Fig. 5.1
Images of CT enterography in acute Crohn’s disease. a Appearance of double-balloon enteroscopy shows a longitudinal ulcer in the terminal ileum. b The coronal view of CT enterography shows “target sign” in the ileum. c The axial view of CT enterography shows mural stratification in the ileum
Fig. 5.2
Images of CT enterography in chronic Crohn’s disease. a Appearance of double-balloon enteroscopy shows a longitudinal ulcer in the terminal ileum with a stricture. b The coronal view of CT enterography shows a mural linealization with a contralateral sacculation in the ileum
New endoscopic modalities including capsule endoscopy and balloon-assisted endoscopy allow more detailed assessment of the intraluminal pathology of small-bowel CD; however, intestinal adhesions or strictures often hamper the performance of these endoscopic examinations in patients with CD.
In recent years, cross-sectional imaging modalities such as CT and MRI are strongly recommended to be used in the diagnosis and monitoring of the disease activity of CD in the US and Europe [9]. These imaging devices can visualize not only the intestinal wall of the small bowel, but also extra-enteric complications such as fistulae and abscesses in a minimally invasive manner.
In those cross-sectional imaging modalities, CTE was first introduced by Raptopoulos et al. in 1997 [10], and has been the most widely used imaging technique for CD in the US and Europe because of its short scan time, high spatial resolution, usefulness, and tolerability [11].
5.3 Technique
CTE is an imaging method that enables good visualization of the intestinal wall and lumen of the small intestine. CTE is performed by multi-detector row CT (MDCT) with intravascular contrast, after the small intestine is dilated with large volumes (1.3–1.8 l) of neutral or low-density oral enteric contrast material.
For the success of the procedure, it is necessary for patients to ingest at least 1.3 l of oral contrast agent over 60 min. In the US and Europe, a low-density barium sulfate contrast especially designed for CTE, 0.1% VoLumen® (Bracco, Milan, Italy) is commercially available. However, any materials with isotonic and CT attenuation properties similar to that of water can be used for CTE [12]. In our facility, patients drink total 1.8 l of isotonic magnesium citrate solution (Magcorol P®, HORII Pharm., Osaka, Japan) at a steady rate (approximately 450 ml every 15 min) over 1 h before CT scanning, prior to performance of the per rectal balloon-assisted endoscopy in the afternoon of the same day. Anti-peristaltic agents such as glucagon and butylscopolamine are usually administered immediately prior to CT in order to avoid image degradation from peristalses. One hundred and fifty ml of Omnipaque 300 (Daiichi-Sankyo Pharm. Inc., Tokyo) are administered intravenously at 4 ml/s. Supine single-phase images by a more than 64-slice CT scanner are acquired 50–60 s after intravenous contrast administration at 2 mm of slice thickness, with a reconstruction interval of 0.75 mm.
5.4 Findings of IBD
For improvement in accuracy of both luminal navigation and interpretation, it is recommended that reading of CT findings should start with a multiplanar review [11]. Although differential contrast enhancement is important to distinguish abnormal from normal segments, it should be noted that the jejunum enhances more than the ileum, and also that collapsed bowel loops appear to enhance more than the distended loops.
The colon is frequently well distended, and it is possible to assess the associated pathology in the absence of an intraluminal contrast medium; it is, however, important to be aware that the evaluation of colonic pathology using CTE is limited.
Macari et al. [13] described several criteria to help to characterize abnormal small-bowel segments, including pattern of contrast enhancement, length of involvement, degree and symmetry of wall thickening, location in proximal/distal jejunum/ileum, location of pathology within the small-bowel wall (mucosal/submucosal/serosal) and associated abnormality in the adjacent mesentery or vessels.
Active small-bowel CD shows bowel-wall thickening, mural hyper-enhancement, “target” appearance with mural stratification, engorged vasa recta (the “comb sign”) and increased density in perienteric mesenteric fat. Chronic changes in CD include fibrotic strictures and submucosal fatty deposition in the bowel wall [14].
Small-bowel mural thickness greater than 3 mm should be considered abnormal. In the pathology of CD, the small-bowel wall is affected asymmetrically, predominantly the mesenteric border, frequently leading to asymmetric inflammation and fibrosis, with pseudosacculation of the antimesenteric border. Small-bowel wall enhancement is closely correlated with disease activity [15]. Mural stratification describes the visible layers of the inflamed small bowel wall shown following administration of intravenous contrast in the enteric phase. However, when mural stratification is assessed, it should be considered that between the strongly enhanced mucosa and serosa, the intervening layer of the intestinal wall enhances to a varying degree, due either to intramural edema (isodense with water), indicating active disease, or to intramural fat, indicating chronic inflammation. The comb sign is created by engorged vasa recta, which consists of the vessels penetrating the bowel wall perpendicular to the bowel lumen, and also indicates active inflammation [16]. Fibrofatty proliferation refers to fatty deposition along the mesenteric border of bowel segments affected by CD, and often remains in clinically quiescent disease. However, the presence of increased fat density surrounding thickened or abnormally enhanced bowel is not like fibrofatty proliferation, highly specific in active disease, because it results from inflammatory cell infiltrations.
It is not rare that luminal narrowing is seen in the bowel segment affected by CD. In the assessment of luminal narrowing, the presence of pre-stenotic dilatation may be helpful in defining, locating, and assessing the functional significance of a stricture [16], and also, as mentioned, assessing the signs of acute inflammation can be helpful. Recently, Arai et al. [17] reported that a CTE scoring system for disease severity, which is scored based on bowel-wall thickness, mural hyper-enhancement, and engorged versa recta, is significantly correlated to an endoscopic index. Furthermore, faecal biomarker calprotectin also correlated with the CTE score. Hence, a combination of calprotectin and CTE appears to be effective for monitoring CD activity in patients with small intestinal CD, including patients with strictures that cannot be passed by conventional endoscopy.
