DOI:10.2214/AJR.07.3646
AJR 2008; 191:1483-1492
© American Roentgen Ray Society
Celiac Disease in Adults: Evaluation with MDCT Enteroclysis
Philippe Soyer1,
Mourad Boudiaf1,
Yann Fargeaudou1,
Xavier Dray2,
Lounis Hamzi1,
Kouroche Vahedi2,
Anne Lavergne-Slove3 and
Roland Rymer1
1 Department of Abdominal Imaging, Hôpital Lariboisière-AP-HP-GHU
Nord and University Diderot-Paris 7, 2, rue Ambroise Paré, 75475 Paris
Cedex 10, France.
2 Department of Digestive Diseases, Hôpital Lariboisière-AP-HP-GHU
Nord and University Diderot-Paris, Paris, France.
3 Department of Pathology, Hôpital Lariboisière-AP-HP-GHU Nord and
University Diderot-Paris, Paris, France.
Received January 9, 2008;
accepted after revision June 3, 2008.
Address correspondence to P. Soyer
(philippe.soyer{at}lrb.aphp.fr).
Abstract
OBJECTIVE. The purpose of this article is to present the MDCT
enteroclysis features of the multiple complications of celiac disease and
illustrate why this technique is helpful to adult patients with celiac
disease.
CONCLUSION. MDCT enteroclysis findings can suggest the diagnosis in
adult patients with unknown celiac disease, and many complications of celiac
disease can be recognized because of their characteristic appearance.
Familiarity with these signs can help in appropriate planning of further
diagnostic procedures.
Keywords: celiac disease • celiac sprue • CT-enteroclysis • enteroclysis • MDCT • nontropical sprue • refractory sprue • small-bowel disease • sprue
Introduction
Celiac disease is chronic intol erance of gluten that induces intestinal
mucosal lesions in genetically predisposed patients. Although in most cases
the symptoms and histologic abnormalities completely resolve with use of a
strict gluten-free diet, com plications occur in some patients. The com
plications include small-bowel intus sus ception, ulcerative jejunoileitis,
lymphoma, adenocarcinoma, hyposplenism, cavitating lymphadenopathy syndrome,
and pneu matosis intestinalis. Therefore, once the diagnosis is made, patients
with celiac disease need regular monitoring. Although MDCT enteroclysis has
been found effective for the diagnosis of a variety of small-bowel diseases,
little is known about the utility of this examination in monitoring adult
patients with celiac disease.
The goal of this article is threefold. First, we want to describe the MDCT
enteroclysis features of celiac disease in adults. Second, we aim to discuss
and illustrate the utility of MDCT enteroclysis in the study of complicated
celiac disease. Third, we want to help readers understand the advantages and
limitations of MDCT enteroclysis compared with push enteroscopy and wireless
capsule endoscopy in the appro priate clinical setting.
Celiac Disease
Pathophysiology
The gliadin fraction of wheat gluten and similar alcohol-soluble proteins
(so-called protamins) that are present in other grains, such as barley and
rye, are environmental factors responsible for the gastrointestinal damage of
celiac disease [1,
2]. Celiac disease is an
autoimmune enteropathy caused by an inappropriate T-cell–mediated immune
response to ingested gluten
[3]. The effective treatment of
adult patients with celiac disease is based on total lifelong elimination of
food products containing gluten.
Celiac disease is significantly associated with two specific human
leukocyte antigen (HLA) genes
[4]. Celiac disease is detected
with assays for antihuman tissue transglutaminase antibodies (AtTG) and
antiendomysium antibodies (anti-EMA), which are serum-specific
[5]. One of the targets of the
autoimmune response in celiac disease is tissue transglutaminase (tTG)
[6]. Celiac disease may be
responsible for chronic inflammation and hyperhomocystinemia related to folic
acid malabsorption, which may explain the trend toward deep venous thrombosis
in these patients [7].
Histopathology
The pathologic changes of celiac disease are predominantly seen in the
duodenum and proximal jejunum. However, the extent of the disease is extremely
variable, ranging from segmental to full involvement of the small bowel.
Histologic examination of at least four specimens obtained during endoscopic
duodenal biopsy and from the third part of the duodenum is needed to fully
ascertain the diagnosis [3].
