Double
Contrast
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FREDERICK
Barium M.KELVIN,’
Enema TERRENCE AND
in Crohn’s
Disease
A. ODDSON,1 REED BEN P. BRADENHAM2
Double contrast barium enema examinations in 24 patients with Crohn’s disease of the colon and 29 patients with ulcerative colitis were reviewed without knowledge of the clinical diagnosis. The radiologic diagnosis of Crohn’s disease agreed with the clinical diagnosis in 98% of patients. in this condition the most common radiologic findings were discontinuous or asymmetric disease (88%) and discrete ulcers (67%) often on a normal mucosa. The latter are characteristic of early Crohn’s disease and may enable the radiologist to be the first to suggest the diagnosis, particularly when both sigmoidoscopy and small bowel examination are normal. Of the patients with ulcerative colitis, a positive radiologic diagnosis was made in 83% on the basis of a granular mucosal pattern (79%) and continuous distal involvement (86%). The high accuracy of the double contrast technique, especially In Crohn’s disease, and the relative specificity of the signs that it can demonstrate suggest that this is the preferred examination in the radiologic evaluation of inflammatory bowel disease.
Double
P. RICE,1
August 1978
Ray Society
and
barium
enema
Methods
examination
logic
by a consultant gastroenterologist. from the series because insufficient
was performed
data
existed
to establish
a firm
Four patients were clinical or patho-
diagnosis
of either
ulcera-
tive colitis or Crohn’s disease of the colon. The mean age of the 24 males and 29 females was 33.6 years (range, 17-59). The mean duration of symptoms was 7.3 years (range, 2 months to 29 years). Sigmoidoscopy was performed in 52 patients, colonoscopy in 1 1 and rectal or colonic biopsies in 32. Six patients had surgical resections of small or large bowel ,
for inflammatory
ary to specific diverticular
bowel
disease.
infection,
disease
The presence
ischemia,
antibiotic
of colitis
second-
administration,
or
was excluded.
Of the 24 patients with Crohn’s disease, 12 had the classic changes of Crohn’s disease on standard radiographic examinations of the small bowel. Six of these patients had discrete or linear colonic ulcers visualized by endoscopy. Pathologic confirmation of Crohn’s disease was obtained in four patients by
examination of resected bowel or suction biopsy. The remaining 12 with Crohn’s disease had radiographically normal
small
bowel.
The
diagnosis
was
made
on the
basis
of
endoscopy and biopsy of the large bowel. Ten patients had discrete or linear ulcers at sigmoidoscopy. Six of these 10 patients and one additional patient with normal sigmoidoscopy underwent skip areas,
diagnostic colonoscopy. and asymmetric colonic
Discrete or linear inflammation were
ulcers, seen in
all seven cases. In this group, one patient subsequently underwent colectomy with pathologic confirmation of Crohn’s disease, and one patient had characteristic granulomas on colonoscopic mucosal biopsy. The remaining patient, who did not have typical endoscopic changes of Crohn’s disease, showed granulomas on rectal mucosal biopsy. The 29 patients with ulcerative colitis were diagnosed on the basis of the typical endoscopic appearance of a diffusely granular or finely ulcerated rectal mucosa. Rectal or colonic biopsies in 18 patients and examination of total colectomy specimens in two provided pathologic confirmation of the clinical diagnosis. All 53 patients were examined using the double contrast barium enema technique. Bowel preparation included a clear liquiddiet,laxatives(except in cases of very active colitis), and a cleansing enema or enemas in the radiology department. Polibar (E-Z-Em Co., Westbury, N.Y.), a high density barium, was used in all patients. The technique was essentially that described by Laufer [7]. The double contrast examination of each patient was subsequently reviewed independently by two of us (R. P. Rice and T. 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 ‘Department of Radiology, Duke University Medical Center,Durham, North Carolina 27710. 2Department of Medicine, Duke University Medical Center, Durham, North Carolina 27710.
131:207-213,
T. GARBUTT,2
Subjects
contrast
clinically excluded
,
Roentgen
JOHN
Colitis
on 57 consecutive patients with ulcerative colitis or Crohn’s disease of the colon. Of the 57, 55 patients were evaluated
Recognition of Crohn’s disease of the colon (granulomatous colitis) [1 2] rests on combined evidence from clinical, pathologic, and radiologic evaluation. Since its clinical features are frequently similar to ulcerative colitis, considerable emphasis must be placed on the pathologic and radiologic findings. Pathologic examination of colons resected for inflammatory bowel disease permits differentiation of the two entities in about 90% of cases [3]. Margulis et al. [4] found the conventional barium enema less accurate. In their series, only 70% of cases with Crohn’s disease of the colon and 79% with ulcerative colitis were correctly diagnosed on retrospective analysis. More recently the double contrast barium enema has been advocated by Laufer and colleagues [58] for detecting the early changes of Crohn’s disease of the colon and ulcerative colitis. They were able to distinguish between the two conditions on radiologic criteria in 50 consecutive cases, with complete agreement with endoscopic and morphologic findings [8]. The above two series are not strictly comparable, since most of the patients in the former had advanced disease resulting in colectomy; therefore, the radiologic interpretation was correlated with the pathologic diagnosis mainly on the basis of resected colon specimens. This paper reports our experience and accuracy with the double contrast technique in differentiating Crohn’s disease of the colon from ulcerative colitis.
