Abstract

Purpose of review Imaging the gut provides information on Crohn's disease activity, identifies
complications and provides insight into patient symptoms. Imaging can help direct therapy and
can predict important patient outcomes. In a rapidly changing, technology-driven field, new
imaging applications add novel insights that we are only beginning to appreciate. The purpose
of this review is to highlight recent advances in imaging as they are applied to the assessment
of patients with Crohn's disease.
Recent findings In the past year, key literature describing cross-sectional imaging techniques,
including computed tomography (CT) based imaging, specifically CT enterography (CTE) and
magnetic resonance enterography (MRE), transcutaneous ultrasound, and PET-based imaging,
has emerged in the field of inflammatory bowel disease. MRI sequences that have been
recently applied to Crohn's disease assessment, including diffusion-weighted imaging (DWI)
and magnetization transfer imaging (MTI), add important new insights. These new data highlight
the current status of available imaging modalities and provide a glimpse into the future of our
practice.
Summary CTE and MRE are our new standard imaging modalities for small bowel Crohn's
disease. PET scanning is promising but currently only used routinely in centers with a strong
research presence in this area. Ultrasound is emerging as a useful, potentially less costly,
radiation-free technique. New MRI sequences offer future promise for effectively monitoring the
natural history of Crohn's disease.
Introduction
Common wisdom has traditionally held that some Crohn's disease patients were destined to
have inflammatory disease, whereas others had fistulizing or stricturing disease. Now we realize
that there is a progression from inflammation to fibrosis that occurs over time.[1] Some patients
progress rapidly enough that they have stricturing or fistulizing complications at their initial
presentation, whereas others may have inflammation that can be static for decades, never
developing complications of fistula or stricture formation. The challenge is to recognize patterns
of disease behavior early in the disease course to allow clinicians to tailor therapy, predict
complications, and use surgical options more effectively. Investigators are studying a variety of
clinical, endoscopic, genetic, serum and stool biomarkers to predict disease behavior. Currently,
we use cross-sectional imaging and other radiographic techniques to determine disease activity
and identify complications at a single point in time. As clinicians begin to think more in terms of
disease progression, we have begun to seek more sophisticated information from our imaging
technologies. Radiologists have broadened their goals to reach beyond optimizing sensitivity
and specificity to include information that reflects pathologic tissue processes like inflammation
and fibrosis. The future of imaging for Crohn's disease resides in technologies that reflect the

interplay between inflammation and fibrosis, and that can detect changes in these pathogenic
responses that occur over time and with treatment.
maging Techniques
Multiple imaging modalities are available for assessing the intestinal tract; each has strengths
and weaknesses and often the tests are complementary. Endoscopy-based techniques such as
colonoscopy, deep small intestinal endoscopy, and capsule endoscopy are highly sensitive, but
only assess the superficial mucosal layers. Cross-sectional imaging is best for visualizing the
deep layers of the gut and assessing for strictures, as well as extraluminal complications such
as fistulae and abscesses. Because of its broad availability and high spatial resolution,
computed tomography (CT) based imaging, especially CT enterography (CTE), has become the
most widely used cross-sectional imaging technology for Crohn's disease.[2] Intrinsic to CT
technology is the radiation utilized to generate the images. Growing concern about the potential
risks associated with cumulative diagnostic radiation exposure, particularly in young patients,
has led to growing interest and research into new techniques to minimize radiation from
diagnostic CT while maintaining diagnostic quality as well as interest in alternative imaging
modalities.[3-5] At the same time, improved spatial resolution of magnetic resonance (MR) based
techniques, along with development of faster imaging sequences have helped overcome bowel
motion-related artifacts, and have driven a rapid increase in the use of MR enterography (MRE)
for Crohn's imaging.[6,7] Further, ultrasound offers excellent tissue discrimination with the
advantage of being relatively low cost, safe and, potentially, office based.[8] A recent systematic
review of the standard imaging modalities applied to Crohn's disease has been published that
highlights advances in the field.[9] This review will consider new and future applications of these
technologies.
Computed Tomography Enterography
CTE has almost completely replaced the traditional small bowel follow through in most
academic centers. The key difference between CTE and standard abdomen and pelvis CT scan
lies in the use of low-density oral contrast that results in a low density of the bowel lumen
compared with the standard 'white out' of barium or iodine-based oral contrast used for standard
scans. In the USA, this is accomplished by the use of FDA-approved VoLumen (Bracco
Diagnostics, Westbury, New York, USA) and in European centers by other agents including
polyethylene glycol or administration of methylcellulose.[10] CTE also utilizes intravenous
iodinated contrast that allows excellent definition of the mucosa revealing enhancement pattern,
a highly sensitive indicator of mucosal inflammation. In addition, it helps better delineate the
mural stratification and allows for stricture assessment. The use of multidetector CT scanners
allows the acquisition of thin axial slices with nearly isotropic voxels which is used to generate
high resolution three-dimensional reconstructed images that provide insight into the distribution,
nature and significance of inflammation and strictures.
Limiting Radiation

