ARTICLES |
Colorectal Cancer Mortality: Effectiveness of Biennial Screening for Fecal Occult Blood
Jack S. Mandel,
Timothy R. Church,
Fred Ederer,
John H. Bond
Affiliations of authors: J. S. Mandel, T. R. Church,
Division of Environmental and Occupational Health, School of Public
Health, University of Minnesota, Minneapolis; F. Ederer, Division of
Biostatistics, School of Public Health, University of Minnesota, and
The EMMES Corporation, Potomac, MD; J. H. Bond, Department of
Medicine, University of Minnesota, and Minneapolis Veterans Affairs
Medical Center.
Correspondence to: Jack S. Mandel, Ph.D., M.P.H., Division of Environmental
and Occupational Health, School of Public Health, University of Minnesota, Box 807 Mayo, 420
Delaware St., S.E., Minneapolis, MN 55455 (e-mail: jmandel{at}cccs.umn.edu).
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ABSTRACT
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BACKGROUND: In 1993, a randomized controlled trial in Minnesota showed, after 13 years
of follow-up, that annual fecal occult blood testing was effective in reducing colorectal cancer
mortality by at least 33%. Biennial screening (i.e., every 2 years) resulted in only a
6% mortality reduction. Two European trials (in England andin Denmark) subsequently
showed statistically significant 15% and 18% mortality reductions with biennial
screening. Herein, we provide updated results through 18 years of follow-up
from the Minnesota trial that address the apparent inconsistent findings among the trials
regarding biennial screening. METHODS: From 1976 through 1977, a total of
46 551 study subjects, aged 50-80 years, were recruited and randomly assigned to an
annual screen, a biennial screen, or a control group. A screen consisted of six guaiac-impregnated
fecal occult blood tests (Hemoccult®) prepared in pairs from each of three consecutive fecal
samples. Participants with at least one of the six tests that were positive were invited for a
diagnostic examination that included colonoscopy. All participants were followed annually to
ascertain incident colorectal cancers and deaths. RESULTS: The numbers of deaths from all
causes were similar among the three study groups. Cumulative 18-year colorectal cancer
mortality was 33% lower in the annual group than in the control group (rate ratio, 0.67;
95% confidence interval [CI] =0.51-0.83). The biennial group had a
21% lower colorectal cancer mortality rate than the control group (rate ratio, 0.79;
95% CI =0.62-0.97). A marked reduction was also noted in the incidence of
Dukes' stage D cancers in both screened groups in comparison with the control group.
CONCLUSION: The results from this study, together with the other two published
randomized trials of fecal occult blood screening, are consistent in demonstrating a substantial,
statistically significant reduction in colorectal cancer mortality from biennial screening.
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INTRODUCTION
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Screening for fecal occult blood statistically significantly
reduces colorectal cancer mortality. In 1993, the Minnesota Colon
Cancer Control Study, a randomized controlled clinical trial, showed
that after 13 years of follow-up, annual fecal occult blood testing
reduced colorectal cancer mortality by at least 33%, a result that
was statistically significant (1). Subsequently, two published
trials (2,3) in England and Denmark showed statistically
significant mortality reductions of 15% and 18% from biennial
(every 2 years) fecal occult blood testing. These results were obtained
despite only about 50% compliance with screening and screening
positivity rates of less than 2%. The Minnesota trial also
evaluated biennial screening. In 1993, when the first results were
published, the cumulative colorectal cancer mortality rate in the
biennial group was only 6% lower than in the control group, an
anomalous result thought to have resulted from a chance excess in the
early years of the trial in colorectal cancer mortality in the biennial
group relative to the control group. Although screening ended in 1992,
the cohort has continued to be followed to ascertain new colorectal
cancer cases and deaths. This article presents an update of colorectal
cancer mortality through 18 years of follow-up.