Histologic lesions are classified into three main groups (Figs.
1,
2,
3) according to the Marsh
criteria as modified by Oberhuber et al.
[8,
9]. Type 1 corresponds to
infiltrative inflammatory lesions with a normal villous architecture; type 2
is characterized by cryptic hyperplastic lesions; and type 3 corresponds to an
increased number of intraepithelial lymphocytes with crypt hyperplasia in
association with mild villous atrophy (type 3A), moderate villous atrophy
(type 3B), or total villous atrophy (type 3C)
[9].
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Fig. 1 —39-year-old woman with celiac disease. Photograph of
histologic specimen obtained during duodenal biopsy reveals Marsh type 1
lesions consisting of numerous intraepithelial lymphocytes (infiltrative
inflammatory lesions) (arrowheads) in absence of atrophic lesions. V
= villi of normal size and absence of atrophy, C = crypts, which are free of
hyperplasia. (H and E, x100)
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Fig. 2 —42-year-old woman with celiac disease. Photograph of
histologic specimen obtained during duodenal biopsy shows Marsh type 2
lesions, which are cryptic and hyperplastic (arrows) and have
increased number of mitoses (arrowheads) (up to three per crypt). (H
and E, x100)
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Fig. 3 —53-year-old man with celiac disease. Photograph of histologic
specimen obtained during duodenal biopsy shows Marsh type 3C lesions, which
are characterized by total absence of villi (total villous atrophy), and
numerous intraepithelial lymphocytes that have hyperplastic granular
components (arrows) and distorted profile. (H and E, x100)
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Clinical Features
Celiac disease can cause a spectrum of symptoms ranging from a subclinical
form, which may be incidentally detected in patients without symptoms, to the
classic malabsorptive form
[10,
11]. Laboratory tests show
variable degrees of malabsorption, including ane mia secondary to mal
absorption of iron, folic acid, or vitamin B12; hypocalcemia; hypo
albuminemia; and vitamin deficit. Celiac disease also can be associated with
thrombocytosis, thrombocytopenia, leuko penia, venous thromboembolism, hypo
splenism, and immunoglob ulin A deficiency. Gastro intestinal neoplasms
especially are found in patients with persisting mucosal injury who do not
completely adhere to a gluten-free diet
[12].
Refractory celiac disease (also called refractory sprue) is defined as
symptomatic severe enteritis that does not respond to at least 6 months of a
strict gluten-free diet. Patients with this condition are at high risk of
complications. Refractory celiac disease syndromes are classified into types 1
and 2. Type 1 has a normal intraepithelial lymphocyte phenotype, and type 2 is
characterized by clonal expansion of an aberrant intraepithelial lymphocyte
population [3]. Unlike type 1
refractory celiac disease, which has a relatively benign course, type 2
refractory celiac disease has prelymphoma potential
[13]. Besides the general
complications of celiac disease, which include intestinal ulcerations, pneu
matosis intestinalis, pneumo peritoneum, hypo splenism, hepatobiliary disease,
neurop athy, and malignant neoplasms, com pli cations such as ulcerative
jejunoileitis, cavi t ating mesenteric lymphadenopathy syn drome, and
enteropathy-associated T-cell lymphoma are found only in patients with
refractory celiac disease [14,
15]. It also has been found
[13] that the increased risk
of enteropathy-associated T-cell lymphoma specifically involves patients with
type 2 refractory celiac disease and not patients with type 1 disease (52% vs
0%).
Malignant neoplasms are the most common cause of death in celiac disease
[12,
16]. Enteropathy-associated
T-cell lymphoma is the cause of death in 46% of patients with type 2
refractory celiac disease
[13]. Because of an increased
incidence of gastrointestinal neoplasms, mainly adeno carcinoma of the small
bowel and enteropathy-associated T-cell lymphoma, the mortality rate among
adult patients with celiac disease is almost double the rate in the general
population [16]. Therefore,
among patients with known celiac disease who strictly follow a gluten-free
diet, abdominal pain should always raise suspicion of malignant neoplasia.
