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Original Research |

Screening Colonoscopy and Risk for Incident Late-Stage Colorectal Cancer Diagnosis in Average-Risk Adults: A Nested Case–Control Study

Chyke A. Doubeni, MD, MPH; Sheila Weinmann, PhD; Kenneth Adams, PhD; Aruna Kamineni, PhD; Diana S.M. Buist, PhD; Arlene S. Ash, PhD; Carolyn M. Rutter, PhD; V. Paul Doria-Rose, PhD; Douglas A. Corley, MD, PhD; Robert T. Greenlee, PhD; Jessica Chubak, PhD; Andrew Williams, PhD; Aimee R. Kroll-Desrosiers, MS; Eric Johnson, MS; Joseph Webster, BA; Kathryn Richert-Boe, MD; Theodore R. Levin, MD; Robert H. Fletcher, MD, MSc; and Noel S. Weiss, MD, DrPH
[+] Article and Author Information

From University of Pennsylvania, Philadelphia, Pennsylvania; Meyers Primary Care Institute/Reliant Medical Group and University of Massachusetts Medical School, Worcester, Massachusetts; Kaiser Permanente Northwest, Portland, Oregon; HealthPartners Health System, Minneapolis, Minnesota; Group Health Research Institute and University of Washington, Seattle, Washington; National Cancer Institute, National Institutes of Health, Bethesda, Maryland; Kaiser Permanente Division of Research, Oakland, California; Marshfield Clinic Research Foundation, Marshfield, Wisconsin; Kaiser Permanente Hawaii, Honolulu, Hawaii; and Harvard Medical School, Boston, Massachusetts.

Note: This study was performed as part of a multicenter cancer screening comparative effectiveness research project, SEARCH (Screening Effectiveness and Research in Community-based Healthcare), which was supported by grant UC2CA148576 from the National Cancer Institute of the National Institutes of Health.

Disclaimer: The contents of this report are solely the responsibility of the authors and do not necessarily represent the official views of the National Institutes of Health or the National Cancer Institute.

Acknowledgment: The authors thank the SEARCH coordinators (Debra Bonollo, Shawn Gagne, Gabrielle Gundersen, Denise Schwarzkopf, and Cyndee Yonehara) for coordinating data collection on this project, the medical records auditors (Amy Stone Murai, RN, MS, APRN-C, CHRC, at Kaiser Permanente Hawaii; Janet Guilbert and Doris Hoyer at Reliant Medical Group; Elie Castro and Melanie Currier at the Group Health Research Institute; and Kim Olsen at Kaiser Permanente Northwest), and Hirut Fassil for help with manuscript preparation.

Grant Support: By grant UC2CA148576 from the National Cancer Institute of the National Institutes of Health. Additional support was provided to Dr. Doubeni through awards K01-CA127118, K01-CA127118-S1, and U01-CA151736, also from the National Institutes of Health. Data collection on cancer incidence for this study was supported in part by data infrastructure developed by the HMO Cancer Research Network at participating sites. Group Health Research Institute's Cancer Surveillance System is funded in part by contracts N01-CN-67009 and N01-PC-35142 from the Surveillance, Epidemiology and End Results Program of the National Cancer Institute, with additional support from the State of Washington.

Potential Conflicts of Interest: Disclosures can be viewed at www.acponline.org/authors/icmje/ConflictOfInterestForms.do?msNum=M12-1665.

Reproducible Research Statement: Study protocol: Not available, but additional details of the study design and implementation are available from Dr. Doubeni (e-mail, chyke.doubeni@uphs.upenn.edu). Statistical code and data set: Available from Dr. Doubeni (e-mail, chyke.doubeni@uphs.upenn.edu).

Requests for Single Reprints: Chyke A. Doubeni, MD, MPH, Department of Family Medicine and Community Health, Perelman School of Medicine, University of Pennsylvania, 3400 Spruce Street, Gates 2, Philadelphia, PA 19104; e-mail, chyke.doubeni@uphs.upenn.edu.

Current Author Addresses: Dr. Doubeni: Department of Family Medicine and Community Health, Perelman School of Medicine, University of Pennsylvania, 3400 Spruce Street, Gates 2, Philadelphia, PA 19104.

