CT of Bowel Wall Thickening: Significance and Pitfalls of Interpretation

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1 CT of owel Wall Thickening: Significance and Pitfalls of Interpretation C T has become the most important imaging technique for evaluating the abdomen and pelvis. CT is used to examine patients with acute abdominal complaints, known or suspected malignancy, abdominal and pelvic trauma, and inflammatory conditions. When CT images of the abdomen and pelvis are interpreted, the focus is often placed on the peritoneal cavity, the mesentery, and the parenchymal organs. common misconception is that CT provides only limited information with respect to the gastrointestinal tract. In fact, recent technologic advances and accumulated experience in image interpretation suggest that substantial information regarding gastrointestinal tract disorders can be obtained. Normal variants as well as abnormal conditions may cause thickening of the bowel wall. In this review, the normal CT appearance of the bowel wall and the different causes of bowel wall thickening will be described. The various criteria that allow one to differentiate normal variants and abnormal conditions are reviewed, including attenuation pattern of bowel wall thickening; degree of bowel wall thickening; circumferential symmetric thickening versus asymmetric thickening; focal, segmental, or diffuse involvement; and associated perienteric abnormalities. Normal Gastrointestinal Tract The normal small-bowel wall is thin, measuring between 1 and 2 mm when the lumen is well distended (Fig. 1). However, the thickness of the normal small-bowel wall varies slightly depending on the degree of luminal distention. s a result, different criteria have been used to diagnose small-bowel wall thickening [1 6]. When the lumen of the small bowel is distended, the wall is often not seen. If the bowel is partially collapsed, the wall measures between 2 and 3 mm and is of symmetric thickness. In these cases it is important to compare the degree of thickness of similarly distended segments to exclude disorders. measurement of 2 3 mm as the upper limit of normal thickness has been used by some authors [3, 4]. Others have advocated any perceptible thickening to indicate disorders [5, 6]. However, potential pitfalls exist with this latter approach. We have observed that when the normal small bowel is filled with water, its wall may appear thicker (Fig. 2). In case of uncertainty regarding the presence of a disease process, a smallbowel series should be performed. Fig. 1. Normal enhancement and appearance of small bowel in 77-year-old woman. xial CT scan obtained at level of kidneys with IV contrast material and water as oral contrast agent shows enhancement of normal bowel wall. Note thinly enhancing valvulae conniventes (arrow ). This finding is often better seen when water alone is given as oral contrast agent. Enhancement may be obscured with positive contrast in lumen. Review Michael Macari 1 and Emil J. althazar The normal thickness of the colonic wall varies greatly depending on the degree of distention. When the colon is distended, the wall should measure less than 3 mm; it is often imperceptible [7]. Frequently, because of fecal contents, fluid, or colonic redundancy, the true thickness is difficult to ascertain. Carefully following the colonic wall to a region where the colon is well distended with gas will often reveal the true thickness (Fig. 3). The normal bowel wall enhances after an adequate bolus of IV contrast material (Fig. 1). The enhancement is often more easily identified in patients who have been given water as an oral contrast agent. In these cases, the enhancing bowel wall is well depicted adjacent to the low-attenuation fluid in the lumen. Enhancement is usually greater on the mucosal aspect of the bowel wall. This enhancement should not be mistaken for a disease process. Recognizing that the wall is not thickened and Received June 27, 2000; accepted after revision November 1, oth authors: Department of Radiology, NYU Medical Center, Tisch Hospital, 560 First ve., Ste. HW 207, New York, NY ddress correspondence to M. Macari. JR 2001;176: X/01/ merican Roentgen Ray Society JR:176, May

2 Macari and althazar that no perienteric inflammation is present will allow one to differentiate normal enhancement from a disease process. owel Wall Thickening owel wall thickening may be related to a number of entities, including normal variants, inflammatory conditions, and neoplastic disease. The CT findings that need to be analyzed when assessing thickened bowel include pattern of attenuation; degree of thickening; symmetric versus asymmetric thickening; focal, segmental, or diffuse involvement; and associated perienteric abnormalities. Evaluation of these parameters, which are reviewed in the following text, will lead to a more accurate differential diagnosis. Fig. 3. Normal colonic wall thickness in 81-year-old woman with breast cancer. Contrast-enhanced axial CT scan of cecum suggests bowel wall thickening with target appearance (arrow ). However, ventral wall is thin, without target appearance (arrowhead ). Occasionally, residual fluid in bowel can mimic submucosal edema and bowel wall thickening, as in this case. Identifying focal area of distention without