MR Enterography in the Management of Patients with Crohn

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SMALL BOWEL IMAGING
1827
MR Enterography in
the Management of
Patients with Crohn
Disease1
CME FEATURE
See accompanying
test at http://
www.rsna.org
/education
/rg_cme.html
LEARNING
OBJECTIVES
FOR TEST 6
After reading this
article and taking
the test, the reader
will be able to:
■■Summarize
how
MR enterography
compares with
other techniques for
small-bowel imaging in patients with
Crohn disease.
■■Describe
how
to perform MR
enterography and
interpret its results
in the assessment of
Crohn disease.
■■Discuss
the role of
MR enterography in
the management of
small-bowel Crohn
disease.
John R. Leyendecker, MD • Richard S. Bloomfeld, MD • David J. DiSantis,
MD • Gregory S.Waters, MD • Ryan Mott, MD • Robert E. Bechtold, MD
Crohn disease is a complex pathologic process with an unpredictable
lifelong course that includes frequent relapses. It often affects young
patients, who are most vulnerable to the potential adverse effects of
repeated exposure to ionizing radiation from computed tomography
performed for diagnosis and surgical planning. The small intestine is
the bowel segment that is most frequently affected, but it is the least
accessible with endoscopic techniques. Magnetic resonance (MR)
enterography has the potential to safely and noninvasively meet the
imaging needs of patients with Crohn disease without exposing them
to ionizing radiation. Appropriate use of MR enterography requires a
carefully crafted protocol to depict signs of active inflammation as well
as complications such as bowel obstruction, fistulas, and abscesses.
Interpretation of MR enterographic images requires familiarity with
the imaging signs and mimics of active bowel inflammation and stenosis. Although MR enterography currently is helpful for management
in individual patients, the standardization of acquisition protocols and
interpretive methods would increase its usefulness for more rigorous,
systematic assessments of Crohn disease treatment regimens.
©
RSNA, 2009 • radiographics.rsna.org
TEACHING
POINTS
See last page
Abbreviations: CDAI = Crohn disease activity index, SSFP = steady-state free precession, 3D = three-dimensional
RadioGraphics 2009; 29:1827–1846 • Published online 10.1148/rg.296095510 • Content Codes:
From the Departments of Radiology (J.R.L., D.J.D., R.E.B.), Gastroenterology (R.S.B.), Surgery (G.S.W.), and Pathology (R.M.), Wake Forest University School of Medicine, Medical Center Blvd, Winston-Salem, NC 27157. Recipient of an Excellence in Design award for an education exhibit at
the 2008 RSNA Annual Meeting. Received March 12, 2009; revision requested April 16 and received June 4; accepted June 5. J.R.L. is a speaker for
and received research funding from Bracco Group and is a member of the speakers bureau for Bayer; R.S.B. received research support from Johnson
& Johnson and is a member of the speakers bureaus for Johnson & Johnson, Abbott Laboratories, and Shire. All other authors have no financial relationships to disclose. Address correspondence to J.R.L. (e-mail: [email protected]).
1
©
RSNA, 2009
1828 October Special Issue 2009
radiographics.rsna.org
Introduction
Crohn disease is an idiopathic chronic inflammatory disease of the gastrointestinal tract that has
varying levels of severity, diverse manifestations,
and an unpredictable course. Crohn disease has
a prevalence of around 100–200 per 100,000
people in North America and Europe, with approximately 400,000–600,000 people affected
in North America (1). The etiology of Crohn
disease is complex and likely multifactorial, with
genetic, immunologic, infectious, microvascular, and possibly environmental and lifestyle
factors contributing (2,3). Enteric involvement
tends to be segmental, and inflammation often is
transmural. Superficial mucosal (aphthous) and
deep linear ulcers may be present, separated by
segments of uninvolved mucosa (“skip lesions”)
(Fig 1), depending on the severity and chronicity
of Crohn disease. Coalescent longitudinal and
transverse ulcers yield a “cobblestone” appearance of the bowel mucosa, a finding seen in more
advanced cases of Crohn disease (4). Histologic
hallmarks of Crohn disease include expansion
of the lamina propria with chronic inflammatory cells, crypt architectural distortion, cryptitis,
crypt abscesses, ulcers, noncaseating granulomas, transmural lymphoid aggregates, thickening of the muscularis mucosae, and submucosal
fibrosis (Fig 2) (4).
Crohn disease is chronic, has a peak age of
onset in the 2nd–4th decades of life, and follows
an unpredictable course with periodic recurrences and exacerbations (1). Patients frequently
are subjected to multiple imaging examinations
in which they are exposed to ionizing radiation,
often beginning in adolescence or early adulthood. The small bowel is the most common site
of Crohn disease and the least accessible with
endoscopy. Often, the disease involves the terminal ileum by the time it is diagnosed. Although
upper gastrointestinal involvement is rare, Crohn
disease may affect any segment, or multiple noncontiguous segments, of the small bowel. Over
time, in many patients, penetrating or stricturing
disease develops that sometimes requires surgical intervention (5). Common complications of
small-bowel Crohn disease include bowel obstructions, fistulas, and abscesses.
Figure 1. Crohn disease in a 68-year-old man.
