Original Article
Randomized Comparison of Surveillance Intervals after Colonoscopic Removal of Newly Diagnosed Adenomatous Polyps
N Engl J Med 1993; 328:901-906April 1, 1993
- Abstract
Background
The identification and removal of adenomatous polyps and post-polypectomy surveillance are considered to be important for the control of colorectal cancer. In current practice, the intervals between colonoscopies after polypectomy are variable, often a year long, and not based on data from randomized clinical trials. We sought to determine whether follow-up colonoscopy at three years would detect important colonic lesions as well as follow-up colonoscopy at both one and three years.
Methods
Patients were eligible if they had one or more adenomas, no previous polypectomy, and a complete colonoscopy and if all their polyps had been removed. They were randomly assigned to have follow-up colonoscopy at one and three years or at three years only. The two study end points were the detection of any adenoma, and the detection of adenomas with advanced pathological features (defined as those >1 cm in diameter and those with high-grade dysplasia or invasive cancer).
Results
Of 2632 eligible patients, 1418 were randomly assigned to the two follow-up groups, 699 to the two-examination group and 719 to the one-examination group. The percentage of patients with adenomas in the group examined at one and three years was 41.7 percent, as compared with 32.0 percent in the group examined at three years (P = 0.006). The percentage of patients with adenomas with advanced pathological features was the same in both groups (3.3 percent).
Conclusions
Colonoscopy performed three years after colonoscopic removal of adenomatous polyps detects important colonic lesions as effectively as follow-up colonoscopy after both one and three years. An interval of at least three years is recommended before follow-up examination after colonoscopic removal of newly diagnosed adenomatous polyps. Adoption of this recommendation nationally should reduce the cost of post-polypectomy surveillance and screening.
Media in This Article
Table 1
Reasons for Exclusion from the Study.Table 2
Characteristics of the Patients at Enrollment, According to Follow-up Group.Article Activity
- Article
Adenomatous polyps have been identified with increasing frequency in recent years as a result of the introduction of screening with tests of stool for occult blood and flexible-instrument sigmoidoscopy and wider use of colonoscopy, colonoscopic polypectomy, and double-contrast barium enemas. It is widely held that adenomatous polyps are precursors of colorectal cancer and that their removal is important because of its potential for reducing the incidence and mortality of colorectal cancer1-5. These concepts have formed the basis for the removal of adenomatous polyps on detection and for the implementation of follow-up surveillance programs6-10. Periodic surveillance examinations have been considered necessary because of the high frequency of adenomatous polyps detected at follow-up. The clinical relevance of most adenomas found at follow-up, however, has not been established. In current practice, surveillance intervals after polypectomy vary, are often a year long, and have not been based on data from randomized clinical trials.
The National Polyp Study was organized in 1978 by a joint research committee of the American Gastroenterological Association, the American Society for Gastrointestinal Endoscopy, and the American College of Gastroenterology to assess post-polypectomy surveillance11. The study was designed to be a multicenter, randomized clinical trial with wide geographic representation, enrolling only patients with newly diagnosed adenomas in whom all examinations were performed by the investigators and incorporating a prospective, independent pathological review11. The principal goal of this trial was to address the hypothesis that after newly diagnosed adenomatous polyps are excised by colonoscopy, follow-up colonoscopy at three years will detect important colonic lesions as effectively as follow-up colonoscopy at both one and three years. The results of this trial should be relevant to the cost effectiveness of both post-polypectomy surveillance and screening programs, since adenomatous polyps are the most frequent neoplasms found by screening.
Methods
Enrollment
All patients referred for initial colonoscopy or polypectomy at seven participating centers who did not have a family or personal history of familial polyposis, inflammatory bowel disease, or a personal history of polypectomy or colorectal cancer were identified prospectively from November 1980 through February 1990. Patients were excluded if colonoscopy revealed colorectal cancer, nonadenomatous polyps, malignant polyps (adenomas with cancer invading beyond the musculari mucosa), a sessile adenoma with a base longer than 3 cm, or the absence of polyps. Patients were eligible if they underwent a complete colonoscopy to the level of the cecum, with removal of all polyps detected, and were found to have one or more adenomas. The study protocol was approved annually by the institutional review board of each participating center. The following information was ascertained for all patients11: reason for referral, age and sex, and the presence or absence of a family history of colorectal cancer, a personal history of other cancers, and polyps in first-degree relatives.