adjacent fluid will clarify wall thickness. Fig. 2. Perceived pitfall in interpretation of bowel wall thickening caused by mixing of water and oral contrast material in 47-year-old man with history of lymphoma., xial CT scan through upper abdomen shows apparent homogeneous circumferential thickening of wall of jejunum loops (arrow ), a finding suspicious for lymphoma., Radiograph from upper gastrointestinal series performed 2 days after shows normal small bowel (arrow). ttenuation of the Thickened owel Wall The attenuation pattern of a thickened segment of bowel wall is an important criteria for establishing a differential diagnosis. In most cases, the attenuation pattern of a thickened bowel wall is directly related to the administration of IV contrast material (Fig. 4). If IV contrast material is not administered, most cases of bowel wall thickening will show homogeneous attenuation. Two notable exceptions to this are the presence of central fat deposition and intestinal pneumatosis (Figs. 5 and 6). In these cases, variations in attenuation of the bowel wall can be depicted on CT without IV contrast material because of the marked differences in tissue attenuation. The presence or absence of enhancement can be evaluated in a number of ways, including comparing the attenuation of the thickened segment with other segments of bowel, comparing unenhanced and contrast-enhanced scans, or, if unenhanced images are not available, obtaining delayed images. fter IV contrast material administration, there are two Fig. 4. Target sign detected only after IV contrast administration in 64-yearold man with pain and bloody diarrhea., CT scan obtained without IV contrast material shows moderate circumferential thickening of sigmoid colon (arrow ). ttenuation of bowel wall is homogeneous. Without IV contrast material, further characterization is not possible., Contrast-enhanced axial CT image obtained 48 hr after at same level shows thickened sigmoid with target configuration (arrow). Findings suggest inflammation or ischemia. Endoscopy and biopsy confirmed ischemic colitis JR:176, May 2001

3 CT of owel Wall Thickening Fig. 5. Deposition of fat in submucosa producing target sign in 85-year-old man with history of chronic ulcerative colitis. Contrast-enhanced axial CT scan of rectum shows target configuration with central low attenuation in submucosa (arrow ). Central low attenuation is same density ( 80 H) as surrounding perirectal fat, indicating submucosal fat deposition. Patient was asymptomatic at time of examination. distinct patterns of bowel wall attenuation: homogeneous and heterogeneous (ppendix 1). Homogeneous ttenuation The differential diagnosis of a thickened bowel wall that shows homogenous attenuation on CT includes submucosal hemorrhage or hematoma [8, 9], infarcted bowel [10, 11], neoplasm [12 15], chronic Crohn s disease [3], radiation injury [10], and pseudothickening related to incomplete distention and residual fluid [1]. Submucosal hemorrhage. The diagnosis of submucosal intestinal hemorrhage is usually made when CT depicts circumferential and symmetric bowel wall thickening in patients who are undergoing anticoagulation therapy or who have an underlying bleeding diathesis (Fig. 7). On CT, most cases of submucosal hemorrhage show homogeneous high attenuation of the thickened segment and lack of enhancement [8, 9]. Patients often have a history of coagulopathy and, in most cases, the small bowel is affected in a segmental distribution [9]. In patients with suspected submucosal hemorrhage, an unenhanced CT examination is often helpful in establishing the diagnosis by showing high attenuation in the thickened segment [8, 9]. The high attenuation is due to acute bleeding in the bowel wall. Ischemia and infarction. The appearance of the gastrointestinal wall varies on IV contrast-enhanced CT as the bowel wall progresses from ischemia to infarction. When the wall is ischemic, it is often circumferentially thickened and may contain a target or halo configuration of attenuation [9, 10] (Fig. 8). In other cases of ischemic bowel, the wall is thickened and no enhancement is identified [10, 11]. In these cases, homogeneous attenuation of the bowel wall will be seen. Detecting lack of enhancement can be difficult, but comparing adjacent loops helps to show this finding [11] (Fig. 9). In our experience, complete lack of enhancement is rarely identified in these patients. Etiologies of ischemia and infarction include thromboembolism, low flow (related to poor cardiac output), and strangulation obstruction [10]. Chronic Crohn s disease and chronic radiation changes. Chronic Crohn s disease and chronic radiation enteritis may show homogenous attenuation on contrast-enhanced CT [3, 10]. In patients with long-standing Crohn s disease or radiation injury, transmural fibrosis develops. In the chronic phase, the typical findings on IV contrast enhanced CT of a target appearance are no longer present [3, 10]. Neoplasm. Gastrointestinal neoplasms can present with homogeneous attenuation of the thickened segment on contrast-enhanced CT [12 14]. In these instances, other criteria (degree, symmetry, length of involved segment, and associated perienteric abnormalities) are important in establishing the correct diagnosis. In cases of neoplasm, homogeneous