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Role of CT colonography in inflammatory bowel disease
European Journal of Radiology 69 (2009) 404–408
Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Review
Role of CT colonography in inflammatory bowel disease Daniele Regge a,∗ , Emanuele Neri b , Francesca Turini b , Gabriele Chiara a a b
Institute for Cancer Research and Treatment, Candiolo, Turin, Italy Diagnostic and Interventional Radiology, University of Pisa, Italy
a r t i c l e
i n f o
Article history: Received 14 November 2008 Accepted 14 November 2008 Keywords: CT colonography Inflammatory bowel disease Colon cancer
a b s t r a c t CT colonography (CTC), or virtual colonoscopy, is a non-invasive imaging method that uses CT data sets combined with specialized imaging software to examine the colon. CTC is not used routinely in patients with inflammatory bowel disease (IBD). However, investigating contemporarily the colon, other abdominal organs and the peritoneum with CTC is at times useful in patients with IBD, especially when other diagnostic tools fail. Furthermore, since symptoms of colorectal cancer sometimes superimpose to those of inflammatory disease, it may happen to image patients with IBD incidentally. If clinical signs are suggestive for inflammatory disease, exam technique should be modified accordingly and distinguishing radiological findings searched for. © 2009 Elsevier Ireland Ltd. All rights reserved.
Contents 1. 2. 3. 4. 5. 6. 7. 8. 9.
Exam technique . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Post-processing and exam evaluation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Radiological findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ulcerative colitis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Crohn’s disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Carcinoma complicating IBD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Complications of inflammatory bowel disease. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Performance of CTC in IBD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Indications to CTC in IBD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Exam technique CTC requires a clean and distended colon. If exam quality is poor lesions protruding within the bowel lumen might be difficult to detect and collapsed segments may mimic wall thickening. Even though to date there is no consensus on which is the best regimen for bowel preparation, most authors now prefer faecal tagging [1–5]. Marking fluid and faeces with oral-based barium and/or iodine regimens improves lesion detection, allows differentiation between lesions and faecal residues and reduces or abolishes the need for catharsis, thus increasing exam acceptability [4–6]. Barium-based products are effective in tagging faeces; however, barium is insoluble in water and therefore marked faeces do not merge with fluid and lie at the bottom of pools [5]. Inhomogeneous tagging may limit bowel wall visualisation and reduce the
∗ Corresponding author. Tel.: +39 0119933367; fax: +39 0119933527. E-mail address: [email protected] (D. Regge). 0720-048X/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2008.11.027
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efficacy of electronic cleansing software. Iodine-based products produce homogeneous tagging of both fluid and solid residues and, by recalling fluid in the colon, create a regular air–liquid interface that improves exam quality [5]. However, severe adverse reactions have been reported following oral administration of iodine compounds in approximately 1 in 2.5 million cases [7]. While these are exceptional events, some authors suggest that it is safer to administer the iodine bolus in hospital, starting 2–3 h before examination [8]. Same-day tagging regimens are advantageous when the small bowel needs to be evaluated in addition to the colon, as in Crohn’s disease, since in most cases fluid in the small bowel loops is also adequately tagged (Figs. 1 and 2). Bowel distension is obtained by introducing air, CO2 or water through a small rubber rectal tube. Air insufflation is performed manually using a balloon pump while pneumocolon with CO2 is usually obtained using an automatic insufflating device. CO2 is well tolerated by patients, as it is rapidly absorbed by the intestinal mucosa [9], and exam quality is comparable or better than that of the air enema [10]. In 40% the ileo-cecal valve is incompetent and this allows retrograde dis-
D. Regge et al. / European Journal of Radiology 69 (2009) 404–408
Fig. 1. CT colonography performed with same-day fluid tagging, using gastrografin as oral tagging agent. The water-iodinated solution was administered 3 h before the exam in a patient with positive fecal occult blood test. At CTC (a) the iodine contrast was homogeneously distributed in both the right (A, ascending) and left (D, descending) colon. The careful analysis of the extracolonic compartment revealed a diffuse thickening of the terminal ileum (arrows) and other jejunal loops (arrow head); the iodinated contrast, still present in the lumen of the bowel loops, was helpful to identify the wall thickening. An X-ray study of the entire small bowel was performed (b) and showed multiple stenotic bowel loops. With the integration of the clinical signs and laboratory findings a definite diagnosis of Crhon’s disease was made.
