Original Article
Ulcerative Colitis and Colorectal Cancer — A Population-Based Study
N Engl J Med 1990; 323:1228-1233November 1, 1990
- Abstract
- Abstract
Background.
The risk of colorectal cancer is increased among patients with ulcerative colitis. The magnitude of this increase in risk and the effects of the length of follow-up, the extent of disease at diagnosis, and age at diagnosis vary substantially in different studies.
Methods.
To provide accurate estimates of the risk of colorectal cancer among patients with ulcerative colitis, we studied a population-based cohort of 3117 patients given a diagnosis of ulcerative colitis from 1922 through 1983 who were followed up through 1984.
Results.
Ninety-two cases of colorectal cancer occurred in 91 patients. As compared with the expected incidence, the incidence of colorectal cancer in the cohort was increased (standardized incidence ratio [ratio of observed to expected cases] = 5.7; 95 percent confidence interval, 4.6 to 7.0). Less extensive disease at diagnosis was associated with a lower risk; for patients with ulcerative proctitis, the standardized incidence ratio was 1.7 (95 percent confidence interval, 0.8 to 3.2); for those with left-sided colitis, 2.8 (95 percent confidence interval, 1.6 to 4.4); and for those with pancolitis (extensive colitis, or inflammation of the entire colon), 14.8 (95 percent confidence interval, 11.4 to 18.9). Age at diagnosis and the extent of disease at diagnosis were strong and independent risk factors for colorectal cancer. For each increase in age group at diagnosis (<15 years, 15 to 29 years, 30 to 39 years, 40 to 49 years, 50 to 59 years, and ≥60 years), the relative risk of colorectal cancer, adjusted for the extent of disease at diagnosis, decreased by about half (adjusted standardized incidence ratio = 0.51; 95 percent confidence interval, 0.46 to 0.56). The absolute risk of colorectal cancer 35 years after diagnosis was 30 percent for patients with pancolitis at diagnosis and 40 percent for those given this diagnosis at less than 15 years of age.
Conclusions.
Close surveillance and perhaps even prophylactic proctocolectomy should be recommended for patients given a diagnosis of pancolitis, especially those who are less than 15 years of age at diagnosis. (N Engl J Med 1990; 323:1228–33.)
Media in This Article
Figure 1
Cumulative Incidence of Colorectal Cancer for Patients with Pancolitis, According to Age at Diagnosis.Table 1
Time of Diagnosis, Age at Diagnosis, and Extent of Disease at Diagnosis among Patients in the Study Cohort.Article Activity
- Article
SINCE the association between ulcerative colitis and colorectal cancer was first reported in the 1920s,1 it has been confirmed in many studies from different countries,2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 and the causality of the association is now generally accepted.17 The quantitative estimates of this risk, however, have varied widely among different studies. This variation probably results from the smallness of the samples and the questionable validity of results from studies of selected patient groups at referral centers. The possible effects of the length of follow-up, the extent of disease at diagnosis, and age at diagnosis have also remained unclear. Larger, population-based studies have therefore been asked for repeatedly.18 19 20
To provide more accurate estimates of risk, we investigated a population-based cohort made up of all 3117 patients who received a diagnosis of ulcerative colitis from 1922 through 1983 in one geographic area in Sweden. We gathered information on the extent of disease at diagnosis, age at diagnosis, and surgical procedures (such as proctocolectomy) carried out during the follow-up period. Follow-up was virtually complete through 1984, and observation time ranged from 1 to 60 years after diagnosis.
Methods
Patients
Six counties in central Sweden (the Uppsala Health Care Region), with 1.2 million inhabitants in 1965 and 1.3 million in 1983, were included in the study. From 1965 through 1983, the National Board of Health and Welfare collected information about residents in the region who were hospitalized.21 The information in this inpatient registry included the dates of admission and discharge, diagnosis, nature of surgical procedures, and dates of surgical procedures.
