It is estimated that 1 in 20 Americans will develop colorectal cancer (CRC) within their lifetime. As the major determinant of survival of the disease is the stage at which the cancer is discovered, choice and accurate performance of screening tests are paramount. Here, testing scenarios for CRC are discussed, and several screening tests, including the double-contrast barium enema, are evaluated as to their quality, cost-efficiency, and reimbursement status.
is Professor of Clinical Radiology and Clinical Internal Medicine
at the University of Virginia School of Medicine and Co-Director
of the Division of Thoracoabdominal Imaging at the University of
Virginia Health Sciences Center in Charlottesville, VA.
olorectal cancer (CRC) is a lethal disease and is gaining attention
as an important public heath issue. The American Cancer Society
estimates that 129,400 new cases of CRC will occur in the United
States in 1999.
One out of every 20 Americans will develop this cancer within their
CRC is the second leading cause of cancer deaths, exceeded only by
lung cancer. Approximately 56,600 Americans will die of CRC this
year, and well over 6 million Americans alive today will succumb to
A number of risk factors for CRC are well documented.
A genetic predisposition to CRC is present in those persons with a
family history of CRC or adenomas in first degree relatives,
familial adenomatous polyposis (FAP) syndrome, or hereditary
non-polyposis colorectal cancer (HNPCC) syndrome. Individuals who
have a personal history of CRC or adenomatous polyps are at
increased risk of having subsequent colon neoplasms.
Chronic inflammatory bowel disease, especially ulcerative colitis,
places a patient in jeopardy for acquiring CRC. Women who have had
breast, ovarian, or endometrial cancer also may develop CRC as part
of the Lynch II syndrome.
However, to put things in perspective, it should be recognized that
individuals at high and moderate risk make up only a small fraction
of the general population, and 70 to 80% of CRC occurs sporadically
in persons with no known risk factors.
Most CRC develops from adeno-
matous polyps--the well-recognized
An exception to this is found in patients with chronic inflammatory
disease of the large bowel, where a malignancy can develop within
dysplastic mucosa without passing through a polypoid stage.
Although most CRC arises from adenomas, the majority of adenomas do
not become cancers. It is estimated that 95% of all 5-mm diameter
adenomas will remain benign.
Unfortunately, we have no way to identify the one adenoma in 20
that will become malignant. However, we do know that the larger the
polyp, the more likely it is to harbor malignancy (table 1).
An adenomatous polyp which is less than 10 mm in diameter has
approximately a 1.0% chance of containing an invasive carcinoma.
Cancer is found in 5 to 10% of polyps between 1 and 2 cm in size
and in 11 to 46% of polyps over 2 cm in diameter. Based on autopsy
data, the anticipated malignancy conversion rate for large adenomas
is 3% per year.
The major determinant of CRC survival is the stage at which the
cancer is discovered.
A tumor confined to the mucosa (carcinoma-in-situ) has a 100%
5-year survival rate after surgery; the prognosis for survival
becomes progressively worse for patients with a greater depth of
colon wall invasion, local spread to adjacent structures, regional
lymph node involvement, and distant metastases (table 2). Detection
and endoscopic removal of precursor adenomas can prevent CRC, and
early-stage cancer detection can lead to surgical cure.
There are three clinical scenarios in which testing for the
presence of CRC or its precursors may be considered. The first is
diagnostic testing of persons suspected of having CRC or polyps
because of signs or symptoms of the disease. This would include
individuals with documented intestinal bleeding, manifested either
by visible blood per rectum or invisible bleeding detected by a
fecal occult blood test (FOBT). Diagnostic testing also would apply
to persons with unexplained anemia, change in bowel habits, or
weight loss. Secondly, surveillance testing is appropriate for
patients at increased risk of developing CRC because of a personal
history of CRC, polyps, or inflammatory bowel disease, or a strong
family history of CRC or adenomatous polyps. Lastly, the term CRC
screening describes testing in average-risk individuals in the
appropriate age group without signs or symptoms of the disease.
Rationale for screening
The rationale for recommending CRC screening in the asymptomatic
general population is that about 75% of all CRC occurs in people
classified as "average" risk.
This malignancy is a major cause of morbidity and mortality, yet it
is both curable and preventable.
Clinical studies have found that periodic screening and removal of
adenomatous polyps decreases the incidence of CRC, and detection of
early-stage cancers reduces CRC mortality.
