Fig year-old man with aortic dissection. Contrast-enhanced
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1 Pictorial Essay CT Manifestations of owel Ischemia Chung Kuao Chou 1 owel ischemia represents a process of insufficient blood supply of the small or large bowel with the consequences ranging from a transient, totally reversible attack to a lethally catastrophic event. This condition may result directly from arterial occlusion (thromboembolism of the superior mesenteric artery or its branches, vasculitis of various autoimmune diseases, and external compression of the artery by adhesion, volvulus, hernia, and intussusception), hypotension (congestive heart failure, hypovolemia, and sepsis), or vasoconstrictive medications (digitalis, norepinephrine, and ergotamine). owel ischemia may also be associated with impaired venous drainage (thrombosis of the mesenteric and portal veins, interference of intramural venous outflow by distention and elevated intraluminal pressure that occurs proximal to a stenotic lesion, and compression of the mesenteric veins by tumor, adhesion, volvulus, hernia, and intussusception) [1 8]. The severity of the ischemic attack depends on the acuteness, duration, degree, and state of the collateral circulation; extent of the involved area; and promptness in correcting the underlying pathologic process. The damage starts with the mucosa, which is most vulnerable to the ischemic insult, extends outward through the submucosa and the proper muscular layer, and ends at the serosa. The extent of the injury may range from mucosal, to mural, to transmural necrosis. We describe different conditions of the ischemic event and their corresponding CT appearances. Fig year-old man with aortic dissection. Patient did not receive oral contrast material as evidenced by lowdensity gastric fluid. Contrast-enhanced axial CT scan reveals clear distinction between normally enhanced (arrows) and unenhanced (arrowheads) collapsed smallbowel loops. Normally enhanced duodenum and proximal jejunum were supplied by anastomotic branches from gastroduodenal artery and possible minimally patent jejunal artery. orta () and superior mesenteric artery (SM) were occluded with thrombi-filled false lumen. Fig year-old man with aortic dissection. Contrast-enhanced axial CT scan shows wall of fluid-distended small-bowel loops either normally enhanced (arrow) or totally unenhanced (arrowheads). Unenhanced bowel wall was isodense and not differentiable from intraluminal fluid. Fig year-old woman with abdominal angina. Contrast-enhanced axial CT scan shows some small-bowel loops (arrowhead) with bowel wall density lower than other loops (arrow) but higher than luminal fluid. This enhancement is graded as suboptimal, implying that blood flow is present but less than normal. Received pril 9, 2001; accepted after revision July 11, Department of Radiology, Chi Mei Foundation Hospital, 901 Chung Hwa Rd., Tainan 71010, Taiwan, Republic of China. ddress correspondence to C. K. Chou. JR 2002;178: X/02/ merican Roentgen Ray Society JR:178, January
2 Chou Fig year-old woman with atrial fibrillation., Superior mesenteric arteriogram clearly shows embolus (arrow) and suboptimally enhanced zones (arrowheads)., Superior mesenteric arteriogram (same as ) obtained during venous phase shows suboptimally enhanced zones (arrowheads) with much less venous return than normally enhanced zones (arrow). This indicates intermediate degree of blood supply between normally enhanced and nearly totally unenhanced status. The CT examinations were performed on a Sytec 4000 scanner (General Electric Medical Systems, Milwaukee, WI). The slice thickness was 7 or 10 mm with a gap of 3 or 0 mm, respectively. Oral contrast medium was not routinely used. The unenhanced images were taken from the diaphragm to the lower borders of the kidneys. The enhanced images were taken from the diaphragm to the symphysis pubis. The IV contrast medium used was Telebrix 30 meglumine (Laboratorie Guerbet , ulnay and S. ois, Roissy CdG Cedex, France). The dosage was a rapid manual injection of ml. Persistent rterial Insufficiency Without Reperfusion (Pale Ischemic Type) Sometimes, the ischemic event persists long enough without reperfusion and becomes destined to its final outcome: necrosis of the whole bowel wall. The intramural arteriocapillaries first lose part of their volume as the earlier entered blood flows out from the veins, even though some blood may seep back from the veins. t this moment, the CT shows a thin, poorly or suboptimally enhanced bowel wall (Figs. 1 4). Occasionally, detailed ischemic mucosal folds can be seen (Fig. 5). Poor enhancement along the antimesenteric side is suggestive of nonocclusive ischemia (Fig. 6). The intestinal fluid is decreased because the enterocytes cannot produce a normal amount of secretions if the arterial supply is blocked. The bowel wall is first pale and then turns to black and becomes thinned as a result of intravascular volume loss and collapse of necrotic tissue [1, 5]. Not uncommonly, the infarcted bowel is described as grossly dark red or purple and filled with bloody fluid. In fact, this description represents a reperfused instead of a nonreperfused ischemic bowel because there should not be a lot of erythrocytes or plasma extravasating through the damaged and Fig year-old man with smallbowel necrosis. Contrast-enhanced axial CT scan shows dilated small bowel with normally enhanced (arrow) and unenhanced mucosal folds (arrowheads). 5 6 Fig year-old man with hypotension before CT examination. Contrast-enhanced axial CT scan reveals some small-bowel loops with poor wall enhancement along antimesenteric side (arrowheads), so-called watershed zone, consistent with nonocclusive ischemia. Fig year-old man with atrial fibrillation. and, Contrast-enhanced axial CT scan reveals free gas in smallbowel mucosal folds and bowel wall (arrows, ), ascending colonic wall (c), and mesenteric (arrowhead) and intrahepatic portal veins. Poor portal perfusion of zones (asterisks, ) supplied by gas-filled portal veins was noted. 88 JR:178, January 2002
