Eivind Strm, MD

John L. Larsen, MD, PhD

Index terms:
Barium enema examination, 75.1281,
75.1282
Colon, neoplasms, 75.321
Colon, radiography, 75.1281,
75.1282
Colonoscopy, 75.129
Efficacy study
Radiology 1999; 211:211214
1

From the Department of Radiology,

University Hospital of Bergen, Haukeland Hospital, N-5021 Norway. Received December 22, 1997; revision
requested March 10, 1998; revision
received August 7; accepted October
26. Supported in part by the legacy of
the Blix family. Address reprint requests to E.S.
r RSNA, 1999

Colon Cancer at Barium Enema

Examination and Colonoscopy:
A Study from the County
of Hordaland, Norway1
PURPOSE: To evaluate the efficacy of barium enema examination as routinely
performed in the detection of colon cancer in the inhabitants of a well-defined and
circumscribed geographic region.
MATERIALS AND METHODS: The study comprised 571 patients with histopathologically verified colon cancer during 19901993 from the county of Hordaland. The
barium enema examination results were reviewed retrospectively.
RESULTS: The correct diagnosis was reached in 351 cases (sensitivity, 90.9%) in 386
tumor locations on the basis of the results of 381 barium enema examinations.
Cancer or an important precancerous lesion was overlooked in 26 cases (6.7%), and
the examination was not feasible in nine cases (2.3%). The correct diagnosis was
reached in 172 cases (sensitivity, 80.0%) in patients with 215 tumor locations on the
basis of the results of 213 colonoscopies. Cancer or an important precancerous lesion
was overlooked in 13 cases (6.0%). The examination was technically not successful
(ie, the affected area was not reached with the scope) in 30 cases (13.9%).
CONCLUSION: Barium enema examination is valuable in the diagnosis of colon
cancer and compares favorably with colonoscopy. The main reason for missed
radiologic diagnosis is failure to observe important lesions visible on the radiographs.

Author contributions:
Guarantors of integrity of entire study,
E.S., J.L.L.; study concepts, J.L.L.; study
design, J.L.L., E.S.; definition of intellectual content, E.S., J.L.L.; literature
research, E.S., J.L.L.; data acquisition
and analysis, E.S.; manuscript preparation, editing, and review, E.S., J.L.L.

Colorectal carcinoma is among the most common cancers in the Western world, and in
Norway it is the second most common in both women and men after breast cancer and
prostate cancer, respectively (1). Despite the increased use of colonoscopy in Norway to
about 27,000 examinations every year, the procedure is outnumbered by the 40,000
barium enema examinations performed (2). Barium enema examination is still the most
important tool used in the detection of colon tumors in Norway, whereas rectal tumors are
diagnosed mainly by means of rectoscopy.
Previous investigations (35) concerning the accuracy of barium enema examination in
the detection of colon neoplasms have shown a wide range of sensitivity and specificity.
Perusal of the pertinent literature demonstrates that this discrepancy may to a large extent
be caused by different selections of the population under study. To reflect the value of
routine barium enema examinations in an unselected population, we performed a
retrospective investigation encompassing diagnostic studies performed during 3 years in
patients with histopathologically certified carcinomas within the county of Hordaland in
western Norway.
The 3-year time span was chosen for practical reasons; older material will not always be
available. The objection could be made that a 3-year interval between the histopathologic
identification of the cancer and the diagnostic examination will mean that the more
rapidly growing tumors will lead to overestimation of the insensitivity of the applied
diagnostic methods. A closer analysis of our material does, however, make this objection
negligible.
Our purpose was to evaluate the efficacy of barium enema examination as routinely performed
in the detection of colon cancer in the inhabitants of a well-defined and circumscribed
geographic region and to compare barium enema examination with colonoscopy in the same
geographic region and explore the reasons for missed radiologic diagnoses.
211

