Colon: Non Neoplastic Disease: Imaging of the Idiopathic Inflamatory Bowel Diseases

Karen M. Horton, MD, Bronwyn Jones, MD, Elliot K. Fishman, MD

Introduction

Despite the widespread use of fiberoptic endoscopy, radiologic imaging continues to play a significant role in the diagnosis, evaluation, and management of patients with inflammatory bowel disease. In the past, barium studies were the primary method available for examination of the small bowel and colon. However, today's radiologist can employ a variety of state of the art imaging modalities to evaluate the gastrointestinal tract as well as extraintestinal manifestations of gastrointestinal diseases.

This chapter will discuss the variety of radiologic imaging techniques currently utilized in evaluation of patients with Crohn's disease and ulcerative colitis. Important radiologic features will be reviewed and illustrated.

Current Imaging Modalities

Contrast Studies

Contrast studies are the cornerstone in radiologic diagnosis of inflammatory bowel disease and are sensitive in demonstrating the mucosal extent of disease. The most common contrast examinations performed today include: small bowel series, enteroclysis, barium enema, and the upper gastrointestinal series.

The Small Bowel Series vs. the Enteroclysis

Two methods are available for radiographic examination of the small intestine: small bowel series and enteroclysis. Over the last several years, there has been considerable debate in the radiologic literature as to which of these procedures is superior. The traditional small bowel series is faster, safer, and involves considerably less radiation than enteroclysis such as adhesions and Meckel's diverticulum, but has a higher complication rate and is technically more demanding. Overall, the accuracy of the two techniques for Crohn's disease is probably similar, as long as both are performed with careful attention to detail2, 3.

In the standard small bowel series, the patient drinks 2-4 twelve ounce cups of a relatively thin barium suspension. At regular intervals (20-30 minutes on average) an overhead abdominal radiograph is taken in order to follow the progression of the barium through the small intestine. When the barium reaches the right colon (typically 30-90 min.), the patient is taken into the fluoroscopic suite. Under fluoroscopy, the radiologist vigorously compresses the small bowel while moving the patient in various positions in order to unwind superimposed loops. A series of compression spot radiographs are obtained, with special attention to the terminal ileum.

In cases where the terminal ileum is not well visualized, air can be administered through a rectal tube until it reaches the ileocecal region. This technique is a valuable adjunct to the routine small bowel series. Alternatively, a special radiograph called the prone-angled compression view can be obtained to allow better visualization of the pelvic small bowel loops which often are overlapped on routine AP radiographs 4.

During enteroclysis, a tube is passed through the nose and advanced through the esophagus and stomach, and into the jejunum, just past the ligament of Treitz. A small balloon is then inflated to keep the tube in place and to prevent regurgitation of contrast. In some centers, the patient is given a mild sedative, such as Valium5. Under fluoroscopic guidance, 200-250 cc of specially formulated barium is infused through the tube at a rate of 50-100 cc/min. Next, the radiologist infuses 750-1000 cc of a methylcellulose solution. This combination of barium and methylcellulose results in distention and coating of the small bowel loops (Fig 1). The appearance is similar to a double contrast enema. Thus, this technique is sometimes referred to as a small bowel enema. Some advocate single contrast enteroclysis, and would therefore not use methylcellulose.

The Barium Enema

The double contrast barium enema is a safe and effective imaging tool for the evaluation of patients with inflammatory bowel disease. Its ability to demonstrate the depth of ulcers and presence of fistulae represent a distinct advantage over colonoscopy. In addition, a barium enema is usually able to effectively image areas of colon which cannot be reached in cases of incomplete colonoscopy6, which occurs in almost 10% of colonoscopic examinations7. Therefore, barium enema and colonoscopy with biopsy should be considered complementary studies.

The double contrast barium enema is performed by carefully administering a viscous high density barium sulfate suspension through a rectal tube. Next, under fluoroscopic guidance and with various patient positioning, air is gently introduced through the tube until the entire colon is distended with air and coated with barium. This examination requires careful attention to technique so that optimal coating of the colon is achieved. Excess barium or air will result in inadequate visualization of the colon.

Spot films are often taken by the radiologist during filling of the colon. Next, a series of overhead films are taken by the technologist after the patient has been positioned appropriately to demonstrate the entire colon. Finally, a post evacuation film completes the study. Often, the terminal ileum will be demonstrated best or only on the post evacuation film, after the colon has actively contracted.

Single contrast examination of the colon is also helpful in cases of suspected obstruction or fistula, but cannot demonstrate subtle mucosal involvement or shallow ulceration. During this examination, the radiologist administers a thinner barium suspension or in some cases a water soluble solution through a rectal tube. Under fluoroscopic guidance the radiologist palpates/compresses the colon and takes spot films. The technologist will then take a standard series of overhead films after careful positioning of the patient. Finally a radiograph is taken after the patient has evacuated the barium. Again, careful attention to technique is essential to obtain high quality radiographs.

Upper Gastrointestinal Series

The upper gastrointestinal series allows evaluation of the esophagus, stomach and duodenal C-loop. The examination can be performed by either single or double contrast techniques.

The single contrast exam involves the patient drinking a thin suspension of barium or a water soluble contrast solution. Fluoroscopic spot radiographs of the esophagus, stomach and duodenum are taken by the radiologist. Subtle mucosal involvement is not reliably detected using single contrast techniques.

