DOI:10.2214/AJR.05.0511
AJR 2006; 187:522-531
© American Roentgen Ray Society
MR Enteroclysis of Inflammatory Small-Bowel Diseases
Bart M. Wiarda1,
Ernst J. Kuipers2,
Martin A. Heitbrink1,
Arnoud van Oijen3 and
Jaap Stoker4
1 Department of Radiology, Medical Center Alkmaar, Wilhelminalaan 12, 1815 JD
Alkmaar, The Netherlands.
2 Department of Gastroenterology and Hepatology, Erasmus University Medical
Center, Rotterdam, The Netherlands.
3 Department of Gastroenterology, Medical Center Alkmaar, Alkmaar, The
Netherlands.
4 Department of Radiology, Amsterdam Medical Center, University of Amsterdam,
Amsterdam, The Netherlands.
Received March 23, 2005;
accepted after revision May 29, 2005.
Address correspondence to B. M. Wiarda.
Abstract
OBJECTIVE. MR enteroclysis has been introduced in the workup of
small-bowel diseases. The major advantage of this technique over others is the
combined visualization of luminal, mural, and extramural abnormalities. In
this article we propose an MR enteroclysis protocol, present a stepwise
approach for evaluation of these examinations, and discuss the different
inflammatory conditions that can be detected.
CONCLUSION. MR enteroclysis can be considered the current first-line
imaging technique for inflammatory small-bowel disorders.
Keywords: enteroclysis gastrointestinal radiology inflammatory bowel disease MRI small bowel
Introduction
MRI with enteroclysis can be used as the initial imaging method for
small-bowel diseases. The enteroclysis technique enables optimal distention of
the small bowel, which results in accurate visualization of stenoses and
obstructions [1]. The
high-volume-induced reflex atony leads to well-defined visualization of the
bowel wall almost without peristalsis-induced artifacts. MR enteroclysis has
shown excellent correlation with conventional enteroclysis in grading
small-bowel obstruction and functional information while also providing
transmural and extramural visualization
[2].
MRI Technique
After placement of a nasoduodenal catheter under fluoroscopy, the
small-bowel is distended with 1,000-3,000 mL of methylcellulose (0.5%) and
water solution using an electric infusion pump (Roentgen Contrast Mittel
Pumpe, Nicholas), located outside the scanner room, at an infusion rate of
80-200 mL/min. The MR protocol (Table
1) consists of MR fluoroscopy using a thick-slab 50-mm coronal
HASTE sequence with fat saturation, starting at the beginning of the infusion
and repeated every 8 seconds during normal breathing. This allows for the
study contrast passage speed, luminal distention, peristalsis, and retrograde
filling of the stomach. Subsequently, every 5 minutes, depending on the degree
of distention observed from the HASTE images, coronal and axial true fast
imaging with steady-state precession (FISP) sequences with fat saturation are
performed with a slice thickness of 5 mm to study morphologic changes.
Finally, with maximal distention, multislice HASTE images with fat saturation
and unenhanced and enhanced (0.1 mmol/kg gadolinium) coronal and axial fast
low-angle shot (FLASH) 2D images with fat saturation are obtained 60 seconds
after contrast injections are made.
Normal Appearance
The coronal thick-slab HASTE images give valuable information, both for
identifying fixed bowel loops and luminal stenosis and for timing of
morphologic sequences with optimally distended bowel loops (Figs.
1A,
1B,
1C, and
1D). The higher spatial and
contrast resolution of the morphologic series facilitates evaluation of
surface structures (e.g., folds, ulcerations), bowel wall morphology, and
thickness and extramural abnormalities (e.g., lymphadenopathy, increased
mesenteric vascularization, and abscess)
(Fig. 2). Bowel wall thickness
larger than 3 mm must be considered abnormal
[3]. We used morphologic
sequences to identify and localize abnormalities. Enhanced T1-weighted
fat-saturation series are used to establish enhancement of the abnormalities
and evaluate disease activity, especially in Crohn's disease.

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Fig. 1A 63-year-old woman with suspected Crohn's disease. Coronal
thick-slab HASTE fat-saturation image shows adequate distention of jejunal
loops (arrowheads) but collapsed or stenotic terminal ileum
(arrow).