attenuation correlates with size of the tumor [15]. Smaller tumors present either as circumferential areas of bowel wall thickening or as asymmetric areas of bowel wall thickening with homogeneous enhancement (Fig. 10). Small-bowel lymphoma is often depicted on CT as a segmental area of circumferential thickening with homogeneous attenuation and enhancement [12, 14]. recent study found that in 33 (72%) of 46 patients with small-bowel lymphoma, the involved bowel showed single or multiple focal areas of gross circumferential wall thickening with homogeneous attenuation [14] (Fig. 11). Pitfalls. Residual fluid within the lumen coating the mucosa of the bowel wall may be perceived as a thickened segment without enhancement (Fig. 2). In these cases, a disease process may be difficult to exclude, and correlation with a small-bowel series may be needed [1]. Fig. 6. Improved detection and evaluation of intramural air with wide window and low level settings in 34-year-old woman with IDS and diarrhea., Contrast-enhanced axial CT scan (window width and level, 420 and 30 H) at level of cecum shows gas surrounding cecum (arrow )., Same CT slice as (window width and level, 1550 and 460 H, respectively) better shows that central low attenuation (gas) is in wall (arrow ) of cecum, which is compatible with pneumatosis. Patient was treated with antibiotics, improved within a week, and did not require colectomy. JR:176, May

4 Macari and althazar Fig. 7. Intramural hemorrhage in 64-year-old man with bowel wall thickening (homogeneous attenuation). Contrast-enhanced axial CT scan of abdomen shows segmental circumferential thickening with homogeneous attenuation of a loop of jejunum (arrow ). Differential diagnosis includes hemorrhage, ischemia, and lymphoma. ecause of history of anticoagulation therapy and abrupt onset, hemorrhage is most likely. Unenhanced study can better define high attenuation. Heterogeneous (Stratified) ttenuation Heterogeneous attenuation is the second pattern that may be depicted in a thickened segment of bowel wall. When the attenuation of a thickened bowel wall is heterogeneous, the wall may display a stratified pattern or a mixed pattern of attenuation. Recognizing alternating (stratified) layers of attenuation in a thickened segment of bowel wall helps in the differential diagnosis. The stratified pattern may be in the form of a double halo or a target configuration. The double halo sign consists of an inner low-attenuation (edema) ring surrounded by an outer higher attenuation ring. In the target sign, inner and outer layers of high attenuation surround a central area of decreased (edema) attenuation [1]. These signs are best visualized during the late arterial and early portal venous phases of IV contrast material enhancement [1]. On unenhanced or delayed (>2 min) IV contrast enhanced CT, these signs may not be visualized (Fig. 4). The high attenuation present with these signs is related to hyperemia [1]. Inflammation and ischemia. The double halo and target signs have similar significance in that they usually indicate an acute inflammatory or ischemic condition. The double halo sign was first reported by Frager et al. [16] in patients with Crohn s disease. In addition to Crohn s disease, this pattern of attenuation may be present in ulcerative colitis, infectious enterocolitis, radiation enteritis, vasculitis, lupus erythematosus, and bowel edema in patients with cirrhosis [1, 3, 16 39] (Figs ). The finding of stratified attenuation in a thickened segment, although nonspecific, is used mainly to exclude malignant conditions. Correlation with clinical history and associated findings on CT related specifically to the bowel wall and the surrounding mesentery may allow one to narrow the differential diagnosis. Fig. 8. Ischemic bowel with mural thickening and target configuration of attenuation in 71-year-old woman., Contrast-enhanced axial CT scan at level of terminal ileum shows circumferential small-bowel wall thickening with target configuration (arrow )., Contrast-enhanced axial CT scan at level of superior mesenteric artery shows intraluminal filling defect (arrow ) consistent with mural thrombus. Thrombus was confirmed at follow-up angiography. Neoplasm. notable exception to this accepted general rule (target sign = inflammation) is the rare occurrence of this sign in infiltrating scirrhous carcinoma of the stomach and colon. Rigidity (after attempted air insufflation), severe luminal narrowing, abrupt transition, and regional lymphadenopathy usually help in establishing the correct diagnosis. Pitfalls. potential pitfall may arise when residual fluid and oral contrast material fill the bowel lumen to mimic a target sign [2]. Seeing that the bowel is partially filled with fluid and that adjacent areas of the bowel are well distended with gas will usually allow these pitfalls to be recognized (Fig. 3). Moreover, usually no perienteric disease is associated with these fluid-filled segments, which also tends to exclude an acute inflammatory process. The deposition of submucosal fat in the large and small bowels has been documented in patients with both acute and chronic inflammatory disorders of the bowel [40, 41]. One study found submucosal fat deposition in 61% of patients with ulcerative colitis but in