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Original Research |

One-Year Risk for Advanced Colorectal Neoplasia: U.S. Versus U.K. Risk-Stratification Guidelines

María Elena Martínez*, PhD; Patricia Thompson, PhD; Karen Messer, PhD; Erin L. Ashbeck, MPH; David A. Lieberman, MD; John A. Baron, MD; Dennis J. Ahnen, MD; Douglas J. Robertson, MD; Elizabeth T. Jacobs, PhD; E. Robert Greenberg, MD; Amanda J. Cross, PhD; and Wendy Atkin*, PhD
[+] Article and Author Information

* Drs. Martínez and Atkin contributed equally to this manuscript.


From the Moores Cancer Center and University of California, San Diego, School of Medicine, La Jolla, California; Arizona Cancer Center and College of Medicine and Mel and Enid Zuckerman Arizona College of Public Health, University of Arizona, Tucson, Arizona; Portland Veterans Affairs Medical Center, Portland, Oregon; University of North Carolina School of Medicine, Chapel Hill, North Carolina; Denver Veterans Affairs Medical Center and University of Colorado School of Medicine, Denver, Colorado; White River Junction Veterans Affairs Medical Center, White River Junction, Vermont; Fred Hutchinson Cancer Research Center, Seattle, Washington; National Cancer Institute, Rockville, Maryland; and Imperial College, London, United Kingdom.

Disclaimer: The views expressed in this document are those of the authors and do not necessarily reflect the official position of the European Commission. Neither the European Commission nor any other organization nor any person acting alone or on behalf of others can be held responsible for any use that may be made of the information in this document.

Grant Support: By the European Union Health Programme (Development of European Guidelines for Quality Assurance of Colorectal Cancer Screening; grant agreement 2005317); the International Agency for Research on Cancer; and the U.S. Public Health Service grants CA-41108, CA-23074, CA95060, CA37287, CA104869, CA23108, CA59005, and CA26852 from the National Cancer Institute.

Potential Conflicts of Interest: Disclosures can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M12-1274.

Reproducible Research Statement: Study protocol: Available from Dr. Martínez (e-mail, e8martinez@ucsd.edu). Statistical code and data set: Not available.

Requests for Single Reprints: María Elena Martínez, PhD, Moores Cancer Center, University of California, San Diego, 3855 Health Sciences Drive 0901, La Jolla, CA 92093-0901; e-mail, e8martinez@ucsd.edu.

Current Author Addresses: Drs. Martínez and Messer: Moores Cancer Center, University of California, San Diego, 3855 Health Sciences Drive 0901, La Jolla, CA 92093-0901.

Drs. Thompson, Ashbeck, and Jacobs: Arizona Cancer Center, 1515 North Campbell Avenue, PO Box 245024, Tucson, AZ 85724.

Dr. Lieberman: Division of Gastroenterology, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, L461, Portland, OR 97239-3098.

Dr. Baron: University of North Carolina at Chapel Hill, 4160-B Bioinformatics Building CB 7080, Mason Farm Road, Chapel Hill, NC 27599-7080.

Dr. Ahnen: Denver Veterans Affairs Medical Center 111E, 1055 Clermont Street, Denver, CO 80220.

Dr. Robertson: The Geisel School of Medicine at Dartmouth and The Dartmouth Institute, Chief, Section of Gastroenterology, Veterans Affairs Medical Center, White River Junction, VT 05009.

Dr. Greenberg: Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, 1100 Fairview Avenue North, Seattle, WA 98109.

Dr. Cross: Division of Cancer Epidemiology and Genetics, National Cancer Institute, Executive Plaza South, Room 3050, Bethesda, MD 20892-7335.

Dr. Atkin: Department of Surgery and Cancer, Imperial College London, St. Mary's Campus, Norfolk Place, London W2 1PG, United Kingdom.

Author Contributions: Conception and design: M.E. Martínez, D.A. Lieberman, D.J. Ahnen, E.R. Greenberg, W. Atkin.

Analysis and interpretation of the data: M.E. Martínez, P. Thompson, K. Messer, E.L. Ashbeck, D.A. Lieberman, J.A. Baron, D.J. Ahnen, D.J. Robertson, E.T. Jacobs, E.R. Greenberg, A.J. Cross, W. Atkin.

Drafting of the article: M.E. Martínez, P. Thompson, K. Messer, E.L. Ashbeck, D.A. Lieberman, E.T. Jacobs, E.R. Greenberg, W. Atkin.

Critical revision of the article for important intellectual content: M.E. Martínez, P. Thompson, K. Messer, E.L. Ashbeck, D.A. Lieberman, J.A. Baron, D.J. Ahnen, D.J. Robertson, E.T. Jacobs, E.R. Greenberg, A.J. Cross, W. Atkin.

