Prevention of Colorectal Cancer by Colonoscopic Polypectomy
Sidney J. Winawer, Ann G. Zauber, May Nah Ho, Michael J. O'Brien, Leonard S. Gottlieb, Stephen S. Sternberg, Jerome D. Waye, Melvin Schapiro, John H. Bond, Joel F. Panish, Frederick Ackroyd, Moshe Shike, Robert C. Kurtz, Lynn Hornsby-Lewis, Hans Gerdes, Edward T. Stewart, and The National Polyp Study Workgroup
Background The current practice of removing adenomatous polypsof the colon and rectum is based on the belief that this willprevent colorectal cancer. To address the hypothesis that colonoscopicpolypectomy reduces the incidence of colorectal cancer, we analyzedthe results of the National Polyp Study with reference to otherpublished results.
Methods The study cohort consisted of 1418 patients who hada complete colonoscopy during which one or more adenomas ofthe colon or rectum were removed. The patients subsequentlyunderwent periodic colonoscopy during an average follow-up of5.9 years, and the incidence of colorectal cancer was ascertained.The incidence rate of colorectal cancer was compared with thatin three reference groups, including two cohorts in which colonicpolyps 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 clinicallyfor a total of 8401 person-years, and 80 percent returned forone or more of their scheduled colonoscopies. Five asymptomaticearly-stage colorectal cancers (malignant polyps) were detectedby colonoscopy (three at three years, one at six years, andone at seven years). No symptomatic cancers were detected. Thenumbers of colorectal cancers expected on the basis of the ratesin the three reference groups were 48.3, 43.4, and 20.7, forreductions in the incidence of colorectal cancer of 90, 88,and 76 percent, respectively (P<0.001).
Conclusions Colonoscopic polypectomy resulted in a lower-than-expectedincidence of colorectal cancer. These results support the viewthat colorectal adenomas progress to adenocarcinomas, as wellas the current practice of searching for and removing adenomatouspolyps to prevent colorectal cancer.
The prevalence of adenomatous polyps of the colon and rectumin the United States and other Western countries is high, asis the incidence of colorectal cancer1,2. Many people with polypshave been identified in recent years as a result of screeningwith stool-blood tests and flexible sigmoidoscopy and the frequentuse of colonoscopy3,4,5. It is current practice to remove polypswhen detected, search the colon for additional polyps, and arrangefor long-term follow-up of the subject6. This practice is basedon the concept that adenomatous polyps are the precursor ofcolorectal cancer and that removing them will prevent colorectalcancer7. Proof of this concept would provide evidence that adenomasprogress to adenocarcinomas and support the effectiveness ofthe current practice of identifying and removing adenomatouspolyps. This paper reports the results of the National PolypStudy, which addressed the hypothesis that colonoscopic polypectomyreduces the incidence of colorectal cancer. Previous papershave reported information regarding the organization, design,patient characteristics, follow-up results, and pathologicalfindings of this study8,9,10.
Methods
Patients
All patients referred to the seven participating centers forinitial colonoscopy or polypectomy between November 1980 andFebruary 1990 who did not have a family or personal historyof familial polyposis, inflammatory bowel disease, history ofpolypectomy, or history of colorectal cancer were prospectivelyevaluated for enrollment in the study8,9,10. After colonoscopy,patients were excluded if they had no polyps, nonadenomatouspolyps, malignant polyps, a sessile adenoma larger than 3 cmin diameter, or colorectal cancer. Eligible patients had atleast one histologically documented adenoma of the colon orrectum and had undergone a complete colonoscopy during whichall identified polyps were removed. Consenting patients wererandomly assigned to more frequent (examinations in years 1and 3) or less frequent (examination in year 3) follow-up withcolonoscopy and barium enema. The patients were also offereda follow-up examination at six years. All patients completeda questionnaire, had fecal occult-blood testing, and were contactedannually by telephone by a study coordinator8,10. The patientshad clinical follow-up regardless of where their diagnostictests or treatment was conducted. All endoscopic, pathological,and surgical findings from other institutions were obtainedand reviewed. Data on the patients in both arms of the studywere pooled for the analysis of the incidence of colorectalcancer. Death certificates were obtained for all patients whodied, and patients' records, pathology reports, slides, andx-ray films were reviewed by a mortality review committee. Allpathology slides were reviewed by the pathology review committee.
Reference Groups
Three reference groups were used to determine the expected incidencerates of colorectal cancer in the study cohort.