Although most cancers develop from adenomas, the malignant
potential of these precursor polyps is low and slow to develop.
Only 5% of 5-mm adenomas become malignant, and it takes a minimum
of 5 years, and an average of 10 years, for a small adenoma to
develop into carcinoma.
The demonstrated stability of most polyps and the generally long
lead time for malignant transformation are reasons for optimism in
determining strategies for detecting and removing precancerous
polyps and early-stage cancers.
Adenomas can be found in approximately 25% of people by age 50
years, and the prevalence increases to 50 to 60% by the age of 80
The incidence of CRC has shown an increase after age 40 and
accelerates sharply after age 50, with 90% of cancers occurring in
persons 50 years of age and older (figure 1).
Thus, a CRC screening strategy should logically begin no later than
50 years of age, and testing should be performed at intervals that
allow timely detection of previously overlooked small polyps, as
well as new lesions, that have enlarged to sizes of 10 mm or
It is projected that universal CRC screening has the potential to
increase the current 5-year survival rate of 63% for whites and 53%
for African Americans to 91% for all Americans.
Sadly, fewer than 20% of American adults currently undergo CRC
There are at least six desirable attributes in any CRC screening
test: 1) it should be widely available and easily accessible; 2) it
should reliably detect premalignant polyps and early-stage cancer,
not just advanced disease; 3) the test should reliably exclude the
presence of the disease in normal individuals; 4) it should produce
minimal discomfort to assure patient acceptance and compliance; 5)
it must have a low risk of serious complications; and 6) the
cost-benefit ratio must seem reasonable to the payer. Four
generally-accepted tests are available for CRC screening: fecal
occult blood test (FOBT), sigmoidoscopy, barium enema, and
colonoscopy. Unfortunately, none of these tests is ideal for
screening average-risk individuals.
Fecal occult blood test
The FOBT is universally available, simple to perform,
noninvasive, very safe, and of relatively low cost. It has been
well documented that FOBT screening achieves a statistically and
clinically significant reduction in death from CRC.
Its biggest drawback, however, is that it is unreliable.
In persons who have positive test results, CRC is found only in 2
to 17%; thus, the large majority of reactive tests are
false-positive. The test also has a high false-negative rate. The
average sensitivity reported for FOBT is in the range of 40 to 60%
for cancers and 5 to 10% for adenomas.
This is due to the intermittent nature, or even absence, of
bleeding from these lesions. In addition, the FOBT has poor patient
compliance, and it does not provide direct structural evaluation of
the large intestine. The general recommendation that the FOBT be
repeated annually is based on the theory that a test of low
sensitivity may be more effective if repeated often.
For those individuals who elect a periodic total colon examination
with colonoscopy or double-contrast barium enema (DCBE), there is
no need for an annual FOBT.
This examination is widely available, minimally invasive,
relatively safe, and only moderately expensive. Sigmoidoscopy is
well tolerated by most individuals, so sedation is not commonly
used. Reports of bowel perforation are rare.
Examination with a flexible 60 cm scope is preferred over a 25 cm
rigid sigmoidoscope because of the greater length of colon that can
be evaluated. Still, the flexible instrument permits visualization
of only about 40% of the large intestine and can be expected to
detect the presence of no more than 40 to 60% of CRC and polyps.
In patients under 50 years of age, this test may be considered
adequate for screening because 75% of polyps will be located in the
rectosigmoid colon. However, as patients grow older, an increasing
number of tumors are located in the more proximal colon and beyond
the reach of the sigmoidoscope (figure 2).
After age 60, a majority of polyps are beyond the reach of the
sigmoidoscope, and this CRC screening strategy is no longer as
effective or cost-effective.
The barium enema and colonoscopy
Colonoscopy and the barium enema are the only currently
available screening tests capable of providing structural
evaluation of the entire colon from the rectum to the cecum. The
American Cancer Society (ACS) terms both procedures "total colon
Although published reports indicate that the air- or
double-contrast barium enema (DCBE) and the single-contrast barium
enema (SCBE) are approximately equivalent in sensitivity for the
diagnosis of colonic cancer and large polyps,
the DCBE is generally considered superior for detection of rectal
lesions and small polyps, making it the radiologic screening
examination of choice.
The SCBE remains useful in selected screening situations, such as
with very elderly and/or immobile patients.