Definitive Diagnosis of Celiac Disease
The definitive diagnosis of celiac disease in adults requires both
endoscopic duodenal biopsy that shows characteristic histologic findings and a
favorable response to a gluten-free diet
[3,
17]. It is important to
understand that because the histologic findings in celiac disease are
characteristic but not specific, a favorable response to a gluten-free diet is
needed for a definite diagnosis. Total villous atrophy, which was the only
histologic feature compatible with the diagnosis of celiac disease in the
past, is now considered the terminal stage of evolving intestinal mucosal
damage [1,
17].
Basic MDCT Enteroclysis Features and Correlation with Histopathologic and Endoscopic Findings
MDCT Enteroclysis Protocol
MDCT enteroclysis examinations are routinely performed with the same
protocol. A dedicated 8-French nasojejunal tube (815 NF, Biosphere Medical) is
advanced beyond the duodenojejunal flexure under fluoroscopic guidance. Room
temperature water is infused with a pressure-controlled electric pump at a
rate of 150–160 mL/min. The pressure is controlled to be less than 1,600
mm Hg. The mean quantity of water is 1,600 mL with a total water volume less
than 2,000 mL. Approximately 1 minute before the start of image acquisition,
15 mL of an antispasmodic solution that contains 10 mg of tiemonium
methylsulphate (Viscéralgine, Laboratoires Organon) is administered IV
to reduce motion artifacts caused by small-bowel peristalsis
[18,
19]. Other antispasmodic a
gents, such as N-butylscopolammonium bro mide (Buscopan, Boehringer
Ingelheim) at a dose of 20 mg or glucagon (GlucaGen, Novo Nordisk) at a dose
of 1 mg [20,
21], are available for
reducing small-bowel peristalsis. Anti spasmodic agents must be used with
caution, however, because of possible contra indications.
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Fig. 4A —47-year-old man with unknown celiac disease. Coronal CT
reformation of MDCT enteroclysis scan shows reversed jejunoileal fold pattern
consisting of rarity of jejunal folds (arrows) associated with
greater number of ileal folds (arrowheads). Appearance suggests
celiac disease.
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Patients are placed in the supine position headfirst with respect to the
scanner gantry. We use a single-source 4-MDCT scanner (Somatom Plus 4 Volume
Zoom, Siemens Medical Solutions) with the following parameters: field of view,
279–380 mm; beam collimation, 10 mm (4 x 2.5 mm configuration);
tube potential, 120 kVp; gantry revolution time, 0.5 second; table speed, 12.5
mm per rotation, resulting in a beam pitch of 1.25. An online real-time
anatomy-adapted attenuation-based tube-current modulation technique (CareDose,
Siemens Medical Solutions) is used with the tube current set to 120–170
effective mAs. At the start of the procedure, an automated power injector is
used for IV injection of 120 mL of nonionic iodinated contrast material
through a 20-gauge catheter into an antecubital vein at a rate of 3 mL/s.
The delay between the start of contrast administration and the start of CT
acquisition varies depending on the clinical indication. For patients referred
because of suspected tumor complicating celiac disease, two imaging passes are
performed: one pass during the arterial phase with bolus tracking and
automated triggering (CARE Bolus, Siemens Medical Solutions) and the other
pass during the enteric phase. For patients with no suspected tumor, a single
pass is performed 50 seconds after the start of bolus injection, when
bowel-wall enhancement is optimal (enteric phase)
[22]. The bolus-tracking
technique is used to define the optimal time after IV administration of
iodinated contrast material that would provide optimal contrast enhancement of
the small bowel during the arterial phase. MDCT enteroclysis is performed from
the dome of the liver to the lower margin of the symphysis pubis in a
cephalocaudal direction after breath-hold instruction is given.
Continuous infusion of water through the nasojejunal tube is maintained
during image acquisition. Most patients tolerate the procedure well
[18]. The axial data are
reconstructed twice with a B30 soft-tissue reconstruction kernel, first with
5-mm thickness at 5-mm intervals and then with a 2.5-mm thickness at 3-mm
intervals. The second set of reconstructed axial images is reformatted in the
coronal and sagittal planes with a thickness of 3 mm at 3-mm intervals.
Multiplanar reformatted views are rapidly made interactively with a
commercially available attached workstation. Processing of reformatted images
takes less than 10 minutes. Both transverse and multiplanar reformatted MDCT
enteroclysis images are originally acquired with a standard window level (50
HU) and width (350 HU); specific adjustments are made for the patient being
examined.