tension of the ileum; while this may be confusing when only the large bowel needs to be evaluated (i.e. when cancer is searched for), it is of advantage in Crohn’s disease where information on all the digestive tube needs to be collected. Other authors prefer water enema and routine intravenous contrast media administration to evaluate enhancement of the bowel wall when inflammatory bowel disease is suspected or known at the time of examination [11,12]. Enema is performed by rectal administration of 500–1000 mL of lukewarm water and is probably safer. Because gaseous or fluid contrast is introduced through a rectal catheter, CTC is contraindicated in patients with clinical signs of severe inflammation or of perforation. Bowel perforation is a rare event following CTC [13]. However, of the 24 cases reported to date, a significant number (i.e. four cases; 16,7%) occurred in patients with active IBD, of whom two with ulcerative colitis [14,15] and two with Crohn’s disease [16,17]. Spasmolytic agents are not recommended routinely for CTC but their administration may be considered when patients complain pain during rectal administration of room air or CO2 and when there is insufficient colon distension, as may occur with diverticulitis or IBD. CT scanning is performed during breath hold in the
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Fig. 2. CTC colonography performed, in a patient with ulcerative colitis, to exclude the presence of colorectal cancer. The water-iodinated solution was administered 3 h before the exam. Axial CTC (a) showed a diffuse thickening of the entire colonic wall. The coronal multiplanar reconstruction (b) revealed the loss of the colonic folds (arrows) in the transverse and sigmoid colon.
prone and supine position. Dual acquisition significantly improves CTC accuracy for both large and small lesions [18,19]. Multislice CT scanners should be mandatory, because they allow larger volume coverage and a thinner collimation thus reducing motion artefacts and increasing resolution on the z-axis. The scanning protocol must be targeted to the clinical issue. If IBD is known at the time of scanning or detected during the first acquisition, CTC must be performed as a regular abdominal scan, with intravenous contrast media administration and adequate tube current values. Thin slices thickness, preferably less than 1.0 mm, and a reconstruction interval allowing for at least a 20% slice overlap should be implemented in order to obtain high quality multiplanar and 3D reconstructions; too much overlap is detrimental as it does not improve exam quality but increases unnecessarily the number of scan slices. 2. Post-processing and exam evaluation Different multipurpose and specialized software are available for colon evaluation from CT or MR data sets. A simple way to examine the colon is by panning through 2D images. The 2D interpretation technique, advocated by many CTC experts, should be performed on a workstation that allows comparison of supine and prone axial datasets and multiplanar reconstructions, also along curved planes. Curvilinear reformation is useful when fistulae or abdominal fluid collections follow complicated paths. The 2D reading technique does not require dedicated software and is therefore available on every workstation. Some workstations allow 3D visu-
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D. Regge et al. / European Journal of Radiology 69 (2009) 404–408
alisation of regions of interest identified on the 2D multiplanar images. Observing objects on 3D may aid in differential diagnosis for example between a thickened fold and a protruding lesion, such as an inflammatory polyp. A second group of software programs extract images of the air-filled colon, generate an automated centerline for luminal navigation, and electronically remove from images the opaque residual fluid in a routine post-processing step commonly defined as electronic cleansing [20,21]. The diagnostic interface allows for a virtual “fly-through” tour of the 3D image and rapid correlation with the two-dimensional images for any suspected abnormality. When using a primary 3D interpretation technique with CTC, complete 3D navigation from rectum to cecum and from cecum to rectum is important to maximize polyp detection. This method may be more accurate than 2D interpretation, especially to visualize smaller lesions, but is more time consuming [22,23] and is probably overrated to evaluate IBD were focus is more on the bowel wall and on extracolonic findings. Although debate continues regarding which rendering technique should be used for primary evaluation, it is now clear that the 2D and 3D techniques are complementary, each increasing the value of CT for colonic lumen and wall evaluation. 3. Radiological findings When evaluating patients with IBD at CTC, it is important to search for specific features and associated complications such as bowel wall thickness and contrast enhancement; mesenteric, perirectal, retroperitoneal, and omental fat attenuation; lymph node number and size; extraluminal contrast collections, abscesses, fistulas, and sinus tracts; mesenteric or perivisceral masses and the size of the presacral space [24]. 