is a Radiologist, Medisch Centrum Alkmaar, Alkmaar, The
is a Professor of Radiology, University of Nebraksa Medical
Center, Omaha, NE. At the time this article was written,
were affiliated with Erasmus MC-University Medical Center.
Dr. Poley, Dr. Siersema,
are Gastroenterologists, and Dr. Kuipers is a Professor of
Gastroenterology, Department of Gastroenterology &
Hepatology, Erasmus MC.
is a Radiologist, a Professor of Radiology, and Chairman of the
Department of Radiology, Erasmus MC-University Medical Center
Rotterdam, Rotterdam, The Netherlands. Portions of this article
were previously presented in: Geenen RWF, Hussain SM, Poley JW,
et al. Combined bright and black lumen MR. Colonography in
patients with inflammatory bowel disease (IBD). Preliminary
results. Presented at The Scientific Assembly and Annual Meeting
of the Radiological Society of North America; November 28, 2004;
Inflammatory bowel disease (IBD) is characterized by an
inappropriate and ongoing activation of the bowel mucosal immune
system in the presence of a normal bacterial flora.
The current general view is that IBD manifests itself under certain
environmental conditions on a genetic basis.
The etiology and pathophysiology of IBD consist of 4 interacting
factors: genetic, environmental, microbial, and immune.
It includes 2 distinct diseases: ulcerative colitis (UC) and
Crohn's disease (CD).
In 10% of patients with IBD that is limited to the colon, it is
initially not possible to distinguish UC from CD; this is the
so-called indeterminate colitis (IC).
With their high incidence and prevalence, both UC and CD are
huge healthcare problems in the Western world. Extrapolation of
reported incidence and prevalence rates of UC in North America show
that 7000 to 46,000 new cases of UC are diagnosed annually and that
approximately 780,000 people have UC.
Extrapolation of European incidence and prevalence figures for UC
produces estimates of 50,000 to 68,000 new cases of UC annually and
approximately 1 million UC patients.
Extrapolation of epidemiological figures for CD show that 10,000 to
47,000 residents of the United States and Canada are diagnosed with
CD each year and that approximately 630,000 have CD.
Extrapolation of European data gives incidence rates of 23,000 to
41,000 annually and prevalence rates of 850,000,
with up to 25% of the UC and CD cases manifesting in childhood.
The median age of CD diagnosis is reported to be 29.5 years.
Generally, UC is diagnosed 5 to 10 years later than is CD.
Ulcerative colitis is a chronic inflammatory process that is
limited to the colorectal mucosa.
The rectal mucosa is invariably affected, and inflammation and
superficial ulceration extend proximally from the anal margin.
Depending on the extension of the disease process, a patient may
have proctitis, left-sided colitis (extension into the descending
colon), extensive colitis (involvement of the transverse colon),
Pathologically, the disease process is continuous and the cutoff
between colitis and normal mucosa is sharp.
In 15% to 20% of patients with severe UC, a so-called backwash
ileitis develops, which almost always resolves after total
Data on UC suggest that this disease results from environmental
factors that trigger a breakdown of the mucosal immune response
regulation to enteric bacteria in genetically susceptible
Crohn's disease is characterized by transmural inflammation that
can affect any part of the gastrointestinal tract with relapses and
remissions throughout its course.
Data suggest that intestinal inflammation arises from abnormal
immune reactivity to bacterial flora in the intestine of
genetically susceptible individuals.
The colon and ileum are the most involved parts of the
gastrointestinal tract in two thirds of CD patients. Involvement of
other parts of the digestive tract does occur but is uncommon.
Three patterns of isolated colonic CD are found: CD isolated to the
rectum, stricturing CD, and diffuse Crohn's colitis.
Pathologically, CD is a discontinuous patchy or focal process.
Ulcers vary from superficial aphtoid ulcers to deep fissuring
ulcers, which can give rise to fistulae or abscesses. Strictures
can occur at sites of transmural inflammation.
