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Pictorial Essay
CT Manifestations of Bowel Ischemia
Chung Kuao Chou 1
B
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
Fig. 1.—51-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. Aorta (A) and superior mesenteric artery (SMA)
were occluded with thrombi-filled false lumen.
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) [1–8]. 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. 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.
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.
Received April 9, 2001; accepted after revision July 11, 2001.
1
Department of Radiology, Chi Mei Foundation Hospital, 901 Chung Hwa Rd., Tainan 71010, Taiwan, Republic of China. Address correspondence to C. K. Chou.
AJR 2002;178:87–91 0361–803X/02/1781–87 © American Roentgen Ray Society
AJR:178, January 2002
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Chou
Persistent Arterial Insufficiency Without
Reperfusion (Pale Ischemic Type)
A
B
Fig. 4.—74-year-old woman with atrial fibrillation.
A, Superior mesenteric arteriogram clearly shows embolus (arrow ) and suboptimally enhanced zones
(arrowheads ).
B, 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.
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 bor-
ders 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 Guerbet93600, Aulnay and S. Bois, Roissy CdG Cedex, France). The dosage was a rapid manual
injection of 100–150 mL.
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 (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. 5.—42-year-old man with smallbowel necrosis. Contrast-enhanced
axial CT scan shows dilated small
bowel with normally enhanced
(arrow ) and unenhanced mucosal
folds (arrowheads ).
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.
5
6
Fig. 7.—76-year-old man with atrial
fibrillation.
A and B, Contrast-enhanced axial
CT scan reveals free gas in smallbowel 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.
A
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B
AJR:178, January 2002
CT of Bowel Ischemia
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.
Fig. 9.—70-year-old man with septic
shock.
A, Unenhanced axial CT scan shows
ascending and transverse colonic
wall was thickened (arrowheads ) and
of attenuation.
B, 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.
A
B
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.
Fig. 11.—70-year-old woman with
atrial fibrillation.
A, Unenhanced axial CT scan shows
intermediate density–thickened transverse colonic wall (arrowhead).
B, 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.
A
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B
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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 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. 7).
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. 9 and 10). As the ruptures between
the damaged endothelial cells further enlarge,
the RBC 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. 12.—84-year-old man with atrial
fibrillation who received digitalis.
A, 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.
B, 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.
A
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.
90
B
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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CT of Bowel Ischemia
A
B
C
Fig. 15.—Three patients with small-bowel volvulus.
A, 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.
B, 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.
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. 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.
Ischemia Due To Closed-Loop SmallBowel 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
AJR:178, January 2002
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).
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.
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 diag-
nosis of bowel ischemia should be based on a
correlation of the image findings, laboratory
data, and clinical history.
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