Reference Group 1
The first reference group was a retrospective cohort of 226patients studied at the Mayo Clinic in Rochester, Minnesota,between 1965 and 1970 who had polyps 1 cm or larger in diameterthat were above the reach of a rigid sigmoidoscope and weredetected by barium enema; these patients had declined surgicalpolypectomy11. Patients presenting with colorectal cancer wereexcluded. The patients were followed for an average of nineyears, and 32 colon cancers were detected. The cumulative incidenceof colon cancer was 4 percent at 5 years and 14 percent at 10years. Of the cancers detected, 21 (66 percent) were detectedat the same site as the index polyp, and 11 (34 percent) wereat sites distant from it.
Reference Group 2
The second reference group was a retrospective cohort of 1618patients who underwent excision of rectal adenomas between 1957and 1980 at St. Mark's Hospital in London12. Patients presentingwith colorectal cancer or given a diagnosis of colorectal cancerwithin two years after the excision of adenomas were excluded.The average age of the patients at the time of diagnosis ofthe adenoma was 58 years; 66 percent were men. The patientswere followed for an average of 14 years, and 35 colon cancerswere detected. The standardized incidence ratio for colon cancerwas 2.1.
Reference Group 3
The Surveillance, Epidemiology, and End Results (SEER) Programof the National Cancer Institute monitors the incidence of colorectalcancer and the mortality rates from this disease in 10 registriesthat represent people at average risk in the general populationin the United States13. The age- and sex-specific rates of colorectalcancer for calendar years 1983 to 1987 were used, since thisperiod represents the midpoint of accrual and follow-up forthe cohort in the National Polyp Study.
Statistical Analysis
The number of person-years at risk was calculated for each patientaccording to age, sex, and the size of the largest adenoma atinitial examination. Person-years at risk were calculated fromthe date of initial colonoscopy to the end of the study in February1990, death, or for those lost to follow-up, the last date onwhich the patient was known to be alive. The numbers of person-yearsat risk were used in conjunction with the rates of colorectalcancer in the reference populations to determine the numberof colorectal cancers expected in the study cohort after adjustmentfor age and sex14.
Since the Mayo Clinic group consisted of a cohort with largepolyps ( 1 cm), the rates of colorectal cancer expected in theNational Polyps Study group could be determined only for patientswith large adenomas. For the Mayo Clinic cohort, the risk ofcolon cancer per year of follow-up was derived from the cumulativeincidence curve for cancer detected at any site within the colonand was converted to an incidence rate. The number of person-yearsat risk for patients in the National Polyp Study who had largeadenomas was multiplied by the colon cancer rate for the MayoClinic cohort to yield the number of colorectal cancers expected.The age and sex distribution of the Mayo Clinic patients withlarge polyps was assumed to be similar to that of the studypatients with large adenomas; no data on age and sex were reported11.The number of cancers expected in patients with large adenomaswas also based on the Mayo Clinic rates of cancer at the indexsite only (66 percent of the cancers detected) and at sitesdistant from the index site (34 percent of the cancers detected).The age- and sex-specific rates for SEER were applied to thenumber of person-years at risk for patients in the NationalPolyp Study who had small or medium-size adenomas in order toobtain the number of colorectal cancers expected in this subgroup.The number of cancers expected in the patients with large adenomasand those with small or medium-size adenomas were totaled toobtain an overall expected number for the comparison with theMayo Clinic values.
To obtain rates expected for the National Polyp Study cohortbased on the values for the St. Mark's group, the standardizedincidence ratio for colon cancer of 2.1 in the latter groupwas multiplied by the age- and sex-specific rates of colorectalcancer for the SEER Program, since the study cohort was an Americanrather than a British population. These rates were applied tothe age- and sex-specific number of person-years in the studycohort to obtain the number of cancers expected on the basisof the St. Mark's data. It was assumed that the age and sexdistribution of the St. Mark's group was similar to that ofthe study cohort. The age- and sex-specific rates for the SEERProgram were multiplied by the age- and sex-specific numberof person-years at risk for the entire National Polyp Studycohort to obtain the number of cases expected on the basis ofgeneral population rates.
Cumulative incidence curves were calculated by the Kaplan-Meiermethod. The observed number of colorectal cancers was assumedto follow a Poisson distribution. A two-sided P value of 0.05or less was considered to indicate statistical significance.The standardized incidence ratio of the number of cases of colorectalcancer observed divided by the number expected and the 95 percentconfidence interval were calculated for each reference group15.The standardized incidence ratio was the number of colorectalcancers occurring in the National Polyp Study expressed as aproportion of the number of cancers that would be expected tooccur if, within each age- and sex-specific group, the ratesin the National Polyp Study cohort were the same as those inthe reference group. The reduction in the incidence of colorectalcancer 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 werefollowed until death, for a total of 8401 person-years at risk(average, 5.9); 39 patients were lost to follow-up during thestudy. Eighty percent returned for one or more of their scheduledcolonoscopies10. At the time of enrollment, 494 patients (35percent) had adenomas larger than 1 cm in diameter and 137 patients(10 percent) had adenomas with high-grade dysplasia10. A totalof 1310 patients (92 percent) had been referred for colonoscopybecause of symptoms or positive results on screening or a diagnostictest8. Results of the genetic epidemiology study16 of this cohortindicated that 1 percent of the patients had three or more first-degreerelatives with colorectal cancer, but none of the families satisfiedthe Amsterdam criteria for hereditary nonpolyposis colorectalcancer17.