Am J Rontg.nol © 1978 American
and Ulcerative
207
1977. Address
reprint
requests
to F. M. Kelvin.
0361 -803X/78/08-0207
$00.00
208
KELVIN TABLE
Radiologic Radiologic
1
Findings Ul:rative
Finding
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of Colon
Crohn’s disease: Specific: Discontinuous or asymmetric Discrete ulcers Transverse stripes Longitudinal fissures Deep ulcers (3 mm or more) Right sided disease alone Strongly suggestive: Terminal ilealdisease Cobblestoning Ulcerative colitis:
.
disease
21(88) 16 (67) 10 (42) 7 (29) 6 (25) 4 (16)
. . . . . .
12 (50) 8 (33)
2 (6) 1 (3)
Specific: Granular mucosa Diftuse rectal disease Strongly suggestive; continuous disease Nonspecific findings: Stricture Pseudopolyps Total colitis Note. -Data on Numbers
24
in parentheses
patients
with Crohn’s are percentages.
23 (79) 23 (79) 25(86)
15 (63) 2(8) 2 (8)
8 (27) 4(14) 4 (14)
disease
and
29 with
A
Note. -Numbers
in parentheses
colitis.
Diagnosis
Diagnosis
Crohn’s disease: Correct diagnosis Indeterminate colitis Ulcerative colitis: Correct diagnosis indeterminate colitis Normal
ulcerative
2
of Radiologic
Radiologist Radiologic
Crohn’s disease, the colonic changes in themselves were specific enough to allow a confident radiologic diagnosis. The average accuracy of radiologic diagnosis of ulcerative colitis was 83%. All patients in whom the radiologic and clinical diagnoses agreed showed evidence of continuous involvement (86%), a granular mucosa (79%) or diffuse rectal disease (79%). The latter two features were seen only in ulcerative colitis. Both radiologists agreed with the clinical diagnosis of Crohn’s disease in all patients except one, in whom the only abnormality was a stricture at the rectosigmoid junction. In four patients with ulcerative colitis (representing
five radiologic
interpretations),
the
radiologic
features were nonspecific enough to result in a diagnosis of colitis of indeterminate nature. Three other patients with ulcerative colitis showed no abnormality on barium enema examination. Discussion
TABLE Accuracy
3(12)
ET AL.
B
24 (100) .
.
25 (86) 2(7) 2(7)
Average Accuracy (%)
23 (96) .
1 (4)
23 (79) 3(10.5) 3(10.5)
98 .
.
83 .
.
.
.
are percentages.
Radiographic features considered useful in the differential diagnosis of the two conditions were individually assessed by both radiologists. Each feature was counted as positive only when both radiologists judged it to be present. Subsequently, a diagnosis of Crohn’s disease of the colon, ulcerative colitis, indeterminate colitis, or normal was made by each radiologist. Resufts
The incidence of the radiographic features and the accuracy of diagnosis are shown in tables 1 and 2. The average accuracy of the two radiologists in diagnosing Crohn’s disease of the colon was 98%. Every patient with Crohn’s disease showed discontinuous or eccentric involvement (88%) and/or discrete ulcers (67%). These features formed the basis for the radiologic diagnosis. Other specific but less common signs were transverse stripes, longitudinal fissures, deep ulcers, and disease limited to the right side of the colon. Although small bowel reflux with a characteristically abnormal terminal ileum was evident on eight of the 24 patients with
It is pertinent to attempt to differentiate between Crohn’s disease of the colon and ulcerative colitis, since the complications and prognosis of the two conditions 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 medical therapy, is often complicated by the development of abscesses and fistulae, and has a high incidence of postoperative recurrence. Crohn’s
Disease
The changes of Crohn’s disease in the small bowel are usually characteristic. In this series, only half the patients with Crohn’s disease of the colon had an abnormal small bowel follow-through examination. Whereas some reports have suggested small bowel involvement to occur in 80% [10] to 100% [1 1] of patients with Crohn’s disease of the colon, others have found the incidence to be as low as 41% [12], 43% [4], and 56% [8]. These varying incidences probably in part reflect false negative radiographic small bowel examinations which have been shown to occur in about 50%-70% of patients who subsequently undergo histologic examination of the small bowel [13, 14]. Therefore, it is important to realize tbe frequency with which the small bowel follow-through examination appears normal in Crohn’s disease of the colon. In this group of patients, early radiographic diagnosis of the condition may depend on a colon examination capable of demonstrating fine mucosal changes. “Aphthoid” or discrete ulcers are among the earliest demonstrable mucosal lesions of Crohn’s disease and are well known to pathologists [15]. They often occur on a background of normal mucosa. Less commonly they are seen within or at the margins of an area of severe disease. These ulcers can frequently be seen en face on double contrast examination as round or oval well defined collections of barium, varying in size from one to several millimeters (figs. 1 and 2), often with a surrounding halo (fig. 1). The well defined border corresponds to
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DOUBLE
Fig. 1. -Crohn’s colon. B,Enlarged
Fig. 2.-Crohn’s descending colon
CONTRAST
IN INFLAMMATORY
disease. A, Distal colon with several view of discrete ulcers demonstrating
large discrete halo (arrows)
COLON
ulcers on background surrounding several
209
DISEASE
of normal ulcers.
