19. CT in Inflammatory Bowel Disease

245D.C. Baumgart (ed.), Crohn’s Disease and Ulcerative Colitis: From Epidemiology and Immunobiology to a Rational Diagnostic and Therapeutic Approach , DOI 10.1007/978-1-4614-0998-4_19,© Springer Science+Business Media, LLC 2012K eywords C T • S mall bowel • C T enterography • C rohn’s disease • R adiation risk CT enterography (CTE) is a high spatial resolution CT exam of the abdomen and pelvis, following the administration of a large volume of enteric contrast agent that distends the small bowel. It provides exquisite images of the small bowel wall, lumen, and perienteric tissues. Over the past decade, CTE has become a widely available test interpreted with local expertise, and is complementary to other imaging modalities, providing unique information that impacts clinical management of patients with inflammatory bowel disease (IBD).R ole of CTE in IBD CTE is used to image the small bowel to detect IBD and alternative diagnoses (such as pancreatic disease, sprue, and small bowel tumors). For known patients with Crohn’s disease, in particular, CTE is used to detect the location(s) and severity of enteric inflammation; the presence, location, and type of penetrating disease (fistula, abscess, or phlegmon); and the location and degree of obstruction caused by inflammatory and fibrostenotic strictures. In ulcerative colitis, CTE is used to gauge the extent of colonic inflammation, usually used in conjunction with ileocolonoscopy, and to exclude small bowel involvement prior to colectomy. Both Crohn’s disease and ulcerative colitis also cause a variety of extraenteric complications, such as neoplasia, mesenteric thromboses, neph-rolithiasis, cholelithiasis, sacroiliitis, etc., that can be visualized by CT. CTE also detects complica-tions from surgical and medical therapies, such as avascular necrosis, leak, pancreatitis, etc.P atient Preparation and Image Acquisition Patients generally are requested to fast 4 h prior to CTE so that ingested materials are not in the stom-ach or small bowel. An enteric contrast agent is then administered in multiple aliquots over 45–60 min C hapter 19C T in Inflammatory Bowel DiseaseJ oel G . F letcherJ . G . F letcher, MD ( )D epartment of Radiology ,M ayo Clinic ,200 First Street SW ,R ochester ,M N 55905 ,U SAe -mail: Fletcher.joel@246J.G. Fletcher prior to CT examination. Enteric contrast agents generally contain sugar alcohols or osmotic laxatives to prevent resorption of water along the course of the small bowel, thereby improving ileal distention[1, 2 ] . Commonly used enteric contrast agents include low-contrast barium solution (which containssorbitol, V olumen ®, Bracco Diagnostics, Princeton, NJ), polyethylene glycol electrolyte solution, or methylcellulose solution. Side effects from oral contrast are minimal but can include nausea, time-limited diarrhea, and excess gas [ 1 ] . Neutral enteric agents distend the lumen better than water and provide a long temporal window over which imaging can occur and still provide adequate luminal distention. In the hospital setting, water is typically given as an oral contrast agent, as patients typically have an underlying degree of bowel obstruction, and a predisposition to nausea is increased. Glucagon or buscopan can be given to limit peristalsis but has not been proven to improve test performance. I ntravenous iodinated contrast is given at a rapid rate (e.g., ³ 4 cc/s) to enhance the bowel wall, with CT imaging typically initiated during an enteric phase of contrast enhancement, when small bowel enhancement is maximal, typically occurring 50 s after initiation of the IV injection of contrast[3 ] . Alternatively, imaging can be performed in the portal or hepatic phase, when the radiologic imag-ing of solid organs is optimal, without decrement in the identification of mural inflammation [ 4 ] .C T parameters governing spatial resolution and imaging speed are chosen so that the entire abdo-men and pelvis can be imaged in 20 s or less (i.e., single breathhold) and so that spatial resolution in non-axial planes is optimized. With multi-detector CT with 16 detector rows or more, the mini-mal detector configuration less than 1 mm is chosen so that isotropic coronal images can be obtained. Generally, narrow slice thickness of 3 mm or less is reconstructed in the axial and coronal place for image review. Imaging is typically performed at a tube voltage of 120 kV , which facilitates excellent image quality across the entire gamut of patient sizes and can generally be performed with a CT dose index of <18 mGy (or an effective dose of 12 mSv) [ 5 ] , owing to the high contrast of the enhancing bowel. Further, reduction in radiation dose is easily obtained through reduction in tube current (i.e., mAs) by employing automatic exposure control and/or kV selection [ 6, 7 ] . Automatic exposure control is used on most modern multi-detector CT scanners to modulate the tube current as the X-ray tube travels around the patient and as the patient travels through the scanner, generally reducing dose on the order of 30% [ 8 ] . Selection of kV can lower the tube energy in smaller patients and simultaneously increases