From the inpatient registry we selected diagnoses that might include cases of ulcerative colitis, using codes (572.00, 572.09, 572.11, 572.20, and 572.21) from the Swedish adaptation of the International Classification of Diseases, seventh edition (ICD-7), for the period from 1965 through 1968 and codes (561.04, 562.10, 563.00, 563.10, 563.99, 564.10, and 569.02) from the eighth edition (ICD-8) for the period from 1969 through 1983. To identify all patients with a diagnosis of ulcerative colitis, whether they were treated as outpatients or inpatients, we also reviewed the records at all the departments of clinical pathology in the region. Any patient in whom a histopathological examination suggested ulcerative colitis was identified. All patient charts were reviewed to confirm or reject the diagnosis of ulcerative colitis, for which we used the diagnostic criteria described by Garland et al.22
We identified 2509 patients in whom ulcerative colitis was diagnosed for the first time from 1965 through 1983 and who lived in the region ("incident cases"). Using the same criteria and case-finding methods, we were also able to identify 613 patients in whom ulcerative colitis was diagnosed before 1965 within the region (the earliest case was diagnosed in 1922) who were living there on January 1, 1965 ("prevalent cases"). None of these 613 patients were identified by us as a result of being given a diagnosis of colorectal cancer, but all had had at least one consultation or a period of inpatient care for ulcerative colitis after December 31, 1964. Five patients were excluded — one for whom data were inadequate and four in whom colorectal cancer was diagnosed before the diagnosis of ulcerative colitis — leaving a total of 3117 patients (1750 men and 1367 women) available for follow-up.
The patients were classified in three different groups according to the extent of their disease at diagnosis: those with proctitis and no involvement proximal to the rectosigmoid junction; those with left-sided colitis and no involvement proximal to the hepatic flexure; and those with pancolitis and involvement proximal to the hepatic flexure. To ensure a consistent estimate of the extent of disease at the time of diagnosis, we used the results of a barium-enema test. Since the introduction of colonoscopy at the end of the 1970s, the results of this investigation have been used in the absence of a barium-enema roentgenogram. Among patients given a diagnosis before 1965, the proportion with proctitis was smaller than among those given a diagnosis later, but the distribution according to age at diagnosis was similar (Table 1Table 1
Time of Diagnosis, Age at Diagnosis, and Extent of Disease at Diagnosis among Patients in the Study Cohort.). Because the proportion of patients with proctitis increased continuously from 1965 through 1983 (from 26 percent in 1965 through 1969 to 54 percent in 1980 through 1983), the smaller proportion of patients with proctitis among those given a diagnosis before 1965 may indicate that this trend began before 1965.Follow-up
All Swedish citizens are identifiable by a unique 10-digit national registration number.23 Using computerized linkage procedures, we were able to identify all instances of the surgical removal of the large bowel, colorectal cancer, and death. In the inpatient register, patients who had undergone a proctocolectomy, colectomy, or rectal amputation from 1965 through 1983 were identified. A population-based epidemiologic study of ulcerative colitis in Uppsala County from 1945 through 196416 provided additional information on operations before 1965. In addition to operations for a malignant neoplasm in the large bowel, 235 proctocolectomies, 131 colectomies, and 9 rectal amputations were performed through 1983.
Since 1958 it has been required that all newly diagnosed malignant tumors be reported to the National Cancer Registry by both the physician and the pathologist or cytologist.24 Almost all malignant tumors are therefore reported by two care givers, and the frequency of unreported cases is estimated at about 3 percent.25 At the time of this study, the registry was complete as of December 31, 1984, our closing date for follow-up.
The Registry of Causes of Death includes information on all deceased persons listed in the parish registries, whether they died in Sweden or abroad.26 The underlying cause of death was generally determined from data on medical death certificates, which were designed in accordance with the internationally established form.
Statistical Analysis
We calculated the number of person-years at risk for colorectal cancer beginning with the diagnosis of ulcerative colitis or in 1958, if a patient was given a diagnosis of ulcerative colitis before that year. Each member of the cohort was followed to the date of diagnosis of colorectal cancer (data from the National Cancer Registry), date of death (data from the Registry of Causes of Death), date of proctocolectomy, or closing date of this study (December 31, 1984). If a member of the cohort underwent a colectomy that left the rectum intact, this member was excluded from the calculation of the number of person-years at risk for colon cancer but included in the computation for rectal cancer. The corresponding procedure was used if a patient underwent only a rectal amputation and was thus still at risk for colon cancer.
