Abstract
Background:
Several methods are recommended equally strongly for colorectal cancer screening in average-risk persons. Risk stratification would enable tailoring of screening within this group, with less invasive tests (sigmoidoscopy or occult blood tests) for lower-risk persons and colonoscopy for higher-risk persons.
Objective:
To create a risk index for advanced neoplasia (colorectal cancer and adenomas or serrated polyps ≥1.0 cm, villous histology, or high-grade dysplasia) anywhere in the colorectum, using the most common risk factors for colorectal neoplasia.
Design:
Cross-sectional study.
Setting:
Multiple endoscopy units, primarily in the Midwest.
Patients:
Persons aged 50 to 80 years undergoing initial screening colonoscopy (December 2004 to September 2011).
Measurements:
Derivation and validation of a risk index based on points from regression coefficients for age, sex, waist circumference, cigarette smoking, and family history of colorectal cancer.
Results:
Among 2993 persons in the derivation set, prevalence of advanced neoplasia was 9.4%. Risks for advanced neoplasia in persons at very low, low, intermediate, and high risk were 1.92% (95% CI, 0.63% to 4.43%), 4.88% (CI, 3.79% to 6.18%), 9.93% (CI, 8.09% to 12.0%), and 24.9% (CI, 21.1% to 29.1%), respectively ( P < 0.001). Sigmoidoscopy to the descending colon in the low-risk groups would have detected 51 of 70 (73% [CI, 61% to 83%]) advanced neoplasms. Among 1467 persons in the validation set, corresponding risks for advanced neoplasia were 1.65% (CI, 0.20% to 5.84%), 3.31% (CI, 2.08% to 4.97%), 10.9% (CI, 8.26% to 14.1%), and 22.3% (CI, 16.9% to 28.5%), respectively (P < 0.001). Sigmoidoscopy would have detected 21 of 24 (87.5% [CI, 68% to 97%]) advanced neoplasms.
Limitations:
Split-sample validation; results apply to first-time screening.
Conclusion:
This index stratifies risk for advanced neoplasia among average-risk persons by identifying lower-risk groups for which noncolonoscopy strategies may be effective and efficient and a higher-risk group for which colonoscopy may be preferred.
Primary Funding Source:
National Cancer Institute, Walther Cancer Institute, Indiana University Simon Cancer Center, and Indiana Clinical and Translational Sciences Institute.
References
- 1.
Steele CB ,Rim SH ,Joseph DA ,King JB ,Seeff LC ;Centers for Disease Control and Prevention (CDC) . Colorectal cancer incidence and screening—United States, 2008 and 2010. MMWR Surveill Summ. 2013;62 Suppl 3:53-60. [PMID: 24264490] MedlineGoogle Scholar - 2.
Zauber AG ,Lansdorp-Vogelaar I ,Knudsen AB ,Wilschut J ,vanBallegooijen M ,Kuntz KM . Evaluating test strategies for colorectal cancer screening: a decision analysis for the U.S. Preventive Services Task Force. Ann Intern Med. 2008;149:659-69. [PMID: 18838717] doi:10.7326/0003-4819-149-9-200811040-00244 LinkGoogle Scholar - 3.
Whitlock EP ,Lin JS ,Liles E ,Beil TL ,Fu R . Screening for colorectal cancer: a targeted, updated systematic review for the U.S. Preventive Services Task Force. Ann Intern Med. 2008;149:638-58. [PMID: 18838718] doi:10.7326/0003-4819-149-9-200811040-00245 LinkGoogle Scholar - 4.
Heitman SJ ,Manns BJ ,Hilsden RJ ,Fong A ,Dean S ,Romagnuolo J . Cost-effectiveness of computerized tomographic colonography versus colonoscopy for colorectal cancer screening. CMAJ. 2005;173:877-81. [PMID: 16217110] CrossrefMedlineGoogle Scholar - 5.
Frazier AL ,Colditz GA ,Fuchs CS ,Kuntz KM . Cost-effectiveness of screening for colorectal cancer in the general population. JAMA. 2000;284:1954-61. [PMID: 11035892] CrossrefMedlineGoogle Scholar - 6.
