AJR 2002; 178:87-91
© American Roentgen Ray Society
CT Manifestations of Bowel Ischemia
Chung Kuao Chou1
1
Department of Radiology, Chi Mei Foundation Hospital, 901 Chung Hwa Rd.,
Tainan 71010, Taiwan, Republic of China.
Received April 9, 2001;
accepted after revision July 11, 2001.
Address correspondence to C. K. Chou.
Introduction
Bowel 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). Bowel 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)
[1,2,3,4,5,6,7,8].
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.
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-93600, Aulnay and S. Bois, Roissy CdG Cedex, France). The
dosage was a rapid manual injection of 100-150 mL.
Persistent Arterial 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. At this moment, the CT shows a thin, poorly or suboptimally
enhanced bowel wall (Fig.
1,2,3,4A,4B).
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 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 RBC 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 RBC 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. As
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.
7A,7B).
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Fig. 1. —51-year-old man with aortic dissection. Patient did not
receive oral contrast material as evidenced by low-density gastric fluid.
Contrast-enhanced axial CT scan reveals clear distinction between normally
enhanced (arrows) and unenhanced (arrowheads) collapsed
small-bowel loops. Normally enhanced duodenum and proximal jejunum were
supplied by anastomotic branches from gastroduodenal artery and possible
minimally patent jejunal artery. Aorta (A) and superior mesenteric artery
(SMA) were occluded with thrombi-filled false lumen.
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Fig. 2. —63-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.
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Fig. 3. —62-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.
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Fig. 4B. —74-year-old woman with atrial fibrillation. Superior
mesenteric arteriogram (same as A) 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.
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Fig. 6. —76-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.
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Fig. 7A. —76-year-old man with atrial fibrillation. Contrast-enhanced
axial CT scan reveals free gas in small-bowel mucosal folds and bowel wall
(arrows, A), ascending colonic wall (c), and mesenteric
(arrowhead) and intrahepatic portal veins. Poor portal perfusion of
zones (asterisks, B) supplied by gas-filled portal veins was
noted.
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Fig. 7B. —76-year-old man with atrial fibrillation. Contrast-enhanced
axial CT scan reveals free gas in small-bowel mucosal folds and bowel wall
(arrows, A), ascending colonic wall (c), and mesenteric
(arrowhead) and intrahepatic portal veins. Poor portal perfusion of
zones (asterisks, B) supplied by gas-filled portal veins was
noted.
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Transient Arterial 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.
9A,9B
and 10). As the ruptures
between the damaged endothelial cells further enlarge, the RBC also leak,
resulting in a thickened soft-tissue-density bowel wall with or without
mucosal enhancement (Figs.
11A,11B
and
12A,12B).
The thickened mucosal folds or thumprinting 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.
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Fig. 8. —57-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.
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Fig. 9B. —70-year-old man with septic shock. 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.
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Fig. 10. —64-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.
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Fig. 11B. —70-year-old woman with atrial fibrillation. Contrast-enhanced
axial CT scan obtained after IV contrast administration shows bowel wall was
enhanced (arrowhead), with increase of approximately 30-40 H on
average, consistent with contrast medium extravasation into hemorrhagic
wall.
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Fig. 12A. —84-year-old man with atrial fibrillation who received
digitalis. Contrast-enhanced axial CT scan shows mucosa was normally enhanced
(black arrowheads). Submucosa shows either edematous change
(arrow), nearly isodense to ascites, or hemorrhagic change (white
arrowhead), hyperdense to ascites.
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Fig. 12B. —84-year-old man with atrial fibrillation who received
digitalis. Angiogram obtained during venous phase shows normal mucosal
enhancement (arrowhead) and thickened unenhanced submucosa
(arrow), indicating submucosa has been mainly occupied by reperfused
extravasated blood.
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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 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. As 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.
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Fig. 13. —77-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.
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Fig. 14. —68-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.
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Ischemia Due To Closed-Loop Small-Bowel Obstruction
Closed loop small-bowel obstruction is caused by adhesion, incarcerated
hernia, or volvulus. Both the artery and vein are compressed. Because 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.
15A). 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. 15B).
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Fig. 15A. —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.
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Fig. 15B. —Three patients with small-bowel volvulus. Contrast-enhanced
axial CT scan shows that closed bowel loop (arrowheads) in
48-year-old man was nearly totally filled with fluid. Bowel wall was thin and
unenhanced.
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Mesenteric edema or hemorrhage (Fig.
15A) 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 RBC are released
into the lumen (Fig. 15C).
This appearance may occur in all of the conditions previously mentioned.
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Fig. 15C. —Three patients with small-bowel volvulus. 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.
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Bowel 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. A correct diagnosis of bowel
ischemia should be based on a correlation of the image findings, laboratory
data, and clinical history.
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Introduction
Persistent Arterial...