mucosa
in descending
disease. A, Severe stricturing of right colon and pseudodiverticula in transverse colon. Sigmoid and lower 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 disease. It is doubtful whether these discrete ulcers, when small, can be seen on a conventional barium enema study. In our series they were present in 67% of patients with Crohn’s disease, a similar incidence to that reported by Laufer and Hamilton [8]. In neither of these
two series were they seen in ulcerative colitis. These discrete ulcers may have important therapeutic as well as diagnostic significance because, if left behind at surgery, they may form the basis for postoperative “recurrence.” In two patients reported by Brahme and Wenckert [16], symptoms recurred within 3 months of
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210
KELVIN
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, 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 considered pathognomonic of Crohn’s disease. However, since they are not seen in ulcerative colitis, they are of considerable 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 disease process results i n pseudodiverticula (fig 24) Discontinuous or asymmetric involvement was present in 88% of our patients with Crohn’s disease, representing the most common abnormality. No patient with ulcerative colitis showed this patchy distribution. The combination of submucosal swelling and transverse 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 contradistinction to haustra which usually have a slight curvature 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 ulcerative colitis. This is not surprising since ulcerative 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 shape of colonic ulcers and suggested these varying shapes may have diagnostic significance. Friedland [18] stressed that it is the depth of the ulcers, rather than their shape, that is important in differentiating the two conditions. The distribution of colonic involvement has been emphasized in the literature. We found, like Margulis et al. [4], that disease limited to the right side of the colon
ET AL.
,
.
always ment
indicated
of the cecum
Crohn’s
invariably
disease.
Patients
had disease
with
.
involve-
of the terminal
v_.. few remaining definite curve.
,_.._
haustra Several
--------------------. more proximally pseudodiverticula
and distally that are also present.
--
have
slight
but
ileum. In contrast to the significance of right-sided coIonic disease, changes limited to the distal colon occurred in both ulcerative colitis and Crohn’s disease. The rectum in Crohn’s disease often appears normal on barium enema. When rectal involvement occurs in this condition, it usually manifests itself as discrete ulcers. These were present on radiologic examination in four of our patients. Using the conventional barium enema, Margulis et al. [4] found that the individual radiographic signs in Crohn’s disease of the colon and ulcerative colitis
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DOUBLE
CONTRAST
IN
INFLAMMATORY
out
I
“e_
Fig. flexure. sures
5.-Crohn’s Numerous
(arrows)
discrete
ulcers
can
disease. transverse be seen
on normal
Deep ulcers stripes with in descending
mucosa
in sigmoid
are evident in some longitudinal colon. Note
splenic fisseveral
colon.
showed considerable overlap. The frequency and specificity of the signs present on double contrast barium enema in our patients with Crohn’s disease explain the greater accuracy of the technique in this condition. Ulcerative
Colitis
The earliest colonic change in ulcerative colitis is from the normal featureless mucosa to one with a diffusely fine granular pattern (fig. 6) [19, 20]. The diffuse nature of the involvement in the affected area contrasts vividly with the patchy changes seen in Crohn’s disease. Sigmoidoscopy has shown the fine granular pattern to correspond to an edematous, uneven mucosa without evidence of gross ulceration. Therefore, the contour of the colon is smooth at this stage. More severe involvement is radiologically identified by the presence of marginal ulceration. In our series 79% of patients with ulcerative colitis had granular mucosa. Thorough bowel preparation is crucial in patients with suspected inflammatory bowel disease, since even a small amount of debris in the colon can produce a finely granular pattern that may mimic ulcerative colitis. It is noteworthy that the presence of a diffuse finely granular mucosa is probably not detectable on conventional barium enema study. This may explain the greater accuracy of the double contrast technique in the
COLON
Fig. 6.-Ulcerative rectum. Compare
211
DISEASE
colitis.
with
Diffusely
normal
granular
mucosa
mucosa
of sigmoid
is seen
through-
colon.
