An adequate luminal distention is prerequisite for CTE. Optimized luminal distention provides rapid and efficient luminal navigation, accurate detection and characterization of small bowel abnormalities. Patients drink approximately 1.0 to 1.5 L of oral contrast over 45 to 60 minutes. There are various oral contrast agents to obtain the distention of small bowel loops.2 The negative contrast agent such as polyethylene glycol solution (PEG), suspension of 0.1% barium sulphate and water-methylcellulose solution is preferred because they allow better depiction of bowel wall enhancement. Water-methylcellulose solution has been gradually replaced by PEG or suspension of 0.1% barium sulphate. Our current protocol is summarized in Table 1.

In CTE, oral contrast agent is administered by the oral route. However, contrast infusion through nasojejunal tube may be performed. The CT imaging after total opacification of the small bowel by such infusion is called as CT enteroclysis. Although the CT enteroclysis has better jejunal distention and higher specificity for detecting pathologic small bowel,2 there are unavoidable limitations such as patient's discomfort related with nasojejunal tube insertion and the increased radiation dose.3 Therefore, CTE has become a more preferred imaging technique for evaluating IBD because of the superior patient compliance and procedural convenience.

CTE imaging protocol is as follows in our institute. It was performed using multidetector CT (Sensation-16 or Sensation-64; Siemens Medical Systems, Erlangen, Germany). Intravenous contrast material (120 to 150 mL) (Omnipaque 300 mg I/mL; Amersham Health Inc., Princeton, NJ, USA) was administered at a rate of 3 mL/sec. A bolus-tracking program was used to obtain singe enteric phase CT data after the intravenous injection of contrast agent. The region of interest cursor for bolus tracking was placed in the descending aorta at the level of the first lumbar vertebra for real time serial monitoring.

Acquisition of enteric phase images was commenced at 35 seconds after the trigger (trigger threshold level, 100 Hounsfield unit [HU]). Axial and coronal images were reconstructed and transferred to a picture archiving and communication system for image interpretation (slice thickness of 3 mm, and a reconstruction interval of 3.0 mm).

Crohn disease has a variety of appearances at CTE depending on whether the activity is acute inflammatory or chronic fibrostenosing and whether there are complications such as fistula or abscess. On CTE, enteric findings such as mural hyperenhancement, bowel wall thickening, mural stratification and extraenteric findings such as engorged vasa recta ("comb sign"),5 and increased attenuation of the mesenteric fat are features of active inflammatory small bowel Crohn disease.6,7

Among these findings, combination of mural hyperenhancement and bowel wall thickening is the most sensitive CTE findings suggesting the active inflammatory Crohn disease.7 While early studies suggested that bowel wall thickness correlated best with disease activity,7,8 more recent studies have suggested that mural hyperenhancement may be a more sensitive sign.9

Mural hyperenhancement refers to segmental hyperenhancement of the small bowel wall compared with the adjacent small bowel loops (Figs. 1, 2).7,9 It is important to compare the bowel loops with similar degree of distension because normal collapsed loops show greater attenuation than that of distended bowel loop. Quantitative measurement techniques have been used to objectively correlate mural hyperenhancement and bowel wall thickness with disease activity. Using a mural attenuation threshold of 109 HU and an abnormal to normal loop enhancement ratio of more than 1.3, CTE is highly correlated with histologic findings of active disease. Visual assessment, however, presents higher specificity than do quantitative measurements.9

Bowel wall thickening refers to wall thickness of greater than 3 mm in a distended bowel loop (Figs. 1-3). It is the most frequently observed CT finding in Crohn disease, presenting in up to 82% of patients.10

