Double Contrast Barium Enema in Crohn’s Disease and Ulcerative Colitis

FREDERICK M.KELVIN,’ TERRENCE A. ODDSON,1 REED P. RICE,1 JOHN T. GARBUTT,2

AND BEN P. BRADENHAM2

Double contrast barium enema examinations in 24 patients Subjects and Methods

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with Crohn’s disease of the colon and 29 patients with ulcera-

Double contrast barium enema examination was performed
tive colitis were reviewed without knowledge of the clinical
on 57 consecutive patients with ulcerative colitis or Crohn’s
diagnosis. The radiologic diagnosis of Crohn’s disease agreed
disease of the colon. Of the 57, 55 patients were evaluated
with the clinical diagnosis in 98% of patients. in this condition
clinically by a consultant gastroenterologist. Four patients were
the most common radiologic findings were discontinuous or
excluded from the series because insufficient clinical or patho-
asymmetric disease (88%) and discrete ulcers (67%) often on
logic data existed to establish a firm diagnosis of either ulcera-
a normal mucosa. The latter are characteristic of early Crohn’s
tive colitis or Crohn’s disease of the colon.
disease and may enable the radiologist to be the first to
The mean age of the 24 males and 29 females was 33.6 years
suggest the diagnosis, particularly when both sigmoidoscopy
(range, 17-59). The mean duration of symptoms was 7.3 years
and small bowel examination are normal. Of the patients with
(range, 2 months to 29 years). Sigmoidoscopy was performed in
ulcerative colitis, a positive radiologic diagnosis was made in
52 patients, colonoscopy in 1 1 and rectal or colonic biopsies in
,
83% on the basis of a granular mucosal pattern (79%) and
32. Six patients had surgical resections of small or large bowel
continuous distal involvement (86%). The high accuracy of the
for inflammatory bowel disease. The presence of colitis second-
double contrast technique, especially In Crohn’s disease, and
ary to specific infection, ischemia, antibiotic administration, or
the relative specificity of the signs that it can demonstrate
diverticular disease was excluded.
suggest that this is the preferred examination in the radiologic
Of the 24 patients with Crohn’s disease, 12 had the classic
evaluation of inflammatory bowel disease.
changes of Crohn’s disease on standard radiographic examina-
tions of the small bowel. Six of these patients had discrete or
linear colonic ulcers visualized by endoscopy. Pathologic con-
Recognition of Crohn’s disease of the colon (granuloma-
firmation of Crohn’s disease was obtained in four patients by
tous colitis) [1 2] rests on combined
, evidence from
examination of resected bowel or suction biopsy.
clinical, pathologic, and radiologic evaluation. Since its
The remaining 12 with Crohn’s disease had radiographically
clinical features are frequently similar to ulcerative coli- normal small bowel. The diagnosis was made on the basis of
tis, considerable emphasis must be placed on the path- endoscopy and biopsy of the large bowel. Ten patients had
ologic and radiologic findings. Pathologic examination discrete or linear ulcers at sigmoidoscopy. Six of these 10
of colons resected for inflammatory bowel disease per- patients and one additional patient with normal sigmoidoscopy
mits differentiation of the two entities in about 90% of underwent diagnostic colonoscopy. Discrete or linear ulcers,
cases [3]. skip areas, and asymmetric colonic inflammation were seen in
Margulis et al. [4] found the conventional barium all seven cases. In this group, one patient subsequently under-
enema less accurate. In their series, only 70% of cases went colectomy with pathologic confirmation of Crohn’s dis-
with Crohn’s disease of the colon and 79% with ulcera- ease, and one patient had characteristic granulomas on colon-
oscopic mucosal biopsy. The remaining patient, who did not
tive colitis were correctly diagnosed on retrospective
have typical endoscopic changes of Crohn’s disease, showed
analysis. More recently the double contrast barium
granulomas on rectal mucosal biopsy.
enema has been advocated by Laufer and colleagues [5- The 29 patients with ulcerative colitis were diagnosed on the
8] for detecting the early changes of Crohn’s disease of basis of the typical endoscopic appearance of a diffusely gran-
the colon and ulcerative colitis. They were able to distin- ular or finely ulcerated rectal mucosa. Rectal or colonic biopsies
guish between the two conditions on radiologic criteria in 18 patients and examination of total colectomy specimens in
in 50 consecutive cases, with complete agreement with two provided pathologic confirmation of the clinical diagnosis.
endoscopic and morphologic findings [8]. The above All 53 patients were examined using the double contrast
two series are not strictly comparable, since most of the barium enema technique. Bowel preparation included a clear
patients in the former had advanced disease resulting in liquiddiet,laxatives(except in cases of very active colitis), and
a cleansing enema or enemas in the radiology department.
colectomy; therefore, the radiologic interpretation was
Polibar (E-Z-Em Co., Westbury, N.Y.), a high density barium,
correlated with the pathologic diagnosis mainly on the was used in all patients. The technique was essentially that
basis of resected colon specimens. This paper reports described by Laufer [7].
our experience and accuracy with the double contrast The double contrast examination of each patient was subse-
technique in differentiating Crohn’s disease of the colon quently reviewed independently by two of us (R. P. Rice and T.
from ulcerative colitis. A. Oddson). Neither radiologist knew the clinical diagnosis.