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METHODS
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Detailed descriptions of the study design have already been published (1,4-7). Briefly, during the period from 1976 through 1977, 46 551 men and
women aged 50-80 years were recruited from Minnesota and randomly assigned, with
stratification by age, sex, and residence, to annual screening, biennial screening, or a control
(usual care) group. Participants in the screened groups were asked to prepare six
guaiac-impregnated Hemoccult® (SmithKline Diagnostics, Palo Alto, CA) slides from
samples obtained in pairs from each of three consecutive fecal samples. The slides were mailed
for processing to a central laboratory; except for the initial 3 years of screening, the slides were
rehydrated with a drop of deionized water prior to adding the reagent. Rehydration resulted in
increased positivity and sensitivity (7). Individuals with one or more
positive slides out of a set of six were invited to the University of Minnesota for a diagnostic
work-up that included colonoscopy. If colonoscopy was incomplete, a double-contrast barium
enema was performed. This study was approved by the University of Minnesota Committee on
the Use of Human Subjects in Research in accordance with U.S. Department of Health and
Human Services assurance that written informed consent was obtained from every study
participant.
The study was initially designed with a 5-year screening period during which five annual screens
and three biennial screens were to be completed. The screening began in February 1976 and was
completed by December 1982 (phase I). During the subsequent follow-up phase, it became
apparent that the death rate in the control group was considerably lower than expected due to a
large healthy volunteer effect (8,9). This led to a recommendation from
the study's Policy and Data Monitoring Group to reinstitute screening. A second phase of
screening began in February 1986 and concluded in February 1992 (phase II). As a result of the
hiatus between phases, screen group participants had an interval ranging from 3 to 5 years
between the end of the last screening interval of phase I and the first screen attempt of phase II.
Because subjects were randomly assigned over a 2-year period, the hiatus between phases varied
from individual to individual. Furthermore, because phase I consisted of five 1-year screening
intervals for the annual group and three 2-year screening intervals for the biennial group, the
average hiatus duration in the annual group was about a year longer than in the biennial group. In
all, 11 screens were offered to the annual group and six to the biennial group.
Throughout the study, participants were mailed an annual questionnaire to ascertain colorectal
cancer cases among all control group participants, among those screened group participants not
taking part in the screening program, and among those diagnosed with the disease between
screens (interval cases). The questionnaire also served to identify participants who died since last
contact.
Colorectal cancer cases reported in the annual survey have been processed through a validation
procedure that included a review of medical and hospital records to verify the diagnosis. A tissue
specimen has been obtained and reviewed by the study pathologists to verify the diagnosis and, if
colorectal cancer, to classify the stage of cancer according to Dukes' (10,11). To determine the underlying cause of death, a Deaths Review Committee
reviewed, without knowledge of study group assignment, all autopsy reports and the medical and
hospital records of all decedents in whom gastrointestinal disease was known or suspected to be
present at the time of death (12). Since screening ended in 1992, the
cohort has continued to be followed by the annual survey to ascertain colorectal cancer incident
cases and deaths.
Mortality data were analyzed in the same manner as in Mandel et al. (1),
with the exception that no further adjustment for group-sequential monitoring was done since
analysis of the 13-year follow-up results. Cumulative estimates of mortality from colorectal
cancer at the end of each follow-up year were made with the life table technique, with deaths
from other causes censored (13,14). Because sequential monitoring ended
in 1992, the 95% confidence intervals (CIs) on 18-year cumulative mortality rates were
not adjusted for the earlier group-sequential analyses and are thus nominal for the 95%
confidence coefficients. Since these intervals are given for the purpose of estimation and not
hypothesis testing, no further adjustment is necessary. It is expected that with further follow-up,
the width of CIs will continue to decrease.
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RESULTS
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During the screening intervals (from 1976 through 1982 and from 1986
through 1992), about one million Hemoccult® tests were processed.
Compliance with annual and biennial screening averaged 75% and
78% per screen, respectively (15).
Ninety-five percent of the participants with a positive screen received diagnostic follow-up.