Multiplication of the number of person-years for five-year age groups within the cohort by the corresponding age-specific incidence rate24 yielded the number of expected cases of colorectal cancer for each successive year of observation. The standardized incidence ratio, defined as the ratio of observed to expected numbers of cases of colorectal cancer, was used as a measure of relative risk. The 95 percent confidence interval of the standardized incidence ratio was then calculated on the assumption that the observed number of cases in each subgroup followed a Poisson distribution. A standardized mortality ratio was calculated on the basis of data on underlying causes of death from the Registry of Causes of Death26 in order to assess to what extent mortality from colorectal cancer in our cohort mirrored morbidity from colorectal cancer. A life-table approach was used to assess the cumulative probability of the development of colorectal cancer, beginning with the date of diagnosis.27
We decided to analyze the cohort according to sex, age group at diagnosis (<15, 15 to 29, 30 to 39, 40 to 49, 50 to 59, and ≥60 years of age), extent of disease at the time of diagnosis (proctitis, left-sided colitis, or pancolitis), and length of follow-up (by five-year intervals) after the diagnosis of ulcerative colitis. To determine whether any selection bias occurred among prevalent cases (those diagnosed before 1965), we initially analyzed the prevalent cases and the incident cases separately.
For further analyses, in which each subgroup was evaluated independently, we used Poisson regression analyses.28 The variable length of follow-up was coded either as a linear term or as both linear and quadratic terms (orthogonal polynomials). Age at diagnosis, extent of disease at diagnosis, sex, and time of diagnosis (before or after 1965) were treated as nominal variables with corresponding reference levels. The improvement in goodness of fit for different Poisson regression models was assessed by comparing the values for deviance and degrees of freedom for each model considered.28
Results
Univariate Analyses
Colorectal cancer was diagnosed in 91 patients during the follow-up period (1958 through 1984), 5.7 times the expected number of cases (16.0; 95 percent confidence interval, 4.6 to 7.0) (Table 2Table 2
Relative Risk of Colorectal Cancer among Patients with Ulcerative Colitis, According to the Length of Follow-up and the Time of Diagnosis.*). Colorectal cancer was the underlying cause of 45 deaths, 4.4 times the expected number (10.2; 95 percent confidence interval, 3.2 to 5.9).Since one patient had colon cancer followed by rectal cancer three years later, 57 cases of cancer of the colon and 35 cases of cancer of the rectum occurred; the corresponding standardized incidence ratios were 5.8 (95 percent confidence interval, 4.4 to 7.5) and 5.7 (95 percent confidence interval, 3.9 to 7.9). Because of the minimal difference between these ratios, colon and rectal cancers have been analyzed and reported together, although they were also analyzed separately and no differences were detected.
The relative risk of colorectal cancer did not differ between men and women but did increase with increasingly extensive disease at diagnosis (Table 3Table 3
Relative Risk of Colorectal Cancer among Patients with Ulcerative Colitis, According to Sex, Extent of Disease at Diagnosis, and Age at Diagnosis.*). In patients with proctitis, the relative risk of rectal cancer was 2.1 (95 percent confidence interval, 0.6 to 5.2) and that of colon cancer was 1.5 (95 percent confidence interval, 0.5 to 3.6). The relative risk decreased with increasing age at diagnosis (Table 3).Stratified Analyses
Patients given a diagnosis before 1965 had a higher relative risk of colorectal cancer than those in whom ulcerative colitis was diagnosed from 1965 through 1983 (8.1 vs. 4.0) (Table 2). However, when the comparison was confined to those followed for 19 or fewer years, this difference diminished (6.8 vs. 4.0) (Table 2). When we analyzed only those given a diagnosis of pancolitis who were followed for 19 or fewer years, the difference in relative risk between the two groups decreased further (12.9 [95 percent confidence interval, 6.9 to 22.1] vs. 10.5 [95 percent confidence interval, 6.6 to 15.8]). Because our analyses showed that the prevalent cases and the incident cases were comparable in terms of relative risk (data not shown), we have treated them as a homogeneous group.