During the double contrast examination the patient ingests 4-6 g of effervescent gas crystals followed by a thick barium suspension. This results in air distention of the upper gastrointestinal tract which is coated with barium. The radiologist then positions the patient appropriately and obtains a series of spot radiographs. Esophageal peristalsis is also assessed in the prone, right anterior oblique position using a thin barium suspension.

Computed Tomography (CT)

CT has become a valuable diagnostic tool in the evaluation of patients with inflammatory bowel disease and is considered complementary to traditional contrast examinations. Although barium contrast studies are superior in demonstrating mucosal extent of disease, CT can accurately image the bowel wall as well as extraluminal extension of disease8. Therefore, CT can significantly affect patient management9 . In addition, it is important to recognize the CT features of inflammatory bowel disease, as CT may be the first imaging study performed in a patient presenting with nonspecific abdominal pain.

Accurate CT imaging of the small bowel and colon requires careful attention to technique. The following is our protocol:

The patient routinely drinks approximately 750-1000 cc of a 3% oral iodinated contrast solution 60-90 minutes before the scan and an additional 250 cc of oral contrast immediately before the study. This allows adequate contrast opacification of the stomach and small bowel. If colonic pathology is suspected, it is important to adequately opacify the entire colon. In these cases, oral contrast is administered the night before the study as well as prior to the scan to ensure that contrast opacifies the colon as well as the small bowel. Alternatively, in urgent cases, or in patients in whom limited rectosigmoid disease is suspected, a 3-4% iodinated contrast solution can be administered gently through a rectal tube. The use of air and/or water to distend the colon has also been reported. 10

The administration of intravenous contrast is essential for complete evaluation of patients with inflammatory bowel disease, especially if extracolonic extension of disease is suspected. We routinely administer 100-120 cc of Omnipaque 350 at a rate of 2-3 cc/sec. injected through a peripheral vein. Intravenous contrast is not administered if an enterovesical fistula is suspected clinically.

On standard CT scanners, the abdomen should be routinely imaged from the level of the diaphragm through the perineum11. Consecutive slices with 5-8 mm collimation are obtained contiguously at 10 mm intervals. Additional scans are then performed through specific areas of concern.

Today, spiral CT technology allows faster, sub-second, scanning which can be combined with rapid contrast infusion and narrow collimation. The entire upper abdomen can be imaged in a single 30 sec. breath hold. This essentially eliminates misregistration artifacts due to patient movement or respiration. Using spiral CT, 5 mm collimation can be performed with a table speed of 8 mm/sec., with reconstruction every 5 mm. Our standard spiral CT protocol is to begin scanning 45-50 seconds after initiation of contrast injection.

MR

Multiplanar capability, high contrast resolution and the lack of ionizing radiation make MR an ideal abdominal imaging modality. However, the application of MR for gastrointestinal tract imaging has been limited. In the past, image acquisition times were prohibitively long, image quality was significantly degraded by movement and bowel peristalsis, and there was no adequate oral contrast agent available.

Currently, recent technical advancements have reduced imaging times significantly, thus decreasing artifacts from motion. In addition, there is active ongoing research in a variety of possible MR intraluminal contrast agents including: water, barium12,perflubron (perfluorooctylbromide)13, per-rectal vegetable oil14.

Because of these recent advancements there is now increasing interest in the application of MR for imaging of inflammatory bowel disease, including Crohn's disease and ulcerative colitis.

Several studies of MR imaging in Crohn's disease suggest that MR may be useful in evaluating the severity of disease and may provide information complementary to the clinical evaluation15. Bowel wall thickening can be detected and is considered a reliable sign of disease as is marked enhancement16.

Although direct MR imaging of the bowel is limited at this time, MR is an effective modality for evaluation of complications of Crohn's disease including sinus tracts, fistulae and abscesses 17, 18 and has been found to be especially useful in the evaluation of perianal and perirectal disease. 17.

However further advancements will be necessary before MRI becomes a practical gastrointestinal tract imaging modality for inflammatory bowel disease.

Ultrasonography

Ultrasonography is a safe, noninvasive imaging modality that is gaining wider acceptance as a technique for imaging the gastrointestinal tract, especially in children. In Europe ultrasound is extensively used as a screening technique for disease of the gastrointestinal tract. Right lower quadrant sonography, using modern 3.5 or 5.0 MHz transducers allows accurate visualization of the distal small bowel. Wall thickening and echotexture can therefore be evaluated. In addition, ultrasound of the colon can also be performed after water enema in patients with Crohn's or ulcerative colitis in order to evaluate wall thickening. The application of color Doppler imaging and Power Doppler may allow differentiation of active bowel thickening (increased blood flow) from chronic wall thickening/fibrosis (no increased flow)19. Similarly, Doppler ultrasound can also demonstrate hemodynamic changes in patients with active inflammatory bowel disease which are not present in patients with quiescent disease20 (Fig 2).

A recent study by Solvig et al compared ultrasound and enteroclysis findings in patients with Crohn's disease. The ultrasound and enteroclysis findings correlated in 18/20 patients and also the ultrasound examination was normal in 37 of 39 patients with a normal enteroclysis21. Another study by Hata, concluded that ultrasound has a sensitivity of 86% for Crohn's disease and 89% for ulcerative colitis22.

