Original Article
Prevention of Colorectal Cancer by Colonoscopic Polypectomy
N Engl J Med 1993; 329:1977-1981December 30, 1993
- Abstract
Background
The current practice of removing adenomatous polyps of the colon and rectum is based on the belief that this will prevent colorectal cancer. To address the hypothesis that colonoscopic polypectomy reduces the incidence of colorectal cancer, we analyzed the results of the National Polyp Study with reference to other published results.
Methods
The study cohort consisted of 1418 patients who had a complete colonoscopy during which one or more adenomas of the colon or rectum were removed. The patients subsequently underwent periodic colonoscopy during an average follow-up of 5.9 years, and the incidence of colorectal cancer was ascertained. The incidence rate of colorectal cancer was compared with that in three reference groups, including two cohorts in which colonic polyps were not removed and one general-population registry, after adjustment for sex, age, and polyp size.
Results
Ninety-seven percent of the patients were followed clinically for a total of 8401 person-years, and 80 percent returned for one or more of their scheduled colonoscopies. Five asymptomatic early-stage colorectal cancers (malignant polyps) were detected by colonoscopy (three at three years, one at six years, and one at seven years). No symptomatic cancers were detected. The numbers of colorectal cancers expected on the basis of the rates in the three reference groups were 48.3, 43.4, and 20.7, for reductions in the incidence of colorectal cancer of 90, 88, and 76 percent, respectively (P<0.001).
Conclusions
Colonoscopic polypectomy resulted in a lower-than-expected incidence of colorectal cancer. These results support the view that colorectal adenomas progress to adenocarcinomas, as well as the current practice of searching for and removing adenomatous polyps to prevent colorectal cancer.
Media in This Article
Figure 1
Cumulative Incidence of Colorectal Cancer in the National Polyp Study Cohort.Table 1
Characteristics of the Five Patients with Colorectal Cancer (Malignant Polyp) Detected at Follow-up Colonoscopy.Article Activity
- Article
The prevalence of adenomatous polyps of the colon and rectum in the United States and other Western countries is high, as is the incidence of colorectal cancer1,2. Many people with polyps have been identified in recent years as a result of screening with stool-blood tests and flexible sigmoidoscopy and the frequent use of colonoscopy3-5. It is current practice to remove polyps when detected, search the colon for additional polyps, and arrange for long-term follow-up of the subject6. This practice is based on the concept that adenomatous polyps are the precursor of colorectal cancer and that removing them will prevent colorectal cancer7. Proof of this concept would provide evidence that adenomas progress to adenocarcinomas and support the effectiveness of the current practice of identifying and removing adenomatous polyps. This paper reports the results of the National Polyp Study, which addressed the hypothesis that colonoscopic polypectomy reduces the incidence of colorectal cancer. Previous papers have reported information regarding the organization, design, patient characteristics, follow-up results, and pathological findings of this study8-10.
Methods
Patients
All patients referred to the seven participating centers for initial colonoscopy or polypectomy between November 1980 and February 1990 who did not have a family or personal history of familial polyposis, inflammatory bowel disease, history of polypectomy, or history of colorectal cancer were prospectively evaluated for enrollment in the study8-10. After colonoscopy, patients were excluded if they had no polyps, nonadenomatous polyps, malignant polyps, a sessile adenoma larger than 3 cm in diameter, or colorectal cancer. Eligible patients had at least one histologically documented adenoma of the colon or rectum and had undergone a complete colonoscopy during which all identified polyps were removed. Consenting patients were randomly assigned to more frequent (examinations in years 1 and 3) or less frequent (examination in year 3) follow-up with colonoscopy and barium enema. The patients were also offered a follow-up examination at six years. All patients completed a questionnaire, had fecal occult-blood testing, and were contacted annually by telephone by a study coordinator8,10. The patients had clinical follow-up regardless of where their diagnostic tests or treatment was conducted. All endoscopic, pathological, and surgical findings from other institutions were obtained and reviewed. Data on the patients in both arms of the study were pooled for the analysis of the incidence of colorectal cancer. Death certificates were obtained for all patients who died, and patients' records, pathology reports, slides, and x-ray films were reviewed by a mortality review committee. All pathology slides were reviewed by the pathology review committee.