The potential adverse effects of cumulative radiation dosage from diagnostic imaging have
gained attention in the medical community and in the lay press.[3] Measurement of effective
radiation doses in CT is dependent on several factors, such as scanning technique and patient
body habitus. One study by Jaffe et al. [11] found that the mean effective dose for abdominopelvic
multidetector CT was 16.1 mSv, which was up to five times higher than small bowel follow
through examination. Recently, several changes have been introduced to CT scanning
techniques that allow the acquisition of 'low-dose CT', leading to decrease in the overall dose of
radiation delivered to the patient undergoing CT examination while maintaining image quality.
These changes include the use of automatic tube current modulation (ATCM) and low-voltage
(kVp) settings used in the CT scanner along with introduction of new image reconstruction
algorithms that reduce the image noise typically associated with these techniques.[12,13]Dose
reduction efforts have resulted in markedly decreased radiation exposure.[14,15] The most recent
algorithms have the potential to reduce radiation exposure from CT scanning below 1 mSV with
good diagnostic accuracy (Fig. 1).[16] This is well below the annual ambient radiation exposure
from environmental sources. Still, the impact of cumulative radiation from repeated scans over
time still deserves consideration and alternatives should be used whenever possible. However,
the risk of missing a complication or the risk of not having the needed information to determine
appropriate therapy is also real. Therefore, in settings wherein MRI technology is not available
or not practical, CTE is a valuable tool.

(Enlarge Image)
Figure 1.
Two coronal reformatted images in a patient with Crohn's disease show active inflammatory
stricture in a jejunal bowel segment (arrow) and adjacent small abscess (arrowhead). The
examination was performed with reduced dose technique (total estimated radiation dose of 1.3
mSv) and the images were reconstructed utilizing a newly available image reconstruction
algorithm to reduce the noise typically associated with the low dose technique. The images
show good diagnostic accuracy for identifying the inflamed bowel segment, stricture formation
and abscess.
Magnetic Resonance Enterography
MRI techniques are based on the energy emitted when protons are released from alignment
after application of radio frequency pulses in a high-strength magnetic field. Scanners are
'tuned' to evaluate T1 and T2 relaxation times generating weighted images that highlight fat and
water, two key bodily substances. T2 weighted images help evaluate for bowel wall thickening

and edema. Gadolinium-enhanced T1 weighted images are used to assess the bowel wall
enhancement characteristics and to visualize the surrounding vasculature and tissues. The MRI
scanning protocols consist of various combinations of sequences that highlight different aspects
of the tissue to accomplish different goals. The technical aspects including a review of
pathologic findings have been detailed in a recent two-part review by Sinha et al. [6,7]
The small intestine provides unique challenges for MRI including uneven bowel distention,
inconsistent mucosal and bowel wall contrast, and intestinal motility. These challenges have
been addressed by specific protocols and sequences. Biphasic oral contrast agents such as
VoLumen, a non-absorbable oral contrast that can help evenly distend the small bowel lumen,
enable evaluation of the bowel wall demonstrating low T1 and high T2 signal intensity that
reproduce water intensity while more evenly distending the bowel, particularly the distal bowel.
These agents allow assessment of mucosal enhancement on T1 weighted images, and on T2
weighted images create high contrast between the wall (low T2 signal) and the lumen (high T2
signal) enabling sensitive assessment of fold and wall thickness. The deleterious effects of
random bowel motility on MRI image quality, effects that are not improved by breath holding or
gaiting as is done for respiratory or cardiac motion compensation, are partially controlled by the
use of antiperistaltic agents such as intravenous glucagon or similar agents administered during
the sequence acquisition. Finally, application of fat suppression highlights tissue edema on the
T2 weighted images. Just like CTE, enhancement and hypervascularity on MRE identify bowel
regions with histologic inflammation.[6,7] Identification of involved bowel regions is indicated by
increased mucosal enhancement, wall thickening and stratification, along with mesenteric
findings on T1 and T2 weighted images. Like CTE, MRE is sensitive to inflammation, but a
recent carefully done histologic study failed to demonstrate specific MRI findings that correlated
with fibrosis.[17] As with CTE, the factor most closely correlated with tissue fibrosis was tissue
inflammation confirming that the two are closely linked pathologically.[17,18]
Performance Characteristics of Computed Tomography Enterography and Magnetic
Resonance Enterography
Several recent studies add important information to our understanding of MRE as a tool to
assess disease severity and identify complications of Crohn's disease. Fiorino et al. [19] showed
that CTE and MRE similarly identify disease localization, wall thickening, bowel wall
enhancement (with MRE being slightly more sensitivity for ileal wall enhancement than CTE),
fistulae and mesenteric adenopathy. In this study, stricture identification was significantly more
sensitive with MRE than CTE. Sensitivities and specificities of MRE for small intestinal findings
in Crohn's disease were similar to other reported studies with 0.88 [0.780.99, confidence
interval (CI) 95%] sensitivity and 0.88 (0.681.0, CI 95%) specificity for localization of disease,
bowel wall thickening, and bowel wall enhancement. Identification of enteroenteric fistulas was
broadly similar between CTE and MRE (0.04 vs. 0.02; P = 0.08, respectively). The study
concluded that both CTE and MRE are highly effective techniques in assessing ileocolonic
Crohn's disease with broadly similar accuracy.