Endoscopy and Pathological Review
All endoscopic examinations were performed by study investigators. Each polyp removed was placed in a bottle, labeled according to the anatomical segment involved (cecum, ascending colon, hepatic flexure, transverse colon, splenic flexure, descending colon, sigmoid, or rectum), and classified as sessile or pedunculated. The size of the polyp before polypectomy was estimated with use of the open biopsy forceps, and the method of removal (i.e., biopsy fulguration or cautery snare) was recorded. Polyps were classified as small ( ≤ 0.5 cm in diameter), medium (0.6 to 1.0 cm), or large (>1.0 cm). Serial sections of each polyp were obtained from the participating institutions and coded consecutively on an individual-case basis for simultaneous examination at a multihead microscope by the three review pathologists according to uniform criteria established at the beginning of the study; a consensus was reached about each polyp without knowledge of the clinical data or the study center from which it came12. The number of sections varied according to the size of the polyp. Additional sections were obtained if high-grade dysplasia or invasive cancer was present. Adenomas were classified as tubular or villous. Villous adenomas were classified according to the proportion of villous component: class A, 1 to 25 percent; class B, 26 to 75 percent; class C, 76 to 99 percent; and class D, 100 percent. This report is based on the classification of the polyps after pathological review. An adenoma was defined as having advanced pathological features if it was large (>1.0 cm) or had high-grade dysplasia or invasive cancer.
Stratification, Randomization, and Follow-up
Eligible patients consenting to enroll in the study were stratified according to the study center, the number of adenomas (single or multiple), and the histologic type of adenoma (tubular or villous). The patients were randomly assigned within the appropriate stratum to have a follow-up examination either one and three years after colonoscopy (the two-examination group) or three years after colonoscopy (the one-examination group). (A follow-up colonoscopy six years after the examination at entry was also offered to both groups.) Blocked randomization within strata was used to ensure balance between the two groups over time. The study coordinator contacted all patients annually to complete an interval-history questionnaire and to schedule colonoscopies.
Statistical Analysis
A total enrollment of 1400 patients was planned, under the assumption that 975 patients would survive and undergo a follow-up colonoscopy within the study period. The study was designed to detect a difference in the percentage of patients who had adenomas with advanced pathological features detected at one year of 3 percent (the two-examination group), in comparison to 7 percent at three years (the one-examination group), with a power of 80 percent and a level of significance of 0.05 (two-sided); the difference between percentages was equivalent to a relative risk of 2.3 or more. The relative risk that any adenomas as well as adenomas with advanced pathological features would be detected at follow-up three years after entry colonoscopy (the one-examination group) as compared with only one year (the two-examination group) was calculated along with a 95 percent confidence interval. Logistic regression was used to assess the odds of detecting adenomas with advanced pathological features at three years as compared with one year, with control for the stratification variables of the histologic type of adenoma, number of adenomas, and study center13. In addition, logistic regression was used to assess independent risk factors for adenomas with advanced pathological features detected at the first follow-up examination and to examine the effects of any interaction between study-group assignment and characteristics at enrollment. The likelihood-ratio test was used to determine whether a variable was an independent risk factor for the detection of adenomas with advanced pathological features.
Similar analyses were performed with respect to adenomas with advanced pathological features detected at the second follow-up examination in the two-examination group as compared with those detected at follow-up in the one-examination group. The percentage of patients who had adenomas with advanced pathological features detected at either follow-up examination in the two-examination group was compared with the percentage with such adenomas in the one-examination group. The Wilcoxon test was used to determine whether the number of adenomas detected at follow-up differed in the two groups14. All P values are two-sided; all analyses were performed with SAS and BMDP software packages15,16.
