Reducing Mortality from Colorectal Cancer by Screening for Fecal Occult Blood
Jack S. Mandel, John H. Bond, Timothy R. Church, Dale C. Snover, G. Mary Bradley, Leonard M. Schuman, Fred Ederer, for The Minnesota Colon Cancer Control Study
Background Although tests for occult blood in the feces arewidely used to screen for colorectal cancers, there is no conclusiveevidence that they reduce mortality from this cause. We evaluateda fecal occult-blood test in a randomized trial and documentedits effectiveness.
Methods We randomly assigned 46,551 participants 50 to 80 yearsof age to screening for colorectal cancer once a year, to screeningevery two years, or to a control group. Participants who werescreened submitted six guaiac-impregnated paper slides withtwo smears from each of three consecutive stools. About 83 percentof the slides were rehydrated. Participants who tested positiveunderwent a diagnostic evaluation that included colonoscopy.Vital status was ascertained for all participants over 13 yearsof follow-up. A committee determined causes of death. A singlepathologist determined the stage of cancer for each tissue specimen.Differences in mortality from colorectal cancer, the primarystudy end point, were monitored with the sequential log-rankstatistic.
Results The 13-year cumulative mortality per 1000 from colorectalcancer was 5.88 in the annually screened group (95 percent confidenceinterval, 4.61 to 7.15), 8.33 in the biennially screened group(95 percent confidence interval, 6.82 to 9.84), and 8.83 inthe control group (95 percent confidence interval, 7.26 to 10.40).The rate in the annually screened group, but not in the bienniallyscreened group, was significantly lower than that in the controlgroup. Reduced mortality in the annually screened group wasaccompanied by improved survival in those with colorectal cancerand a shift to detection at an earlier stage of cancer.
Conclusions Annual fecal occult-blood testing with rehydrationof the samples decreased the 13-year cumulative mortality fromcolorectal cancer by 33 percent.
In 1993 there will be approximately 152,000 new cases of colorectalcancer in the United States and 57,000 deaths from this disease1.The cause of colorectal cancer is unknown, although associationshave been reported with family history, diet, alcohol, and sedentaryhabits2. In the absence of definitive information to supportprimary-prevention programs, attention has focused on the useof screening to detect this cancer earlier, when interventionmay reduce mortality3.
Although the concept of occult-blood detection has existed since1864, there was little interest in its application to the earlydetection of large-bowel cancer until 1967, when Greegor proposeda test for home use that involved guaiac-impregnated paper slides4.There has been no direct evidence, however, of the efficacyof screening with this test in reducing mortality from colorectalcancer.
Randomized trials of fecal occult-blood screening are ongoing,5,6,7,8,9,10,11,12but interim results of these studies have so far not providedconclusive evidence of the effectiveness of screening. Likewise,a nonrandomized study involving 21,756 participants systematicallyassigned to screening or to a control group reported a significantshift to an earlier stage of cancer at diagnosis and a significantincrease in survival with colorectal cancer, but a nonsignificantreduction in mortality due to colorectal cancer in the screeninggroup3.
In this article, we report the results of the Minnesota ColonCancer Control Study and present conclusive evidence from arandomized trial of the effectiveness of fecal occult-bloodscreening in reducing mortality from colorectal cancer.
Methods
Details of the study design have been reported elsewhere13,14,15and are summarized here. From 1975 through 1977, 46,551 participants50 to 80 years of age were recruited from among volunteers forthe American Cancer Society and fraternal, veterans, and employeegroups in Minnesota. Persons who at the time of enrollment reporteda history of colorectal cancer, familial polyposis, or chroniculcerative colitis and persons known to be bedridden or otherwisedisabled were not enrolled in the trial. No effort was madeto interview or examine prospective participants or to reviewtheir medical records. After stratification according to age,sex, and place of residence, the participants were randomlyassigned to screening once a year, to screening once every twoyears (biennially), or to a control group.
The participants in the two groups assigned to screening wereeach asked to submit six guaiac-impregnated paper slides (Hemoccult);the slides contained two smears from each of three consecutivestools. The participants were instructed to abstain from redmeat, poultry, fish, and certain raw vegetables and fruits andto stop taking vitamin C tablets and aspirin for 24 hours beforeand during the collection of the samples; adherence to thisregimen was not verified. The slides were tested at the laboratoriesof the University of Minnesota Hospital according to a standardized,controlled procedure. The mailing of slides from areas throughoutMinnesota delayed their processing for up to eight days. Becausethe drying caused by this delay may have decreased the sensitivityof the test, the procedure of rehydrating each slide with adrop of deionized water during processing was begun in 1977.All slides were rehydrated from 1982 through the end of screeningin February 1992.