Basic MDCT Enteroclysis Features: Small-Bowel Abnormalities
A reversed jejunoileal fold pattern, which presumably is caused by a
compensatory response of the ileum to severe villous atrophy of the proximal
small bowel, is highly suggestive of celiac disease
[23]. This feature associates
ileal jejunization with a major loss of jejunal folds. A greater number of
ileal folds are observed in contrast to a rarity or even absence of jejunal
folds. Loss of jejunal folds are radiologic evidence of celiac disease with
total villous atrophy in most cases
[24]. These features are well
visualized at MDCT enteroclysis (Fig.
4A,
4B).
Other intraabdominal abnormalities can be found in adult patients with
celiac disease. The most frequent abnormalities include mesenteric
lymphadenopathy and engorge ment of mesenteric vessels
[25,
26]
(Fig. 5). Engorgement of
mesenteric vessels correlates with increased blood flow on Doppler studies
[27]. Findings such as
bowel-wall thickening and ascites are less frequent
[23,
25,
26,
28]. Lymphadenopathy is more
frequently found in patients with refractory type 2 celiac disease and in
patients with enteropathy-associated T-cell lymphoma
[26]. On conventional MDCT
(without enteroclysis), loops of small bowel have an abnormally enlarged
diameter, most often in conjunction with an excess of intraintestinal fluid.
Because the technique distends the small bowel, spontaneous distention due to
disease cannot be evaluated with MDCT enteroclysis
[25]. The presence of
intramural fat in the submucosal layers of the duodenum and jejunum has been
reported to be a feature suggestive of the diagnosis of celiac disease, being
found in 13.4% of 82 patients with celiac disease in one study
[29].
Histopathologic, Push Enteroscopic, and Wireless Capsule Endoscopic Findings
The typical intestinal endoscopic features of celiac disease include a
duodenal micronodular or mosaic pattern, reduction of duodenal and jejunal
folds, and loss or scalloping of duodenal and jejunal folds. No definite
correlation exists between the histologic and endoscopic findings. Wireless
capsule endoscopy and push enteroscopy reveal various features when atrophic
lesions are histologically present. The mosaic pattern is more frequent than
the nodular pattern (Figs. 6
and 7).
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Fig. 6 —57-year-old man with celiac disease. Push enteroscopic image
shows nodular pattern (arrowheads) of jejunal mucosa consistent with
celiac disease. Diagnosis was confirmed at histopathologic analysis of biopsy
specimen.
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Fig. 7 —37-year-old woman with celiac disease. Wireless capsule
endoscopic image shows atrophic jejunal mucosa (arrowheads), which
suggests presence of celiac disease. Diagnosis was confirmed at
histopathologic analysis.
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Complications of Celiac Disease
Transient Small-Bowel Intussusception
Transient intussusception in celiac disease is rarely symptomatic and
presumably is related to uncoordinated peristalsis in dilated flaccid loops of
small bowel [24]. It must be
emphasized that transient small-bowel intussusception also is visible on CT
images obtained without enteroclysis, having an estimated frequency of 21%
[25]. On MDCT enteroclysis
scans, transient small-bowel intussusception is correctly identified owing to
the presence of a typical bowel-within-bowel feature, which produces a target
sign with or without a fatty component
[30]. Transient
intussusception is more frequently found in patients with severe celiac
disease (i.e., type 2 refractory celiac disease)
[26]. When the intussusception
is less than 3 cm long, occurs in the absence of a lead-point tumor, and is
not responsible for small-bowel obstruction at MDCT enteroclysis, the findings
are consistent with transient self-limiting small-bowel intussusception
[31]
(Fig. 8). However, because
gastrointestinal malignant tumors can cause intussusception in adult patients
with celiac disease, MDCT enteroclysis images have to be carefully analyzed
for confident exclusion of lymphoma and carcinoma
[18] (Fig.
9A,
9B,
9C).
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Fig. 8 —70-year-old man with transient small-bowel intussusception in
association with celiac disease. Axial MDCT enteroclysis scan shows target
sign (arrowheads) corresponding to transient small-bowel
intussusception. No tumor is present.