The role of ultrasound in the gastrointestinal tract is still evolving. Although recent work is promising, ultrasound continues to be very operator dependent and is adversely affected by such factors as obesity and intraluminal gas. This will likely limit its widespread application for imaging the bowel in this country.

Nuclear Medicine

With the availability of radionuclide-labeled white blood cells, nuclear scintigraphy is quickly emerging as a promising technique for visualizing actively inflamed bowel. In the past, the major radionuclide used in evaluating patients with active inflammatory bowel disease was gallium 6723-25. Although this agent was considered sensitive and specific for the diagnosis of active bowel disease, gallium is normally excreted by the bowel, making interpretation of studies very difficult, even after adequate bowel preparation.

Today, new radionuclides are available including indium-labeled and technetium-labeled white blood cells. In these studies, blood is removed from the patient and the white blood cells are separated and labeled, then reinjected. The radionuclide accumulates at sites of acute inflammation or infection. On imaging, typically performed at 6, 12 and 24 hours, any bowel activity is abnormal and signifies active inflammation/infection. Focal intraabdominal activity is suggestive of abscess.

Several studies have demonstrated good correlation between the results of indium-labeled white cell studies and colonoscopy, barium enema and clinical symptoms in patients with active inflammatory bowel disease26-29. Technetium- 99m-hexamethyl-propylamine-oxime (HMPAO) is another white blood cell labeling agent which is less expensive, results in decreased patient radiation dose and better image quality. This agent has also been shown to be helpful is assessment of the existence, extent and intensity of active inflammation in inflammatory bowel disease patients30 and is likely to replace indium in the future. In a study of 115 patients with Crohn's disease and 21 patients with ulcerative colitis, sensitivities for active disease were 98% and 98% at 1 and 3 hours, respectively30. Specificity was 100% and 83% at 1 and 3 hours respectively. Both indium- and technetium-labeled white blood cells have been shown to be useful in screening patients for active inflammatory bowel disease.31.32.

As new more selective radionuclides become available, the role of nuclear scintigraphy in evaluation of patients with inflammatory bowel disease will likely expand. At this time, the strength of these radionuclides is the ability to screen patients for disease and to differentiate active from inactive disease. However, because of the limited spatial resolution and difficulty at present in differentiating between inflammatory and infectious bowel diseases, the use of scintigraphy is limited to problem cases where other imaging modalities are equivocal.

Examinations of Historic Interest

Rectal Parietography

In the late 1950s and early 1960's investigators noticed an increased presacral space in patients with ulcerative colitis. Rectal parietography was a technique which attempted to determine whether this widening was due to rectal wall thickening33. During the procedure, a 15cm needle (1.2mm diameter) was inserted into the presacral space using a lateral approach. After 1cc Urografin was injected to confirm the position of the needle tip, 200-400 cc of oxygen was infused. The rectum was then filled with barium. The rectal thickness could then be measured. A rectal wall thickness greater than 10mm supported the diagnosis of ulcerative colitis.

Mesenteric Angiography

Mesenteric angiography was sometimes used in the 1960's to distinguish between Crohn's disease and ulcerative colitis in difficult cases where barium enema was equivocal34. Angiography was performed of the superior and inferior mesenteric arteries using a vasodilating substance and a metrizoate contrast medium. In patients with Crohn's disease, the angiographic findings included a reduced number of arteries within the bowel wall and the presence of irregular or tortuous vessels. The main angiographic changes in ulcerative colitis were hypervascularity of the diseased bowel with increased accumulation of contrast within the wall and rapid venous return34.

Radiographic Findings in Crohn's Disease

Contrast Studies Site of Involvement

Crohn's disease can affect any portion of the gastrointestinal tract.

The terminal ileum is the most common site of involvement and is the only site of involvement in up to 30% of patients. However, ileal disease often occurs in combination with right colon involvement 35. The combination of small bowel and colon involvement occurs in 50% of patients36, 37.

Diseased limited to the colon occurs in only 19% of patients. The rectum is involved in approximately 50% of patients and spared in the remaining 50% but isolated anal and perianal involvement is rare and only found in 2%. Anorectal disease can include erosions, ulcers, hemorrhoids, perineal abscess, fissures and fistulae38, 39.

With double contrast technique, up to 13% of patients with Crohn's disease will show early signs of involvement of the upper gastrointestinal tract40. These patients typically will also have concomitant disease in the small bowel or colon40. Duodenal involvement is commoner in young patients than in older patients.

The site and radiographic appearance of disease tends to run in families. In a recent study of 554 patients by Bayless et al41,95 (17%) had a family history of Crohn's disease. 86 % of these families were concordant in at least 2 members for the site of the Crohn's disease and 82% were concordant for the clinical type of disease (i.e. obstructing, fistulizing, etc.). These results suggest that there may be multiple distinct, possibly inherited, forms of Crohn's disease.

Small Bowel and Colon

Mucosal Granularity

The earliest radiographic finding on contrast studies in Crohn's disease is a diffuse granular appearance to the normally smooth mucosa of an involved bowel segment42. This pattern is most commonly seen in the small bowel, but can rarely be detected in the esophagus as well.