Five asymptomatic colorectal cancers (malignant polyps) weredetected at follow-up colonoscopy in five patients, none ofwhom had rectal bleeding or a change in bowel habits (Table 1).No patient had a symptomatic cancer or died of colorectalcancer. The cumulative incidence of colorectal cancer -- bothexpected and observed -- in the study cohort, based on the ratesin the three reference groups, is shown in Figure 1. The expectednumber of colorectal cancers in the study cohort, based on theMayo Clinic, St. Mark's, and SEER rates, and the level of statisticalsignificance are shown in Table 2. In each case, the observedincidence of colorectal cancer in the study cohort was significantlylower (P<0.001) than the expected incidence. The standardizedincidence ratio was 0.10 (95 percent confidence interval, 0.03to 0.24) for the Mayo Clinic group, 0.12 (95 percent confidenceinterval, 0.04 to 0.27) for the St. Mark's group, and 0.24 (95percent confidence interval, 0.08 to 0.56) for the SEER group.The observed incidence of colorectal cancer per 1000 person-yearswas 0.6 in the study cohort, whereas the expected incidencewas 5.8 according to the Mayo Clinic data, 5.2 according tothe St. Mark's data, and 2.5 according to the SEER data.
Figure 1. Cumulative Incidence of Colorectal Cancer in the National Polyp Study Cohort.
The observed incidence is compared with the expected incidence based on data from the three reference groups: the Mayo Clinic cohort (United States), the St. Mark's cohort (United Kingdom), and the SEER Program (United States)11,12,13.
Table 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.
Additional comparisons were based on the Mayo Clinic referencegroup. The observed and expected numbers of colorectal cancersin the subgroup of patients in the National Polyp Study whohad large adenomas at enrollment were 3 and 40.2, respectively,for a standardized incidence ratio of 0.07 (95 percent confidenceinterval, 0.02 to 0.22). For those in the subgroup with smallor medium-size adenomas at enrollment, 2 cancers were observedand 8.1 were expected (standardized incidence ratio, 0.25; 95percent confidence interval, 0.03 to 0.89). Thus, the incidenceof colorectal cancer was lower than expected in patients withlarge as well as small or medium-size adenomas at enrollment.Even if the SEER rates were used for patients with large adenomasat enrollment, the incidence was lower than expected (standardizedincidence ratio, 0.24; 95 percent confidence interval, 0.05to 0.70). According to the Mayo Clinic data, 34.6 cancers wereexpected at the index site (standardized incidence ratio, 0.14;95 percent confidence interval, 0.05 to 0.33) and 21.8 wereexpected 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 numberof person-years patients were at risk during the first two yearsof follow-up. The expected number of colorectal cancers basedon the reduced number of person-years at risk was 36.3 (standardizedincidence ratio, 0.14; 95 percent confidence interval, 0.04to 0.32) for the Mayo Clinic reference group, 30.5 (standardizedincidence ratio, 0.16; 95 percent confidence interval, 0.05to 0.38) for the St. Mark's reference group, and 14.5 (standardizedincidence ratio, 0.34; 95 percent confidence interval, 0.11to 0.81) for the SEER reference group. Consequently, the incidenceof colorectal cancer was at least 66 percent lower than expected,even after the exclusion of the number of person-years patientswere at risk during the first two years after the initial colonoscopy.
Discussion
These results suggest that colorectal cancer can be preventedby colonoscopic removal of all identified adenomatous polyps,a finding that supports the concept of the progression of adenomato adenocarcinoma and the current practice of colonoscopic polypectomy.Ideally, proof of the hypothesis that polypectomy reduces theincidence of colorectal cancer should be based on a randomizedclinical trial in which the incidence during follow-up was determinedin a control group of patients who had adenomatous polyps documentedhistologically but left in situ and compared with the incidencein a group of patients whose adenomatous polyps were removed.Such a design is neither ethical nor feasible. Therefore, weselected an alternative method, conducting an observationalstudy in which reference groups were used to determine the numberof colorectal cancers expected in the patients enrolled in theNational Polyp Study. The number of colorectal cancers observedwas then compared with the number expected.
