(Radiographics. 2002;22:1093-1107.)
© RSNA, 2002
Algorithmic Approach to CT Diagnosis of the Abnormal Bowel Wall1
Jack Wittenberg, MD,
Mukesh G. Harisinghani, MD,
Kartik Jhaveri, MD,
Jose Varghese, MD and
Peter R. Mueller, MD
1 From the Division of Abdominal Imaging and Intervention, Massachusetts General Hospital, 55 Fruit St, Boston, MA 02114. Recipient of a Certificate of Merit award for an education exhibit at the 2001 RSNA scientific assembly. Received February 15, 2002; revision requested March 11 and received April 10; accepted April 16. Address correspondence to J.W. (e-mail: jwittenberg@partners.org).
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Abstract
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Computed tomography demonstrates intestinal wall abnormalities that can be analyzed by categorizing attenuation changes in the intestinal wall and transposing morphologic characteristics learned from barium studies. These attenuation patterns include white, gray, water halo sign, fat halo sign, and black. The white pattern represents avid contrast material enhancement that uniformly affects most of the thickened bowel wall. If the bowel wall is enhanced to a degree equal to or greater than that of venous opacification in the same scan, it should be classified in the white attenuation pattern. Common diagnoses with this pattern include idiopathic inflammatory bowel diseases and vascular disorders. The gray pattern is defined as a thickened bowel wall with limited enhancement whose homogeneous attenuation is comparable with that of enhanced muscle. This pattern is used to differentiate between benign and malignant disease, but it is the least specific of the patterns and should be combined with morphologic observations. The water halo sign indicates stratification within a thickened bowel wall that consists of either two or three continuous, symmetrically thickened layers. Common diagnoses with this sign include idiopathic inflammatory bowel diseases, vascular disorders, infectious diseases, and radiation damage. The fat halo sign refers to a three-layered target sign of thickened bowel in which the middle or "submucosal" layer has a fatty attenuation. Common diagnoses with this sign include Crohn disease in the small intestine and idiopathic inflammatory bowel diseases in the colon. Black attenuation is the equivalent of pneumatosis, and this pattern is commonly seen in ischemia, infection, and trauma.
© RSNA, 2002
Index Terms: Computed tomography (CT), tissue characterization, 74.12112, 75.12112 • Intestines, CT, 74.12112, 75.12112
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LEARNING OBJECTIVES FOR TEST 2
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After reading this article and taking the test, the reader will be able to:
- Identify various CT enhancement patterns of diseased bowel wall.
- Confidently discriminate between most neoplastic and benign intestinal conditions.
- Avoid common causes of misinterpretation.
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Introduction
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Computed tomography (CT) is increasingly being used as a screening technique for patients with symptoms of intestinal disease because of (a) growing confidence in CT in general as a problem solver, especially for many gastrointestinal disorders; (b) a wide margin of clinical diagnostic error in the differentiation of intestinal from other abdominal diseases; (c) its potential for providing information for a comprehensive diagnosis and staging of abdominal neoplasms; and (d) its wide availability and ease of performance. Predictably, CT will uncover abnormalities in patients with or without symptoms referable to the intestinal tract. A wide spectrum of intestinal wall morphologic and enhancement abnormalities can be seen with bowel disorders. Once an abnormality is detected, the radiologist needs a systematic approach for determining the specific cause of the intestinal abnormality.
In this article, an organizational framework is proposed that distills both enhancement and morphologic observations for refining CT interpretation of both small and large intestinal diseases. The proposed approach is based on alternative attenuation values of the bowel wall. The spectrum of these mural attenuation patterns includes white (avid contrast material enhancement), gray, water halo sign, fat halo sign, and black (pneumatosis). Differentiating these patterns, sometimes supplemented by geographic and morphologic bowel wall features, will considerably narrow the diagnostic possibilities, particularly in the differentiation of benign from malignant disease. Herein, we review the CT scanning technique used for intestinal screening examinations and describe the five categories of attenuation patterns, along with a limited differential diagnosis and a review of common pitfalls.
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Scanning Technique
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Many patients with bowel wall abnormalities present with acute, subacute, or chronic gastrointestinal symptoms, some patients may have nonspecific abdominal complaints or none at all. Therefore, the CT imaging technique applied in the overwhelming proportion of patients is a conventional one. In a few cases, the CT technique will prospectively be specifically tailored to the suspected diagnosis. The tailored examination could include use of arterial as well as portal venous phase contrast material enhancement, delayed scans, decubitus positioning (1), or an enema (2). Although these refinements might retrospectively contribute additional clues in some cases, their routine incorporation is impractical, particularly with the scant patient history, physical observations, or laboratory information ordinarily available.