The participants were notified of the results of screening.Those with one or more slides testing positive in the set ofsix were urged to return for evaluation at the hospital. Initially,the diagnostic protocol included a history and physical examination,rigid proctosigmoidoscopy, single-column barium-enema radiography,complete blood count, urinalysis, routine tests of blood chemistry,upper gastrointestinal series, chest radiography, electrocardiography,and colonoscopy. In 1978, the use of single-column barium-enemaradiography was discontinued, because this procedure missed20 percent of the cancers detected by colonoscopy16. Thereafter,double-contrast barium enemas were administered to about 5 percentof the patients when colonoscopy was incomplete or suboptimal.The use of rigid proctosigmoidoscopy and upper gastrointestinalseries was abandoned in 1982. Proctosigmoidoscopy was unnecessarywith colonoscopy, and the upper gastrointestinal series didnot uncover substantial disease requiring treatment.
During colonoscopy, biopsies of visible lesions were performed,and the lesions were removed when possible. All substantialabnormalities, particularly polyps and cancers, were treated,and the patients were followed by either their physicians orthe university staff.
Some participants with positive guaiac tests who saw their ownphysicians for the diagnostic evaluation did not undergo colonoscopy.Detailed information on the results of the examination was obtainedfrom the attending physician.
The participants in all three study groups received mailed questionnairesannually to ascertain their vital status, the occurrence ofcolorectal cancer and polyps in the control-group participants,and the detection of any colorectal lesions by other means thanthe study screening in members of the screened groups. Participantswho did not return the questionnaire were telephoned and askedfor this information. For all reported lesions, medical recordsconcerning the diagnosis were obtained.
Death certificates were obtained for all patients who died.The uncoded death certificates, along with the relevant medicalrecords, were submitted without study-group designation to aDeaths Review Committee consisting of two pathologists, an oncologist,and a gastroenterologist, none of whom were otherwise involvedwith the study, in order to determine whether colorectal cancerhad been the underlying cause of death.
The study pathologist staged the slides of pathological specimensobtained from patients with colorectal cancer, using the Turnbullmodification of the 1932 Dukes' staging system17,18. When neitherlymph nodes nor adequately oriented sections of the tumor wereavailable for staging, the cancer was categorized as unstaged.The cause of death as determined by the Deaths Review Committeeand the stage as determined by the study pathologist were usedin the present analyses.
A sample containing 15,000 participants in each group and 45,000overall was initially determined13. The initial protocol specifiedfive years of screening and five years of follow-up, with thescreening phase to end in 1982. In 1985, the Policy and DataMonitoring Group recommended that screening be reinstituted,because the number of deaths from colorectal cancer in the controlgroup was lower than had been initially projected19,20. Screeningwas reinstituted in February 1986, and it continued throughFebruary 1992.
Differences in mortality from colorectal cancer, the primarystudy end point, between each of the two screening groups andthe control group were monitored in a group-sequential analysisby means of the sequential log-rank statistic as computed fromlife tables21,22 through year 13, the last complete year offollow-up in this analysis. A one-sided type I error rate of0.025 was applied to each comparison with 80 percent power againstthe alternative hypothesis of a 25 percent reduction in mortalityfrom colorectal cancer. To adjust each sequential statisticaltest for multiple examinations of the data, stopping boundariesfor rejecting the null hypothesis were computed23 with use ofa constant spending rate for the type I error and for acceptingthe null hypothesis by the stochastic curtailment method ofLan and Wittes,24 with 95 percent confidence intervals for therate ratios for mortality adjusted for sequential analysis25.Total mortality, the incidence of colorectal cancer, and thesurvival of patients with colorectal cancer were analyzed withoutmonitoring by life-table methods21,22. The decision to publishresults was made after a review of the most recent data on mortalityfrom colorectal cancer showed that the stopping boundary hadbeen crossed in the annually screened group. In a supportinganalysis, proportional-hazards (Cox) regression was used toadjust for age, sex, and place of residence26.
The sensitivity of the screening test was determined with theassumptions that cases of colorectal cancer discovered withinone year after positive screening were true positives (casesdetected by screening) and that those discovered within oneyear after negative screening were false negatives.
Results
Randomization was effective in creating a balance among thethree study groups with respect to age and sex (Table 1) andplace of residence (data not shown).
Table 1. Age and Sex of the Participants at the Time of Randomization, According to Study Group.