Endoscopic image shows multiple ulcerations in
the terminal ileum (arrow) and edematous mucosa, findings typical of active inflammation.
Clinicians often use medical history, laboratory
data, and physical examination to assess disease
activity and complications, but these tools are relatively nonspecific. Clinical observations of disease
activity are subjective and prone to significant interobserver variability (6). Because the symptoms
of active inflammation and those of complications
may be indistinguishable, imaging often is needed.
These challenges highlight the need for a
cross-sectional imaging technique that is sensitive
enough to allow detection of bowel inflammation
and its complications and that allows differentiation between acute disease that can be managed
medically and disease that requires surgery. In
addition, the ideal imaging test would be reproducible, well tolerated by patients, and free of
ionizing radiation.
In this article, we explain how to perform MR
enterography in patients with Crohn disease and
how to interpret MR enterographic images, and
we describe the expanding role of MR enterography in the clinical management of Crohn disease.
Why Use MR Imaging
to Assess Small-Bowel
Involvement in Crohn Disease?
Imaging of patients with Crohn disease traditionally has included a combination of fluoroscopic
and computed tomographic (CT) techniques to
assess the small bowel. The former method consists of small-bowel follow-through examinations
RG ■ Volume 29 • Number 6
Leyendecker et al 1829
Figure 2. Crohn disease with acute and chronic inflammation in a 30-year-old woman. (a) Coronal gadoliniumbased contrast material–enhanced fat-suppressed T1-weighted gradient-echo MR image shows luminal narrowing,
mural thickening, and mildly increased vascularity of the terminal ileum (arrow). (b) Photomicrograph (original
magnification, ×20; hematoxylin-eosin stain) of a resected bowel segment shows mucosal ulceration (arrows), a finding indicative of acute inflammation. Evidence of chronic inflammation also is seen, with expansion of the lamina
propria by inflammatory cells, crypt architectural distortion, and submucosal fibrosis (*).
and enteroclysis, which provide views of the bowel
lumen and mucosal surface but only limited, indirect information about extraenteric complications.
CT provides detailed information about the bowel
wall and extraenteric structures at the expense of
mucosal detail. Recognizing the complementary
nature of these techniques, investigators have
sought to combine the best of both in CT enteroclysis and CT enterography (7,8). Despite the
diagnostic success attained with these CT techniques, their use is limited because of their dependence on ionizing radiation, a significant liability
given the need for repetitive imaging in a subset of
young patients with Crohn disease (9).
Reported radiation doses for multidetector CT of the abdomen and pelvis vary widely,
ranging from 6 to 28 mSv (10–12). For example, Jaffe et al (9) reported an effective dose of
16.1 mSv for abdominal and pelvic multidetector CT. The hazards of radiation exposure, particularly in the young, are well known, although
the details are controversial. Standard radiation
doses for multidetector CT are within accepted
limits; 50 mSv is the yearly limit for radiation
workers in the United States. However, some estimates suggest that an effective dose of 10 mSv
may correspond to an estimated excess risk of
1 in 2000 for developing fatal cancer (13). This
alone should spur interest in the use of magnetic
resonance (MR) imaging for the evaluation of
younger patients with Crohn disease.
Without the risks of ionizing radiation, MR
imaging provides superior soft-tissue contrast and
excellent depiction of fluid and edema. Enhancement with gadolinium-based contrast material
increases the ability to detect subtle inflammation.
Unlike CT, steady-state free precession (SSFP)
MR imaging sequences can depict bowel motility,
a potential advantage when attempting to distinguish between fixed and transient segments of
narrowing. Sequences may be repeated to capture
multiple discrete vascular phases, reassess abnormal bowel segments, or improve image quality
without increasing the radiation risk to the patient.
MR imaging is more reliable than fluoroscopic
enteroclysis for correctly identifying areas of Crohn
disease involvement, except perhaps for mucosal
abnormalities (14,15). The relative merits of CT
and MR enterography, apart from the issue of
radiation exposure, are less clear; in particular,
there is uncertainty as to which method better
depicts wall thickening and enhancement (16,17).
Horsthuis et al (18) conducted a meta-analysis
and reported that there was no statistically significant difference between MR imaging and CT in
the ability to depict inflammatory bowel disease,
including extraenteric complications, on a perpatient basis across multiple studies.
Video capsule endoscopy may be used to evaluate disease activity in the small bowel of patients
with Crohn disease or to determine if Crohn disease is present in the small bowel of patients under consideration for surgical therapy for colitis.
Comparisons between video capsule endoscopy
and MR imaging for assessment of small-bowel
Crohn disease have shown these techniques to be
complementary, with video capsule endoscopy
better depicting mucosal disease and MR imaging showing additional transmural and extramural findings (19,20). Aside from its inability to
depict the bowel wall and extraluminal findings,
video capsule endoscopy may be limited by bowel
strictures and obstructions (21). In a recent study
by Solem et al (22) of 41 patients studied with a
variety of imaging techniques in addition to video
capsule endoscopy, 17% had an asymptomatic
partial small-bowel obstruction, although none of
the obstructions caused capsule retention.