Under optimal patient circumstances, image quality of MRE rivals CTE. However, in a recent
study comparing the two modalities, the image quality of CTE was found to be superior to MRE.
Interobserver and intermodality agreement between CTE and MRE was found to be high for
both scans.[20] For disease evaluation, the interobserver agreement was high for CTE and
moderate for MRE. On the contrary, the intermodality agreement was fair to substantial
depending on the reader. This suggests that the evaluation of small bowel Crohn's disease is
both observer and modality dependent. However, despite these differences, both techniques
had comparable diagnostic yields. Therefore, given an experienced radiologist, both MRE and
CTE are comparable alternatives for assessing Crohn's disease.
Compared with CTE, MRE is more expensive, takes longer to perform due to multiple sequence
acquisitions compared to the single acquisition in CT and fewer radiologists are trained or feel
comfortable reading MRI scans. Further, although variations in CTE protocols exist, CTE
protocols are much more standardized between institutions and more easily applied and
interpreted in community practice. Therefore, MRE has been slow to gain use beyond major
medical centers. As MRI technology becomes more widely applied to the abdomen, MRE will
likely become more commonplace, just as CTE is replacing standard abdomen and pelvis CT
for imaging the small intestine.
Distinguishing Inflammation from Fibrosis
The ability of CTE to detect fibrosis or distinguish between inflammation and fibrosis is not well
established. This is an area of enormous clinical importance because the presence of a
predominately fibrotic stricture would direct a patient toward surgical therapy rather than
continued medical therapy. Some gastroenterologists and radiologists are quick to equate mural
thickening without enhancement to fibrostenotic disease. However, caution should be used in
equating lack of mural enhancement with fibrosis. Our experience is that very few, if any,
surgical samples have only fibrosis; the best predictor of fibrosis is the presence of
inflammation.[18] Inflammation and fibrosis seems so closely linked pathologically that we agree
with Zappa et al. [17] who found that fibrosis correlated well with inflammation and that the two
are inseparable and that 'it may not be relevant to make an exclusive distinction, as is usually
done, between inflammatory patients and fibrotic patients'.[18]
Special MRI Sequences
Most studies of CTE and MRE evaluate the ability of these techniques to detect inflamed bowel
wall regions. Determining the severity of inflammation is less straightforward. The ability to
determine severity of inflammation is complex and includes an inflammatory component at each
point and the length of involvement, as well as involvement of the thickness of the bowel wall.
Recently, Rimola et al.[21] using ileocolonoscopy-derived Crohn's Disease Endoscopic Index of
Severity have developed a MRI Index of Activity with elements that correlated with the
endoscopic gold standard. A more extensive scoring system that incorporates clinical,
endoscopic, and imaging parameters is being considered for a future study.[22]

An imaging parameter being explored for assessment of inflammation, diffusion-weighted