Overview of UC and CD imaging
Imaging in patients with (suspected) IBD colitis has 3 major
goals: Distinguishing UC from CD, assessment of disease activity
and extension, and cancer surveillance in long-standing colonic
Colonoscopy is the primary imaging modality for IBD. The
disadvantage of this technique is its relative invasiveness as
compared with radiological techniques such as computed tomography
(CT), ultrasound, magnetic resonance imaging (MRI), and
scintigraphy. Diagnostic colonoscopy carries a small risk of 1:3000
to 1:5000 for perforation.
Double-contrast barium enema (DCBE), CT, and scintigraphy involve a
radiation burden to the patient, which is undesirable, since these
patients are often young and since (because of the chronic course
of IBD) repeated examinations are often necessary over a number of
years. Also, DCBE carries a small risk (1:25,000) of perforation.
The only noninvasive examination methods that do not have any
radiation exposure to the patient are ultrasound and MRI.
Ultrasound has the disadvantage of being more operator-dependent
than is MRI.
The main goal of this review article is to summarize the
literature about MRI in patients with IBD colitis and present MRI
features of IBD colitis. The article also discusses the status of
other examination methods and compares them with the results of
Examination and imaging techniques
Double-contrast barium enema
This examination method can be used to assess the extent and
severity of IBD and to differentiate UC from CD.
Precise data on sensitivity and specificity for diagnosis and for
determining the extent and severity of colonic IBD are lacking. In
the modern colonoscopy era, DCBE is rarely used in IBD patients.
The calculated effective DCBE radiation dose is reported to be 6.4
to 17.0 mSv.
This method is more sensitive than DCBE in detecting early IBD
Furthermore, it is the primary method for obtaining tissue samples
for histologic examination. Even in normal macroscopic mucosa,
histologic changes that are diagnostic for IBD can be seen.
Therefore, it is important to take biopsies even from
A colonoscopic accuracy of 89% for distinguishing UC from CD has
The sensitivity for the diagnostic value of ultrasound in the
diagnosis of CD has been reported to be 67% to 96% and specificity
79% to 97%.
For UC, the main problem for ultrasound is that the rectum is a
relatively inaccessible area; proctitis is correctly detected by
ultrasound in only 15% of cases.
The reported sensitivity for UC detection by ultrasound is 77% to
Attempts have been made to assess disease activity by adding power
Doppler to the ultrasound examination. This is based on the
assumption that inflammation leads to neovascularization and
dilation of feeding arteries and draining veins, which results in
increased blood flow through the splanchnic circulation and bowel
wall. Conflicting results have been reported regarding the
correlation between splanchnic circulatory changes and disease
Only a few studies have compared CT results with the results of
other imaging methods for evaluation of IBD. CT sensitivity for
colonic IBD changes has been reported to be 69% to 84%.
An emerging technique is CT colonography. To the authors'
knowledge, 3 studies discussing the value of this technique exist.
Biancone et al
report the results of CT colonography in 16 patients with CD and an
ileocolonic anastomotic stricture. CT colonography had a
sensitivity of 73% and a specificity of 100% compared with
colonoscopy for detection of anastomotic recurrence.
Ota et al
showed that CT colonography had a good correlation with DCBE and
colonoscopy for the detection of elevated lesions, such as
inflammatory polyps and cobblestoning. Andersen et al
found a sensitivity for CT colonography of 100% for endoluminal
lesions. Acute IBD was correctly identified in 63.6% and chronic
IBD in 100%.
For ulcerated lesions, DCBE and colonoscopy were superior to CT
The median effective radiation dose of CT colonography is reported
to be 7.2 mSv.
The 2 radiopharmaceuticals suitable for IBD detection are 111In
oxine and 99mTc-hexamethylpropyleneamine oxime (HMPAO)-labeled
Since 99mTc-HMPAO has a higher sensitivity for the small bowel and
gives better quality images and because of superior resolution and
count density, it is the preferred agent.
Reported sensitivities and specificities for IBD detection are 83%
to 98% and 92% to 100%, respectively.
The mean effective radiation dose for 99mTc-HMPAO is reported to be
3.3 mSv and 4.5 mSv for 111In-oxine.
