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GASTROINTESTINAL IMAGING
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Small bowel
COMPUTED
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TOMOGRAPHY
GastroIntestInal
Adult celiac disease
cumulatIve
CelIac
Index
dIsease
terms: and its complications
IntestInes, CT
IntestInes, radiography
Radiographic Findings
In Uncomplicat#{149}d C#{149}llacDisoas#{149}
THE SMALL BOWEL FOLLOW THROUGH mality may be present in any disease
IN CELIAC DISEASE associated with small intestinal hypomotility or
obstruction (4-8). Segmentation and floccula-
The radiographic findings in adult celiac tion of barium indicate increased intraluminal
disease on small bowel follow through exami- fluid and delayed transit time, but these find-
nation are usually nonspecific or secretion re- ings are nonspecific. Thickening of jejunal folds
lated artifacts (4). Diffuse small bowel dilata- is an artifact of increased intestinal secretion.
tion is the most frequent finding, but this abnor-
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Figure 1
(A) Normal Jejunum In the normal jejunal mucosa, the villi, V. are 3-
4 times the height of the crypts, C. Epithelial cells develop in the
crypts of Lieberkuhn and migrate toward the tops of the villi. (Figures
A-C are all magnified equally.) (B) Cellac disease with complete vii-
bus atrophy In celiac disease, villi are either absent or diminished in
height and the mucosa has a flat or mildly undulating surface. Al-
though the villi are absent, there is a relative preservation of the muco-
sal thickness by hyperplasia of the crypts, C, and an inflammatory infil-
trate and edema of the lamina propria, I. (C) Ceilac disease with par-
tial villous atrophy Occasionally, destruction of the villi is
incomplete, resulting in partial villous atrophy (arrow). Mild crypt hy-
perplasia is seen in this case. Villous atrophy in celiac disease may be
patchy in distribution and of variable severity.
THE SMALL BOWEL ENEMA (4). The small bowel enema may be used to
IN CELIAC DISEASE identify celiac disease in patients with a con-
fusing clinical presentation; in known celiac
The small intestine is best imaged by dis- disease, it may be used (I) to evaluate pa-
tending the lumen before flocculation of ban- tients who have a poor response to gluten
um has occurred (Figure 2). This prerequisite withdrawal, (2) to exclude malignant on other
for an optimal small bowel examination can complications and (3) to serve as a baseline to
be achieved by small bowel enema (enteno- permit earlier, more reliable recognition of ma-
clysis), because jejunal intubation allows con- lignant neoplasms at a later date.
trolled and rapid infusion of contrast agents
S
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a
.
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U
a Figure2
S Normal small Intestine (A) Nor-
U
mal jejunum During small bowel
0
S enema, the normal jejunum has a
a 3-4 cm luminal diameter, with 4-
U 6 valvulae conniventes (folds) pen
a, inch. Each fold is straight, uniform,
E 1-2 mm in width, and perpendicu-
0
U Ian or only slightly angled relative
C
to the jejunal wall. (B) Delayed
views A delayed closeup of the
same small intestinal loop shown
in Figure 1A was obtained approxi-
mately 30 minutes after barium in-
fusion. In comparison with the ear-
ly tnansradiant phase in Figure 1A,
the small bowel loop shows a di-
minished luminal diameter and an
apparent increase in fold thick-
ness. Figures 2A and B show that
‘1
small bowel distentioniscritical in I I
the assessment of fold size. The
apparent increase in fold thickness 2A
in the delayed views is probably an
artifact of diminished Iuminal diam-
eter. Because small bowel enemas
achieve greater IuminoI distention
than small bowel follow through
examinations, the small bowel en-
ema is superior for determining
fold thickness.
2B
C
3
0
0
Technique washout and flocculation of the barium 3
have occurred. 0
0
The small bowel enema should be modi- 4. Measure the number of folds per inch in the a
fied as follows in patients with suspected mal- proximal jejunum (Figure 3) and, if possible, S
a,
absorption: in the distal ileum.
C)
I Increase the volume of barium (240-260
. ml This technique minimizes early flocculation of S
of 80% W/V barium). barium resulting from the increased luminal dis- a
0
2. Increase the speed of infusion of barium tension, increased intraluminal fluid, and intes-
and methyl cellulose (100-I 10 mI/minute). tinal hypomotility associated with celiac dis- 0
S
3. Take early spot radiographs during initial fill- ease. a0
ing of the small bowel with barium, before S
Figure 3
Cellac disease The number of
folds per inch (----) are counted in
the proximal jejunum, J. Note the
smooth mucosal surface seen in
most patients during small bowel
enema.