Results
Enrollment
A total of 9112 patients referred for colonoscopy who had no history of polypectomy, inflammatory bowel disease, familial polyposis, or colorectal cancer were identified at the seven clinical centers. Of 3778 patients in whom polyps were detected, 2632 (69.7 percent) had adenomas and were eligible for randomization; 1418 (53.9 percent) of the patients with adenomas who were eligible consented to participate. Of these patients, 13 percent required more than one colonoscopy to remove all the polyps detected. The reasons for exclusion from the study are shown in Table 1Table 1
Reasons for Exclusion from the Study.. The characteristics of the adenomas in the patients who did not undergo randomization were similar to those of the patients who did. Of the 1418 patients consenting to randomization, 699 were assigned to the two-examination group and 719 to the one-examination group. The characteristics of the two groups were comparable (Table 2Table 2Characteristics of the Patients at Enrollment, According to Follow-up Group.).Overall Findings at First Follow-up Examination
Of the 660 patients in the two-examination group who were in the study for at least one year, 545 (82.6 percent) returned for the first follow-up examination. Of the 547 patients in the one-examination group who were in the study for at least three years, 428 (78.2 percent) returned for their follow-up examination. The characteristics of the patients in both groups who returned for their first follow-up examination were comparable. The median interval between enrollment and the initial follow-up examination was 1.15 years in the two-examination group and 3.15 years in the one-examination group. Follow-up clinical status was determined for 97.2 percent of the patients (1379 of 1418). None had severe complications resulting in serious morbidity or death.
The findings at the first follow-up examination at one year in the two-examination group and at three years in the one-examination group were comparable with respect to the polyps, adenomas, and types of adenomas detected (Table 3Table 3
Findings at Follow-up Colonoscopy after Polypectomy.). The majority of the patients in whom adenomas were detected at the first follow-up examination had small adenomas that were predominantly tubular. Among those with adenomas at the first follow-up, the average number of adenomas detected was 1.5 in the two-examination group and 1.6 in the one-examination group (P = 0.20); their mean size was 0.5 cm in both groups.Adenomas with Advanced Pathological Features at First Follow-up Examination
The two groups were comparable at the first follow-up examination with respect to the number of patients (14) and the percentage of patients who had adenomas with advanced features (two-examination group vs. one-examination group, 2.6 percent vs. 3.3 percent; relative risk, 1.3; 95 percent confidence interval, 0.6 to 2.6). No invasive cancers were detected at the first follow-up examination in the two-examination group, and two (both Dukes' stage A, or T1N0M0) in large adenomas (2.5 cm) were detected in the one-examination group. The results were similar when the stratification variables of study center, number of adenomas at enrollment, and proportion of villous component were taken into account (relative risk, 1.3; 95 percent confidence interval, 0.6 to 2.7).
Risk Factors for Adenomas and Adenomas with Advanced Pathological Features
Age, the number of adenomas, and the size of the largest adenoma at enrollment were shown by multivariate analysis to be independent risk factors for any adenoma detected at the first follow-up examination (Table 4Table 4
Multivariate Analysis of Enrollment Risk Factors for Adenomas at First Follow-up Examination.). However, the only factor found to be significant in the detection of adenomas with advanced pathological features at follow-up was the number of adenomas at enrollment (P<0.001) (Table 5Table 5
Multivariate Analysis of Enrollment Risk Factors for Adenomas with Advanced Pathological Features at First Follow-up Examination.).Second Follow-up Examination
Of the 431 patients in the two-examination group who completed the first follow-up examination and were in the study for at least three years, 338 (78.4 percent) returned for the second examination. The characteristics of the patients who returned for a second colonoscopy were similar to those of the patients who completed the first examination. The median interval between enrollment and the second follow-up examination was 3.18 years. There was a marked reduction in the percentage of patients with adenomas detected (relative risk, 0.7), as well as in the percentage who had adenomas with advanced pathological features (relative risk, 0.3), at the second follow-up examination in the two-examination group, as compared with the follow-up examination at three years in the one-examination group. At the second examination, 73 patients (21.6 percent) were found to have adenomas, and 3 (0.9 percent) had adenomas with advanced pathological features. Among the patients who had adenomas with advanced pathological features, one had an invasive cancer (Dukes' stage B1, or T2N0M0) in a large adenoma (1.5 cm).