Mural stratification is visualization of the bowel wall layers on CT after intravenous contrast administration.6,7 Bilaminar mural stratification refers to mucosal hyperenhancement and decreased intramural attenuation. Trilaminar mural stratification refers to alternating areas of high and low attenuation due to mucosal and serosal hyperenhancement and low intramural attenuation (Figs. 1, 2). The low intramural attenuation can represent edema, inflammatory infiltrate, or fat. Mural stratification due to intramural edema is more indicative of active disease compared to a homogenously enhanced wall,8,11 while the presence of intramural fat indicates a more chronic process.6 One thing to notice is that mural stratification is not specific for Crohn disease and may be seen with other small bowel inflammatory conditions, such as ischemia, ulcerative colitis, and radiation enteritis.10

Increased attenuation of the mesenteric fat is due to edema and engorgement of the vasa recta (Fig. 1). The "comb sign" refers to engorged vasa recta that penetrate the bowel wall perpendicular to the bowel lumen, simulating the appearance of a comb (Fig. 2). Increased attenuation of the mesenteric fat in combination with the "comb" sign is the most specific CT finding for active Crohn disease.12 It correlates with clinically advanced, active, and extensive Crohn disease.5,11,12 The "comb sign" on CTE is also reported to be associated with higher C-reactive protein levels12 and more intensive medication regime than for patients with normal vasculature.11

It is important to differentiate active inflammatory small bowel strictures from fibrotic strictures in patients with Crohn disease, because the former are mostly managed medically whereas the latter may require surgical intervention (e.g., balloon dilation, strictureplasty, or resection).3 CTE signs of chronic fibrostenosing disease are strictures without mural hyperenhancement or other signs of active inflammation, submucosal fat deposition, sacculations, and fibrofatty proliferation (Fig. 4).6,13

In fibrostenosing Crohn disease, mural stratification may be absent because of the transmural fibrosis and/or muscular hypertrophy and collagen deposition leading to a homogeneous and less-intense enhancement.10 Strictures may occur in patients with active inflammatory disease due to inflammation with edema and bowel spasm. However, strictures are more frequent with chronic fibrosis.14,15 Differential point is that a stricture in acute disease is manifested by mural hyperenhancement, more severe bowel wall thickening, and mural stratification. Submucosal fatty deposition in the bowel wall is also considered chronic changes of Crohn disease.6 However, active inflammation and fibrosis often coexist in the same patient or even in the same affected bowel segments in Crohn disease.

As the mesenteric border of bowel is preferentially affected by the inflammatory process of Crohn disease, the bowel loops often exhibit asymmetric mural fibrosis and shortening. Eventually, asymmetric fibrosis of the bowel loops combined with the increase in intraluminal pressure during the peristaltic movements results in sacculation of the antimesenteric wall (Fig. 3A).16

Fibrofatty proliferation has been long recognized as a hallmark of Crohn disease (Fig. 3B). It extends from the mesenteric attachment and partially covers the chronically inflamed bowel loop. Recent studies suggest that the hypertrophied mesenteric fat might have a role-related to the fat's capacity to produce tumor necrosis factor α-in sustaining the inflammatory process in Crohn disease.17

The transmural inflammation of the bowel in Crohn disease coupled with increased intraluminal pressure proximal to the site of strictures can lead to extension of the inflammatory process across the serosal surface into the adjacent mesentery or structures. CTE has an important role in the evaluation of extraenteric complications of Crohn disease. The most common extraenteric complications include fistula, sinus tract, and abscess.15,18,19

Blind-ending inflammatory tracts form a sinus that can lead to a fistula if it communicates with another structure or fluid cavity. On CTE, sinus (Fig. 3C) or fistula (Figs. 2B, C, 5) are demonstrated as tethering of bowel loops and visualization of linear, enhancing tracts with or without communication with adjacent structures such as peritoneal or retroperitoneal spaces, skin or adjacent organs, or bowel, respectively.20 The most common type of fistula in Crohn disease is a perianal fistula (Fig. 5B). Other types of fistulas in Crohn disease include enterocutaneous, rectovaginal, enterovaginal, and enterovesicular fistulas.19 CTE has a high sensitivity for diagnosing fistulas. A recent study reported that CTE correctly identifies the presence or absence of fistulae in 94% of patients.15 The improved detection of fistulas by CTE compared to earlier studies likely reflects the improved spatial resolution due to thinner slice collimation and higher quality multiplanar images.