MR Enterography
versus MR Enteroclysis
The benefits of using enteric contrast material to
achieve bowel distention for cross-sectional imaging are not disputed, although the optimal type of
contrast material and method of administration
remain somewhat controversial. For the purposes
of this article, when enteric contrast material
is administered through an enteric tube we use
the term enteroclysis, and when it is administered
orally we use the term enterography. Current data
suggest that although bowel distention achieved
with the enteric intubation technique generally is
superior to that achieved with enterography, the
improved distention does not necessarily translate into a clinically significant improvement in
diagnostic effectiveness (23,24).
A recent study by Masselli et al (15) confirmed the benefit of enteric intubation for bowel
distention but reported equivalent diagnostic performances with the enteric and oral techniques
in identifying stenoses and fistulas. However, MR
enteroclysis was superior to MR enterography in
demonstrating mucosal abnormalities (15). The
importance of detecting mucosal disease in patients without bowel obstruction has diminished
in the era of capsule endoscopy. Patient acceptance, which favors MR enterography over MR
enteroclysis, also must be considered, because
many patients need multiple examinations (25).
MR Enterography Technique
Patient Preparation
Techniques for performing MR enterography
vary among institutions, but it is generally agreed
that administering an enteric contrast agent is
essential to achieve some degree of bowel distention. Instructing patients to fast for approximately 6 hours before the procedure improves
compliance with and tolerance for ingestion of
oral contrast material; nevertheless, to our knowledge, the benefits and lengths of fasting have
not been rigorously studied. Some investigators
have advocated concomitant instillation of rectal
contrast material before imaging to allow simultaneous assessment of the small bowel and colon
(26,27). In addition to improving colon distention, instillation of a rectal enema may improve
distention of the terminal ileum (26,27). Because
the colon is readily accessible at colonoscopy, we
do not routinely perform rectal enemas.
Halting peristalsis reduces blurring and artifacts related to bowel motility. We have found
that, for adults, administering 1 mg of glucagon
intramuscularly after cine imaging and before
contrast-enhanced T1-weighted and fat-suppressed T2-weighted MR imaging serves this
purpose well. Contraindications to the use of
glucagon include known hypersensitivity to the
commercial preparation and known or suspected
pheochromocytoma or insulinoma.
Administration of
Oral Contrast Material
With regard to oral contrast material administration for MR enterography, three issues must be
addressed: (a) the composition of the contrast
material, (b) the volume to be administered, and
(c) the timing of image acquisition after ingestion
of contrast material. A commercial preparation
of 0.1% (wt/vol) barium suspension containing
sorbitol is effective, well tolerated, and convenient
for MR enterography (28,29). Use of this agent
produces high signal intensity in the bowel lumen
on T2-weighted images and low signal intensity
in the lumen on T1-weighted images. The dark
lumen is critical for the detection of mural enhancement on postcontrast T1-weighted images,
but water alone does not provide adequate bowel
distention for MR enterography.
Figure 3. Crohn disease of the ileum and cecum in a 39-year-old woman. (a) Coronal single-shot fast
spin-echo localizer MR image shows small-bowel wall thickening, submucosal edema, and surrounding
fat accumulation (arrows). Dilated jejunum also is seen in the left side of the abdomen (arrowhead). An
underlying bowel obstruction was successfully managed surgically. (b) Coronal SSFP image shows segmental bowel dilatation (arrow) and vascular detail within the small-bowel mesentery (arrowhead).
In the literature, reported volumes of oral contrast material vary considerably, but most studies
report a total volume of 1–2 L. Ingested volumes
of mannitol or sorbitol solution at the higher end
of this range may result in more side effects, such
as diarrhea, excess intestinal gas, and abdominal
cramps, although side effects also may be reduced
by keeping the sugar alcohol concentration below
2.5% (30,31). We administer portions of the commercial oral contrast preparation alternately with
plain water to improve patient tolerance, although
this method is optional. We attempt to achieve a
minimum ingested volume of 1 L, although some
symptomatic patients may be unable to comply.
To allow distal transit, we employ a minimum
delay of 45 minutes from the start of contrast
ingestion to imaging (28,30,32). The additional
administration of intravenous erythromycin and
prone imaging have been recommended to improve gastric emptying and bowel loop separation,
respectively, but we do not implement these strategies in our practice (15,30,32).
Sequences and Protocol
MR enterography imaging protocols vary because of differences in available equipment and
personal preferences. We use a 1.5-T MR imaging system with a 12-channel torso receiver coil
that is capable of parallel imaging and that allows
coronal acquisitions to encompass the entire
small bowel in a single field of view. Despite differences in MR imaging equipment and software,
certain basic elements are common to most
imaging protocols for Crohn disease. We begin
an MR enterography examination with coronal
T2-weighted single-shot fast spin-echo or coronal
half-Fourier acquisition single-shot turbo spinecho imaging of the abdomen and pelvis. These
initial sequences are primarily applied for localization and anatomic overview, although areas of
bowel wall thickening, edema, and luminal dilatation often are visible (Fig 3a).
Next, we apply a multiphase multisection
coronal SSFP MR sequence that covers the entire small bowel and colon. We generally acquire
15–25 phases per section location during free
breathing. These images may then be displayed
as a cine loop to assess bowel motility, exclude
or confirm fixed stenoses and segmental dilatation, and detect adhesions (33–35). Because of
the high image contrast, this type of sequence is
helpful for assessing mesenteric vascularity and
lymphadenopathy (Fig 3b).