Parekh M ,Fendrick AM ,Ladabaum U . As tests evolve and costs of cancer care rise: reappraising stool-based screening for colorectal neoplasia. Aliment Pharmacol Ther. 2008;27:697-712. [PMID: 18248653] doi:10.1111/j.1365-2036.2008.03632.x CrossrefMedlineGoogle Scholar - 7.
Sharaf RN ,Ladabaum U . Comparative effectiveness and cost-effectiveness of screening colonoscopy vs. sigmoidoscopy and alternative strategies. Am J Gastroenterol. 2013;108:120-32. [PMID: 23247579] doi:10.1038/ajg.2012.380 CrossrefMedlineGoogle Scholar - 8.
Levin B ,Lieberman DA ,McFarland B ,Andrews KS ,Brooks D ,Bond J ,et al ;American Cancer Society Colorectal Cancer Advisory Group . 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;134:1570-95. [PMID: 18384785] doi:10.1053/j.gastro.2008.02.002 CrossrefMedlineGoogle Scholar - 9.
Rex DK ,Johnson DA ,Anderson JC ,Schoenfeld PS ,Burke CA ,Inadomi JM ;American College of Gastroenterology . American College of Gastroenterology guidelines for colorectal cancer screening 2009 [corrected]. Am J Gastroenterol. 2009;104:739-50. [PMID: 19240699] doi:10.1038/ajg.2009.104 CrossrefMedlineGoogle Scholar - 10.
U.S. Preventive Services Task Force . Screening for colorectal cancer: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med. 2008;149:627-37. [PMID: 18838716] doi:10.7326/0003-4819-149-9-200811040-00243 LinkGoogle Scholar - 11.
Pignone M ,Russell L ,Wagner J . Economic Models of Colorectal Cancer Screening in Average-Risk Adults: Workshop Summary. Washington, DC: National Academies Pr; 2005. Google Scholar - 12.
Pignone M ,Rich M ,Teutsch SM ,Berg AO ,Lohr KN . Screening for colorectal cancer in adults at average risk: a summary of the evidence for the U.S. Preventive Services Task Force. Ann Intern Med. 2002;137:132-41. [PMID: 12118972] doi:10.7326/0003-4819-137-2-200207160-00015 LinkGoogle Scholar - 13.
Centers for Disease Control and Prevention (CDC). . Vital signs: colorectal cancer screening test use—United States, 2012. MMWR Morb Mortal Wkly Rep. 2013;62:881-8. [PMID: 24196665] MedlineGoogle Scholar - 14.
Tangka FK ,Subramanian S ,Beebe MC ,Hoover S ,Royalty J ,Seeff LC . Clinical costs of colorectal cancer screening in 5 federally funded demonstration programs. Cancer. 2013;119 Suppl 15:2863-9. [PMID: 23868481] doi:10.1002/cncr.28154 CrossrefMedlineGoogle Scholar - 15.
Seeff LC ,Richards TB ,Shapiro JA ,Nadel MR ,Manninen DL ,Given LS ,et al . How many endoscopies are performed for colorectal cancer screening? Results from CDC's survey of endoscopic capacity. Gastroenterology. 2004;127:1670-7. [PMID: 15578503] CrossrefMedlineGoogle Scholar - 16.
Freedman AN ,Slattery ML ,Ballard-Barbash R ,Willis G ,Cann BJ ,Pee D ,et al . Colorectal cancer risk prediction tool for white men and women without known susceptibility. J Clin Oncol. 2009;27:686-93. [PMID: 19114701] doi:10.1200/JCO.2008.17.4797 CrossrefMedlineGoogle Scholar - 17.
Park Y ,Freedman AN ,Gail MH ,Pee D ,Hollenbeck A ,Schatzkin A ,et al . Validation of a colorectal cancer risk prediction model among white patients age 50 years and older. J Clin Oncol. 2009;27:694-8. [PMID: 19114700] doi:10.1200/JCO.2008.17.4813 CrossrefMedlineGoogle Scholar - 18.
