CT Enterography: Principles, Trends, and Interpretation of Findings A Norouzi MD Fall 2013 Introduction With the improved resolution of multidetector computed tomography (CT), CT enterography has become an important method of choice for evaluating small bowel disorders. Although capsule endoscopy provides better mucosal visualization, it does not allow visualization of abnormalities outside the bowel lumen. Moreover, capsule endoscopy cannot be performed when the presence of a stricture is suspected; the endoscopic capsule may become lodged at the diseased segment and cause obstruction. CT enterography is noninvasive, easy to perform, and allows visualization of extraenteric structures as well as of the bowel wall. Its usefulness for detecting small bowel tumors is established; in addition, CT enterography with modified protocols has proved useful for detecting occult gastrointestinal (GI) tract bleeding in hemodynamically stable patients. In the American College of Radiology appropriateness criteria, CT enterography is rated as the most appropriate imaging modality for evaluating known Crohn disease in patients with an acute exacerbation or suspected complications. The main disadvantages of the technique are the requisite exposure of patients to ionizing radiation, of particular concern in young patients; the frequent need for repeated imaging; and the necessity of using intravenous contrast material Although capsule endoscopy is reported to have high sensitivity for evaluation of the small bowel mucosa, CT enterography provides better visualization of the entire small bowel wall and allows detection of extraenteric disease as well. Additional disadvantages of capsule endoscopy for evaluating early-stage disease include a predictable higher rate of false-positive findings due to mucosal breaks and small bowel erosions, which may occur even in healthy patients, as well as the risk of possible impaction of the capsule proximal to a diseased bowel segment. MR enterography recently has been gaining in popularity, especially for follow-up imaging of pediatric and young patients with established inflammatory conditions of the small bowel . The lack of ionizing radiation is an advantage of MR enterography over CT enterography, especially when evaluating patients with known renal dysfunction. However, MR enterography is more time consuming, more costly, and more variable in regard to image quality than CT enterography. In particular, patients who have difficulty holding their breath may be better examined with CT. The results of a prospective study by Schmidt et al show that, in addition to the superior spatial resolution that CT offers, interobserver agreement is better and sensitivity for the detection of active disease is higher with CT. The radiation dose resulting from a CT enterographic examination should be similar to that from a routine abdominopelvic venous phase scan. The radiation dose can be reduced by using the dose modulation option available on most new scanners. In addition, the use of advanced reconstruction techniques, such as iterative reconstruction, enables further dose reduction. In our experience, simply reducing the voltage to 80 or 100 kV allows a significant dose reduction in patients with an average or below average body mass index. In our practice, we regularly perform CT enterography with a mean estimated dose of 4–8 mSv. CT Enterographic Technique Patients undergoing CT enterography are asked to withhold all oral intake, starting 4 hours before the examination. To improve visualization of the mucosa and achieve better bowel distention, a negative oral contrast agent is administered. Our current regimen with regard to the timing of administration of oral contrast agents involves the ingestion of a total of 1.35 L over 1 hour: 450 mL at 60 minutes, 450 mL at 40 minutes, 225 mL at 20 minutes, and 225 mL at 10 minutes before scanning. After the oral contrast agent is ingested, a bolus of intravenous contrast material (125 ml ) followed by 50 mL of saline solution is administered with a power injector at a rate of 4 mL/sec. Helical scanning is performed from the diaphragm to the symphysis pubis, beginning 65 seconds after the administration of intravenous contrast material, and includes a single (venous) phase for the evaluation of known or suspected Crohn disease or dual (arterial and venous) phases for the evaluation of mesenteric vessels, GI tract bleeding, and suspected tumors. Scanning parameters include a section thickness of 0.625 mm and interval of 0.625 mm. At present, CT enterography is most commonly used for diagnosing and assessing inflammatory bowel disease, localizing sites of GI tract bleeding, detecting small bowel neoplasms. Crohn Disease Crohn disease predominantly involves the small bowel, particularly the terminal ileum, but is also commonly associated with extraintestinal manifestations. Small bowel involvement in Crohn disease is typically transmural, with characteristic skip lesions . The main diagnostic purpose of CT enterography in the setting of Crohn disease is to differentiate active