The annually screened group completed 75.2 percent of the screeningoffered, and the biennially screened group completed 78.4 percent(Table 2). Ninety percent of each group completed at least onescreening. All the screenings were completed by 46.2 and 59.7percent of the groups screened annually and biennially, respectively.
Table 2. Compliance with Screening and Diagnostic Protocols and Results of Examinations, According to Study Group.
Seventy-five percent of the participants testing positive wereexamined at the University of Minnesota Hospital (Table 2),20 percent were followed by their own physicians, and 5 percentdeclined to consult a physician. The proportion examined outsidethe university was higher in the case of women and increasedwith age for both men and women, from less than 10 percent forparticipants under 65 to approximately 40 percent for thoseover 80. Over 96 percent of those examined at the universityunderwent colonoscopy. Of those examined elsewhere, 44 percenthad a colonoscopy, 42 percent had flexible sigmoidoscopy andbarium enema but no colonoscopy, 11 percent had repeat stoolblood tests, and 3 percent were told by their physician thatno examination was necessary.
Of 12,246 colonoscopies performed at the university, 4 resultedin perforation of the colon (all requiring surgery), and 11in serious bleeding (3 requiring surgery).
Vital status was determined for each study participant through13 years of follow-up. Death certificates were obtained for99.9 percent of the participants who died, and medical recordswere available for 99 percent of the participants. Except fordeaths from colorectal cancer, the distribution according tounderlying cause of death as recorded on the death certificatewas similar in the three study groups (Table 3).
Table 3. Distribution of Causes of Death According to Study Group, on the Basis of Death Certificates.
Over the first 13 years of follow-up, there were 1002 casesof colorectal cancer, 10,097 deaths, and 320 deaths from colorectalcancer among the 46,551 participants (Table 4). Although thecumulative incidence of colorectal cancer was virtually identicalin the three groups, the cumulative annual mortality rate fromcolorectal cancer was lower in the annually screened group (5.88per 1000) than in the biennially screened group (8.33 per 1000)and the control group (8.83 per 1000). The rate ratio for mortalityfrom colorectal cancer (the mortality rate in each screenedgroup divided by the mortality rate in the control group) wassignificantly below 1 in the annually screened group (rate ratio,0.67; 95 percent confidence interval, 0.50 to 0.87), but notin the group screened every two years (rate ratio, 0.94; 95percent confidence interval, 0.68 to 1.31). These results reveala significant reduction in mortality at 13 years of follow-upin the annually screened group as compared with the controlgroup (Figure 1). Adjustment for age, sex, and place of residenceby Cox proportional-hazards regression26 did not alter thisconclusion.
Figure 1. Cumulative Mortality from Colorectal Cancer, According to Study Group.
Bars represent ±2 SE.
Early in the study, the biennially screened group had a highercumulative mortality and incidence of colorectal cancer thanthe control group (Figure 1 and Figure 2). By year 13, the trendhad reversed, and there was a slight reduction in mortalityas compared with the control group. The statistic for the bienniallyscreened group did not cross the stopping boundary, however,indicating that the alternative hypothesis for the bienniallyscreened group (a 25 percent reduction in mortality) was neitheraccepted nor rejected.
Figure 2. Cumulative Incidence of Colorectal Cancer, According to Study Group.
Bars represent ±2 SE. Participants in whom colorectal cancer was diagnosed before randomization are not represented in this figure.
The results for cumulative survival from the time of diagnosisof colorectal cancer (Figure 3) were consistent with the viewthat earlier detection by screening results in improved survivaland reduced mortality from colorectal cancer (Table 4 and Figure 1).Patients with disease detected by screening had higher 13-yearsurvival rates than those with disease not detected by screeningin both screened groups (Figure 4). The 13-year survival ratein the control group (59 percent) was similar to that of thepatients with cancer not detected by screening in each of thescreened groups (58 percent).
Figure 4. Cumulative Survival of Participants with Colorectal Cancer, According to Method of Detection and Study Group.
Bars represent ±2 SE.
The cumulative 13-year incidence rates of colorectal canceraccording to study group and Dukes' cancer stage showed changesin the incidence of Dukes' stage A and stage D cancers in thescreened groups as compared with controls that were consistentwith earlier detection of colorectal cancer by screening (Figure 5).The percent distribution according to stage and group showedthe same pattern of stage shifting that we observed in the cumulativeincidence rates (data not shown).
Figure 5. Cumulative 13-Year Incidence of Colorectal Cancer, According to Study Group and Dukes' Stage.