Driver JA ,Gaziano JM ,Gelber RP ,Lee IM ,Buring JE ,Kurth T . Development of a risk score for colorectal cancer in men. Am J Med. 2007;120:257-63. [PMID: 17349449] CrossrefMedlineGoogle Scholar - 19.
Betés M ,Muñoz-Navas MA ,Duque JM ,Angós R ,Macías E ,Súbtil JC ,et al . Use of colonoscopy as a primary screening test for colorectal cancer in average risk people. Am J Gastroenterol. 2003;98:2648-54. [PMID: 14687811] MedlineGoogle Scholar - 20.
Cai QC ,Yu ED ,Xiao Y ,Bai WY ,Chen X ,He LP ,et al . Derivation and validation of a prediction rule for estimating advanced colorectal neoplasm risk in average-risk Chinese. Am J Epidemiol. 2012;175:584-93. [PMID: 22328705] doi:10.1093/aje/kwr337 CrossrefMedlineGoogle Scholar - 21.
Kaminski MF ,Polkowski M ,Kraszewska E ,Rupinski M ,Butruk E ,Regula J . A score to estimate the likelihood of detecting advanced colorectal neoplasia at colonoscopy. Gut. 2014;63:1112-9. [PMID: 24385598] doi:10.1136/gutjnl-2013-304965 CrossrefMedlineGoogle Scholar - 22.
Lin OS ,Kozarek RA ,Schembre DB ,Ayub K ,Gluck M ,Cantone N ,et al . Risk stratification for colon neoplasia: screening strategies using colonoscopy and computerized tomographic colonography. Gastroenterology. 2006;131:1011-9. [PMID: 17030171] CrossrefMedlineGoogle Scholar - 23.
Tao S ,Hoffmeister M ,Brenner H . Development and validation of a scoring system to identify individuals at high risk for advanced colorectal neoplasms who should undergo colonoscopy screening. Clin Gastroenterol Hepatol. 2014;12:478-85. [PMID: 24022090] doi:10.1016/j.cgh.2013.08.042 CrossrefMedlineGoogle Scholar - 24.
Yeoh KG ,Ho KY ,Chiu HM ,Zhu F ,Ching JY ,Wu DC ,et al ;Asia-Pacific Working Group on Colorectal Cancer . The Asia-Pacific Colorectal Screening score: a validated tool that stratifies risk for colorectal advanced neoplasia in asymptomatic Asian subjects. Gut. 2011;60:1236-41. [PMID: 21402615] doi:10.1136/gut.2010.221168 CrossrefMedlineGoogle Scholar - 25.
Brenner H ,Altenhofen L ,Stock C ,Hoffmeister M . Natural history of colorectal adenomas: birth cohort analysis among 3.6 million participants of screening colonoscopy. Cancer Epidemiol Biomarkers Prev. 2013;22:1043-51. [PMID: 23632815] doi:10.1158/1055-9965.EPI-13-0162 CrossrefMedlineGoogle Scholar - 26.
von Elm E ,Altman DG ,Egger M ,Pocock SJ ,Gøtzsche PC ,Vandenbroucke JP ;STROBE Initiative . The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Ann Intern Med. 2007;147:573-7. [PMID: 17938396] doi:10.7326/0003-4819-147-8-200710160-00010 LinkGoogle Scholar - 27.
Collins GS ,Reitsma JB ,Altman DG ,Moons KG . Transparent Reporting of a multivariable prediction model for Individual Prognosis or Diagnosis (TRIPOD): the TRIPOD statement. Ann Intern Med. 2015;162:55-63. [PMID: 25560714] doi:10.7326/M14-0697 LinkGoogle Scholar - 28.
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. [PMID: 10900275] CrossrefMedlineGoogle Scholar - 29.
