Original Article
A Case–Control Study of Screening Sigmoidoscopy and Mortality from Colorectal Cancer
N Engl J Med 1992; 326:653-657March 5, 1992
- Abstract
- Abstract
Background
The efficacy of sigmoidoscopic screening in reducing mortality from colorectal cancer remains uncertain. A randomized trial would be ideal for clarifying this issue but is very difficult to conduct. Case–control studies provide an alternative method of estimating the efficacy of screening sigmoidoscopy.
Methods
Using data on the 261 members of the Kaiser Permanente Medical Care Program who died of cancer of the rectum or distal colon from 1971 to 1988, we examined the use of screening by rigid sigmoidoscopy during the 10 years before the diagnosis and compared it with the use of screening in 868 control subjects matched with the case subjects for age and sex.
Results
Only 8.8 percent of the case subjects had undergone screening by sigmoidoscopy, as compared with 24.2 percent of the controls (matched odds ratio, 0.30; 95 percent confidence interval, 0.19 to 0.48). Adjustment for potential confounding factors increased the odds ratio to 0.41 (95 percent confidence interval, 0.25 to 0.69). The negative association was as strong when the most recent sigmoidoscopy was 9 to 10 years before diagnosis as it was when examinations were more recent. By contrast, for 268 subjects with fatal colon cancer above the reach of the sigmoidoscope and for 268 controls, the adjusted odds ratio was 0.96 (95 percent confidence interval, 0.61 to 1.50). The specificity of the negative association for cancer within the reach of the sigmoidoscope is consistent with a true efficacy of screening rather than a confounding by unmeasured selection factors.
Conclusions
Screening by sigmoidoscopy can reduce mortality from cancer of the rectum and distal colon. Screening once every 10 years may be nearly as efficacious as more frequent screening. (N Engl J Med 1992; 326:653–7.)
Media in This Article
Table 1
Demographic and Clinical Characteristics of the Subjects with Fatal Cancers within Reach of the Rigid Sigmoidoscope, and of the Controls.Table 2
History of Screening Tests during the 10-Year Period before the Diagnosis of Fatal Cancer within Reach of the Rigid Sigmoidoscope in the Case Subjects.Article Activity
- Article
SIGMOIDOSCOPY in asymptomatic persons appears to be a highly sensitive method for the early detection of both cancer and adenomatous polyps of the distal colon and rectum. Sigmoidoscopy is also relatively costly and uncomfortable, however, and there are no data from appropriately controlled studies to support its efficacy in reducing mortality. For these reasons, periodic screening by sigmoidoscopy has not been endorsed in several recent reviews.1 2 3 A randomized trial of screening sigmoidoscopy would require a very large number of subjects, a long duration, or both to detect reductions in mortality from cancer, and it would be hampered by noncompliance.
The case–control approach has been suggested as an efficient alternative design for the evaluation of screening tests and preventive maneuvers4 5 6 and has been used to evaluate Pap tests,7 , 8 mammography,9 the detection of prostatic cancer by digital rectal examination,10 vaccine efficacy,11 and the use of bicycle helmets.12 To test for an effect of screening on mortality from cancer, previous exposure to the screening test is compared in subjects who died of cancer and in a general population sample. A lower frequency of screening among those who died provides evidence in support of a protective influence of screening on mortality. Persons with fatal, rather than incident, cancers are the appropriate case subjects, since the primary purpose of screening is to prevent death. Screening may in fact lead to increased early diagnosis of cancer, and if these subjects were included in the case group, there would be an apparent positive association between screening and the incidence of cancer.
Because screening is not randomly assigned in a case–control study, selection factors related to both the likelihood of undergoing a screening sigmoidoscopic examination and the risk of dying from colorectal cancer may confound estimates of efficacy. In this case–control study, we classified fatal colorectal cancers according to whether they were within or beyond the reach of the sigmoidoscope, to assess the possible influence of such factors.
Methods
Study Setting
Periodic screening by rigid sigmoidoscopy for persons 40 to 50 years of age and older has been encouraged at three facilities of the Kaiser Permanente Medical Care Program of Northern California (in Hayward, Oakland, and San Francisco) since approximately 1960. Most program members receive all their outpatient care within the health plan, since care is comprehensive and there are no additional fees for procedures such as sigmoidoscopy. Thus, exposure to sigmoidoscopy could be reliably ascertained by reviewing medical records.