This distinctive radiographic appearance is produced by a network of radiolucent foci which measure 0.5- 1 mm in diameter and represents edema and lymphocytic infiltration of the villi 43. Electron microscopic studies of early Crohn's disease show that the villi are not only edematous but clubbed and branching, also contributing to the granularity.

Fold and Wall Thickening

Thickening of the bowel wall is a common radiographic finding in Crohn's disease involving both the small bowel and colon.

On contrast studies, the normal small bowel fold and wall thickness should be <3 mm. In Crohn's disease, a transmural disease, as the edema and inflammation involve deeper portions of the wall, thickening of the small bowel folds occurs which can be detected on contrast studies. The fold thickening is often eccentric, discontinuous and irregular ("skip areas"), reflecting the underlying pathology. Small bowel wall thickening can also be seen as parallel separation of adjacent loops (Fig 4).

Colonic wall thickening also occurs in patients with Crohn's disease, and as in the small bowel, typically appears patchy, discontinuous and asymmetric, reflecting the underlying pathology. The asymmetry of the disease involvement can result in the formation of pseudodiverticula (Fig 5). This discontinuous appearance ("skip areas") is an important feature which distinguishes Crohn's disease from ulcerative colitis, which usually appears confluent, continuous and circumferential.

Strictures

Rigid wall thickening and fibrosis can also occur in the small bowel and colon in Crohn's patients and presents as segmental areas of luminal narrowing. The deformity may affect only a portion of the bowel wall or may be circumferential, resulting in the formation of a stricture. On contrast examination, these strictures typically appear as segmental narrowings without normal mucosal pattern and with smooth tapered ends. The stricturing can be marked, especially in the terminal ileum. This is sometimes referred to as the "string sign" (Fig 6). Marked stricturing in the small bowel or colon may result in obstruction.

Lymphoid Hyperplasia

Extensive "lymphoid hyperplasia" may be an early sign of Crohn's disease in the small bowel and colon. True lymphoid hyperplasia shows small regular 2-3mm filling defects in a carpet-like pattern (Fig7). Variability in size or larger than 3mm lymphoid follicles should suggest inflammation of the lymphoid follicle and is suggestive of Crohn's disease. The aphthoid ulcer is actually an ulcerated lymphoid follicle. Sometimes there is marked enlargement of these lymphoid follicles in patients with Crohn's' disease, mimicking lymphoma (Fig 8).

Ulceration

Aphthoid or discrete ulcers are among the earliest mucosal lesions which are demonstrated on contrast studies. They often occur on a background of normal mucosa or less commonly, at the margin of a severely diseased segment44. These lesions often appear on double contrast studies as round or oval well defined barium collections measuring a few mm in size. The borders of the ulcers are typically well-defined, often with a surrounding halo of edema (Fig 9).

Aphthoid ulcers are seen on double contrast barium enemas in up to 70% of patients with Crohn's disease 44, 45. These lesions typically are not shown with single contrast studies except with exquisite compression studies, as they typically are shallow and do not give a profile abnormality. Ulcers > 3 mm in depth are more commonly seen in Crohn's disease than in ulcerative colitis. Other descriptive terms have been used such as the "rose thorn" and "collar button " ulcers. Originally it was though that the rose thorn signified Crohn's and the collar button was specific for ulcerative colitis. It was then realized that these ulcers reflect depth; the rose thorn ulcer is a deeper ulcer which is typically seen in Crohn's disease, while the collar button ulcer is more shallow and thus seen in ulcerative colitis.

Aphthous ulcers can be detected in inflammatory colitidies (i.e. Shigellosis, amebic colitis) and therefore are not pathognomonic of Crohn's disease 44.

Cobblestoning

Cobblestoning is another radiographic feature which is very characteristic of Crohn's disease, and often considered pathognomonic (Fig 10). Cobblestoning consists of a combination of submucosal edema and deep transverse and longitudinal fissuring which collects barium. This combination gives an appearance similar to a cobblestone street.

Fistulae

Fistulae are a frequent complication of Crohn's disease. They may be grouped into three general categories: enterocutaneous, entero-enteric and fistulae involving the bowel and adjacent organs, such as the bladder (enterovesical) or psoas muscles.

Enterocutaneous fistula can be diagnosed using radiographic contrast studies and appear as extraluminal contrast collections. If an enterocutaneous fistula is suspected, water soluble contrast should be used, as barium may remain, coating the fistulous tract, indefinitely. The fistula can be visualized leading from the diseased contrast filled bowel loop to the skin surface. Cross-table lateral views may be necessary to visualize fistulae. In other cases, water soluble contrast can be directly injected into the skin opening. If the contrast fills a bowel loop, the presence of an enterocutaneous fistula is confirmed.

Entero-enteric fistula can also be diagnosed with contrast studies and requires careful attention to detail. Small bowel to small bowel fistulae are especially difficult to diagnose and demand vigorous compression and high quality radiographs. Fistula appear as linear contrast collections between bowel loops . When multiple, the fistulae can form a "star burst" pattern (Fig 11).

