Colonic Neoplasia: A Meta-Analysis
To investigate the association between proximal colonic neoplasia and distal lesions as a function of the lesion type. The extent to which health, demographic, and study characteristics moderate this association was also examined.
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STUDY ELIGIBILITY CRITERIA
Studies allowing the calculation of OR of proximal neoplasia
(PN) and proximal advanced neoplasia (PAN) for distal hyperplastic polyps (HP), nonadvanced adenomas (NAA), adenomas (AD), and advanced neoplasia (AN); also, studies for which the proportions of subjects with isolated (i.e., not accompanied by distal lesions) PN (IPN) and PAN (IPAN) over the total number of subjects with PN or PAN could be calculated.
STUDY APPRAISAL AND SYNTHESIS METHODS
Thirty-two studies were included for calculating OR between proximal neoplasia and distal lesions and 40 studies for proportions of IPN and IPAN. Subgroup analyses were conducted for presence of symptoms, prevalence of PN and PAN, age, proportion of males, geographic region, study design, and demarcation point.
The association between distal lesions and proximal neoplasia increased with the severity of the distal lesions. Odds of PN were higher in subjects with HP compared to subjects with a normal distal colon. Odds of PN and PAN were higher in subjects with NAA, AD, and AN than in subjects with a normal distal colon. PAN were more strongly associated with distal lesions in asymptomatic populations, in young populations, and in populations with a low prevalence of PAN. In approximately 60% of the subjects with PN and PAN, these neoplasia were isolated.
The present results may be affected by publication bias and dichotomization in the subgroup analyses. Limitations related to the individual studies include self-selection, lesion misclassification and misses, and technological advances leading to changes in the detection of lesions during the time span of the included studies.
CONCLUSIONS AND IMPLICATIONS OF KEY FINDINGS
All types of distal lesions are predictive of PN. All types of distal neoplasia are predictive of PAN. The association between distal lesions and proximal neoplasia increases with the severity of the distal lesion. The association between distal lesions and proximal advanced neoplasia is stronger in low-risk groups as compared to high-risk groups.
- Benson VS, Patnick J, Davies AK, Nadel MR, Smith RA, Atkin WS. Colorectal cancer screening: A comparison of 35 initiatives in 17 countries. Int J Cancer. 2008;122:1357–67. CrossRef
- Winawer SJ, Zauber AG. The advanced adenoma as the primary target of screening. Gastrointest Endosc Clin N Am. 2002;12:1–9. CrossRef
- Winawer SJ, Zauber AG, Fletcher RH, 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. CA Cancer J Clin. 2006;56:143–59. CrossRef
- Levin B, Lieberman DA, 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. CA Cancer J Clin. 2008;58:130–60. CrossRef
- Institute for Clinical Systems Improvement. Health care guideline: Colorectal cancer screening. Thirteenth edition, 2010. Available from: http://www.icsi.org/colorectal_cancer_screening/colorectal_cancer_screening_5.html.
- Binda V, Pereira-Lima J, Nunes CA, Falkemberg LT, Azambuja DB, Cruz JV. Is there a role for sigmoidoscopy in symptomatic patients? Analysis of a study correlating distal and proximal colonic neoplasias detected by colonoscopy in a symptomatic population. Arq Gastroenterol. 2007;44:2–7. CrossRef
- Brady PG, Straker RJ, McClave SA, Nord HJ, Pinkas M, Robinson BE. Are hyperplastic rectosigmoid polyps associated with an increased risk of proximal colonic neoplasms? Gastrointest Endosc. 1993;39:481–5. CrossRef
- Foutch PG, DiSario JA, Pardy K, Mai HD, Manne RK. The sentinel hyperplastic polyp: A marker for synchronous neoplasia in the proximal colon. Am J Gastroenterol. 1991;86:1482–5.
- Lieberman DA, Smith FW. Screening for colon malignancy with colonoscopy. Am J Gastroenterol. 1991;86:946–51.