Identification of Case Subjects
Case subjects included plan members 45 years old or older who were found to have adenocarcinoma of the colon or rectum between 1971 and 1987 and who died of the cancer by the end of 1988. Persons with less than one year of membership before diagnosis were excluded. Potential case subjects were identified from files provided by the Bay Area Resource for Cancer Epidemiology (the San Francisco Bay Area Surveillance, Epidemiology and End Results Registry), which collects and reviews all diagnoses of cancer from area facilities. Death was ascertained either directly from registry information (1331 patients) or by automated linkage to California state death certificates13 through December 1988 (381 patients who were high-probability matches).
Two chart reviewers examined the medical records of each of these 1712 patients. The first reviewer verified the histologic diagnosis of adenocarcinoma and its anatomical location, determined whether the cancer had caused the patient's death (using a written protocol and adjudication by a physician when needed), and recorded symptom status and mode of diagnosis. The primary analyses in this report include all 261 cases of fatal adenocarcinoma that could have been detected by rigid sigmoidoscopy (i.e., all cancers of the rectum or rectosigmoid and cancers of the sigmoid colon that were visualized by rigid sigmoidoscopy or described as within 20 cm of the anus in pathological or surgical reports). A random sample of 268 fatal cancers that were above this point (and were therefore not detectable by rigid sigmoidoscopy) was selected from the remaining cases of fatal colon cancer for separate analysis.
Identification of Controls
Four control subjects per case subject were drawn from the Kaiser Permanente Medical Care Program membership lists for the three facilities and matched with the case subjects according to age (within one year), sex, and date of entry into the health plan (within one year). Each control subject also had to be alive and a member of the health plan when the case subject died. Control subjects with a history of adenomatous polyps or nonfatal colorectal cancer were not excluded. For some case subjects, fewer than four controls who met all the matching and inclusion criteria could be found. Among the final 261 case–control sets, there were 136 with four controls, 81 with three, 37 with two, and 7 with one. One control was selected for each of the 268 patients with fatal cancer that was above the reach of the sigmoidoscope.
Documentation of Sigmoidoscopy, Other Screening Tests, and Potential Confounding Variables
The first reviewer masked the medical records of eligible case subjects and their controls at a date immediately before the onset of symptoms or the screening test that led to the diagnosis in the case subject. The second reviewer, who was therefore unaware of the subject's case–control status, then reviewed the subject's outpatient medical records for the previous 10 years, recording all instances of sigmoidoscopy, digital rectal examination, fecal-occult-blood testing, barium-enema examination, and colonoscopy. The date, indication, and findings were recorded for each test.
The indication was categorized as follows: for screening, for possible symptoms, for clear-cut symptoms, or as follow-up of another positive test. Only 1.5 percent of all tests fell into the ambiguous category of "possible symptoms." A double review of 144 records for quality control revealed agreement on the indication for 97 percent of the sigmoidoscopies, 96 percent of the digital rectal examinations, and 92 percent of the fecal-occult-blood tests. In the analyses reported here, we considered only the tests judged to have been performed for screening.
Several possible confounding factors were also recorded. These included a history of adenomatous polyps or colorectal cancer before the 10-year review period, a family history of colorectal cancer noted before the case was diagnosed, and a diagnosis of ulcerative colitis or hereditary polyposis at any time before the diagnosis of the fatal cancer. These factors could lead to both increased screening and an increased risk of colorectal cancer, thereby decreasing or obscuring a protective effect of screening. The number of periodic health examinations during the 10-year period was also recorded as a marker for unmeasured features of lifestyle that might be associated with a tendency to be screened and, independently, with a lower risk of death from colorectal cancer.
Statistical Analysis
All our analyses considered the 10-year period just before the onset of symptoms that led to the diagnosis of the fatal colorectal cancer. For cancers that were detected by a screening test, the tests that led to the diagnosis were also included in all analyses. The same 10-year period was examined for the matched control subjects. If data on a case subject or control were available for less than the full 10 years, only the years for which data were available for all members of the set were considered. Conditional logistic-regression models for matched sets were used to estimate odds ratios and for all adjusted analyses.
An overall odds ratio was calculated for having had any screening test within the 10-year period as compared with no screening test. Adjustment was then made for confounding factors, including a personal history of colorectal cancer or polyps, a family history of colorectal cancer, the number of screening digital rectal examinations and fecal-occult-blood tests, and the number of health checkups during the 10-year period.
To address the question of the optimal screening interval, we divided the 10-year period into segments and calculated the odds ratios for having a screening test during each segment in separate models and simultaneously. In another approach, odds ratios were calculated for having one's most recent screening test during each 2-year segment, with the reference group being persons who had no screening tests during the 10-year period. To reduce any possible bias from the fact that persons who have had negative screening tests for a cancer will subsequently have a lower incidence of that cancer than persons who have not had the screening test,14 we excluded from these analyses 8 case subjects and 106 controls who had more than one screening sigmoidoscopy during the 10-year period.