Comparison of Two Examinations with One Examination
In the two-examination group 141 patients (41.7 percent) were found to have adenomas at either the first or second follow-up examination. The relative risk that any adenoma would be detected at two examinations as compared with one examination was 1.3 (95 percent confidence interval, 1.1 to 1.6). However, the percentage of adenomas with advanced pathological features detected at two examinations was the same as the percentage detected at one examination (3.3 percent) (Table 6Table 6
Comparison of the Findings at Both Follow-up Examinations in the Two-Examination Group with the Findings in the One-Examination Group.). The average number of follow-up colonoscopies was 2.06 in the two-examination group (both examinations combined) and 1.03 in the one-examination group.Discussion
This study demonstrates that patients who had newly diagnosed adenomas removed by colonoscopy were likely to have additional polyps detected at follow-up examinations. The polyps detected at follow-up in the majority of these patients were adenomas that contrasted with the adenomas found at enrollment in that they were predominantly small and tubular, with low-grade dysplasia. Only a small fraction of patients were found to have adenomas with advanced pathological features on follow-up. The clinical relevance of the interval between examinations can be assessed by comparing the frequency of adenomas with advanced pathological features detected in patients at follow-up colonoscopies. There were no significant overall differences between the pathological characteristics of the adenomas found at the first follow-up examination whether it was performed at three years (one-examination group) or at one year (two-examination group). Furthermore, the proportion of adenomas with advanced pathological features detected in the two-examination group at one year was similar to that detected in the one-examination group at three years. In addition, the percentage of patients who had adenomas with advanced pathological features in the two-examination group at both one and three years was the same as in the one-examination group at three years. Therefore, this study provides evidence supporting the stated hypothesis: after newly diagnosed adenomatous polyps have been removed by colonoscopy, follow-up colonoscopy at three years detects important colonic lesions as effectively as follow-up colonoscopy at both one and three years. On the basis of these findings, an interval of at least three years is recommended before follow-up examination after the removal of newly diagnosed adenomatous polyps.
Studies in the pre-colonoscopy era reported that the percentage of adenomas detected after polypectomy ranged from 20 to 60 percent17,18. Since the introduction of colonoscopy, several studies6-12 have reported percentages in this range. Data from the National Polyp Study on the detection of adenomas at follow-up agreed with these results. However, our study differed from the previous studies in that it enrolled patients at many centers; enrolled them only if they had a newly diagnosed adenoma, which eliminated the effect of variability in the number of previous surveillance colonoscopies; and was a prospective randomized trial. One requirement for enrollment was complete colonoscopy to the level of the cecum, with removal of all identified polyps regardless of size. In addition, all polyps removed in the National Polyp Study were reviewed by an independent pathology committee.
It is not clear which adenomas found at follow-up are true metachronous adenomas and which are missed synchronous adenomas. Although all adenomas that were identified by the study investigators were removed, not all adenomas that are present in the colon are detected at the time of a single colonoscopy. Other studies have estimated that half the adenomas found at follow-up are missed synchronous adenomas and half are metachronous tumors10,20. The value of frequent examinations is questionable, since the missed adenomas are usually small and are mostly unimportant pathologically. The almost complete follow-up of the entire cohort (97.2 percent) was additional assurance that colonic lesions of clinical importance were not missed because of either inadequate colonoscopy or failure of a patient to return for colonoscopy.