Large-bowel IBD imaging has been performed with field strengths
ranging from 0.1T to 3T. The combination of sequences used most
often is T2-weighted (T2W) turbo spin-echo (TSE) with T1-weighted
(T1W) gradient echo (GRE). The T1W GRE is mostly performed before
and after administration of gadolinium (Gd) in conjunction with fat
suppression techniques. As early as 1997, it was shown that T1W GRE
images in conjunction with intravenous Gd and oral barium were
superior to T1W spin-echo (SE) and T2W TSE images for the depiction
of normal and abnormal bowel wall, the depiction of mural
thickening, and the overall visualization of the gastrointestinal
Several years later, the same group reported that Gd-enhanced T1W
GRE imaging better depicted the extent and severity of CD than did
T2W single-shot (SS) TSE sequences.
Others concluded that SS sequences and Gd-enhanced T1W GRE
sequences with fat suppression are complementary. Post-Gd sequences
depicted inflammatory changes much better, whereas SS sequences
defined air-filled loops much better because of the lack of
air-related susceptibility artifact.
In a group of patients with CD, it was concluded that T2W MRI
depicts CD lesions and assesses mural and transmural inflammation
with the same accuracy as Gd-enhanced T1W MRI. These results were
obtained with the use of an oral superparamagnetic contrast agent.
Recently, 3 groups described the use of MR colonography in IBD.
The technique involves filling the colon with water or a water/Gd
enema in order to distend it. This is used in conjunction with
3-dimensional (3D) T1W GRE techniques before and after the
administration of intravenous Gd.
Filling and distension of the colon makes it possible to use
more sophisticated postprocessing techniques, such as virtual
colonoscopy. Whether filling and postprocessing techniques are
helpful in diagnosing the type, severity, and extent of colonic IBD
is unknown. A review on scanning techniques and reconstruction
possibilities has been published.
For water enema MR colonography, it has been reported that a
combination of T2W balanced GRE (B-GRE) and 3D T1W GRE after
intravenous Gd is a good combination for MR colonography. The B-GRE
gives superb contrast and motion insensitivity, and the 3D T1W GRE
has the ability to image the whole colon within 1 breath-hold while
maintaining relatively high spatial resolution.
In a small group of 5 patients, water enema MRI colonography was
performed with both a 3D T1W GRE sequence (before and after
administration of intravenous Gd) and a 2-dimensional (2D) T2W
B-GRE sequence. Both sequences showed equal results in the
visualization of IBD, but the image quality of the 2D T2W B-GRE
sequence was rated superior over the 3D T1W GRE.
MRI appearance of normal colon wall
Several authors have described the MR features of normal and
abnormal bowel wall in both patients and healthy volunteers.
These articles were published in the early and mid 1990s. In
interpreting the results, however, it is important to keep in mind
that current MRI sequences for abdominal imaging are much faster
and have a higher temporal and spatial resolution than those
reported in these articles. Normal colonic wall has signal
intensity (SI) between that of water and muscle on T1W sequences,
has a slightly higher SI than the surrounding fat on T1W sequences
with fat suppression, and has signal intensity between that of fat
and water on T2W sequences.
Normal colonic wall thickness is 3 to 4 mm,
although others report <5 mm.
After Gd enhancement, the wall appears as a thin enhancing line
Normal contrast enhancement is reported to be minimal.
An enhancement percentage of 108% for normal colonic wall has been
Ajaj et al
reported a mean colonic wall thickness in healthy volunteers on a
3D T1W GRE sequence after intravenous Gd of 2 mm, while D'Arienzo
reported a <4mm wall thickness in healthy volunteers. Wall
thickness of noninflamed segments in patients with UC was 3.7 mm ±
MRI features of IBD
The most striking abnormalities in both UC and CD are wall
thickening and increased enhancement.
Measured wall thickness is dependent on the spatial resolution
of the sequence and the precision of the measurement. A true cutoff
point between normal and inflamed bowel wall cannot be established
by interpreting the literature. The median wall thickness in CD
that is reported in different studies ranged from 4.9 to 6.7 mm and
in UC from 4.7 to 9.8 mm.