Teaching
Point
Teaching
Point
After glucagon is administered, we acquire
coronal fat-suppressed three-dimensional (3D)
T1-weighted breath-hold gradient-echo images
of the abdomen and pelvis before and after intravenous gadolinium-based contrast material is administered. We typically acquire an arterial phase
image 25 seconds after contrast material administration, followed by two additional coronal
acquisitions, allowing the patient to breathe for a
brief period between each acquisition. Although
the value of rapid dynamic imaging in the assessment of bowel wall enhancement in patients
with Crohn disease has been questioned, we have
found that when several complete volumetric
data sets are acquired within 2 minutes after contrast material administration, at least one data set
generally is motion free and includes the period
of peak bowel wall enhancement, which can vary
between patients (36,37). These coronal contrastenhanced images allow assessment of the vasculature, lymph nodes, and bowel wall enhancement
(Fig 4). Enteric fistulas and abscesses also are
depicted. We frequently include a set of delayed
contrast-enhanced axial images for multiplanar
correlation (Fig 5).
Immediately after the coronal contrastenhanced acquisitions, we obtain a set of axial
fat-suppressed T2-weighted images to assess the
bowel wall and surrounding tissues for fluid and
edema (Fig 6) (38,39). We also routinely obtain
a set of coronal diffusion-weighted images (b =
800 sec/mm2), although the utility of diffusionweighted imaging in the MR imaging assessment
of Crohn disease remains an area of investigation.
It is hoped that diffusion-weighted images will
help identify areas of active inflammation, fistulas, and abscess formation (Fig 7).
Figure 4. Crohn disease and chronic superior mesenteric vein thrombosis in a 60-year-old woman. Coronal
partial-volume maximum intensity projection image
from contrast-enhanced fat-suppressed T1-weighted 3D
gradient-echo MR imaging shows segmental bowel wall
thickening and intense mucosal enhancement (white arrows), lymphadenopathy (arrowheads), and mesenteric
venous collaterals (black arrow). The patient’s condition
improved with medical therapy.
Interpretation of MR
Enterographic Images
Spectrum of Findings of
Small-Bowel Crohn Disease
Crohn disease may be classified as active inflammatory (without fistulas or stenoses), penetrating, or fibrostenotic disease, depending on the
imaging features (40,41). Patients may exhibit
characteristics of more than one disease subtype,
Figure 5. Utility of axial contrast-enhanced imaging in evaluating Crohn disease. Axial contrast-enhanced fat-suppressed T1-weighted 3D gradient-echo
MR image obtained in a 28-year-old man shows two
ileocolic fistulas (arrows) that were difficult to detect
on coronal images.
Figure 6. Mural edema and inflammatory fluid in a patient with Crohn disease. Axial fat-suppressed T2-weighted
MR image shows high-signal-intensity
bowel wall (arrow) and fluid surrounding the distal ileum (arrowhead).
Figure 7. (a) Coronal diffusion-weighted image (b = 800 sec/mm2) obtained in a young man with Crohn disease shows two focal areas of increased signal intensity (arrows). (b) Coronal contrast-enhanced fat-suppressed
T1-weighted 3D gradient-echo MR image obtained at the same level as a shows that the high-signal-intensity
areas correspond to extraluminal fluid collections (arrows), which were initially thought to represent small-bowel
loops at CT and MR imaging. An abscess was diagnosed, but an attempt at percutaneous drainage was aborted
because of difficulty in distinguishing the abscess from adjacent bowel. The diagnosis was confirmed at surgery.
and it is common for a single resected bowel
specimen to contain areas of acute inflammation, chronic inflammation, and fibrosis (Fig 2).
The role of radiologists is to describe the features of each subtype that are seen at imaging.
Correlation with clinical data helps determine
the significance of the findings.
Active Inflammation.—At pathologic analysis,
active inflammation is characterized by varying
degrees of neutrophilic crypt injury. In mildly active Crohn disease, a small fraction of crypts are
infiltrated by neutrophils (cryptitis), with
Figure 8. Stratified enhancement of bowel in a
53-year-old man with active Crohn disease. Coronal
contrast-enhanced fat-suppressed T1-weighted 3D gradient-echo MR image shows stratified mural enhancement in a small-bowel loop (arrow). The hyperenhancing inflamed mucosa at the center is surrounded by a
lower-signal-intensity ring of submucosal edema and
an outer ring of enhancing serosa, creating a targetlike
appearance at cross-sectional imaging.
Figure 9. Increased mesenteric vascularity (comb
sign) due to acute inflammation in a 28-year-old man
with active Crohn disease. Coronal contrast-enhanced
fat-suppressed T1-weighted 3D gradient-echo image shows increased vascularity (arrow) adjacent to a
hyperenhancing thickened segment of ileum (arrowhead). This patient’s condition improved with medical
management.
associated crypt destruction and mucin depletion.
As the degree of activity increases, there is a corresponding increase in the proportion of involved
crypts and the severity of crypt injury, including
crypt epithelial necrosis, intraluminal exudate
(crypt abscess), and eventual ulcer formation.