The relative risk of colorectal cancer decreased both in patients with pancolitis and in those with left-sided colitis as the patient's age at the time of the diagnosis increased (Table 4Table 4
Relative Risk of Colorectal Cancer among Patients with Ulcerative Colitis, According to the Extent of Disease at Diagnosis and Age at Diagnosis.*). In those with proctitis, no age group had a significantly increased relative risk of colorectal cancer (data not shown). In the older groups, there was an excess of colorectal cancers diagnosed within two years of the diagnosis of ulcerative colitis. Excluding these cases reduced the standardized incidence ratios slightly, mainly among those 50 years or older at the time of diagnosis (Table 4).The hypothesis that a patient with ulcerative colitis is at maximal risk for the development of cancer at about 50 years of age regardless of the age at onset or duration of disease8 was analyzed by means of stratification for age at the time of the diagnosis of pancolitis (Table 5Table 5
Relative Risk of Colorectal Cancer among Patients with Ulcerative Colitis (Pancolitis), According to Age at Diagnosis of Ulcerative Colitis and Age at Diagnosis of Colorectal Cancer.*). The consistently higher relative risk for those given a diagnosis of pancolitis at an early age, as compared with those given the diagnosis later in life, and the absence of any decrease in the relative risk among patients 60 years of age or older seem to refute that hypothesis.Multivariate Analyses
We studied the simultaneous effects of age group, extent of disease at diagnosis of ulcerative colitis, and length of follow-up; the addition of sex, diagnosis before or after 1965, and the quadratic term in length of follow-up did not significantly improve any of the Poisson regression models examined. The results from the best model are presented in Table 6Table 6
Adjusted Standardized Incidence Ratio (ASIR) for the Development of Colorectal Cancer in Patients with Ulcerative Colitis.*. Besides confirming the results of the univariate and stratified analyses, the regression analysis also revealed that, overall, the relative risk of colorectal cancer among patients with ulcerative colitis decreased as the length of follow-up increased.Using a second approach, we included age at diagnosis in the model as a linear term. The results generated by that model were very similar to those shown in Table 6, with an adjusted standardized ratio of 0.51 (95 percent confidence interval, 0.46 to 0.56) for age at diagnosis and 0.84 (95 percent confidence interval, 0.78 to 0.90) for length of follow-up.
Cumulative Incidence
The rarity of colorectal cancer among young people is one reason for the increased standardized incidence ratio among those who were young at the time of diagnosis of ulcerative colitis, as compared with those who were older. By analyzing the cumulative incidence of colorectal cancer, one can assess the influence of length of follow-up independently of the differences in the incidence of colorectal cancer in different age groups in the background population.
Figure 1Figure 1
Cumulative Incidence of Colorectal Cancer for Patients with Pancolitis, According to Age at Diagnosis. shows the cumulative incidence of colorectal cancer for three different age groups at diagnosis (0 to 14, 15 to 39, and 40 or more years of age) for patients with pancolitis. The cumulative incidence is not estimated for categories with fewer than 20 patients. Among patients who were less than 40 years old when pancolitis was diagnosed, the cumulative incidence ("absolute risk") of colorectal cancer up to 25 years after diagnosis was about 13 percent. However, with longer follow-up those given the diagnosis before they were 15 years of age had a higher cumulative risk than patients who were older at the time of diagnosis (40 percent after 35 years as compared with 30 percent for the whole cohort). In patients who were 40 years old or older when pancolitis was diagnosed, the cumulative incidence of colorectal cancer within 20 years of diagnosis was higher than it was for those given the diagnosis of pancolitis at younger ages (16 percent vs. 5 percent). Colorectal cancer was less frequent among those who had left-sided colitis than among those with the other diagnoses. The cumulative incidence for those with left-sided colitis was 5 percent or less, with the exception of those given the diagnosis between the ages of 15 and 29, for whom the cumulative incidence of colorectal cancer 30 years after diagnosis was 12 percent.Discussion
This study confirms the existence of an increased risk of colorectal cancer among patients with ulcerative colitis. The relative risk was the same for cancer of the colon and cancer of the rectum and among men and women. The extent of disease at diagnosis and the age at diagnosis were strong and independent determinants of this increase in relative risk. The relative risk of colorectal cancer was 14.8 for patients with pancolitis, 2.8 for those with left-sided colitis, and 1.7 for those with proctitis, as compared with the general population. In the multivariate analysis, age at diagnosis was a strong, independent determinant of the risk of colorectal cancer even after control for the length of follow-up. However, the cumulative incidence of colorectal cancer among patients with pancolitis was similar for the age groups less than 40 years old at the time of diagnosis when they were followed up for as long as 25 years, but those who were 40 years of age or older at diagnosis had an increased cumulative incidence (as compared with the younger age groups) up to 20 years after diagnosis.
Closer surveillance of patients with ulcerative colitis may have led to increased identification of colorectal cancers in the study population as compared with the general population. Increased ascertainment in the study population would imply the detection of colorectal cancers at earlier stages and probably improved survival after diagnosis. However, the standardized incidence ratio for colorectal cancer was similar to the standardized mortality ratio for colorectal cancer, a finding that suggests that type of bias was unimportant. The results of this study may underestimate the relative risk of colorectal cancer because colectomies in those who moved from the region would not have been identified. The effect of this underestimation on our estimates of risk is probably negligible, however, because of the small amount of emigration from the region.