MATERIALS AND METHODS

We received personal identification data
from the National Cancer Registry of
Norway regarding all cases of histopathologically verified cancer of the colon reported in the five hospitals (Haukeland
University Hospital, Bergen; Diakowissehjemmets Hospital Haraldsplass, Bergen;
Stord County Hospital; Voss County Hospital; Odda County Hospital) in the
county of Hordaland, Norway, during the
4 years 19901993. Medical records were
also obtained from two private clinics
(Betanien Hospital, Fyllingsdalen; Bergen
Ro
ntgeninstitutt, Bergen) and one private medical center (Christen J. Bang,
Nesttun). Only patients who had the
diagnosis confirmed by means of histopathologic findings were included in the
study. Suspected but not proved cases
were excluded. The radiologic and the
colonoscopic reports were supplied by
the institutions where the examinations
had been performed.
The region of Hordaland has approximately 430,000 inhabitants, amounting
to one-tenth of the Norwegian population (6). We included only cases with
complete histopathologic and radiologic
or colonoscopic records, with a total of
581 tumors in 571 patients. Ten patients
(five men and five women) had two simultaneous tumors in different locations. We
recorded whether the patients had undergone barium enema examination or colonoscopy within the past 3 years before
the histopathologic diagnosis and the
results of these examinations as stated in
the patients records. The supposed nature of the lesion and its location were
recorded, and the information given was
compared to the final results. Barium
enema examination was performed in
381 patients, and colonoscopy was performed in 213 patients.
The radiographs for all false-negative
radiologic studies were reviewed by two
radiologists (E.S., J.L.L.) who had access
to the surgical findings, histopathologic
findings, and autopsy results. Neither of
these two radiologists had personally examined any of the included patients.
Because the main reason for a falsenegative diagnosis in the barium enema
examinations was missed perception of
an apparent lesion, reexamination of the
radiographs did not lead to interobserver
variation between the authors. In 239 of
the tumor locations, single-contrast
barium enema examinations were performed, and in 147 locations the doublecontrast technique was used.
The age distribution of the patients is
212 Radiology April 1999

TABLE 1
Age Distribution of Patients
Patient Age
Range (y)

No. of Tumors*
(n 581)

3039
4049
5059
6069
7079
8089
9099

5 (0.9)
22 (3.8)
58 (10.0)
143 (24.6)
217 (37.4)
124 (21.3)
12 (2.1)

TABLE 2
Results of Barium Enema
Examinations in 381 Patients with
386 Tumors
Examination Results

No. of Tumors*
(n 386)

Correct diagnosis
Missed cancer
Technically not successful

351 (90.9)
26 (6.7)
9 (2.3)

* Data in parentheses are percentages.

Note.Mean age, 71.1 years; age range,

3194 years.
* Data in parentheses are percentages.

TABLE 3
Distribution of Tumors Diagnosed at
Barium Enema Examination
shown in Table 1. As expected, there was
a marked increase in cancer in the older
age groups. Of the 571 patients, there
were 315 women (55%) and 256 men
(45%).
The barium enema examinations were
performed in one university hospital, four
local hospitals, and two private clinics. In
addition, colonoscopy was performed at
the five hospitals and one private medical
center. This allowed evaluation of the
daily performances of a large number of
physicians. The retrospective approach
provided the opportunity to test the methods as practiced under normal circumstances without interfering with the daily
workload of the departments or inspiring
the diagnosticians to make extraordinary
efforts.

RESULTS
In barium enema examinations in 381
patients, the correct diagnosis was reached
for 351 of 386 tumors (sensitivity, 90.9%
[351 of 386]) (Table 2). Cancer or a precancerous lesion was overlooked in 26 cases
(6.7%). The examination was technically
not possible in nine cases (2.3%), most of
these being caused by the inability of the
patient to cooperate. The distribution of
the tumors is shown in Table 3. Previous
investigators (7) found a redistribution in
the location of colon cancers, with more
malignancies in the proximal part of the
bowel in recent years than in earlier years.
This agrees with our study in which more
than one-third (37.9%) were located in
the cecum, ascending colon, or ileocecal
junction (Table 3). Tumors of the rectum
were not included in the present study.
In colonoscopies in 213 patients with
215 tumors, the correct diagnosis was
reached in 172 cases (sensitivity, 80.0%
[172 of 215]) (Table 4). Cancer or a defi-

