Screening for Colorectal Cancer in Adults at Average Risk: A Summary of the Evidence for the U.S. Preventive Services Task Force

By M. Pignone, M. Rich, S. Teutsch, A. Berg, K. Lohr. Annals of Internal Medicine, 2002

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The U.S. Preventive Services Task Force (USPSTF) last considered its recommendations regarding colorectal cancer screening in 1996 (1). At that time, the available evidence included one randomized, controlled trial showing that fecal occult blood testing (FOBT) reduced mortality rates (2); a casecontrol study showing that persons having sigmoidoscopy were less likely to die of colorectal cancer (3); and one nonrandomized, controlled trial of FOBT combined with rigid sigmoidoscopy that suggested some benefit from the two tests together (4). On the basis of this evidence, the USPSTF recommended screening for colorectal cancer with FOBT, sigmoidoscopy, or both (a grade B recommendation) but did not recommend for or against other means of screening (digital rectal examination, double-contrast barium enema, or colonoscopy) because the available evidence was insufficient. (See the companion article in this issue for a description of the USPSTF classification of recommendations.) The Task Force also recommended that FOBT be performed yearly but did not specify an interval for sigmoidoscopy. Since 1996, important new evidence has emerged regarding the effectiveness of colorectal cancer screening. We performed an updated systematic review to help the USPSTF evaluate new evidence on the effectiveness of different colorectal cancer screening tests as it updated its previous recommendation. We examined the evidence concerning the effectiveness of screening in adults older than 50 years of age who are at average risk for colorectal cancer. The effectiveness, accuracy, and adverse effects of digital rectal examination (with or without a single office-based FOBT), traditional three-card FOBT (hereafter referred to as FOBT), sigmoidoscopy, FOBT with sigmoidoscopy, double-contrast barium enema, and colonoscopy were examined. Other tests or combinations of tests have not been well evaluated and are not discussed here. A more detailed report of our review can be found on the Web site of the U.S. Agency for Healthcare Research and Quality (www.ahrq.gov/clinic/uspstfix.htm) (5). The USPSTF's updated recommendations for colorectal cancer screening recommendations can be found in the companion article in this issue (6). Methods To identify the relevant literature, we used the Guide to Clinical Preventive Services, 2nd edition (1); existing systematic reviews; focused MEDLINE literature searches from 1966 through September 2001; and hand searches of key articles. When available, systematic reviews were used to identify older relevant studies. Literature searches were used to identify newer studies. Detailed descriptions of the literature searches can be found in the Appendix. To identify relevant studies, one reviewer examined the abstracts of the articles identified in the initial search. A second reviewer examined the excluded articles. Disagreements about inclusion were resolved by consensus. Two reviewers examined the full text of the remaining articles to determine final eligibility. We used evidence from randomized, controlled trials or observational studies that measured patient outcomes, particularly changes in colorectal cancer mortality rates and incidence. When such data were not available, we included indirect information on the accuracy of screening tests. Details about study inclusion are available in the Appendix. We rated the quality of the included articles by using the criteria developed by the USPSTF Methods group (7), which are described in the accompanying article in this issue (6). We used the final set of eligible articles to create evidence tables and a draft report. The draft report was extensively peer reviewed by the USPSTF, experts in the field, governmental agencies, and nongovernmental organizations. Role of the Funding Source This evidence report was funded through a contract to the Research Triangle InstituteUniversity of North Carolina Evidence-based Practice Center from the Agency for Healthcare Research and Quality. Staff of the funding source contributed to the study design, reviewed draft and final manuscripts, and made editing suggestions. Results Our general search identified 719 articles published since 1995 on colorectal cancer screening. We retained 19 of these articles in our final document. Specific searches from 1966 through 2001 for articles about the accuracy of barium enema and complications of screening yielded 621 and 839 articles, respectively. After review, we retained 13 articles about barium enema and 19 articles about complications of screening. We also included 15 articles identified from the previous USPSTF review or from hand searches of other articles. Table 1 our findings. Table 1. Characteristics of Screening Tests for Colorectal Cancer Digital Rectal Examination Effectiveness A casecontrol study from the Kaiser Permanente Medical Care Program in northern California examined