It might be more appropriate to use the date on which symptoms began rather than the date of diagnosis in calculating the length of follow-up. Reliable information on the onset of symptoms is impossible to retrieve retrospectively from patients' charts, however. In addition, differential misclassification might have arisen from an enhanced interest on the part of the treating physician in tracing the first symptoms of ulcerative colitis after the diagnosis of a subsequent colorectal cancer. Therefore, the date of diagnosis was considered the most reliable starting point.
The excess cancers noted within two years after the diagnosis of colitis may have occurred in patients with long-lasting asymptomatic colitis that escaped diagnosis until a subsequent colorectal cancer caused symptoms. This would imply that having asymptomatic, undiagnosed ulcerative colitis also entails an increased risk of cancer. When colorectal cancer is the reason for the diagnosis of ulcerative colitis, this selection bias would then lead to an overestimation of the relative risk of colorectal cancer. Although undiagnosed ulcerative colitis does occur,29 its prevalence is unknown, making it impossible to estimate its association with colorectal cancer.
The estimates of risk in different studies of colorectal cancer in patients with ulcerative colitis differ markedly,2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 but with two exceptions they show increased relative and absolute risks of colorectal cancer. In one of the two exceptional studies,2 no association was found between ulcerative colitis and colorectal cancer, probably because of a high rate of colectomy and a short follow-up — 10 or fewer years after diagnosis. In the other,9 no censoring of data was done for colectomy, which was performed in more than 30 percent of the patients; the cumulative incidence of 1.4 percent applies to the whole cohort, with a follow-up between 4 and 22 years. The cumulative incidence in the other studies 25 to 35 years after diagnosis ranges from 8 percent15 to 43 percent,4 and the standardized incidence ratio ranges from 2 to 30.11 , 13 After stratification according to the extent of disease at diagnosis and adjustment for the smallness of the samples, the differences in cumulative incidence were markedly reduced. Because of the small samples, stratification according to age at diagnosis was carried out in just three studies,4 , 8 , 15 all of which found relative risks similar to those observed in our study.
The only study4 that analyzed the risk of colorectal cancer in patients given a diagnosis of ulcerative colitis before the age of 15 has been criticized because all the patients were identified at a referral center. The cumulative incidence of cancer in that study (43 percent 35 years after diagnosis) is the highest reported. In our population-based cohort, the cumulative incidence in this group was 40 percent after 35 years, which is very close to that found by Devroede et al.4 Since patients from referral centers usually have more severe disease, this similarity implies that the severity of disease is not an important determinant of the risk of colorectal cancer.
There may be a genetic predisposition to colorectal cancer in certain patients with ulcerative colitis.8 In one study, the age at the time of diagnosis among those with a family history of inflammatory bowel disease was less than among those without such a history.30 These findings and the independent effect of a young age at diagnosis on the risk of colorectal cancer suggest that a genetic susceptibility to ulcerative colitis may be an independent risk factor for the later development of colorectal cancer.
No previous study has analyzed the relative risk of colorectal cancer among patients with ulcerative proctitis alone. In several studies, however, both patients with left-sided colitis and those with proctitis had a lower relative risk of colorectal cancer than did those with pancolitis.6 , 8 , 10 , 13 , 14 , 16 In our study, the relative risk of colorectal cancer was not significantly increased in patients with proctitis alone. The overall relative risk for those with left-sided colitis was much lower than that for those with pancolitis. In the younger groups, however, especially among patients 15 to 29 years of age at the time of diagnosis, left-sided colitis entailed a relative risk of colorectal cancer that was close to that for pancolitis. In the groups that were older at the time of diagnosis, however, the relative risk was close to 1.0.
Our findings and those of Devroede et al.4 suggest that among patients with ulcerative colitis that is diagnosed before the age of 15, prophylactic proctocolectomy might be an alternative to close surveillance in reducing mortality from colorectal cancer. Our data do not support the proposed use of an upper age limit after which no screening procedures should be used among patients with pancolitis.8 Patients with proctitis or left-sided colitis that is diagnosed after the age of 30 do not appear to have a substantial increase in risk, however.
Supported by a grant from the National Foundation for Ileitis and Colitis and by the Nanna Svartz Grant Council.
We are indebted to Dr. Richard Rothenberg for his valuable support.
Source Information
From the Department of Surgery (A.E., H.-O.A.) and the Unit of Cancer Epidemiology (H.-O.A.), University Hospital, Uppsala, Sweden, and the Centers for Disease Control, Atlanta (C.H., M.Z.). Address reprint requests to Dr. Ekbom at the Department of Surgery, University Hospital, S-751 85 Uppsala, Sweden.
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