3 CT of owel Ischemia Fig year-old man with aortic dissection. Contrast-enhanced axial CT scan shows mucosa was edematous and suboptimally enhanced (arrow) compared with other normally enhanced mucosa (arrowhead). Submucosal edema was evident. Fig year-old man with septic shock., Unenhanced axial CT scan shows ascending and transverse colonic wall was thickened (arrowheads) and of attenuation., Contrast-enhanced axial CT scan shows mucosa was normally enhanced (arrow ) after IV contrast administration. Edematous submucosa (arrowhead) reveals mild enhancement, with increase of approximately 10 H on average, indicating contrast medium extravasation. Fig year-old man with paroxysmal atrial fibrillation. Superior mesenteric arteriogram obtained during venous phase shows contrast medium stasis in thickened wall (arrow) consistent with contrast extravasation into edematous submucosa during reperfusion stage. Fig year-old woman with atrial fibrillation., Unenhanced axial CT scan shows intermediate density thickened transverse colonic wall (arrowhead)., Contrast-enhanced axial CT scan obtained after IV contrast administration shows bowel wall was enhanced (arrowhead), with increase of approximately H on average, consistent with contrast medium extravasation into hemorrhagic wall. JR:178, January
4 Chou ruptured microvascular wall into the mucosa, submucosa, or bowel lumen if the arterial supply is severely reduced, either occlusively or nonocclusively, without a subsequent reperfusion taking place. Microscopically, inflammatory cell infiltration in response to bacterial invasion is much more prominent than RC extravasation in the nonreperfused attenuated wall. The evolution of bloody diarrhea or bloody intraluminal fluid is most likely due to an outpouring of the reperfused blood from the infarcted mucosa or submucosa into the lumen. Even though the residual blood in the capillaries that flows back from the venules may cause extravasation of RC in the mucosa (lamina propria of the villi) or scattered hemorrhagic foci in the submucosa or subserosa, it is unlikely for this small amount of hemorrhage to cause considerable wall thickening. s bacteria proliferate and more gas is produced, the intraluminal gas may dissect into the necrotic wall (pneumatosis intestinalis), spread through the mesenteric veins, and finally flow into the portal veins (Fig. 7). Transient rterial Insufficiency with Subsequent Reperfusion (Hemorrhagic Type) If the pathologic processes were corrected (by lysis of the embolus, reestablishment of blood pressure, release of external compression, or prompt development of collateral circulation), the reentered blood might cause different CT appearances, depending on the degree of disruption of the vascular wall integrity. The intestinal microvessel derives its oxygen supply through direct diffusion from the blood. When the arterial supply is insufficient for a certain period and returns later, the microvascular endothelium and the mucosal epithelium become damaged, and the permeability increases proportionately to the duration of oxygen deprivation and the degree of the reperfusion injury. If the degree is mild, only water molecules leak into the extravascular space and cause a mucosal or submucosal edema appearance on CT (Fig. 8). When the damage becomes more severe, the molecules of contrast medium follow the previously escaped fluid and cause various degrees of mucosal or submucosal enhancement (Figs. 9 and 10). s the ruptures between the damaged endothelial cells further enlarge, the RC also leak, resulting in a thickened softtissue-density bowel wall with or without mucosal enhancement (Figs. 11 and 12). The thickened mucosal folds or thumbprinting appearance seen radiologically are caused by submucosal edema or hemorrhage. The mucosa may remain intact or become necrotic. In the case of reperfusion, the bowel is grossly dark red, the wall is thickened, and the lumen is largely filled with bloody fluid in contrast with appearances of the nonreperfused condition. Impaired Venous Drainage When the mesenteric venous drainage is impaired, the intravascular volume increases, and the hydrostatic pressure rises as the arterial blood continues flowing into the capillary bed and venules of the bowel and mesentery. The elevated hydrostatic pressure causes the molecules of water or contrast material, or Fig year-old man with atrial fibrillation who received digitalis., Contrast-enhanced axial CT scan shows mucosa was normally enhanced (black arrowhead). Submucosa shows either edematous change (arrow), nearly isodense to ascites, or hemorrhagic change (white arrowhead), hyperdense to ascites., ngiogram obtained during venous phase shows normal mucosal enhancement (arrowhead) and thickened unenhanced submucosa (arrow), indicating submucosa has been mainly occupied by reperfused extravasated blood. Fig year-old woman with portal vein encasement by tumor infiltration. Contrast-enhanced axial CT scan shows mucosa (arrowheads) was not enhanced and not differentiable from submucosal edema. Other small bowels showed various degrees of enhancement. Fig year-old man with adhesion-induced small-bowel obstruction. Contrast-enhanced axial CT scan shows mucosa was normally enhanced and submucosa was thickened and of various densities (arrows), indicating extravasation of contrast material or blood. 90 JR:178, January 2002