Reference Groups
Three reference groups were used to determine the expected incidence rates of colorectal cancer in the study cohort.
Reference Group 1
The first reference group was a retrospective cohort of 226 patients studied at the Mayo Clinic in Rochester, Minnesota, between 1965 and 1970 who had polyps 1 cm or larger in diameter that were above the reach of a rigid sigmoidoscope and were detected by barium enema; these patients had declined surgical polypectomy11. Patients presenting with colorectal cancer were excluded. The patients were followed for an average of nine years, and 32 colon cancers were detected. The cumulative incidence of colon cancer was 4 percent at 5 years and 14 percent at 10 years. Of the cancers detected, 21 (66 percent) were detected at the same site as the index polyp, and 11 (34 percent) were at sites distant from it.
Reference Group 2
The second reference group was a retrospective cohort of 1618 patients who underwent excision of rectal adenomas between 1957 and 1980 at St. Mark's Hospital in London12. Patients presenting with colorectal cancer or given a diagnosis of colorectal cancer within two years after the excision of adenomas were excluded. The average age of the patients at the time of diagnosis of the adenoma was 58 years; 66 percent were men. The patients were followed for an average of 14 years, and 35 colon cancers were detected. The standardized incidence ratio for colon cancer was 2.1.
Reference Group 3
The Surveillance, Epidemiology, and End Results (SEER) Program of the National Cancer Institute monitors the incidence of colorectal cancer and the mortality rates from this disease in 10 registries that represent people at average risk in the general population in the United States13. The age- and sex-specific rates of colorectal cancer for calendar years 1983 to 1987 were used, since this period represents the midpoint of accrual and follow-up for the cohort in the National Polyp Study.
Statistical Analysis
The number of person-years at risk was calculated for each patient according to age, sex, and the size of the largest adenoma at initial examination. Person-years at risk were calculated from the date of initial colonoscopy to the end of the study in February 1990, death, or for those lost to follow-up, the last date on which the patient was known to be alive. The numbers of person-years at risk were used in conjunction with the rates of colorectal cancer in the reference populations to determine the number of colorectal cancers expected in the study cohort after adjustment for age and sex14.
Since the Mayo Clinic group consisted of a cohort with large polyps (≥ 1 cm), the rates of colorectal cancer expected in the National Polyps Study group could be determined only for patients with large adenomas. For the Mayo Clinic cohort, the risk of colon cancer per year of follow-up was derived from the cumulative incidence curve for cancer detected at any site within the colon and was converted to an incidence rate. The number of person-years at risk for patients in the National Polyp Study who had large adenomas was multiplied by the colon cancer rate for the Mayo Clinic cohort to yield the number of colorectal cancers expected. The age and sex distribution of the Mayo Clinic patients with large polyps was assumed to be similar to that of the study patients with large adenomas; no data on age and sex were reported11. The number of cancers expected in patients with large adenomas was also based on the Mayo Clinic rates of cancer at the index site only (66 percent of the cancers detected) and at sites distant from the index site (34 percent of the cancers detected). The age- and sex-specific rates for SEER were applied to the number of person-years at risk for patients in the National Polyp Study who had small or medium-size adenomas in order to obtain the number of colorectal cancers expected in this subgroup. The number of cancers expected in the patients with large adenomas and those with small or medium-size adenomas were totaled to obtain an overall expected number for the comparison with the Mayo Clinic values.