4. Ulcerative colitis This disease is pathologically characterized by extensive ulceration and diffuse inflammation of the mucosa. It usually begins in the rectum and extends proximally to involve part or the entire colon [24]. In the natural course of ulcerative colitis it is possible to distinguish an acute and a subacute/chronic phase which present with different radiological findings. The early stages of ulcerative colitis are manifested colonoscopically by a granular mucosal pattern attributable to edema, hyperemia, and abnormal mucin production, but these changes are usually beneath the spatial resolution of CT and that explains why in the early disease course, CT scans often are normal [25]. In this stage CTC does not play a role in the evaluation of the disease. With progressive disease, severe mucosal ulceration can denude certain portions of the colonic wall, leading to inflammatory pseudopolyps that can be visualized on CT scans [24]. A diffuse and symmetric wall thickening may be a common feature of subacute and chronic ulcerative colitis, probably due to a markedly hypertrophy of the muscularis mucosae. Forceful contraction of this hypertrophied longitudinal muscle may pull the mucosa away from the submucosa, producing diffuse or segmental narrowing of the lumen [26,27]. The submucosa becomes thickened because of the deposition of fat or, in acute and subacute cases, edema (Fig. 2). On axial CT scans, these mural changes produce the halo sign, a low-attenuation ring in the bowel wall due to deposition of submucosal fat [28]. This sign is not specific and also can be seen in Crohn’s disease, infectious enterocolitis, pseudomembranous colitis, ischemic and radiation enterocolitis, mesenteric venous thrombosis, bowel edema, and graft-versus-host disease [24,28]. Hallmarks of chronic ulcerative colitis are rectal narrowing and widening of the presacral space. On CT axial scans the rectum is seen as a target, and the proliferation of perirectal fat can be characterized by an increased number of nodular and streaky soft-tissue
densities with an abnormal attenuation value (10–20 UH higher than that of normal extraperitoneal or mesenteric fat) due to the influx of inflammatory cells and edema [24]. 5. Crohn’s disease Crohn’s disease can affect any portion of the gastrointestinal tract, most commonly the terminal ileum and proximal colon. The acute, active phase of Crohn’s disease is characterized by focal inflammation, aphthoid ulceration with adjacent cobblestoning, a chronic inflammatory reaction with lymphoid aggregates and granulomas that may be transmural, fissures, and fistulas. The chronic, resolving phase of this disorder is associated with fibrosis and stricture formation [24,29,30]. The earliest macroscopic manifestations of Crohn’s disease are enlarged lymphoid follicles and aphthoid ulcerations, but these changes are beneath the spatial resolution of CT. Consequently, when the disease is limited to the mucosa, CT scans usually are normal [24]. Although inflammatory and postinflammatory pseudopolyps may be identified on CT scans, the most frequent finding in Crohn’s disease is wall thickening (Fig. 1). The mean wall thickness in Crohn disease (11–13 mm) is usually greater than in ulcerative colitis (7.8 mm) [28,31]. Wall thickening in ulcerative colitis may be diffuse and symmetric, whereas wall thickening in Crohn’s disease may be eccentric and segmental with skip regions. The asymmetry of the disease involvement, which typically occurs along the mesenteric border of the intestine, can result in the formation of pseudodiverticula along the antimesenteric border. Pseudodiverticula are small outpouchings of the colonic wall that occur opposite regions of fibrosis and scarring [28]. During the acute-no cicatrizing phase of Crohn’s disease, the small bowel and colon show mural stratification and often the halo sign is seen [24,30]. Inflamed mucosa and serosa may show significant contrast enhancement after bolus IV administration of contrast material, and the intensity of enhancement should correlate with the clinical activity of the disease [24]. In patients with long-standing Crohn’s disease and transmural fibrosis, mural stratification is lost, so that the affected bowel wall typically tends to enhance homogeneously, although edema within the wall may result in low attenuation [28,31]. CT can readily differentiate the extraluminal manifestations of Crohn’s disease such as the fibrofatty proliferation of the mesentery which is the most common cause of separation of bowel loops [25,32]. On CT scans, the sharp interface between bowel and mesentery is lost and the attenuation value of fat is elevated by 20–60 UH because of the influx of inflammatory cells and fluid [24]. Mesenteric adenopathy, with lymph node size ranging from 3 to 8 mm, also may be present. When the lymph nodes are larger than 1 cm, the presence of lymphoma or carcinoma, both of which occur with greater frequency in Crohn’s disease, must be excluded [24,33]. Contrast-enhanced CT scans often show hypervascularity of the involved mesentery, manifesting as vascular dilatation, tortuosity, prominence, and wide spacing of the vasa recta. These distinctive vascular changes have been called vascular jejunizalion of the ileum or the comb sign [34]. 6. Carcinoma complicating IBD Patients with ulcerative colitis have a markedly increased risk of developing cancer of the colon and rectum [35]. Therefore, CT scans in patients with long-standing ulcerative colitis should be scrutinized for asymmetric mural thickening, focal loss of mural stratification, and mural thickening of greater than 1.5 cm, all features suggesting malignancy [24]. Patients with chronic Crohn’s disease show an increased incidence of adenocarcinoma and lymphoma of the small bowel and colon, particularly in the bypassed or
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excluded segments of the gut [33]. Because these bowel loops cannot be studied by conventional barium or endoscopic techniques, CT is helpful in detecting a tumor mass and providing accurate tumor staging [24].