Numbers shown above the bars are numbers of cases of colorectal cancer per 1000. Participants in whom colorectal cancer was diagnosed before randomization are not represented in this figure.
Table 5 shows that there were twice as many Dukes' stage D cancersin the control group as in the annually screened group (65 vs.33, respectively). These cancers accounted for 54 and 40 percent,respectively, of the deaths from colorectal cancer in thesegroups. The percent survival at five years was only 2.4 forpatients with Dukes' stage D cancers, as compared with earlier-stagecancers, for which survival ranged from 94.3 percent (Dukes'stage A) to 56.6 percent (Dukes' stage C).
Table 5. Colorectal Cancers, According to Study Group and Dukes' Stage, and Five-Year Survival According to Stage.
A notable feature of this study was the effect of rehydrationof the slides on test results. Overall, 82.5 percent of theslides were rehydrated. As a result of rehydration, the rateof positive results increased more than fourfold, from 2.4 to9.8 percent (Table 6). There was a marked increase in positivitywith age, particularly for the rehydrated slides. The positivityrate for such slides increased from 8 percent in the case ofparticipants 50 to 59 years of age at entry into the study to16 percent in the case of participants 80 or over, and the ratewas higher in men than in women (data not shown). The age trendwas less marked in the case of slides that were not rehydrated;positivity rates increased slightly, from 1.8 percent for participants50 to 59 years of age to 2.4 percent for those 80 or over.
Table 6. Positivity, Sensitivity, Specificity, and Positive Predictive Value of Testing for Colorectal Cancer, According to Rehydration Status of Slides, in Both Screening Groups Combined.
Rehydration increased the sensitivity of the test for colorectalcancer from 80.8 to 92.2 percent and decreased the specificityfrom 97.7 to 90.4 percent (Table 6). With the loss of specificity,the positive predictive value decreased from 5.6 to 2.2 percent.
From the abstracted records for the cases of colorectal cancer,it was determined that in only 1.8 percent of the cases in thecontrol group was the diagnosis made after a positive fecaloccult-blood test, as compared with 49.5 and 38.3 percent ofthose in the annually and biennially screened groups, respectively.
Discussion
This randomized trial demonstrates a significant reduction inmortality from colorectal cancer as a result of screening withfecal occult-blood tests. A 33 percent decline in mortalitywas observed in the annually screened group as compared withthe control group. The 6 percent reduction observed in the bienniallyscreened group, though not statistically significant, was consistentwith the finding in the annually screened group, in that cumulativemortality in the biennially screened group was intermediatebetween that of the annually screened group and the controls.Additional follow-up is necessary to evaluate the efficacy ofscreening every two years.
The survival data were consistent with the mortality data. Survivalwas better in the annually screened group than in the controlgroup. The efficacy of screening was further supported by thefact that patients with disease detected by screening had significantlybetter survival than patients with disease not so detected andby the fact that patients with disease not detected by screeningand controls had similar survival.
Staging of the cancers according to study group yielded resultsconsistent with the mortality rates. There was a significantlyhigher 13-year incidence of Dukes' stage D cancers in the controlgroup than in the screened groups. The reduction in these cancersin the annually screened group as compared with the controlgroup was larger in the current study (48 percent) than thereductions reported to date in the three European trials (10to 38 percent)5,6,7,8,9,10,11,12. The Swedish study, the onlyEuropean study in which slides were rehydrated, had the largestreduction in Dukes' stage D cancers (38 percent)5,6.
There were twice as many stage D cancers in the control groupas in the annually screened group. The detection of a cancerbefore its development into a stage D cancer had a profoundeffect on mortality, since only 2.4 percent of patients withstage D cancers survived five years, whereas for patients withcancers in earlier stages, five-year survival ranged from 94percent for stage A to 57 percent for stage C.
The 37 percent reduction in the incidence of Dukes' stage Dcancers in the biennially screened group, as compared with thecontrol group, did not result in a significant reduction inmortality from colorectal cancer. This may be due to the higherincidence of colorectal cancer and to the higher mortality fromthis cancer in the biennially screened group early in the study,which may have resulted from a chance imbalance in the randomizationprocedure. With continued follow-up, a significant reductionin mortality could emerge. It is not possible to determine theeffect of the three-year hiatus in screening.