only 8% of patients with Crohn s disease [23]. lthough a stratified pattern of attenuation is present with submucosal fat deposition, recognizing the very low attenuation (negative Hounsfield unit value) of the submucosa will allow an accurate diagnosis to be established (Fig. 5). Finally, pneumatosis may present as a striated pattern of attenuation [42]. Occasionally, small amounts of gas may be overlooked when CT Fig. 9. Closed-loop small-bowel obstruction with ischemic bowel in 83-year-old woman. Contrast-enhanced axial CT image at level of pelvis shows typical configuration of closedloop obstruction with dilated small-bowel loops in radial distribution, minimal to no mural thickening, and homogeneous attenuation (open arrows). Note loops in closed-loop obstruction do not enhance to same degree as loops not in closed loop (solid arrow ), suggesting ischemia. Ischemic bowel with infarction was present at subsequent surgery JR:176, May 2001

5 CT of owel Wall Thickening Fig. 10. Well-differentiated adenocarcinoma in 26-year-old man with bowel obstruction. Contrast-enhanced axial CT scan at level of cecum shows homogeneous attenuation (enhancement) of circumferentially thickened cecum (straight arrows). Small amount of fluid is seen in lumen (arrowhead ). Note multiple obstructed loops of small bowel with air fluid levels (curved arrow ). Surgery revealed well-differentiated adenocarcinoma of cecum. Fig. 12. Target sign in 35-year-old woman with history of ulcerative colitis. Contrast-enhanced axial CT image of rectum shows mild wall thickening with classic target appearance and inner enhancement of mucosa (short white arrow ) and outer enhancement of muscular layer (long white arrow ) surrounding low-attenuation edematous submucosa (black arrow ). scans are viewed at standard abdominal window and level settings (Fig. 6). In these cases, viewing the scans at wider window and lower level settings facilitates visualization of the gas. ir trapped between the bowel wall and residual fluid in the lumen may mimic pneumatosis (Fig. 15), which usually occurs in the cecum or stomach. In these cases, the perceived pneumatosis will be seen on the dependent aspect of the bowel where the residual fluid is present. Recognizing that the more ventral aspect of the bowel wall does not show the appearance will usually allow this pitfall to be avoided. Heterogeneous (Mixed) ttenuation The final category of attenuation pattern in thickened bowel is mixed attenuation. In these cases, the grossly thickened bowel wall shows several irregular zones of lower attenuation haphazardly located adjacent to areas of higher attenuation. The findings are related to ischemia and necrosis and are seen in high-grade, poorly differentiated gastrointestinal neoplasms such as adenocarcinoma and stromal cell tumors. Larger tumors frequently undergo central necrosis and will show heterogeneous enhancement on contrast-enhanced scans. This Fig. 11. Lymphoma of small bowel in 30-year-old man. Contrast-enhanced axial CT image of mid abdomen shows homogeneous attenuation (enhancement) of markedly thickened small bowel (arrows). Thickening involves a short segment of small bowel. Despite smallbowel thickening, mild dilatation of lumen is seen. Findings are strongly suggestive of small-bowel lymphoma. Note retroperitoneal lymphadenopathy (arrowhead ). iopsy revealed non-hodgkin s lymphoma. Fig. 13. Target sign in 37-year-old man with history of acute Crohn s disease. Contrast-enhanced axial CT image shows marked circumferential thickening of terminal ileum. Target appearance is present, with enhancement of mucosa (short arrow ) and outer enhancement of muscular layer (long arrow ) surrounding low-attenuation edematous submucosa (arrowhead ). heterogeneous enhancement is seen in large tumors and is related to rapid growth, ischemia, and necrosis. Mucinous adenocarcinomas often contain poorly defined central areas of low attenuation related to intracellular tumor mucin deposition and may show heterogeneous attenuation after contrast administration (Fig. 16). Degree of owel Wall Thickening The second variable that aids in establishing a differential diagnosis when evaluating bowel wall thickening is the degree of thickening (ppendix 2). Entities that cause mild bowel JR:176, May

6 Macari and althazar Fig. 14. Target sign in 37-year-old woman with history of lupus erythematosus. Contrast-enhanced axial CT image at level of mid abdomen shows diffuse marked circumferential thickening of colon. Target appearance is present, with enhancement of mucosa (short white arrow) and outer enhancement of muscular layer and serosa (long white arrow ) surrounding low-attenuation edematous submucosa. Small amount of ascites is present (arrowhead ). wall thickening (1 2 cm) often overlap and include inflammatory conditions and neoplasms. In general, benign conditions result in bowel wall thickening of less than 2 cm, whereas wall thickening greater than 3 cm is usually present in neoplastic conditions [1, 12, 14, 43]. Mild Thickening In cases of mild bowel wall thickening, a nonneoplastic (inflammatory or infectious) condition is usually present. Two of the more common inflammatory conditions of the bowel are ulcerative colitis and Crohn s disease. ecause the disease process is limited to