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 [0.78–0.99, confidence

interval (CI) 95%] sensitivity and 0.88 (0.68–1.0, 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.[23–27] 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-to-

assess 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. CT-

based 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-to-

assess 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. CT-

based 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.

References1. Louis E, Collard A, Oger AF, et al. Behaviour of Crohn's disease according to the Vienna classification:

changing pattern over the course of the disease. Gut 2001; 49:777–782.

2. Huprich JE, Fletcher JG. CT enterography: principles, technique and utility in Crohn's disease. Eur J Radiol

2009; 69:393–397.

3. Brenner DJ, Hall EJ. Computed tomography: an increasing source of radiation exposure. N Engl J Med 2007;

357:2277–2284.

4. Palmer L, Herfarth H, Porter CQ, et al. Diagnostic ionizing radiation exposure in a population-based sample of

children with inflammatory bowel diseases. Am J Gastroenterol 2009; 104:2816–2823.

5. Kroeker KI, Lam S, Birchall I, et al. Patients with IBD are exposed to high levels of ionizing radiation through

CT scan diagnostic imaging: a five-year study. J Clin Gastroenterol 2011; 45:34–39.

•This study assesses the total effective dose of ionizing radiation from abdominal diagnostic imaging in patients with inflammatory bowel disease over a 5-year period.

6. Sinha R, Verma R, Verma S, Rajesh A. MR enterography of Crohn disease. Part 1. Rationale, technique, and

pitfalls. AJR 2011; 197:76–79.

••This is the first of a comprehensive two-part review on usefulness of MRE for Crohn's disease.

7. Sinha R, Verma R, Verma S, Rajesh A. MR enterography of Crohn disease. Part 2. Imaging and pathologic

findings. AJR 2011; 197:80–85.

••This is the second of a comprehensive two-part review on usefulness of MRE for Crohn's disease.

8. Strobel D, Goertz RS, Bernatik T. Diagnostics in inflammatory bowel disease: ultrasound. World J

Gastroenterol 2011; 17:3192–3197.

•This is a review of the usefulness of ultrasound for the evaluation of inflammatory bowel disease.

9. Panes J, Bouzas R, Chaparro M, et al. Systematic review: the use of ultrasonography, computed tomography

and magnetic resonance imaging for the diagnosis, assessment of activity and abdominal complications of Crohn's disease. Aliment Pharmacol Ther 2011; 34:125–145.

•This is a systematic review of the major imaging diagnostic modalities. Highly useful tables are included.

10. Minordi LM, Vecchioli A, Poloni G, et al. Enteroclysis CT and PEG-CT in patients with previous small-bowel

surgical resection for Crohn's disease: CT findings and correlation with endoscopy. Eur Radiol 2009; 19:2432–2440.

11. Jaffe TA, Gaca AM, Delaney S, et al. Radiation doses from small-bowel followthrough and abdominopelvic

MDCT in Crohn's disease. Am J Radiol 2007; 189:1015–1022.

12. Summers RM. Dose reduction in CT: the time is now. Acad Radiol 2010; 17:1201–1202.

13. Kalra MK, Maher MM, Toth TL, et al. Techniques and applications of automatic tube current modulation for CT.

Radiology 2004; 233:649–657.

14. Kambadakone AR, Chaudhary NA, Desai GS, et al. Low-dose MDCT and CT enterography of patients with

Crohn disease: feasibility of adaptive statistical iterative reconstruction. Am J Roentgenol 2011; 196:W743–W752.

•This review discusses new techniques to limit radiation exposure to multidetector CT scans in patients with Crohn's disease.

15. Kaza RK, Platt JF, Al-Hawary MM, et al. CT enterography at 80 kVp with adaptive statistical iterative

reconstruction versus at 120 kVp with standard reconstruction: image quality, diagnostic adequacy, and dose reduction. Am J Roentgenol. doi:;198:10.2214/AJR.11.6597 (in press).

•This is an example of the new techniques to limit radiation exposure related to diagnostic CT imaging.

16. Leea TY, Chhemb RK. Impact of new technologies on dose reduction in CT. Eur J Radiol 2010; 76:28–35.

17. Zappa M, Stefanescu C, Cazals-Hatem D, et al. Which magnetic resonance imaging findings accurately

evaluate inflammation in small bowel Crohn's disease? A retrospective comparison with surgical pathologic analysis. Inflamm Bowel Dis 2011; 17:984–993.