The three reference groups provided a range of expected ratesconsistent with the rates of colorectal cancer in a cohort withadenomas for the period 1980 through 1990. The Mayo Clinic datawere derived from a retrospective cohort study of patients withpolyps measuring 1 cm or more in diameter that were detectedby a barium enema; the patients declined to undergo surgeryand were followed for an average of nine years11. The remainderof the colon was evaluated only by barium enema; this probablyaccounted for the appearance of cancer not only at the siteof the identified polyps, but also at distant sites. We usedthe total number of colon cancers detected in the Mayo Clinicreference group regardless of their anatomical location. Theincidence of colorectal cancer in the National Polyp Study cohortwas significantly lower (90 percent) than expected on the basisof the rate in the Mayo Clinic group.
The St. Mark's data were also derived from a retrospective cohortstudy12. This cohort consisted of patients who had a rectosigmoidadenomatous polyp removed. It is reasonable to assume that approximately50 percent of the cohort had additional (synchronous) adenomatouspolyps above the rectosigmoid colon and would therefore havebeen expected to have additional (metachronous) adenomas2,3,6.The incidence of colorectal cancer in the National Polyp Studycohort was significantly lower (88 percent) than expected onthe basis of the rate in the St. Mark's cohort.
The rate of colorectal cancer in the population covered by theSEER data would be expected to be lower than that in eitherof the other two reference groups, since the population consistsof average-risk people rather than patients with adenomas13.A proportion of the general population harbor adenomas, butthese are mostly less than 1 cm in diameter, usually with themost benign histologic characteristic (tubular adenoma), andare not associated with an increased risk of colorectal cancer1,12,18,19.A comparison of the actual incidence of colorectal cancer inthe National Polyp Study cohort with that expected on the basisof SEER rates is the most rigorous test of the hypothesis thatcolonoscopic polypectomy reduces the incidence of colorectalcancer. The incidence in the study cohort was significantlylower (76 percent) than expected on the basis of the rate inthe SEER group. This is the result of clearing the entire colonof all identified polyps by colonoscopy10.
A retrospective analysis of a cohort of patients undergoingcolonoscopy between 1974 and 1985 suggested that polypectomyreduced the incidence of colorectal cancer20. In another retrospectivestudy, the rate of death from colorectal cancer was higher inpatients with adenomatous polyps who did not have polypectomythan in the general population21. Although the removal of polypsby rigid sigmoidoscopy resulted in a lower-than-expected incidenceof rectosigmoid cancer,22 the histologic characteristics ofthe polyps removed and the completeness of the follow-up werenot reported. A reduction in mortality from distal-colon cancerin two case-control studies of sigmoidoscopy could possiblybe 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 rectalpolyps removed and a significant increase in rectal cancer inwomen that was attributed to the incomplete removal of rectalpolyps12.
Were the five cancers found in this study new lesions or lesionsmissed during a previous examination? The characteristics ofthe polyps removed at enrollment have been described previously9,10.The two cancers (malignant polyps) measuring less than 1 cmin diameter that were detected at six and seven years may havebeen new growths, but it is less clear whether the three largercancers (malignant polyps) detected at three years were newor were missed at the time of the initial colonoscopy.
Was the lower-than-expected incidence of colorectal cancer inthe study cohort related to the exclusion of patients with colorectalcancer at enrollment? We think not. Patients with colorectalcancer were also excluded from the St. Mark's and Mayo Clinicreference groups, as were patients in whom colorectal cancerdeveloped during the first two years of follow-up in the St.Mark's group, but colonoscopy was not done at base line to excludecolonic polyps in either group. In addition, the incidence ofcolorectal cancer was 77 percent lower than the incidence expectedon the basis of the rate of cancer at sites distant from theindex polyp in the Mayo Clinic group. The results were similareven after the exclusion of the number of person-years patientswere at risk during the first two years after colonoscopy.
We conclude that the incidence of colorectal cancer is reducedby colonoscopic polypectomy. These results provide evidenceof the progression of adenoma to adenocarcinoma and of the effectivenessof the current practice of searching for and removing adenomatouspolyps in the colon.
Supported by a grant (CA 26852) from the National Institutesof Health and sponsored by the American GastroenterologicalAssociation, 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.).
Other members of the National Polyp Study Workgroup are listed in the Appendix.
Address reprint requests to Dr. Winawer at the Gastroenterology and Nutrition Service, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
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Appendix
The following members of the National Polyp Study Workgroupalso 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; VanNuys, Calif. -- M. Auslander, D. Kasimian, L. Kussin, and C.Scoggins; and Boston (Pathology Review Center) -- C. Magrath.
Screening for Colorectal Cancer
Dubois G., The French Working Group on Colorectal Cancer Screening , Redelmeier D. A., Toribara N. W., Sleisenger M. H.
Extract |
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N Engl J Med 1995;
333:460-461, Aug 17, 1995.
Correspondence
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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. 