Final approval of the article: M.E. Martínez, P. Thompson, K. Messer, E.L. Ashbeck, D.A. Lieberman, J.A. Baron, D.J. Ahnen, D.J. Robertson, E.T. Jacobs, E.R. Greenberg, A.J. Cross, W. Atkin.

Provision of study materials or patients: M.E. Martínez, D.J. Ahnen, E.R. Greenberg.

Statistical expertise: K. Messer.

Obtaining of funding: M.E. Martínez, D.A. Lieberman, E.R. Greenberg, W. Atkin.

Administrative, technical, or logistic support: M.E. Martínez, P. Thompson, E.R. Greenberg.

Collection and assembly of data: M.E. Martínez, J.A. Baron, D.J. Ahnen, E.R. Greenberg, A.J. Cross.


Ann Intern Med. 2012;157(12):856-864. doi:10.7326/0003-4819-157-12-201212180-00005
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Chinese translation

Background: Guidelines from the United Kingdom and the United States on risk stratification after polypectomy differ, as do recommended surveillance intervals.

Objective: To compare risk for advanced colorectal neoplasia at 1-year colonoscopy among patients cross-classified by U.S. and U.K. surveillance guidelines.

Design: Pooled analysis of 4 prospective studies between 1984 and 1998.

Setting: Academic and private clinics in the United States.

Patients: 3226 postpolypectomy patients with 6- to 18-month follow-up colonoscopy.

Measurements: Rates of advanced neoplasia (an adenoma ≥1 cm, high-grade dysplasia, >25% villous architecture, or invasive cancer) at 1 year, compared across U.S. and U.K. risk categories.

Results: Advanced neoplasia was detected 1 year after polypectomy in 3.8% (95% CI, 2.7% to 4.9%) of lower-risk patients and 11.2% (CI, 9.8% to 12.6%) of higher-risk patients by U.S. criteria. According to U.K. criteria, 4.4% (CI, 3.3% to 5.4%) of low-risk patients, 9.9% (CI, 8.3% to 11.5%) of intermediate-risk patients, and 18.7% (CI, 14.8% to 22.5%) of high-risk patients presented with advanced neoplasia; U.K. high-risk patients comprised 12.1% of all patients. All U.S. lower-risk patients were low-risk by U.K. criteria; however, more patients were classified as low-risk, because the U.K. guidelines do not consider histologic features. Higher-risk U.S. patients were distributed across the 3 U.K. categories. Among all patients with advanced neoplasia, 26.3% were reclassified by the U.K. criteria to a higher-risk category and 7.0% to a lower-risk category, with a net 19.0% benefiting from detection 2 years earlier. Overall, substitution of U.K. for U.S. guidelines resulted in an estimated 0.03 additional colonoscopy every 5 years per patient.

Limitations: Patients were enrolled 15 to 20 years ago, and quality measures for colonoscopy were unavailable. Patients lacking follow-up colonoscopy or with surveillance colonoscopy after 6 to 18 months and those with cancer or insufficient baseline adenoma characteristics were excluded (2076 of 5302).

Conclusion: Application of the U.K. guidelines in the United States could identify a subset of high-risk patients who may warrant a 1-year clearing colonoscopy without substantially increasing rates of colonoscopy.

Primary Funding Source: European Union Public Health Programme.

Figures

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Figure 1.

U.S. and U.K. colonoscopy surveillance guidelines, according to risk group.

Participants in the pooled studies required ≥1 adenoma to be eligible. HGD = high-grade dysplasia; LGD = low-grade dysplasia.

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Appendix Figure.

Advanced neoplasia at a 1-y colonoscopy according to U.S. and U.K. risk groups.

APPS = Antioxidant Polyp Prevention Study; BC = β-carotene; CPPS = Calcium Polyp Prevention Study; PPT = Polyp Prevention Trial; WBF = Wheat Bran Fiber.

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Figure 2.

Patients classified by U.S. colonoscopy surveillance risk groups, reclassified according to U.K. colonoscopy surveillance risk groups.

Colonoscopy risk classifications with corresponding U.S. (references 6 and 9) and U.K. (references 7 and 8) surveillance recommendations and absolute risk for advanced neoplasms and HGD/CRC found at colonoscopy 1 y after polypectomy (n = 3226) are shown. Advanced neoplasia is defined as ≥1 of the following characteristics: large adenoma (≥1 cm), presence of HGD, adenoma with tubulovillous or villous architecture, or CRC. CRC = colorectal cancer; HGD = high-grade dysplasia; LGD = low-grade dysplasia.

* Values reported in this column are percentages.

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UK post-polypectomy surveillance colonoscopy guideline
Posted on January 14, 2013
Douglas K. Rex
(Chair) US Multi-Society Task Force on Colorectal Cancer
Conflict of Interest: None Declared

Martinez et al (1) found that the UK colonoscopy post-polypectomy surveillance guideline identified a high-risk group of patients who benefit from repeat colonoscopy at 1 year after baseline, but for whom the US Multi-Society Task Force (MSTF) guideline recommends colonoscopy at 3 years (2). Martinez et al acknowledged that advanced lesions detected at 1 year in the high risk group were likely missed during the baseline examinations. Multiple adenomas are well established as a predictor of missed lesions in tandem colonoscopy studies. The potential implications of this study for the U.S. guideline are substantial.