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Fig. 9A —82-year-old woman with ileal lymphoma-associated celiac
disease. Axial MDCT enteroclysis scan shows target sign (arrows)
corresponding to small-bowel intussusception secondary to lymphoma
(arrowhead). Tumor was located in ileum.
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Fig. 9B —82-year-old woman with ileal lymphoma-associated celiac
disease. Axial MDCT enteroclysis scan at lower level than A shows
typical bowel-within-bowel feature (arrows) and intussusception
longer than 3 cm.
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Ulcerative Jejunoileitis
Ulcerative jejunoileitis consists of mul tiple benign ulcers of variable
depth. The exact origin of these ulcers is unclear. This condition can
manifest acutely or develop gradually. It occurs predominantly in the jejunum,
occasionally in the ileum, and rarely in the colon, and it mostly appears in
patients with type 2 refractory celiac disease
[14,
15]. Patients most frequently
present with fever, weight loss, abdominal pain, diarrhea, and anorexia. The
symptoms of ulcerative jejunoileitis are similar to those of celiac disease
complicated by a malignant neoplasm
[32]. On small-bowel
follow-through images, the ulcers may be visible as focal constrictions. A
spiculated pattern and alternating areas of narrowing and dilatation also have
been seen with this technique
[24]. It is commonly
acknowledged, however, that small-bowel enteroclysis is more efficient than
small-bowel follow-through for the detection of ulcerations
[33]. On MDCT enteroclysis
scans, ulcerative jejunoileitis appears as circumferential thickening of the
bowel wall with a bilaminar configuration that combines mucosal
hyperenhancement and thickening of the small-bowel wall with soft-tissue
attenuation [18] (Fig.
10A,
10B,
10C,
10D). This MDCT enteroclysis
finding is highly suggestive of the diagnosis of ulcerative jejunoileitis in
adult patients with celiac disease
[18]. Complications of
ulcerative jejunoileitis include hemorrhage, perforation, and small-bowel
obstruction. Some patients have coexisting lymphoma, or lymphoma develops
later. Therefore, careful histopathologic examination and immunologic staining
of specimens from patients with ulcerative jejunoileitis are recommended to
identify occult lymphoma that may necessitate additional therapy.
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Fig. 10A —48-year-old man with ulcerative jejunoileitis associated with
refractory celiac disease. Axial MDCT enteroclysis scan depicts
circumferential thickening (arrows) of ileal wall that exhibits
stratification with bilaminar appearance. Hyperenhancing internal layer is
present in association with soft-tissue-attenuation external layer. There is
no evidence of malignancy. (Reprinted with permission from Boudiaf M, Jaff A,
Soyer P, Bouhnik Y, Hamzi L, Rymer R. Small-bowel diseases: prospective
evaluation of multi-detector row helical CT enteroclysis in 107 consecutive
patients. Radiology 2004; 233:338–344
[18])
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Fig. 10D —48-year-old man with ulcerative jejunoileitis associated with
refractory celiac disease. Axial MDCT enteroclysis scan obtained after partial
resection of ileum shows findings (arrowheads) similar to those
observed preoperatively (i.e., stratification with bilaminar appearance) and
that are highly suggestive of recurrence at site of anastomosis. Diagnosis of
recurrence was confirmed histologically.
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Enteropathy-Associated T-Cell Lymphoma
Lymphoma is the most common malignant disease complicating celiac disease
[12,
34]. Most lymphomas are of
T-cell origin, but gastrointestinal B-cell lymphoma and extraintestinal
lymphoma also are found [35].
In the general population, T-cell lymphoma of the gastrointestinal tract is
rare, representing fewer than 1% of non-Hodgkin's lymphomas
[32,
36]. In patients with celiac
disease, lymphoma has three clinical patterns. It can cause abdominal pain and
diarrhea despite strict adherence to a gluten-free diet; it can cause bowel
perforation, obstruction, and hemorrhage; or it can antedate clinical
recognition of celiac disease
[37]. Enteropathy-associated
T-cell lymphoma typically forms circumferential ulcers with short strictures
in the proximal small bowel.