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Fig. 1B 63-year-old woman with suspected Crohn's disease. Coronal
true fast imaging with steady-state precession (FISP) fat-saturation image
obtained at same time as A shows wall thickening of terminal ileum
(arrows) with collapsed or stenotic lumen. Note normal folds without
wall thickening of jejunal loops (arrowheads).
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Fig. 1D 63-year-old woman with suspected Crohn's disease. Coronal
true FISP fat saturation image obtained at same time as C shows
distended terminal ileum with wall thickening without stenosis
(arrow). Thick-slab HASTE imaging facilitates optimal timing of true
FISP fat-saturation sequences with maximal distention. This increases
certainty of grading small-bowel stenosis.
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Fig. 2 35-year-old woman with healthy-appearing small-bowel. During
optimal distention, coronal true fast imaging with steady-state precession
fat-saturation image shows normal folds in jejunum (arrowheads) and
no stenosis or bowel wall thickening in terminal ileum (arrows).
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Crohn's Disease
Crohn's disease can be localized in every segment of the small bowel, with
a predilection for the terminal ileum. The major advantage of MR enteroclysis
over other techniques for detection of small-bowel abnormalities is
visualization of the complete small bowel and extramural disease
manifestations without the use of ionizing radiation. The imaging protocol
enables identification of both the diagnosis and the extent of the disease.
Functional information can be used to differentiate between collapsed normal
bowel wall, active disease, inactive disease, and bowel wall stenosis (Figs.
3A and
3B). Within the morphologic
series, the most important characteristics for disease activity (i.e., bowel
wall edema, ulcerations, and increased mesenteric vascularization [comb sign])
are contained (Figs. 4A and
4B). The contrast-enhanced
series contributes to the differentiation between active and chronic disease.
Specific characteristics for Crohn's diseasethat is, creeping fat
(increased mesenteric fat), skip lesions, and fistulascan be identified
on both the morphologic and contrast-enhanced series. Characteristics of
active inflammation of the small bowel are bowel wall edema, ulcerations,
increased mesenteric vascularization, increased enhancement of the bowel wall,
and mesenteric lymph nodes [4]
(Figs. 5A,
5B, and
5C). In acute inflammation,
the bowel wall can have a layered pattern. A double-halo sign is related to
submucosal edema (Figs. 6A,
6B, and
6C). Inactive disease is
characterized by no abnormalities (i.e., optimal distention of bowel loops,
healthy peristalsis, and no stenosis) or bowel wall thickening with relative
low signal intensity representing fibrosis with limited, homogeneous contrast
enhancement (Fig. 7). Fat
accumulation in the submucosa can be found in the subacute or chronic stage
(Fig. 8). MRI can show
infiltration of mesenteric fat that may evolve into a fistula
(Fig. 9). Intraluminal fluid
and the use of an IV contrast medium can improve the detection of fistulas.
Abscesses are more readily identified on the sequences performed after the
injection of IV contrast medium (Fig.
10). MRI also allows the evaluation of complications associated
with Crohn's disease, including intussusception, stricture formation, and
carcinoma.

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Fig. 3A 31-year-old man with known Crohn's disease. Coronal true fast
imaging with steady-state precession (FISP) and fat saturation shows almost no
distention of jejunum (arrowheads) and suggesting a wide-open
terminal ileum (arrows).
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Fig. 3B 31-year-old man with known Crohn's disease. Coronal true FISP
image obtained with fat saturation during optimal distention shows normal
jejunal loops (arrowheads) and short segment of bowel wall thickening
of terminal ileum with high-grade stenosis (arrows). Optimal
distention contributes to differentiation between stenosis and collapsed bowel
loops.
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Fig. 4A 38-year-old woman with suspected Crohn's disease. Coronal
true fast imaging with steady-state precession (FISP) and fat saturation
without optimal distention of small-bowel loops shows wall thickening of ileum
(arrows), with increased mesenteric vascularization (comb sign,
arrowheads) and creeping fat (dot).