7. Complications of inflammatory bowel disease Abscesses are detected almost exclusively in Crohn disease and not in ulcerative colitis [28,34]. An abscess can be confined to the bowel wall and pericolic fat or involve adjacent structures such as the bladder, psoas muscle, and pelvic sidewall. Abscesses are most frequently associated with small-bowel disease or ileocolitis. On CT scans, abscesses usually appear as circumscribed round or oval water-density masses with an attenuation of 10–30 UH [24]. If the abscess has a well-formed capsule, it may show peripheral contrast enhancement, whereas the liquefied central area of the abscess, which may contain necrotic material, does not [24]. Fistulas and sinus tracts are hallmarks of Crohn’s disease, affecting approximately 20–40% of patients [24,25]. Enteroentric, enetrocolic, colocolic, enterovescical, enterocutaneous, perianal, and rectovaginal fistulas have all been detected with CT. If an enterovesical fistula is suspected, it is often helpful to perform CT with oral or rectal contrast material but no intravenous contrast material. If positive contrast material is detected in the bladder, it must have originated from the intestine, thus confirming the presence of an enterovesical fistula. If intravenous contrast material is administered, positive contrast material can reach the bladder via the ureters or intestine [28].
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9. Indications to CTC in IBD Conventional colonoscopy is required for diagnosis and staging of IBD. However, patients the have had an incomplete or inconclusive colonoscopy, and possibly an ultrasound study showing some degree of wall thickening, will require a radiological study. In the older, frail or non-collaborating patient CTC is probably the best choice due to its high spatial and temporal resolution. CTC is the only technique that is able to indentify endoluminal, intramural and extracolonic findings and, to some degree, allow differential diagnosis between ulcerative colitis, Crohn’s disease and other kinds of inflammatory colitis. If assessment of disease activity is requested the study should be performed during intravenous contrast material injection [34]. In monitoring therapy, dynamic contrast-enhanced MRI is probably the best choice due to its high contrast resolution [41]. However, MRI requires state of the art equipment, not always available, and patients need to be collaborative. CTC is a valid alternative if the above reported conditions are not present. Patients with IBD, especially those with ulcerative colitis, are at increased risk of developing CRC cancer starting 8–10 years from diagnosis and should undergo conventional colonoscopy periodically [42]. Subjects that refuse to repeat colonoscopy or have not completed colonoscopy should undergo CTC. CTC should be contraindicated in patients with acute symptoms due to the risk of complications. In these conditions conventional CT is safer and usually give all the necessary information to the clinician. In conclusion CTC allows the identification of endoluminal, intramural and extraintestinal sign of IBD. The test may be useful in specific clinical situations but should be avoided in the severely ill patient.
References 8. Performance of CTC in IBD There are very few studies reporting the performances of CTC in IBD [36–38] and consequently indications are not yet well established. In principle, CTC has some advantages over conventional CT in that it allows visualisation of the mucosal interface. This allows depiction of protruding lesions (i.e. inflammatory polyps, adenomas and cancer) and of deep ulcers. Andersen et al. report 100% per-patient and per-polyp sensitivity in the identification of endoluminal lesions of all sizes, including 2 carcinomas, 2 large adenomas, and 9 medium and small lesions [38]. However, the number of patients included in the study was of 21 of whom only 4 (19%) were positive for endoluminal findings. Other details, such as the granular appearance of the mucosa in ulcerative colitis or the cobblestone pattern of Crohn’s disease, may be depicted if scanning is performed with sub-millimetre slices [37]. Carrascosa et al. were able to identify the granular appearance of the colonic mucosa in four patients with ulcerative colitis and deep ulcers in two patients with Crohn’s disease, using 0.8 mm slice thickness and a 50% slice overlap [36]. A second advantage of CTC over conventional CT lies in its capability of assessing the degree of narrowing when strictures are not yet clinically relevant, in that they have not yet configured an occlusive condition. Finally, CTC allows more reliable measurements of wall thickness and therefore may accurately asses intramural extent and aid differentiation between Crohn’s disease, were wall thickening is usually more pronounced, from ulcerative colitis [32,33,39]. Conversely, information on wall enhancement, assessment of extracolonic findings, such as perimesenteric fat stranding, fistulas and fluid collections, and identification of extraintestinal complications can be readily obtained with a conventional CT scan or with other axial imaging techniques, such as ultrasound or MRI [40].