detection of mild ulcerative colitis. Fennessy et al. [21], using conventional barium enemas, were unable to diagnose, even retrospectively, 18% of patients with mild disease. Using the double contrast technique, Simpkins and Stevenson [22] failed to detect early changes in only 3.2% of their patients. In two of our patients the rectum appeared entirely normal radiologically, but more proximally there was diffuse granularity of the colon indicating the presence of ulcerative colitis. It is important not to be deflected from the diagnosis of ulcerative colitis merely because the rectum shows no radiologic abnormality. Rectal sparing on radiologic examination occurred in about 20% of patients in our as well as other series [4, 9]. All patients in whom ulcerative colitis was radiologically recognized showed continuous disease with uniformly diffuse involvement (fig. 7). No patient unequivocally exhibited the patchy disease that is so characteristic of Crohn’s colitis. Pseudopolyps are more common in ulcerative colitis, but may also occur in Crohn’s disease. Their nonspecificity makes their identification of little diagnostic value. Similarly, the presence of strictures or total colon involvement was not markedly different in the two diseases. Of the three patients with ulcerative colitis and a normal barium enema, two were asymptomatic at the time of examination and the third had inactive disease at colonoscopy. Four patients had a barium enema showing changes that were nonspecific. Two of these four patients with ulcerative colitis had proctoscopic evidence of mild and limited disease. Problems in the radiologic detection of mild ulcerative colitis or disease limited to the rectum fortunately are balanced by the positivity of sigmoidoscopic diagnosis as occurred in all our 29 patients. The value of the radiologic examination
KELVIN
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212
Fig. 7.-Ulcerative Spot film of splenic
colitis. A,Continuous flexure clearly showing
disease diffusely
evidenced granular
of the colon in ulcerative colitis is more to document the extent, severity, and possible complications of the disease than to establish the diagnosis. One of the major concerns in the evaluation of colitis has been the safety of performing the double contrast barium enema because of the risk of exacerbating the condition or even producing a perforation. We have not observed any untoward effect resulting from the procedure and, indeed, have noted that many patients find the examination less uncomfortable than the conventional examination. More extensive experience at other centers has confirmed the safety of the technique in active inflammatory bowel disease [19, 20]. When significant discomfort is experienced, intravenous injection of 0.5 mg of glucagon produces considerable relief and permits a greater degree of air distension of the colon. Patients with toxic megacolon constitute a contraindication to any form of barium enema study. Examination of patients with very severe active colitis is deferred until there is clinical improvement. Patients with less severe active colitis can be examined provided the bowel preparation is modified. It is our policy in these patients to omit any laxatives and use only a clear liquid diet and cleansing enemas. Our findings suggest that the double contrast technique is a safe and accurate method of diagnosing inflammatory bowel disease, particularly Crohn’s disease of the colon. Changes of inflammatory bowel disease may be recognized at an early stage, during which the presence of discrete ulcers suggesting Crohn’s disease
ET AL.
by granular mucosa.
mucosal
pattern
distal
to midtransverse
B,
colon.
and a granular mucosa suggesting ulcerative colitis should be carefully sought. Specific signs in these conditions seem to be present more frequently when the double contrast technique is used. REFERENCES 1.
Lockhart-Mummery
gional from
HE,
enteritis) ulcerative
BC: Crohn’s
Morson
of the
large
colitis.Gut
intestine
1 :87-105,
and
disease (reits distinction
1960
2. Wolf BS, Marshak RH: Granulomatous colitis (Crohn’s disease of the colon). Am J Roentgenol 88:662-670, 1962 3. Price AB, Morson BC: Inflammatory bowel disease: the surgical pathology of Crohn’s Hum Pathol 6:7-29,1975
disease
and ulcerative
4. Margulis AR, Goldberg HI, Lawson Rambo ON, Noonan CD, Amberg spectrum
of
ulcerative
and
genographic-pathologic
TL, Montgomery CK, JR: The overlapping
granulomatous
study.
colitis.
colitis:
a roent-
113:325-
Am J Roentgenol
334, 1971 5.
Laufer
I: The
ulcerative
radiologic
colitis
demonstration
by double
contrast
of early technique.
changes in J Can Assoc
Radiol 26:116-121, 1975 6. Laufer I, Mullens JE, Hamilton J: Correlation of endoscopy and double contrast radiography in the early stages of ulcerative
and
granulomatous
colitis.
Radiology
118:1-5,
1976 7.
Laufer
bowel 8.
Laufer
I: Air
disease.
contrast
studies
of the
Crit Rev Diagn Imaging I, Hamilton J: The radiological
colon
in
inflammatory
9:421-447, differentiation
1977 be-
tween ulcerative and granulomatous colitis by double contrast radiology. Am J Gastroenterol 66:259-269, 1976 9. Devroede GJ: Differential diagnosis of colitis. Can J Surg
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DOUBLE
CONTRAST
IN INFLAMMATORY
17:369-374, 1974 10. Marshak RH: Granulomatous disease of the intestinal tract (Crohn’s disease). Radiology 114:3-22, 1975 11. Brahme F: Granulomatous colitis: roentgenologic appearance and course of the lesions. Am J Roentgenol 99:35-44, 1967 12. Stanley P, Kelsey Fry I, Dawson AM, Dyer N: Radiological signs of ulcerative colitis and Crohn’s disease of the colon. Clin Radiol 22:434-442, 1971 13. Nelson JA, Margulis AR, Goldberg HI, Lawson TL: Granulomatous colitis: significance of involvement of the terminal ileurn. Gastroenterology 64:1071-1076, 1973 14. Korelitz BI, Present DH, Alpert LI, Marshak RH, Janowitz HD: Recurrent regional ileitis after ileostomy and colectomy for granulomatous colitis. N EngI J Med 287:110-115, 1972 15. Morson BC: Histopathology in regional enteritis (Crohn’s disease), in Skandia International Symposia, edited by Engel A, Larsson T, Stockholm, Nordiska Bokhandelns, 1971, pp 15-33
COLON
DISEASE
213
16. Brahme F, Wenckert A: Spread of lesions in Crohn’s disease of the colon. Gut 11:576-584, 1970 17. Welin 5, Welin G: A pathognomonic roentgenologic sign of regional ileitis (Crohn’s disease). Dis Colon Rectum 16:473478, 1973 18. Friedland GW: The radiological differential diagnosis between ulcerative and granulomatous (Crohn’s) colitis. Calif Med 119:14-21, 1973 19. Welin 5, Brahme F: The double contrast method in ulcerative colitis. Acta Radiol (Stockh) 55:257-271, 1961 20. Bartram C: Radiology in the current assessment of ulcerative colitis. Gastrointest Radio/i :383-392, 1977 21. Fennessy JJ, Sparberg M, Kirsner JB: Early roentgen manifestations of mild ulcerative colitis and proctitis. Radiology 87:848-858, 1966 22.