Wang Y ,Jacobs EJ ,Patel AV ,Rodríguez C ,McCullough ML ,Thun MJ ,et al . A prospective study of waist circumference and body mass index in relation to colorectal cancer incidence. Cancer Causes Control. 2008;19:783-92. [PMID: 18322811] doi:10.1007/s10552-008-9141-x CrossrefMedlineGoogle Scholar - 30.
Giacosa A ,Franceschi S ,LaVecchia C ,Favero A ,Andreatta R . Energy intake, overweight, physical exercise and colorectal cancer risk. Eur J Cancer Prev. 1999;8 Suppl 1:S53-60. [PMID: 10772419] MedlineGoogle Scholar - 31.
Giovannucci E ,Ascherio A ,Rimm EB ,Colditz GA ,Stampfer MJ ,Willett WC . Physical activity, obesity, and risk for colon cancer and adenoma in men. Ann Intern Med. 1995;122:327-34. [PMID: 7847643] doi:10.7326/0003-4819-122-5-199503010-00002 LinkGoogle Scholar - 32.
Hosmer DW ,Lemeshow S . Applied Logistic Regression, Second Edition. New York: J Wiley; 2000. Google Scholar - 33.
Sullivan LM ,Massaro JM ,D'Agostino RB . Presentation of multivariate data for clinical use: The Framingham Study risk score functions. Stat Med. 2004;23:1631-60. [PMID: 15122742] CrossrefMedlineGoogle Scholar - 34.
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. [PMID: 14678915] doi:10.7326/0003-4819-139-12-200312160-00005 LinkGoogle Scholar - 35.
Taylor DP ,Burt RW ,Williams MS ,Haug PJ ,Cannon-Albright LA . Population-based family history-specific risks for colorectal cancer: a constellation approach. Gastroenterology. 2010;138:877-85. [PMID: 19932107] doi:10.1053/j.gastro.2009.11.044 CrossrefMedlineGoogle Scholar - 36.
Seeff LC ,Manninen DL ,Dong FB ,Chattopadhyay SK ,Nadel MR ,Tangka FK ,et al . Is there endoscopic capacity to provide colorectal cancer screening to the unscreened population in the United States? Gastroenterology. 2004;127:1661-9. [PMID: 15578502] CrossrefMedlineGoogle Scholar - 37.
Steele RJ ,McDonald PJ ,Digby J ,Brownlee L ,Strachan JA ,Libby G ,et al . Clinical outcomes using a faecal immunochemical test for haemoglobin as a first-line test in a national programme constrained by colonoscopy capacity. United European Gastroenterol J. 2013;1:198-205. [PMID: 24917960] doi:10.1177/2050640613489281 CrossrefMedlineGoogle Scholar - 38.
Ballew C ,Lloyd BG ,Miller SH . Capacity for colorectal cancer screening by colonoscopy, Montana, 2008. Am J Prev Med. 2009;36:329-32. [PMID: 19285198] doi:10.1016/j.amepre.2008.11.021 CrossrefMedlineGoogle Scholar - 39.
Rodríguez-Moranta F ,Trapero-Bertran M ,Castells A ,Mas-Canal X ,Balaguer F ,Pellisé M ,et al . Endoscopic requirements of colorectal cancer screening programs in average-risk population. Estimation according to a Markov model. Gastroenterol Hepatol. 2008;31:405-12. [PMID: 18783684] CrossrefMedlineGoogle Scholar - 40.
Regula J ,Rupinski M ,Kraszewska E ,Polkowski M ,Pachlewski J ,Orlowska J ,et al . Colonoscopy in colorectal-cancer screening for detection of advanced neoplasia. N Engl J Med. 2006;355:1863-72. [PMID: 17079760] CrossrefMedlineGoogle Scholar - 41.
Ferlitsch M ,Reinhart K ,Pramhas S ,Wiener C ,Gal O ,Bannert C ,et al . Sex-specific prevalence of adenomas, advanced adenomas, and colorectal cancer in individuals undergoing screening colonoscopy. JAMA. 2011;306:1352-8. [PMID: 21954479] doi:10.1001/jama.2011.1362 CrossrefMedlineGoogle Scholar - 42.