Tumor Location
Cecum, ascending colon,
ileocecal junction
Transverse colon with flexures
Descending colon
Sigmoid colon
Rectosigmoid
Polyps, appendix

No. of Tumors*
(n 581)
220 (37.9)
91 (15.7)
34 (5.8)
185 (31.8)
30 (5.2)
21 (3.6)

* Data in parentheses are percentages.

nite precancerous lesion was not found in

13 cases (6.0%), even though the region
of involvement was reportedly reached
by the endoscopist. The examination was
technically not successful (ie, the affected
area was not reached with the scope) in
30 cases (13.9%).
Of the 26 barium enema examinations
in which cancer was overlooked, the radiographs were available for retrospective
evaluation in 23 patients and missing in
three patients (Table 5). Fifteen examinations were double contrast, and 11 were
single contrast. Because 239 of the barium
enema examinations were single contrast
and 147 were double contrast, sensitivities of 95.4% (228 of 239) and 89.8%
(132 of 147), respectively, were found.
Two patients had two tumors each, one of
which was correctly diagnosed and one of
which was overlooked (Table 6).

DISCUSSION
Carcinoma of the colon is a potentially
curable disease, highly dependent on early
diagnosis. It is therefore important to
perform quality controls of the diagnostic methods used and to pinpoint fallacies and institute measures to prevent
them. The present multicenter study reflects the situation in Norway, where raStrm and Larsen

TABLE 4
Results of Colonoscopic Examinations
in 213 Patients with 215 Tumors
Examination Results

No. of Tumors*
(n 215)

Correct diagnosis
Missed cancer
Technically not successful

172 (80.0)
13 (6.0)
30 (13.9)

* Data in parentheses are percentages.

TABLE 5
Barium Enema Examinations with
Overlooked Tumors
Error Type
Perceptive error
Technical error
Combined perceptive and
technical error
Tumor not visualized despite
good technique
Radiographs not available for
reexamination

No. of Tumors
(n 26)
13
5
4
1
3

diologic education and practice is uniform. In conformity with previous

investigators (812), we found perceptive
errors to be the most frequent cause of
false-negative diagnosis.
Because many radiologists in Norway
perform their examinations and interpret
their findings alone, double or triple reading of the radiographs is uncommon.
These methods have been shown to increase the efficacy of barium enema examination substantially (10,11). However, simple arithmetic shows that double
reading of the 40,000 barium enema examinations, each requiring 6 minutes, performed in Norway every year would amount
to 4,000 hours, or approximately the workload of two experienced radiologists.
As Rice (3) points out, it is likely that
there exists a huge discrepancy in quality
between published reports and everyday
practice, at least in the United States in
both academic institutions and private
practice. The design of the present study
was, therefore, retrospective to avoid interference with examination practice and
to reflect the everyday practice of Norwegian radiologists.
Even though double or triple reading is
not usual in Norway, the study demonstrates the high quality of the barium
enema examinations, considering that
this is a study of nonselected investigators or institutions. Especially encouraging is the fact that technical factors alone
Volume 211 Number 1

TABLE 6
Comparison of Techniques for Found and Overlooked Tumors
at Various Locations

Tumor Location

No. of Tumors
Diagnosed at
Barium Enema
Examination
(n 581)

No. of Tumors
Missed at
Barium Enema
Examination
(n 26)

No. of Tumors
Missed at
Colonoscopy
(n 13)

Cecum, ascending colon, ileocecal junction

Transverse colon with flexures
Descending colon
Sigmoid colon
Rectosigmoid
Polyps, appendix

220 (38)
91 (16)
34 (6)
185 (32)
30 (5)
21 (4)

13 (50)
4 (15)
1 (4)
7 (27)
1 (4)
0

6 (46)
2 (15)
0
5 (38)
0
0

Note.Data in parentheses are percentages.

