Affiliation of authors: P. A. Newcomb, L. M. Morimoto, A. Templeton, J. D. Potter (Cancer Prevention Research Program), B. E. Storer (Clinical Statistics), Fred Hutchinson Cancer Research Center, Seattle, WA.
Correspondence to: Polly Newcomb, Ph.D., Fred Hutchinson Cancer Research Center, 1100 Fairview Ave. North, MP-900, P.O. Box 19024, Seattle, WA 98109-1024 (e-mail: pnewcomb{at}fhcrc.org).
ABSTRACT
Screening sigmoidoscopy is associated with a reduction in both the incidence and mortality of colorectal cancer. Although current guidelines recommend sigmoidoscopy screening every 5 years, the duration of risk reduction is not known. We conducted a population-based casecontrol study to examine the association between sigmoidoscopy screening and colorectal cancer incidence. We collected information on screening history and risk factors from case patients with distal (n = 1026) and proximal (n = 642) colorectal cancer and from 1294 control subjects from October 1998 through February 2002. Screening sigmoidoscopy was associated with a statistically significant reduction in the incidence of distal colorectal cancer (odds ratio [OR] = 0.24, 95% confidence interval [CI] = 0.17 to 0.33). These reductions were sustained for up to 16 years with little attenuation. We also observed strong inverse associations between cancer incidence and sigmoidoscopy in analyses that included subjects with symptom-related tests. Current recommendations regarding the frequency of sigmoidoscopy screening may be unnecessarily aggressive.
We used an institutionally approved protocol to identify eligible case patients, which included all male and female residents of King, Snohomish, and Pierce counties (WA) who were newly diagnosed with invasive colorectal adenocarcinoma [International Classification of Diseases for Oncology codes C18.0, C18.2.9, and C20.0.9 (18)] from October 1998 through February 2002, as identified through the Puget Sound Surveillance, Epidemiology, and End Results (SEER) Program1 registry, and who were aged 2074 years at diagnosis. SEER reports include information on cancer stage and grade, the patients first course of treatment, and demographics. All eligible subjects had a publicly available telephone number. Of the 2185 eligible case patients identified, 131 (6%) were deceased, 66 (3%) had physicians who refused permission to contact them, 22 (1%) could not be located, and 240 (11%) refused to participate, resulting in a final sample size of 1726 case patients (overall response rate of 79%).
Community-based control subjects were randomly selected according to the age and sex distribution of the case patients by using Washington State drivers license data for individuals aged 2064 years and Health Care Financing Administration files for individuals older than 64 years. Of the 1891 potential control subjects identified, 38 (2%) had died, 19 (1%) could not be located, and 510 (27%) refused to participate. The final study sample included 1324 control subjects (overall response rate of 70%).
We used a structured 50-minute telephone interview to obtain information from the study subjects on known or suspected risk factors for colorectal cancer, including their screening histories prior to 1 year before diagnosis (for case patients) or before interview date (for control subjects). Information on screening tests (fecal occult blood test, sigmoidoscopy, and colonoscopy) included the date of (or subjects age at) first and last tests, number of tests, and the reason for the test; we also collected information about the subjects demographics, personal medical history, family history of cancer, medication use, and lifestyle factors such as level of physical activity, occupation, alcohol consumption, and diet.
Subjects were classified as having undergone colorectal cancer screening (i.e., screening-only sigmoidoscopy) if they had sigmoidoscopy without having had prior symptoms, regardless of their family history of colorectal cancer. We considered the associations between screening-only sigmoidoscopy and colorectal cancer incidence and between any sigmoidoscopy (including symptom-related) and colorectal cancer incidence. To eliminate the possibility of bias that might arise from the selection of individuals who were at reduced risk of colorectal cancer because they had had a previous screen that was negative (19), subjects who had undergone more than one test were excluded from the analysis of the association between single-screen-only sigmoidoscopy and colorectal cancer incidence. It is possible, however, that some individuals who had multiple tests may have been at higher than average risk of disease due to the fact that they had frequent sigmoidoscopies because they were previously diagnosed with polyps, which are a precursor of colorectal cancer (20). Our analyses included only those tests performed more than 1 year prior to diagnosis or interview date, to avoid the clustering of screening tests that may have occurred shortly before diagnosis (21). Odds ratios (ORs) and 95% confidence intervals (CIs) for the association between screening and colorectal cancer incidence were estimated from a logistic regression model. Covariates were age (in 5-year intervals), sex, family history of colorectal cancer, postmenopausal hormone use (females), level of education, smoking history, body mass index (BMI), and the number of previous tests (for individuals who had more than one sigmoidoscopy). We excluded case patients with missing information about the affected subsite within the colon (n = 10). We also excluded subjects with incomplete information on screening (case patients, n = 48; control subjects, n = 30). All statistical tests were two-sided.