The conventional CT technique consists of scanning the abdomen after the oral and intravenous administration of contrast material. Helical scanning with contiguous 5-mm sections is performed from the diaphragm to the symphysis pubis. All patients, when possible, receive orally 600–900 mL of 2.5% diluted sodium amidotrizoate and meglumine amidotrizoate mixture (Gastrografin; Schering, Berlin, Germany) approximately 4 hours, 2 hours, and immediately before scanning. In addition, 150 mL of nonionic water-soluble iodinated contrast medium (Oxilan; Cook, Bloomington, Ind) is intravenously injected (MCT Plus; Medrad, Pittsburgh, Pa) at a rate of 2 mL/sec through a 20-gauge intravenous catheter, and scanning is performed after a 70-second delay.
Because many bowel wall observations may be very subtle, use of thin-section, high-volume, rapid-bolus scanning technique with state-of-the-art CT technology is important in discriminating intestinal abnormalities. Intravenous administration of contrast material is often preferable, and in most cases critical, for discovering certain bowel wall abnormalities that otherwise may be inapparent or very subtle. Because administration of oral contrast material is usually routine, the bowel wall is invariably assessed in the presence of positive luminal contrast material. However, nonopaque fluid distention may reveal luminally oriented features possibly obscured by the oral contrast material.
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Classification of CT Enhancement Patterns
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Interpretive Criteria
Although subjective assessment and assignment of a bowel wall attenuation abnormality to a category may prove challenging, doing so will considerably narrow the diagnostic possibilities. Supplemental morphologic mural and regional factors provide additional, or in some cases even superior, insight into the specific diagnosis. In the descriptions of the CT attenuation patterns that follow, conventional morphologic features accumulated from years of interpreting barium studies are outlined in those categories for which incorporating such features is likely to be most helpful (1). Of course, reliable clinical information must always be factored into the final diagnosis.
The appearance, degree, and consistency of bowel wall enhancement have been well described (1,3). The presence of bowel wall thickening, as an isolated finding, has limited value for analyzing a specific injury (4). When the lumen is distended, normal bowel wall thickness is 1–2 mm; when the lumen is collapsed, normal thickness may be 3–4 mm (1). Although different degrees of wall thickness favor certain diagnoses, the overlap of these findings among alternative diseases negates the precision of this approach (5,6). One always needs to juggle assessment of abnormal thickness with the degree of luminal distention. Intestines are not only mobile but subject to a great deal of normal and abnormal intrinsic functional influence, particularly limiting ideal small bowel distention. Although use of CT enteroclysis can provide a remedy to this problem (7,8), this technique is impractical to perform routinely in all patients with acute abdominal problems, and it is impossible to predict prospectively the cases in which it might be useful. However, for some patients, CT enteroclysis could help radiologists avoid the trap of the undistended, pseudothickened wall and could be used as a supplemental examination in less urgent cases.
In each of the five categories of attenuation patterns—white, gray, water halo sign, fat halo sign, and black—(Figs 1, 2), a description of the bowel wall attenuation findings is given, along with a limited differential diagnosis and a review of common pitfalls. The differential diagnosis is operationally divided into the more generic and common diagnoses versus the uncommon or rare ones. The common diagnoses are not meant to be all inclusive; rather, those mentioned are statistically more common. It should be emphasized that the same diagnosis (eg, idiopathic inflammatory bowel disease) may be mentioned for several attenuation patterns, with the different appearances representing different phases and physiology of the disease process. Likewise, more than one pattern may coexist in the same examination. Each pattern can be analyzed independently and thereafter amalgamated into the best fit diagnosis.
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Figure 1. Plot summarizes the spectrum of five attenuation patterns observed in bowel wall disease. * = use of intravenously administered contrast material is required to assess the pattern accurately.
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Figure 2a. Mural enhancement characteristics of the five attenuation patterns. (a) White attenuation. Intravenous contrast material-enhanced CT scan of a case of colonic varices demonstrates the thickened wall of the sigmoid colon with uniform avid contrast material enhancement (solid straight arrows), dilated perisigmoid veins (curved arrow), and ascites (open arrow). (b) Gray attenuation. Intravenous contrast-enhanced CT scan of a case of colonic adenocarcinoma demonstrates the thickened wall of the mid-descending colon (straight arrow) with attenuation similar to that of adjacent muscle (curved arrow). (c) Water halo sign. Intravenous contrast-enhanced CT scan of a case of pseudomembranous colitis shows an outer enhanced layer (white arrows) surrounding a water attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (d) Fat halo sign. CT scan of a case of ulcerative colitis shows an outer enhanced layer (straight solid arrows) surrounding a fat attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (e) Black attenuation. CT scan of a case of cecal pneumatosis in ischemic colitis shows rounded mural gas attenuation collections (straight solid arrows), as well as the outer margin of the colonic wall (curved arrows) and lumen (open arrow).