Enterocolic fistula are diagnosed when contrast appears in the colon prematurely during a small bowel series. For example, if contrast appears in the left colon before the right colon fills, there must be an entero-colic communication. Anovaginal, rectovaginal, rectourethral, gastrocolic, and duodenal colic fistulae have been reported 46-49. If a perianal fistula or a colorectal fistula is suspected, a single contrast water soluble enema is usually performed to demonstrate the fistula. Linear extraluminal collections of contrast may be seen in the pericolic tissues, sometimes opacifying adjacent structures (i.e. vagina).

Enterovesical fistula are difficult to demonstrate by conventional radiographic methods, but can be identified during a small bowel examination when contrast or air is identified within the bladder. However, CT is more sensitive50.

Polyps

Inflammatory polyps, postinflammatory polyps and pseudopolyps can all occur in Crohn's disease, although they are more common in ulcerative colitis. The colon is the most common location for polyps formation.

Inflammatory polyps can occur in the setting of any active inflammatory disease. Inflammatory polyps appears as polypoid fillings defects on contrast examinations which cannot be differentiated from adenomatous polyps . Endoscopy and biopsy is necessary for diagnosis.

Postinflammatory polyps can occur in Crohn's disease or ulcerative colitis and merely reflect previous extensive ulceration with sparing of some of the mucosa. Postinflammatory polyps form when extensive ulcerations heal, leaving a round or finger-like projection of submucosa covered by mucosa on all sides51 . They appear as multiple filiform filling defects on barium enema . Also, bridging post inflammatory polyps may be formed by ulceration undermining a patch of non-ulcerated mucosa.

Pseudopolyp is a term given to an area of inflamed mucosa surrounded by extensive ulceration. Due to the surrounding ulceration, this area may give the appearance of a filling defect or polyp. In Crohn's, pseudopolyps may occur in the small bowel or colon and when multiple may produce an appearance similar to true cobblestoning51 . Although pseudopolyps are benign, they may bleed and occasionally become so large that they obstruct the colon52.

Extraluminal Disease

CT is currently the imaging modality of choice for evaluation of extraluminal extent of disease in patients with Crohn's disease. However, extraluminal inflammatory masses can be suggested on small bowel series or barium enema when extrinsic compression of bowel is present. Similarly, the separation/displacement of small bowel loops may indicate the presence of adenopathy, mesenteric inflammation, mesenteric fatty replacement (creeping fat) or an interloop abscess. In addition, complications of Crohn's disease such as perforation or intussusception can be demonstrated on contrast studies, although CT examination is more sensitive ( see CT - complications).

Upper Gastrointestinal Tract

Esophagus

Crohn's disease of the esophagus is not common and only rarely occurs as an isolated finding. Crohn's disease elsewhere in the gastrointestinal tract is usually evident.

As in the small bowel and colon, aphthoid ulcers are the earliest radiographic findings in Crohn's disease of the esophagus and appear radiographically as punctate, linear or ring-like collections of barium with a radiolucent halo53. These ulcers can be subtle and will only be recognized with optimal double contrast technique.

As the disease progresses, the ulcers may enlarge and deepen (Fig 15). A diffuse esophagitis may occur and results in fold thickening or a diffusely cobblestoned mucosa54. Rarely intramural or extraesophageal fistula can occur. Progressive fibrosis can lead to esophageal stricturing55.

Filiform polyps have also been reported in the esophagus56. On occasion these have been very large, producing severe dysphagia.

Stomach

When Crohn's disease occurs in the stomach, it typically involves the antrum or body and antrum57. If the stomach is involved, the duodenum is also usually affected53.

Radiographic features of gastric Crohn's disease include, aphthous ulcers which tend to be localized to the antrum or body and antrum, fold thickening, larger ulcers or occasionally cobblestoning of the mucosa. Scarring and fibrosis may result in antral narrowing, which is often referred to as a "ram's horn"58 appearance (Fig 16). Fistulae involving the stomach are very rare but do occur53. Occasionally, a focal area of Crohn's may simulate a mass lesion.

Duodenum

The radiographic findings in Crohn's disease involving the duodenum are similar to those found else where and include, aphthous ulcers, larger ulcers, and fold thickening. The appearance may mimic peptic ulcer disease. As the disease progresses, there may be effacement of the mucosa, or stenosis due to fibrosis and scarring. If the scarring is asymmetric pseudodiverticula may be visualized59 (Fig 17).

CT Findings

Primary Disease

The most characteristic finding on CT in Crohn’s disease is wall thickening involving the distal small bowel and/or colon (Fig 18). Wall thickening can be diffuse or eccentric with skip areas. In advanced cases of Crohn’s disease the wall often measures greater than 1 cm in thickness60 (Fig 19). In a study by Philpotts et al, the mean colon wall thickness in Crohn colitis was 13 mm and the appearance was homogeneous. This was significantly greater than in ulcerative colitis, where the mean wall thickness was 7.8 mm and the appearance heterogeneous.61. Although wall thickening in Crohn's disease is commonly the result of submucosal inflammation, edema, fibrosis, or fat, hypertrophy of the muscularis propria also occurs. In cases of significant persistent segmental wall thickening, the possibility of stricture should be considered. In some patients, a layer (halo) of low density representing submucosal edema 62or fat deposition63 can be identified within the bowel wall (Fig 20). Although more commonly seen in patient's with ulcerative colitis, this submucosal halo can also be present in Crohn's disease. In addition to the bowel wall thickening, inflammatory stranding in the adjacent mesenteric or pericolonic fat can be present and usually signifies active inflammation (Fig 19).