Most of the slides were rehydrated, resulting in increased positivitybut also in an increased number of colonoscopies and in decreasedspecificity of the test. The large number of false positiveresults clearly affects the assessment of cost and benefit.During the study, 38 percent of those screened annually and28 percent of those screened biennially had at least one colonoscopy.The increase in positivity resulting from rehydration of theslides and the consequent increase in the use of colonoscopymay have increased the likelihood that nonbleeding cancers inearlier stages would be detected by chance in persons who testedpositive for other reasons. This could partly explain the significantreduction in mortality in the group screened annually, the improvementin survival, and the shift to detection at an earlier stageof cancer. The extensive use of colonoscopy could also havecontributed to the decline in mortality through the removalof polyps. The small differences among the study groups in theincidence of colorectal cancer suggest, however, that polypremoval has not yet contributed substantially to the reductionin mortality. During the first eight years of follow-up, theincidence of colorectal cancer was about the same in all threegroups. During the next five years, the rate of increase inthe cumulative incidence of this cancer was lower in each screenedgroup than in the control group. The effect of polyp removalon the subsequent incidence of cancer may become clearer withadditional follow-up. It is also possible that polyp removalin the screened groups and the expected reduction in the subsequentincidence of cancer were offset by an increased discovery ofcancers through screening. It is, of course, also possible thatin this study the removal of polyps had little or no effecton mortality.
Had there been frequent fecal occult-blood testing performedoutside the protocol in the control group, such testing couldhave diminished the difference in mortality. The small percentage(1.8 percent) of colorectal cancers in the control group thatwere associated with fecal occult-blood testing indicates, however,that these tests had little effect on the results.
Unequal ascertainment of cancers in the study groups could havebiased the results. Because of colonoscopy, there was a higherlikelihood of ascertaining cancers in the patients who werescreened than in the controls. However, the nearly equal incidencerates in the three study groups argue against an ascertainmentbias.
About 22 percent of the patients with colorectal cancer in thescreened groups, but few of those in the control group, weretreated at the University of Minnesota Hospital. A differencein treatment between the university and other hospitals couldhave resulted in a spurious difference in survival. When treatmentprocedures were analyzed according to sex, age, screening group,anatomical location, and Dukes' stage, no significant treatmentdifferences were revealed between study groups28. The possibilityof confounding was addressed by the Cox regression analysis,which showed that age, sex, and place of residence at enrollmentdid not affect mortality from colorectal cancer.
This study demonstrates that a 33 percent reduction in mortalityfrom colorectal cancer can be achieved by annual fecal occult-bloodtesting with rehydrated slides and colonoscopic follow-up inpatients with positive test results. Whether a similar resultcan be attained without rehydration -- that is, with a testof lower sensitivity -- is unknown at this time. The resultwas obtained with an annual screening program (with a three-yearhiatus in screening) during which 10 percent of the screenedgroup did not receive any study screening tests, only 46 percenthad all 11 screening tests, and 17.5 percent of the slides werenot rehydrated. A greater reduction in mortality might be obtainedwith more adherence to protocol.
In the formulation of public health policy for mass screening,cost is important. Fecal occult-blood testing with rehydratedsamples should lead to a fourfold increase in the number ofpositive tests and diagnostic procedures involving colonoscopy.The increase in cost is substantial and will have to be weighedagainst the estimated benefit of a 33 percent reduction in mortalityfrom colorectal cancer.
Supported by research contracts (NIH/N01-CB-95613, N01-CB-61005,and N01-CB-53862) with the National Cancer Institute.
Source Information
From the Divisions of Environmental and Occupational Health (J.S.M., T.R.C.), Epidemiology (L.M.S.), and Biostatistics (F.E.), the School of Public Health; and the Departments of Medicine (J.H.B.) and Laboratory Medicine and Pathology (D.C.S., G.M.B.), the School of Medicine -- all at the University of Minnesota, Minneapolis; and the Emmes Corporation, Potomac, Md. (F.E.). The following persons participated in the study: V. Gilbertsen (deceased), R. McHugh, G. Johnson, G. Watt, M. Geisser, D. Engelhard, S. Williams, and D. Stewart (deceased); Deaths Review Committee -- S. Ewing, D. Plimpton, A. Theologides, and L. Weiland; Policy and Data Monitoring Group -- T. Chalmers, G. Hutchinson, R. Mayer, A.B. Miller, S. Shapiro, W. Taylor, and B. Tilley; National Cancer Institute -- S. Taube, P. Prorok, and I. Masnyk.
Address reprint requests to Dr. Mandel at the Division of Environmental and Occupational Health, School of Public Health, University of Minnesota, Box 807 UMHC, 420 Delaware St., S.E., Minneapolis, MN 55455.
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A correction has been published: N Engl J Med 1993;329(9):672.