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Figure 2b. Mural enhancement characteristics of the five attenuation patterns. (a) White attenuation. Intravenous contrast material-enhanced CT scan of a case of colonic varices demonstrates the thickened wall of the sigmoid colon with uniform avid contrast material enhancement (solid straight arrows), dilated perisigmoid veins (curved arrow), and ascites (open arrow). (b) Gray attenuation. Intravenous contrast-enhanced CT scan of a case of colonic adenocarcinoma demonstrates the thickened wall of the mid-descending colon (straight arrow) with attenuation similar to that of adjacent muscle (curved arrow). (c) Water halo sign. Intravenous contrast-enhanced CT scan of a case of pseudomembranous colitis shows an outer enhanced layer (white arrows) surrounding a water attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (d) Fat halo sign. CT scan of a case of ulcerative colitis shows an outer enhanced layer (straight solid arrows) surrounding a fat attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (e) Black attenuation. CT scan of a case of cecal pneumatosis in ischemic colitis shows rounded mural gas attenuation collections (straight solid arrows), as well as the outer margin of the colonic wall (curved arrows) and lumen (open arrow).
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Figure 2c. Mural enhancement characteristics of the five attenuation patterns. (a) White attenuation. Intravenous contrast material-enhanced CT scan of a case of colonic varices demonstrates the thickened wall of the sigmoid colon with uniform avid contrast material enhancement (solid straight arrows), dilated perisigmoid veins (curved arrow), and ascites (open arrow). (b) Gray attenuation. Intravenous contrast-enhanced CT scan of a case of colonic adenocarcinoma demonstrates the thickened wall of the mid-descending colon (straight arrow) with attenuation similar to that of adjacent muscle (curved arrow). (c) Water halo sign. Intravenous contrast-enhanced CT scan of a case of pseudomembranous colitis shows an outer enhanced layer (white arrows) surrounding a water attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (d) Fat halo sign. CT scan of a case of ulcerative colitis shows an outer enhanced layer (straight solid arrows) surrounding a fat attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (e) Black attenuation. CT scan of a case of cecal pneumatosis in ischemic colitis shows rounded mural gas attenuation collections (straight solid arrows), as well as the outer margin of the colonic wall (curved arrows) and lumen (open arrow).
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Figure 2d. Mural enhancement characteristics of the five attenuation patterns. (a) White attenuation. Intravenous contrast material-enhanced CT scan of a case of colonic varices demonstrates the thickened wall of the sigmoid colon with uniform avid contrast material enhancement (solid straight arrows), dilated perisigmoid veins (curved arrow), and ascites (open arrow). (b) Gray attenuation. Intravenous contrast-enhanced CT scan of a case of colonic adenocarcinoma demonstrates the thickened wall of the mid-descending colon (straight arrow) with attenuation similar to that of adjacent muscle (curved arrow). (c) Water halo sign. Intravenous contrast-enhanced CT scan of a case of pseudomembranous colitis shows an outer enhanced layer (white arrows) surrounding a water attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (d) Fat halo sign. CT scan of a case of ulcerative colitis shows an outer enhanced layer (straight solid arrows) surrounding a fat attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (e) Black attenuation. CT scan of a case of cecal pneumatosis in ischemic colitis shows rounded mural gas attenuation collections (straight solid arrows), as well as the outer margin of the colonic wall (curved arrows) and lumen (open arrow).
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Figure 2e. Mural enhancement characteristics of the five attenuation patterns. (a) White attenuation. Intravenous contrast material-enhanced CT scan of a case of colonic varices demonstrates the thickened wall of the sigmoid colon with uniform avid contrast material enhancement (solid straight arrows), dilated perisigmoid veins (curved arrow), and ascites (open arrow). (b) Gray attenuation. Intravenous contrast-enhanced CT scan of a case of colonic adenocarcinoma demonstrates the thickened wall of the mid-descending colon (straight arrow) with attenuation similar to that of adjacent muscle (curved arrow). (c) Water halo sign. Intravenous contrast-enhanced CT scan of a case of pseudomembranous colitis shows an outer enhanced layer (white arrows) surrounding a water attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (d) Fat halo sign. CT scan of a case of ulcerative colitis shows an outer enhanced layer (straight solid arrows) surrounding a fat attenuation layer (curved arrows). Luminal contrast material is also seen (open arrow). (e) Black attenuation. CT scan of a case of cecal pneumatosis in ischemic colitis shows rounded mural gas attenuation collections (straight solid arrows), as well as the outer margin of the colonic wall (curved arrows) and lumen (open arrow).
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Category 1: White Attenuation
The pattern of white attenuation represents avid contrast material enhancement that uniformly affects the majority of the thickened bowel wall (Fig 2a). The observation can only be applied after the intravenous administration of contrast material, and, on occasion, it is best appreciated in loops of bowel not distended with oral contrast material, since intense interstitial opacification may be confused with luminal oral contrast material (Fig 3). The diameters of the supplying pericolonic vessels may, but do not always, appear prominent (Fig 4).