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Fig. 4B 38-year-old woman with suspected Crohn's disease. Coronal
true FISP fat-saturation image obtained during optimal distention shows that
thickened ileum loop has intermediate- to high-grade stenosis
(arrows). In accordance with A, comb sign
(arrowheads) and creeping fat (dot) are visualized.
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Fig. 5A 21-year-old man with proven Crohn's disease. Coronal true
fast imaging with steady-state precession (FISP) and fat saturation shows two
segments of bowel wall thickening, mucosal ulcerations (arrowhead),
and stenosis with prestenotic dilatation (thick solid arrow) of
ileum. This figure also shows fibrofatty proliferation (creeping fat,
dot), mesenteric lymph nodes (thin arrow), and increased
mesenteric vascularity (comb sign, open arrow). Distal from diseased
proximal segment is second segment of thickened ileum loop
(asterisk): skip lesion.
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Fig. 5B 21-year-old man with proven Crohn's disease. Coronal fast
low-angle shot (FLASH) 2D fat-saturation image obtained after contrast
injection shows increased contrast enhancement of two thickened segments of
small-bowel loops (skip lesions, arrows) and increased mesenteric
vascularity (comb sign, open arrow).
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Fig. 6A 42-year-old man with known Crohn's disease. Axial true fast
imaging with steady-state precession (FISP) and fat saturation shows diffuse
thickening, edema (arrow), and irregular mucosa of mainly mucosa of
bowel wall of ileum. Small amount of ascites (asterisk) was found in
this region.
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Fig. 6B 42-year-old man with known Crohn's disease. Axial enhanced
fast low-angle shot (FLASH) 2D fat-saturation image shows diffuse thickening,
irregular mucosa (arrowhead), and intense contrast enhancement of
mainly mucosa of bowel wall of ileum (arrow). This implies active
disease. Active disease is also visible in sigmoid and rectum (open
arrows).
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Fig. 7 46-year-old woman with midgut malrotation type 1 and
suspected Crohn's disease. Coronal true fast imaging with steady-state
precession (FISP) and fat saturation shows thickening of terminal ileum
(arrow), without increased contrast enhancement (not shown). Wall
thickness of cecum (arrowhead) is normal. Absence of ulcerations,
bowel wall edema, and increased contrast enhancement are features of inactive
Crohn's disease.
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Fig. 8 60-year-old man with proven Crohn's disease. Coronal true
fast imaging with steady-state precession (FISP) and fat saturation shows fat
accumulation in submucosa (arrowhead), which implies subacute or
chronic disease stage. Fistula between two ileum loops (arrow) is
also visualized.
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Fig. 9 45-year-old woman with proven Crohn's disease. Axial true
fast imaging with steady-state precession (FISP) and fat saturation shows
fistula between small bowel and soft-tissue layers of abdominal wall
(arrow).
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Fig. 10 37-year-old woman with known Crohn's disease. Axial fast
low-angle shot (FLASH) 2D fat-saturation image obtained after contrast
injection shows thickened ileum loop with intense contrast enhancement
(arrow). On left side of this loop is small abscess
(arrowhead).
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Fig. 11 75-year-old woman with recently proven celiac disease.
Coronal true fast imaging with steady-state precession (FISP) and fat
saturation shows decrease in jejunal folds (arrowheads) and increase
in ileal folds ("ileal jejunization," arrows), which are
characteristic features of celiac disease.
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Fig. 12 31-year-old woman with abdominal pain and diarrhea. Axial
true fast imaging with steady-state precession (FISP) and fat saturation shows
diffuse thickened jejunum loop (arrow) with edema of all wall layers,
especially serosa. Without proven cause, her complaints resolved
spontaneously. In follow-up, no relapse of complaints is established. This
case is example of jejunitis without proven cause.
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Fig. 13 65-year-old man with left flank pain and infectious
jejunitis. Axial true fast imaging with steady-state precession (FISP) and fat
saturation shows thickened jejunal folds (arrows). Normal folds in
distal jejunum (arrowhead) are shown. Parapelvic cyst can be seen in
right kidney. Stool of this patient was giardiasis-positive.