Abscesses are easily detected by CTE which is usually contiguous to the diseased bowel segment and is seen in the mesentery or retroperitoneal space (Fig. 2).6 The accurate detection of abscesses and fistulas has high importance not only because it affects the decision to treat medically or surgically, but also it can affect the method of surgical approach (laparoscopic vs. open). A recent study by Bruining et al.21 showed that CTE affected on the physician's level of confidence for the findings of active small bowel disease, fistula, abscess, or stricture formation, which was altered in more than 90% of cases, with clinically significant changes in up to 77.6%. Booya et al.22 also reported detection of clinically unsuspected penetrating disease on CTE examinations, leading to alteration in therapy in up to 61% of patients with Crohn disease.

Other extraenteric manifestations of Crohn disease, such as mesenteric lymphadenopathy, cholelithiasis, nephrolitiasis, sacroiliitis, and primary sclerosing cholangitis, can also be evaluated.6

CTE can also be used to assess treatment response in Crohn disease, which manifests as decreasing mural hyperenhancement and bowel wall thickening, and improvement in the engorged vasa recta.8,23,24 Hara et al.8 observed that CTE interpretation of the disease progression or regression correlated with symptoms in 16/20 (80%) patients. Wu et al.23 reported that CTE findings have high correlation with clinical remission. According to their results, mural hyperenhancement and bowel wall thickening, the most sensitive signs of active disease, were decreased significantly after effective therapy, using a combination of clinical, endoscopic, pathologic, and laboratory findings as the criteria of disease remission. They also observed that the pattern of mural stratification changed with the trend from trilaminar or bilaminar stratification with mucosal hyperenhancement toward homogenous or bilaminar stratification without mucosal hyperenhancement. In addition, CTE can be used in evaluating postoperative recurrence of Crohn disease, which is most frequently seen at or immediately proximal to the anastomotic site.

Radiation concern is an important issue in CTE because patients with Crohn disease are relatively younger and are expected to undergo multiple follow-up CT studies.35 Desmond et al.36 reported that portion of CT scans contributing to cumulative effective dose increased from 46.3% during the first 5 years to 84.7% during the final 5 years in their 15-year study of patients with IBD. This increase is likely due to the increased use of CT. In addition, a very recent study of Korean patients with IBD showed that 34.7% of patients with Crohn disease were exposed to harmful levels of radiation (cumulative effective dose >50 mSv) and CT accounted for 81.6% of total effective dose.37 Therefore, radiation dose reduction technique should be applied in CTE image acquisition protocol. Various techniques have been developed to reduce the radiation dose to the patient. First one is tube current (mA) modulation, which modulates the mAs based on the body thickness of each individual patient with sustaining diagnostic image quality.38 Second one is tube potential modulation (kV). Lowering tube potential is effective for dose reduction. In addition, lowering kV typically leads to an increase in iodine contrast, which may be helpful for detecting enhanced inflammatory bowel thickening. However, it allows more noise. Therefore, lower dose with constant image quality (contrast noise ratio) is essential in application of lowering tube potential.39 New image reconstruction technique such as iterative reconstruction enables the noise reduction using CT projection data in the lowering kV setting. Kaza et al.40 reported that CTE at 80 kVp with iterative reconstruction can produce diagnostically acceptable image quality with effective dose, 4.6 mSV, while the effective dose of routine CTE at 120 kVp was 15.8 mSV. There are more important dose reduction strategies apart from these advanced technologies. One is to minimize the number of dynamic CT phases. Wold et al.41 reported that arterial phase imaging is not contributory for detection of active Crohn disease. Single-phase imaging at CTE is sufficient in most cases of evaluation of Crohn disease (Fig. 13).