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Figure 3. White attenuation: enhancement of the small intestine in shock bowel. On an intravenous contrast-enhanced CT scan, the jejunum demonstrates increased enhancement (black arrows). The attenuation is greater than that of the inferior vena cava (curved arrow). The enhancement qualities could be confused for luminal oral contrast material but none was given (Inset: straight white arrow = fluid in stomach.).
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Figure 4. White attenuation: enhancement in acute ulcerative colitis. On an intravenous contrast-enhanced CT scan, the thickened wall of the rectosigmoid segment demonstrates uniform increased enhancement (straight black arrows) similar to the attenuation of the external iliac vein (curved arrow). Pericolonic vessels are dilated (white arrow).
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At least two pathophysiologic events likely underlie this attenuation pattern: (a) vasodilation and/or (b) injury to intramural vessels with accompanying interstitial leakage. "Shock bowel" (ie, diffuse ischemia of the small bowel in hypotensive adults who have sustained blunt trauma) (Fig 3) is the prototypic example of the latter pathophysiology. Hypoperfusion results in increased vascular permeability to macromolecules and albumin, which leads to diffuse bowel wall thickening and increased enhancement on CT scans because of slowed perfusion and interstitial leakage of molecules of contrast material (9,10). Reversal of shock bowel with successful treatment of the hypovolemia suggests that the white attenuation pattern represents a reversible ischemic change without clinical significance (9,10). The relative attenuation of the white category (Figs 3, 4) is at least the same as, or greater than, venous opacification seen in the same scan, but it is absolutely dependent on the volume and rapidity of delivery of intravenous contrast material and the timing of the scan. In the majority of our cases with this pattern, the previously described conventional imaging parameters were used.
Absence of enhancement or decreased enhancement of the bowel wall may be the most specific finding for bowel ischemia (11). Although counterintuitive, the ischemic segment may also appear with increased enhancement, which is caused by altered vascular permeability and perfusion problems (ie, delayed return of venous blood with subsequent slowing of the arterial supply or arteriospasm) (11,12) (Fig 5).
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Figure 5. White attenuation: enhancement in ischemic duodenitis and jejunitis. Intravenous contrast-enhanced CT scan shows enhanced segments of duodenum (large straight black arrow) and jejunum (curved arrow). Note absence of oral contrast material in the stomach (white arrow). Dissection is present in the aorta (arrowhead) and superior mesenteric artery (small straight black arrow).
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The increased wall enhancement associated with inflammatory bowel disease (Figs 4, 6, 7) reflects the hyperemic and hypervascular state seen classically with acute inflammation (13–15). This hypervascularity is reflected in mesenteric changes of vascular dilation and tortuosity (Figs 4, 6, 7). The prominence and increased separation of vasa recta in the ileum has been called vascular jejunization of the ileum or "comb sign" (14,16) (Fig 6).
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Figure 6. White attenuation: enhancement in ileal Crohn disease. On an intravenous contrast-enhanced CT scan, the enhanced thickened wall of the small bowel (solid arrows) is slightly higher attenuation than the inferior vena cava (open black arrow). The vasa recta are dilated (arrowhead) and separated by increased fat deposition ("creeping fat sign"). Open white arrow = enlarged mesenteric node.
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Figure 7. White attenuation: enhancement in acute ulcerative colitis. On an intravenous contrast-enhanced CT scan, the attenuation of enhanced segments of colon (solid white arrows) is similar to that of the inferior vena cava (black arrow). The pericolonic vasa recta are dilated (open arrow).
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Differential Diagnosis.—
The common diagnoses in which the white attenuation pattern is seen include idiopathic inflammatory bowel diseases and vascular disorders. The uncommon diagnosis in which this pattern occurs is malignancy.
Pitfalls.—
At present, the identification of bowel enhancement appropriate to be classified in the white attenuation pattern is largely subjective, certainly rarely achieving the attenuation value of a major arterial vessel when viewed on the same section. The lowest Hounsfield unit for the least bright enhancement that still qualifies as "white" is unknown and is unlikely to be a useful number because of the variability in technical factors as well as the patient’s circulatory dynamics.
Our present approach is to use the internal standard of venous enhancement. If the bowel wall is enhanced to a degree that is equal to or greater than that of venous opacification in the same scan (Figs 3–7), it should be classified in the white attenuation pattern. Therefore, making an eyeball venous comparison is practical, and if Hounsfield unit measurements are needed for confirmation, it most likely means that the classification as white is equivocal at best. In such a case, a prudent conservative philosophy may dictate classifying the finding to the gray attenuation category (Fig 8). On the other hand, observation of clearly dilated peri-intestinal vessels should lead one to classify the equivocal finding to the white attenuation category (Fig 7).
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Figure 8. Gray attenuation: enhancement of colonic walls in ischemic colitis. On an intravenous contrast-enhanced CT scan, the attenuation of the walls of the colon (solid straight arrows) falls short of the attenuation of the superior mesenteric venous branch (curved arrow) and inferior vena cava (open arrow). Therefore, in this case, interpretation should be assigned to the gray attenuation pattern.