- Lin OS, Schembre DB, McCormick SE, et al. Risk of proximal colorectal neoplasia among asymptomatic patients with distal hyperplastic polyps. Am J Med. 2005;118:1113–9. CrossRef
- Pennazio M, Arrigoni A, Risio M, Spandre M, Rossini FP. Small rectosigmoid polyps as markers of proximal neoplasms. Dis Colon Rectum. 1993;36:1121–5. CrossRef
- Provenzale D, Martin ZZ, Holland KL, Sandler RS. Colon adenomas in patients with hyperplastic polyps. J Clin Gastroenterol. 1988;10:46–9. CrossRef
- Provenzale D, Garrett JW, Condon SE, Sandler RS. Risk for colon adenomas in patients with rectosigmoid hyperplastic polyps. Ann Intern Med. 1990;113:760–3.
- Rex DK, Smith JJ, Ulbright TM, Lehman GA. Distal colonic hyperplastic polyps do not predict proximal adenomas in asymptomatic average-risk subjects. Gastroenterology. 1992;102:317–9.
- Byeon JS, Yang SK, Kim TI, et al. Colorectal neoplasm in asymptomatic Asians: a prospective multinational multicenter colonoscopy survey. Gastrointest Endosc. 2007;65:1015–22. CrossRef
- Imperiale TF, Wagner DR, Lin CY, Larkin GN, Rogge JD, Ransohoff DF. Using risk for advanced proximal colonic neoplasia to tailor endoscopic screening for colorectal cancer. Ann Intern Med. 2003;139:959–65.
- Leung WK, Ho KY, Kim W, et al. Colorectal neoplasia in Asia: a multicenter colonoscopy survey in symptomatic patients. Gastrointest Endosc. 2006;64:751–9. CrossRef
- Lieberman DA, Weiss DG, Bond JH, Ahnen DJ, Garewal H, Chejfec G. Use of colonoscopy to screen asymptomatic adults for colorectal cancer. N Engl J Med. 2000;343:162–8. CrossRef
- Liou JM, Lin JT, Huang SP, et al. Screening for colorectal cancer in average-risk Chinese population using a mixed strategy with sigmoidoscopy and colonoscopy. Dis Colon Rectum. 2007;50:630–40. CrossRef
- Liu HH, Wu MC, Peng Y, Wu MS. Prevalence of advanced colonic polyps in asymptomatic Chinese. World J Gastroenterol. 2005;11:4731–4.
- Jass JR, Iino H, Ruszkiewicz A, et al. Neoplastic progression occurs through mutator pathways in hyperplastic polyposis of the colorectum. Gut. 2000;47:43–9. CrossRef
- Hawkins NJ, Ward RL. Sporadic colorectal cancers with microsatellite instability and their possible origin in hyperplastic polyps and serrated adenomas. J Natl Cancer Inst. 2001;93:1307–13. CrossRef
- Böhm SK. Hyperplastic polyps of the colorectum—Do they possess a malignant potential? The molecular classification of colorectal cancer and the serrated pathway. Gastrointest Oncol. 2002;4:97–117. CrossRef
- Boland CR, Montgomery CK, Kim YS. A cancer associated mucin alteration in benign colonic polyps. Gastroenterology. 1982;82:664–72.
- O'Brien MJ, O'Keane JC, Zauber A, Gottlieb LS, Winawer SJ. Precursors of colorectal carcinoma. Biopsy and biologic markers. Cancer. 1992;70:1317–27. CrossRef
- Mysliwiec PA, Brown ML, Klabunde CN, Ransohoff DF. Are physicians doing too much colonoscopy? A national survey of colorectal surveillance after polypectomy. Ann Intern Med. 2004;141:264–71.
