Original Article
Long-Term Risk of Colorectal Cancer after Excision of Rectosigmoid Adenomas
N Engl J Med 1992; 326:658-662March 5, 1992
- Abstract
- Abstract
Background and Methods
Surveillance by repeated colonoscopy is currently recommended for patients with colorectal adenomas. We assessed the long-term risk of colorectal cancer after rigid-instrument sigmoidoscopy and polypectomy in 1618 patients with rectosigmoid adenomas (tumors of the rectum or distal sigmoid colon) who did not undergo surveillance. A total of 22,462 person-years of observation were accrued (mean, 14 years per patient).
Results
The incidence of subsequent rectal cancer in these patients was similar to that in the general population (standardized incidence ratio, 1.2; 95 percent confidence interval, 0.7 to 2.1). Most rectal cancers developed in patients whose adenomas had been inadequately removed; the risk was very low after complete removal.
The risk of subsequent colon cancer depended on the histologic type, size, and number of adenomas in the rectosigmoid. Among 842 patients with a rectosigmoid adenoma that was tubulovillous, villous, or large (≥1 cm), colon cancer developed in 31 patients. The standardized incidence ratio was 3.6 overall (95 percent confidence interval, 2.4 to 5.0) and 6.6 (95 percent confidence interval, 3.3 to 11.8) if there were multiple rectosigmoid adenomas. Among the remaining 776 patients with only small, tubular adenomas (whether single or multiple), colon cancer developed in only 4 patients. The standardized incidence ratio in this group was 0.5 (95 percent confidence interval, 0.1 to 1.3).
Conclusions
Follow-up colonoscopic examinations may be warranted in patients with tubulovillous, villous, or large adenomas in the rectosigmoid, particularly if the adenomas are also multiple. In patients with only a single, small tubular adenoma that is only mildly or moderately dysplastic (43 percent of our series), however, surveillance may not be of value because the risk of cancer is so low. (N Engl J Med 1992;326:658–62.)
Media in This Article
Table 1
Characteristics of the Rectosigmoid Adenomas of the Study Cohort at Entry, According to Sex.*Table 2
Relative Risk of Rectal and Colon Cancer According to Sex.*Article Activity
- Article
THERE is controversy about the correct care for patients after the removal of adenomas found at sigmoidoscopy, particularly the need for regular follow-up colonoscopic examinations.1 , 2 Some specialists recommend that colonoscopy be performed every three to five years.3 Others argue that colonoscopy is a time-consuming and expensive procedure with some risk,4 , 5 which should be reserved for patients with an increased risk of colorectal cancer.
The aim of the present study was to determine which subgroups of patients with rectosigmoid adenomas are at an increased risk of colorectal cancer after polypectomy, in order to provide a rational basis for their follow-up. Consequently, we examined the subsequent development of colorectal cancer in a cohort of 1618 patients in whom adenomas had been excised from the rectosigmoid, at a time when surveillance after polypectomy was not routinely practiced.
Methods
Patients
From 1957 to 1980, 2169 patients (1419 men and 750 women) referred with symptoms of a colorectal disorder (mostly rectal bleeding) underwent excision of one or more colorectal adenomas at St. Mark's Hospital, London. We studied the subsequent risk of cancer in the subgroup of these patients who did not have a history of colorectal cancer and whose adenomas had been excised from the rectum, distal sigmoid colon, or both (rectosigmoid) by means of a 25-cm rigid sigmoidoscope. Patients who had undergone colonoscopy (244 patients) or surgical excision of colonic adenomas (64 patients) were excluded.
Adenomas and other cancers detected within two years of the initial examination were considered to have been present at entry. Therefore, patients with cancer diagnosed at entry (22 patients) or within two years (3 patients) and those with less than two years of follow-up (203 patients) were excluded from the analysis. Of the patients followed for less than two years, 103 died of a cause unrelated to their adenoma, and 100 were lost to follow-up. Ten patients more than 85 years old at the time of the first examination and five patients with inflammatory bowel disease were also excluded from the study.