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Category 2: Gray Attenuation
The pattern of gray attenuation is defined as a thickened bowel wall that shows little clear-cut enhancement and whose homogeneous attenuation is comparable with that of enhanced muscle (Figs 2b, 8). The classification of gray attenuation, which spans the interval between white attenuation and the water halo sign of category 3, should be assigned only after intravenous administration of contrast material. An unenhanced thickened gray wall may be harboring additional information best appreciated after contrast material enhancement (1) (Fig 9). The gray attenuation pattern is the least specific of the five attenuation categories for diagnosis, and it is common in both benign and malignant diseases. Macari and Balthazar (6) noted that bowel wall thickening of less than 2 cm was more characteristic of benign conditions, whereas thickening greater than 3 cm was usually present in neoplastic cases. However, the considerable overlap between these two groups mandates that additional morphologic observations should be employed before a case in this category is finally interpreted.
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Figure 9a. Water halo sign in ischemic colitis following administration of intravenous contrast material. (a) Nonenhanced CT scan shows wall thickening of the distal transverse and proximal descending colon (straight arrows). The attenuation is largely of the gray attenuation pattern, although a partial halo sign is indistinctly evident (curved arrow). (b) On the intravenous contrast-enhanced CT scan, a complete gray halo is clearly evident in the descending colon (straight arrows) and partially in the transverse colon (curved arrow).
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Figure 9b. Water halo sign in ischemic colitis following administration of intravenous contrast material. (a) Nonenhanced CT scan shows wall thickening of the distal transverse and proximal descending colon (straight arrows). The attenuation is largely of the gray attenuation pattern, although a partial halo sign is indistinctly evident (curved arrow). (b) On the intravenous contrast-enhanced CT scan, a complete gray halo is clearly evident in the descending colon (straight arrows) and partially in the transverse colon (curved arrow).
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The morphologic criteria have been extrapolated from the most reliable observations from barium studies (1,6,17) (Table 1, Fig 10). When these criteria are applied to interpretation of CT scans, however, they do not have the same prevalence and reliability accrued with fluoroscopy because the dynamic observation, palpation, and distention control available with fluoroscopy are not attainable with conventional CT. If the morphologic criteria for a malignant disorder are observed on CT scans, they are worth incorporating in the case analysis; however, their absence should not be regarded as useful for excluding tumor. Even their presence must be carefully scrutinized for evidence of incomplete luminal distention.
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Figure 10a. Morphologic signs aiding diagnosis with the gray attenuation pattern. (a) Intravenous contrast-enhanced CT scan shows segmental annular thickening of the sigmoid colon (straight arrows) with sharp angular margins at either end (curved arrows) in adenocarcinoma. (b) Intravenous contrast-enhanced CT scan shows smooth, tapered margins (white arrows) at the edge of a mass in the sigmoid colon (black arrow) affected by diverticulitis.
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Figure 10b. Morphologic signs aiding diagnosis with the gray attenuation pattern. (a) Intravenous contrast-enhanced CT scan shows segmental annular thickening of the sigmoid colon (straight arrows) with sharp angular margins at either end (curved arrows) in adenocarcinoma. (b) Intravenous contrast-enhanced CT scan shows smooth, tapered margins (white arrows) at the edge of a mass in the sigmoid colon (black arrow) affected by diverticulitis.
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Differential Diagnosis.—
The gray attenuation pattern and accompanying morphologic characteristics are used in differentiating between benign and malignant disease.
Pitfalls.—
A common cause of false-positive diagnosis in either the small intestine or colon is incomplete luminal distention (1,6,13). If incomplete luminal distention of the colon is suspected, gravity maneuvers or the more time-consuming CT enema can be employed. The latter technique can also be applied if false-negative observations are suspected. If incomplete luminal distention of the small bowel is suspected, either CT enteroclysis or immediate repeat target scanning after administering more oral contrast material can be employed (7). False-positive findings of mural thickening in the small intestine often arise, particularly in the jejunum, from inhomogeneous layering of oral contrast material and endogenous luminal contents (Fig 11).
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Figure 11. Pseudothickening of the jejunum. On an intravenous contrast-enhanced CT scan, several jejunal segments demonstrate apparent thickening (straight arrows) at the same time that collections of antidependent luminal gas in adjacent segments demonstrate a normal paper-thin wall (curved arrows). This pseudothickened appearance is produced by streaming of lower-attenuation fluid within the center of an oral contrast-enhanced lumen.