Criteria for the Diagnosis creased number of folds per inch is present in
of Cellac Disease
the ileum (9,10). These findings are sometimes
present on small bowel follow through exami-
While the findings on small bowel follow nations (9,).
through examination are often nonspecific, Data from a recent study by Herlinger and
the findings on small bowel enema may be Maglinte (10) indicate that the small bowel en-
characteristic of celiac disease (Figure 4). In ema may be strongly suggestive of celiac dis-
many patients, a decreased number of folds ease in nearly 75% of patients who have the
per inch is present in the jejunum and an in- disease (Figure 5).
S
0
0
S
0
0
U Figure4
: Radiographic findings in uncompll-
( cated cellac disease (A) During
0 a small bowel enema, a paucity of
.! folds is seen in the proximal jeju-
g num, J. A greater than normal
:a number of folds is seen in the ile-
E um, I. (B) Delayed view, small
0 bowel enema A delayed radio-
graph, obtained after 45 minutes,
shows “haziness” of the barium,
indicative of flocculation resulting
from increased luminal secretion.
Fold thickness appears to be in-
creased. Diminished luminal diam-
etercannot account forallofthe
apparent increase in fold thick-
ness, since the loops are not sig-
nificantly collapsed. Therefore, we
postulate that increased fold thick-
ness is probably an artifact of in-
creased intestinal secretion.(C)
CT scan Separation of valvulae 4A
conniventes (arrow) and diffusely
dilated small bowel loops may be
shown by computed tomography.
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4B
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AVERAGE FOLDS PER INCH
PROXAfrL R4N
Figure 5
Criteria for the diagnosis of celiac
disease (A) If three or fewer
folds per inch are seen in the jeju-
num, a diagnosis of celiac disease
is strongly favored. Four folds per
inch in the jejunum is indetermi-
nate for celiac disease. Five folds
or more per inch makes a diagno-
sis of celiac disease unlikely. (B)
An increased number of folds in
the ileum may be present and may
be an adaptive response to in-
3 4 crease the functional surface area
AVERAGE FOL.DS/PICH 5A (9). Marked overlap of loops in the
pelvic ileum makes measurement
AVERAGE FOLDS PER INCH of fold number per inch difficult in
DISTAL LEUM approximately one-third of pa-
14 tients, however. Thus, the finding
EUACS
of an increased number of folds
12 = CNTROL5 per inch in the ileum is only sug-
gestive of the diagnosis of celiac
10 disease.
8
2__niLr_
4
A,
0 1 2 3 4 5 6 7
AVERA FOLDS/t4cH 5B
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0
a
S
Ancillary Radiographic Findings
: MOSAIC PATTERN
S
0
0 In almost all patIents with cellac dIsease,
.2 the mucosa is divided into 1-2 mm polygonal
- islands surrounded by distinct grooves, forming
a a “mosaic pattern” (Figure 6) (11). Despite
these pathologic changes, the jejunal surface
has a flat, featureless appearance on small
bowel enema in most patients. In approxi-
mately 10% of celiac patients, however, this
mosaic pattern can be identified on small
bowel enema (Figures 7 and 8).
Figure7
Mosaic pattern A closeup view of the jejunum
shows tubular, featureless loops. In some areas (ar-
rows), a mosaic pattern is depicted as 1 mm radio-
lucent mucosal islands surrounded by barium filled
grooves (1 1).
Figure6
Mosaic pattern In the jejunum A photograph from a
dissecting microscope shows islands of mucosa
surrounded by deep grooves. Many (8-40) crypt
openings (arrow) are found on each mound of the
mosaic mucosa. (Courtesy of MS. Losowksy,
M.D.)
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Figure 8
Mosaic pattern (A) A mosaic paffern is shown in the shallow ban-
um pool as 0.5-1 mm radiolucencies (arrows). (B) A digitized and
reversed image of Figure 8A emphasizes the mosaic paffern (arrows)
of celiacdisease.
PEPTIC DUODENITIS
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Figure9
U Peptic duodenitis 1-4 mm polyp-
.2 oid islands are seen in the mucosa
.; of the duodenal bulb and inthe , -
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(arrows).
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INTUSSUSCEPTION
Figure 10
Transient lntussusceptlon In celiac
disease Two intussusceptions
(large arrows) are shown in this
small bowel follow through exami-
nation.An intraluminal filling
defect
(intussusceptum) is surrounded
by a coil spring appearance (the
mucosa of the intussuscipiens).
The lumen of the intussusceptum
is filled with barium (small an-
rows).