Simpkins
KC, Stevenson
contrast accuracy
barium enema in colitis: in reflecting sigmoidoscopic
45:486-492,
1972
GW:
The
modified
MalmO
double
an assessment of its findings. Br J Radio!
Contrast
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FREDERICK
Barium M.KELVIN,’
Enema TERRENCE AND
in Crohn’s
Disease
A. ODDSON,1 REED BEN P. BRADENHAM2
Double contrast barium enema examinations in 24 patients with Crohn’s disease of the colon and 29 patients with ulcerative colitis were reviewed without knowledge of the clinical diagnosis. The radiologic diagnosis of Crohn’s disease agreed with the clinical diagnosis in 98% of patients. in this condition the most common radiologic findings were discontinuous or asymmetric disease (88%) and discrete ulcers (67%) often on a normal mucosa. The latter are characteristic of early Crohn’s disease and may enable the radiologist to be the first to suggest the diagnosis, particularly when both sigmoidoscopy and small bowel examination are normal. Of the patients with ulcerative colitis, a positive radiologic diagnosis was made in 83% on the basis of a granular mucosal pattern (79%) and continuous distal involvement (86%). The high accuracy of the double contrast technique, especially In Crohn’s disease, and the relative specificity of the signs that it can demonstrate suggest that this is the preferred examination in the radiologic evaluation of inflammatory bowel disease.
Double
P. RICE,1
August 1978
Ray Society
and
barium
enema
Methods
examination
logic
by a consultant gastroenterologist. from the series because insufficient
was performed
data
existed
to establish
a firm
Four patients were clinical or patho-
diagnosis
of either
ulcera-
tive colitis or Crohn’s disease of the colon. The mean age of the 24 males and 29 females was 33.6 years (range, 17-59). The mean duration of symptoms was 7.3 years (range, 2 months to 29 years). Sigmoidoscopy was performed in 52 patients, colonoscopy in 1 1 and rectal or colonic biopsies in 32. Six patients had surgical resections of small or large bowel ,
for inflammatory
ary to specific diverticular
bowel
disease.
infection,
disease
The presence
ischemia,
antibiotic
of colitis
second-
administration,
or
was excluded.
Of the 24 patients with Crohn’s disease, 12 had the classic changes of Crohn’s disease on standard radiographic examinations of the small bowel. Six of these patients had discrete or linear colonic ulcers visualized by endoscopy. Pathologic confirmation of Crohn’s disease was obtained in four patients by
examination of resected bowel or suction biopsy. The remaining 12 with Crohn’s disease had radiographically normal
small
bowel.
The
diagnosis
was
made
on the
basis
of
endoscopy and biopsy of the large bowel. Ten patients had discrete or linear ulcers at sigmoidoscopy. Six of these 10 patients and one additional patient with normal sigmoidoscopy underwent skip areas,
diagnostic colonoscopy. and asymmetric colonic
Discrete or linear inflammation were
ulcers, seen in
all seven cases. In this group, one patient subsequently underwent colectomy with pathologic confirmation of Crohn’s disease, and one patient had characteristic granulomas on colonoscopic mucosal biopsy. The remaining patient, who did not have typical endoscopic changes of Crohn’s disease, showed granulomas on rectal mucosal biopsy. The 29 patients with ulcerative colitis were diagnosed on the basis of the typical endoscopic appearance of a diffusely granular or finely ulcerated rectal mucosa. Rectal or colonic biopsies in 18 patients and examination of total colectomy specimens in two provided pathologic confirmation of the clinical diagnosis. All 53 patients were examined using the double contrast barium enema technique. Bowel preparation included a clear liquiddiet,laxatives(except in cases of very active colitis), and a cleansing enema or enemas in the radiology department. Polibar (E-Z-Em Co., Westbury, N.Y.), a high density barium, was used in all patients. The technique was essentially that described by Laufer [7]. The double contrast examination of each patient was subsequently reviewed independently by two of us (R. P. Rice and T. 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 ‘Department of Radiology, Duke University Medical Center,Durham, North Carolina 27710. 2Department of Medicine, Duke University Medical Center, Durham, North Carolina 27710.
131:207-213,
T. GARBUTT,2
Subjects
contrast
clinically excluded
,
Roentgen
JOHN
Colitis
on 57 consecutive patients with ulcerative colitis or Crohn’s disease of the colon. Of the 57, 55 patients were evaluated
Recognition of Crohn’s disease of the colon (granulomatous colitis) [1 2] rests on combined evidence from clinical, pathologic, and radiologic evaluation. Since its clinical features are frequently similar to ulcerative colitis, considerable emphasis must be placed on the pathologic and radiologic findings. Pathologic examination of colons resected for inflammatory bowel disease permits differentiation of the two entities in about 90% of cases [3]. Margulis et al. [4] found the conventional barium enema less accurate. In their series, only 70% of cases with Crohn’s disease of the colon and 79% with ulcerative colitis were correctly diagnosed on retrospective analysis. More recently the double contrast barium enema has been advocated by Laufer and colleagues [58] for detecting the early changes of Crohn’s disease of the colon and ulcerative colitis. They were able to distinguish between the two conditions on radiologic criteria in 50 consecutive cases, with complete agreement with endoscopic and morphologic findings [8]. The above two series are not strictly comparable, since most of the patients in the former had advanced disease resulting in colectomy; therefore, the radiologic interpretation was correlated with the pathologic diagnosis mainly on the basis of resected colon specimens. This paper reports our experience and accuracy with the double contrast technique in differentiating Crohn’s disease of the colon from ulcerative colitis.