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Category 3: Water Halo Sign
The water halo sign is used as a generic term to indicate stratification within a thickened bowel wall that consists of either two or three continuous, symmetrically thickened layers. A halo sign with two layers (double halo) is composed of either a higher-attenuation outer annular ring (muscularis propria) surrounding a second, luminally oriented annular ring of gray attenuation (6,13,18,19) (Fig 2c) or a higher-attenuation inner layer and an outer ring of gray attenuation (Fig 12). A third variant, the target sign, is composed of three rings: outer high-attenuation muscularis propria, a middle ring of gray attenuation, and a luminally oriented ring of high attenuation (1,20) (Fig 13). The lower-attenuation (gray) layer of the water halo sign is believed to represent edema (thought to be its dominant component) and can be assumed to be located in the submucosa (6,18).
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Figure 12a. Water halo sign in the small intestine and colon. (a) Intravenous contrast-enhanced CT scan shows an inner layer of a strangulated, ischemic segment of small bowel (small straight solid arrows) surrounded by a lower-attenuation layer (curved arrows). Note the brightness of the dilated, obstructed proximal small bowel wall (open arrow), which approximates the attenuation of the external iliac vein (arrowhead). However, since the wall of dilated bowel is not thickened, it would not be considered abnormal. Large straight solid arrow = ascites. (b) Water halo sign in pseudomembranous colitis. On an intravenous contrast-enhanced CT scan, the thickened inner layer of the rectosigmoid (straight arrows) is surrounded by a thicker outer layer (curved arrows).
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Figure 12b. Water halo sign in the small intestine and colon. (a) Intravenous contrast-enhanced CT scan shows an inner layer of a strangulated, ischemic segment of small bowel (small straight solid arrows) surrounded by a lower-attenuation layer (curved arrows). Note the brightness of the dilated, obstructed proximal small bowel wall (open arrow), which approximates the attenuation of the external iliac vein (arrowhead). However, since the wall of dilated bowel is not thickened, it would not be considered abnormal. Large straight solid arrow = ascites. (b) Water halo sign in pseudomembranous colitis. On an intravenous contrast-enhanced CT scan, the thickened inner layer of the rectosigmoid (straight arrows) is surrounded by a thicker outer layer (curved arrows).
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Figure 13. Small bowel with target sign in angioedema. On an intravenous contrast-enhanced CT scan, several segments of small bowel demonstrate three uniformly thick layers. The layers grossly correspond to muscularis propria (straight solid arrows), submucosa (curved arrow), and mucosa (open arrow). Arrowhead = ascites.
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For simplicity sake, we use the water halo sign to refer to all three of these configurations, since at the present it is not clear that pathologic events, differential diagnosis, specificity, or prognosis can be assigned to these alternative halo configurations. The inner and outer rings of the target signs can conveniently be regarded as the "mucosa" and "muscularis propria," respectively, with the higher attenuation being the consequence of preferential enhancement. It is uncertain, however, whether either ring represents the true histologic boundaries of those structures, particularly the mucosa. The water halo sign is most valuable as an unequivocal observation of bowel wall injury, often of an acute nature (6). Furthermore, although a myriad of small or large bowel pathologic conditions can produce these signs, malignancy rarely manifests with the classic water halo sign (Fig 14).
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Figure 14. Incomplete water halo sign in sigmoid lymphoma. On an intravenous contrast-enhanced CT scan, the narrowed lumen is surrounded by an asymmetrically thickened, lower-attenuation layer (straight solid arrows). The surrounding outer layer is incomplete (curved arrows). Note the abrupt, angular margin of the mass (open arrow).
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Differential Diagnosis.—
The common diagnoses in which the water halo sign is seen include idiopathic inflammatory bowel diseases, vascular disorders, infectious diseases, and radiation damage. The uncommon diagnosis in which this pattern occurs is malignancy.
Pitfalls.—
Hounsfield unit measurement and histologic correlation suggest that the pathophysiologic underpinning of the water halo sign is most likely edema (6,18,21). The finding is therefore categorized as the water halo sign to distinguish it from the fat halo sign of category 4. Although eyeball differentiation of the two signs is usually sufficient, a positive Hounsfield unit value rather than the negative Hounsfield unit value of fat helps confirm the finding. Application of morphologic criteria (Table 2) is appropriate, but, unless malignant criteria are unequivocally present, a benign diagnosis should be given. Halo stratification is most apparent after intravenous administration of contrast material (Fig 9) and may not be detected without it. For this reason, final classification in the gray attenuation category or as a water halo sign requires intravenous administration of contrast material. The "mucosal" attenuation of the target sign is best appreciated when the bowel is distended with water-attenuation contrast material (Figs 12, 13).
Category 4: Fat Halo Sign
The pattern of the fat halo sign refers to a three-layered target sign of thickened bowel in which the middle or "submucosal" layer has a fatty attenuation (5,6,13,22) (Fig 2d). The darker attenuation of intramural fat can usually be visually distinguished from the grayer tone of the water halo sign (Figs 2c, 15). If the attenuation of the dark ring is measured in Hounsfield units, the numbers will largely be below -10 HU. Regardless of assessment method, however, the attenuation is rarely equal to that of pure mesenteric or retroperitoneal fat, either because of partial volume effect or coexistent edema (Fig 15). The outer edge of the muscularis propria may either be well demarcated or indistinct because of stranding in surrounding fat.