Two types of ulcers are seen in Crohn disease:
superficial aphthous ulcers and deep fissuring
ulcers. Deep fissuring ulcers are more problematic than superficial aphthous ulcers; they break
through the mucosa and into the deeper layers of
the bowel wall, initially resulting in submucosal
inflammation and edema. At MR enterography,
submucosal edema in the small bowel appears
as wall thickening and produces increased signal intensity on T2-weighted images (Fig 6)
(38,39,42). Mucosal and serosal enhancement,
combined with intervening submucosal edema,
contribute to a stratified or layered appearance on
contrast-enhanced T1-weighted fat-suppressed
images (Fig 8) (43,44).
Some investigators have reported that
deep ulcers may be seen at MR enterography,
whereas superficial ulcers defy detection (45).
Increased mesenteric vascularity adjacent to
the inflamed bowel loop (the comb sign) often
is present in the setting of acute inflammation
and is best identified on contrast-enhanced T1weighted fat-suppressed images or SSFP images
(Fig 9) (44). These sequences also clearly demonstrate reactive mesenteric lymphadenopathy,
a finding frequently seen in patients with active
Crohn disease (Fig 4). Some investigators have
Teaching
Point
Figure 10. Enterovesical fistula in a 49-year-old woman
with Crohn disease and no history of recent bladder catheterization. (a) Axial fat-suppressed T2-weighted MR image shows an air bubble (arrow) in the bladder. (b) Coronal SSFP MR image shows tethering of the right bladder
dome and an adjacent cluster of bowel loops (arrow)
interconnected by fistulas and adhesions. (c) Coronal
contrast-enhanced fat-suppressed T1-weighted 3D gradient-echo MR image shows a fistula between an ileal loop
and the bladder (arrow). These findings were confirmed
at surgery and pathologic analysis. The patient’s condition
improved after surgery.
controversial, and first-line medical treatment
regimens vary by practitioner and institution.
Mesalamine, steroids, immunomodulators, and
biologics (drugs that specifically target components of the immune system) are all used to
varying degrees for the management of uncomplicated active Crohn disease.
identified lymph node enhancement as a finding that allows differentiation between active
inflammatory and fibrostenosing disease, but the
added value of this potential finding is unclear
at present (46).
Typically, active inflammatory disease without fibrostenosing or penetrating complications
is managed medically. The optimal medical
management of Crohn disease is somewhat
Penetrating Disease.—Deep ulcer formation
may lead to transmural inflammation and sinus
tract formation, which may progress to fistulation.
Fistulas may bridge adjacent loops of small bowel
or cross from small bowel to the colon, stomach,
bladder, or skin (Figs 5, 10). Penetrating disease
Figure 11. Penetrating disease with early abscess
formation in a 47-year-old woman with Crohn disease. Coronal contrast-enhanced fat-suppressed T1weighted 3D gradient-echo MR image shows a fistulous tract between the distal ileum and a small abscess
(arrow). Acute and chronic transmural inflammation
with fistula formation were confirmed at surgery and
pathologic analysis.
may cause the formation of abscesses, which often
can be managed percutaneously (Figs 7, 11). The
presence of penetrating disease in the absence of
an abscess often alters medical therapy; clinicians
generally avoid the use of steroids in such cases
and may consider antibiotic or biologic therapy.
Fistulas, sinus tracts, and abscesses are visible on contrast-enhanced T1-weighted fatsuppressed MR images because of their avidly
enhancing walls (47). In our experience, adhesions between adjacent bowel loops can be distinguished from fistulas because adhesions are
fibrotic and tend to be thinner and enhance later
than fistulas, whereas fistulas are composed of
more vascular inflammatory tissue (Fig 12). Enteroenteric fistulas often form a complex network
between closely adherent small-bowel loops that
may appear as a stellate configuration on contrast-enhanced MR images (Fig 13).
Fibrostenosing Disease.—Over time, chronic
inflammation within the bowel wall progresses to
mural fibrosis. When fibrosis is associated with
stricture formation, bowel obstruction may de-
Figure 12. Peritoneal adhesion in a 49-year-old
woman with Crohn disease (same patient as in Fig
10). Coronal SSFP image shows an adhesion (arrow)
between adjacent small-bowel loops, remote from the
region of enterovesical fistula formation.
Figure 13. Enteroenteric fistulas in a 37-year-old
man with Crohn disease. Axial contrast-enhanced
fat-suppressed T1-weighted 3D gradient-echo image
shows the stellate appearance of small-bowel loops (arrow) that are interconnected by enteroenteric fistulas.
These findings were confirmed at surgery.
velop. It is important to identify fibrotic strictures
with certainty because they are unresponsive to
medical therapy. Fibrotic strictures resulting in
symptomatic bowel obstruction typically require
surgical resection.
On cine images, fibrotic strictures appear as
aperistaltic bowel segments that often demonstrate
fixed mural thickening and luminal narrowing
(Fig 14). The thickened submucosa of a strictured,
fibrotic bowel segment does not typically display
increased signal intensity on T2-weighted images
in the absence of active disease because of the lack
of mural inflammation and edema. The presence
Teaching
Point
Figure 14. Fibrostenosing disease in a 28-year-old woman with long-standing Crohn disease. (a) Coronal
SSFP image shows two jejunal strictures (arrows) that appeared stationary at cine imaging. No increased vascularity or lymphadenopathy is present in the adjacent mesentery. (b) Image obtained during a small-bowel
barium study several years earlier shows the same strictures (arrows), providing evidence of their chronicity.