the effect of screening with digital rectal examination on death from colorectal cancer (8). The investigators identified patients 45 years of age and older who died of distal rectal cancer between 1971 and 1986 and selected matched controls from the patient membership. They examined medical records to determine whether the patients and controls had undergone screening digital rectal examination within a year of cancer diagnosis. Investigators found no difference between groups after controlling for potential confounders, although the confidence interval was wide (odds ratio, 0.96 [95% CI, 0.56 to 1.7]). Accuracy The potential sensitivity of screening digital rectal examination is low; fewer than 10% of cases of colorectal cancer are within reach of the examining finger (28). The specificity of positive results on digital rectal examination has not been examined in outpatients at average risk for colorectal cancer. In-Office Fecal Occult Blood Testing after Digital Rectal Examination Effectiveness No studies have examined the effect of a single in-office FOBT after digital rectal examination on colorectal cancer incidence or mortality rates. Accuracy A single in-office FOBT is likely to be less sensitive than the traditional three-card FOBT performed at home because only one sample is taken (9). In a large study from Japan, Yamamoto and Nakama (10) found that the first test card detected only 58% of cancer found after a three-card test. The single in-office FOBT may be less specific than a properly performed three-card FOBT because the in-office test does not allow degradation of the vegetable peroxidases that sometimes produce false-positive results (9). In addition, the potential trauma from the in-office examination itself may also result in lower specificity (9). Two studies of poor to fair quality that used existing data to retrospectively compare the specificity of the single in-office FOBT and the three-card home FOBT (11, 12) found little difference in specificity between the two groups. However, the validity of these studies is limited because neither could ensure that similar patient samples received each test. Fecal Occult Blood Testing Effectiveness In addition to an older randomized trial performed in Minnesota (2), which was available to the USPSTF in 1996, two newer randomized, controlled trials have examined the effectiveness of biennial FOBT for reducing death from colorectal cancer (13, 14). These more recent trials, from the United Kingdom (13) and Denmark (14), found 15% and 18% reductions in mortality rates, respectively, with biennial testing. Neither trial used slides that were rehydrated before development (Table 2). Table 2. Trials of Fecal Occult Blood Testing The Minnesota trial compared annual and biennial testing with no screening and rehydrated most test cards (83%). Cumulative colorectal cancer mortality rates after 18 years of follow-up were 33% (CI, 17% to 49%) lower among persons randomly assigned to undergo annual FOBT than in a control group that was not offered screening (absolute rates, 9.5 deaths per 1000 participants vs. 14.1 deaths per 1000 participants; difference, 4.6 deaths per 1000 participants) (2). Biennial screening, which did not show a reduction in mortality rates at 13-year follow-up, produced a 21% (CI, 3% to 38%) reduction in mortality rate at 18 years (15). The 18-year follow-up also showed that the incidence of colorectal cancer decreased by 20% (CI, 10% to 30%) and 17% (CI, 6% to 27%) in the groups screened annually and biennially, respectively, compared with controls (16). Because of differences in hydration, test frequency, duration, and effect size, the results of these trials could not be combined in a meta-analysis. Accuracy A systematic review from 1997 found that the sensitivity of a single unrehydrated FOBT for cancer was approximately 40%; its specificity seems to range from 96% to 98%. Rehydration was found to increase sensitivity to between 50% and 60% but decreased specificity to 90% (9, 29). In a recent study, Lieberman and colleagues (17) found that the sensitivity of rehydrated FOBT for cancer was 50% (CI, 30% to 70%). For advanced neoplasia (cancer and polyps that are large, villous, or dysplastic), sensitivity was 24% (CI, 19% to 29%) and specificity was 94% (CI, 93% to 95%). In the annual screening arm of the 13-year Minnesota trial, which primarily used rehydrated test cards and had a high initial rate of participation (approximately 90%), 49% of patients who developed colorectal cancer were identified through screening. Thirty-eight percent of all patients had had at least one colonoscopy (2). Biennial screening detected 39% of patients with cancer in the intervention group, and 28% of patients required colonoscopy. Compared with the Minnesota trial, the two European trials were population-based, lasted 8 to 10 years, used only biennial testing, and had lower participation rates (60% to 70% of patients completed the first screening). Screening detected 27% of patients in the intervention group who developed colorectal cancer, a

Subfields: Oncology

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