The major complications of celiac disease histologic response to a gluten free diet) (16).
include intestinal ulceration and pneumatosis, Another 25% of patients with ulcerative jejun-
neuropathy, hyposplenism, the cavitary mes- oileitis have “unclassified spnue” with malab-
entenic lymph node syndrome and the devel- sorption and a flat jejunal biopsy, but no ne-
opment of malignant neoplasms (214,15). sponse to a gluten free diet (16). Complica-
Symptoms from a complicating disorder may tions of ulcerative jejunoileitis include
be the first clinically recognized manifestation hemorrhage, perforation, and obstruction ow-
of celiac disease. Treatment failure, despite di- ing to a structural abnormality. Some such pa-
etary restriction suggests that the diagnosis of tients have concurrent lymphoma or may de-
celiac disease is incorrect, that the patient has velop lymphoma.
failed to comply with the treatment regimen, or Areas of ulceration are most frequently
that some complication has supervened. found in the jejunum (Figures 1 IC and D), oc-
casionally in the ileum, or rarely in the colon
ULCERATIVE JEJUNOILEITIS (16). In a series of patients with ulcerative je-
junoileitis and celiac disease or unclassified
Multiple chronic, benign ulcers of the small sprue, ulcers were found on small bowel follow
intestine are an uncommon but, when present, through examination in only 2 of 15 patients
frequently fatal complication of adult celiac (16). Because the small bowel follow through
disease (16-19). These ulcers are of unknown was abnormal in such a small percentage of
etiology and occur most frequently in the fifth patients with ulcerative jejunoileitis, Baen et al
or sixth decades of life (16). Patients often have recommended exploratory lapanotomy
complain of fever, acute abdominal pain, dis- on patients with a suspected intestinal compli-
tention, and weight loss-symptoms similar to cation and malabsonption, to rule out ulcer-
those of celiac disease complicated by a ma- ative jejunoileitis or lymphoma. Although we
lignant neoplasm. Approximately 50% of pa- have not performed a scientific study, we be-
tients with ulcerative jejunoileitis have celiac lieve that the small bowel enema may demon-
disease by clinical and pathologic criteria (i.e., strate ulcerative jejunoileitis in a significant pen-
a flat jejunal biopsy as well as a clinical and centage of these patients (Figures 1 1 and 12).
Figure 1 1A
Acute ulcerative JeJunltls A spot
radiograph exposed during the ear-
ly single contrast phase of a small
bowel enema shows a rigid jejunal
loop with irregularly thickened
folds (white arrows) and thick
walls. These findings cannot be
distinguished from Iymphoma
complicating celiac disease. Unin-
volved jejunum shows separation
of valvulae conniventes (black an-
row). This figure shows that ulcers
are often shallow, diffuse, and dif-
ficult to detect in ulcerative jejuno-
ileitis, but the pseudomembranes
and submucosal edema, demon-
stnated in Figure 1 1D result in
“thickening of the mucosal folds”.
IIA
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Figures 1 1B-D
(B) A CT scan performed five days after the small bowel enema
shows an irregularly thickened small bowel wall (arrows). (C) The
surgical resection specimen shows pseudomembranes, M, covering
the ulcerated epithelium, E. The small bowel folds are enlarged (an-
rows). (D) Microscopically (hematoxylin and eosin stain), pseudo-
membranes of inflammatory cells, fibnin, and sloughed epithelial cells
(thick arrows) are adherent to multiple sites of mucosal ulceration
(open arrows). Submucosal edema contributes to increased wall and
fold thickness. Residual villi in this section (curved arrows) are only
mildly flattened. Villous atrophy was demonstrated in the more pnoxi-
mal jejunum.
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Figure 12
Chronic ulcerative Jejunitis Multiple short
strictures (arrows) are present in the jeju-
num.
Figure 13
Hyposplenlsm A small spleen
(arrow) is seen in this patient with
celiac disease and hyposplenism.
A 35 g, 2 x 3 cm spleen was
found at autopsy.
CAVITARY MESENTERIC
LYMPH NODE SYNDROME
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Figures 14A-C
Cavitary mesenteric lymph node syndrome (A) lidification of fat) shows numerous solid and cavi-
Multiple masses with fluid levels are centrally locat- tany masses, N, in the jejunoileal mesentery. Bowel
ed in the abdomen. At first glance, the fluid levels in loops (arrows) are seen at the periphery of the
the round masses suggest dilated small bowel specimen. (C) A low power photomicrograph (he-
loops. Note, however, that the cavitated masses matoxylin and eosin stain) shows a mass with a
(arrows) contain fluid-fat levels rather than air-fluid central cavity of hyaline material, H, and small lipid
levels, and are not filled by the oral contrast agent. droplets (arrow) surrounded by a thick fibrotic cap-
(B) An autopsy specimen (after refrigeration and so- sule,C.
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Figure 14D
A medium power photomicrognaph (hematoxylin and eosin stain)
from the peripheral zone of one cavitary mass shows residual lymph
node architecture including lymph node remnants, L, and a fibrotic
capsule.