To obtain rates expected for the National Polyp Study cohort based on the values for the St. Mark's group, the standardized incidence ratio for colon cancer of 2.1 in the latter group was multiplied by the age- and sex-specific rates of colorectal cancer for the SEER Program, since the study cohort was an American rather than a British population. These rates were applied to the age- and sex-specific number of person-years in the study cohort to obtain the number of cancers expected on the basis of the St. Mark's data. It was assumed that the age and sex distribution of the St. Mark's group was similar to that of the study cohort. The age- and sex-specific rates for the SEER Program were multiplied by the age- and sex-specific number of person-years at risk for the entire National Polyp Study cohort to obtain the number of cases expected on the basis of general population rates.
Cumulative incidence curves were calculated by the Kaplan-Meier method. The observed number of colorectal cancers was assumed to follow a Poisson distribution. A two-sided P value of 0.05 or less was considered to indicate statistical significance. The standardized incidence ratio of the number of cases of colorectal cancer observed divided by the number expected and the 95 percent confidence interval were calculated for each reference group15. The standardized incidence ratio was the number of colorectal cancers occurring in the National Polyp Study expressed as a proportion of the number of cancers that would be expected to occur if, within each age- and sex-specific group, the rates in the National Polyp Study cohort were the same as those in the reference group. The reduction in the incidence of colorectal cancer was calculated according to the following equation: 100 (1 - the standardized incidence ratio).
Results
Of the 1418 patients who entered the study, 993 (70 percent) were men and 425 (30 percent) were women, with a mean (±SD) age of 61 ±10 years (range, 22 to 88). Of these patients, 1210 were followed until the end of the study, and 169 were followed until death, for a total of 8401 person-years at risk (average, 5.9); 39 patients were lost to follow-up during the study. Eighty percent returned for one or more of their scheduled colonoscopies10. At the time of enrollment, 494 patients (35 percent) had adenomas larger than 1 cm in diameter and 137 patients (10 percent) had adenomas with high-grade dysplasia10. A total of 1310 patients (92 percent) had been referred for colonoscopy because of symptoms or positive results on screening or a diagnostic test8. Results of the genetic epidemiology study16 of this cohort indicated that 1 percent of the patients had three or more first-degree relatives with colorectal cancer, but none of the families satisfied the Amsterdam criteria for hereditary nonpolyposis colorectal cancer17.
Five asymptomatic colorectal cancers (malignant polyps) were detected at follow-up colonoscopy in five patients, none of whom had rectal bleeding or a change in bowel habits (Table 1Table 1
Characteristics of the Five Patients with Colorectal Cancer (Malignant Polyp) Detected at Follow-up Colonoscopy.). No patient had a symptomatic cancer or died of colorectal cancer. The cumulative incidence of colorectal cancer -- both expected and observed -- in the study cohort, based on the rates in the three reference groups, is shown in Figure 1Figure 1Cumulative Incidence of Colorectal Cancer in the National Polyp Study Cohort.. The expected number of colorectal cancers in the study cohort, based on the Mayo Clinic, St. Mark's, and SEER rates, and the level of statistical significance are shown in Table 2Table 2
Comparison of the Observed Incidence of Colorectal Cancer in the National Polyp Study Cohort with That Expected on the Basis of Data from the Three Reference Groups.. In each case, the observed incidence of colorectal cancer in the study cohort was significantly lower (P<0.001) than the expected incidence. The standardized incidence ratio was 0.10 (95 percent confidence interval, 0.03 to 0.24) for the Mayo Clinic group, 0.12 (95 percent confidence interval, 0.04 to 0.27) for the St. Mark's group, and 0.24 (95 percent confidence interval, 0.08 to 0.56) for the SEER group. The observed incidence of colorectal cancer per 1000 person-years was 0.6 in the study cohort, whereas the expected incidence was 5.8 according to the Mayo Clinic data, 5.2 according to the St. Mark's data, and 2.5 according to the SEER data.Additional comparisons were based on the Mayo Clinic reference group. The observed and expected numbers of colorectal cancers in the subgroup of patients in the National Polyp Study who had large adenomas at enrollment were 3 and 40.2, respectively, for a standardized incidence ratio of 0.07 (95 percent confidence interval, 0.02 to 0.22). For those in the subgroup with small or medium-size adenomas at enrollment, 2 cancers were observed and 8.1 were expected (standardized incidence ratio, 0.25; 95 percent confidence interval, 0.03 to 0.89). Thus, the incidence of colorectal cancer was lower than expected in patients with large as well as small or medium-size adenomas at enrollment. Even if the SEER rates were used for patients with large adenomas at enrollment, the incidence was lower than expected (standardized incidence ratio, 0.24; 95 percent confidence interval, 0.05 to 0.70). According to the Mayo Clinic data, 34.6 cancers were expected at the index site (standardized incidence ratio, 0.14; 95 percent confidence interval, 0.05 to 0.33) and 21.8 were expected at distant sites (standardized incidence ratio, 0.23; 95 percent confidence interval, 0.07 to 0.54).