the mucosa in patients with ulcerative colitis and is often transmural in Crohn s disease, bowel wall thickening is usually greater in Crohn s disease. One study found the mean thickness of the colon wall in Crohn s disease was 11.0 mm compared with 7.8 mm in patients with ulcerative colitis [23] (Figs. 12 and 13). In most cases of intestinal infection involving the small bowel, the wall is either normal or mildly thickened. Marked Thickening Infection and inflammation. With severe infections of the colon, the wall may become markedly thickened by edematous haustral folds (up to 2 cm or even greater) (Fig. 17). On CT, the finding of barium trapped between these folds is known as the accordion sign [24] (Fig. 18). The accordion sign has been detected in 4 19% of patients with documented Clostridium difficile colitis and has been considered specific [24 26]. However, other causes, especially cytomegalovirus in IDS patients, as well as a variety of other infectious and inflammatory conditions, have shown massive colonic wall thickening and a similar mucosal pattern to that shown by the accordion sign [27, 28] (Fig. 14). The usefulness of the accordion sign relates to the depiction of severe submucosal edema in a segmental or diffuse colitis caused by either an infection or ischemia. Neoplasm. Primary intestinal neoplasms often present as short segments of bowel wall thickening (Fig. 10). Sarcoma (gastrointestinal stromal tumors) usually presents as a bulky exophytic mass with heterogeneous attenuation (Fig. 19). Small-bowel lymphoma rarely obstructs the lumen, and it often presents as a Fig. 15. Intraluminal air mimicking pneumatosis in 58-year-old man. Unenhanced axial CT scan at level of stomach shows gas (arrow ) between wall of stomach and residual gastric fluid mimicking pneumatosis. Note pneumobilia (arrowhead ) from previous procedure. Fig. 16. Heterogeneous low-attenuation enhancement in mucinous adenocarcinoma with irregular circumferential bowel wall thickening in 64- year-old man with abdominal pain. Contrast-enhanced axial CT image of splenic flexure shows irregular wall thickening (arrows) with heterogeneous areas of low attenuation in colon wall (arrowhead ). Large mucinous adenocarcinoma was found at surgery JR:176, May 2001

7 CT of owel Wall Thickening Fig. 17. Diffuse marked colonic thickening with target appearance in pseudomembranous colitis in 18-year-old woman with diarrhea. Contrast-enhanced axial CT image of mid abdomen shows diffuse marked circumferential wall thickening of cecum and descending colon with target appearance (arrows). Findings are consistent with inflammatory colitis; stool was positive for Clostridium difficile cytotoxin. markedly thickened segment ranging from 1.5 to 7 cm (mean, 2.6 cm) [14] (Fig. 11). Fig. 19. Exophytic intestinal mass in 84-year-old man with bowel obstruction. Contrast enhanced axial CT image shows large bulky exophytic mass extending from jejunum with heterogeneous attenuation (white arrows). Small bubble of gas is present in mass (black arrow ), suggesting fistula in bowel. Surgery revealed malignant gastrointestinal stromal tumor. Symmetric Versus symmetric Thickening nother feature to evaluate in cases of bowel wall thickening is whether the involved segments are symmetrically or asymmetrically thickened (ppendix 3). Symmetric thickening is present when the involved segment shows the same degree of thickening throughout the circumference of the abnormal segment. symmetric thickening relates to different degrees of eccentric thickening around the circumference of the involved segment. Symmetric thickening is seen in intestinal inflammatory conditions, infections, bowel edema, and ischemia [1] (Figs ). In addition, the bowel is usually symmetrically thickened in cases of submucosal hemorrhage [8, 9] (Fig. 7). Some neoplasms may also display symmetric thickening, especially scirrhous carcinoma and, occasionally, lymphoma [1, 14] (Fig. 11). symmetric or eccentric bowel thickening is mainly seen with malignant conditions. n exception to this is cases of long-standing Crohn s disease in which the bowel may be asymmetrically thickened. Usually, associated mesenteric findings will help establish the diagnosis of Crohn s disease in these cases. Most neoplasms present with asymmetric thickening, including stromal tumors, adenocarcinoma, carcinoids, metastases, and, occasionally, lymphoma. bulky exophytic mass is usually present in patients with gastrointestinal stromal tumors, metastases, and, occasionally, lymphoma. Irregular short asymmetric lesions with abrupt margins are the hallmark Fig. 18. ccordion sign in 44-year-old man with diarrhea and Clostridium difficile colitis. Contrast-enhanced axial CT image of mid abdomen shows marked thickening of haustra (arrowheads). arium (arrow ) trapped between thickened haustra mimic appearance of accordion. of primary intestinal adenocarcinoma and metastatic disease [12] (Fig. 20). Focal, Segmental, or Diffuse owel Wall Thickening and Location The extent and location of bowel wall involvement should be evaluated. It is important to determine if the bowel wall thickening is focal (a few centimeters), segmental (10 30 cm), or diffuse (involving most of the small bowel or colon). lthough inflammatory or neoplastic conditions may overlap