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Figure 15. Fat halo sign (target configuration) in chronic ulcerative colitis. On the intravenous contrast-enhanced CT scan, the central fatty submucosal layer has dark attenuation (arrowheads) and is surrounded by higher-attenuation inner (curved arrows) and outer (open arrows) rings grossly corresponding to the mucosa and muscularis propria, respectively. The darker submucosal layer is not as dark as surrounding mesenteric fat but is sufficiently dark to be distinguished as fat.
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The observation of the fat halo sign in the small intestine is, for all intents and purposes, diagnostic of Crohn disease and by itself is a sign of a chronic phase. However, the fat halo sign may be observed in a patient in whom Crohn disease is manifest in other abnormal bowel segments without a fat component and with other attenuation patterns more indicative of acute or subacute activity (13). We have observed a single case of small intestinal fat halo sign in an asymptomatic patient who had undergone radiation therapy to the abdomen 30 years previously (Fig 16). Fat in the small intestine has also been attributed to the effects of cytoreductive therapy (23).
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Figure 16. Fat halo sign in chronic radiation enteritis. Intravenous contrast-enhanced CT scan demonstrates several segments of small bowel with walls thickened by a central band of lower attenuation, consistent with that of fat (arrowheads). The target configuration is evident in one segment that lacks luminal oral contrast material (solid arrow). Other segments with a fatty layer have luminal contrast enhancement, which conceivably could be obscuring a higher-attenuation "mucosal" layer (open arrows).
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In the colon, the signs are the same, but the differential diagnosis includes ulcerative colitis (13). One study has shown that the fat target sign is more common in ulcerative colitis than in Crohn disease (5). Cytoreductive therapy has also been described as a cause of a colonic fat halo sign (23).
Differential Diagnosis.—
The common diagnoses in which the fat halo sign is seen include Crohn disease in the small intestine and ulcerative colitis or Crohn disease in the colon. The rare diagnoses in which this pattern occurs include cytoreductive therapy exposure and chronic radiation enteritis.
Pitfalls.—
Intramural fat may exist in both the distal ileum (Fig 17a) and colon (Fig 18) as a "normal" variant in patients without gastrointestinal symptoms or a history of gastrointestinal disease. In the small intestine, normal intramural fat is seen most commonly in the terminal ileum. In the colon, it is found most often in the descending colon. The normal intramural fat layer is generally very thin, usually thinner than the fat stratum seen with idiopathic inflammatory bowel diseases (Fig 17b). The muscularis propria is also uniformly thin, rarely exceeding 1 mm in thickness. There are rarely, if ever, surrounding mesenteric abnormalities. The observation of the normal fat halo sign is most frequently made in undistended or poorly distended bowel loops.
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Figure 17a. Normal ileal fat halo sign versus abnormal ileal fat halo sign of Crohn disease. (a) Intravenous contrast-enhanced CT scan of a patient with no present or prior history of intestinal disease shows a fat halo sign in the terminal ileum (arrow). Note the sharply marginated interfaces between all layers and surrounding fat. Both muscularis propria and submucosal layers are very thin. (b) Intravenous contrast-enhanced CT scan of a patient with Crohn disease demonstrates the fat halo sign (target configuration) in the terminal ileum (straight arrow). All three layers are slightly thickened for the degree of distention, and their interfaces are not sharply defined. Reaction in the contiguous mesentery (curved arrow) is compatible with creeping fat.
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Figure 17b. Normal ileal fat halo sign versus abnormal ileal fat halo sign of Crohn disease. (a) Intravenous contrast-enhanced CT scan of a patient with no present or prior history of intestinal disease shows a fat halo sign in the terminal ileum (arrow). Note the sharply marginated interfaces between all layers and surrounding fat. Both muscularis propria and submucosal layers are very thin. (b) Intravenous contrast-enhanced CT scan of a patient with Crohn disease demonstrates the fat halo sign (target configuration) in the terminal ileum (straight arrow). All three layers are slightly thickened for the degree of distention, and their interfaces are not sharply defined. Reaction in the contiguous mesentery (curved arrow) is compatible with creeping fat.
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Figure 18. Normal colonic fat halo sign. Intravenous contrast-enhanced CT scan of a patient with no present or prior history of intestinal disease shows a fat halo sign in the mid-descending colon (straight arrow). The interfaces of the rings are thin and sharply marginated. Similar fat halo configurations were seen on other sections of the descending colon. Linear fat deposits are also seen in the wall of the ascending colon (curved arrow). Note the volume of subcutaneous fat.
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Although very thin submucosal fat and muscularis propria colonic layers are clues to colonic normality, the fat halo sign in the normal terminal ileum may be more difficult to unequivocally distinguish from minimal Crohn disease in other bowel segments. Other intestinal wall abnormalities or local mesenteric changes including lymphadenopathy do not accompany this normal variant. Clinical history must be considered in the final diagnosis.