Am J Rontg.nol © 1978 American
and Ulcerative
207
1977. Address
reprint
requests
to F. M. Kelvin.
0361 -803X/78/08-0207
$00.00
208
KELVIN TABLE
Radiologic Radiologic
1
Findings Ul:rative
Finding
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of Colon
Crohn’s disease: Specific: Discontinuous or asymmetric Discrete ulcers Transverse stripes Longitudinal fissures Deep ulcers (3 mm or more) Right sided disease alone Strongly suggestive: Terminal ilealdisease Cobblestoning Ulcerative colitis:
.
disease
21(88) 16 (67) 10 (42) 7 (29) 6 (25) 4 (16)
. . . . . .
12 (50) 8 (33)
2 (6) 1 (3)
Specific: Granular mucosa Diftuse rectal disease Strongly suggestive; continuous disease Nonspecific findings: Stricture Pseudopolyps Total colitis Note. -Data on Numbers
24
in parentheses
patients
with Crohn’s are percentages.
23 (79) 23 (79) 25(86)
15 (63) 2(8) 2 (8)
8 (27) 4(14) 4 (14)
disease
and
29 with
A
Note. -Numbers
in parentheses
colitis.
Diagnosis
Diagnosis
Crohn’s disease: Correct diagnosis Indeterminate colitis Ulcerative colitis: Correct diagnosis indeterminate colitis Normal
ulcerative
2
of Radiologic
Radiologist Radiologic
Crohn’s disease, the colonic changes in themselves were specific enough to allow a confident radiologic diagnosis. The average accuracy of radiologic diagnosis of ulcerative colitis was 83%. All patients in whom the radiologic and clinical diagnoses agreed showed evidence of continuous involvement (86%), a granular mucosa (79%) or diffuse rectal disease (79%). The latter two features were seen only in ulcerative colitis. Both radiologists agreed with the clinical diagnosis of Crohn’s disease in all patients except one, in whom the only abnormality was a stricture at the rectosigmoid junction. In four patients with ulcerative colitis (representing
five radiologic
interpretations),
the
radiologic
features were nonspecific enough to result in a diagnosis of colitis of indeterminate nature. Three other patients with ulcerative colitis showed no abnormality on barium enema examination. Discussion
TABLE Accuracy
3(12)
ET AL.
B
24 (100) .
.
25 (86) 2(7) 2(7)
Average Accuracy (%)
23 (96) .
1 (4)
23 (79) 3(10.5) 3(10.5)
98 .
.
83 .
.
.
.
are percentages.
Radiographic features considered useful in the differential diagnosis of the two conditions were individually assessed by both radiologists. Each feature was counted as positive only when both radiologists judged it to be present. Subsequently, a diagnosis of Crohn’s disease of the colon, ulcerative colitis, indeterminate colitis, or normal was made by each radiologist. Resufts
The incidence of the radiographic features and the accuracy of diagnosis are shown in tables 1 and 2. The average accuracy of the two radiologists in diagnosing Crohn’s disease of the colon was 98%. Every patient with Crohn’s disease showed discontinuous or eccentric involvement (88%) and/or discrete ulcers (67%). These features formed the basis for the radiologic diagnosis. Other specific but less common signs were transverse stripes, longitudinal fissures, deep ulcers, and disease limited to the right side of the colon. Although small bowel reflux with a characteristically abnormal terminal ileum was evident on eight of the 24 patients with
It is pertinent to attempt to differentiate between Crohn’s disease of the colon and ulcerative colitis, since the complications and prognosis of the two conditions 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 medical therapy, is often complicated by the development of abscesses and fistulae, and has a high incidence of postoperative recurrence. Crohn’s
Disease
The changes of Crohn’s disease in the small bowel are usually characteristic. In this series, only half the patients with Crohn’s disease of the colon had an abnormal small bowel follow-through examination. Whereas some reports have suggested small bowel involvement to occur in 80% [10] to 100% [1 1] of patients with Crohn’s disease of the colon, others have found the incidence to be as low as 41% [12], 43% [4], and 56% [8]. These varying incidences probably in part reflect false negative radiographic small bowel examinations which have been shown to occur in about 50%-70% of patients who subsequently undergo histologic examination of the small bowel [13, 14]. Therefore, it is important to realize tbe frequency with which the small bowel follow-through examination appears normal in Crohn’s disease of the colon. In this group of patients, early radiographic diagnosis of the condition may depend on a colon examination capable of demonstrating fine mucosal changes. “Aphthoid” or discrete ulcers are among the earliest demonstrable mucosal lesions of Crohn’s disease and are well known to pathologists [15]. They often occur on a background of normal mucosa. Less commonly they are seen within or at the margins of an area of severe disease. These ulcers can frequently be seen en face on double contrast examination as round or oval well defined collections of barium, varying in size from one to several millimeters (figs. 1 and 2), often with a surrounding halo (fig. 1). The well defined border corresponds to
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DOUBLE
Fig. 1. -Crohn’s colon. B,Enlarged
Fig. 2.-Crohn’s descending colon
CONTRAST
IN INFLAMMATORY
disease. A, Distal colon with several view of discrete ulcers demonstrating
large discrete halo (arrows)
COLON
ulcers on background surrounding several
209
DISEASE
of normal ulcers.