The 2012 MSTF post-polypectomy recommendations emphasize that the ability of any surveillance guideline to protect patients from colorectal cancer depends on the effectiveness of baseline colonoscopies (2). The MSTF has recommended since 2002 that colonoscopists establish the quality of their mucosal inspection technique and lesion recognition skills by measurement of their individual adenoma detection rates (3). Low adenoma detection rates are a powerful predictor of cancers that develop during the interval between colonoscopies (4).

The colonoscopies in the studies used by Martinez et al to compare the effects of the UK to US guidelines were performed at least 4 years prior to the first recommendation to measure adenoma detection rates (3). No information on adenoma detection rates of the study colonoscopists is available (1). There is a possibility that interval cancers observed in the studies at 1 year occurred largely in patients whose baseline colonoscopies were performed by poor detectors.

The MSTF looks forward to studies reporting the risk of interval cancers at 1 year in the UK high-risk group, with results stratified by the adenoma detection rates of colonoscopists performing the baseline examinations. In the interim, the MSTF continues to recommend colonoscopy at 3 years for the UK high risk group, provided that baseline examinations are complete to the cecum and have adequate bowel preparation. This recommendation is based largely on a randomized controlled trial which showed that a single examination at 3 years was as effective as examinations at 1 and 3 years for preventing incident advanced neoplasms (5). Most importantly, the MSTF recommends that all colonoscopists measure their adenoma detection rates. The MSTF considers high quality mucosal inspection and effective polypectomy during baseline examinations to be the most important and cost-effective strategies for colonoscopic prevention of colorectal cancer.

References:

1. Martinez ME, Thompson P, Messer K, Ashbeck EL, Lieberman DA, Baron JA, et al. One-year risk for advanced colorectal neoplasia: U.S. versus U.K. risk-stratification guidelines. Ann Intern Med. 2012;157(12):856-64.

2. Lieberman DA, Rex DK, Winawer SJ, Giardiello FM, Johnson DA, Levin TR. Guidelines for colonoscopy surveillance after screening and polypectomy: a consensus update by the US Multi-Society Task Force on Colorectal Cancer. Gastroenterology. 2012;143(3):844-57.

3. Rex DK, Bond JH, Winawer S, Levin TR, Burt RW, Johnson DA, et al. Quality in the technical performance of colonoscopy and the continuous quality improvement process for colonoscopy: recommendations of the U.S. Multi-Society Task Force on Colorectal Cancer. Am J Gastroenterol. 2002;97(6):1296-308.

4. Kaminski MF, Regula J, Kraszewska E, Polkowski M, Wojciechowska U, Didkowska J, et al. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med. 2010;362(19):1795-803.

5. Winawer S, Zauber A, Ho M, O’Brien M, Gottlieb L, Sternberg S, et al. Randomized comparison of surveillance intervals after colonoscopic removal of newly diagnosed adenomatous polyps. N Engl J Med. 1993;328:901-6.

Author's Response
Posted on February 8, 2013
Maria Martinez
UCSD
Conflict of Interest: None Declared

We thank Dr. Rex for his thoughtful discussion of the implications of our report for the U.S. colonoscopy surveillance guidelines. His letter particularly emphasizes the importance of improving endoscopy quality, a point that we acknowledged in our report. Indeed, 73% (200/273) of all advanced neoplasms and 69% (18/26) of high-grade dysplasias/cancers that were detected at the one-year colonoscopy in our population occurred among patients who would not be categorized as high-risk by the U.K. guidelines. However, while focusing on colonoscopy performance clearly deserves a high priority, it should also be acknowledged that examination is not likely to be perfect if multiple adenomas are detected (as Dr. Rex has noted), and current surveillance intervals are based on estimates of the rate of advanced neoplasms over time from studies similar to those included in our study. Although we lack data on adenoma detection rates for the endoscopists who performed the examinations that form the basis for our report, it would seem imprudent to totally discount the 2.0% (8/391) risk for high-grade dysplasia and invasive cancer at one year that we observed in the U.K. high-risk group. Thus, our findings showing that some patients are particularly likely to have an advanced neoplasm at one year should continue to be an important consideration in guiding follow-up surveillance.

María Elena Martínez, PhD

Moores Cancer Center and University of California, San Diego, La Jolla, CA

Dennis Ahnen, MD

Denver Veterans Affairs Medical Center and University of Colorado School of Medicine,

Denver, CO

E. Robert Greenberg, MD

Fred Hutchinson Cancer Research Center, Seattle, WA

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