There is voluminous literature comparing DCBE and colonoscopy
for the diagnosis of CRC and polyps, but most reports are
retrospective studies in symptomatic patients or those with rectal
bleeding. There are no published clinical studies specifically
evaluating whether screening DCBE or screening colonoscopy alone
reduces the incidence or mortality from colorectal cancer in people
at average risk for the disease.
For comparative studies, colonoscopy usually is designated as the
"gold standard." This may lead to an overestimation of the
sensitivity of colonoscopy, because all false-negative
colonoscopies are assumed to be true negatives. This comparison
also leads to a bias against the specificity of the DCBE, as all
false-negative colonoscopies are assumed to be false-positive
The best controlled studies comparing colonoscopy and DCBE show
that while colonoscopy detects more small polyps, there is little
difference in the ability of these tests to detect large polyps
(>=10 mm) and cancers. The combined false-positive rate (higher
for DCBE) and rate of inadequate examinations (higher for
colonoscopy) are about the same for the two procedures.
is likely correct in commenting that the "barium enema is neither
as good as radiologists claim nor as bad as endoscopists believe.
Colonoscopy is neither as good as endoscopists claim nor as bad as
In the best hands, both colonoscopy and DCBE are reported to
have a sensitivity of about 90% for detection of clinically
significant polyps and CRC.
However, both tests are operator dependent, and this level of
lesion detection is unlikely to be achieved in clinical practice
except by experts under ideal circumstances. Results from the
studies with the fewest biases suggest that the sensitivity of the
DCBE is between 50 and 80% for polyps of less than 10 mm, 70 and
90% for polyps greater than 10 mm, and about 90% for CRC.
Studies using the barium enema as the gold standard consistently
show that colonoscopy misses about 10 to 20% of confirmed lesions
detected by barium enema.
Studies using same day back-to-back colonoscopy as a gold standard
show a miss rate for colonoscopy of 16 to 27% for polyps of 5 mm in
diameter or less, 12 to 13% for polyps of 6 to 9 mm, and up to 6%
for polyps measuring 10 mm or greater.
While colonoscopy generally is considered superior to DCBE for
detection of polyps of less than 6 mm in size, the rate of
colonoscopic perforation is greater than the low incidence of
malignancy in these small polyps; thus, the need to detect such
small polyps has been seriously questioned.
Why do colonoscopy and DCBE fail to diagnose some colorectal
tumors? During colonoscopy, undetected lesions usually are missed
either because the tumor site is not reached or the lesion is
passed by the scope but not identified by the endoscopist. A
prospective survey study done in 1984 by the American Society of
Gastrointestinal Endoscopy showed that 26% of colonoscopies
performed by the 672 responding society members were incomplete.
Other studies report failure to reach the cecum in anywhere from 5
to 45%, with operator experience and newer scope designs being
significant factors in attaining the higher rates of success.
Other causes of incomplete colonoscopy are poor bowel cleansing,
excessive bowel redundancy, benign or malignant stricture, and
severe diverticulosis (figure 3). Because the right colon
frequently harbors polyps and cancers, incomplete studies require
that either a repeat colonoscopy or a barium enema be performed
When lesions are passed but not detected by colonoscopy, it usually
is because the lesion was hidden behind a fold, particularly on the
inside of a tight turn, such as that which occurs at colonic
flexures (figure 5).
Conversely, a barium enema rarely fails to reach the cecum and
allow complete colon evaluation. When carcinomas are missed on a
DCBE, the lesions are visible about 90% of the time on
retrospective review of the films; thus, a technical problem or
perceptive error by the radiologist usually is responsible for
failure to report the lesion or properly interpret its nature.
Because human error is a frequent cause of failure to make a
correct diagnosis, it has been postulated that performing
double-reading of barium enema examinations could raise the
diagnostic sensitivity of the study, possibly to as high as 94%.
Both colonoscopy and DCBE are painful or, at best, uncomfortable
procedures. It is not clear which is more acceptable to patients.
Medications to provide analgesia, sedation, and amnesia are
regularly given during colonoscopy but are rarely used during
barium enema studies. Because of the delayed amnestic effect of
drugs like medazolam (Versed, Roche Laboratories, Nutley NJ), it is
not surprising that patients surveyed several weeks after
undergoing the two procedures recall that they found the procedures
to be equally well tolerated or that they preferred colonoscopy.