in the length of involvement, the analysis helps in narrowing the differential diagnosis (ppendix 4). With few exceptions, long segments of involvement are seen in benign conditions. Focal Involvement Focal thickening is seen in both benign and malignant processes. Most neoplasms of the gastrointestinal tract present as a focal area of bowel wall thickening (Figs. 10 and 20). Inflammatory processes that may present as focal areas of bowel wall thickening include diverticulitis, appendicitis, and, occasionally, tuberculosis. Segmental Involvement segmental distribution of involvement is usually caused by an inflammatory process. Conditions associated with segmental involvement include Crohn s disease, infectious ileitis, radiation enteritis, and ischemia [1, 38]. Other considerations for segmental involvement include intramural hemorrhage and lymphoma (Figs. 7 and 11). JR:176, May

8 Macari and althazar Diffuse Involvement Diffuse thickening of the bowel wall is seen with a variety of inflammatory conditions, including ulcerative colitis, infectious enteritis, edema from low-protein states, portal hypertension associated with cirrhosis, and low-flow ischemia [30, 32, 33, 39] (Fig. 21). Segmental or diffuse thickening may be seen in patients with small-bowel vasculitis, as often occurs in systemic lupus erythematosus [35 37] (Fig 12). Fig. 20. CT scans of focal asymmetric thickening in 59-year-old man show importance of rectal distention., xial scan at level of rectum shows lack of distention (arrow ), which limits the examination., xial scan at same level as performed after administration of rectal air shows focal asymmetrically thickened ulcerated mass (arrow ) on nondependent wall of rectum. iopsy revealed rectal adenocarcinoma. Fig. 21. Diffuse mild colonic wall thickening in 35-year-old woman. Contrast-enhanced axial CT image shows mild circumferential wall thickening of ascending and descending colons (arrows). Diffuse mild colitis suggests infection or ulcerative colitis. Endoscopy revealed ulcerative colitis. ssociated bnormalities Last, a major advantage of CT over endoscopy or barium studies is the ability of CT to show extraintestinal manifestations of disease. These associated findings include lymph nodes; mesenteric stranding and calcification; abscess, sinus tracts, and fistulas; proliferation of fat; vascular occlusion; and solid organ abnormalities. Lymph Nodes The number, size, location, and attenuation of lymph nodes in the abdominal and pelvic cavities are important associated findings when examining patients with thickened bowel [43 46]. ttenuation. The attenuation of lymph nodes and the presence or absence of calcification should be evaluated [45, 46]. Low-attenuation lymph nodes with a rim of contrast enhancement or calcified lymph nodes should alert one to the possibility of tuberculosis, other mycobacterial infections, or histoplasmosis (Fig. 22). In a patient with IDS, the presence of high-attenuation lymph nodes suggests the possibility of Kaposi s sarcoma. In this condition, the lymph nodes are hyperemic and will show enhancement during CT performed with IV contrast material. Neoplasm. On CT, focal colonic wall thickening may present a challenge in the differential diagnosis. When present, especially in the sigmoid or descending colon, the main differential diagnosis is adenocarcinoma versus diverticulitis (Fig. 23). recent study found that pericolonic lymph nodes adjacent to the focal area of colonic thickening are more commonly seen in patients with colon cancer. Pericolonic inflammatory changes are more commonly seen in diverticulitis [43]. In addition to low-attenuation lymph nodes caused by tuberculosis, metastatic lymphadenopathy from mucinous tumors of Fig year-old woman with low-attenuation caseating lymph nodes in intestinal tuberculosis., Contrast-enhanced axial CT image of cecum shows irregular focal thickening (arrow ) with associated small regional lymph nodes (arrowhead ). Findings mimic cecal carcinoma., Contrast-enhanced axial CT image 1 cm cephalad to shows larger lymph node with central low attenuation (arrow ). Endoscopy and biopsy revealed cecal tuberculosis JR:176, May 2001

9 CT of owel Wall Thickening Fig. 23. enign versus malignant colonic lesion: importance of lymphadenopathy., Contrast-enhanced axial CT scan of descending colon in 43-year-old man shows mild bowel wall thickening (straight arrow ) with fluid in adjacent paracolic gutter (arrowhead ). Small diverticulum is present (curved arrow ). Findings are consistent with mild focal diverticulitis, which resolved after antibiotic therapy., 66-year-old man with left-sided abdominal pain. Contrast-enhanced axial CT image at level of descending colon shows mild thickening (long arrow ) with fluid and stranding in adjacent paracolic gutter (arrowhead ). In addition, cluster of small lymph nodes is seen in adjacent pericolonic fat (short arrow ). This finding (lymphadenopathy) is more commonly present in focal adenocarcinoma than in diverticulitis. Surgery revealed adenocarcinoma, and seven of nine lymph nodes tested positive for lymphadenopathy. Fig. 24. Mesenteric mass with calcification and adjacent desmoplastic reaction in 80-year-old woman with abdominal pain. Contrast-enhanced axial CT image of abdomen shows soft-tissue mass with small calcifications (black arrow ) in mesentery (straight white arrow ). Note desmoplastic response with stranding of adjacent fat and associated bowel wall thickening (curved arrow ). Surgery revealed carcinoid tumor. Fig. 25. bscess in Crohn s disease in 21-year-old man. Contrast-enhanced axial CT image of pelvis shows segmental distal ileal thickening with target sign (white arrow ) and abscess in right iliopsoas muscle (black arrow ). Fig. 26. Colonic edema in cirrhosis in 50-year-old man. Contrast-enhanced axial CT image of right colon shows mild circumferential wall thickening in right colon and target appearance consistent with edema (arrow ). Patient did not have pain or diarrhea. CT of liver (not shown) showed findings consistent with cirrhosis. JR:176, May