Figure 15. Partial small-bowel obstruction caused
by stricture and an impacted coin in a 30-year-old
man with Crohn disease and abdominal pain. The
patient had swallowed the coin several years earlier.
It was seen at previous CT but was not thought
to be the cause of obstruction. Coronal SSFP image shows a dilated small-bowel segment with
chronic stasis of contents with fecalization (arrow)
proximal to a linear signal void (arrowhead), which
represents the coin. At subsequent surgery, a shortsegment fibrous stricture that had caused impaction
of the coin was resected. The patient’s symptoms
improved after surgery.
Additional Findings
of a fibrotic stricture does not exclude the possibility of coexistent active inflammation elsewhere in
the bowel. Bowel dilatation proximal to a fixed,
narrowed segment implies obstruction. Fecalization of the small-bowel contents may be visible at
MR imaging and CT but is not highly specific to
small-bowel obstruction (Fig 15) (48).
We primarily perform MR enterography to assess
the small bowel in patients with Crohn disease.
However, active Crohn colitis may be incidentally
discovered at MR imaging even in the absence of
a prepared colon or when an enema has not been
administered (Fig 16). In such cases, the colon
demonstrates hyperenhancement, mural thickening, and mesenteric vascular engorgement. The
role of diffusion-weighted imaging in the assessment of Crohn disease activity has not been
established, but we have seen several cases of active Crohn colitis in which conspicuity of the inflamed colon was increased on diffusion-weighted
images (Fig 16c).
Figure 16. Crohn colitis in a 31-year-old woman. (a) Coronal SSFP image shows thickening of the
descending colon (arrow), with surrounding fatty proliferation and increased mesenteric vascularity.
(b) Coronal contrast-enhanced fat-suppressed T1-weighted 3D gradient-echo image shows avid enhancement of the colon (arrow) and mesenteric vessels. (c) Coronal diffusion-weighted image (b = 800 sec/mm2)
shows restricted diffusion in the affected segment of colon (arrow).
Coronal contrast-enhanced images obtained
for assessment of mural enhancement provide
excellent depiction of the abdominal vasculature
and should be routinely scrutinized for evidence
of vascular complications such as venous thrombosis (Fig 4).
Interpretive Pitfalls
Teaching
Point
A number of imaging features may lead to incorrect diagnoses when interpreting MR enterographic images. Although submucosal edema
often is present in acutely inflamed bowel segments, it is not unusual to encounter extensive
submucosal edema “upstream” from a high-grade
obstruction. In such cases, acute inflammation
may be present to some extent. The transition
between acutely inflamed small bowel and noninflamed but obstructed edematous small bowel
can be difficult to delineate. In our experience,
noninflamed obstructed bowel typically has a
conspicuous submucosal layer with very low
signal intensity on T1-weighted images and very
high signal intensity (equal to that of simple
fluid) on T2-weighted images, findings due to the
presence of submucosal edema (Fig 17).
However, the mucosal and serosal layers in noninflamed obstructed bowel are thin and enhance
normally (unlike those in acutely inflamed segments), and the bowel lumen is dilated.
In patients with Crohn disease, not all smallbowel obstructions are the result of fibrotic strictures, and not all dilated small-bowel segments
are obstructed. Peritoneal adhesions are common
in Crohn disease and may lead to obstruction. In
such cases, radiologists should look for acutely
angled or tethered bowel loops, an abrupt transition in luminal diameter, and an absence of
mural thickening. A short-segment stricture also
may be associated with an abrupt transition in
caliber, although it is typically seen in the absence
of bowel tethering (Fig 18). Lack of a clearly
Figure 17. Submucosal edema associated with obstruction due to Crohn disease in a 37-year-old
man. (a) Coronal single-shot fast spin-echo image shows an obstructing stricture of the terminal ileum (arrow) and a segment of more proximal small bowel with a high-signal-intensity submucosa (arrowhead). (b) Coronal contrast-enhanced fat-suppressed T1-weighted 3D gradient-echo image shows
enhancement of the strictured segment and an enteroenteric fistula (arrow). The proximal small-bowel
loop has a low-signal-intensity submucosa and thin mucosal and serosal layers (arrowhead). These findings are indicative of obstruction without inflammation, which was confirmed at surgery.
Figure 18. Weblike stricture in a 35-year-old man with a history of Crohn disease and abdominal pain.
(a) Coronal single-shot fast spin-echo image shows an abrupt change in small-bowel caliber in the right
lower quadrant (arrow). Contrast-enhanced images showed no evidence of active inflammation. (b) Endoscopic image obtained during double-balloon enteroscopy shows one of several short-segment strictures
that were found (arrow). The strictures recurred after balloon dilatation and required surgical resection.
Figure 19. Functional bowel abnormality in
a young woman with a history of Crohn disease and abdominal pain. Coronal single-shot
fast spin-echo image obtained through the anterior abdomen shows markedly dilated jejunal
loops (arrow) without a clear transition point
identified. At surgery performed for symptoms,
a leathery segment of small bowel was found
to be firmly attached to the anterior abdominal
wall by dense adhesions, but the adhesions
did not appear to be causing obstruction. The
patient’s symptoms failed to improve despite
resection of the diseased segment.