The reverse is true when patients are questioned immediately
following the two procedures, as was done in a randomized study by
Stein of 190 patients agreeing to undergo CRC screening by both
When her patients were questioned immediately afterwards, moderate
to severe pain was reported by 85% of individuals during
colonoscopy and by 46% during DCBE. The intensity of the pain on a
scale of 1 to 10 (nonesevere) was 6.0 for colonoscopy and 3.4 for
DCBE. The length of time that the patients experienced pain was
related to the length of the procedure, which averaged 31 minutes
for colonoscopy and 14 minutes for DCBE.
Serious complications as a result of colonoscopy or DCBE are
infrequent. However, perforation is 10 to 90 times more common
during colonoscopy (1:500 to 1:1000) than during DCBE (1:10,000 to
Fatalities are 100 to 200 times more frequent with colonoscopy
(1:5000 to 1:10,000) than with DCBE (1:1,000,000).
In addition, with colonoscopy, reports indicate that 3:1000 have
major hemorrhage and 5:1000 experience clinically significant
The radiation dose received by an individual during barium enema
examination has been of concern to many patients and physicians. In
reality, the dose is relatively small. During a barium enema,
patients are exposed to 300 to 500 mrem, which compares to a
radiation dose of 300 mrem during mammography. Considering the age
and frequency at which screening is commonly recommended, a CRC
screening strategy using barium enema every 5 to 10 years would
deliver a lifetime dose that is considerably lower than that for
annual screening mammography. There is no direct evidence that
barium enema examinations cause clinically important increases in
the risk of cancer or other tissue damage.
Little attention has been paid to the potential for disease
transmission between patients from fecal contamination of
instruments. The U.S. Food and Drug Administration and three state
health departments found that 24% of fiber-optic endoscopes
harbored a significant number of viable bacteria after they had
undergone routine disinfection. As a result, they report that
"outbreaks with substantial morbidity and mortality have occurred."
Other scattered reports in the literature have described minor
epidemics caused by contaminated endoscopes.
To our knowledge, no studies have investigated the potential for
viral transmission by contaminated endoscopes. Conversely, with
barium enemas, disease transmission by instruments is not an issue,
as only disposable administration sets and contrast media are used
to perform the examination.
With the current focus on cost containment in medical care, it
is important to appreciate that colonoscopy is much more expensive
than DCBE: In most reported series, colonoscopy is 3 to 5 times
more costly. In performing CRC screening of large populations, this
cost differential is multiplied and becomes enormous. Also
contributing to the economic impact of colonoscopy is the fact that
the patient must have a recovery period of 1 to 2 hours following
the administration of conscious sedation and can not immediately
drive an automobile or return to work following the procedure.
Because of a lack of large clinical trials comparing CRC
screening tests in an average-risk population, computer models have
been used to evaluate the cost-effectiveness of the four common
screening tests: FOBT, flexible sigmoidoscopy, DCBE, and
colonoscopy. Data largely derived from studies in symptomatic
patients have been extrapolated to predict the most effective
screening strategies for asymptomatic subjects.
After review of the applicable literature, Eddy discovered that
the most cost-effective way to decrease the death rate from cancer
is to perform a barium enema every 3 to 5 years (figure 6);
slightly less cost-effective was colono-scopy performed every 5
years. Eddy found that more frequent testing was more costly and
was ineffective in saving additional lives.
In 1995, the Congressional Office of Technology Assessment
published a comprehensive study which found that all four of the
CRC screening strategies offer health benefits at a price
considerably less than the benchmark value--roughly $40,000 per
added year of life--commonly applied to preventive technologies.
Despite using an assumption that the sensitivity of DCBE for polyps
and cancer is only 70% in an average-risk screening population,
they found that DCBE and colonoscopy are comparably cost-effective
screening strategies at both 5-year and 10-year intervals (figure
In 1997, an expert panel convened by the United States Agency
for Health Care Policy and Research concluded from computer
simulations that a screening barium enema every 5 years and
screening colonoscopy every 10 years are approximately equivalent
in the ability to save lives. In 1998, Glick et al reported the
results of another computer model, also using a conservative
assumption of 70% sensitivity for detection of polyps and cancer by
DCBE compared to a liberal assumption of 90% sensitivity for
colonoscopy. Despite this, their data also indicate that the DCBE
is comparatively cost-effective as a screening procedure in
All four of the above mentioned studies observed that screening
sigmoidoscopy alone (at any interval) is less effective that the
other screening strategies. It should be noted, however, that all
of the commonly recommended strategies for CRC screening are more
cost-effective than breast cancer screening with mammography and
cervical cancer screening using the Papanicolaou technique.