The study population consisted of the remaining 1618 patients (1061 men and 557 women) who had had adenomas removed from the rectosigmoid only and who were followed for at least two years. None had a colonoscopic examination within two years of entry into the study. Their ages at entry ranged from 21 to 85 years (mean, 58).
Adenomas
The number, size, and location of the adenomas were determined from the patients' hospital records. The size was confirmed by measuring the maximal diameter of the fixed specimen and was categorized as less than 1 cm, 1 to 2 cm, or more than 2 cm. The tumor was classified on the basis of histologic features, according to the criteria of the World Health Organization,6 as tubular, tubulovillous, or villous. Dysplasia was graded as mild, moderate, or severe.7 To avoid interobserver variation, slides of every polyp were reexamined by a single observer. All adenomas detected within two years of presentation were assumed to have been present at the initial examination and were counted as lesions present at entry, although 97 percent of adenomas were detected at the first visit. Patients with multiple adenomas were categorized according to the largest tumor diameter, the most villous histology, and the most severe grade of dysplasia.
Follow-up
Most patients had no special follow-up for their adenomas, and most were discharged after they had been treated for the condition for which they had been referred. All follow-up in this study was passive. The status of the patients at the end of the study was determined from the National Health Service Central Register, which provided copies of death certificates and registrations of cases of cancer. Follow-up was terminated at one of the following end points: the development of colorectal cancer, death, colonoscopy, the patient's 86th birthday, or May 1988.
Because of local referral practices, almost all the patients returned to St. Mark's Hospital if colorectal symptoms recurred. The results of all clinical examinations after entry were recorded. Most examinations were undertaken to assess recurring symptoms. Routine colonoscopic surveillance for colorectal adenomas was introduced at the hospital in 1980, when recruitment for this study was terminated.
Statistical Analysis
The observed numbers of cases of colon cancer and rectal cancer were compared with the expected numbers for these sites on the basis of age, sex, and calendar-year—specific rates for the South Thames Health Region, London, with use of the program MAN-YEARS.8 The expected numbers were based on cases during a risk period beginning two years after the initial sigmoidoscopic examination, and the ratio of observed to expected cases was reported as a standardized incidence ratio. Tests for significance and exact 95 percent confidence intervals for standardized incidence ratios were calculated under the assumption that the observed number of cases would follow a Poisson distribution.9
For univariate comparisons of standardized incidence ratios, a global chi-square test was used to test for heterogeneity, and a modification of Armitage's test9 , 10 was used to test for trend. For multivariate comparisons, the Cox proportional-hazards model11 was used, with a forward stepwise-regression procedure (with the statistical package BMDP). The assumption about proportionality was checked for the final model. Tests for significance were based on changes in the log (partial) likelihood.
A case–control study was incorporated to investigate the differences between men and women in the risk of rectal cancer. Controls for the patients with rectal cancer were selected from the remainder of the cohort, with matching for the year of entry (±5 years), age at entry (±5 years), the number of years at risk, and the number, size, histology, and grade of dysplasia of the removed adenomas. Controls and case patients were not matched for sex. The morphology of the adenomas (sessile or pedunculated), the method and completeness of excision, and the length of clinical follow-up after excision were determined from the patients' hospital records.
Results
In both the men and the women, 86 percent of the rectosigmoid adenomas were single (Table 1Table 1
Characteristics of the Rectosigmoid Adenomas of the Study Cohort at Entry, According to Sex.*). The women had adenomas that were 1 cm in diameter or larger, were tubulovillous or villous, or had moderate or severe dysplasia more often than the men. The proportion of tumors that were large, were villous, or had severe dysplasia increased significantly with age in both men and women, but the differences between the sexes persisted after adjustment for age.The total period of follow-up after entry was 22,462 person-years, an average of 13.8 years per patient; 1448 patients were followed for at least 5 years, 1052 for at least 10 years, 686 for at least 15 years, and 334 for at least 20 years. The average follow-up periods of men and women were similar.