It is important that CT scanning extend to the perineum, as perirectal-perianal abnormalities are demonstrated on CT in up to 37% of Crohn's patients.11 Findings include inflammation of perirectal fat, bowel wall thickening, fistulae or sinus tracts, and abscess.11 (Fig 21)

Mesenteric Disease

Another characteristic CT findings in patients with Crohn's disease is fibrofatty proliferation ("creeping fat"), which appears as an increased quantity of mesenteric fat which can be extensive (Fig 20). Fibrofatty proliferation can displace bowel and sometimes simulates a mass or abscess on plain abdominal radiographs or barium studies. Small mesenteric lymph nodes and mesenteric inflammation can also result in separation of bowel loops.

Intraabdominal abscess often appears as a soft tissue density or low density mass which often contains air and/or extravasated oral contrast (Fig 22). An abscess can be confined to the bowel wall, can extend into the mesentery, or can involve adjacent structures such as the bladder, psoas muscle, or pelvic sidewall (Fig 23). Percutaneous drainage of intraabdominal abscesses can be safely performed by the radiologist under CT guidance64.

Complications

Because CT can accurately demonstrate the bowel wall as well as extraluminal extension of disease, a variety of complications of Crohn’s disease can be effectively diagnosed with CT 65. In fact, CT was shown to affect patient management in 28% of patients with symptomatic Crohn's disease9 . In this study, in 22 of 80 patients, CT revealed previously unexpected findings which subsequently led to a change in medical or surgical management. These findings included fistulae, abscess, avascular necrosis of the femoral head, osteomyelitis, and venous thrombosis.

Complications commonly imaged with CT include:

(1) Obstruction

CT is valuable in patients with suspected small bowel obstruction, and can frequently determine the cause of obstruction and whether there is evidence of strangulation.66 (Fig 24) In patients with Crohn's disease, small bowel obstruction can result from stricture, inflammatory masses or adhesions following surgical resections. CT is also helpful in distinguishing obstruction from ileus.

(2) Fistulae

In addition to enterovesical fistulae, enterocutaneous, perianal, and rectovaginal fistulae can all be reliably detected with CT. They appear as extraluminal linear contrast collections with surrounding inflammation (Fig 25). If a rectovaginal or perianal fistula is suspected, contrast can be administered via the rectum for better visualization.

(3) Genitourinary complications.

CT is a sensitive method for evaluating the bladder and can reliably detect bladder involvement in Crohn's disease67 Bladder involvement may consist of focal bladder wall thickening with or without an adjacent extravesical soft tissue inflammatory mass50. Enterovesical fistula can also be imaged and appear as intravesical air, usually with associated bladder wall thickening and/or extravesical inflammatory mass50 (Fig 26). If an enterovesical fistula is suspected, intravenous contrast should not be administered. Then, if contrast is detected in the bladder, it must be oral contrast which entered the bladder though a enterovesical fistula.

Ureteral obstruction, commonly of the right ureter, can also result from mesenteric inflammation or abscess. This can easily be detected on CT performed with intravenous contrast.

(4) Cancer

Over the years, numerous studies have attempted to determine the relationship between Crohn's disease and the development of malignancies. A recent extensive review of the literature supports the concept that there is an increased risk of small bowel adenocarcinoma, colorectal cancer and possibly cholangiocarcinomas in patients with Crohn's disease.68 Although screening patients with Crohn's disease is controversial at this time, it is clear that CT should play an important role in cancer detection and staging (Fig 27).

Radiographic Findings in Ulcerative Colitis

Contrast Studies

Site of Involvement

Classically, ulcerative colitis involves the rectosigmoid colon and extends proximally, involving the colon continuously. Although the rectum appears radiographically normal in up to 20% of patients, rectosigmoid involvement is present in 95% of patients at proctosigmoidoscopy69. Isolated disease in the right colon does not occur.

The involved portions of the colon are symmetrically, concentrically diseased, which is distinct from the segmental, eccentric, and asymmetric pattern of involvement in Crohn's disease.

Terminal ileum disease is demonstrated in 10-25% of patents with ulcerative colitis69 and is often referred to as "backwash ileitis". Typically only a segment of ileum, usually the distal 5-25 cm. is involved and appears patulous and inflamed. Extensive ulceration or stricturing of the terminal ileum as seen in Crohn's disease, does not occur. This backwash ileitis only occurs in the presence of pancolitis and is though to be related to reflux of colonic contents into the small bowel.

COLON

Mucosal granularity

The earliest radiographically detectable evidence of disease in ulcerative colitis is a granularity of the colon surface which is associated with edema and hyperemia70 (Fig 28 and 29). The granular pattern is thought to result from abnormalities in the quality and quantity of mucus produced by the affected mucosa71. The granularity usually diffusely involves the affected portion of colon. This will be demonstrated on double contrast enema but will not be appreciated on single contrast studies which underestimate the extent of early disease.

Ulceration

Early ulcers in ulcerative colitis appear as fine speckled barium collections superimposed on a granular appearing mucosa. These fine ulcerations, also called mucosal stippling, may also produce a shaggy, spiculated contour to the bowel wall. This is sometimes best appreciated on the post-evacuation radiograph.