mucosa
in descending
disease. A, Severe stricturing of right colon and pseudodiverticula in transverse colon. Sigmoid and lower 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 disease. It is doubtful whether these discrete ulcers, when small, can be seen on a conventional barium enema study. In our series they were present in 67% of patients with Crohn’s disease, a similar incidence to that reported by Laufer and Hamilton [8]. In neither of these
two series were they seen in ulcerative colitis. These discrete ulcers may have important therapeutic as well as diagnostic significance because, if left behind at surgery, they may form the basis for postoperative “recurrence.” In two patients reported by Brahme and Wenckert [16], symptoms recurred within 3 months of
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210
KELVIN
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, 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 considered pathognomonic of Crohn’s disease. However, since they are not seen in ulcerative colitis, they are of considerable 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 disease process results i n pseudodiverticula (fig 24) Discontinuous or asymmetric involvement was present in 88% of our patients with Crohn’s disease, representing the most common abnormality. No patient with ulcerative colitis showed this patchy distribution. The combination of submucosal swelling and transverse 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 contradistinction to haustra which usually have a slight curvature 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 ulcerative colitis. This is not surprising since ulcerative 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 shape of colonic ulcers and suggested these varying shapes may have diagnostic significance. Friedland [18] stressed that it is the depth of the ulcers, rather than their shape, that is important in differentiating the two conditions. The distribution of colonic involvement has been emphasized in the literature. We found, like Margulis et al. [4], that disease limited to the right side of the colon
ET AL.
,
.
always ment
indicated
of the cecum
Crohn’s
invariably
disease.
Patients
had disease
with
.
involve-
of the terminal
v_.. few remaining definite curve.
,_.._
haustra Several
--------------------. more proximally pseudodiverticula
and distally that are also present.
--
have
slight
but
ileum. In contrast to the significance of right-sided coIonic disease, changes limited to the distal colon occurred in both ulcerative colitis and Crohn’s disease. The rectum in Crohn’s disease often appears normal on barium enema. When rectal involvement occurs in this condition, it usually manifests itself as discrete ulcers. These were present on radiologic examination in four of our patients. Using the conventional barium enema, Margulis et al. [4] found that the individual radiographic signs in Crohn’s disease of the colon and ulcerative colitis
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DOUBLE
CONTRAST
IN
INFLAMMATORY
out
I
“e_
Fig. flexure. sures
5.-Crohn’s Numerous
(arrows)
discrete
ulcers
can
disease. transverse be seen
on normal
Deep ulcers stripes with in descending
mucosa
in sigmoid
are evident in some longitudinal colon. Note
splenic fisseveral
colon.
showed considerable overlap. The frequency and specificity of the signs present on double contrast barium enema in our patients with Crohn’s disease explain the greater accuracy of the technique in this condition. Ulcerative
Colitis
The earliest colonic change in ulcerative colitis is from the normal featureless mucosa to one with a diffusely fine granular pattern (fig. 6) [19, 20]. The diffuse nature of the involvement in the affected area contrasts vividly with the patchy changes seen in Crohn’s disease. Sigmoidoscopy has shown the fine granular pattern to correspond to an edematous, uneven mucosa without evidence of gross ulceration. Therefore, the contour of the colon is smooth at this stage. More severe involvement is radiologically identified by the presence of marginal ulceration. In our series 79% of patients with ulcerative colitis had granular mucosa. Thorough bowel preparation is crucial in patients with suspected inflammatory bowel disease, since even a small amount of debris in the colon can produce a finely granular pattern that may mimic ulcerative colitis. It is noteworthy that the presence of a diffuse finely granular mucosa is probably not detectable on conventional barium enema study. This may explain the greater accuracy of the double contrast technique in the
COLON
Fig. 6.-Ulcerative rectum. Compare
211
DISEASE
colitis.
with
Diffusely
normal
granular
mucosa
mucosa
of sigmoid
is seen
through-
colon.