inflammatory strictures from fibrotic strictures in order to guide therapy. Active bowel disease is more likely to be treated medically, whereas surgery and strictureplasty may be considered in the setting of fibrotic strictures. Skip lesions in Crohn disease. Axial CT enterographic section depicts two inflammatory small bowel strictures (arrows) separated by a segment of normal distended small bowel (arrowheads), characteristic findings of Crohn disease. CT features of active Crohn disease include mucosal hyperenhancement, wall thickening (thickness > 3 mm), mural stratification with a prominent vasa recta (comb sign), mesenteric fat stranding, all of which are exquisitely demonstrated at CT enterography The capability of CT enterography for depicting extraenteric disease allows the simultaneous diagnosis of complications associated with Crohn disease, such as obstruction, sinus tract, fistula, and abscess formation. Axial CT enterographic section shows mucosal hyperenhancement (black arrow) and mural stratification (white arrow) of the terminal ileum, an appearance that contrasts markedly with that of nondiseased ileal segments Axial CT enterographic section from another patient shows mesenteric hypervascularity (arrowheads) adjacent to the involved bowel segment. Coronal volume-rendered CT enterographic sections from two patients (a and b) demonstrate prominence of the vasa recta, or “comb sign” (arrows). The term mural stratification denotes the visualization of bowel wall layers at CT. At CT enterography, the edematous bowel wall has a trilaminar appearance, with enhanced outer serosal and inner mucosal layers and an interposed submucosal layer of lower attenuation . However, this feature is not specific to Crohn disease; it is seen also in other inflammatory bowel diseases and even in some cases of bowel ischemia. In active Crohn disease, increased attenuation of the mesenteric fat is often seen. This appearance is due to the transmural extension of inflammation across the serosa and to engorgement of the hyperemic vasa recta surrounding the inflamed bowel segment. Prominence of the vasa recta adjacent to the inflamed loop of bowel is termed the “comb sign” . This sign, along with increased mesenteric fat attenuation, is the most specific CT feature of active Crohn disease. Findings that might be seen in inactive longstanding Crohn disease include submucosal fat deposition, pseudosacculation, surrounding fibrofatty proliferation, and fibrotic strictures. Involvement of the mesenteric border of the affected bowel segment in the inflammatory process, with associated asymmetric fibrosis and pseudosacculation of the antimesenteric border, is a hallmark . CT enterography has high sensitivity for the detection of bowel strictures occurring as a complication of Crohn disease. Reversible strictures produced by active disease demonstrate mucosal hyperenhancement, mural stratification, fat stranding, and engorgement of the vasa recta; however, a lack of enhancement and loss of stratification might be seen in the presence of transmural fibrosis . It is important to differentiate between reversible and irreversible strictures because the former warrant medical management, whereas the latter may require surgical intervention. Inflammatory bowel stricture in a patient with active Crohn disease. (a) Axial CT enterographic section shows involvement of a long segment of the terminal ileum in an inflammatory stricture represented by mucosal hyperenhancement (arrowhead) and bowel wall thickening with mural stratification (arrow). (b) Coronal volume-rendered CT enterographic section shows luminal narrowing (arrow) and proximal dilatation (*) of the small bowel, findings indicative of obstruction. Submucosal fat deposition in longstanding Crohn disease. Axial CT enterographic section shows abnormally low attenuation of the bowel wall (arrowheads), a finding consistent with submucosal fat deposition. Large bowel involvement in Crohn disease. Axial CT enterographic sections obtained in different patients show luminal narrowing and dilatation in a segment of the ascending colon (arrow in a), a perianal abscess (arrow in b) rectosigmoid involvement (black arrowhead in c), and a comb sign (white arrowheads in c). Small bowel capsule endoscopy is usually contraindicated when inflamed or fibrotic strictures cause narrowing of the intraluminal diameter to less than 1 cm, a condition in which there is an increased risk of capsule retention leading to bowel obstruction. The rate of capsule retention in patients with both Crohn disease and small bowel stricture is relatively high (13%) . To avoid this complication, patency capsule endoscopy or CT enterography may be performed to evaluate the patency of the small bowel before capsule endoscopy is undertaken. CT enterography is useful also for detecting reactive lymphadenopathy in the mesentery adjacent to stenosed bowel segments; this finding is an important indicator of active disease. Capsule impaction in bowel stricture due to Crohn disease. Anteroposterior radiograph (a) and axial CT enterographic