Results
Analyses of Cases of Fatal Cancer within Reach of the Sigmoidoscope
Ten years of data were available for more than half the case–control sets, and at least five years of data were available for nearly 75 percent (Table 1Table 1
Demographic and Clinical Characteristics of the Subjects with Fatal Cancers within Reach of the Rigid Sigmoidoscope, and of the Controls.). A history of colorectal cancer or adenomatous polyps before the 10-year observation period and a family history of colorectal cancer were each noted more frequently among case subjects than among controls. The fatal cancers included 97 (37.2 percent) from the distal 7 cm of the rectum, 64 (24.5 percent) from higher in the rectum, 53 (20.3 percent) from the rectosigmoid, and 47 (18.0 percent) from the distal sigmoid colon.A significantly smaller proportion of case subjects (8.8 percent) than controls (24.2 percent) had undergone screening by rigid sigmoidoscopy during the 10-year period (Table 2Table 2
History of Screening Tests during the 10-Year Period before the Diagnosis of Fatal Cancer within Reach of the Rigid Sigmoidoscope in the Case Subjects.). The case subjects also had fewer periodic health checkups, screening digital rectal examinations, and screening occult-blood tests than the controls. The number of sigmoidoscopies was strongly correlated with the number of periodic health examinations (r = 0.50) in the control group, and to a lesser extent with the number of rectal examinations (r = 0.34) and occult-blood tests (r = 0.13).The unadjusted odds ratio for exposure to one or more screening sigmoidoscopies during the 10-year period was 0.30 for case subjects as compared with controls (Table 3Table 3
Odds of Having Had at Least One Screening Sigmoidoscopy during the 10-Year Period before the Diagnosis of Fatal Cancer in the Case Subjects.). This association did not differ significantly according to sex (0.27 for men and 0.34 for women) or age at diagnosis (0.41 for those under 65 years of age and 0.24 for those 65 and older).Adjustment for a history of colorectal cancer or polyps or a family history of colorectal cancer lowered the odds ratio slightly to 0.25 (data not shown). Further adjustment for the number of periodic health examinations, used as a marker for features of lifestyle that could lead to increased screening and a lower risk of mortality, thereby exaggerating a negative association, raised the odds ratio to 0.41. An increased number of these examinations was itself related to a reduced risk of fatal colorectal cancer (odds ratio for each additional checkup, 0.79; 95 percent confidence interval, 0.73 to 0.86). Adjustment for the number of rectal examinations and occult-blood tests did not appreciably alter the odds ratios.
Analyses of Cases of Fatal Cancer beyond the Reach of the Sigmoidoscope
By contrast, little evidence of the efficacy of screening was found in the analysis of 268 case subjects with fatal cancers beyond the usual reach of the rigid sigmoidoscope and their controls (Table 3), particularly after adjustment for the number of periodic health examinations. The odds ratio for fecal-occult-blood testing was slightly below 1.0 (odds ratio for each additional test, 0.87). However, the 95 percent confidence interval was quite wide (0.72 to 1.05), in part because the frequency of testing during the period examined (largely before 1980) was very low for both case subjects and controls.
Analyses of the Screening Interval
Table 4 shows the screening frequencies according to two-year segments for the case subjects and controls. The proportion of the case subjects who underwent screening sigmoidoscopy was well below that of the controls in each segment. In a single multivariate model that considered three segments (0 to 3 years, 4 to 5 years, and 6 to 10 years) simultaneously, the odds ratios for having had a screening sigmoidoscopy were 0.63, 0.36, and 0.42, respectively, for the case subjects as compared with the controls. In the analysis of the most recent screening sigmoidoscopy (Table 5), having had one's most recent examination 9 to 10 years before the diagnosis of the fatal cancer in the case subject was associated with a risk as low as that associated with having had it in the 2 years just before diagnosis. In this analysis, the small numbers of exposed case subjects yielded point estimates with wide confidence intervals for the two-year segments.
There were 14 subjects whose fatal cancers were diagnosed within three years of a screening sigmoidoscopic examination. The examination detected the cancer in three of these subjects and was the first sigmoidoscopic examination for each of them. In 4 of the 11 who had a negative sigmoidoscopic examination, the lesion was above the recorded depth of insertion of the sigmoidoscope. The remaining seven subjects had cancers in the area examined during sigmoidoscopy. These seven therefore had either lesions that were missed or cancers that developed during the one to three years after the negative sigmoidoscopic examination.