or combined with error of perception

contributed to only nine of the 23 overlooked tumors with radiographs available
(Table 5), demonstrating that the technical training of the radiologists has been
adequate.
It can be argued that a malignant tumor may have developed in the interval
between the barium enema examination
and the detection of the tumor, thus
giving the examination a false low sensitivity. As Table 5 shows, however, 13
patients had radiographs showing a tumor that was not detected at the first
reading. Technical and combined (technical and perceptual) errors in nine patients
had a delay in tumor discovery of 15, 15,
11, 4, 1, 1, 0, 0, and 0 months. The last
four patients of Table 5, one with nonvisualization of the tumor and three with
missing radiographs, had their tumors
discovered 20, 4, 3, and 2 months after
their first barium enema examination. It
is thus likely that no more than four
patients could have possibly developed a
malignant growth during the delay time.
When analyzing the possibility of tumor originating between the barium enema examination and the definitive diagnosis in four cases, we discovered that in
the first case there were 6 months between barium enema examination and a
colonoscopic examination that showed a
3-cm tumor in the sigmoid colon. In the
second case, the time span was 1 month
before a tumor in the descending colon
was discovered at colonoscopy, and the
third case had a time lapse of 15 months
before a repeated barium enema examination showed a polypous tumor in the
cecum. In the fourth case, the patient
underwent surgery 2 days after the barium
enema examination, and in addition to
the originally detected tumor, a cancerous polyp was found in the transverse
colon.

The present study findings support earlier evidence (8,9) that tumors located in
the proximal part of the colon are overlooked more easily than tumors located
in the distal part of the colon. This fact
needs to be emphasized when educating
radiologists.
When evaluating the effects of overlooked tumors, we found that the available data are sparse, but Bolin et al (13)
calculated the doubling time of colon
cancer to be 195620 days. Nevertheless,
a subgroup of colon cancers with a very
rapid growth rate seems to exist (14).
Patients who are clinically suspected of
having cancer and who have negative
barium enema examination or colonoscopic examination results should therefore be reexamined early.
It is not possible for us to make unambiguous comparisons of quality between
the results of double- and single-contrast
barium enema examinations for a variety
of reasons; the two techniques tended to
be used in different patient groups with
distinct clinical problems. In some cases,
a combination of techniques was used,
and double-contrast barium enema examination was used more often in younger, better cleansed, and potentially
healthier patients. In contrast, the usual
routine was to use single-contrast barium
enema examination in older patients, or
in an acute situation, such as when trying
to visualize the cause of an acute obstruction of the large bowel. Neither does the
study allow a randomized comparison of
barium enema examination versus colonoscopy, again owing to different patient
populations, but it does show how the
different methods compare when used in
daily routines.
Regarding colonoscopy, it is important
to stress that an examination in which
the cecum and the ascending colon
are not visualized should be followed

Barium Enema Examination and Colonoscopy: A Study from Norway 213

promptly by a barium enema examination. The fact that most patients suspected of having carcinoma of the colon
find colonoscopy much more disagreeable (15) should also be taken into account when deciding which diagnostic
strategy to follow. Furthermore, the radiographs of the barium enema examination
are available for a second opinion by
another diagnostician if necessary,
whereas colonoscopic examination findings are only subjectively documented.
Barium enema examination involves only
a small risk of perforation (04 cases per
10,000 examinations), whereas this risk is
greater for colonoscopy (1020 cases per
10,000 examinations) (4). The main advantages of colonoscopy are the ability to
remove polyps and perform biopsy of
undetermined lesions. It was previously
thought that most cancers evolved from
polyps, but this theory is now much
disputed (16).
Economic factors should also be taken
into consideration. In Norway, the government pays the main part of the health
expenses, and the prices are low. The cost
of diagnostic colonoscopy in Norway is
NKr 825 (U.S. $110), whereas the fee for a
single- or double-contrast barium enema
examination is NKr 500 (U.S. $65) or NKr
650 (U.S. $85), respectively; the differ-

214 Radiology April 1999

ence in cost between these examinations

is usually greater in other countries. Both
the diagnostic results presented in this
study and economic factors provide a
good case for barium enema examination
as a suitable tool for the diagnosis of
colon cancer. In conclusion, routinely
performed barium enema examinations
are effective in the diagnosis of colon
cancer and can in this respect compete
with colonoscopy. Perceptual errors are
the main cause of misdiagnosis.

8.

9.

10.

11.

Acknowledgment: We thank Sally Tveit for

invaluable help in preparing the manuscript.
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Strm and Larsen