Although more characteristic of Crohn's or infectious colitis, discrete isolated ulcers can occur in patients with ulcerative colitis72. These small ulcers appear as small round contrast collections surrounded by lucent halos of edema. They are generally diffusely and symmetrically distributed over the involved region. This is in contrast to the ulcerations in Crohn's disease which are typically asymmetric and patchy in distribution. As the disease progresses, ulcerations can penetrate deeper into the wall of the colon and produces a variety of sizes and shapes. When the ulceration undermines the submucosal layer, a collar button ulcer can be seen71. However, the collar button ulcer is not unique to ulcerative colitis (Fig 30).

Folds

Early in ulcerative colitis, haustral folds appear thickened and nodular due to inflammation and edema. However, as the disease progresses, the haustral fold become blunted or may be completely lost due to relaxation of the taeniae coli muscle 73 (Fig 30) The haustra may reappear after the colon has healed and the taeniae have regained tonus73, 74.

Colonic shortening

Colonic shortening, as demonstrated by barium enema is characteristic of ulcerative colitis (Fig 30). The exact cause of the shortening has not been ascertained. However, Gore believes that the shortening may be produced by thinning and relaxation of the muscularis mucosae in conjunction with luminal narrowing and loss of haustra 74.

Polyps

Postinflammatory polyps can occur in patients with ulcerative colitis and appear as multiple thin filiform filling defects on barium enema (Fig 13). In most cases when postinflammatory polyps are present, there is no evidence of active colitis. Postinflammatory polyps are benign and are not associated with malignant transformation.

Pseudopolyps, areas of inflamed mucosa surrounded by extensive ulceration, also occur in patients with severe ulcerative colitis.

Stricture

Colonic strictures are not uncommon in patients with ulcerative colitis, and are usually associated with longstanding total colonic disease. The rectum and sigmoid are most commonly involved75.(Fig 28). Most of the narrowings seen in ulcerative colitis are benign and in most cases are due to smooth muscle hypertrophy and are therefore potentially reversible75.

On barium enema, a stricture appears as a symmetric segment of narrowing with tapered margins. However, due to the fact that carcinoma in ulcerative colitis tends to be plaque-like and flat rather than polypoid in appearance, narrowings detected on barium enema in patients with ulcerative colitis are referred for colonoscopy and biopsy to confirm or deny the possibility of cancer.

Dysplasia

Mucosal dysplasia is a premalignant histologic condition which occurs in the colon of patients with ulcerative colitis. It is usually diagnosed on surveillance biopsy, as it frequently is not recognized grossly at colonoscopy76.

Mucosal dysplasia has been detected using double contrast barium enema, although not consistently77-79 According to Frank et al, dysplasia may appear as an irregular area of nodularity with sharply angled edges (Fig 28). Other authors have described fine granularity, minute spiculations or a reticular mucosa pattern78 If the double contrast barium enema detects possible dysplasia, that area can be targeted for colonoscopy and biopsy. However, barium enema is not considered a sensitive method for dysplasia detection, and regular colonoscopy and biopsy is the recommended surveillance regimen.

Colon cancer

The association of chronic ulcerative colitis and the development of colorectal cancer is well known. The carcinoma which develops is often flat and infiltrating and can be difficult to detect on barium enema 80, 81 (Fig 32). Some carcinomas may infiltrate the submucosa and muscular wall without demonstrating a significant mucosal or intraluminal component. This type of lesion can produce very subtle contour abnormalities or luminal narrowing . Therefore, at barium enema any non distensible segment of colon should be referred for endoscopy and biopsy.

Toxic dilatation

Toxic dilatation of the colon is a serious, life threatening complication of inflammatory bowel disease. It is most commonly recognized as a complication of ulcerative colitis , although it may occur in Crohn's disease or infectious colitis. Toxic dilatation is the result of acute transmural inflammation and is usually associated with fever, elevated sedimentation rate and leukocytosis.

Radiographically, the most prominent radiographic feature of toxic megacolon is dilatation of the colon, most commonly observed in the transverse colon, the most anterior portion of the colon in the supine position. The average width of the transverse colon in toxic megacolon is >9 cm, compared with the normal transverse colon which measures <6 cm82. In addition to the dilation, the haustral folds are typically edematous , giving the bowel wall a nodular contour.

The diagnosis of toxic megacolon is usually made on plain films of the abdomen (Fig 33). By repositioning the patients and redistributing the air column, different portions of the colon can be evaluated. Because the colon is acutely inflamed and at risk for perforation, a contrast enema is contraindicated. Plain films at 12 hour intervals (or more frequently depending of the patient's clinical condition) should be taken to monitor the size of the bowel lumen and to check for pneumoperitoneum. Bowel perforation may be silent as the patient is typically on high dose steroids to reduce the inflammation of the bowel.

Ileal Pouch-Anal Anastomosis

The ileal pouch is a well accepted surgical option for patients who require a total colectomy for chronic ulcerative colitis or familial adenomatous polyposis. The surgery consists of the construction of an ileal reservoir which is anastomosed to the anus after total colectomy. This avoids the creation of a permanent external stoma and usually results in good functional results. The procedure is associated with a variety of complications which can be effectively imaged using contrast radiography.