imaging (DWI), reflects the changes in the water mobility caused by interactions with cell
membranes, macromolecules, and alterations of the tissue environment. DWI is sensitive to
molecular diffusion based on the Brownian motion of the spins in biological tissues. This
technique has been widely used for intracranial disease, and has shown promise in the
abdomen for evaluation of various hepatic, renal, and pancreatic diseases. DWI is now being
explored for the evaluation of Crohn's disease.[2327] DWI provides information that complements
T1/T2 weighted images demonstrating hyperintense signal or restricted diffusion in involved
bowel segments. As a diffusion sequence is part of a routine MRI at many centers, one may
notice results of diffusion sequences being reported even before the full significance in Crohn's
disease has been determined. Hopefully, the rapidly emerging data in this field will shed some
light on the significance of these findings.
Advanced sequences like dynamic contrast-enhanced MRI have emerged from the oncology
world and are based on sensitivity to altered blood flow. Several studies have addressed the
timing of the scan in relation to the injection of gadolinium contrast and its ability to describe
tissue inflammation.[28,29]Dynamic contrast-enhanced MRI quantitatively assesses
pharmacokinetic models that correlate with angiogenesis, an important pathologic consequence
of chronic inflammation.[30,31] The qualitative and quantitative analysis of time-signal intensity
curves obtained with dynamic contrast-enhanced MRI can help differentiate active vs. inactive
Crohn's disease.[32] However, detailed histologic correlation studies on more than a handful of
patients are lacking. Dynamic contrast-enhanced MRI requires specifically timed contrast
administration and is not likely to become part of our routine scan protocols in the near future.
Magnetization transfer imaging in MRI is being explored as the only MRI sequence shown to
correlate specifically with fibrosis. Magnetization transfer takes advantage of a different set of
molecular properties than standard T1 and T2 imaging. Magnetization transfer reflects the
energy transferred from protons in free mobile water molecules to protons in water molecules
associated with large molecules such as collagen. Therefore, stiff body substances such as
muscle or fibrotic tissue have a high magnetization transfer effect, whereas magnetization
transfer is relatively insensitive to inflammation and tissue edema. Our group has demonstrated
that magnetization transfer ratio can semi-quantitatively detect collagen in an animal model of
Crohn's disease.[33] Further, the technique is sensitive to the development of fibrosis over time
and with treatment.[33,34]
Surface Ultrasound and Ultrasound Elastography
High-resolution transducers and methods such as measurement of flow parameters in the
superior mesenteric artery and contrast enhancement have increased the ability of surface
ultrasound to visualize inflamed small and large bowel. Advantages over other cross-sectional
imaging techniques include the opportunity for bedside/office performance, lower cost, and lack
of ionizing radiation, all of which have driven the increased use of ultrasound for assessment of
inflammatory bowel disease, particularly in European centers. A recent study applied

intravenous contrast-enhanced ultrasound to distinguish inflammatory vs. fibrotic stenosis in the

distal small bowel. Using clinical assessment of stenosis type, contrast-enhanced ultrasound
was not able to distinguish between inflammatory and fibrotic strictures. They found that the
ultrasound-determined bowel wall vascularity did not improve the diagnostic power of the
examination.[35] Ultrasound elastography imaging (UEI) is a promising approach that measures
tissue strain in response to an applied force that indirectly reflects fibrosis. This technique has
been applied to evaluate chronicity of deep venous thrombosis, degree of fibrosis in hepatic
cirrhosis, and kidney rejection after transplantation. UEI has been applied to Crohn's disease
where it has shown promise in animal models.[36,37] The technique has promise for distinguishing
inflamed vs. fibrotic strictures.[37]
PET Sequences
PET using fluorine-18-labeled-fluoro-2-deoxy-D-glucose (FDG) is a functional imaging method
that is sensitive to glucose metabolism. FDG accumulates in areas of active inflammation due to
leukocyte overexpression of glucose transporters, and increased metabolic activity. PET can
identify inflamed areas of the large and small bowel and can be combined with MR or CT for
localization of disease activity.[38,39] Like MRI techniques and ultrasound methods, PET warrants
consideration as an objective, noninvasive, quantifiable method for assessing Crohn's disease
activity potentially serving as an endpoint for clinical trials, allowing differentiation between
inflammatory and fibrotic strictures, and perhaps allowing for screening for inflammatory
pathway cancers. A recent study investigated the diagnostic value of PET CT to determine
whether PET added value to the standard CTE.[40] The investigators found no additional
inflamed segments beyond the ones identified by CTE. Interestingly, low FDG uptake in an
abnormal bowel segment correlated with failure of medical therapy. Although pathologic
correlation was lacking, the authors of the study speculated that these segments indicated
fibrostenotic disease. Whether the information derived from PET imaging justifies the
approximately 4 mSV additional radiation exposure related to the radiolabeled probe requires
additional investigation.
Imaging Pelvic Crohn's Disease
Perianal Crohn's disease is the one clinical setting wherein the superiority of MRI vs. other
cross-sectional imaging techniques is less intensely debated. MRI has sensitivity for detecting
perianal fistulas of over 80% with an accuracy of over 90%.[41]Pelvic MRI is sensitive to changes
in perianal Crohn's disease that occur with surgical treatment and antitumor necrosis factor
(TNF) therapy.[42] Decrease in contrast enhancement was associated with clinical improvement
in fistula after 1 year of anti-TNF therapy.[43] Pelvic MRI is also useful in patients with difficult-toassess vulvar Crohn's disease, particularly in the pediatric population.[44] Diffusion-weighted
imaging has recently been applied to perianal fistulae and may be an adjunct to T2 weighted
imaging in assessing the presence of edema, especially in patients with risk factors for contrast
agents.[45] Endoscopic ultrasound (EUS) is another useful technique for assessing perianal