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Contents lists available at ScienceDirect
European Journal of Radiology journal homepage: www.elsevier.com/locate/ejrad
Review
Role of CT colonography in inflammatory bowel disease Daniele Regge a,∗ , Emanuele Neri b , Francesca Turini b , Gabriele Chiara a a b
Institute for Cancer Research and Treatment, Candiolo, Turin, Italy Diagnostic and Interventional Radiology, University of Pisa, Italy
a r t i c l e
i n f o
Article history: Received 14 November 2008 Accepted 14 November 2008 Keywords: CT colonography Inflammatory bowel disease Colon cancer
a b s t r a c t CT colonography (CTC), or virtual colonoscopy, is a non-invasive imaging method that uses CT data sets combined with specialized imaging software to examine the colon. CTC is not used routinely in patients with inflammatory bowel disease (IBD). However, investigating contemporarily the colon, other abdominal organs and the peritoneum with CTC is at times useful in patients with IBD, especially when other diagnostic tools fail. Furthermore, since symptoms of colorectal cancer sometimes superimpose to those of inflammatory disease, it may happen to image patients with IBD incidentally. If clinical signs are suggestive for inflammatory disease, exam technique should be modified accordingly and distinguishing radiological findings searched for. © 2009 Elsevier Ireland Ltd. All rights reserved.
Contents 1. 2. 3. 4. 5. 6. 7. 8. 9.
Exam technique . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Post-processing and exam evaluation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Radiological findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ulcerative colitis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Crohn’s disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Carcinoma complicating IBD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Complications of inflammatory bowel disease. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Performance of CTC in IBD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Indications to CTC in IBD . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Exam technique CTC requires a clean and distended colon. If exam quality is poor lesions protruding within the bowel lumen might be difficult to detect and collapsed segments may mimic wall thickening. Even though to date there is no consensus on which is the best regimen for bowel preparation, most authors now prefer faecal tagging [1–5]. Marking fluid and faeces with oral-based barium and/or iodine regimens improves lesion detection, allows differentiation between lesions and faecal residues and reduces or abolishes the need for catharsis, thus increasing exam acceptability [4–6]. Barium-based products are effective in tagging faeces; however, barium is insoluble in water and therefore marked faeces do not merge with fluid and lie at the bottom of pools [5]. Inhomogeneous tagging may limit bowel wall visualisation and reduce the
∗ Corresponding author. Tel.: +39 0119933367; fax: +39 0119933527. E-mail address: [email protected] (D. Regge). 0720-048X/$ – see front matter © 2009 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ejrad.2008.11.027
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efficacy of electronic cleansing software. Iodine-based products produce homogeneous tagging of both fluid and solid residues and, by recalling fluid in the colon, create a regular air–liquid interface that improves exam quality [5]. However, severe adverse reactions have been reported following oral administration of iodine compounds in approximately 1 in 2.5 million cases [7]. While these are exceptional events, some authors suggest that it is safer to administer the iodine bolus in hospital, starting 2–3 h before examination [8]. Same-day tagging regimens are advantageous when the small bowel needs to be evaluated in addition to the colon, as in Crohn’s disease, since in most cases fluid in the small bowel loops is also adequately tagged (Figs. 1 and 2). Bowel distension is obtained by introducing air, CO2 or water through a small rubber rectal tube. Air insufflation is performed manually using a balloon pump while pneumocolon with CO2 is usually obtained using an automatic insufflating device. CO2 is well tolerated by patients, as it is rapidly absorbed by the intestinal mucosa [9], and exam quality is comparable or better than that of the air enema [10]. In 40% the ileo-cecal valve is incompetent and this allows retrograde dis-
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Fig. 1. CT colonography performed with same-day fluid tagging, using gastrografin as oral tagging agent. The water-iodinated solution was administered 3 h before the exam in a patient with positive fecal occult blood test. At CTC (a) the iodine contrast was homogeneously distributed in both the right (A, ascending) and left (D, descending) colon. The careful analysis of the extracolonic compartment revealed a diffuse thickening of the terminal ileum (arrows) and other jejunal loops (arrow head); the iodinated contrast, still present in the lumen of the bowel loops, was helpful to identify the wall thickening. An X-ray study of the entire small bowel was performed (b) and showed multiple stenotic bowel loops. With the integration of the clinical signs and laboratory findings a definite diagnosis of Crhon’s disease was made.