The MDCT enteroclysis appearance of intestinal lymphoma complicating celiac
disease is variable, including a nodular appearance, an exophytic mass, or
circumferential thickening of the small-bowel wall. An aneurysmal pattern,
which combines cavitary dilatation of the small-bowel lumen and annular wall
thickening, can be observed (Fig.
11A,
11B,
11C). The presence of this
so-called aneurysmal dilatation sign
[38] suggests the diagnosis of
enteropathy-associated T-cell lymphoma
[39] but also is found in
cases of small-bowel tumors not related to celiac disease, such as
adenocarcinoma [19], lymphoma
not related to enteropathy
[39], and mesenchymal tumors
[40]. Lymphoma usually
involves the small bowel in either a multifocal or a diffuse distribution. A
short segment occasionally is involved.
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Fig. 11A —77-year-old woman with jejunal T-cell lymphoma associated
with refractory celiac disease. Axial MDCT enteroclysis scan shows proximal
jejunal mass (arrowheads) with pseudoaneurysmal pattern suggesting
malignant tumor.
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Fig. 11B —77-year-old woman with jejunal T-cell lymphoma associated
with refractory celiac disease. Coronal CT reformation of MDCT enteroclysis
scan clarifies presence of tumor (arrowheads) with irregular
margins.
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Although detection of enlarged mesenteric lymph nodes on MDCT enteroclysis
does not necessarily indicate the presence of lymphoma in patients with celiac
disease and can be found in cases of mesenteric panniculitis
[41], this finding raises
suspicion of lymphoma that has to be ruled out
(Fig. 12). In some cases,
enlarged mesenteric lymph nodes may be the single clue to the diagnosis of
enteropathy-associated T-cell lymphoma in the absence of endoscopically
visible small-bowel tumor
[42]. Therefore, in the
evaluation of patients with type 2 refractory celiac disease who are at high
risk of enteropathy-associated T-cell lymphoma, biopsy of enlarged mesenteric
lymph nodes is mandatory to exclude this serious complication
[42].
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Fig. 12 —40-year-old man with enteropathy-associated T-cell lymphoma
associated with celiac disease. Axial MDCT enteroclysis scan obtained without
small-bowel distention shows multiple enlarged mesenteric lymph nodes
(arrowheads), which correspond to T-cell lymphomatous involvement.
Histopathologic analysis after small-bowel biopsy showed total villous atrophy
and major intraepithelial infiltration by aberrant (CD3 positive, CD8
negative) clonal intraepithelial proliferation of T cells.
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Carcinoma
Carcinomas of the esophagus, pharynx, duodenum, jejunum, and rectum are
found more frequently in patients with celiac disease than in the general
population [12].
Adenocarcinoma of the small bowel may arise through an adenoma–carcinoma
sequence [43]. Therefore, MDCT
enteroclysis should be performed to rule out carcinoma in patients with celiac
disease who have symptoms despite adherence to a strict gluten-free diet (Fig.
13A,
13B).
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Fig. 13A —55-year-old woman with jejunal adenocarcinoma associated with
celiac disease. Axial MDCT enteroclysis scan shows large jejunal mass
(arrowheads) displaying aneurysmal pattern suggestive of malignant
small-bowel tumor. Tip of nasojejunal tube (arrow) is evident.
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Hyposplenism
Celiac disease is a well-known cause of splenic atrophy, found in
30–50% of adult patients with celiac disease
[24] (Fig.
14A,
14B,
14C). It has been found
[44] that the mean splenic
volume in a population of adult patients with celiac disease is 162
cm3 (range, 37–321 cm3); in the healthy
population, the mean volume is 215 cm3 (range, 107–341
cm3). The degree of splenic atrophy correlates with the severity of
disease [26]. Because splenic
size has been found to correlate with splenic function, it is not surprising
that there is a trend toward serious infectious diseases due to
Streptococcus pneumoniae in these patients
[45,
46].
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Fig. 14A —37-year-old man with cavitating mesenteric lymphadenopathy
syndrome and splenic atrophy associated with celiac disease. Cavitating
lymphadenopathy is most often mesenteric, but other locations are possible.
Axial MDCT enteroclysis scan shows mesenteric lymph node with markedly
hypoattenuating center (arrowhead).