Ranges of wall thickness were 2 to 12 mm for CD and 3.5 to 11.6 mm
In general, the more severe the inflammation, the thicker the
After medical treatment, both the colonic and terminal ileal wall
The wall thickness of the terminal ileum has been reported to be
<3 mm in healthy volunteers and 5.9 mm ± 1.3 mm in patients with
When interpreting these results along with the results in healthy
volunteers, a colonic wall thickness <3 mm can be appreciated as
normal, 3 to 4 mm as a "gray zone," and >4 mm as pathologic.
There are many ways to define and measure increased enhancement.
In some articles, it is determined visually, compared with either
enhancement of the liver or of the psoas muscle. Authors use
different formulae on different workstations with different
Gd-enhanced sequences and different sequence timing. The results,
especially the quantitative calculations and measurements, are thus
difficult to reproduce and compare.
In patients with UC, an overlap in the percentage of enhancement
of inflamed and noninflamed segments has been reported, with
enhancement of inflamed segments of 40% to 313%, enhancement of
noninflamed segments at 7% to 63%, and enhancement in a healthy
control group at 10% to 66%.
Both diffuse enhancement (all parts of the bowel wall) and layered
enhancement (more enhancement of mucosa and serosa) have been
reported in patients with CD.
Layered enhancement seems to be a particularly good indicator of
Also, increased mesenteric vascularity, in the form of dilated,
terminal branches of the mesenteric arteries (vasa recta), is a
feature of IBD.
This is the so-called comb sign, which is produced by increased
flow and fibrofatty proliferation in the mesentery of inflamed
This sign is not specific for IBD, as it can also occur in forms of
vasculitis and bowel ischemia.
In a study of patients with CD of the terminal ileum, using T1W GRE
sequences after Gd, the enhancement of inflamed terminal ileum was
266% (range 105% to 450%).
Specific features of UC
Figures 2 through 5 illustrate and Table 1 summarizes the MRI
features of UC. In a specimen study, a high SI of both mucosa and
submucosa of patients with active UC was found on T1W and T2W
In patients with inactive disease, the colonic specimen showed a
low SI of both mucosa and submucosa on T1W and T2W images.
Reported MRI criteria for UC include wall thickening from the
rectum to the proximal colon and enhancement of the mucosa with no
or less enhancement of the submucosa.
This produces a low SI stripe- the so-called submucosal stripe.
Furthermore, increased SI of the pericolonic fat has been reported.
Backwash ileitis in UC shows mild enhancement and no wall
Furthermore, the loss of haustral markings has also been reported
to be an MRI feature of UC.
In cases of long-standing colitis, pseudopolyps can develop.
Specific features of CD
Figures 6 through 8 illustrate and Table 1 lists the specific
MRI features of CD. MRI criteria for CD include involvement of the
terminal ileum, enhancement of the entire bowel wall (full
thickness and transmural enhancement), relative sparing of the
rectum, wall thickening, increased SI of bowel wall and surrounding
fat, asymmetry, skip lesions, fistulae, infiltration of fat around
inflamed bowel wall, abscesses, lymphadenopathy, and fibrofatty
Fibrofatty proliferation is present if an increase in mesenterial
fat results in separation or displacement of adjacent bowel loops.
Comparison of modalities
MRI versus CT
Low et al
made a diagnostic comparison of CT and MRI in 26 patients with CD
who underwent both MRI and CT. Patients fasted for 3 hours before
each study. One hour prior to scanning, patients drank 1350 mL of
2% dilute barium contrast. For MRI, rectal water (500 to 1000 mL)
was administered; for CT, 500 to 1000 mL of iodinated contrast was
administered. For both examinations, 1 mg of intravenous glucagons
was administered. Coronal and axial T1W GRE sequences with a slice
thickness of 10 mm were performed, before and after intravenous Gd.
Helical CT was performed with a pitch of 1 and a collimation of 10
mm. Thickening of the bowel wall and increased enhancement were
evaluated. Colonoscopy, barium enema, or surgery was used as a gold
standard. In a total of 65 diseased bowel segments, 54 were
depicted by MRI and 41 by CT. This resulted in a sensitivity of 83%
and a specificity of 91% for MRI. For CT, these figures were 63%
and 91%, respectively. MRI had an accuracy of 89% and CT of 82%.