fistulae and, when performed by experienced personnel, has similar test characteristics. CTbased scans perform less well in the evaluation of perianal Crohn's disease due to the
decreased contrast resolution and poor definition of the anal sphincter complex as compared
with MRI. MRI is superior in detecting the fistula tract and also in assessing the relationship of
the fistula to the external sphincter, which is of paramount importance for surgical fistula
management. The advantage of EUS is in expense and ease, particularly with an experienced
operator. MRI has the advantage over EUS of giving more of an overview of the disease
process and probable superiority for high or complex fistulas. Imaging of perianal fistulas has
been extensively reviewed
Imaging Pelvic Crohn's Disease
Perianal Crohn's disease is the one clinical setting wherein the superiority of MRI vs. other
cross-sectional imaging techniques is less intensely debated. MRI has sensitivity for detecting
perianal fistulas of over 80% with an accuracy of over 90%.[41]Pelvic MRI is sensitive to changes
in perianal Crohn's disease that occur with surgical treatment and antitumor necrosis factor
(TNF) therapy.[42] Decrease in contrast enhancement was associated with clinical improvement
in fistula after 1 year of anti-TNF therapy.[43] Pelvic MRI is also useful in patients with difficult-toassess vulvar Crohn's disease, particularly in the pediatric population.[44] Diffusion-weighted
imaging has recently been applied to perianal fistulae and may be an adjunct to T2 weighted
imaging in assessing the presence of edema, especially in patients with risk factors for contrast
agents.[45] Endoscopic ultrasound (EUS) is another useful technique for assessing perianal
fistulae and, when performed by experienced personnel, has similar test characteristics. CTbased scans perform less well in the evaluation of perianal Crohn's disease due to the
decreased contrast resolution and poor definition of the anal sphincter complex as compared
with MRI. MRI is superior in detecting the fistula tract and also in assessing the relationship of
the fistula to the external sphincter, which is of paramount importance for surgical fistula
management. The advantage of EUS is in expense and ease, particularly with an experienced
operator. MRI has the advantage over EUS of giving more of an overview of the disease
process and probable superiority for high or complex fistulas. Imaging of perianal fistulas has
been extensively reviewed
Specific Clinical Situations
MRI imaging has been studied in several relevant and practical clinical situations. In the
postoperative setting, endoscopic findings have been shown to predict clinical outcomes.[47] MR
enteroclysis and colonoscopy were shown to have similar value to predict disease recurrence in
postoperative patients suggesting that it may be possible to substitute a minimally invasive MR
enteroclysis, or possibly a noninvasive MRE, for a more invasive colonoscopy for evaluation of
disease recurrence in postoperative Crohn's disease patients.[45]Another common clinical setting
exists when a Crohn's disease patient visits the emergency department for evaluation of
abdominal pain. Typically, a standard positive oral contrast abdominal CT scan is performed. A

follow up negative oral contrast CTE or MRE is often ordered in the following days or weeks in
an attempt to determine more subtle details of the small bowel that were not seen due to the
positive oral contrast used in the standard CT scan. In most cases, this duplication is a waste of
patients' time, money and health care resources since the added diagnostic yield of the second
exam is low.[48] Once availability of these technologies broadens, CTE or MRE would be the
initial and only exam necessary thereby improving diagnostic efficiency.
Conclusion
Mucosal healing is becoming the standard for assessing therapeutic efficacy in Crohn's disease.
Endoscopic evaluation and cross-sectional radiographic imaging are the two commonly used
modalities currently at our disposal for assessing disease activity. Endoscopic evaluation will
always have an important role due to the opportunity to biopsy and perform therapeutic
interventions. However, less invasive cross-sectional imaging provides exquisite images of the
bowel and surrounding tissues that lend amazing insight into disease pathology. The future of
imaging is in harnessing the vast potential of the techniques to assess disease pathology as
they reflect inflammation and fibrosis, and to use that information to predict disease course and
anticipate complications. This will allow a new age of better care for inflammatory bowel disease
patients, wherein the use of potent biological therapies is guided by imaging in addition to
patient symptoms.

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Papers of particular interest, published within the annual period of review, have been highlighted as:
of special interest
of outstanding interest