Radiographic examination of the ileal-anal pouch is routinely performed to exclude leakage and evaluate pouch size and function (Fig 34). At our institution, the reservoir examination is performed in a retrograde fashion through a 12F red rubber catheter using thin barium or water-soluble contrast. Anteroposterior, oblique and lateral spot radiographs of the distended pouch are obtained. Post evacuation anteroposterior and lateral radiographs are also taken. If functional measurements are desired, a simple radiographic evaluation of ileoanal pouch volume can be performed83. With this technique, barium is instilled into the pouch via the rectum while the patients is in the standing position. The total volume infused, volume until reflux into the small bowel and volume voided can be measured. This test gives useful information about pouch performance and spasticity.

Complications which can be diagnosed with pouch contrast radiography include small bowel obstruction, pouch fistula, anastomotic leak, pouchitis, and stricture84.

Continent ileostomy is an alternative to the ileal pouch procedure85. An ileal reservoir is created and then an intussusception created at the stoma itself, resulting in a one way valve effect. The patient can intubate the pouch at regular intervals to empty the reservoir of fluid.

CT

Primary Disease

UC is typically left sided or diffuse, and only rarely involves the right colon exclusively. On CT scan , the most frequent finding is colonic wall thickening, which is present in up to 75% of patients and has a mean thickness of 7.8 mm60, 61. This is significantly less thick than Crohn's disease. The bowel wall thickening in UC is diffuse and symmetric, while Crohn's disease classically appears irregular and asymmetric, due to the transmural nature of the disease (Fig 35). Ulcers, as documented on endoscopy or barium studies, are not typically visualized on CT due to the spatial resolution.

The attenuation of the thickened bowel wall in ulcerative colitis is typically more heterogeneous than in Crohn's disease 61. The halo sign, a low attenuation ring in the bowel wall due to deposition of submucosal fat63, or edema62 may be present. Submucosal fat deposition is seen more commonly in UC than Crohn’s colitis and can be especially dramatic in the rectum (Fig 36). It has not been observed in the acute colitides such as pseudomembranous colitis, ischemic colitis or infectious colitis61. However, submucosal edema has been seen in patients with graft vs. host disease and viral enteritis86.

Other features which can help distinguish UC from Crohn's is the lack of small bowel involvement, abscess, or mesenteric fibrofatty proliferation which are all characteristic findings in Crohn's disease . In addition, rectal and perirectal abnormalities are often prominent features of UC. Marked rectal wall thickening can be seen which results in luminal narrowing (Fig 37). Also, prominent perirectal fibrofatty proliferation and widening of the presacral space has been reported in UC (Fig 36), as well as in Crohn's, pseudomembranous colitis, radiation colitis, pelvic lipomatosis, etc87.

Complications

Toxic Megacolon

Toxic megacolon is a severe, life threatening fulminant transmural colitis most commonly associated with UC. The patient typically presents with profuse bloody diarrhea, abdominal pain, fever and leukocytosis. On CT, there is distention of the colon, most commonly involving the transverse colon which contains large amounts of fluid and air. The haustra appear edematous and distorted, or may be absent. The presence of pneumatosis signifies ischemia and necrosis. The major complication of toxic megacolon is perforation with resulting sepsis, shock and possibly death. Perforation can be detected as extraluminal air on plain films and CT.

Malignancy

This association of UC with colorectal cancer is well established. CT is particularly valuable for characterization of primary colonic malignancies and remains the study of choice for the staging of colonic malignancies, as it can reliably demonstrate regional extension of tumor and well as adenopathy and distant metastases.

On CT, adenocarcinoma of the colon usually appears as a soft tissue attenuation mass with irregular borders. Larger masses may have a low density necrotic center, or occasionally may contain gas, resembling an abscess. Rectal cancers may appear as asymmetric wall thickening which narrows the lumen.

CT is able to detect extension of tumor into the pericolonic fat, invasion of adjacent organs such as bladder or pelvic muscles, and adenopathy. CT is the study of choice for the detection of liver metastases, which will appear as multiple hypodense lesions within the liver after injection of intravenous contrast.

Extraintestinal Complications of Inflammatory Bowel Disease

Patients with inflammatory bowel disease experience a variety of extraintestinal complications which can result in considerable morbidity and in some cases mortality. Many of these conditions are encountered by radiologists.

For instance, musculoskeletal complications such sacroiliitis, arthritis, osteoporosis, and osteomyelitis can be effectively imaged with plain radiographs, bone scintigraphy and MR. Hepatobiliary conditions including fatty infiltration, sclerosing cholangitis, cholangiocarcinoma and cholelithiasis can be evaluated with CT, MR , US and/or cholangiography. Radiologists must be familiar with these and the many other associated multisystem complications.

Conclusion

Although contrast studies remain the principal tools for the diagnosis and evaluation of suspected inflammatory bowel disease, other imaging modalities are now playing a larger role. CT, in particular, is useful for evaluation of extraluminal alxtent of disease, and for complications. In addition, since CT plays an important role in the evaluation of patients with abdominal pain, it may be the initial imaging study performed in patients with inflammatory bowel disease.

In summary, the diagnosis and management of inflammatory bowel disease is complex and requires the cooperation of many medical specialties. Radiologists continue to play a vital role in the evaluation of Crohn's disease and ulcerative colitis, as radiographic studies are considered complementary to endoscopy.