Dr. Weinmann: Center for Health Research, Kaiser Permanente Northwest, 3800 North Interstate Avenue, Portland, OR 97227.

Dr. Adams: HealthPartners Institute for Education and Research, MS 21111R, 8170 33rd Avenue South, PO Box 1524, Minneapolis, MN 55406.

Drs. Kamineni, Buist, Rutter, and Chubak; Mr. Johnson; and Mr. Webster: Group Health Research Institute, 1730 Minor Avenue, Suite 1600, Seattle, WA 98101.

Dr. Ash and Ms. Kroll-Desrosiers: University of Massachusetts School of Medicine, 55 Lake Avenue North, Worcester, MA 01655.

Dr. Doria-Rose: National Cancer Institute, Applied Research Program, 6130 Executive Boulevard, Room 4110, Bethesda, MD 20892-7344.

Dr. Corley: Kaiser Permanente, 2000 Broadway, Oakland, CA 94612.

Dr. Greenlee: Marshfield Clinic Research Foundation, 1000 North Oak Avenue, Mail Stop ML2, Marshfield, WI 54449.

Dr. Williams: Kaiser Permanente Hawaii, 501 Alakawa Street, Suite 201, Honolulu, HI 96817.

Dr. Richert-Boe: Kaiser Permanente Northwest, 500 NE Multnomah Street, Portland, OR 97232.

Dr. Levin: The Permanente Medical Group, 1425 South Main Street, Walnut Creek, CA 94596.

Dr. Fletcher: Harvard Medical School, 133 Brookline Avenue, Boston, MA 02215.

Dr. Weiss: University of Washington, Box 357236, Seattle, WA 98195.

Author Contributions: Conception and design: C.A. Doubeni, S. Weinmann, A. Kamineni, D.S.M. Buist, A.S. Ash, C.M. Rutter, V.P. Doria-Rose, D.A. Corley, R.T. Greenlee, J. Chubak, K. Richert-Boe, T.R. Levin, R.H. Fletcher, N.S. Weiss.

Analysis and interpretation of the data: C.A. Doubeni, S. Weinmann, A. Kamineni, D.S.M. Buist, A.S. Ash, C.M. Rutter, V.P. Doria-Rose, D.A. Corley, J. Chubak, A. Williams, A.R. Kroll-Desrosiers, J. Webster, R.H. Fletcher, N.S. Weiss.

Drafting of the article: C.A. Doubeni, K. Adams, N.S. Weiss.

Critical revision of the article for important intellectual content: C.A. Doubeni, S. Weinmann, K. Adams, A. Kamineni, D.S.M. Buist, A.S. Ash, C.M. Rutter, V.P. Doria-Rose, D.A. Corley, R.T. Greenlee, J. Chubak, A. Williams, E. Johnson, K. Richert-Boe, T.R. Levin, R.H. Fletcher, N.S. Weiss.

Final approval of the article: C.A. Doubeni, S. Weinmann, K. Adams, A. Kamineni, D.S.M. Buist, A.S. Ash, C.M. Rutter, V.P. Doria-Rose, D.A. Corley, R.T. Greenlee, J. Chubak, A. Williams, E. Johnson, K. Richert-Boe, T.R. Levin, R.H. Fletcher, N.S. Weiss.

Provision of study materials or patients: S. Weinmann, A. Kamineni, D.S.M. Buist, A. Williams, K. Richert-Boe.

Statistical expertise: C.A. Doubeni, A.S. Ash, C.M. Rutter, A.R. Kroll-Desrosiers.

Obtaining of funding: C.A. Doubeni, D.S.M. Buist.

Administrative, technical, or logistic support: C.A. Doubeni, S. Weinmann, D.S.M. Buist, A. Williams, J. Webster.

Collection and assembly of data: C.A. Doubeni, S. Weinmann, K. Adams, A. Kamineni, D.A. Corley, R.T. Greenlee, J. Chubak, A. Williams, J. Webster, K. Richert-Boe, R.H. Fletcher, N.S. Weiss.


Ann Intern Med. 2013;158(5_Part_1):312-320. doi:10.7326/0003-4819-158-5-201303050-00003
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Chinese translation

Background: The effectiveness of screening colonoscopy in average-risk adults is uncertain, particularly for right colon cancer.