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Fig. 14B —37-year-old man with cavitating mesenteric lymphadenopathy
syndrome and splenic atrophy associated with celiac disease. Cavitating
lymphadenopathy is most often mesenteric, but other locations are possible.
Axial MDCT enteroclysis scan shows associated small spleen
(arrowhead).
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Fig. 14C —37-year-old man with cavitating mesenteric lymphadenopathy
syndrome and splenic atrophy associated with celiac disease. Cavitating
lymphadenopathy is most often mesenteric, but other locations are possible.
Histologic photograph shows lymph node with central acidophilic necrosis in
association with peripheral rim (arrowheads). (H and E,
x25)
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Cavitating Mesenteric Lymphadenopathy Syndrome
As described by Matuchansky et al.
[47] the association of
villous atrophy, splenic atrophy, and mesenteric cavitating lymphadenopathy is
highly suggestive of the diagnosis of celiac disease. If the association is
present, lymph nodes in the jejunal and ileal mesentery are affected by
acidophilic central liquid necrosis and have a peripheral fibrotic rim (Fig.
14A,
14B,
14C). At MDCT enteroclysis,
the central areas of such involved lymph nodes have an attenuation of 0 HU or
less. In general, such lymphadenopathy is found in association with marked
villous atrophy. Detection of these findings should raise suspicion of
lymphoma, but an association between the two entities is not the rule
[37].
Pneumatosis
Pneumatosis intestinalis is defined by the presence of gas within the bowel
wall. In the general population, pneumatosis intestinalis is a rare finding
suggesting the presence of potentially alarming conditions, such as acute
small-bowel ischemia, that necessitate surgery
[48]. In the setting of celiac
disease, it is speculated that pneumatosis may reflect dissection of
intraluminal gas into the inflamed small-bowel wall without accompanying
intraabdominal abnorm alities
[49]. In addition, in patients
with celiac disease, MDCT can show pneumoperitoneum, which may be due to
subserosal rupture of bubbles into the peritoneum. Therefore, in patients with
celiac disease, pneumatosis intestinalis may be found in association with
pneumoperitoneum in the absence of small-bowel ischemia or perforation
[49]. On abdominal
radiographs, follow-through studies, and barium enema images, it may be
difficult to differentiate gas within the gastrointestinal wall from
intraluminal gas. In this regard, MDCT is more discriminating than
conventional imaging.
In adult patients with celiac disease, pneumatosis intestinalis is not
always an indication for bowel resection; as a rule, the presence of
pneumatosis intestinalis does not correlate with the presence of bowel ische
mia. A literature review [49]
on the rare finding of pneumatosis intestinalis in the setting of celiac
disease showed that in all reported cases, even when pneumatosis was accom
panied by pneumoperitoneum, these alarm ing findings were proven to be of
benign origin; that is, there was no evidence of bowel ischemia, perforation,
or peritonitis (Fig. 15). As a
consequence, the presence of pneumo peritoneum in adult patients with celiac
disease must be integrated into a more com prehensive evaluation that includes
clinical examination of the abdomen to avoid unnec essary surgery.
Conservative management is needed when no clinical features consistent with
peritonitis are present
[50].
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|
Fig. 15 —33-year-old woman with celiac disease. Axial MDCT scan
obtained without small-bowel distention shows gas (arrowheads) in
bowel wall that resolved spontaneously. Patient was treated conservatively in
absence of clinical symptoms.
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Associated Hepatobiliary Disease
Celiac disease can be associated with a variety of hepatobiliary diseases.
Hepatic steatosis can be associated with or be the revealing symptom of celiac
disease. It manifests as mild biochemical ab normalities in the absence of
clinically visible cholestasis
[51]. Venous thrombosis
involving the portal vein or hepatic veins
[7] also may be found. A
possible association between celiac disease and primary biliary cirrhosis has
been suggested [52] because
the two diseases have been found together in a few cases. When primary biliary
cirrhosis is suspected because of alterations in results of hepatic tests, MR
cholangiography is more effective than MDCT enteroclysis for discerning the
biliary disease. Cases have been reported
[53] in which nodular
regenerative hyperplasia of the liver has been found in patients with celiac
disease.
Advantages and Limitations of MDCT Enteroclysis over Other Techniques
In addition to MDCT enteroclysis, CT enterography and MR enterography have
shown promise in the evaluation of the small bowel of adult patients with
celiac disease
[54–56].