- Farraye FA, Wallace M. Clinical significance of small polyps found during screening with flexible sigmoidoscopy. Gastrointest Endosc Clin N Am. 2002;12:41–51. CrossRef
- Levin TR, Palitz A, Grossman S, et al. Predicting advanced proximal colonic neoplasia with screening sigmoidoscopy. JAMA. 1999;281:1611–7. CrossRef
- Gondal G, Grotmol T, Hofstad B, Bretthauer M, Eide TJ, Hoff G. Grading of distal colorectal adenomas as predictors for proximal colonic neoplasia and choice of endoscope in population screening: experience from the Norwegian Colorectal Cancer Prevention study (NORCCAP). Gut. 2003;52:398–403. CrossRef
- Anderson JC, Alpern Z, Messina CR, et al. Predictors of proximal neoplasia in patients without distal adenomatous pathology. Am J Gastroenterol. 2004;99:472–7. CrossRef
- Dave S, Hui S, Kroenke K, Imperiale TF. Is the distal hyperplastic polyp a marker for proximal neoplasia? A systematic review. J Gen Inten Med. 2003;18:128–37. CrossRef
- Lewis JD, Ng K, Hung KE, Bilker WB, Berlin JA, Brensinger C, Rustgi AK. Detection of proximal adenomatous polyps with screening sigmoidoscopy. A systematic review and meta-analysis of screening colonoscopy. Arch Intern Med. 2003;163:413–20. CrossRef
- Lin OS, Gerson LB, Soon MS, Schembre DB, Kozarek RA. Risk of proximal colon neoplasia with distal hyperplastic polyps. A meta-analysis. Arch Intern Med. 2005;165:382–90. CrossRef
- Lieberman D. Race, gender, and colorectal cancer screening. Am J Gastroenterol. 2005;100:2756–8. CrossRef
- Nelson RL, Persky V, Turyk M. Carcinoma in situ of the colorectum: SEER trends by race, gender, and total colorectal cancer. J Surg Oncol. 1999;71:123–9. CrossRef
- Imperiale TF, Wagner DR, Lin CY, Larkin GN, Rogge JD, Ransohoff DF. Results of screening colonoscopy among persons 40 to 49 years of age. N Engl J Med. 2002;346:1781–5. CrossRef
- Strul H, Kariv R, Leshno M, et al. The prevalence rate and anatomic location of colorectal adenoma and cancer detected by colonoscopy in average-risk individuals aged 40–80 years. Am J Gastroenterol. 2006;101:255–62. CrossRef
- Hammer K, Hammer J, Oesterreicher C, Pötzi R. Advanced distal colonic lesions as predictors of advanced lesions in the proximal colon. Medicine. 2000;79:127–34. CrossRef
- O'Brien K, Sweeney BF Jr, Conger N, Fischer JR, Lang KA. Prevalence of proximal adenomas after an adenoma is found on flexible sigmoidoscopy. Cancer Detect Prev. 2003;27:259–65. CrossRef
- Borenstein M, Hedges LV, Higgins JPT, Rothstein HR. Introduction to meta-analysis. UK: West Sussex, John Wiley & Sons, Ltd.; 2009. CrossRef
- Ang YS, Macaleenan N, Mahmud N, Keeling PWN, Kelleher DP, Weir DG. The yield of colonoscopy in average-risk patients with non-specific colonic symptoms. Eur J Gastroenterol Hepatol. 2002;14:1073–7. CrossRef
- Betés Ibáñez M, Muñoz-Navas MA, Duque JM, et al. Diagnostic value of distal colonic polyps for prediction of advanced proximal neoplasia in an average-risk population undergoing screening colonoscopy. Gastrointest Endosc. 2004;59:634–41. CrossRef
- Choe JW, Chang HS, Yang SK, et al. Screening colonoscopy in asymptomatic average-risk Koreans: Analysis in relation to age and sex. J Gastroenterol Hepatol. 2007;22:1003–8. CrossRef
- Chung YW, Han DS, Park YK, Son BK, Paik CH, Jeon YC, Sohn JH. Risk of advanced proximal adenoma and cancer according to rectosigmoid findings in the Korean population. Dig Dis Sci. 2006;51:2206–12. CrossRef
- Erarslan E, Turkay C, Isik A, Uz B, Kaya A, Bavbek N. Prevalence of proximal neoplasms among asymptomatic patients according to distal colorectal findings. Dig Dis Sci. 2009;54:1312–6. CrossRef
- Ikeda Y, Mori M, Miyazaki M, Yoshizumi T, Maehara Y, Sugimachi K. Significance of small distal adenoma for detection of proximal neoplasms in the colorectum. Gastrointest Endosc. 2000;52:358–61. CrossRef
- Johnson DA, Gurney MS, Volpe RJ, et al. A prospective study of the prevalence of colonic neoplasms in asymptomatic patients with an age-related risk. Am J Gastroenterol. 1990;85:969–74.