Received December 20, 1977; accepted after revision March 17,1978.

Presented at the annual meeting of the American Roentgen Ray Society, Boston, September 1977.
‘Department of Radiology, Duke University Medical Center,Durham, North Carolina 27710. Address reprint requests to F. M. Kelvin.
2Department of Medicine, Duke University Medical Center, Durham, North Carolina 27710.

Am J Rontg.nol 131:207-213, August 1978 207 0361 -803X/78/08-0207 $00.00

© 1978 American Roentgen Ray Society
 208 KELVIN ET AL.

TABLE 1 Crohn’s disease, the colonic changes in themselves were

Radiologic Findings specific enough to allow a confident radiologic diagno-
sis.
Radiologic Finding
Ul:rative The average accuracy of radiologic diagnosis of ulcer-
of Colon ative colitis was 83%. All patients in whom the radiologic
Crohn’s disease: . and clinical diagnoses agreed showed evidence of con-
Specific: tinuous involvement (86%), a granular mucosa (79%) or
Discontinuous or asymmetric disease 21(88) .
diffuse rectal disease (79%). The latter two features were
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Discrete ulcers 16 (67) .

seen only in ulcerative colitis.
Transverse stripes 10 (42) .

Longitudinal fissures 7 (29) .

Both radiologists agreed with the clinical diagnosis of
Deep ulcers (3 mm or more) 6 (25) . Crohn’s disease in all patients except one, in whom the
Right sided disease alone 4 (16) . only abnormality was a stricture at the rectosigmoid
Strongly suggestive: junction. In four patients with ulcerative colitis (repre-
Terminal ilealdisease 12 (50) 2 (6)
Cobblestoning 8 (33) 1 (3) senting five radiologic interpretations), the radiologic
Ulcerative colitis: features were nonspecific enough to result in a diagnosis
Specific: of colitis of indeterminate nature. Three other patients
Granular mucosa 23 (79) with ulcerative colitis showed no abnormality on barium
Diftuse rectal disease 23 (79)
enema examination.
Strongly suggestive; continuous
disease 3(12) 25(86)
Nonspecific findings: Discussion
Stricture 15 (63) 8 (27)
It is pertinent to attempt to differentiate between
Pseudopolyps 2(8) 4(14)
Total colitis 2 (8) 4 (14) Crohn’s disease of the colon and ulcerative colitis, since
Note. -Data on 24 patients with Crohn’s disease and 29 with ulcerative colitis. the complications and prognosis of the two conditions
Numbers in parentheses are percentages. differ. For example, the risk of carcinoma of the colon is
considerably greater in ulcerative colitis [9]. Crohn’s
disease tends to show a less satisfactory response to
TABLE 2 medical therapy, is often complicated by the develop-
ment of abscesses and fistulae, and has a high incidence
Accuracy of Radiologic Diagnosis
of postoperative recurrence.
Radiologist Average
Radiologic Diagnosis Accuracy Crohn’s Disease
A B (%)
The changes of Crohn’s disease in the small bowel are
Crohn’s disease:
Correct diagnosis 24 (100) 23 (96) 98 usually characteristic. In this series, only half the patients
Indeterminate colitis . . . 1 (4) . . with Crohn’s disease of the colon had an abnormal small
Ulcerative colitis: bowel follow-through examination. Whereas some re-
Correct diagnosis 25 (86) 23 (79) 83
ports have suggested small bowel involvement to occur
indeterminate colitis 2(7) 3(10.5) . .