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Other Inflammatory Small-Bowel Diseases
Other inflammatory small-bowel diseases can have features that resemble
Crohn's disease, such as wall thickening, loss of folds, ulcerations,
stenosis, and increased mesenteric vascularization (comb sign). Identification
of disease-specific features is therefore important in the diagnosis of
Crohn's disease and includes creeping fat, skip lesions, and fistulas.
Celiac disease is a gluten-sensitive malabsorption syndrome, characterized
by villous atrophy and crypt hyperplasia of the small intestinal mucosa,
occurring at any age. Imaging features of celiac disease are small-bowel
atonia, mucosal fold thickening, increased fold separation, and increased
ileal folds ("ileal jejunization")
[5]
(Fig. 11). In a quarter of the
patients with proven celiac disease, no macroscopic abnormalities can be
found.
Jejunitis can be described as a most likely inflammatory entity of only the
jejunum without a proven cause. It is characterized by a thickening of all
jejunal wall layers with serosal edema
(Fig. 12). The findings can
resolve completely and should be differentiated from jejunitis in Crohn's
disease using specific Crohn's disease features.
Inflammation related to bacteria or parasites causes diffuse wall and fold
thickening and resolves completely after therapy
(Fig. 13). Intestinal
tuberculosis is a rare manifestation in which the ileocecal region is commonly
involved. In the acute stage, ulcerations can be seen; in the subacute stage,
scarring effects on the bowel wall can be identified.
Eosinophilic gastroenteropathy is a rare disorder characterized by
peripheral and tissue eosinophilia infiltrating all three layers of the bowel
wall and can involve any segment of the gastrointestinal tract, especially the
stomach and small bowel. It is characterized by a loss of all mucosal folds in
the small bowel, bowel wall thickening, and atonia
[6] (Figs.
14A and
14B).

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Fig. 14A 66-year-old woman with proven eosinophilic gastroenteropathy.
Coronal true fast imaging with steady-state precession (FISP) shows diffuse
loss of mucosal folds and diffuse thickened wall of all small-bowel loops
(arrows). Lack of motility on thick-slab HASTE sequence with fat
saturation (not shown) is also characteristic of this disease.
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Sclerosing encapsulating peritonitis is a rare disorder, occurring in
patients undergoing peritoneal dialysis. Lack of peristalsis at MR fluoroscopy
and diffuse bowel wall thickening in the appropriate clinical setting provide
the diagnosis. Peritoneal calcifications are conspicuous at CT
[7] (Figs.
15A,
15B, and
15C).

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Fig. 15A 44-year-old woman with peritoneal dialysis and sclerosing
encapsulating peritonitis. Coronal true fast imaging with steady-state
precession (FISP) and fat saturation shows diffuse pronounced small-bowel wall
thickening (arrows) and central localization. Thick-slab HASTE
fat-saturation images reveal lack of motility (not shown).
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Fig. 15B 44-year-old woman with peritoneal dialysis and sclerosing
encapsulating peritonitis. Coronal fast low-angle shot (FLASH) 2D
fat-saturation image obtained after contrast injection shows increased diffuse
enhancement of small-bowel wall (arrows).
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Radiation enteritis is a complication after radiation therapy that occurs
often within 2 years, sometimes as long as 10-20 years, after radiation
therapy. The disease is characterized by diffuse mild thickening, intense
contrast enhancement, loss of folds, and lack of peristalsis of the
small-bowel loops in the area of previous radiation therapy
[8] (Figs.
16A and
16B).

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Fig. 16A 75-year-old woman with radiation enteritis, 20 years after
abdominal hysterectomy and radiation therapy for endometrial carcinoma. Axial
true fast imaging with steady-state precession (FISP) and fat saturation shows
diffuse mild thickened distended ileum loops (arrows), without
peristalsis (not shown). Note colostomy bag ventral of right abdominal wall
after resection of colon carcinoma 2 years ago.
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Fig. 16B 75-year-old woman with radiation enteritis, 20 years after
abdominal hysterectomy and radiation therapy for endometrial carcinoma.
Coronal fast low-angle shot (FLASH) 2D image shows increased contrast
enhancement of thickened ileum loops (arrows) in contrast with normal
enhancement of colon (arrowhead).
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