10 Macari and althazar the colon will often be of low attenuation. When large bulky retroperitoneal lymph nodes are present adjacent to or in areas removed from a region of bowel wall thickening, a diagnosis of lymphoma is suggested (Fig. 11). Mesenteric Stranding and Calcification Stranding. When stranding of the perienteric fat is present adjacent to a thickened segment of bowel, an inflammatory process should be suspected. When this finding is not present, the differential diagnosis includes lymphoma and hemorrhage (Figs. 7 and 11). frequent pitfall when interpreting CT with apparent bowel wall thickening is differentiating a disease process from pitfalls related to residual fluid. When the perienteric fat is normal adjacent to a thickened segment of bowel, an acute inflammatory condition is less likely (Fig. 2). Calcification. Mesenteric calcifications are seen in benign and malignant conditions. enign mesenteric calcifications may be present in granulomatous processes such as tuberculosis, sarcoidosis, or, rarely, fungus. These calcifications may be present in mesenteric lymph nodes or solid organs such as the liver or spleen. The presence of mesenteric calcification does not imply that the abnormal bowel wall thickening is related to a granulomatous disease; it merely suggests that these conditions should be considered in the differential diagnosis. Malignant neoplasms may present on CT with calcifications in the mesentery, which is occasionally seen in patients with treated lymphoma. Calcified foci in the mesentery can also be seen in mucinous metastases from ovarian or gastrointestinal neoplasms. nother neoplastic process that can present with a calcified soft-tissue mass in the mesentery is carcinoid tumor [12]. In these cases, a significant desmoplastic process in the mesentery is sometimes present, tethering adjacent loops of small bowel toward the calcified central mass (Fig. 24). The small bowel is often thickened, which is likely related to the peptides secreted by the carcinoid tumor and secondary edematous changes. bscess, Sinus Tracts, and Fistulas CT findings of mild, symmetric bowel wall thickening with or without a target configuration in the distal ileum lead to a differential diagnosis of infectious enteritis, Crohn s disease, vasculitis, and radiation enteritis. Secondary findings that help establish the diagnosis of Crohn s disease include fistulas, sinus tracts, perienteric abscess, and fibrofatty proliferation [3, 20] (Fig. 25). Fibrofatty Proliferation Intestinal tuberculosis is particularly difficult to distinguish from Crohn s disease [21, 22]. Important clues in differentiating the cause of the abnormal bowel are fibrofatty proliferation or marked lymphadenopathy. Marked low-attenuation lymphadenopathy in abdominal tuberculosis is often the cause of displacement of small-bowel loops on barium studies, whereas fibrofatty proliferation is usually the cause of bowel displacement in Crohn s disease [22]. Solid Organs When evaluating diffuse or segmental bowel wall thickening, findings in the parenchymal organs can be helpful in establishing the differential diagnosis. Focal or segmental bowel wall thickening with associated splenomegaly suggests the diagnosis of lymphoma. The differential diagnosis for diffuse colonic edema is infectious, idiopathic (ulcerative), or ischemic colitis. However, patients with cirrhosis may also develop intestinal edema. The edema most often occurs in the small bowel and occasionally in the stomach and colon, especially the right colon [6, 39] (Fig. 26). Conclusion owel wall thickening revealed on CT is seen as normal variants, inflammatory conditions, and gastrointestinal neoplasms. careful analysis of several parameters described in this review pattern of attenuation and enhancement; degree, symmetry, and extent of thickening; and associated abnormalities will avoid most pitfalls, indicate a diagnosis of primary intestinal lesions, or offer a pertinent differential diagnosis. lthough none of the solitary CT findings is by itself specific, the association of several abnormal parameters will lead to a correct diagnosis or will narrow the differential diagnosis in most cases. When confusing or overlapping CT parameters are encountered or uncertainties persist, barium examinations should be liberally used as complementary diagnostic studies. References 1. althazar EJ. CT of the gastrointestinal tract: principles and interpretation. JR 1991;156: Shirkhoda. Diagnostic pitfalls in abdominal CT. 