Normal 2(7) 3(10.5) . .

in 80% [10] to 100% [1 1] of patients with Crohn’s disease
Note. -Numbers in parentheses are percentages. of the colon, others have found the incidence to be as
low as 41% [12], 43% [4], and 56% [8]. These varying
Radiographic features considered useful in the differential di- incidences probably in part reflect false negative radio-
agnosis of the two conditions were individually assessed by graphic small bowel examinations which have been
both radiologists. Each feature was counted as positive only shown to occur in about 50%-70% of patients who
when both radiologists judged it to be present. Subsequently, a subsequently undergo histologic examination of the
diagnosis of Crohn’s disease of the colon, ulcerative colitis, small bowel [13, 14]. Therefore, it is important to realize
indeterminate colitis, or normal was made by each radiologist. tbe frequency with which the small bowel follow-through
examination appears normal in Crohn’s disease of the
Resufts
colon. In this group of patients, early radiographic diag-
The incidence of the radiographic features and the nosis of the condition may depend on a colon examina-
accuracy of diagnosis are shown in tables 1 and 2. The tion capable of demonstrating fine mucosal changes.
average accuracy of the two radiologists in diagnosing “Aphthoid” or discrete ulcers are among the earliest
Crohn’s disease of the colon was 98%. Every patient with demonstrable mucosal lesions of Crohn’s disease and
Crohn’s disease showed discontinuous or eccentric in- are well known to pathologists [15]. They often occur on
volvement (88%) and/or discrete ulcers (67%). These a background of normal mucosa. Less commonly they
features formed the basis for the radiologic diagnosis. are seen within or at the margins of an area of severe
Other specific but less common signs were transverse disease. These ulcers can frequently be seen en face on
stripes, longitudinal fissures, deep ulcers, and disease double contrast examination as round or oval well de-
limited to the right side of the colon. Although small fined collections of barium, varying in size from one to
bowel reflux with a characteristically abnormal terminal several millimeters (figs. 1 and 2), often with a surround-
ileum was evident on eight of the 24 patients with ing halo (fig. 1). The well defined border corresponds to
 DOUBLE CONTRAST IN INFLAMMATORY COLON DISEASE 209
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Fig. 1. -Crohn’s disease. A, Distal colon with several large discrete ulcers on background of normal mucosa in descending
colon. B,Enlarged view of discrete ulcers demonstrating halo (arrows) surrounding several ulcers.

