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2000 ARRS Executive Council Award II |
1
Department of Radiology, Stanford University Medical Center, 300 Pasteur Dr.,
Rm. H1307, Stanford, CA 94305.
2
Department of Radiology, Mail stop 114, Veterans Administration Palo Alto
Health Care System, 3801 Miranda Ave., Palo Alto, CA 94304.
Received February 24, 2000;
accepted after revision May 31, 2000.
Address correspondence to R. B. Jeffrey.
Abstract
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SUBJECTS AND METHODS. Sonograms of thickened bowel walls were reviewed in 37 patients with proven gastrointestinal abnormalities. Sonographic findings were correlated with clinical presentation, endoscopy, histology, laboratory data, barium studies, and CT.
RESULTS. Twenty-eight patients presented acutely, and nine patients had chronic or subacute disease processes. Two of the 28 patients had concurrent acute and chronic processes. In 27 of 28 patients with acute processes, the abnormal bowel segments were characterized by an echogenic submucosal layer thicker than 2.5 mm. In contrast, nine patients with chronic or subacute processes had relatively uniform hypoechoic thickening of the bowel wall with loss of visualization of a discrete echogenic submucosal layer. CT was available for comparison in 30 of 37 patients. Of the 28 patients with acute abnormalities, the thickened echogenic submucosal layer on sonography corresponded to either low-attenuation submucosal edema (n = 25) or acute submucosal hemorrhage (n = 3).
CONCLUSION. The finding of a thickened submucosal layer suggests an acute disease process of the bowel and corresponds to either submucosal edema or hemorrhage.
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Graded-compression sonography of the bowel was performed using commercially available units (Acuson 128XP or Sequoia systems; Acuson, Mountain View, CA) using high-frequency (7-10 MHz) linear or curvilinear array transducers. Images of the abnormal bowel segment were obtained in transverse and longitudinal planes. Sonograms were reviewed by two radiologists who identified and agreed on the pertinent findings. For each patient, bowel wall thickness was measured as the average of several measurements on multiple images. When a distinct submucosal layer was visualized, its thickness was also measured.
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Twenty-eight patients had acute gastrointestinal abnormalities (1 day to 2 weeks in duration). The final diagnoses in these 28 patients included Crohn's disease (n = 7), pseudomembranous colitis (n = 4), infectious colitis (n = 3), intramural hemorrhage (n = 2), hemorrhagic infarction (n = 1), infarction (n = 1), lupus vasculitis (n = 2), ischemic colitis (n = 3), and one each of ulcerative colitis, diverticulitis, graft-versus-host disease, mesenteric venous obstruction, and appendicitis. Two of the 28 patients (one with lupus vasculitis and one with ulcerative colitis) had acute and chronic disease processes concurrently. In 27 of 28 patients with acute abnormalities, the echogenic submucosal layer was more than 2.5 mm thick (Figs. 1A,1B,2A,2B,3A,3B,4A,4B,4C,4D). The patient with hemorrhagic infarction of 4 days' duration did not fit this pattern and had a complex but predominantly hypoechoic thickened wall (Fig. 5A,5B).
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Nine patients had subacute or chronic gastrointestinal abnormalities (duration of symptoms, >2 weeks). The final diagnoses in these nine patients included ischemic colitis (n = 2), hemorrhage (n = 1), lymphoma (n = 2), carcinoma (n = 2), metastatic breast carcinoma (n = 1), and leiomyosarcoma (n = 1). In addition, two of the 28 patients in the acute category had known concurrent chronic disease processes. These include one case each of lupus vasculitis and ulcerative colitis. Of the 11 patients with chronic gastrointestinal abnormalities, 10 had a pattern of uniformly hypoechoic thickened bowel wall with loss of sonographic visualization of the normal echogenic submucosal layer. In one patient, the echogenic layer was still faintly visible. All 11 patients had clinical, endoscopic, and pathologic findings consistent with chronic abnormalities: ischemia, vasculitis, ulcerative colitis, chronic hemorrhage, or malignancy (Fig. 6A,6B).
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Regardless of the acuity of the disease process, all patients with focal gastrointestinal abnormalities had a thickened bowel wall ranging from 4 to 21 mm in total thickness. The mean total wall thicknesses in the chronic and acute cases were similar, 9.3 and 8.7 mm, respectively. In the chronic cases, the submucosal layer was not identifiable and therefore could not be measured. In the acute cases, the submucosal layers ranged from 2.5 to 6.8 mm, averaging 4.1 mm and accounting for nearly half the total wall thickness.
In all 30 cases in which CT was performed, the location and extent of bowel wall thickening observed on sonography was confirmed. In the three cases of acute hemorrhage (1 infarction), unenhanced CT showed high attenuation (>30 H) in the bowel wall. Isodense thickening (<20 H) was noted in the patient with subacute hemorrhage. In 18 patients with acute disease, the CT findings were typical of the "double ring" or target sign of low attenuation (<20 H), consistent with submucosal edema.
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In one illustrative case, a patient with known ulcerative colitis and prior documented pancolitis had acute left-sided exacerbation (Fig. 4A,4B,4C,4D). Submucosal edema with increased thickness of the submucosal layer was seen on sonography and confirmed on CT in the acute inflamed descending colon. The ascending colon demonstrated chronic changes with hypoechoic thickening. These findings were also confirmed on CT.
One exception to this pattern was evident in a patient with acute hemorrhage of the small bowel accompanied by infarction (Fig. 5A,5B). The bowel wall thickening was predominantly hypoechoic in this patient. It is possible that the associated ischemic necrosis may have substantially disrupted the submucosal layer and affected the sonographic reflectivity of the bowel wall.
CT in patients with submucosal edema results in low attenuation within the bowel wall often producing the double ring or target appearance [17, 18]. One plausible explanation for submucosal edema is that an acute inflammatory or infectious process produces vasodilatation with increased capillary permeability resulting in extravasation of proteinaceous fluid in a loosely packed submucosal layer. This in turn results in increased sonographic reflectivity and a thickened echogenic submucosal layer.
Another cause of increased echogenicity of the submucosal layer was acute hemorrhage. Hyperdense bowel wall thickening (>30 H) was observed on unenhanced CT in three patients who presented with acute intramural hemorrhage.
In contrast, diffuse hypoechoic thickening of the bowel wall with loss of visualization of a discreet submucosal layer correlated with more subacute or chronic disease processes. The differential diagnosis for the pattern of diffuse hypoechoic thickening is quite broad and includes chronic inflammatory or infectious disorders, subacute hemorrhage, ischemia, or neoplasm. Submucosal edema is a nonspecific process and may be related to a variety of gastrointestinal diseases.
One potential value of recognizing the pattern of increased thickness of the submucosal layer is combining the gray-scale findings with color or power Doppler sonography [19, 20]. Submucosal edema in conjunction with hyperemia of the bowel seen on color or power Doppler sonography strongly suggests vasodilatation related to an infectious or inflammatory process.
Intramural hemorrhage, on the other hand, should be accompanied by normal to diminished vascularity [20]. Thus, the gray-scale finding of increased echogenicity of the bowel wall in conjunction with color Doppler sonographic findings may aid in the differential diagnosis of focal abnormalities of the gastrointestinal tract.
In summary, a thickened echogenic submucosal layer observed on sonography is suggestive of an acute gastrointestinal disease process such as submucosal edema or hemorrhage. By contrast, uniformly hypoechoic bowel wall thickening with loss of characteristic strata suggests subacute or chronic disease. These findings in conjunction with color Doppler sonography may aid in more precisely characterizing gastrointestinal lesions.
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