Category 5: Black Attenuation
The pattern of black attenuation is the equivalent of pneumatosis (Fig 2e). Use of CT, which is more accurate than conventional radiography in the detection and characterization of pneumatosis, has largely eliminated the concept of "benign" or "malignant" pneumatosis (24). Other than the rare, large cystic collections (Fig 19), all pneumatosis should be considered as part of an acute injury to the bowel. Although pneumatosis is usually considered a sign of life-threatening injury, on occasion (eg, after intestinal anastomotic surgery), it may not be so (Fig 20). Any process that is accompanied by a break in the mucosa can introduce intramural gas.
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Figure 19. Pneumatosis in the small bowel wall and mesentery. Intravenous contrast-enhanced CT scan of a symptomatic postoperative patient shows rounded (straight solid arrows) and linear (curved arrow) mural gas collections with contiguous mesenteric gas collections (open arrow). Surgery demonstrated no bowel or mesenteric disease, and patient made an uneventful recovery.
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Figure 20a. Cystic pneumatosis unassociated with bowel wall disease. (a) Intravenous contrast-enhanced CT scan obtained with the usual window settings demonstrates no thickened colonic wall (arrows) or significant intraluminal observations. (b) Same section obtained with wider window settings demonstrates multiple, gas-containing cystic areas (arrowheads). Normal adjacent colon lacks similar findings (arrows).
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Figure 20b. Cystic pneumatosis unassociated with bowel wall disease. (a) Intravenous contrast-enhanced CT scan obtained with the usual window settings demonstrates no thickened colonic wall (arrows) or significant intraluminal observations. (b) Same section obtained with wider window settings demonstrates multiple, gas-containing cystic areas (arrowheads). Normal adjacent colon lacks similar findings (arrows).
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Differential Diagnosis.—
The common diagnoses in which the black attenuation pattern is seen include ischemia, infection, and trauma. The uncommon diagnosis in which this pattern occurs is iatrogenic injury.
Pitfalls.—
The challenge is not only to detect small collections of intramural gas but to avoid confusing them with intraluminal gas collections that cling to the mucosa. Initial positive detection is made by recognizing gas bubbles within the dependent bowel wall (Figs 2e, 19, 20), some of which have a geometric rather than round configuration. Identifying gas within intramural or extramural vessels is also diagnostic of pneumatosis. Confidently diagnosing gas in the antidependent wall is more challenging because it may be mimicked by gas bubbles at the top of intraluminal fluid. Most challenging is differentiating dependently located gas bubbles in the cecum and ascending colonic wall from gas trapped between fecal debris and mucosa (Fig 21). Repositioning and rescanning the patient in a decubitus position sometimes clears up this dilemma (1). The superior and inferior mesenteric veins and liver should always be inspected for intravenous gas to support the diagnosis of pneumatosis.
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Figure 21. Pseudopneumatosis. Intravenous contrast-enhanced CT scan demonstrates small, rounded, gas bubbles (straight solid arrows) in the periphery of the lumen contiguous to the colonic wall. The bubbles do not rise to the antidependent air-fluid level (curved arrow) and are presumably trapped in the lumen between fecal material. Open arrow = surgical clips.
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Combination of Attenuation Patterns
A single disease may simultaneously demonstrate different attenuation patterns in contiguous segments of bowel (Fig 22). This appearance presumably represents alternative but coexistent pathophysiologic events. Idiopathic inflammatory bowel disease is the classic example of such a phenomenon (1,6,13) (Fig 23). Analysis of each segment of affected small or large intestine is judged by its separate category.
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Figure 22. Both gray attenuation and water halo sign in ischemic colitis. On an intravenous contrast-enhanced CT scan, the distal transverse colon demonstrates gray thickening (straight arrow), whereas the descending colon has a halo sign (curved arrow).
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Figure 23. Both white attenuation and water halo sign in acute ischemic enterocolitis. On an intravenous contrast-enhanced CT scan, multiple loops of small intestine demonstrate increased contrast enhancement within thickened walls (black arrows). Colon demonstrates the water halo sign (curved arrows).
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Conclusions
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An approach for classifying bowel wall abnormality was presented based on variations in bowel wall attenuation and stratification characteristics and supplemented by morphologic criteria that may be useful in equivocal cases. Although the classification is most useful in distinguishing benign from malignant diseases, it is also applicable in distinguishing among common, nontumorous intestinal diseases. Its advantage is that it is based on five common CT attenuation patterns; its disadvantage is that it is not perfectly discriminating. Perhaps the approach can serve as a stimulus for radiologists to refine the system to attain the latter goal.
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Footnotes
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See the commentary by Federle
following this article.
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References
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Abstract
LEARNING OBJECTIVES FOR TEST...