Fig. 2.-Crohn’s disease. A, Severe stricturing of right colon and pseudodiverticula in transverse colon. Sigmoid and lower
descending colon appear grossly normal. B, Spot film of sigmoid and lower descending colon showing small discrete ulcers
(arrows).

the clearcut margin often seen on endoscopy in Crohn’s two series were they seen in ulcerative colitis. These
disease. It is doubtful whether these discrete ulcers, discrete ulcers may have important therapeutic as well
when small, can be seen on a conventional barium as diagnostic significance because, if left behind at
enema study. In our series they were present in 67% of surgery, they may form the basis for postoperative “re-
patients with Crohn’s disease, a similar incidence to that currence.” In two patients reported by Brahme and
reported by Laufer and Hamilton [8]. In neither of these Wenckert [16], symptoms recurred within 3 months of
 210 KELVIN ET AL.

surgery, and substantial extension of disease at the site

of previously unrecognized small ulcers in the remaining
colon was found on repeat double Contrast examination.
Three patients in our series showed discrete ulcers as
the main or only finding, and in two of these patients the
symptoms were present for less than 3 months. This
leads us to believe that the double contrast technique is
particularly useful in the early stages of Crohn’s disease,
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since the conventional examination cannot be relied on

to show the same degree of detail. Discrete ulcerations
of the colonic mucosa may be seen in other inflammatory
colitides (e.g. , amebic colitis) and should not be consid-
ered pathognomonic of Crohn’s disease. However, since
they are not seen in ulcerative colitis, they are of consid-
erable value in the differential diagnosis of nonspecific
inflammatory bowel disease.
One of the hallmarks of Crohn’s disease is its patchy
distribution. This may manifest itself as discontinuous
lesions along the length of the bowel or in a more
localized fashion as asymmetric involvement of one area
(fig. 3). Occasionally the asymmetric nature of the dis-
ease process results i n pseudodiverticula (fig 24)
. . Dis-
continuous or asymmetric involvement was present in
88% of our patients with Crohn’s disease, representing
the most common abnormality. No patient with ulcera-
tive colitis showed this patchy distribution.
The combination of submucosal swelling and trans-
verse fissuring may result in deep transverse grooves.
These grooves appear on radiological examination as
transverse stripes of contrast medium. They tend to be
crowded together and are straight in outline, in contra-
distinction to haustra which usually have a slight curva-
ture and are generally more widely separated (fig. 4). We
observed transverse stripes in 42% of patients with
Crohn’s disease and did not find them in any patient with
ulcerative colitis. Welin and Welin [17] considered these
transverse stripes to be a pathognomonic sign of Crohn’s
disease. Longitudinal fissures were also seen in our
series (fig. 5), though less frequently (29%).
The depth of the ulcers in inflammatory bowel disease
may be of considerable diagnostic help. Deep ulcers (3
mm or more) were present in 25% of cases with Crohn’s
disease (fig. 5); they were not seen in ulcerative colitis.
Stanley et al. [12] found deep ulcers frequently (66%) in
Crohn’s disease, but in only two of 33 patients with v_.. ,_.._ --------------------. --

ulcerative colitis. This is not surprising since ulcerative few remaining haustra more proximally and distally that have slight but
definite curve. Several pseudodiverticula are also present.
colitis is predominantly a disease involving the mucosa,
in contrast to the transmural nature of Crohn’s disease.
Many authors have used exotic terms to describe the ileum. In contrast to the significance of right-sided co-
shape of colonic ulcers and suggested these varying Ionic disease, changes limited to the distal colon oc-
shapes may have diagnostic significance. Friedland [18] curred in both ulcerative colitis and Crohn’s disease. The
stressed that it is the depth of the ulcers, rather than rectum in Crohn’s disease often appears normal on
their shape, that is important in differentiating the two barium enema. When rectal involvement occurs in this
conditions. condition, it usually manifests itself as discrete ulcers.
The distribution of colonic involvement has been em- These were present on radiologic examination in four of
phasized in the literature. We found, like Margulis et al. our patients.
[4], that disease limited to the right side of the colon Using the conventional barium enema, Margulis et al.
always indicated Crohn’s disease. Patients with involve- [4] found that the individual radiographic signs in
ment of the cecum invariably had disease of the terminal Crohn’s disease of the colon and ulcerative colitis
 DOUBLE CONTRAST IN INFLAMMATORY COLON DISEASE 211
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Fig. 6.-Ulcerative colitis. Diffusely granular mucosa is seen through-

out rectum. Compare with normal mucosa of sigmoid colon.