Malignant tumors are the most common Lymphoma is the most common malignant
cause of death in celiac disease (1). In most lesion complicating celiac disease (23,24). Al-
patients dying from a superimposed malignant though previously termed “malignant histiocy-
neoplasm, the diagnosis of celiac disease has tosis”, most if not all intestinal lymphomas are
been made as an adult. The possibility of a of T-cell origin (25). The prognosis for these pa-
malignant lesion should be considered in any tients is poor. Such lymphomas usually involve
celiac patient with recurrent symptoms after a the small bowel either in a multifocal on diffuse
period of dietary control. Some elderly pa- distribution (24) (Figures 15, 16, and 17) (24).
tients may have symptoms related to the ma- Occasionally, a short segment is involved (Fig-
lignant tumor, before the diagnosis of celiac une 17). About 33% of patients also have liver,
disease has been established, however. spleen, on lymph node involvement. Peripheral
lymphadenopathy is uncommon (24).
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A small bowel follow through examination 17). The radiographic distinction of lymphoma 3.
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has been considered so unreliable for the di- from ulcerative jejunoileitis may be difficult; 3
agnosis of lymphoma complicating celiac dis- and ulcerative jejununoileitis may coexist with a
ease that some authors have advocated ex- lymphoma.
ploratory lapanotomy if there is a strong clinical Detection of paraaortic or mesentenic
suspicion of Iymphoma (1,16). We have been Iymphadenopathy on CT does not necessarily
successful in detecting lymphoma complicat- indicate lymphoma (26). Such lymphadenopa-
ing celiac disease on small bowel enema. thy may represent reactive hyperplasia and si-
These lymphomas may be manifested by en- nus histiocytosis (26) or the early stages of the
Iarged, nodular folds, ulcers, or extrinsic mass cavitary mesentenic lymph node syndrome.
effects (Figures 16 and 17). Even on small bow- Reactive hyperplasia may respond to a gluten
el enema, the diagnosis of lymphoma compli- free diet (26).
cating celiac disease may be subtle (Figure
Figure 16
Lymphoma complicating celiac disease Mucosal
ulceration (thick arrow) and enlarged nodular folds
(curved arrow) are due to lymphoma infiltrating the
small bowel. A lange extrinsic mass effect (small an-
rows) indicates that tumor extends into the mesen-
Figure 15 tery.
Lymphoma complicating cellac disease Enlarged,
nodular folds (arrows) are present.
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Figure17
Subtle T-cell lymphoma in cellac disease (A) An overhead radio-
graph from a small bowel enema shows a few small nodules in one
loop of proximal jejunum (enclosed section). The remainder of the
small intestine is normal. (B) A closeup view shows nodular, mildly
enlarged folds (arrows). (C) A biopsy specimen from the proximal je-
junum shows a mononuclear infiltrate in the lamina propnia, I, and
submucosa and absence of intestinal villi (arrows) (hematoxylin and
eosin stain). (D) A high power view (hematoxylin and eosin stain)
shows a lymphomatous infiltrate in the Iamina propnia. Gene near-
rangement studies demonstrated the 1-cell nature of the lymphoma.
Intestinal Carcinoma
Figure 19
Adenocarcinoma of the duodenum In cellac disease Separation of
valvulae conniventes in the proximal jejunum, J, strongly suggests the
diagnosis of celiac disease. An annular lesion (arrow) is seen in the
ascending portionofthe duodenum.
Figure 18
Squamous cell carcinoma of the
esophagus complicating cellac dis-
ease A polypoid, ulcerated mass
protrudes into the midesophagus.
Summary
While a small bowel follow through exami- Other authors have suggested that be-
nation may suggest the diagnosis of celiac dis- cause the small bowel follow through exami-
ease, a specific diagnosis can be made on nation is inadequate for diagnosing the com-
small bowel enema in nearly 75% of patients. plications of cellac disease, exploratory lapa-
Demonstration of three or fewer folds per inch rotomy may be needed to rule out lymphoma
in the jejunum strongly favors the diagnosis of on ulcerative jejunoileltis. Our experience, how-
celiac disease. Demonstration of five or more ever, indicates that the small bowel enema
folds per inch in the jejunum makes the diag- may be helpful (1) in screening for celiac dis-
nosis of celiac disease unlikely. Demonstration ease in patients with atypical clinical presen-
of an increased number of folds per inch in the tations, (2) in establishing a baseline for earlier
ileum also supports the diagnosis of celiac dis- recognition of a malignant neoplasm, and (3)
ease. A tubular, featureless lumen and mosaic in detecting a malignant tumor or other com-
pattern are additional findings consistent with plications.
celiac disease.
References
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(celiac disease). In: Berk JE, ed. Bockus gastroenterol- JJ. Nontropical sprue with pneumafosis coli. AJR 1981;
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1757. 15. Khouri MR. Levine MS. Dabezies M, Saul SH. Benign
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