In this trial, the presence of multiple adenomas at enrollment was found to be a predictor of adenomas with advanced pathological features at the first follow-up examination. Older age ( ≥ 60 years) and large adenomas (>1.0 cm) were also notable factors but were not significant independent variables according to multivariate analysis. The family histories of probands in the National Polyp Study21 are also being studied as possible risk factors for metachronous adenomas with advanced pathological features. It would be desirable to increase the interval between follow-up examinations in a subgroup of patients who are at low risk for adenomas with advanced pathological features after undergoing polypectomy. A cross-sectional analysis of the study's data22 supports the concept of a long natural history of colorectal cancer evolving through the adenoma stage. In addition, data recently published23 on rigid-instrument sigmoidoscopy in persons at average risk for colorectal cancer suggest that a long interval between examinations may be appropriate. The present study indicates that the first follow-up colonoscopy need not be performed in patients with newly diagnosed adenomas until at least three years after the initial colonoscopy. Perhaps even longer intervals are allowable, particularly if the first follow-up examination is negative or does not reveal adenomas with advanced pathological features.
In this study we have considered adenomas with advanced pathological features to represent an intermediate biologic end point of future colorectal cancer. The validity of this concept has been examined: according to a recently published British study,24 excision of rectosigmoid adenomas of 1 cm or more, without further intervention, was associated with a 3.6-fold increase in the long-term risk of colon cancer in the general population if a single polyp was present, and with a 6.6-fold increase if multiple polyps were present. Spencer et al.25 found a relative risk of colon carcinoma of only 1.2 in a Minnesota cohort that had been treated for polyps measuring less than 1 cm. In a later study from the same center,26 patients with adenomatous polyps measuring more than 1 cm had a significantly increased risk of colon cancer. These results support the view that adenomas with advanced pathological features are valid indicators of the risk of colorectal cancer.
We conclude that the first follow-up colonoscopy can be delayed in most patients with newly diagnosed adenomas until three years after all polyps identified during initial colonoscopy have been removed. Patients with malignant polyps or large sessile adenomas and those in whom all identified polyps have not been removed may require earlier follow-up colonoscopies. Widespread adoption of this recommendation could result in large savings nationally, better use of resources, and fewer complications in patients being followed after polypectomy27.
Supported by a grant (CA-26852) from the National Institutes of Health.
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., R.C.K., M. Shike); Mallory Institute of Pathology, Boston City Hospital, Boston (M.J.O., L.G.); Mount Sinai Hospital, New York (J.D.W.); Veterans Affairs Medical Center, Minneapolis (J.B.); Valley Presbyterian Hospital, Van Nuys, Calif. (M. Schapiro); Milwaukee County Medical Complex, Milwaukee (E.T.S.); Cedars-Sinai Medical Center, Los Angeles (J.P.); and Massachusetts General Hospital, Boston (F.A.).
Address reprint requests to Dr. Winawer at the Gastroenterology and Nutrition Service, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021.
The following are other members of the National Polyp Study Workgroup who participated in this study: Memorial Sloan-Kettering Cancer Center, New York: C.J. Lightdale, H. Gerdes, L. Hornsby-Lewis, M. Edelman, M. Fleisher, B. Diaz, J. Lapidus, B. Flehinger, and R.A. McMahon; Strang Clinic, New York: C. Miller; Mount Sinai Hospital, New York: A. Szporn, N. Harpaz, M. Khilnani, and S. Yessayan; Veterans Affairs Medical Center, Minneapolis: H. Ansel, S. Ewing, and T. Dobson; Milwaukee County Medical Complex, Milwaukee: W. Hogan, J. Helm, R. Komorowski, and E. McLaughlin; St. Luke's Hospital, Racine, Wis.: J. Geenen, R. Venu, G.K. Johnson, and N. DeBoer; Massachusetts General Hospital, Boston: S. Hedberg, P. Shellito, D. Hall, G. Dickersin, and N. Horton; Cedars-Sinai Medical Center, Los Angeles: J. Sherman, J.A. Hamlin, S. Geller, and M. Kojimoto; Valley Presbyterian Hospital, Van Nuys, Calif.: M. Auslander, D. Kasimian, L. Kussin, and C. Scoggins; and Mallory Institute of Pathology, Boston (Pathology Review Center): C. Magrath.
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