Eighty-three percent of the positive screens in the annual group and 84% in the biennial
group underwent a complete large bowel examination consisting of colonoscopy or
double-contrast barium enema and flexible sigmoidoscopy. Some of the others had a flexible
sigmoidoscopy or a barium enema or submitted another fecal occult blood test. Five percent of
the participants declined to consult a physician. The annual screen group participants had an
average of 3.7 screens in phase I and 4.0 screens in phase II; biennial screen group participants
had an average of 2.3 and 2.1 screens per phase. The mean hiatus between phases was 4.48 years
for annual group participants and 3.65 years for the biennial group participants, a difference of
0.83 years.
Follow-up for vital status through year 18 was complete for 88.8%, 89.1%, and
88.5% of annual, biennial, and control group participants, respectively. Death certificates
were obtained for 99.7%, 99.8%, and 99.8% of known decedents in the three
groups, respectively. Through 18 years of follow-up, there were 717 908 total
person-years of observation, approximately equally divided among the three study groups (Table
1).
There have been 15 635 deaths, representing about one third
of the study cohort. Colorectal cancers account for 2.9% of the deaths.
As expected, the cumulative rates of death from all causes were the same in the three study
groups, 342, 340, and 343 per 1000 population in the annual, biennial, and control groups,
respectively. There were no notable differences in any major cause of death categories (Table 2).
However, there was a statistically significant deficit of colorectal cancer
deaths in each screened group relative to the control group (Table 1).
The
cumulative colorectal cancer mortality rate in the annual group was 33% lower than in the
control group (rate ratio, 0.67; 95% CI = 0.51-0.83). The biennial group had a
21% lower colorectal cancer mortality rate than the control group (rate ratio, 0.79;
95% CI = 0.62-0.97). Early in the study, the cumulative colorectal cancer mortality
was greater in the biennial than in the control group (Fig. 1).
The trend
was reversed by the 11th year of follow-up and resulted in a 21% cumulative reduction by
year 18.

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Fig. 1. Cumulative mortality by years since randomization (time
on study) for each randomization group (annual, biennial, and control),
with the bars at 4, 8, 13, and 18 years representing 95% confidence
intervals. Early in the study, cumulative colorectal cancer mortality
was greater in the biennial group than in the control group. The trend
was reversed by the 11th year of follow-up and resulted in a 21%
reduction by year 18.
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A total of 1292 adenocarcinomas of the colon and rectum were diagnosed and validated over the
18-year period. A notable feature of the distribution of these cancers by stage is the incidence of
Dukes' stage D cancer among the study groups (Fig. 2).
Because
the 5-year survival rate for Dukes' stage D cancer was only 2.5% compared with
94.3%, 84.4%, and 56.6% for stages A, B, and C, respectively, stage D
cancers contribute substantially to the number of colorectal cancer deaths. The annual and
biennial screening groups, respectively, had 47% and 32% fewer Dukes'
stage D cancers than the control group. This pattern was also observed in the 13-year analysis, for
which we reported a 48% and 37% reduction in Dukes' stage D cancer in the
two screened groups compared with the control group (1). Between years
13 and 18, when little screening was offered by the study, the percent reduction in Dukes'
stage D cancer was 33% and 15%, respectively, for the annual and biennial groups
relative to the control group.

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Fig. 2. Cumulative 18-year incidence rate per 1000 by Dukes'
stage (10) of cancer and study group for all cases of
colorectal cancer. A total of 1292 adenocarcinomas of the colon and
rectum were diagnosed and validated over the 18-year period. A notable
feature of the distribution of these cancers by stage is the incidence
of Dukes' stage D among the study groups. Because the 5-year survival
rate for Dukes' stage D cancer was only 2.5% compared with
94.3%, 84.4%, and 56.6% for stages A, B, and C,
respectively, stage D cancers contribute substantially to the number of
colorectal cancer deaths. The annual and biennial screening groups,
respectively, had 47% and 32% fewer Dukes' stage D cancers
than the control group.
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DISCUSSION
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At the end of 13 years, we reported that the cumulative colorectal
cancer mortality rate was only 6% lower in the biennial group
relative to the control group (1). This appeared to be
inconsistent with the large benefit found for annual screening and the
37% reduction in Dukes' D stage cancers in the biennial group
compared with the control group. At the time, we stated that the higher
colorectal cancer mortality rate in the biennial group compared with
the control group in the early years of the study was probably due to
chance and that additional follow-up might lead to a statistically
significant reduction in mortality. This has proven to be the case.