MRI versus DCBE
Sardanelli et al
reported the results of a study comparing MRI with DCBE in 6
patients with UC. MRI was performed after bowel cleansing, and the
colon was filled with a mixture of air and superparamagnetic iron
particles. Intravenous Gd was also administered. A T1W GRE sequence
with 8-mm thickness and an 0.8-mm interslice gap was used. In
addition to the previously mentioned wall thickness and enhancement
percentage, the authors reported that MRI findings of disease
extension were consistent with the DCBE findings.
Nozue et al
also described their results in 6 patients with UC. In 5 of the 6
patients, MRI was in accordance with DCBE and endoscopy for
assessing disease extent.
MRI versus ultrasound
Table 2 presents the conflicting results of 4 published articles
that compared MRI findings with those of ultrasound.
The study by Potthast et al
is more focused on small bowel abnormalities. In addition to
sensitivity and specificity for diagnosing CD in the terminal
ileum, this article also described other parameters. Sensitivity of
MRI for the number of affected bowel segments was 97.5% with a
specificity of 100%, whereas ultrasound scored 76% and 75%,
respectively. For stenosis, MRI had a sensitivity of 100% and a
specificity of 96%, and ultrasound a sensitivity of 58% and
specificity of 100%. For abscesses, MRI showed a sensitivity of
100% and a specificity of 97%, whereas ultrasound showed a
sensitivity of 89% and a specificity of 92%. For fistulae, MRI had
a sensitivity of 87% and a specificity of 93%, while ultrasound had
a sensitivity of only 31% and a specificity of 100%.
MRI versus nuclear medicine
Neurath et al
reported the results of a study of 59 patients with CD, who
underwent fluorodeoxyglucose-positron emission tomography (FDG-PET)
scanning, antigranulocyte scintigraphy, and MRI. In 28 patients,
there was also involvement of the terminal ileum and colon. These
patients also underwent ileocolonoscopy, which served as the gold
standard. MRI was performed on a 1T system. Axial and coronal T2W
TSE sequences, coronal T1W GRE sequences before and after
intravenous Gd, and axial and coronal T1W GRE fat-saturated
sequences after Gd were peformed. No colon filling was
performed-only small bowel filling with 1 L of mannitol solution
orally. Slice thickness was 8 mm. For the detection of inflamed
areas in the terminal ileum and the colon, FDG-PET had a
sensitivity of 85% and a specificity of 89%. MRI had a sensitivity
of 67% and a specificity of 93% and scintigraphy a sensitivity of
41% and a specificity of 100%.
MRI versus colonoscopy
Several articles have compared findings of MRI and colonoscopy
and have reported sensitivity and specificity values
Schreyer et al
and Ajaj et al
have described the results of MR colonography, and their results
are conflicting. Sensitivity on a per-patient basis ranges from 75%
to 91%. On a per-segment basis, reported sensitivities range from
32% to 89%. A specificity of 71% on a per-patient basis is
mentioned by Koh and coworkers
only. Specificity on a per-segment basis has been reported from 67%
to 100%. Since MR colonography is a developing technique, its final
place in the diagnosis of IBD is yet to be determined. Sensitivity
and specificity values might improve in the near future with faster
scanning techniques and 3T MRI.
Summary of MRI studies
The most striking MRI abnormalities encountered in IBD colitis
are wall thickening and increased enhancement. A thickness ≥4 mm
has to be considered pathologic, whereas a thickness of 3 to 4 mm
should raise suspicion and other IBD characteristics should be
sought. Besides these shared characteristics, UC and CD have their
own more or less specific characteristics (Table 1).
The first goal in imaging patients with suspected IBD colitis is
to distinguish UC from CD. The extent to which MRI can accomplish
this remains uncertain. In a study performed in the early 1990s,
MRI provided the correct diagnosis in 17 of 18 patients.
Alternatively, MRI permitted the correct diagnosis in only 50% of
the patients with CD in a study of pediatric patients.