Adenocarcinomas of the large bowel developed in 49 patients (3 percent) a mean of 13 years after entry; 14 patients had rectal cancers, and 35 had colon cancers. The sites of the colon cancers were distributed as follows: sigmoid colon, 8 patients; descending colon, 3; transverse colon, 5; hepatic flexure, 1; ascending colon, 1; cecum, 6; and site not specified, 11. Seven hundred three patients (43 percent) died of a cause other than rectal or colon cancer, 35 (2 percent) were lost to follow-up, 15 (1 percent) emigrated, and 192 (12 percent) had a colonoscopic examination (26 for Symptoms and 166 for routine surveillance) an average of eight years after entry; data on these 192 patients were censored at that point.
Subsequent clinical examinations other than colonoscopy were undertaken in 697 patients (43 percent); rigid-instrument sigmoidoscopy was performed in 509 patients (31 percent), and barium enemas were administered in 188 (12 percent). As a result of these examinations, 49 adenomas were removed, 21 from the rectum and 28 from the colon. Of these, 7 adenomas in the rectum and 11 in the colon were larger than 1 cm in diameter.
Subsequent Rectal Cancer
Overall, the risk of rectal cancer among the patients was similar to that in the general population (Table 2Table 2
Relative Risk of Rectal and Colon Cancer According to Sex.*), but the risk among the women was 10 times that among the men (P<0.0001). In univariate analyses, the risk was not influenced by the number of adenomas present (Table 3Table 3
Relative Risk of Rectal and Colon Cancer According to Characteristics of the Excised Adenomas.*), but it increased significantly with an increase in the tumor size, the degree of villous histology, and the severity of dysplasia.A multivariate model was used to group the patients with rectal cancer according to risk: the low-risk group comprised patients with only small (<1 cm), mildly or moderately dysplastic, tubular adenomas, and the high-risk group comprised the remaining patients. All 3 of the men and 9 of the 11 women who subsequently had rectal cancer were in the high-risk group, but only among the women was the observed number of cases significantly higher than expected (Table 4Table 4
Relative Risk of Rectal Cancer According to Sex and Risk Group.). The increased risk was confined to women treated before 1965 (8 cases observed vs. 1.3 expected). These findings prompted a more thorough examination of the adenomas in the patients with rectal cancer, by means of a case–control study.In the case–control study in which we investigated the differences between men and women in the rate of rectal cancer, 74 control patients (43 men and 31 women) met the criteria for matching. Eleven of the 14 case patients had sessile, inadequately excised adenomas, with minimal follow-up to detect local recurrence. In six case patients (three men and three women) the index adenomas were examined by biopsy but not excised, and in five other case patients large (≥1 cm), sessile adenomas were treated by fulguration that did not ensure complete excision. The other three case patients, all women, had had pedunculated adenomas that were completely removed 17 or 18 years earlier. By comparison, most of the control patients (77 percent) had had pedunculated adenomas. Of the 17 controls (7 men and 10 women) with sessile adenomas, 3 were treated by complete excision and a further 12 had repeated rectal examinations for up to 30 years; 7 of these 12 controls were treated for a recurrence. Thus, it would appear that the incidence of subsequent rectal cancer was strongly associated with a history of incompletely excised sessile adenomas, and these were more common in the women.
Subsequent Colon Cancer
Unlike the standardized incidence ratios for the men and women with rectal cancer, those for the men and women with colon cancer did not differ significantly (P>0.1); the ratio was approximately 2 for either sex (Table 2). Risk among patients with colon cancer increased significantly with age (P<0.001, data not shown), but at a rate similar to that in the general population, so that the standardized incidence ratios were not influenced by age.