Despite the higher colorectal cancer death rate early in the study, the
biennial group, through 18 years of follow-up, shows a statistically
significant 21% colorectal cancer mortality reduction from the
control group. This result is more consistent with the reduction in
Dukes' D stage cancers observed earlier (1).
Lang and Ransohoff (16) proposed that between 35% and
54% of colorectal cancer deaths prevented in the Minnesota trial resulted from the chance
detection of nonbleeding cancers by colonoscopy. In a subsequent paper, Ederer et al. (17) using the Lang-Ransohoff model, but with actual rather than
estimated data from the Minnesota trial, showed that only between 16% and 25% of
the mortality reduction was due to chance detection. The remainder, 75%-84%, was
due to sensitive detection by fecal occult blood testing.
Two European randomized trials (2,3) have also found statistically
significant colorectal cancer mortality reductions from biennial screening with Hemoccult®.
The Nottingham trial (2), involving 152 850 participants
randomly assigned to biennial screening or a control group, evaluated a nonrehydrated
Hemoccult® test with a relatively low positivity rate (2.1% on first screen and
1.2% on the three to six subsequent screens) and a low sensitivity (53.6%) but high
specificity (98%) for cancer. This trial, despite low compliance with screening (about
50%) and relatively short follow-up (median, 7.8 years), reported a statistically significant
15% mortality reduction.
The Funen trial (3), involving 61 933 participants, found a
statistically significant 18% mortality reduction. This trial also evaluated biennial
screening with a nonrehydrated Hemoccult® test (3). The positivity
rate was 1% on the first screen and ranged from 0.8% to 1.8% on the four
subsequent screens. Sensitivity of the test was 51% and specificity was 99%.
Compliance with each of the five screens averaged about 56% and average follow-up was
10 years.
Three important conclusions emerge from the results of these three randomized controlled trials
involving more than 250 000 participants. First, the results published to date are
consistent in showing a statistically significant colorectal cancer mortality reduction from
biennial screening. The differences in magnitude of the reduction, which ranged from 15%
to 21%, may be due to differences in the characteristics of the trials, such as compliance,
positivity, test sensitivity, and length of follow-up, or due to chance. Second, the actual benefit to
those who comply with screening for fecal occult blood is likely greater than 33% and
21% for annual and biennial screening with rehydrated Hemoccult® and greater than
15%-18% for biennial screening with nonrehydrated Hemoccult® tests. The
observed mortality reduction in the three randomized trials is diluted by noncompliance with
screening in the screened groups and contamination by screening in the control group and
diminished by the hiatus in screening in the Minnesota trial and the relatively short follow-up
periods (8 and 10 years) in the European trials. Third, both annual testing and biennial testing for
fecal occult blood are effective methods for statistically significantly reducing colorectal cancer
mortality, with the benefit from annual screening appearing to be greater than for biennial
screening.
It has been suggested that the results of the European trials have greater external validity than the
Minnesota trial because, unlike the Minnesota trial, which enrolled volunteers, these studies
randomly assigned all eligible members of the population to the screen or control groups, seeking
consent only from the screening group, but including the experience of all individuals
irrespective of group assignment or consent (3). Compliance is usually
lower in an unselected population than in volunteers. However, the low compliance with
screening in the European trials may not represent future compliance, in that the individuals
solicited for the trials did not have the incentive of knowing that screening would prove to be
effective in reducing colorectal cancer mortality. Now that there is definitive evidence of the
effectiveness of screening, compliance with screening might improve as public health education
programs are implemented. The challenge is to develop effective strategies to increase screening
rates in the average-risk population.
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NOTES
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Supported by Public Health Service (PHS) contracts N01CB95613, N01CB61005, and
N01CB53862 and by PHS grant R01CA65728 from the National Cancer Institute, National
Institutes of Health, Department of Health and Human Services; and by a cooperative agreement
from the Centers for Disease Control and Prevention through the Association of Schools of
Public Health.
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