The mean age was 60.6 years (range = 2075 years) for case patients and 62.0 years (range = 2075 years) for control subjects. Overall, case patients were more likely than control subjects to report having a family history of colorectal cancer (26% versus 15%), to have a higher BMI (mean BMI, 27.8 kg/m2 versus 26.7 kg/m2), and to be current or former smokers (62% versus 57%). Among the women in our study, case patients were less likely than control subjects to have used postmenopausal hormones (45% versus 50%). Among the case patients, 35% were diagnosed with localized disease, 50% were diagnosed with regional disease, and 15% were diagnosed with distant metastases. Among the control subjects, 50% reported ever having a sigmoidoscopy and 27% reported ever having a screening sigmoidoscopy.
Sigmoidoscopy was associated with a statistically significant and sustained reduction in the incidence of distal colorectal cancers. Compared with individuals who had never had a screening sigmoidoscopy ("Never any screening test"), those who had ever had a screening sigmoidoscopy ("Ever any screening test") had an OR for distal colorectal cancer of 0.24 (95% CI = 0.17 to 0.33) (Table 1). This OR was similar to the OR for distal colorectal cancer among those reporting a single screening sigmoidoscopy (OR = 0.30, 95% CI = 0.20 to 0.43). This association between screening sigmoidoscopy (whether single or multiple) and reduced incidence of distal colorectal cancer was observed for individuals who reported having a screening sigmoidoscopy during all time intervals examined within the past 16 years relative to diagnosis or interview. The OR for distal colorectal cancer was also statistically significant when we included individuals with symptom-related sigmoidoscopies (i.e., "any test") in the analysis (OR = 0.47, 95% CI = 0.37 to 0.60). There was little evidence that this inverse relative risk was attenuated with increasing time since last screening. There was also some evidence that ever having had a sigmoidoscopy was associated with a modest reduction in the risk of proximal lesions (OR = 0.83, 95% CI = 0.66 to 1.04), although the inverse association was inconsistent across screening intervals.
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Our study had some limitations. First, we relied on self reports of screening history. However, several studies (2225) have found that, in general, colon cancer screening procedures are validly reported by individuals. In one recent study comparing self reports with medical records (24), sigmoidoscopy was found to have a sensitivity of 95% and a specificity of 92%. Second, the proportion of individuals who used colorectal cancer screening in our study was slightly lower than that reported for participants in The Centers for Disease Control and Preventions Behavioral Risk Factors Surveillance System (BRFSS) survey, a random digit dialing telephone survey (26). However, because response rates in the BRFSS were only approximately 60%, the enrolled comparison group may be healthier and therefore more likely to seek screening than the general population. We believe it likely that the screening practices of our control subjects were more representative of the screening practices of the general population. Finally, although this was a large study, the sample size was limited in some screening duration categories.
Despite the evidence for the efficacy of screening in reducing colorectal cancer incidence and mortality, screening for this disease is underutilized. Currently, 34% of U.S. adults older than 50 years have had a sigmoidoscopy or a colonoscopy within the past 5 years (26). Although the efficacy of colonoscopy must be greater than that of sigmoidoscopy (27), the acceptability (28, 29), cost-effectiveness (30,31), and more widespread delivery of sigmoidoscopy argues in favor of this approach for screening. The findings from our study support the recommendation of a sigmoidoscopy (with colonoscopic follow-up) every 10 years. This approach, if more widely used, could substantially reduce the incidence of mortality from colorectal cancer. If the current proportion of U.S. adults older than 50 years who have a sigmoidoscopy every 10 years doubled, the incidence of distal colorectal cancer would be reduced by approximately 19 000 cases annually.
NOTES
Supported by Public Health Service grant U01 CA074794 (to the Seattle Colorectal Cancer Family Registry) from the National Cancer Institute, National Institutes of Health, Department of Health and Human Services, and through cooperative agreements with members of the Colon Cancer Family Registry and principal investigators.
We thank Noel Weiss for advice and consultation at various stages of this project, and Ric Johnston and John Hampton for statistical advice and programming.
1 Editorss note: SEER is a set of geographically defined, population-based central cancer registries in the United States, operated by local nonprofit organizations under contract to the National Cancer Institute (NCI). Registry data are submitted electronically without personal identifiers to the NCI on a biannual basis, and the NCI makes the data available to the public for scientific research.
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Manuscript received July 5, 2002; revised November 4, 2002; accepted January 30, 2003.
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