section (b) demonstrate the impaction of an endoscopic capsule (black arrow) within the lumen of a thick-walled diseased ileal segment (white arrow in b). The excellent spatial resolution and multiplanar imaging capability of CT enterography make it the modality of choice for evaluating complications such as enteroenteric fistula, enterovesical fistula, and interloop abscess. CT enterography resulted in accurate detection of fistulas in 94% of cases . A review of multiplanar reformatted images improves visualization of fistulas and aids in preoperative planning. Fistulas usually appear as enhancing linear extraluminal tracts connecting bowel loops and may or may not contain fluid . Fistula formation in Crohn disease. Coronal volume-rendered CT enterographic sections obtained in two patients depict ileo-ileal fistulas (arrowheads in a) and an ileocolonic fistula (arrow in b). Abscesses often are seen in the setting of Crohn disease. They appear as extraluminal fluid collections without communication with the bowel lumen. Because the contents of an abscess may have an appearance and attenuation similar to those of intraluminal contrast material, it is crucial that a lack of communication between the collection and the bowel lumen be established before an abscess is diagnosed. A multiplanar review of images in oblique coronal and sagittal planes is useful in difficult cases, especially in patients with a paucity of abdominal fat. Abscess formation in Crohn disease. Axial (a) and coronal volume-rendered (b) CT enterographic sections show a large fluid collection (arrows) with attenuation similar to that of enteric contrast material. Lack of communication between the collection and the bowel, as well as the marked difference in caliber between the two, helps confirm an extraluminal location of the collection. Note the evidence of active Crohn disease (* in a) in the terminal ileum. Ulcerative Colitis Ulcerative colitis is characterized by a continuous pattern of bowel wall involvement, starting from the rectum, without evidence of skip lesions. Ulcerative colitis predominantly involves the large bowel but may extend to the terminal ileum, a condition referred to as “backwash ileitis” . Extraintestinal manifestations may occur but are uncommon. Ulcerative colitis with backwash ileitis. Axial CT enterographic sections show continuous involvement of the large bowel (white arrrows) and backwash ileitis (black arrow in b) Because the CT appearance of the bowel often is normal early in the course of the disease, CT is not performed for initial diagnostic evaluations . Colonoscopy remains the primary diagnostic method for routine evaluations of the colon . However, when specific features are present, CT enterography can be helpful for achieving an accurate diagnosis and excluding small bowel involvement. For example, severe progressive ulcerative colitis may result in pseudopolyp formations that may be seen at CT. In addition, features such as mural thinning, pneumatosis, and perforation may be detected in cases of toxic megacolon. In cases of longstanding disease, features such as rectal narrowing and presacral fat accumulation can be seen at CT. CT also aids in the diagnosis of complications such as rectal carcinoma. Long-term complications of ulcerative colitis. Axial (a) and coronal reformatted (b) CT enterographic sections depict an enhancing, cauliflower-shaped, polypoid soft tissue mass (arrows) that protrudes into the rectal lumen, a finding consistent with adenocarcinoma, which was surgically proved. GI Tract Bleeding Bleeding in the GI tract has many possible causes, including ulcers, vascular malformations, and tumors. Patients in whom the presence of GI tract bleeding is suspected usually undergo upper and lower GI tract endoscopy for initial evaluation. If the result of endoscopy is negative or inconclusive, multiphase CT may be helpful. Triple phase (arterial, enteric, and delayed phase) CT enterography, in particular, was recently reported to be of value for detecting GI tract bleeding and identifying the source. Active small bowel bleeding at multiphase CT enterography is observed as a gradual accumulation of contrast material within the bowel lumen. Angiodysplasia is the most common cause of occult GI tract bleeding. The structural abnormality usually appears as an avidly enhancing plaque or nodule during the enteric phase and fades during the delayed phase. Less commonly, it might manifest as a focal area of enhancement or an associated early draining vein during the arterial phase. Other causes of GI tract bleeding that may be detected at CT enterography include various types of vascular malformations, neoplasms, and Meckel diverticulum . Small bowel tumors such as leiomyoma and gastrointestinal stromal tumor (GIST) also may be sources of occult GI tract bleeding. Angiodysplasia. Axial (a) and coronal reformatted (b) CT enterographic sections demonstrate a tuftlike area of enhancement in the medial cecal wall (arrow), a finding suggestive of angiodysplasia. Meckel diverticulum. (a) Coronal reformatted CT enterographic section