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11 CT of owel Wall Thickening 24. O Sullivan SG. The accordion sign. Radiology 1998;206: oland GW, Lee MJ, Cats M, Ferraro MJ, Matthia R, Mueller PR. Clostridium difficile colitis: correlation of CT findings with severity of clinical disease. Clin Radiol 1995;50: Fishman EK, Kavuru M, Jones, et al. Pseudomembranous colitis: CT evaluation of 26 cases. Radiology 1991;180: althazar EJ, Megibow J, Fazzini E, Opulencia JF, Engel I. Cytomegalovirus colitis in IDS: radiographic findings in 11 patients. Radiology 1985;155: Macari M, althazar EJ, Megibow J. The accordion sign on CT: a nonspecific finding in patients with colonic edema. Radiology 1999;211: Horton KM, Corl FM, Fishman EK. CT of nonneoplastic diseases of the small bowel. J Comput ssist Tomogr 1999;23: Taourel PG, Deneuville M, Pradel J, Regent D, ruel JM. cute mesenteric ischemia: diagnosis with contrast-enhanced CT. Radiology 1996;199: althazar EJ, Liebskind ME, Macari M. Intestinal ischemia in patients in whom small bowel obstruction is suspected: evaluation of accuracy, limitations, and clinical implications of CT in diagnosis. Radiology 1997;205: Mirvis SE, Shanmuganathan K, Erb R. Diffuse small-bowel ischemia in hypotensive adults after blunt trauma (shock bowel): CT findings and clinical significance. JR 1994;163: Rademaker J. Veno-occlusive disease of the colon: CT findings. Eur Radiol 1998;8: althazar EJ. CT of small-bowel obstruction. (George W. Holmes lecture) JR 1994;162: yun JY, Ha HK, Yu SY, et al. CT features of systemic lupus erythematosus in patients with acute abdominal pain: emphasis on ischemic bowel disease. Radiology 1999;211: Zizic TM, Classen JN, Stevens M. cute abdominal complications of systemic lupus erythematosus and polyarteritis nodosa. m J Med 1982;73: Ko SF, Cheng TT, Ng SH, et al. CT findings at lupus mesenteric vasculitis. cta Radiol 1997;1: lumeke D, Fishman EK, Kuhlman JE, Zinreich ES. Complications of radiation therapy: CT evaluation. RadioGraphics 1991;11: althazar EJ, Gade MF. Gastrointestinal edema in cirrhotics. Gastrointest Radiol 1976;1: PPENDIX 1: Patterns of ttenuation in owel Wall Thickening I. Homogeneous. Common 1. Submucosal hemorrhage 2. Lymphoma 3. Small adenocarcinoma. Uncommon 1. Infarcted bowel 2. Pitfalls related to residual fluid 3. Chronic Crohn s disease 4. Chronic radiation injury II. Heterogeneous. Stratified attenuation 1. Common a. Ischemia b. Infectious enterocolitis c. Crohn s disease, ulcerative colitis d. Vasculitis, lupus, Henoch-Schönlein purpura e. Radiation f. owel edema related to cirrhosis or low-protein state 2. Uncommon a. Infiltrating scirrhous carcinoma (usually stomach or rectum) b. Residual fluid and contrast material c. Submucosal fat deposition d. Pneumatosis. Mixed attenuation, common 1. Large adenocarcinoma 2. Gastrointestinal stromal tumor 3. Mucinous adenocarcinoma 40. Jones, Fishman EK, Hamilton SR, et al. Submucosal accumulation of fat in inflammatory bowel disease: CT/pathologic correlation. J Comput ssist Tomogr 1986;10: Muldowney SM, alfe DM, Hammerman, Wick MR. cute fat deposition in bowel wall submucosa: CT appearance. J Comput ssist Tomogr 1995;19: Feczko PJ, Mezwa DG, Farah MC, White D. Clinical significance of pneumatosis of the bowel wall. RadioGraphics 1992;12: Chintapalli KN, Chopra S, Ghiatas, Esola CC, Fields SF, Dodd GD III. Diverticulitis versus colon cancer: differentiation with helical CT findings. Radiology 1999;210: Rao PM, Rhea JT, Novelline R. CT diagnosis of mesenteric adenitis. Radiology 1997;202: Pombo F, Rodriguez E, Mato J, Perez-Fontan J, Rivera E, Valvuena L. Patterns of contrast enhancement of tuberculous lymph nodes demonstrated by computed tomography. Clin Radiol 1992;46: Yang Z-G, Min P-Q, Sone S, et al. Tuberculosis versus lymphomas in the abdominal lymph nodes: evaluation with contrast-enhanced CT. JR 1999;172: ppendixes 2 4 are on the next page. JR:176, May

12 PPENDIX 2: Degree of owel Wall Thickening PPENDIX 3: Symmetry of owel Wall Thickening PPENDIX 4: Length of owel Wall Thickening Macari and althazar I. Mild Thickening (<2 cm). Common 1. Infectious enterocolitis 2. Ulcerative colitis 3. Crohn s disease 4. Radiation injury 5. Ischemia 6. owel edema in cirrhosis 7. Submucosal hemorrhage. Uncommon 1. denocarcinoma 2. Lymphoma II. Marked Thickening (>2 cm). Common 1. denocarcinoma, gastrointestinal stromal tumor, metastases, lymphoma 2. Severe colitis 3. Systemic lupus erythematosus. Uncommon 1. Crohn s disease, tuberculosis, histoplasmosis, cytomegalovirus 2. Submucosal hemorrhage I. Symmetric. Infections of the small and large bowel. Ulcerative colitis C. Crohn s disease D. Radiation injury E. Ischemia F. owel edema in cirrhosis G. Lymphoma H. Submucosal hemorrhage II. symmetric. denocarcinoma. Gastrointestinal stromal tumor I. Focal (<10 cm). Common 1. Diverticulitis, appendicitis 2. denocarcinoma. Uncommon 1. Lymphoma 2. Tuberculosis 3. Crohn s disease II. Segmental (10 30 cm). Common 1. Lymphoma 2. Crohn s disease 3. Infectious ileitis 4. Radiation 5. Submucosal hemorrhage 6. Ischemia. Uncommon: systemic lupus erythematosus III. Diffuse. Common 1. Ulcerative colitis 2. Infectious enterocolitis 3. Edema from low protein and cirrhosis 4. Systemic lupus erythematosus Uncommon: ischemia JR:176, May 2001