detection of mild ulcerative colitis. Fennessy et al. [21], using conventional barium enemas, were unable to diagnose, even retrospectively, 18% of patients with mild disease. Using the double contrast technique, Simpkins and Stevenson [22] failed to detect early changes in only 3.2% of their patients. In two of our patients the rectum appeared entirely normal radiologically, but more proximally there was diffuse granularity of the colon indicating the presence of ulcerative colitis. It is important not to be deflected from the diagnosis of ulcerative colitis merely because the rectum shows no radiologic abnormality. Rectal sparing on radiologic examination occurred in about 20% of patients in our as well as other series [4, 9]. All patients in whom ulcerative colitis was radiologically recognized showed continuous disease with uniformly diffuse involvement (fig. 7). No patient unequivocally exhibited the patchy disease that is so characteristic of Crohn’s colitis. Pseudopolyps are more common in ulcerative colitis, but may also occur in Crohn’s disease. Their nonspecificity makes their identification of little diagnostic value. Similarly, the presence of strictures or total colon involvement was not markedly different in the two diseases. Of the three patients with ulcerative colitis and a normal barium enema, two were asymptomatic at the time of examination and the third had inactive disease at colonoscopy. Four patients had a barium enema showing changes that were nonspecific. Two of these four patients with ulcerative colitis had proctoscopic evidence of mild and limited disease. Problems in the radiologic detection of mild ulcerative colitis or disease limited to the rectum fortunately are balanced by the positivity of sigmoidoscopic diagnosis as occurred in all our 29 patients. The value of the radiologic examination
KELVIN
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212
Fig. 7.-Ulcerative Spot film of splenic
colitis. A,Continuous flexure clearly showing
disease diffusely
evidenced granular
of the colon in ulcerative colitis is more to document the extent, severity, and possible complications of the disease than to establish the diagnosis. One of the major concerns in the evaluation of colitis has been the safety of performing the double contrast barium enema because of the risk of exacerbating the condition or even producing a perforation. We have not observed any untoward effect resulting from the procedure and, indeed, have noted that many patients find the examination less uncomfortable than the conventional examination. More extensive experience at other centers has confirmed the safety of the technique in active inflammatory bowel disease [19, 20]. When significant discomfort is experienced, intravenous injection of 0.5 mg of glucagon produces considerable relief and permits a greater degree of air distension of the colon. Patients with toxic megacolon constitute a contraindication to any form of barium enema study. Examination of patients with very severe active colitis is deferred until there is clinical improvement. Patients with less severe active colitis can be examined provided the bowel preparation is modified. It is our policy in these patients to omit any laxatives and use only a clear liquid diet and cleansing enemas. Our findings suggest that the double contrast technique is a safe and accurate method of diagnosing inflammatory bowel disease, particularly Crohn’s disease of the colon. Changes of inflammatory bowel disease may be recognized at an early stage, during which the presence of discrete ulcers suggesting Crohn’s disease
ET AL.
by granular mucosa.
mucosal
pattern
distal
to midtransverse
B,
colon.
and a granular mucosa suggesting ulcerative colitis should be carefully sought. Specific signs in these conditions seem to be present more frequently when the double contrast technique is used. REFERENCES 1.
Lockhart-Mummery
gional from
HE,
enteritis) ulcerative
BC: Crohn’s
Morson
of the
large
colitis.Gut
intestine
1 :87-105,
and
disease (reits distinction
1960
2. Wolf BS, Marshak RH: Granulomatous colitis (Crohn’s disease of the colon). Am J Roentgenol 88:662-670, 1962 3. Price AB, Morson BC: Inflammatory bowel disease: the surgical pathology of Crohn’s Hum Pathol 6:7-29,1975
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and ulcerative
4. Margulis AR, Goldberg HI, Lawson Rambo ON, Noonan CD, Amberg spectrum
of
ulcerative
and
genographic-pathologic
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and
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CONTRAST
IN INFLAMMATORY
17:369-374, 1974 10. Marshak RH: Granulomatous disease of the intestinal tract (Crohn’s disease). Radiology 114:3-22, 1975 11. Brahme F: Granulomatous colitis: roentgenologic appearance and course of the lesions. Am J Roentgenol 99:35-44, 1967 12. Stanley P, Kelsey Fry I, Dawson AM, Dyer N: Radiological signs of ulcerative colitis and Crohn’s disease of the colon. Clin Radiol 22:434-442, 1971 13. Nelson JA, Margulis AR, Goldberg HI, Lawson TL: Granulomatous colitis: significance of involvement of the terminal ileurn. Gastroenterology 64:1071-1076, 1973 14. Korelitz BI, Present DH, Alpert LI, Marshak RH, Janowitz HD: Recurrent regional ileitis after ileostomy and colectomy for granulomatous colitis. N EngI J Med 287:110-115, 1972 15. Morson BC: Histopathology in regional enteritis (Crohn’s disease), in Skandia International Symposia, edited by Engel A, Larsson T, Stockholm, Nordiska Bokhandelns, 1971, pp 15-33
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DISEASE
213
16. Brahme F, Wenckert A: Spread of lesions in Crohn’s disease of the colon. Gut 11:576-584, 1970 17. Welin 5, Welin G: A pathognomonic roentgenologic sign of regional ileitis (Crohn’s disease). Dis Colon Rectum 16:473478, 1973 18. Friedland GW: The radiological differential diagnosis between ulcerative and granulomatous (Crohn’s) colitis. Calif Med 119:14-21, 1973 19. Welin 5, Brahme F: The double contrast method in ulcerative colitis. Acta Radiol (Stockh) 55:257-271, 1961 20. Bartram C: Radiology in the current assessment of ulcerative colitis. Gastrointest Radio/i :383-392, 1977 21. Fennessy JJ, Sparberg M, Kirsner JB: Early roentgen manifestations of mild ulcerative colitis and proctitis. Radiology 87:848-858, 1966 22.
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The
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