the iodine contrast, to permit further dose reduc-tions (Fig. 19.1 ), but requires technique charts or vendor-supported software. Alternatively, lower kV (80 or 100 kV) imaging may be chosen to improve iodine signal and contrast to compensate for reduced injection rate or amount of intravenous iodinated contrast (Fig. 19.2).M ultiple practices have demonstrated that there is no reduction in the performance of CTE using lower radiation doses, as the increase in image noise is offset by the high contrast of enhancing bowel loops and penetrating disease [ 9, 10 ] . Noise reduction techniques, which decrease image noise, may make further dose reductions possible, and improve image quality by decreasing image noise so that low-dose images resemble routine-dose images (Fig. 19.3)[11, 12].F ig. 19.1 E xample of dosereduction at lower kV in43-year-old female with priorright hemicolectomy.CTDIvol lowered from24 mGy (routine protocol) to10 mGy after kV selection(80 kV). Note active ileitis inneoterminal ileum ( a rrow )and small fi stulous tractsbetween descending colonand adjacent small bowel( i nset ,a rrows )24719 CT in Inflammatory Bowel Disease I maging FindingsU nderlying Mural InflammationMural hyperenhancement refers to segmentally increased attenuation of bowel loops compared with adjacent loops, and this correlates histologically with areas of active inflammation [ 13].F ig. 19.2 C T enterography performed in a 32-year-old person with indeterminate proctitis and poor intravenous access. To compensate, tube voltage was lowered to 100 kV with initiation of scanning delayed until 70 s. Large coronal image shows mild asymmetric hyperenhancement at terminal ileum reflecting mild inflammation ( l arge white arrow ), while insets show stratification and enhancement of the appendiceal tip ( u pper inset ,a rrow ), and active proctitis with mural stratification, hyperenhancement, and reactive lymphadenopathy ( l ower inset )F ig. 19.3 L ower-dose CT enterography in 63-year-old male showing twofold reduction in image noise from rou-tinely reconstructed image ( a ) to image reconstructed using image noise reduction techniques ( b ) Note that mural stratification and hyperenhancement indicating active ileitis in the terminal ileum ( a rrow ) between ileoileostomy and ileocecal valve can be detected before image quality improvement with noise reduction248J.G. Fletcher F ig. 19.4 T ransverse CT enterography images in a 19-year-old Crohn’s patient with “back pain.” Images demon-strate mural thickening and stratification ( l arge arrows ,a –c ), with a bilaminar appearance to the bowel wall. Note that mural thickening and luminal hyperenhancement are asymmetric ( a ,c ), with one loop demonstrating mesenteric border thickening and hyperenhancement and antimesenteric border pseudosacculation ( s mall arrow ,a ). One inflamed loop demonstrates small penetrating ulcers ( s mall arrow ,b ), whereas another has prominent vasa recta, or “comb sign” ( c ,s mall arrows )Mural hyperenhancement is the most sensitive sign of bowel inflammation, and it can be an isolated finding in mild inflammation. Hyperenhancement alone is a non-specific finding in the small bowel, but asymmetric and patchy hyperenhancement, particularly along the mesenteric border, is indica-tive of Crohn’s disease (Figs. 19.1–19.4).M ural hyperenhancement is often accompanied by wall thickening, which in the small bowel is greater than 3 mm in thickness in a bowel loop that is distended with luminal contrast. Wall thicken-ing in Crohn’s disease is often asymmetric and more prominent along the mesenteric border as well. As mural inflammation increases, wall thickening is often accompanied by mural stratification,which refers to a bi- and trilaminer appearance to the bowel wall (Fig.19.4 ). The presence of both24919 CT in Inflammatory Bowel Disease segmental mural hyperenhancement and wall thickening yields the best imaging criteria for mural inflammation in Crohn’s disease [ 5, 14].P enetrating ulcers can also be seen in inflamed bowel loops, and they may appear as filling defects in the inflamed bowel wall; however, they are more frequently seen at MR enterography. The “comb sign” refers to engorged vasa recta, which supply inflamed bowel loops and penetrates the gut wall perpendicular to the lumen, resembling the shape of a comb [ 15 ] . The comb sign is associated with increased serum C-reactive protein, length of hospitalization, and response to anti-inflammatory treatment (Fig. 19.4)[16– 18].C TE can also display findings of chronic inflammation. Intramural fat can be seen in actively and uninflamed small bowel loops in the colon, indicating chronic inflammation, but intramural fat in the terminal ileum is a normal finding. Alternatively, pseudopolyps are frequently seen through-out the colon after healing of acute inflammation [ 19 ] . Fibrofatty proliferation is seen as prolifera-tion of fat, usually allowing the mesenteric aspect of the bowel loop, displacing nearby abdominal loops, and in the rectum it can resemble pelvic lipomatosis, except that there are prominent perirec-tal vessels and reactive lymphadenopathy.F indings of intestinal inflammation in