Park HW ,Han S ,Lee JS ,Chang HS ,Lee D ,Choe JW ,et al . Risk stratification for advanced proximal colon neoplasm and individualized endoscopic screening for colorectal cancer by a risk-scoring model. Gastrointest Endosc. 2012;76:818-28. [PMID: 22884098] doi:10.1016/j.gie.2012.06.013 CrossrefMedlineGoogle Scholar - 43.
Imperiale TF ,Glowinski EA ,Lin-Cooper C ,Ransohoff DF . Tailoring colorectal cancer screening by considering risk of advanced proximal neoplasia. Am J Med. 2012;125:1181-7. [PMID: 23062404] doi:10.1016/j.amjmed.2012.05.026 CrossrefMedlineGoogle Scholar - 44.
Lieberman DA ,Weiss DG ,Bond JH ,Ahnen DJ ,Garewal H ,Chejfec G . Use of colonoscopy to screen asymptomatic adults for colorectal cancer. Veterans Affairs Cooperative Study Group 380. N Engl J Med. 2000;343:162-8. [PMID: 10900274] CrossrefMedlineGoogle Scholar - 45.
Hassan C ,Pooler BD ,Kim DH ,Rinaldi A ,Repici A ,Pickhardt PJ . Computed tomographic colonography for colorectal cancer screening: risk factors for the detection of advanced neoplasia. Cancer. 2013;119:2549-54. [PMID: 23754679] doi:10.1002/cncr.28007 CrossrefMedlineGoogle Scholar - 46.
Lansdorp-Vogelaar I ,vanBallegooijen M ,Zauber AG ,Boer R ,Wilschut J ,Winawer SJ ,et al . Individualizing colonoscopy screening by sex and race. Gastrointest Endosc. 2009;70:96-108, 108. [PMID: 19467539] doi:10.1016/j.gie.2008.08.040 CrossrefMedlineGoogle Scholar - 47.
Justice AC ,Covinsky KE ,Berlin JA . Assessing the generalizability of prognostic information. Ann Intern Med. 1999;130:515-24. [PMID: 10075620] doi:10.7326/0003-4819-130-6-199903160-00010 LinkGoogle Scholar - 48.
Altman DG ,Royston P . What do we mean by validating a prognostic model? Stat Med. 2000;19:453-73. [PMID: 10694730] CrossrefMedlineGoogle Scholar - 49.
Schroy PC ,Coe A ,Chen CA ,O'Brien MJ ,Heeren TC . Prevalence of advanced colorectal neoplasia in white and black patients undergoing screening colonoscopy in a safety-net hospital. Ann Intern Med. 2013;159:13-20. [PMID: 23817700] doi:10.7326/0003-4819-159-1-201307020-00004 LinkGoogle Scholar - 50.
Levitzky BE ,Brown CC ,Heeren TC ,Schroy PC . Performance of a risk index for advanced proximal colorectal neoplasia among a racially/ethnically diverse patient population (risk index for advanced proximal neoplasia). Am J Gastroenterol. 2011;106:1099-106. [PMID: 21326221] doi:10.1038/ajg.2011.20 CrossrefMedlineGoogle Scholar - 51.
Kwah J ,Schroy PC ,Jacobson BC ,Calderwood AH . Whites and blacks have similar risk of metachronous advanced colorectal neoplasia. Dig Dis Sci. 2014;59:2264-71. [PMID: 24700155] doi:10.1007/s10620-014-3132-4 CrossrefMedlineGoogle Scholar - 52.
Friedenberg FK ,Singh M ,George NS ,Sankineni A ,Shah S . Prevalence and distribution of adenomas in black Americans undergoing colorectal cancer screening. Dig Dis Sci. 2012;57:489-95. [PMID: 22052446] doi:10.1007/s10620-011-1952-z CrossrefMedlineGoogle Scholar
Author, Article, and Disclosure Information
Thomas F. Imperiale,
From Indiana University School of Medicine, Regenstrief Institute, Indiana University Melvin and Bren Simon Cancer Center, Richard L. Roudebush Veterans Affairs Medical Center, and Indianapolis Gastroenterology Research Foundation, Indianapolis, Indiana, and University of North Carolina at Chapel Hill, Chapel Hill, North Carolina.