- Kadakia SC, Wrobleski CS, Kadakia AS, Meier NJ. Prevalence of proximal colonic polyps in average-risk asymptomatic patients with negative fecal occult blood tests and flexible sigmoidoscopy. Gastrointest Endosc. 1996;44:112–7. CrossRef
- Khan A, Shrier I, Gordon PH. Do distal adenomas mandate total colonoscopy? Surg Endosc. 2003;17:886–90. CrossRef
- Nicholson FB, Korman MG, Stern AI, Hansky J. Distribution of colorectal adenomas: implications for bowel cancer screening. Med J Aust. 2000;172:428–30.
- Odelowo OO, Hoque M, Begum R, Islam KK, Smoot DT. Colonoscopy for colorectal cancer screening in African Americans. J Assoc Acad Minor Phys. 2002;13:66–8.
- Okamoto M, Kawabe T, Yamaji Y, et al. Rectosigmoid findings are not associated with proximal colon cancer: Analysis of 6 196 consecutive cases undergoing total colonoscopy. World J Gastroenterol. 2005;11:2249–54.
- Park HW, Byeon JS, Yang SK, et al. Colorectal neoplasm in asymptomatic average-risk Koreans: The KASID prospective multicenter colonoscopy survey. Gut Liver. 2009;3:35–40. CrossRef
- Sciallero S, Costantini M, Bertinelli E, et al. Distal hyperplastic polyps do not predict proximal adenomas: results from a multicentric study of colorectal adenomas. Gastrointest Endosc. 1997;46:124–30. CrossRef
- Thiis-Evensen E, Hoff GS, Sauar J, Majak BM, Vatn MH. Flexible sigmoidoscopy or colonoscopy as a screening modality for colorectal adenomas in older age groups? Findings in a cohort of the normal population aged 63–72 years. Gut. 1999;45:834–9. CrossRef
- Al-Enezi SA, Alsurayei SA, Ismail AE, Aly NYA, Ismail WA, Abou-Bakr AA. Adenomatous colorectal polyps in patients referred for colonoscopy in a regional hospital in Kuwait. Saudi J Gastroenterol. 2010;16:188–93. CrossRef
- Castiglione G, Ciatto S, Mazzotta A, Grazzini G. Sensitivity of screening sigmoidoscopy for proximal colorectal tumours. Lancet. 1995;354:729–7.
- Chiu HM, Wang HP, Lee YC, et al. A prospective study of the frequency and the topographical distribution of colon neoplasia in asymptomatic average-risk Chinese adults as determined by colonoscopic screening. Gastrointest Endosc. 2005;61:547–53. CrossRef
- Gryska RV, Cohen AM. Screening asymptomatic patients at high risk for colon cancer with full colonoscopy. Dis Colon Rectum. 1987;30:18–20. CrossRef
- Kim DH, Lee SY, Choi KS, et al. The usefulness of colonoscopy as a screening test for detecting colorectal polyps. Hepato-Gastroenterology. 2007;54:2240–2.