Objective: To examine the association between screening colonoscopy and risk for incident late-stage colorectal cancer (CRC).

Design: Nested case–control study.

Setting: Four U.S. health plans.

Patients: 1039 average-risk adults enrolled for at least 5 years in one of the health plans. Case patients were aged 55 to 85 years on their diagnosis date (reference date) of stage IIB or higher (late-stage) CRC during 2006 to 2008. One or 2 control patients were selected for each case patient, matched on birth year, sex, health plan, and prior enrollment duration.

Measurements: Receipt of CRC screening 3 months to 10 years before the reference date, ascertained through medical record audits. Case patients and control patients were compared on receipt of screening colonoscopy or sigmoidoscopy by using conditional logistic regression that accounted for health history, socioeconomic status, and other screening exposures.

Results: In analyses restricted to 471 eligible case patients and their 509 matched control patients, 13 case patients (2.8%) and 46 control patients (9.0%) had undergone screening colonoscopy, which corresponded to an adjusted odds ratio (AOR) of 0.29 (95% CI, 0.15 to 0.58) for any late-stage CRC, 0.36 (CI, 0.16 to 0.80) for right colon cancer, and 0.26 (CI, 0.06 to 1.11; P = 0.069) for left colon/rectum cancer. Ninety-two case patients (19.5%) and 173 control patients (34.0%) had screening sigmoidoscopy, corresponding to an AOR of 0.50 (CI, 0.36 to 0.70) overall, 0.79 (CI, 0.51 to 1.23) for right colon late-stage cancer, and 0.26 (CI, 0.14 to 0.48) for left colon cancer.

Limitation: The small number of screening colonoscopies affected the precision of the estimates.

Conclusion: Screening with colonoscopy in average-risk persons was associated with reduced risk for diagnosis of incident late-stage CRC, including right-sided colon cancer. For sigmoidoscopy, this association was seen for left CRC, but the association for right colon late-stage cancer was not statistically significant.

Primary Funding Source: National Cancer Institute of the National Institutes of Health.

Figures

Grahic Jump Location
Figure 1.

Study flow diagram.

CRC = colorectal cancer.

* Control patients were matched on the reference date to case patients according to study site on calendar year of birth, sex, and length of continuous health plan enrollment (5 to 10 y) before the reference date.

† “Strong family history” refers to CRC diagnosed in 1 or more first-degree relatives before age 50 y or 2 or more relatives of any age, or other familial syndromes.

‡ Cancer in segments proximal to the splenic flexure was classified as right colon cancer.

§ “Left colon/rectum” refers to the splenic flexure, descending colon, sigmoid, and rectum.

Grahic Jump Location
Grahic Jump Location
Figure 2.

Sensitivity of the odds ratio estimates for screening colonoscopy on any late-stage colorectal cancer to varying the assumed preclinical period for excluding tests.

The preclinical period is the time from the assumed onset of preclinical late-stage disease to the date of clinical diagnosis, which we varied from 1 to 15 mo. Odds ratios and 95% CIs were obtained with conditional logistic regression, with screening defined as exposure to a definite or probable screening test. Analyses were done on matched case–control sets by using conditional logistic regression, which adjusted for receipt of other screening tests (sigmoidoscopy, barium enema, and fecal occult blood test), census block group poverty levels (as a continuous variable), number of preventive health care visits, family history of colorectal cancer, and comorbidity index score at baseline. Missing poverty level values were multiply imputed using predictive mean matching.

Grahic Jump Location

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Summary for Patients

Screening Colonoscopy and Colorectal Cancer Risk

The full report is titled “Screening Colonoscopy and Risk for Incident Late-Stage Colorectal Cancer Diagnosis in Average-Risk Adults. A Nested Case–Control Study.” It is in the 5 March 2013 issue of Annals of Internal Medicine (volume 158, pages 312-320). The authors are C.A. Doubeni, S. Weinmann, K. Adams, A. Kamineni, D.S.M. Buist, A.S. Ash, C.M. Rutter, V.P. Doria-Rose, D.A. Corley, R.T. Greenlee, J. Chubak, A. Williams, A.R. Kroll-Desrosiers, E. Johnson, J. Webster, K. Richert-Boe, T.R. Levin, R.H. Fletcher, and N.S. Weiss.

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