Comparisons were also made after the exclusion of the number of person-years patients were at risk during the first two years of follow-up. The expected number of colorectal cancers based on the reduced number of person-years at risk was 36.3 (standardized incidence ratio, 0.14; 95 percent confidence interval, 0.04 to 0.32) for the Mayo Clinic reference group, 30.5 (standardized incidence ratio, 0.16; 95 percent confidence interval, 0.05 to 0.38) for the St. Mark's reference group, and 14.5 (standardized incidence ratio, 0.34; 95 percent confidence interval, 0.11 to 0.81) for the SEER reference group. Consequently, the incidence of colorectal cancer was at least 66 percent lower than expected, even after the exclusion of the number of person-years patients were at risk during the first two years after the initial colonoscopy.
Discussion
These results suggest that colorectal cancer can be prevented by colonoscopic removal of all identified adenomatous polyps, a finding that supports the concept of the progression of adenoma to adenocarcinoma and the current practice of colonoscopic polypectomy. Ideally, proof of the hypothesis that polypectomy reduces the incidence of colorectal cancer should be based on a randomized clinical trial in which the incidence during follow-up was determined in a control group of patients who had adenomatous polyps documented histologically but left in situ and compared with the incidence in a group of patients whose adenomatous polyps were removed. Such a design is neither ethical nor feasible. Therefore, we selected an alternative method, conducting an observational study in which reference groups were used to determine the number of colorectal cancers expected in the patients enrolled in the National Polyp Study. The number of colorectal cancers observed was then compared with the number expected.
The three reference groups provided a range of expected rates consistent with the rates of colorectal cancer in a cohort with adenomas for the period 1980 through 1990. The Mayo Clinic data were derived from a retrospective cohort study of patients with polyps measuring 1 cm or more in diameter that were detected by a barium enema; the patients declined to undergo surgery and were followed for an average of nine years11. The remainder of the colon was evaluated only by barium enema; this probably accounted for the appearance of cancer not only at the site of the identified polyps, but also at distant sites. We used the total number of colon cancers detected in the Mayo Clinic reference group regardless of their anatomical location. The incidence of colorectal cancer in the National Polyp Study cohort was significantly lower (90 percent) than expected on the basis of the rate in the Mayo Clinic group.
The St. Mark's data were also derived from a retrospective cohort study12. This cohort consisted of patients who had a rectosigmoid adenomatous polyp removed. It is reasonable to assume that approximately 50 percent of the cohort had additional (synchronous) adenomatous polyps above the rectosigmoid colon and would therefore have been expected to have additional (metachronous) adenomas2,3,6. The incidence of colorectal cancer in the National Polyp Study cohort was significantly lower (88 percent) than expected on the basis of the rate in the St. Mark's cohort.
The rate of colorectal cancer in the population covered by the SEER data would be expected to be lower than that in either of the other two reference groups, since the population consists of average-risk people rather than patients with adenomas13. A proportion of the general population harbor adenomas, but these are mostly less than 1 cm in diameter, usually with the most benign histologic characteristic (tubular adenoma), and are not associated with an increased risk of colorectal cancer1,12,18,19. A comparison of the actual incidence of colorectal cancer in the National Polyp Study cohort with that expected on the basis of SEER rates is the most rigorous test of the hypothesis that colonoscopic polypectomy reduces the incidence of colorectal cancer. The incidence in the study cohort was significantly lower (76 percent) than expected on the basis of the rate in the SEER group. This is the result of clearing the entire colon of all identified polyps by colonoscopy10.