depicts a flaskshaped ileal outpouching with a discernible fundus (arrow) and neck (arrowhead), findings suggestive of a Meckel diverticulum. (b) Axial CT enterographic section from a patient with lower GI tract bleeding shows an enhancing pouchlike formation in the bowel wall (arrow), a finding that represents ectopic gastric mucosa. Small Bowel Neoplasms Small bowel neoplasms are relatively rare and usually produce nonspecific clinical signs and symptoms that result in a late diagnosis. They are an important cause of obscure GI tract bleeding, and they sometimes lead to bowel obstruction. CT has demonstrated a fairly high level of accuracy in the evaluation of small bowel tumors , including GIST, adenocarcinoma, carcinoid, lymphoma, and metastases. When performed with bowel-loop distention with a lowdensity contrast material, intravenous administration of an iodinated contrast agent, and an optimized acquisition protocol, CT enterography is a reliable method for diagnosing and staging small-bowel neoplasms. Benign GISTs may arise in any part of the small bowel, whereas malignant GISTs usually are seen in the distal small bowel. Most GISTs are predominantly extraluminal , although a few have been described as endoluminal . Most have been found in the stomach, followed by the small bowel. Other, less likely locations include the colon and esophagus. It is often difficult to differentiate between benign and malignant GISTs at imaging. CT findings of lesion size larger than 5 cm, heterogeneous enhancement, gastric location, associated metastases, and a cystic-necrotic component were significantly more frequent among tumors with a high mitotic index. GIST. Axial (a) and coronal volume-rendered (b) CT enterographic sections depict a large exophytic mass with central low attenuation (arrows) arising from an ileal loop. The appearance and location of the mass are highly suggestive of GIST. In a series of 1260 small bowel cancers, carcinoid tumors were found to be the most common primary small intestinal cancers identified histologically, followed by adenocarcinomas and lymphomas . A carcinoid tumor often appears as an intensely enhancing mucosal polyp or an enhancing carpet lesion with apparent wall thickening. The ileum is reported to be the most frequent location of carcinoid involvement of the small bowel. Mesenteric carcinoid tumors often lead to a desmoplastic reaction that produces a spiculated masslike appearance. Carcinoid tumors. (a) Axial CT enterographic section obtained in a 51-year-old man shows a small, enhancing lesion in the terminal ileum (arrow), an incidental finding that was proved at pathologic analysis to be a carcinoid. (b) Axial CT enterographic section obtained in another patient demonstrates a mesenteric mass with a spiculated margin (arrows), a finding representative of a mesenteric carcinoid. Adenocarcinoma may manifest as annular narrowing, a discrete tumor mass, or an ulcerative plaque and is most frequently observed in the duodenum. It may lead to progressive small bowel obstruction, intussusception, or, rarely, perforation. Lymphoma is more likely to occur in the ileum than in other small bowel segments. It might manifest as a nodular filling defect, discrete polyp, infiltrating lesion, or exoenteric mass, and it is usually associated with significant lymphadenopathy . With good bowel distention, the nodular thickening that predominantly involves the terminal ileum in cases of small bowel lymphoma is well demonstrated at CT enterography . Lymphomatous involvement of the terminal ileum may lead to the development of intussusception. Small bowel lymphoma. Axial (a) and coronal volume-rendered (b) CT enterographic sections demonstrate multiple focal areas (arrows) of nodular wall thickening involving distal ileal loops. These findings are compatible with lymphoma, which was subsequently proved. Intestinal involvement in metastatic cancer is common. The prevalence of different malignancies varies; however, intestinal involvement, mostly in the form of diffuse peritoneal carcinomatosis, has been reported in 5%–10% of patients with neoplasms such as breast cancer and malignant melanoma. Intestinal metastases may be secondary to intraperitoneal seeding, hematogenous spread, or direct extension from an adjacent visceral or colonic malignancy. Celiac Disease Celiac disease is a chronic inflammatory disorder of the small bowel that is induced in genetically susceptible people by the irritant gluten and, possibly, various environmental cofactors. The disorder may be asymptomatic or characterized by diverse symptoms of malabsorption with varying severity . The burden of undetected celiac disease is high. Researchers have calculated that the ratio of diagnosed cases of celiac disease to cases that are as yet undiagnosed is as high as 1:7. CT enterography can be useful in evaluating patients with celiac disease, especially when the clinical signs and symptoms are nonspecific. The CT findings in celiac disease include small bowel dilatation, small bowel intussusception, villous atrophy, and jejunization of the ileum