In univariate analyses, the risk of colon cancer was related to the size and degree of villous histology of the adenomas, and to a lesser extent to the number of tumors and the severity of dysplasia (Table 3).
In a multivariate model, both tumor histology (odds ratio for tubulovillous or villous, 4.1; P<0.0001 ) and size (odds ratio for ≥1 cm, 2.4; P<0.001) were important predictors (after adjustment for age and sex). However, since size correlated strongly with histology, size offered no additional predictive information after histology was included in the model. The addition of the number of tumors (i.e., single vs. multiple [≥2]) increased the predictive power of the model only slightly (odds ratio, 2.2; P = 0.04). As a result of this analysis, two risk groups for colon cancer were identified on the basis of the features of the rectosigmoid adenomas. The low-risk group consisted of patients with small (<1 cm), tubular tumors, and the high-risk group consisted of patients with tubulovillous, villous, or large (≥1 cm) tumors.
Of the 776 patients with small (<1 cm), tubular adenomas (single or multiple), only 4 subsequently had colon cancer—half the expected number (standardized incidence ratio, 0.5; 95 percent confidence interval, 0.1 to 1.3) (Table 5Table 5
Relative Risk of Colon Cancer According to Risk Group and Number of Adenomas (Single vs. Multiple).). Of the remaining 842 patients with large (≥1 cm), tubulovillous, or villous adenomas (single or multiple), 31 subsequently had colon cancer; thus, the standardized incidence ratio was 3.6 (95 percent confidence interval, 2.4 to 5.0).Among the 64 patients at low risk who had multiple small, tubular adenomas of the rectosigmoid, there were no cases of colon cancer. However, in the high-risk group, the presence of multiple adenomas was associated with a particularly high risk (standardized incidence ratio, 6.6); colon cancer developed in 7 percent of this group.
Of the 35 colon cancers, 16 occurred at sites between the descending colon and cecum. Of these, 14 developed in patients at high risk for colon cancer, and only 2 developed in patients at low risk (standardized incidence ratios, 3.7 and 0.6, respectively). Thus, the presence of large, tubulovillous, or villous adenomas in the rectosigmoid appeared to be predictive of cancer at remote proximal sites in the colon.
Adenomas Detected by Colonoscopy during Follow-up
Of the 192 patients who underwent colonoscopy during follow-up, 89 had a small, tubular adenoma in the rectosigmoid at entry and 103 had an adenoma that was large, tubulovillous, or villous. The mean interval between entry and the first colonoscopic examination was similar in the two groups (seven and eight years, respectively).
The proportion of patients in the high-risk and low-risk groups in whom at least one adenoma was detected at the first follow-up colonoscopic examination was similar (35 percent vs. 46 percent, respectively; P>0.1). However, the patients in the high-risk group were much more likely than those in the low-risk group to have a large (≥1 cm), tubulovillous or villous, or severely dysplastic adenoma (20 percent vs. 8 percent; P = 0.01).
Patients at Low Risk for Colorectal Cancer
Patients who had had only a single small, tubular, mildly or moderately dysplastic adenoma excised from the rectosigmoid were at low risk for both rectal and colon cancer. Of the 697 patients in the cohort (43 percent) who had adenomas with these characteristics, only 1 had rectal cancer and 4 had colon cancer (standardized incidence ratio for colorectal cancer, 0.4; 95 percent confidence interval, 0.1 to 1.0).
Discussion
We quantified the long-term risk of rectal and colon cancer in a large cohort of patients who had histologically confirmed adenomas removed from the rectosigmoid. The patients have been followed for up to 30 years; 52 percent have either died or reached the upper age limit for our study, 86 years.