- Lieberman DA, Smith FW. Frequency of isolated proximal colonic polyps among patients referred for colonoscopy. Arch Intern Med. 1988;148:473–5. CrossRef
- Schoenfeld P, Cash B, Flood A, et al. Colonoscopic screening of average-risk women for colorectal neoplasia. N Engl J Med. 2005;352:2061–8. CrossRef
- Soon M-W, Soon A, Lin T-Y, Lin OS. Distribution of colon neoplasia in Chinese patients: implications for endoscopic screening strategies. Eur J Gastroenterol Hepatol. 2008;20:642–7. CrossRef
- Negri E, Braga C, La Vecchia C, et al. Family history of cancer and risk of colorectal cancer in Italy. Br J Cancer. 1998;77:174–9. CrossRef
- Slattery ML, Friedman GD, Potter JD, Edwards S, Caan BJ, Samowitz W. A description of age, sex, and site distributions of colon carcinoma in three geographic areas. Cancer. 1996;78:1666–70. CrossRef
- Rex DK, Lehman GA, Ulbright TM, et al. Colonic neoplasia in asymptomatic persons with negative fecal occult blood tests: Influence of age, gender, and family history. Am J Gastroenterol. 1993;88:825–31.
- Imperiale TF, Wagner DR, Lin CY, Larkin GN, Rogge JD, Ransohoff DF. Risk of advanced proximal neoplasms in asymptomatic adults according to the distal colorectal findings. N Engl J Med. 2000;343:169–74. CrossRef
- McCashland TM, Brand R, Lyden E, De Garmo P. Gender differences in colorectal polyps and tumors. Am J Gastroenterol. 2001;96:882–6. CrossRef
- Australian Institute of Health and Welfare and the Australasian Association of Cancer Registries. Cancer in Australia 1991-1994 (with projections to 1999). Canberra: AIHW, 1998.
- Brenner H, Hoffmeister M, Stegmaier C, Brenner G, Altenhofen L, Haug U. Risk of progression of advanced adenomas to colorectal cancer by age and sex: estimates based on 840 149 screening colonoscopies. Gut. 2007;56:1585–9. CrossRef
- Nguyen SP, Bent S, Chen YH, Terdiman JP. Gender as a risk factor for advanced neoplasia and colorectal cancer: A systematic review and meta-analysis. Clin Gastroenterol Hepatol. 2009;7:676–81. CrossRef
- Chao A, Gilliland FD, Hunt WC, Bulterys M, Becker TM, Key CR. Increasing incidence of colon and rectal cancer among Hispanics and American Indians in New Mexico (United States), 1969–94. Cancer Causes Control. 1998;9:137–44. CrossRef
- Qing SH, Rao KY, Jiang HY, Wexner SD. Racial differences in the anatomical distribution of colorectal cancer: a study of differences between American and Chinese patients. World J Gastroenterol. 2003;9:721–5.
- Francois F, Park J, Bini EJ. Colon pathology detected after a positive screening flexible sigmoidoscopy: a prospective study in an ethnically diverse cohort. Am J Gastroenterol. 2006;101:823–30. CrossRef
- Theuer CP, Taylor TH, Brewster WR, Campbell BS, Becerra JC, Anton-Culver H. The topography of colorectal cancer varies by race/ethnicity and affects the utility of flexible sigmoidoscopy. Am Surg. 2001;67:1157–61.
- Soon MS, Kozarek RA, Ayub K, Soon A, Lin TY, Lin OS. Screening colonoscopy in Chinese and Western patients: A comparative study. Am J Gastroenterol. 2005;100:2749–55. CrossRef
- Painter J, Saunders DB, Bell GD, Williams CB, Pitt R, Bladen J. Depth of insertion at flexible sigmoidoscopy: implications for colorectal cancer screening and instrument design. Endoscopy. 1999;31:227–31. CrossRef
- Kronborg O. Colon polyps and cancer. Endoscopy. 2000;32:124–30. CrossRef
- Boursi B, Halak A, Umansky M, Galzan L, Guzner-Gur H, Arber N. Colonoscopic screening of an average-risk population for colorectal neoplasia. Endoscopy. 2009;41:516–21. CrossRef
- Keren D, Rainis T, Goldstein O, Stermer E, Lavy A. Significant colonic neoplasia prevalence and ASGE recommendations. Is it time for a change? J Clin Gastroenterol. 2008;42:886–91. CrossRef
- Farrands PA, Hardcastle JD, Chamberlain J, Moss S. Factors affecting compliance with screening for colorectal cancer. Community Med. 1984;6:12–9.