In both techniques, effective small-bowel distention is achieved with oral
hyperhydration, obviating nasojejunal tube placement and increasing patient
tolerance. The role and potential of the two techniques in the elective
investigation of celiac disease have to be further determined and compared
with those of MDCT enteroclysis. MDCT enteroclysis can depict extraintestinal
features, such as enlarged mesenteric lymph nodes corresponding to cavitating
lymphadenopathy and lymphomatous involvement, that are not seen with
small-bowel radiography, small-bowel enteroclysis, or endoscopic examination
[57]. MDCT enteroclysis can be
used to exclude small-bowel stricture before wireless capsule endoscopy,
limiting the risk of capsule retention
[33]. Finally, MDCT
enteroclysis findings suggest the diagnosis in patients with unknown celiac
disease because the images show the typical reversed jejunoileal fold pattern
and other suggestive features. A limitation, however, is that MDCT
enteroclysis does not depict subtle mucosal changes such as ulcerations, which
can be seen with endoscopy
[42]. This limitation is
important because these ulcerations may indicate the presence of ulcerative
jejunoileitis or enteropathy-associated T-cell lymphoma.
Wireless capsule endoscopy shows promise in the evaluation of adult
patients with celiac disease
[42,
58]. Early reports showed that
wireless capsule endoscopy reveals subtle mucosal changes such as ulcerations
in 45% of cases [59] and
facilitates detection of enteropathy-associated T-cell lymphoma, which is not
seen with MDCT enteroclysis in the early stage
[42]. As a consequence, it may
be possible that in the near future, wireless capsule endoscopy will be used
to screen for cancer. To our knowledge, however, no study results validate
this strategy. Wireless capsule endoscopy has proven utility in the evaluation
of patients with celiac disease who report abdominal pain or present with
occult bleeding [59]. In
addition, findings at wireless capsule endoscopy are helpful for planning
further diagnostic procedures, especially push or double-balloon enteroscopy,
to obtain specimens for confirming the presence of enteropathy-associated
T-cell lymphoma or adenocarcinoma
[42,
60,
61]. The use of wireless
endoscopy is limited because assessment is incomplete in 36% of cases
[33,
42]. In addition, wireless
capsule endoscopy may have nonspecific findings, such as mucosal scratches and
nonspecific ulcerations, that necessitate further diag nostic tests for a
definite diagnosis [33]. In
this regard, small-bowel enteroclysis is performed to confirm or exclude the
presence of mucosal abnormality
[62].
We and others [18,
33,
63] have found conventional
small-bowel radiography without enteroclysis to be of limited value. This lack
of value is especially true in cases of subtle mucosal lesions, which are
frequently missed with radiography but are well depicted with small-bowel
enteroclysis [63]. For this
reason, we no longer use small-bowel radiography in the evaluation of patients
with celiac disease.
Double-balloon enteroscopy and push enteroscopy are promising approaches to
investigation of the small bowel
[59,
64], but their value and the
complications in adult patients with celiac disease are not known
[33,
42]. Both techniques are
effective in detection of ulceration and enteropathy-associated T-cell
lymphoma of the proximal jejunum or distal ileum
[65], but study of the small
bowel is incomplete in as many as 40% of cases
[61], so serious complications
can be overlooked. This limitation also applies to push enteroscopy, which
does not show signs of focal superimposed disease such as lymphoma, carcinoma,
and ulcerative jejunoileitis when the disease is located too far from the
duodenojejunal junction or too far from the ileocecal valve
[33]. Because of invasiveness,
both techniques are reserved for patients with refractory celiac disease and
for patients with a history of enteropathy-associated T-cell lymphoma
[66].
Conclusion
The value of MDCT enteroclysis in the diagnosis of complicated celiac
disease is not fully known because comparative studies, including
enteroclysis, wireless capsule endo scopy, and MDCT enteroclysis, are lacking.
Many of the complications of celiac disease, however, can be recognized
because of their characteristic appearance at MDCT enteroclysis. Familiarity
with the appearance of the complications of celiac disease can aid in
appropriate planning of further diagnostic procedures and may improve patient
care.
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Abstract
Introduction