A retrospective analysis of a cohort of patients undergoing colonoscopy between 1974 and 1985 suggested that polypectomy reduced the incidence of colorectal cancer20. In another retrospective study, the rate of death from colorectal cancer was higher in patients with adenomatous polyps who did not have polypectomy than in the general population21. Although the removal of polyps by rigid sigmoidoscopy resulted in a lower-than-expected incidence of rectosigmoid cancer,22 the histologic characteristics of the polyps removed and the completeness of the follow-up were not reported. A reduction in mortality from distal-colon cancer in two case-control studies of sigmoidoscopy could possibly be attributed to the removal of adenomas23,24. Furthermore, in the St. Mark's cohort there was a nonsignificant (60 percent) reduction in the incidence of rectal cancer in men who had rectal polyps removed and a significant increase in rectal cancer in women that was attributed to the incomplete removal of rectal polyps12.
Were the five cancers found in this study new lesions or lesions missed during a previous examination? The characteristics of the polyps removed at enrollment have been described previously9,10. The two cancers (malignant polyps) measuring less than 1 cm in diameter that were detected at six and seven years may have been new growths, but it is less clear whether the three larger cancers (malignant polyps) detected at three years were new or were missed at the time of the initial colonoscopy.
Was the lower-than-expected incidence of colorectal cancer in the study cohort related to the exclusion of patients with colorectal cancer at enrollment? We think not. Patients with colorectal cancer were also excluded from the St. Mark's and Mayo Clinic reference groups, as were patients in whom colorectal cancer developed during the first two years of follow-up in the St. Mark's group, but colonoscopy was not done at base line to exclude colonic polyps in either group. In addition, the incidence of colorectal cancer was 77 percent lower than the incidence expected on the basis of the rate of cancer at sites distant from the index polyp in the Mayo Clinic group. The results were similar even after the exclusion of the number of person-years patients were at risk during the first two years after colonoscopy.
We conclude that the incidence of colorectal cancer is reduced by colonoscopic polypectomy. These results provide evidence of the progression of adenoma to adenocarcinoma and of the effectiveness of the current practice of searching for and removing adenomatous polyps in the colon.
Supported by a grant (CA 26852) from the National Institutes of Health and sponsored by the American Gastroenterological Association, the American Society for Gastrointestinal Endoscopy, and the American College of Gastroenterology.
Source Information
From the National Polyp Study Headquarters, Memorial Sloan-Kettering Cancer Center, New York (S.J.W., A.G.Z., M.N.H., S.S.S., M. Shike, R.C.K., L.H.-L., H.G.); Mallory Institute of Pathology, Boston City Hospital, Boston (M.J.O., L.S.G.); Mount Sinai Hospital, New York (J.D.W.); Valley Presbyterian Hospital, Van Nuys, Calif. (M. Schapiro); Veterans Affairs Medical Center, Minneapolis (J.H.B.); Cedars-Sinai Medical Center, Los Angeles (J.F.P.); Massachusetts General Hospital, Boston (F.A.); and Milwaukee County Medical Complex, Milwaukee (E.T.S.).
Address reprint requests to Dr. Winawer at the Gastroenterology and Nutrition Service, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
Other members of the National Polyp Study Workgroup are listed in the Appendix.