The comparability of this cohort with the general population might be questioned, since all patients were referred because they had colorectal symptoms. However, their overall mortality rate was similar to that of the general population. Moreover, the prevalence of rectosigmoid adenomas (2 percent) in the population from which this series of patients was drawn was similar to that in other series of subjects examined by rigid-instrument sigmoidoscopy.12 13 14 15
We found, as have others,16 17 18 19 that the risk of subsequent rectal cancer after the removal of rectal adenomas was no higher than that in the general population. However, it is possible that after complete excision the risk may actually be lower than in the general population, since most of the cases of rectal cancer occurred among the patients found to have inadequately excised adenomas at entry. The risk of cancer in the form of new adenomas in the rectum appeared to be low. Although 697 patients (43 percent) had subsequent sigmoidoscopic examinations, only 28 rectal adenomas were detected. Thus, it may be concluded that if all adenomas in the rectosigmoid are excised and if follow-up is instituted for adenomas that may not have been completely excised, then the risk of subsequent rectal cancer will remain low for many years after excision.
By contrast, we found the risk of colon cancer in our cohort to be double that in the general population and to be similar in men and women. An approximate doubling of the risk of colon cancer in patients with rectosigmoid polyps detected during rigid-instrument sigmoidoscopy has also been observed in other series.17 18 19 20 The increased risk of colon cancer was confined to patients with large (≥1 cm), tubulovillous, or villous adenomas; patients with only one or more small (<1 cm), tubular adenomas had no increase in risk.
Histologic status appears to be the most important risk factor for colon cancer in this and other studies.20 21 22 23 Because of sampling error, the frequency of detection of focal villous changes is often underestimated.19 , 24 Therefore, it is important also to consider the size of the adenoma. Size is not a sufficiently predictive risk factor,19 however, since a proportion of small adenomas (18 percent in our series) are tubulovillous or villous.
The number of adenomas detected in the rectosigmoid did not influence the classification of patients into groups at low risk and high risk for colon cancer. Patients with small, tubular adenomas were at low risk whether or not they had multiple adenomas, whereas patients with large, tubulovillous, or villous adenomas were at high risk even if they had only a single adenoma. If, however, patients in the high-risk group had multiple adenomas, the risk was particularly high; 7 percent of such patients subsequently had colon cancer.
In our study, approximately 40 percent of patients in both colon-cancer risk groups who underwent colonoscopy during follow-up had adenomas in the colon. However, the adenomas in the low-risk group were mainly small, tubular, and only mildly or moderately dysplastic. Other investigators have made a similar observation.1 , 25 This finding, together with the observation that the risk of colon cancer was low in the low-risk group, suggests that total colonoscopy on a periodic basis may not be of value in these patients.
The results of this study suggest that almost half of patients with rectosigmoid adenomas detected at sigmoidoscopy have only a single small, tubular, mildly or moderately dysplastic adenoma and that they are at no higher risk for colorectal cancer than the rest of the population. A recent cost-effectiveness analysis5 suggests that the costs of regular colonoscopic surveillance in patients at low risk may outweigh the benefits. The patients with other types of tumors are a heterogeneous group, some of whom are at particularly increased risk.
We are indebted to the late Dr. H.J.R. Bussey for the use of his comprehensive records, which allowed the identification of all the patients in the cohort; to Ms. Taahra Ghaazi, Mr. Claude Slatner, Mr. Michael Lai, Mrs. Suzanne Gardiner, and the staffs of the National Health Services Central Register and the medical-records department at St. Mark's Hospital for their help in tracing the patients; to Dr. Robert Edwards for computing and programming assistance; and to Dr. Christopher Williams, Mr. John Northover, and Mr. Paul Boulos for clinical advice.
Source Information
From the Department of Mathematics, Statistics and Epidemiology, Imperial Cancer Research Fund, London (W.S.A., J.C.), and the Department of Pathology, St. Mark's Hospital, London (B.C.M.). Address reprint requests to Dr. Cuzick at the Department of Mathematics, Statistics and Epidemiology, Imperial Cancer Research Fund, P.O. Box 123, Lincoln's Inn Fields, London, WC2A 3PX, United Kingdom.
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