as reflected by a decrease in jejunal folds in contrast with the increasing fold pattern seen in the ileum. An accurate diagnosis can be made with visualization of the reversed jejunoileal fold pattern and at least two other characteristic features (fold thickening, jejunal atrophy, or dilatation) Associated imaging findings include increased splanchnic circulation, transient small bowel intussusception, mesenteric and retroperitoneal lymphadenopathy, and hyposplenism. Lymphomatous infiltration in the context of celiac disease may be seen as polypoidal involvement of the small bowel wall . Celiac disease. (a, b) Axial (a) and coronal reformatted (b) CT enterographic sections show jejunization of the ileal mucosa (arrowheads). Axial CT enterographic section from another patient depicts multiple polypoid lesions (arrowheads) in the small bowel and jejunization of the ileal mucosal pattern, features consistent with subsequent histologic findings of T-cell lymphoma occurring as a complication of celiac disease. Mesenteric Ischemia CT enterography is frequently used for the evaluation of mesenteric ischemia in a subgroup of patients with nonspecific symptoms. CT enterography performed with an optimized multiphase or dual phase technique may directly depict the cause of mesenteric ischemia. It is critical that radiologists understand the underlying disease process so as to accurately interpret the findings and diagnose the cause of mesenteric ischemia. The three main causes of mesenteric ischemia are (a) arterial occlusion or compromise, (b) venous occlusion, (c) low flow states such as poor cardiac output or hypovolemia Superior mesenteric artery occlusion accounts for more than half of all cases of mesenteric ischemia , and nonocclusive ischemia secondary to low flow states accounts for 30%. Venous occlusion is the least common cause of mesenteric ischemia. New treatment methods based on minimally invasive techniques (eg, intra-arterial thrombolysis or angioplasty, anticoagulation therapies) make the CT detection of arterial or venous occlusion important. Most cases of acute mesenteric ischemia are due to emboli at the origin of the middle colic artery branch of the superior mesenteric artery, or in the proximal part 3–10 cm from the origin. Multidetector CT, with its increased temporal resolution and decreased section thickness, allows significant improvements in the evaluation of mesenteric vessels, detection of fat stranding, and characterization of bowel wall changes, including thickening or edema (which, although nonspecific, are the most commonly reported findings). The thickened segment of bowel may demonstrate hyperenhancing mucosa, a sign of reactive hyperemia due to reperfusion injury, another important finding. The involved loop of bowel may demonstrate an absence or delay of enhancement in the presence of interrupted blood flow or increased venous pressure. Dilatation of the involved bowel segment due to aperistalsis is another described finding . Pneumatosis is less commonly seen . In addition to visualization of bowel wall changes, CT enterography allows improved evaluation of the mesenteric vasculature and helps determine the underlying cause of vascular compromise . Small bowel ischemia. Axial CT enterographic section obtained in the arterial phase shows an abnormal segment of small bowel with wall thickening and hypoenhancement (white arrows), findings indicative of ischemia due to thromboembolic occlusion (black arrow) of the superior mesenteric artery Other Findings Although CT enterography is a dedicated protocol for the diagnosis of small bowel diseases, incidental findings with this modality may be significant. Such findings might include not only abnormalities internal to the GI tract but also extraluminal, peritoneal, mesenteric, and omental abnormalities; hepatic and pancreatic masses; and disease involving other organs. Mesenteric lymphangioma. Axial CT enterographic section obtained for evaluation of Crohn disease depicts a nonenhancing mesenteric lesion (arrows) with attenuation similar to that of fluid, an incidental finding consistent with mesenteric lymphangioma. Summary CT enterography is an invaluable technique for the evaluation of various small bowel diseases. Its main uses are in the assessment of inflammatory bowel disease, occult GI tract bleeding, and mesenteric ischemia. An optimal technique with adequate bowel distention is required for obtaining accurate diagnostic results. A single (venous) phase technique is used for bowel evaluation, and a dual phase technique is used for evaluation of mesenteric ischemia. A triple phase protocol is currently being optimized for the evaluation of GI tract bleeding. CT enterography also has been shown to be more cost-effective in the long-term assessment and follow-up of patients, especially those with established Crohn disease. MR enterography is being used more frequently because of the advantage of lack of radiation. However, the superior spatial resolution of CT enterography still makes it the initial imaging modality of choice in many adult patients.