tension of the ileum; while this may be confusing when only the large bowel needs to be evaluated (i.e. when cancer is searched for), it is of advantage in Crohn’s disease where information on all the digestive tube needs to be collected. Other authors prefer water enema and routine intravenous contrast media administration to evaluate enhancement of the bowel wall when inflammatory bowel disease is suspected or known at the time of examination [11,12]. Enema is performed by rectal administration of 500–1000 mL of lukewarm water and is probably safer. Because gaseous or fluid contrast is introduced through a rectal catheter, CTC is contraindicated in patients with clinical signs of severe inflammation or of perforation. Bowel perforation is a rare event following CTC [13]. However, of the 24 cases reported to date, a significant number (i.e. four cases; 16,7%) occurred in patients with active IBD, of whom two with ulcerative colitis [14,15] and two with Crohn’s disease [16,17]. Spasmolytic agents are not recommended routinely for CTC but their administration may be considered when patients complain pain during rectal administration of room air or CO2 and when there is insufficient colon distension, as may occur with diverticulitis or IBD. CT scanning is performed during breath hold in the
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Fig. 2. CTC colonography performed, in a patient with ulcerative colitis, to exclude the presence of colorectal cancer. The water-iodinated solution was administered 3 h before the exam. Axial CTC (a) showed a diffuse thickening of the entire colonic wall. The coronal multiplanar reconstruction (b) revealed the loss of the colonic folds (arrows) in the transverse and sigmoid colon.
prone and supine position. Dual acquisition significantly improves CTC accuracy for both large and small lesions [18,19]. Multislice CT scanners should be mandatory, because they allow larger volume coverage and a thinner collimation thus reducing motion artefacts and increasing resolution on the z-axis. The scanning protocol must be targeted to the clinical issue. If IBD is known at the time of scanning or detected during the first acquisition, CTC must be performed as a regular abdominal scan, with intravenous contrast media administration and adequate tube current values. Thin slices thickness, preferably less than 1.0 mm, and a reconstruction interval allowing for at least a 20% slice overlap should be implemented in order to obtain high quality multiplanar and 3D reconstructions; too much overlap is detrimental as it does not improve exam quality but increases unnecessarily the number of scan slices. 2. Post-processing and exam evaluation Different multipurpose and specialized software are available for colon evaluation from CT or MR data sets. A simple way to examine the colon is by panning through 2D images. The 2D interpretation technique, advocated by many CTC experts, should be performed on a workstation that allows comparison of supine and prone axial datasets and multiplanar reconstructions, also along curved planes. Curvilinear reformation is useful when fistulae or abdominal fluid collections follow complicated paths. The 2D reading technique does not require dedicated software and is therefore available on every workstation. Some workstations allow 3D visu-
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alisation of regions of interest identified on the 2D multiplanar images. Observing objects on 3D may aid in differential diagnosis for example between a thickened fold and a protruding lesion, such as an inflammatory polyp. A second group of software programs extract images of the air-filled colon, generate an automated centerline for luminal navigation, and electronically remove from images the opaque residual fluid in a routine post-processing step commonly defined as electronic cleansing [20,21]. The diagnostic interface allows for a virtual “fly-through” tour of the 3D image and rapid correlation with the two-dimensional images for any suspected abnormality. When using a primary 3D interpretation technique with CTC, complete 3D navigation from rectum to cecum and from cecum to rectum is important to maximize polyp detection. This method may be more accurate than 2D interpretation, especially to visualize smaller lesions, but is more time consuming [22,23] and is probably overrated to evaluate IBD were focus is more on the bowel wall and on extracolonic findings. Although debate continues regarding which rendering technique should be used for primary evaluation, it is now clear that the 2D and 3D techniques are complementary, each increasing the value of CT for colonic lumen and wall evaluation. 3. Radiological findings When evaluating patients with IBD at CTC, it is important to search for specific features and associated complications such as bowel wall thickness and contrast enhancement; mesenteric, perirectal, retroperitoneal, and omental fat attenuation; lymph node number and size; extraluminal contrast collections, abscesses, fistulas, and sinus tracts; mesenteric or perivisceral masses and the size of the presacral space [24]. 