5 CT of owel Ischemia C Fig. 15. Three patients with small-bowel volvulus., Contrast-enhanced axial CT scan shows small bowel in 76-year-old man with normal mucosal enhancement (arrowhead) and submucosal enhancement or hemorrhage (arrow). Mesentery (asterisk) has density higher than simple fluid, consistent with hemorrhagic component., Contrast-enhanced axial CT scan shows that closed bowel loop (arrowheads) in 48-year-old man was nearly totally filled with fluid. owel wall was thin and unenhanced. C, Contrast-enhanced axial CT scan shows intermediate density of luminal fluid (asterisk) in 40-year-old woman was consistent with, but not diagnostic of, bloody contents, which was confirmed by surgical specimen. even the erythrocytes, to escape through the enlarged fenestrations of the stretched arteriocapillary endothelium into the submucosa, appearing as submucosal and mesenteric edema or hemorrhage on CT (Figs. 13 and 14). These appearances are similar to those of reperfused ischemia previously described. However, the mechanism is different from that of a directly arterial origin, which is caused by oxygen-deprived and free radical-induced disruption of vascular wall integrity and resultant increased permeability. s the tissue tension in the extravascular compartment of the submucosa increases, the arterial supply may be compromised and the mucosal enhancement decreased. Tissue tension may reach an extent sufficient to cause a complete failure of the arterial supply because of stasis of blood flow or thrombosis of small arterioles and subsequent bowel necrosis (Fig. 13). The mesenteric veins are usually engorged during this condition. Ischemia Due To Closed-Loop Small- owel Obstruction Closed loop small-bowel obstruction is caused by adhesion, incarcerated hernia, or volvulus. oth the artery and vein are compressed. ecause the arterial pressure is higher than the venous pressure, the arterial inflow is usually more than the venous outflow. Thus, the CT appearances are similar to those of impaired venous drainage (Fig. 15). The relatively rich arterial supply may contribute to increased intestinal secretions and rapid fluid-filling of the lumen of the closed bowel loop, which is occluded at both ends. Theoretically, the arterial supply is still adequate if the mucosal enhancement is normal. If the artery were compressed more tightly, the wall enhancement might be suboptimal, and the thickness would not be increased. If the compression is tight enough from the beginning of the obstruction, the wall might be thin and totally unenhanced, similar to that of nonreperfused ischemia (Fig. 15). Mesenteric edema or hemorrhage (Fig. 15) may result from increased vascular permeability as a result of oxygen deprivation or elevated intravascular hydrostatic pressure caused by impaired venous drainage, even though the latter is more common and prominent. Mesenteric vascular engorgement usually occurs with impaired venous drainage. The density of the intraluminal fluid may be increased if RC are released into the lumen (Fig. 15C). This appearance may occur in all of the conditions previously mentioned. owel ischemia may result from a broad spectrum of diseases and may have different appearances depending on various mechanisms and stages. Different appearances may coexist in adjacent segments. correct diagnosis of bowel ischemia should be based on a correlation of the image findings, laboratory data, and clinical history. References 1. Patel, Kaleya RN, Sammartano RJ. Pathophysiology of mesenteric ischemia. In: oley SJ, randt LJ, eds. Surgical clinics of North merica. Philadelphia: Saunders, 1992: Mitsudo S, randt LJ. Pathology of intestinal ischemia. In: oley SJ, randt LJ, eds. Surgical clinics of North merica. Philadelphia: Saunders, 1992: Whitehead R, Gratama S. The large intestine. In: Whitehead R, ed. Gastrointestinal oesophageal pathology. New York: Churchill Livingstone, 1995: artnicke J, alfe DM. CT appearance of intestinal ischemia and intramural hemorrhage. Radiol Clin North m 1994;32: Taourel PG, Deneuville M, Pradel J, Regent D, ruel JM. cute mesenteric ischemia: diagnosis with contrast-enhanced CT. Radiology 1996;199: althazar EJ, Liebeskind 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: Rha SE, Ha HK, Lee SH, et al. CT and MR imaging findings of bowel ischemia from various primary causes. RadioGraphics 2000;20: Zalcman M, Sy M, Donckier V, Closset J, Gansbeke DV. Helical CT signs in the diagnosis of intestinal ischemia in small-bowel obstruction. JR 2000;175: JR:178, January
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