Figure 20. Transient bowel collapse mimicking active inflammation in a 35-year-old man with Crohn
disease. (a) Coronal contrast-enhanced fat-suppressed T1-weighted 3D gradient-echo image shows a
narrowed and avidly enhancing small-bowel segment (arrow). (b) Coronal SSFP image shows normal
distensibility and thin wall of the previously collapsed segment (arrow).
defined transition point in dilated small bowel
is a finding typical of a functional abnormality
in the absence of obstruction. It is important to
distinguish functional bowel abnormalities from
anatomic obstruction because patients with functional bowel abnormalities may not benefit from
surgical intervention (Fig 19).
Collapsed bowel segments may appear thickened, with an avidly enhancing appearance that
mimics that of active inflammation (Fig 20). Cine
Figure 21. Transient intussusception in a symptomatic 45-year-old man with a history of Crohn disease. (a) Coronal SSFP image shows a thickened jejunal loop (arrow). (b) Image from the same study
as a (obtained at a more anterior level) shows intussusception of the jejunum (arrow), which resolved on
later images. Multiple strictures seen elsewhere in the study were surgically treated.
Figure 22. Meckel diverticulum in a 28year-old woman with CT findings that were
initially interpreted as obstruction due to active Crohn disease after a history of suspected
Crohn disease was provided. Coronal SSFP
image from MR enterography shows multiple
dilated small-bowel loops and a blind-ending
structure in the mid abdomen (arrow). The
blind-ending loop did not exhibit normal peristalsis at cine imaging. At surgery, adhesions
related to a Meckel diverticulum were found
to be obstructing the bowel. There was no evidence of Crohn disease.
SSFP imaging may be helpful in demonstrating
the transient nature of bowel collapse. Secondary
signs of acute inflammation, such as increased
mesenteric vascularity, are absent in the setting
of collapsed but otherwise normal bowel. Transient intussusception of jejunum also may mimic
chronic small-bowel Crohn disease (Fig 21).
Not all patients referred for MR enterography
for presumed or possible Crohn disease have the
disease (Fig 22). Furthermore, processes other
than Crohn disease may produce segmental
bowel features very similar to those typical of
Crohn disease (Fig 23). In particular, a targetlike
enhancement pattern of the small bowel may be
seen in radiation-induced or infectious enteritis,
vasculitis, and intestinal ischemia.
Figure 23. Segmental small-bowel ischemia
mimicking Crohn disease in a 63-year-old man
with abdominal pain. Coronal contrast-enhanced
fat-suppressed T1-weighted 3D gradient-echo image shows an avidly enhancing small-bowel segment
(arrow) with the comb sign. Enlarged mesenteric
lymph nodes were seen on other images. At surgery,
the diseased segment was found to be ischemic, and
metastatic carcinoid tumor was discovered in the
mesenteric lymph nodes. The tumor is presumed to
have obstructed the venous drainage of the affected
loop, inducing ischemia.
Figure 24. Process
diagram shows the proposed algorithm for the
use of MR enterography
(MRE) in managing
Crohn disease (CD).
A.I. = active inflammation, SBO = smallbowel obstruction, TI =
terminal ileum.
Potential Impact of MR
Enterography on Patient
Treatment and Clinical Trials
MR enterography has the potential to impact three
aspects of patient care: diagnosis, management,
and clinical trials. Practices vary for management
of Crohn disease; our algorithm should be considered only one possible approach (Fig 24).
Whereas MR enterography may be incorporated into the diagnostic evaluation of a new
patient presenting with symptoms of Crohn
disease, in most cases this is unnecessary. For
many patients, the diagnosis is readily made at
colonoscopy with terminal ileoscopy. However,
patients who present with symptoms consistent
with Crohn disease and who have normal findings at ileocolonoscopy may benefit from MR
enterography to determine if there is enteric inflammation proximal to the terminal ileum. Also,
MR enterography may be useful in identifying
patients with terminal ileitis when intubation of
the terminal ileum during colonoscopy is unsuccessful. Whether MR enterography is preferable
to capsule endoscopy for the assessment of new
patients with small-bowel Crohn disease is unclear at present, except perhaps in the setting of
suspected bowel obstruction.
Figure 25. Serial examinations with MR enterography in a 37-year-old man with Crohn disease (same
patient as in Fig 17). (a) Coronal contrast-enhanced fat-suppressed T1-weighted 3D gradient-echo image
shows avidly enhancing inflamed distal ileum and an enteroenteric fistula (arrow). The patient’s symptoms
improved after a course of medical therapy. (b) Coronal contrast-enhanced fat-suppressed T1-weighted
3D gradient-echo image obtained approximately 6 months later, after symptoms of bowel obstruction
returned, shows a lesser degree of enhancement but interval development of small-bowel dilatation and
mural edema (arrow) proximal to a stricture of the terminal ileum (arrowhead). (c) Photograph shows
the surgically resected strictured segment (arrow), in which extensive submucosal fibrosis was found
at histologic analysis.