ulcerative colitis are similar to Crohn’s. The pattern of inflammation in ulcerative colitis that is most typical is continuous inflammation from the rectum proximally. A patulous ileocecal valve is often seen when inflammation extends to the cecum (Fig. 19.5 ), as well as backwash ileitis, which involves the terminal ileum symmetrically without penetration. Forshortening of the colon it is also seen with chronic ulcerative colitis. As inflamma-tion becomes chronic, intramural fat is deposited throughout the colon, but this finding is not unique to ulcerative colitis.P erienteric InflammationT he most subtle findings of perienteric inflammation in Crohn’s disease are perienteric fat stranding, which correlates with serum C-reactive protein [ 16 ] .Fistulas appear as hyperenhancing extraenteric F ig. 19.5 F ifty-eight-year-old person with a 4-monthhistory of altered bowel pat-tern. Coronal CT enterogra-phy images show fi ndings ofchronic ulcerative colitis,including moderate sigmoidinfl ammation ( a rrow head )and mild chronic proximalcolitis in the descendingcolon and cecum ( s mallarrows ), as manifested byintramural fat, loss of haus-tration, and prominent peri-colic vessels with reactivelymphadenopathy. The ileo-cecal valve is widely patu-lous ( l arge arrow )250J.G. FletcherF ig. 19.6 C TE in a 21-year-old female demonstrating a complex fistula ( l arge arrow,a,b) connecting two loops of ileum ( s mall arrows,t ransverse image,a) in the right lower quadrant, with an inferior arm extending to the dome of the bladder, where there is a 3.2-cm abscess within the bladder wall ( s mall arrows,c oronal image,b). (b is reprinted from Gastroenterology 2011;140:1795–1806)tracts, which may or may not contain air and fluid [20]. Fistulas frequently arise from inflamed bowel loops and cause tethering of the involved loops, frequently forming asterisk-shaped fistula complexes (Fig. 19.6). Fistulas that arise from surgical anastomoses and perianal fistulas are often not hyperenhancing due to their chronic nature. As fistulas extend into the mesentery, they frequently cause mesenteric thromboses, which are associated with Crohn’s related inflammation (Fig. 19.7), and collateralization via the gut arcade is often seen.O bstructionM ural inflammation causes luminal narrowing, but luminal narrowing at enterography does not imply lack of distensibility or stricturing disease. Distensibility can be observed fluoroscopically, for example using peroral pneumocolon. At CTE assessment, luminal narrowing indicating lack of distensibility is only indicated by obstruction significant enough to cause dilation of proximal bowel loops. Most Crohn’s strictures demonstrate a spectrum of inflammatory and fibrotic changes [21], and most Crohn’s strictures will demonstrate some degree of hyperenhancement at imaging, so enhancement alone is not a good indicator of potential response to treatment for a stenotic small bowel segment demonstrating hyperenhancement.C TE Performance and Correlation with Clinical SymptomsC TE has an estimated sensitivity for detecting ileal inflammation of approximately 75–90% using mucosal inspection and biopsy as a reference standard [13, 14, 22, 23].When clinical assessments additionally including surgery, serum, and clinical follow-up are integrated, the sensitivity of enterography for detecting ileal and inflammation improves to 90–95% [5, 24, 25],as studies utiliz-ing ileoscopic reference standards necessarily exclude patients with stenotic ileocecal valves and misclassify patients with proximal ileal disease. The performance of enterography for identifying active jejunal inflammation is likely decreased due to the greater enhancement of jejunal loops and25119CT in Inflammatory Bowel Disease F ig. 19.7 C oronal CTE image in 46-year-old Crohn’s patient with obstructive symptoms demonstrates long segment inflammation ( l arge arrow ,a ) with mural stratification, wall thickening, and comb sign ( b rackets ,a ), with multiple loops of dilated proximal small bowel having prominent mesenteric veins (small white arrow ,a ). Coronal image slightly posteriorly ( b ) with corresponding transverse image ( c ) shows chronic occlusion and narrowing of the supe-rior mesenteric vein ( s mall arrows ,b ;l arge arrow ,c ) and enlarged inferior mesenteric vein ( a rrow head ,b ,c ). (SMA= b lack arrow ,c )the complexity of jejunal folds [ 22 ] , and capsule endoscopy is complementary to CTE for detecting more proximal inflammation [ 23 ] . Like other objective measures of inflammation in Crohn’s disease, enterography findings often do not correlate with symptomatology. In a retrospec-tive study, Higgins et al. found that enterography added unique information to clinical assessment and changed perception of steroid benefit in nearly two-thirds of patients [ 26].In a prospective study of 270 patients at Mayo Clinic, Bruining et al. recorded management decisions before and after252J.G. Fletcher CTE, and found that CT imaging changed management decisions in about half of Crohn’s patients, and a similar portion of those with suspected Crohn’s disease [ 18].C TE has a high accuracy for identifying penetrating disease, which is