Appendix
The following members of the National Polyp Study Workgroup also participated in the study: New York -- C.J. Lightdale, M. Edelman, M. Fleisher, B. Diaz, J. Lapidus, R.A. McMahan, B. Flehinger, M. Mandelman, H. Nazario, H. Colon, P. Kadvan, C. Miller, A. Szporn, N. Harpaz, and M. Khilnani; Minneapolis -- H. Ansel, S. Ewing, and T. Dobson; Milwaukee -- W. Hogan, J. Helm, R. Komorowski, and E. McLaughlin; Racine, Wis. -- J. Geenen, R. Venu, G.K. Johnson, and N. DeBoer; Boston -- S. Hedberg, P. Shellito, D. Hall, G. Dickersin, and N. Horton; Los Angeles -- J. Sherman, J.A. Hamlin, S. Geller, and M. Kojimoto; Van Nuys, Calif. -- M. Auslander, D. Kasimian, L. Kussin, and C. Scoggins; and Boston (Pathology Review Center) -- C. Magrath.
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Maite Betes, Miguel A. Munoz-Navas, Jose' M. Duque, Ramo'n Angos, Elena Macias, Jose C. Subtil, Maite Herraiz, Susana Riva, Miguel Delgado-Rodriguez, Miguel A. Martinez-Gonza'lez. (2003) Use of colonoscopy as a primary screening test for colorectal cancer in average risk people. The American Journal of Gastroenterology 98:12, 2648-2654
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Paul J. Villeneuve, Ann Coombs. (2003) SCREENING FOR COLORECTAL CANCER USING THE FECAL OCCULT BLOOD TEST: AN ACTUARIAL ASSESSMENT OF THE IMPACT OF A POPULATION-BASED SCREENING PROGRAM IN CANADA. International Journal of Technology Assessment in Health Care 19:04,
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C.Daniel Johnson, Alicia Y. Toledano, Benjamin A. Herman, Abraham H. Dachman, Elizabeth G. Mcfarland, Matthew A. Barish, James A. Brink, Randy D. Ernst, Joel G. Fletcher, Robert A. Halvorsen, Amy K. Hara, Kenneth D. Hopper, Robert E. Koehler, David S.K. Lu, Michael Macari, Robert L. Maccarty, Frank H. Miller, Martina Morrin, Erik K. Paulson, Judy Yee, Michael Zalis. (2003) Computerized tomographic colonography: performance evaluation in a retrospective multicenter setting1 1Vital Images Inc. has supported research at UCLA (to D. S. K. L., J. A. B., and E. G. M.). Monex provided support (to M. M.). GE Medical Systems provided software license and research support (to C. D. J., J. A. B., and A. H. D.). Voxar, Inc. produces products that compete with products listed in this paper (to M. A. B.).The study design was approved by the National Cancer Institute Cancer Therapy Evaluation Program. Computerized tomographic colonography examinations for American College of Radiology Imaging Network Protocol A6656 were submitted by E. G. McFarland, Mallinckrodt Institute of Radiology, St. Louis, Missouri; M. Zalis, Massachusetts General Hospital, Boston, Massachusetts; C. D. Johnson, Mayo Clinic, Rochester, Minnesota; M. Macari, New York University, New York, New York; D. Lu, University of California, Los Angeles, California; A. H. Dachman, University of Chicago, Chicago, Illinois; M. Morrin, Beth Israel/Deaconess Hospitals, Boston, Massachusetts; and J. Yee, Veterans Administration Hospital, San Francisco, California. Workstations for performing computerized tomographic colonography interpretations were loaned to the American College of Radiology (ACR) by General Electric, Vital Images, and the Mayo Clinic. Each provided technical support for installation at the ACR. Computerized tomographic colonography examinations were removed and workstations returned after the study interpretations were completed.. Gastroenterology 125:3, 688-695
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Robert Benamouzig, Jacques Deyra, Antoine Martin, Bernard Girard, Eric Jullian, Benoit Piednoir, Daniel Couturier, Thierry Coste, Julian Little, Stanislas Chaussade. (2003) Daily soluble aspirin and prevention of colorectal adenoma recurrence: one-year results of the APACC trial1 1The authors thank the women and men who participated in the study, P. E. Douziech for coordination of treatments, and the hospital pharmacists for preparation of the treatments in the trial centers.. Gastroenterology 125:2, 328-336
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