We have found MR enterography particularly
useful for the detection of active inflammation
and complications in symptomatic patients with
known Crohn disease. MR enterography also
may be helpful when symptoms are considered
atypical for Crohn disease. In such cases, a finding of active bowel inflammation may prompt
more aggressive medical intervention, whereas an
absence of active disease or related complications
may prompt an investigation of other possible
causes to explain the patient’s symptoms.
MR enterography also may be used to monitor disease activity or to assess the effectiveness
of interventions (Fig 25). Clinicians treating
patients with Crohn disease are faced with a
daunting task. Patients with Crohn disease often
present with nonspecific symptoms, and clinical assessment of disease activity is a subjective
process prone to significant interobserver variability (6). Clinical activity of Crohn disease
may be quantified by using scoring systems such
as the Crohn disease activity index (CDAI) or
the Harvey-Bradshaw index (49,50). Although
rarely used in clinical practice, the CDAI is the
mostly widely used scoring system. It consists
of a score between 0 and 600 that is based on
both objective and subjective data collected over
7 days. A score of less than 150 suggests disease remission, and a score of 220–450 suggests
moderate to severe activity.
The variables used to determine the CDAI
score include the number of liquid bowel movements, abdominal pain, general well-being, the
presence of extraintestinal manifestations, the use
of antidiarrheal medication, the presence of an abdominal mass, hematocrit levels, and body weight.
Because such activity indexes are cumbersome to
determine, they are rarely used in routine clinical
practice. Furthermore, it is clear that the CDAI is
imperfect. For example, there are patients who do
not have active Crohn inflammation but have high
scores, and there are patients with active disease
and low scores. There is clearly a need for a more
objective noninvasive measure of disease activity
that can be repeatedly and reproducibly performed
even in young patients. Further investigation is
needed to determine the reproducibility of MR
enterography, and a set of standardized criteria for
image interpretation needs to be established and
rigorously tested before MR enterography can be
adopted as such a measure.
It is impractical for patients enrolled in clinical
trials to undergo colonoscopy before and after intervention. Often, clinical trials attempt to use biologic markers of Crohn disease inflammation, such
as the C-reactive protein level in serum or fecal
calprotectin. These noninvasive biologic markers
have substantial limitations as indicators of the response to medical therapy. MR enterography holds
great promise for assessing response to therapy in
Crohn disease trials. The lack of radiation exposure makes MR imaging more appropriate than
CT for performing multiple enterographic studies
in a single patient. Likewise, it provides further incentive to devise and validate an MR enterography
scoring system that can be used as an objective indicator of Crohn disease inflammatory activity and
as an outcome measure in clinical trials.
Conclusions
MR enterography has the potential to play an
important role in the management of small-bowel
Crohn disease. MR enterography can demonstrate active small-bowel inflammation and complications such as bowel obstruction, penetrating
disease, and abscess formation without the use
of ionizing radiation. At present, MR enterography is most useful for assessment of symptomatic patients with known small-bowel Crohn
disease. However, as techniques improve and
undergo further validation and standardization,
indications for MR enterography may expand
to include assessment of response to therapy in
clinical trials. When interpreting MR enterographic findings, familiarity with the MR imaging
features of acute and chronic Crohn disease and
their mimics improves diagnostic accuracy and
helps optimize management of Crohn disease.
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This article meets the criteria for 1.0 credit hour in category 1 of the AMA Physician’s Recognition Award. To obtain
credit, see accompanying test at http://www.rsna.org/education/rg_cme.html.
RG
Volume 29
Number 6
October 2009
Leyendecker et al
MR Enterography in the Management of Patients with Crohn
Disease
John R. Leyendecker, MD, et al
RadioGraphics 2009; 29:1827–1846 • Published online 10.1148/rg.296095510 • Content Codes:
Page 1831
We apply a multiphase multisection coronal SSFP MR sequence that covers the entire small bowel
and colon. We generally acquire 15 25 phases per section location during free breathing. These
images may then be displayed as a cine loop to assess bowel motility, exclude or confirm fixed
stenoses and segmental dilatation, and detect adhesions. Because of the high image contrast, this type
of sequence is helpful for assessing mesenteric vascularity and lymphadenopathy.
Page 1832
These coronal contrast-enhanced images allow assessment of the vasculature, lymph nodes, and
bowel wall enhancement. Enteric fistulas and abscesses also are depicted.
Page 1834
At MR enterography, submucosal edema in the small bowel appears as wall thickening and produces
increased signal intensity on T2-weighted images. Mucosal and serosal enhancement, combined with
intervening submucosal edema, contribute to a stratified or layered appearance on contrast-enhanced
T1-weighted fat-suppressed images.
Page 1836
On cine images, fibrotic strictures appear as aperistaltic bowel segments that often demonstrate fixed
mural thickening and luminal narrowing. The thickened submucosa of a strictured, fibrotic bowel
segment does not typically display increased signal intensity on T2-weighted images in the absence of
active disease because of the lack of mural inflammation and edema.
Page 1838
A number of imaging features may lead to incorrect diagnoses when interpreting MR enterographic
images. Although submucosal edema often is present in acutely inflamed bowel segments, it is not
-grade obstruction. In
such cases, acute inflammation may be present to some extent.

MR Enterography in the Management of Patients with Crohn

Transcription

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