••This is one of the few studies comparing radiographic findings to resected surgical specimens. This study also highlights the close association between tissue inflammation and fibrosis in Crohn's disease.

18. Adler J, Punglia D, Dillman JR, et al. CT enterography findings correlate with tissue inflammation in resected

small bowel Crohn's disease. Inflamm Bowel Dis 2011. doi: 10.1002/ibd.21801. [Epub ahead of print]

•This study is another of the few studies comparing radiographic findings to resected surgical pathology specimens. This study also highlights the close association between tissue inflammation and fibrosis in Crohn's disease. A thickened ileum on CTE without mucosal enhancement does not equate to tissue fibrosis as commonly thought.

19. Fiorino G, Bonifacio C, Peyrin-Biroulet L, et al. Prospective comparison of computed tomography

enterography and magnetic resonance enterography for assessment of disease activity and complications in ileocolonic Crohn's disease. Inflamm Bowel Dis 2011; 17:1073–1080.

•This is a study concluding that both CTE and MRE are highly effective techniques in assessing ileocolonic Crohn's disease with broadly similar accuracy.

20. Jensen MD, Ormstrup T, Vagn-Hansen C, et al. Interobserver and intermodality agreement for detection of

small bowel Crohn's disease with MR enterography and CT enterography. Inflamm Bowel Dis 2011; 17:1081– 1088.

•This is a study reporting on interobserver and intermodality agreement between CTE and MRE.

21. Rimola J, Ordas I, Rodriguez S, et al. Magnetic resonance imaging for evaluation of Crohn's disease:

validation of parameters of severity and quantitative index of activity. Inflamm Bowel Dis 2011; 17:1759–1768.

•The aim of this study was to develop and validate a Magnetic Resonance Index of Activity to provide quantitative predictors of active CD and severe CD.

22. Pariente B, Cosnes J, Danese S, et al. Development of the Crohn's disease digestive damage score, the

Lemann score. Inflamm Bowel Dis 2011; 17:1415–1422.

•The purpose of this study was to describe plans to develop a Crohn's disease digestive damage score that incorporates imaging parameters in addition to other clinically relevant information.

23. Oto A, Kayhan A, Williams JT, et al. Active Crohn's disease in the small bowel: evaluation by diffusion

weighted imaging and quantitative dynamic contrast enhanced MR imaging. J Magn Reson Imaging 2011; 33:615–624.

••This is a novel study examining the use of diffusion-weighted imaging and quantitative dynamic contrast-enhanced MRI for the assessment of Crohn's disease severity.

24. Kiryu S, Dodanuki K, Takao H, et al. Free-breathing diffusion-weighted imaging for the assessment of

inflammatory activity in Crohn's disease. J Magn Reson Imaging 2009; 29:880–886.

25. Oto A, Zhu F, Kulkarni K, et al. Evaluation of diffusion-weighted MR imaging for detection of bowel

inflammation in patients with Crohn's disease. Acad Radiol 2009; 16:597–603.

26. Oussalah A, Laurent V, Bruot O, et al. Diffusion-weighted magnetic resonance without bowel preparation for

detecting colonic inflammation in inflammatory bowel disease. Gut 2010; 59:1056–1065.

27. Panes J, Ricart E, Rimola J, et al. New MRI modalities for assessment of inflammatory bowel disease. Gut

2010; 59:1308–1309.

28. Knuesel PR, Kubik RA, Crook DW, et al. Assessment of dynamic contrast enhancement of the small bowel in

active Crohn's disease using 3D MR enterography. Eur J Radiol 2010; 73:607–613.

29. Horsthuis K, Nederveen AJ, de Feiter MW, et al. Mapping of T1-values and Gadolinium-concentrations in MRI

as indicator of disease activity in luminal Crohn's disease: a feasibility study. J Magn Reson Imaging 2009; 29:488– 493.

30. Taylor SA, Punwani S, Rodriguez-Justo M, et al. Mural Crohn's disease: correlation of dynamic contrast-

enhanced MR imaging findings with angiogenesis and inflammation at histologic examination – pilot study. Radiology 2009; 251:369–379.

31. Oommen J, Oto A. Contrast-enhanced MRI of the small bowel in Crohn's disease. Abdom Imaging 2011;

36:134–141.

••This is a study exploring the use of contrast-enhanced MRI for small bowel evaluation in Crohn's disease.

32. Giusti S, Faggioni L, Neri E, et al. Dynamic MRI of the small bowel: usefulness of quantitative contrast-

enhancement parameters and time-signal intensity curves for differentiating between active and inactive Crohn's disease. Abdom Imaging 2010; 35:646–653.