Discussion
In this case–control study, subjects who had undergone one or more screening examinations by rigid sigmoidoscopy during the previous 10 years had only 30 percent of the risk of fatal cancer of the rectum or distal colon that nonscreened subjects had. These results are similar to those of another, smaller case–control study.15 Several potential confounding factors were considered. A personal or family history of colorectal cancer or polyps could lead both to more frequent screening and to a higher risk of colorectal cancer. The estimate of risk dropped to 0.25 after adjustment for these factors. Symptoms not mentioned in the medical records might also lead to increased screening.16 If such symptoms were due to undiagnosed cancer, this could have shifted our estimate of the odds ratio upward, leading to an underestimate of true efficacy, particularly in the most recent two-year period.
Selection factors such as a healthy lifestyle or greater compliance with medical treatment among persons who undergo sigmoidoscopy could spuriously exaggerate estimates of efficacy. Adjustment for the number of periodic health examinations increased our estimate of the odds ratio for having undergone screening to 0.41. This variable has been shown to be related to overall mortality in the population in our health plan.17 Information about more specific features of lifestyle, such as diet or level of physical activity, was not available from the medical records. It is unlikely, however, that these factors differed sufficiently between subjects who underwent sigmoidoscopy and those who did not to account for a substantial portion of the remaining association.
The apparent benefit of screening by sigmoidoscopy was confined exclusively to the part of the colon and rectum that can be seen with the rigid sigmoidoscope. It is difficult to conceive of how such anatomical specificity of effect could be explained by confounding.
The low frequency of repeat screening in both the case subjects and the controls made it impossible to compare various screening intervals directly. We therefore examined the length of the period after a negative examination during which the risk of fatal colorectal cancer was decreased. Our data indicate that the risk was markedly lower for at least 10 years after a single sigmoidoscopic examination. This observation is consistent with data suggesting that the length of time from a "clean" bowel to the development of adenomatous polyps and progression to carcinoma is at least 10 years on average.18 19 20 The data from the control group in this study indicate that screening sigmoidoscopy led to the removal of polyps in this population. Of 210 control subjects who had at least one screening sigmoidoscopic examination during the 10-year period, 12 had adenomatous polyps detected and removed as a consequence of screening.
The 11 persons whose fatal cancer was diagnosed within three years after a negative screening sigmoidoscopic examination illustrate the fact that sigmoidoscopy would not be 100 percent efficacious even if repeated fairly frequently. The four cancers that arose above the depth of insertion of the sigmoidoscope reflect the occasional impossibility of fully inserting an endoscope. The remaining seven cancers arose in the part of the bowel judged to have been visualized and free of tumor. These lesions were either missed or developed and progressed to an incurable state within one to three years. It is clear that some lesions are missed on sigmoidoscopy, particularly flat lesions.21 , 22 Colorectal cancer is also known occasionally to arise either spontaneously or in very tiny adenomas.23
Flexible sigmoidoscopy, as performed today, appears to be at least as sensitive as rigid sigmoidoscopy.24 , 25 At least 50 percent of all colorectal cancers and adenomatous polyps26 , 27 arise in the 60-cm portion of the large bowel that can be examined by flexible sigmoidoscopy. Thus, our adjusted odds ratio of 0.41, implying a 59 percent reduction in mortality, suggests that a screening program using flexible sigmoidoscopy could lead to a reduction of at least 30 percent in total mortality from colorectal cancer.
Had these data been available during the deliberations of the U.S. Preventive Services Task Force,1 we believe the task force would have concluded that there was "fair" evidence to warrant including sigmoidoscopy in a periodic health examination. Further information will be needed to define the optimal frequency of screening. Cost effectiveness and acceptability will be greatly enhanced if, as our results suggest, a screening sigmoidoscopic examination every 10 years is nearly as efficacious as more frequent tests. With the further savings that are possible by using examiners who are not physicians,28 , 29 flexible sigmoidoscopy could become a very cost-effective strategy of prevention.
Supported by grants (R01 CA46569 and R35 CA49761) from the National Cancer Institute.
We are indebted to Ms. May Kuwatani and Ms. Betty Jue for their careful work in reviewing the medical records for this study.
Source Information
From the Division of Research, Kaiser Permanente Medical Care Program. Oakland, Calif. (J.V.S., G.D.F., C.P.Q.), and the Department of Epidemiology, School of Public Health and Community Medicine, University of Washington, Seattle (N.S.W.). Address reprint requests to Dr. Selby at the Division of Research, Kaiser Permanente Medical Care Program. 3451 Piedmont Ave., Oakland, CA 94611.
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