- Chao A, Connell CJ, Cokkinides V, Jacobs EJ, Calle EE, Thun MJ. Underuse of screening sigmoidoscopy and colonoscopy in a large cohort of US adults. Am J Public Health. 2004;94:1775–81. CrossRef
- Van Rijn JC, Reitsma JB, Stoker J, Bossuyt PM, Van Deventer SJ, Dekker E. Polyp miss rate determined by tandem colonoscopy: a systematic review. Am J Gastroenterol. 2006;101:343–50. CrossRef
- Rex DK, Cutler CS, Lemmel GT, et al. Colonoscopic miss rates of adenomas determined by back-to-back colonoscopies. Gastroenterology. 1997;112:24–8. CrossRef
- Norfleet RG, Ryan ME, Wyman JB. Adenomatous and hyperplastic polyps cannot be reliably distinguished by their appearance through the fiberoptic sigmoidoscope. Dig Dis Sci. 1988;33:1175–7. CrossRef
- Neale AV, Demers RY, Budev H, Scott RO. Physician accuracy in diagnosing colorectal polyps. Dis Colon Rectum. 1987;30:247–50. CrossRef
- Schoen RE, Gerber LD, Margulies C. The pathologic measurement of polyp size is preferable to the endoscopic estimate. Gastrointest Endosc. 1997;46:492–6. CrossRef
- Gopalswamy N, Shenoy VN, Choudhry U, et al. Is in vivo measurement of size of polyps during colonoscopy accurate? Gastrointest Endosc. 1997;46:497–502. CrossRef
- MacCallum RC, Zhang S, Preacher KJ, Rucker DD. On the practice of dichotomization of quantitative variables. Psychol Methods. 2002;7:19–40. CrossRef
- Tribonias G, Theodoropoulou A, Konstantinidis K, et al. Comparison of standard versus high-definition, wide-angle colonoscopy for polyp detection: a randomized controlled trial. Colorectal Dis. 2010;12:e260–6.
- Rex D. Detection of neoplasia at colonoscopy: what next? Endoscopy. 2008;40:333–5. CrossRef
- Barclay RL, Vicari JJ, Doughty AS, Johanson JF, Greenlaw RL. Colonoscopic withdrawal times and adenoma detection during screening colonoscopy. N Engl J Med. 2006;355:2533–41. CrossRef
- East JE, Stavrindis M, Thomas-Gibson S, Guenther T, Tekkis PP, Saunders BP. A comparative study of standard vs. high definition colonoscopy for adenoma and hyperplastic polyp detection with optimized withdrawal technique. Aliment Pharmacol Ther. 2008;28:768–76. CrossRef
- Rex DK. Colonoscopic withdrawal technique is associated with adenoma miss rates. Gastrointest Endosc. 2000;51:33–6. CrossRef
- Hoff G, Grotmol T, Skovlund E, Bretthauer M. Risk of colorectal cancer seven years after flexible sigmoidoscopy screening: randomised controlled trial. BMJ. 2009;338:b1846. CrossRef
- Atkin WS, Edwards R, Kralj-Hans I, et al. Once-only flexible sigmoidoscopy screening in prevention of colorectal cancer: a multicentre randomised controlled trial. Lancet. 2010;375:1624–33. CrossRef
- Segnan N, Senore C, Andreoni B, et al. Baseline findings of the Italian multicentre randomised controlled trial of “once-only sigmoidoscopy”—SCORE. J Natl Cancer Inst. 2002;94:1763–72. CrossRef
- Weissfeld JL, Schoen RE, Pinsky PF, et al. Flexible sigmoidoscopy in the PLCO cancer screening trial: results from the baseline screening examination of a randomized trial. J Natl Cancer Inst. 2005;97:989–97. CrossRef
- Bretthauer M. Colorectal cancer screening. J Intern Med. 2011;270:87–98. CrossRef
- The Relationship Between Distal and Proximal Colonic Neoplasia: A Meta-Analysis
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