33. Adler J, Swanson S, Schmiedlin-Ren P, et al. Magnetization transfer helps detect intestinal fibrosis in an

animal model of Crohn disease. Radiology 2011; 259:127–135.

•This study applies a MRI sequence that semi-quantitatively detects fibrosis and demonstrates in an animal model that the technique is sensitive to changes in fibrosis that occur over time.

34. Zimmermann EM, Adler J, Rahal K, et al. Rat specific anti-TNFa decreases inflammation and fibrosis in

experimental Crohn's disease. Gastroenterology 2011; 140:S176.

35. Schirin-Sokhan R, Winograd R, Tischendorf S, et al. Assessment of inflammatory and fibrotic stenoses in

patients with Crohn's disease using contrastenhanced ultrasound and computerized algorithm: a pilot study. Digestion 2011; 83:263–268.

•Contrast-enhanced ultrasound was not able to distinguish inflamed vs. fibrotic strictures in this pilot study.

36. Fraquelli M, Sarno A, Girelli C, et al. Reproducibility of bowel ultrasonography in the evaluation of Crohn's

disease. Dig Liver Dis 2008; 40:860–866.

37. Stidham RW, Xu J, Johnson LA, et al. Ultrasound elasticity imaging for detecting intestinal fibrosis and

inflammation in rats and humans with Crohn's disease. Gastroenterology 2011; 141:819–826.

••This study explores ultrasound elasticity imaging for Crohn's disease with pilot data in humans supporting usefulness in differentiating inflammation from fibrosis.

38. Meisner RS, Spier BJ, Einarsson S, et al. Pilot study using PET/CT as a novel, noninvasive assessment of

disease activity in inflammatory bowel disease. Inflamm Bowel Dis 2007; 1:993–1000.

39. Loffler M, Weckesser M, Franzius C, et al. High diagnostic value of 18F-FDGPET in pediatric patients with

chronic inflammatory bowel disease. Ann N Y Acad Sci 2006; 1072:379–385.

40. Ahmadi A, Li Q, Muller K, et al. Diagnostic value of noninvasive combined fluorine-18 labeled fluoro-2-deoxy-

D-glucose positron emission tomography and computed tomography enterography in active Crohn's disease. Inflamm Bowel Dis 2010; 16:974–981.

41. Ziech M, Felt-Bersma R, Stoker J. Imaging of perianal fistulas. Clin Gastroenterol Hep 2009; 7:1037–1045.

42. Gligorijevic V, Spasic N, Bojic D, et al. Role of pelvic MRI in assessment of combined surgical and infliximab

treatment for perianal Crohn's disease. Acta Chirurgica Iugoslavica 2010; 57:89–95.

43. Savoye-Collet C, Savoye G, Koning E, et al. Fistulizing perianal Crohn's disease: contrast-enhanced

magnetic resonance imaging assessment at 1 year on maintenance anti-TNF-alpha therapy. Inflamm Bowel Dis 2011; 17:1751–1758.

•This is a study concluding that MRI is the imaging modality of choice for perianal Crohn's disease and is sensitive to changes that occur with therapy providing novel insights into the important disease complication.

44. Pai D, Dillman JR, Mahani MG, et al. MRI of vulvar Crohn disease. Pediatr Radiol 2011; 41:537–541.

•This is a case report and literature review of use of MRI for evaluating vulvar Crohn's disease.

45. Koilakou S, Sailer J, Peloschek P, et al. Endoscopy and MR enteroclysis: equivalent tools in predicting clinical

recurrence in patients with Crohn's disease after ileocolic resection. Inflam Bowel Dis 2010; 16:198–203.

46. de Miguel Criado J, García del Salto L, Fraga Rivas P, et al. MR imaging evaluation of perianal fistulas:

spectrum of imaging features. Radio Graphics 2012; 32:175–194.

•This is a technical review of imaging evaluation of perianal fistulas.

47. Rutgeerts P, Van Assche G. What is the role of endoscopy in the postoperative management of Crohn's

disease? Inflamm Bowel Dis 2008; 14 (Suppl 2):S179–S180.

48. Schreyer AG, Hoffstetter P, Daneschnejad M, et al. Comparison of conventional abdominal CT with MR-

enterography in patients with active Crohn's disease and acute abdominal pain. Acad Radiol 2010; 17:352–357.

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

• of special interest

•• of outstanding interest