4. Ulcerative colitis This disease is pathologically characterized by extensive ulceration and diffuse inflammation of the mucosa. It usually begins in the rectum and extends proximally to involve part or the entire colon [24]. In the natural course of ulcerative colitis it is possible to distinguish an acute and a subacute/chronic phase which present with different radiological findings. The early stages of ulcerative colitis are manifested colonoscopically by a granular mucosal pattern attributable to edema, hyperemia, and abnormal mucin production, but these changes are usually beneath the spatial resolution of CT and that explains why in the early disease course, CT scans often are normal [25]. In this stage CTC does not play a role in the evaluation of the disease. With progressive disease, severe mucosal ulceration can denude certain portions of the colonic wall, leading to inflammatory pseudopolyps that can be visualized on CT scans [24]. A diffuse and symmetric wall thickening may be a common feature of subacute and chronic ulcerative colitis, probably due to a markedly hypertrophy of the muscularis mucosae. Forceful contraction of this hypertrophied longitudinal muscle may pull the mucosa away from the submucosa, producing diffuse or segmental narrowing of the lumen [26,27]. The submucosa becomes thickened because of the deposition of fat or, in acute and subacute cases, edema (Fig. 2). On axial CT scans, these mural changes produce the halo sign, a low-attenuation ring in the bowel wall due to deposition of submucosal fat [28]. This sign is not specific and also can be seen in Crohn’s disease, infectious enterocolitis, pseudomembranous colitis, ischemic and radiation enterocolitis, mesenteric venous thrombosis, bowel edema, and graft-versus-host disease [24,28]. Hallmarks of chronic ulcerative colitis are rectal narrowing and widening of the presacral space. On CT axial scans the rectum is seen as a target, and the proliferation of perirectal fat can be characterized by an increased number of nodular and streaky soft-tissue
densities with an abnormal attenuation value (10–20 UH higher than that of normal extraperitoneal or mesenteric fat) due to the influx of inflammatory cells and edema [24]. 5. Crohn’s disease Crohn’s disease can affect any portion of the gastrointestinal tract, most commonly the terminal ileum and proximal colon. The acute, active phase of Crohn’s disease is characterized by focal inflammation, aphthoid ulceration with adjacent cobblestoning, a chronic inflammatory reaction with lymphoid aggregates and granulomas that may be transmural, fissures, and fistulas. The chronic, resolving phase of this disorder is associated with fibrosis and stricture formation [24,29,30]. The earliest macroscopic manifestations of Crohn’s disease are enlarged lymphoid follicles and aphthoid ulcerations, but these changes are beneath the spatial resolution of CT. Consequently, when the disease is limited to the mucosa, CT scans usually are normal [24]. Although inflammatory and postinflammatory pseudopolyps may be identified on CT scans, the most frequent finding in Crohn’s disease is wall thickening (Fig. 1). The mean wall thickness in Crohn disease (11–13 mm) is usually greater than in ulcerative colitis (7.8 mm) [28,31]. Wall thickening in ulcerative colitis may be diffuse and symmetric, whereas wall thickening in Crohn’s disease may be eccentric and segmental with skip regions. The asymmetry of the disease involvement, which typically occurs along the mesenteric border of the intestine, can result in the formation of pseudodiverticula along the antimesenteric border. Pseudodiverticula are small outpouchings of the colonic wall that occur opposite regions of fibrosis and scarring [28]. During the acute-no cicatrizing phase of Crohn’s disease, the small bowel and colon show mural stratification and often the halo sign is seen [24,30]. Inflamed mucosa and serosa may show significant contrast enhancement after bolus IV administration of contrast material, and the intensity of enhancement should correlate with the clinical activity of the disease [24]. In patients with long-standing Crohn’s disease and transmural fibrosis, mural stratification is lost, so that the affected bowel wall typically tends to enhance homogeneously, although edema within the wall may result in low attenuation [28,31]. CT can readily differentiate the extraluminal manifestations of Crohn’s disease such as the fibrofatty proliferation of the mesentery which is the most common cause of separation of bowel loops [25,32]. On CT scans, the sharp interface between bowel and mesentery is lost and the attenuation value of fat is elevated by 20–60 UH because of the influx of inflammatory cells and fluid [24]. Mesenteric adenopathy, with lymph node size ranging from 3 to 8 mm, also may be present. When the lymph nodes are larger than 1 cm, the presence of lymphoma or carcinoma, both of which occur with greater frequency in Crohn’s disease, must be excluded [24,33]. Contrast-enhanced CT scans often show hypervascularity of the involved mesentery, manifesting as vascular dilatation, tortuosity, prominence, and wide spacing of the vasa recta. These distinctive vascular changes have been called vascular jejunizalion of the ileum or the comb sign [34]. 6. Carcinoma complicating IBD Patients with ulcerative colitis have a markedly increased risk of developing cancer of the colon and rectum [35]. Therefore, CT scans in patients with long-standing ulcerative colitis should be scrutinized for asymmetric mural thickening, focal loss of mural stratification, and mural thickening of greater than 1.5 cm, all features suggesting malignancy [24]. Patients with chronic Crohn’s disease show an increased incidence of adenocarcinoma and lymphoma of the small bowel and colon, particularly in the bypassed or
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excluded segments of the gut [33]. Because these bowel loops cannot be studied by conventional barium or endoscopic techniques, CT is helpful in detecting a tumor mass and providing accurate tumor staging [24].