detection of mild ulcerative colitis. Fennessy et al. [21],

using conventional barium enemas, were unable to di-
agnose, even retrospectively, 18% of patients with mild
disease. Using the double contrast technique, Simpkins
I “e_ and Stevenson [22] failed to detect early changes in only
3.2% of their patients.
Fig. 5.-Crohn’s disease. Deep ulcers are evident in splenic
flexure. Numerous transverse stripes with some longitudinal fis- In two of our patients the rectum appeared entirely
sures (arrows) can be seen in descending colon. Note several normal radiologically, but more proximally there was
discrete ulcers on normal mucosa in sigmoid colon.
diffuse granularity of the colon indicating the presence
of ulcerative colitis. It is important not to be deflected
showed considerable overlap. The frequency and speci- from the diagnosis of ulcerative colitis merely because
ficity of the signs present on double contrast barium the rectum shows no radiologic abnormality. Rectal
enema in our patients with Crohn’s disease explain the sparing on radiologic examination occurred in about
greater accuracy of the technique in this condition. 20% of patients in our as well as other series [4, 9]. All
patients in whom ulcerative colitis was radiologically
Ulcerative Colitis recognized showed continuous disease with uniformly
The earliest colonic change in ulcerative colitis is from diffuse involvement (fig. 7). No patient unequivocally
the normal featureless mucosa to one with a diffusely exhibited the patchy disease that is so characteristic of
fine granular pattern (fig. 6) [19, 20]. The diffuse nature Crohn’s colitis.
of the involvement in the affected area contrasts vividly Pseudopolyps are more common in ulcerative colitis,
with the patchy changes seen in Crohn’s disease. Sig- but may also occur in Crohn’s disease. Their nonspeci-
moidoscopy has shown the fine granular pattern to ficity makes their identification of little diagnostic value.
correspond to an edematous, uneven mucosa without Similarly, the presence of strictures or total colon in-
evidence of gross ulceration. Therefore, the contour of volvement was not markedly different in the two dis-
the colon is smooth at this stage. More severe involve- eases.
ment is radiologically identified by the presence of mar- Of the three patients with ulcerative colitis and a
ginal ulceration. normal barium enema, two were asymptomatic at the
In our series 79% of patients with ulcerative colitis had time of examination and the third had inactive disease at
granular mucosa. Thorough bowel preparation is crucial colonoscopy. Four patients had a barium enema show-
in patients with suspected inflammatory bowel disease, ing changes that were nonspecific. Two of these four
since even a small amount of debris in the colon can patients with ulcerative colitis had proctoscopic evi-
produce a finely granular pattern that may mimic ulcera- dence of mild and limited disease. Problems in the
tive colitis. It is noteworthy that the presence of a diffuse radiologic detection of mild ulcerative colitis or disease
finely granular mucosa is probably not detectable on limited to the rectum fortunately are balanced by the
conventional barium enema study. This may explain the positivity of sigmoidoscopic diagnosis as occurred in all
greater accuracy of the double contrast technique in the our 29 patients. The value of the radiologic examination
 212 KELVIN ET AL.
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Fig. 7.-Ulcerative colitis. A,Continuous disease evidenced by granular mucosal pattern distal to midtransverse colon. B,
Spot film of splenic flexure clearly showing diffusely granular mucosa.

of the colon in ulcerative colitis is more to document the and a granular mucosa suggesting ulcerative colitis
extent, severity, and possible complications of the dis- should be carefully sought. Specific signs in these con-
ease than to establish the diagnosis. ditions seem to be present more frequently when the
One of the major concerns in the evaluation of colitis double contrast technique is used.
has been the safety of performing the double contrast
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