Furthermore, extra-intestinal complications of CD should be kept in mind, including abscesses, or formation of fistulae between bowel segments and other organs (commonly the anterior abdominal wall, vagina or renal tract), and also the formation of gallstones and urinary calculi resulting from metabolic changes.
5.5 CT Colonography
Computed tomography colonoscopy (CTC) is defined as using helical-CT scanning and computers to produce high-resolution 2-dimensional (2D) and 3-dimensional (3D) imaging [18].
Since Vining et al. launched the first report of CT colonography (CTC) in 1994 [19], CTC has been recognized as a reliable and accurate imaging test for the detection of colorectal cancer as effective as conventional colonoscopy. Although it is well recognized that large polyps (≥10 mm) are accurately identified by CTC, the accuracy of CTC in the identification and characterization of smaller, flat, or depressed lesions is still controversial. Furthermore, histological examination is not available using CTC. Therefore, current CTC indications include the evaluation of patients who had undergone a previous incomplete colonoscopy or those who are unfit for colonoscopy, including elderly and frail individuals, patients with severe underlying clinical conditions, or with contraindication to sedation [20].
Hitherto, there have been very few reports on the ability of CT colonography to diagnose inflammatory bowel diseases [21–23]. Therefore, CTC is not approved as an alternative to standard colonoscopy in patients with UC in the ECCO (European Crohn’s and Colitis Organization) statement published in 2012 [24], although CTE together with MRE has been recognized to be an standard imaging technique with the highest diagnostic accuracy for the detection of intestinal involvement and extra-intestinal lesions in CD [9]. In fact, because colonoscopy can provide direct visualization of the colonic mucosa and the ability to collect a biopsy specimen for the histological diagnosis of IBD, colonoscopy is still the first-line procedure in the initial evaluation of patients with unexplained diarrhea and suspected IBD, especially UC [20]. However, CTC can be useful in patients with IBD, who have had incomplete or inconclusive colonoscopy, or who are unsuitable for colonoscopic examination, as mentioned above. The point to which we must pay attention is that CTC should be avoided in IBD patients presenting acute sever symptoms because of the risk of complications [25]. In these conditions, contrast-enhanced MDCT without CO2 gas insufflation is necessary and sufficient.
5.6 Technique
In patients with IBD, the technique of CTC is the same as in patients with suspected colon cancers.
Briefly, in our institution, patients have a low residue diet on the day before the examination, and take 0.75% sodium picosulfate (Laxisoberon®, Teijin Pharma Ltd., Tokyo, Japan) in the evening. On the morning of the examination, patients ingest a bowel lavage such as polyethylene glycol solution or isotonic magnesium citrate solution as bowel preps prior to CT scan. In CTC aimed to detect polyps, fecal tagging and electronic cleansing are usually performed to reduce the dose of bowel lavage by ingesting oral positive contrast such as a 40% w/v barium suspension with meals or alone. However, fecal tagging is normally omitted for CTC in patients with IBD, because contrast-enhanced MDCT is usually performed to evaluate the condition of the bowel-wall enhancement for assessing the disease activity of IBD, and tagged residues in the colon may make the enhanced bowel wall vague and unclear.
The colon is distended with carbon dioxide via a rectal tube. Carbon dioxide is given at low-pressure less than 25 mmHg by an automated low-pressure delivery system. The total volume of carbon dioxide gas is 1.5–2.5 l for adequate distension. As mentioned above, in IBD patients with acute symptoms, contrast-enhanced MDCT without CO2 gas insufflation is sufficient to obtain the necessary information.
Patients should be scanned in both the prone and supine position; that is not only to keep the visualization of the colonic lumen from the residual material, but also due to the difference of colonic distension per segment by the position of scanning [26].
Intravenous contrast medium is usually used for the assessment of the colonic wall enhancement. The acquisition at supine single phase is performed at 50–60 s after intravenous contrast administration. In cases of evaluating the extra-colonic organs, the scan is also performed in the portal phase.
5.7 Findings of IBD
Colonoscopy has become the major modality for assessing the colonic disease activity in patients with IBD, because it is the only modality to be able to evaluate “mucosal healing”, which recently became the therapeutic goal in both UC and CD. Colonoscopy can provide only the detailed pathology of the colonic mucosa. CTC is able to provide the information of colonic pathology by identifying endoluminal, intramural and extra-colonic findings [27] with its four different views; the virtual endoscopy view, the air image view, the multi-planar reconstruction (MPR) view, and the virtual dissection view (Fig. 5.3). In those images, the virtual dissection view, which is the 3D model of the colon stretched out and sliced open being displayed like the “gross pathology”, and the virtual endoscopy are usually used for screening mucosal lesions such as polyps. When CTC is being applied for the evaluation of IBD, the colonic pathology may be assessed not only endoluminally but also extraluminally by both the MPR and the air image. On the MPR view of CTC, the active UC lesions shows bowel-wall thickening, mural hyper-enhancement, “target” appearance with mural stratification, engorged vasa recta, and increased density in the perienteric mesenteric fat like the appearance of IBD in CT enterography, as well as chronic changes including fibrotic strictures and submucosal fatty deposition in the bowel wall. Further, in the patients with UC, the air image view of CTC can show granular appearance of the colon mucosa, deep ulcerations, pseudopolyps, and loss of haustral folds [28] (Fig. 5.4). These appearances in UC may begin from the rectum and progress proximally in a continuous and circumferential fashion; however, the lesions of CD are distributed discontinuously or in a “patchy” fashion.