7. Complications of inflammatory bowel disease Abscesses are detected almost exclusively in Crohn disease and not in ulcerative colitis [28,34]. An abscess can be confined to the bowel wall and pericolic fat or involve adjacent structures such as the bladder, psoas muscle, and pelvic sidewall. Abscesses are most frequently associated with small-bowel disease or ileocolitis. On CT scans, abscesses usually appear as circumscribed round or oval water-density masses with an attenuation of 10–30 UH [24]. If the abscess has a well-formed capsule, it may show peripheral contrast enhancement, whereas the liquefied central area of the abscess, which may contain necrotic material, does not [24]. Fistulas and sinus tracts are hallmarks of Crohn’s disease, affecting approximately 20–40% of patients [24,25]. Enteroentric, enetrocolic, colocolic, enterovescical, enterocutaneous, perianal, and rectovaginal fistulas have all been detected with CT. If an enterovesical fistula is suspected, it is often helpful to perform CT with oral or rectal contrast material but no intravenous contrast material. If positive contrast material is detected in the bladder, it must have originated from the intestine, thus confirming the presence of an enterovesical fistula. If intravenous contrast material is administered, positive contrast material can reach the bladder via the ureters or intestine [28].
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9. Indications to CTC in IBD Conventional colonoscopy is required for diagnosis and staging of IBD. However, patients the have had an incomplete or inconclusive colonoscopy, and possibly an ultrasound study showing some degree of wall thickening, will require a radiological study. In the older, frail or non-collaborating patient CTC is probably the best choice due to its high spatial and temporal resolution. CTC is the only technique that is able to indentify endoluminal, intramural and extracolonic findings and, to some degree, allow differential diagnosis between ulcerative colitis, Crohn’s disease and other kinds of inflammatory colitis. If assessment of disease activity is requested the study should be performed during intravenous contrast material injection [34]. In monitoring therapy, dynamic contrast-enhanced MRI is probably the best choice due to its high contrast resolution [41]. However, MRI requires state of the art equipment, not always available, and patients need to be collaborative. CTC is a valid alternative if the above reported conditions are not present. Patients with IBD, especially those with ulcerative colitis, are at increased risk of developing CRC cancer starting 8–10 years from diagnosis and should undergo conventional colonoscopy periodically [42]. Subjects that refuse to repeat colonoscopy or have not completed colonoscopy should undergo CTC. CTC should be contraindicated in patients with acute symptoms due to the risk of complications. In these conditions conventional CT is safer and usually give all the necessary information to the clinician. In conclusion CTC allows the identification of endoluminal, intramural and extraintestinal sign of IBD. The test may be useful in specific clinical situations but should be avoided in the severely ill patient.
References 8. Performance of CTC in IBD There are very few studies reporting the performances of CTC in IBD [36–38] and consequently indications are not yet well established. In principle, CTC has some advantages over conventional CT in that it allows visualisation of the mucosal interface. This allows depiction of protruding lesions (i.e. inflammatory polyps, adenomas and cancer) and of deep ulcers. Andersen et al. report 100% per-patient and per-polyp sensitivity in the identification of endoluminal lesions of all sizes, including 2 carcinomas, 2 large adenomas, and 9 medium and small lesions [38]. However, the number of patients included in the study was of 21 of whom only 4 (19%) were positive for endoluminal findings. Other details, such as the granular appearance of the mucosa in ulcerative colitis or the cobblestone pattern of Crohn’s disease, may be depicted if scanning is performed with sub-millimetre slices [37]. Carrascosa et al. were able to identify the granular appearance of the colonic mucosa in four patients with ulcerative colitis and deep ulcers in two patients with Crohn’s disease, using 0.8 mm slice thickness and a 50% slice overlap [36]. A second advantage of CTC over conventional CT lies in its capability of assessing the degree of narrowing when strictures are not yet clinically relevant, in that they have not yet configured an occlusive condition. Finally, CTC allows more reliable measurements of wall thickness and therefore may accurately asses intramural extent and aid differentiation between Crohn’s disease, were wall thickening is usually more pronounced, from ulcerative colitis [32,33,39]. Conversely, information on wall enhancement, assessment of extracolonic findings, such as perimesenteric fat stranding, fistulas and fluid collections, and identification of extraintestinal complications can be readily obtained with a conventional CT scan or with other axial imaging techniques, such as ultrasound or MRI [40].
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