In another pediatric study of IBD patients, MRI had a sensitivity
of 96% and specificity of 92% for distinguishing CD from UC.
The second imaging goal relates to defining disease extent and
activity. Attempts have been made to correlate MRI results, such as
wall thickening and wall enhancement, with endoscopy scores,
activity indices, and laboratory parameters. These study results
are both conflicting and difficult to reproduce because of the
different definitions of endoscopic and MRI severity and the
subjective aspect of activity indices. More uniformity for
endoscopic and MRI grading of inflammation is needed to reliably
compare study results. In UC, a significant correlation between
wall thickness, enhancement percentage, and endoscopic
abnormalities has been reported.
The same has also been reported in a mixed population of CD and UC
A significant correlation has been reported between the Crohn's
Disease Activity Index (CDAI), maximum enhancement, and time to
enhancement peak for the terminal ileum.
A good correlation,
as well as a poor correlation,
between enhancement percentage and endoscopic severity in mixed
patient groups has been reported. Three articles found no
correlation between the CDAI and MRI findings,
while another article found a significant correlation.
Recently, a significant correlation was found between the degree
of bowel wall enhancement and CDAI and between the change of signal
intensity of the bowel wall after the administration of intravenous
Gd and the inflammation severity at colonoscopy.
Furthermore, it has been reported that both wall thickening and
bowel wall enhancement decrease in patients with CD that is moving
from the active phase into remission due to treatment.
In 2 studies, MRI results were compared with Crohn's disease
endoscopic index of severity (CDEIS).
The results of 31 patients undergoing 1.5T MRI showed a
moderate-to-strong correlation between MRI severity and CDEIS (r =
The first publication about the use of 3T abdominal MRI in 20
patients with CD showed no statistically significant correlation
between MRI grading and CDEIS.
On determining the extent of UC, MRI and DCBE have been shown to
have equivalent results, but only in 12 patients from 2 studies.
Conflicting results on the extent of IBD has been reported, both
when MRI was compared with ultrasound and with colonoscopy.
Also, a significant correlation between MR findings and increase
of acute phase reactants had been described.
No data exist on cancer surveillance in long-standing colonic IBD
and the role of MRI in this area.
One study on the diagnostic capabilities of MRI compared with
other techniques showed that MRI has higher sensitivity than CT for
the diagnosis of inflamed bowel segments.
MRI has scored better than scintigraphy, and FDG-PET showed
promising diagnostic results.
Conflicting results have been reported between MRI and ultrasound
and MRI and colonoscopy.
Many reasons for the conflicting study results can be proposed,
such as inclusion of patients with different disease severity,
different MRI and ultrasound definitions of imaging features of
IBD, different "gold" standards, different ultrasonographers and
colonoscopists, and different MRI sequences. The chosen enema
composition also likely plays an important role in achieving higher
sensitivity in MR colonography. Schreyer et al
used a water/Gd enema, which is bright on T1W sequences, and makes
the appreciation of colonic wall enhancement more difficult. Ajaj
used a water enema, which is black on T1W sequences. The enhancing
colonic wall is better appreciated against a black background lumen
and suppressed fat signal than against a white background lumen and
suppressed fat signal. Because of higher sensitivity and
specificity, the black lumen technique seems to be favorable for
IBD detection compared with the bright lumen, although no
comparative research exists.
Recent research shows that because of limited spatial
resolution, MRI is not able to show superficial IBD lesions, such
as superficial ulcerations and mucosal erythema.
This is confirmed by others, showing that slight inflammation of an
anastomosis is diagnosed by colonoscopy but is not visible on MR
Therefore, scientific results point to a role of MRI in IBD
patients with moderate or severe complaints, where wall thickening
and increased enhancement are more likely to be present.
The current status of MRI in IBD colitis is that of a promising,
noninvasive technique for imaging extent of more severe colonic
IBD. When using MRI for this group of patients, one has to keep in
mind that in a normal-appearing colon, superficial ulcerations and
mucosal erythema can be present and that the disease extent is
probably greater than may be indicated on MRI.