The American Cancer Society, American Gastroenterological
Association, American College of Physicians, American College of
Gastroenterology, American Society of Colon and Rectal Surgeons,
American Society for Gastrointestinal Endoscopy, American College
of Radiology (ACR), American Medical Association, and others are
promoting CRC screening and the use of the DCBE as a primary
screening tool in average-risk individuals.
Most of their current recommendations are based on a landmark
article in 1997 by Winawer et al, which established guidelines and
rationale for CRC screening.
The highly respected and frequently quoted ACS guidelines are
rather complex because they are tailored to the risk potential of
each patient group; however, their recommendations are
straightforward for the estimated 70 to 80% of the population who
are at average risk (table 3).
Recently, the potential for universal CRC screening was greatly
enhanced with the approval of Medicare coverage for such screening
tests. Medicare payment was authorized by enactment of The Balanced
Budget Act of 1997;
the details of Medicare coverage were left to the Secretary of
Health and Human Services to define and were published in The
Medicare payment for CRC screening was implemented on January 1,
1998. Currently, the Healthcare Financing Administration (HCFA) is
allowing Medicare coverage of CRC screening for persons aged 50
years and older (table 4). Under their rules, FOBT can be performed
annually, and for average risk individuals, DCBE or sigmoidoscopy
can be performed every 4 years. For high-risk individuals, DCBE or
colonoscopy can be performed every 2 years.
Colonoscopy has not been approved for CRC screening in the
general population due to its higher risk of morbidity and
mortality and its much greater cost.
One would expect that Medicare payment for CRC screening would
stimulate an increase in the number of barium enemas being
performed in this country. However, in the year since the
government authorized Medicare coverage for this service, many, if
not most radiologists have seen no evidence of a jump in the volume
of these studies. Instead, there has actually been a steady decline
in the number of barium enemas performed in this country for the
last 15 years, with a commensurate increase in the number of
What is wrong? One obvious answer is that radiologists have been
much less interested and effective in educating the public and
referring physicians about the benefits of the DCBE than have the
endoscopists regarding colonoscopy. In addition, many radiologists
have focused their attention on mastering newer technologies. As a
result, the quality of barium enema examinations has reportedly
become inconsistent, and many referring physicians have lost
confidence in the value of the examination. If the barium enema is
to be utilized for CRC screening, individual radiologists must
rededicate themselves to improving the quality of the study and
convince their colleagues that it is an effective technique.
Standards and quality control
To improve the uniformity and quality of barium enema
examinations, the American College of Radiology (ACR) has developed
performance standards for these studies.
The standards include: 1) appropriate training/certification of
radiologists and radiologic technologists, 2) equipment standards
and quality control procedures to maintain high-quality
fluoroscopic and radiographic images, 3) effective bowel
preparation to achieve a clean colon, and 4) strict quality control
during the examination using a barium suspension specifically
designed for the procedure, introducing an adequate volume of the
contrast agent(s) to achieve complete colon examination, and using
optimal patient positioning and radiographic technique for film
documentation. The ACR quality controls specific to the DCBE are:
1) complete barium coating of the entire colon, 2) good distension
of the colon with gas, and 3) demonstration of every segment of the
colon in double contrast on at least two radiographs taken in
different positions. The ACR also has developed a Barium Enema
Quality Control Manual to help facilities establish and maintain a
quality control program.
This manual, published in 1998, follows the highly successful
manual on mammography quality control, first published by the ACR
Dr. Richard Mendelson, an Australian radiologist, expressed
clearly the challenge that faces radiologists worldwide when he
wrote, "The DCBE remains a potentially useful tool...but its
continued existence and accuracy are highly dependent on adherence
to strict quality control issues....There needs to be an acceptance
by radiologists that good-quality barium radiology is a challenge
and a goal to be strived for and that gastrointestinal (GI)
radiology is a valid subspecialty."
As new approaches to CRC screening--with blood and stool tumor
markers or new imaging modalities such as CT and MR
colonography--come to market, screening strategies will undoubtedly
change. For the present, however, DCBE has been established as a
safe, accurate, cost-effective, and widely-available total colon
examination. Radiologists are obliged to perform the procedure well
and educate patients and medical colleagues about the advantages of
DCBE as a primary screening test for colorectal cancer and polyps.
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