often unsuspected [ 20, 27, 28 ] . It has an estimated accuracy for identifying enteric fistulas of 86%, with a per-patient sensitiv-ity of 94% and 97–100% in detecting patients with fistulas and phlegmon/abscesses, respectively[27 ] . Booya et al. found that nearly half the patients with penetrating disease had either no clinical suspicion or remote clinical suspicion of penetrating disease at pre-imaging clinical assessment [ 20]. A lthough CTE has a high sensitivity for detecting obstructive strictures in surgical series [ 27],its performance is suboptimal in evaluating low-grade obstruction. Nevertheless, many Crohn’s patients with partial small bowel obstruction at CTE do not have obstructive symptoms. The fact that capsule endoscopy retention rates are highest in this cohort underscores the frequency of asymptomatic stenotic lesions in Crohn’s disease [ 29 ] . In one prospective study, 17% of patients without obstruc-tive symptoms had an inflammatory stricture causing partial small bowel obstruction at CTE (Fig. 19.8)[23 ] . When CTE does not reveal partial obstruction associated with luminal narrowing, capsule endoscopy maybe useful in identifying additional enteric inflammation [ 23, 30 ] .C TE and Multimodality Imaging Assessment Ileocolonoscopic assessment is generally considered complementary to enterography, as a colonos-copy is more sensitive for identifying mucosal inflammation, particularly in the colon, provides cancer surveillance not provided by CTE, and is usually performed with random biopsies, which also assist with risk stratification for cancer [ 23, 31 ] . While CTE is more sensitive than fluoroscopic analysis, particularly in identifying penetrating complications of Crohn’s disease [ 25],fluoroscopy can provide functional information relating to luminal distensibility and partial obstruction that can-not be ascertained from volumetric CT imaging at a single time point. Capsule endoscopy is more sensitive at identifying mucosal inflammation than enterography (particularly in the jejunum), but is less specific and cannot identify perienteric complications, and usually requires pre-imaging assessment or use of a patency capsule [ 23, 32, 33]F ig. 19.8 F orty-six-year-old female with prior right hemicolectomy and frequent diarrhea thought to be without obstructive symptoms. CT enterography demonstrates two regions of luminal narrowing ( l arge arrows ,a )with proximally dilated loops ( a rrow heads ,a ,b ). Luminal narrowing at anastomosis ( s mall arrow ,a ) does not cause proximal dilation of neoterminal ileum ( s mall arrow ,b ). At operative assessment the two strictures in the mid small bowel underwent strictureplasty, but ileocolic anastomosis was distensible253 19 CT in Inflammatory Bowel DiseaseM R enterography has an estimated performance for the detection of mural inflammation similar to CTE [24, 25], but is not available at all centers, requires much more imaging time, and is likely more prone to interobserver variability [34]. While the American College of Radiology recom-mends CTE as the most appropriate imaging test for patients with suspected Crohn’s disease, or known Crohn’s patients with fevers and abdominal pain [35], MR enterography is likely more appropriate for the follow-up of patients with known Crohn’s disease for monitoring therapeutic response or those with obstructive symptoms [36]. MR is also able to stage perianal fistulas when they are present. Because of the improved spatial and temporal resolution of CT compared to MR, CTE can be used as a subsequent test when MR enterography demonstrates complex penetrating disease that may require surgical or interventional treatment.B enefits and Risks of CT ImagingT he principal benefits of CT imaging in patients with Crohn’s disease is to identify suspected and occult mural inflammation and penetrating complications that will change medical or interventional treatment. Protean patient symptomatology and the poor relationship between symptoms and bio-logic activity in Crohn’s disease result in substantial benefit to patients from imaging [18].However, CT utilizes low levels of ionizing radiation. While the low risk estimates of radiation-induced malignancy are uncertain enough that the absence of risk cannot be excluded on a scientific basis for a single CT exam [37, 38], a small risk should be assumed to protect patients [39, 40],particu-larly for younger patients who are at greatest risk [41]. Ameliorating conditions which make CT a more appropriate test compared with imaging alternatives include patient symptomatology, absence of prior imaging, contemplated surgical intervention, higher age, and contraindications to MRI. A principal advantage of CTE is its widespread availability at most medical institutions, being performed and interpreted with a high degree of local expertise.S ummaryC TE has become an accepted adjunctive test in the evaluation of patients with IBD. Its role is to detect mural inflammation and penetrating complications of Crohn’s disease which are clinically occult, and its routine use results in substantial impact on patient management decisions. 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