Acknowledgment: The authors thank Curlie Morrow, BSBA, for project management and Janetta Matesan for data management.
Grant Support: By the National Cancer Institute (R01-CA104459); the Walther Cancer Institute, Indianapolis, Indiana; the Indiana University Melvin and Bren Simon Cancer Center; and a project development team within the Indiana Clinical and Translational Sciences Institute (grant UL1TR001108 from the National Center for Research Resources, National Institutes of Health), Indianapolis, Indiana.
Disclosures: Dr. Imperiale reports grants from the National Cancer Institute, the Walther Cancer Foundation, the Indiana Clinical and Translational Sciences Institute, and the Indiana University Melvin and Bren Simon Cancer Center during the conduct of the study. Authors not named here have disclosed no conflicts of interest. Disclosures can also be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?ms Num=M14-1720.
Editors' Disclosures: Christine Laine, MD, MPH, Editor in Chief, reports that she has no financial relationships or interests to disclose. Darren B. Taichman, MD, PhD, Executive Deputy Editor, reports that he has no financial relationships or interests to disclose. Cynthia D. Mulrow, MD, MSc, Senior Deputy Editor, reports that she has no relationships or interests to disclose. Deborah Cotton, MD, MPH, Deputy Editor, reports that she has no financial relationships or interest to disclose. Jaya K. Rao, MD, MHS, Deputy Editor, reports that she has stock holdings/options in Eli Lilly and Pfizer. Sankey V. Williams, MD, Deputy Editor, reports that he has no financial relationships or interests to disclose. Catharine B. Stack, PhD, MS, Deputy Editor for Statistics, reports that she has stock holdings in Pfizer.
Reproducible Research Statement:Study protocol and data set: Not available. Statistical code: Available from Dr. Imperiale (e-mail, timperia@iu.
Corresponding Author: Thomas F. Imperiale, MD, Indiana University Medical Center, Regenstrief Institute, 1050 Wishard Boulevard, Indianapolis, IN 46202; e-mail, timperia@iu.
Current Author Addresses: Dr. Imperiale: Indiana University Medical Center, Regenstrief Institute, 1050 Wishard Boulevard, Indianapolis, IN 46202.
Dr. Monahan: Indiana University School of Medicine, 410 West 10th Street, Suite 3000, Indianapolis, IN 46202.
Mr. Stump: Department of Biostatistics, Indiana University School of Medicine, 410 West 10th Street, Suite 3000, Indianapolis, IN 46202.
Ms. Glowinski: Indianapolis Gastroenterology Research Foundation, 8051 South Emerson Avenue, Suite 200, Indianapolis, IN 46237.
Dr. Ransohoff: University of North Carolina at Chapel Hill, CB 7080, Chapel Hill, NC 27599-7080.
Author Contributions: Conception and design: T.F. Imperiale, D.F. Ransohoff.
Analysis and interpretation of the data: T.F. Imperiale, P.O. Monahan, T.E. Stump, D.F. Ransohoff.
Drafting of the article: T.F. Imperiale, P.O. Monahan, T.E. Stump.
Critical revision of the article for important intellectual content: T.F. Imperiale, P.O. Monahan, T.E. Stump, D.F. Ransohoff.
Final approval of the article: T.F. Imperiale, P.O. Monahan, T.E. Stump, E.A. Glowinski, D.F. Ransohoff.
Provision of study materials or patients: T.F. Imperiale.
Statistical expertise: P.O. Monahan, T.E. Stump.
Obtaining of funding: T.F. Imperiale.
Administrative, technical, or logistic support: E.A. Glowinski.
Collection and assembly of data: T.F. Imperiale, E.A. Glowinski.
This article was published online first at www.annals.org on 11 August 2015.
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