AJR 2002; 179:1287-1292
© American Roentgen Ray Society
Budd-Chiari Syndrome: Evaluation with Multiphase Contrast-Enhanced Three-Dimensional MR Angiography
Ay
e Erden1,
lhan Erden1,
Selim Karayalçin2 and
Cihan Yurdaydin2
1 Department of Radiology, Ankara University, Medical School, Talatpaa
Bulvari Sihhiye, 06100 Ankara, Turkey.
2 Department of Gastroenterology, Ankara University, Medical School, Sihhiye,
06100 Ankara, Turkey.
Received March 11, 2002;
accepted after revision May 13, 2002.
Address correspondence to A. Erden.
Introduction
Budd-Chiari syndrome is caused by the obstruction of the hepatic venous
outflow or the inferior vena cava above the hepatic veins. When it is
untreated, the mortality rate for patients is high. Because the clinical
presentation of this syndrome is nonspecific, radiologic investigation and
liver biopsy are important diagnostic steps
[1]. Contrast-enhanced MR
angiography permits morphologic and functional assessment of parenchymatous
organs during the dynamic investigation of the vascular system. The multiphase
nature of this imaging method provides versatile information for the workup of
this particular entity.
We present the spectrum of vascular and hepatic parenchymal abnormalities
in Budd-Chiari syndrome observed on multiphase contrast-enhanced
three-dimensional MR angiography.
Changes in Vascular System
Hepatic Artery
Multiphase contrast-enhanced MR angiography has the major advantage of
allowing both arterial and venous systems of an organ to be studied with one
injection of contrast material. The axial reformations, in addition to the
coronal source images, are useful in showing the origin and course of the
hepatic artery.
The hepatic artery system in Budd-Chiari syndrome has several important
aspects. First, the hepatic artery can be the major supplier of blood to the
liver when the portal vein becomes the draining vein in Budd-Chiari syndrome
[2]. Second, hepatic artery
anatomic variations must be shown in patients with Budd-Chiari syndrome who
are candidates for liver transplantation. Third, narrowing, stretching, or
distortion of the hepatic artery on MR angiography may be the indirect signs
of severe morphologic changes in liver parenchyma
(Fig. 1). Finally,
hepatocellular carcinoma may be associated with Budd-Chiari syndrome
[1,
3] in as many as 6.4% of
patients [4]. Strong
enhancement during the arterial phase is a significant sign of this neoplasm
on multiphase MR angiography of the liver
[5].
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Fig. 1. —Arterial phase coronal maximum-intensity-projection MR image
shows portal hilus at lateral surface of liver (arrow) in 48-year-old
woman with chronic Budd-Chiari syndrome. Consequently, hepatic artery enters
into parenchyma from lateral aspect of liver. Normal anatomic characteristics
of liver segments can no longer be identified. Hepatic artery (HA) is
stretched and displaced inferiorly by enlarged caudate lobe. SA = splenic
artery.
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Portal Vein System
The portal vein and its intrahepatic branches may be influenced by
structural changes of the liver tissue in Budd-Chiari syndrome. Because the
hepatic veins constitute the sole efferent vascular drainage of the liver,
obstruction or increased pressure in these vessels or their radicles results
in increased sinusoidal and portal pressure. In regions with complete hepatic
vein obstruction, resistance to portal flow is increased and may stop and even
reverse. It has been shown that after hepatic venous occlusion, the portal
vein becomes the draining vein, and the occluded area is supplied with
arterial blood alone [2].
An important indication of multiphase contrast-enhanced three-dimensional
MR angiography in Budd-Chiari syndrome is to show the patency of the portal
vein system. In patients with this syndrome, stasis in the portal system may
cause thrombosis [6]
(Fig. 2). The accurate
delineation of the portal system is particularly important when assessing the
possible treatment options (e.g., shunt surgery or transjugular intrahepatic
portosystemic shunt placement). Surgical shunt patency can also be documented
on contrast-enhanced MR portography (Fig.
3).
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Fig. 2. —Portal venous phase coronal MR image shows focal stenosis
(short arrow), which can be residue of thrombotic process, in
superior mesenteric vein at level of gastrocolic trunk in 41-year-old man with
chronic Budd-Chiari syndrome. Note segmental narrowing and angulation of
inferior vena cava (long arrow).
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Fig. 3. —Sagittal maximum-intensity-projection MR image shows patency
of H-graft (arrow) between superior mesenteric vein (SMV) and
inferior vena cava (IVC) in 26-year-old man treated with mesocaval shunt.
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Hepatic Vein System
According to our observations, normal main hepatic veins are best
visualized on subvolume targeted maximum intensity projections obtained in the
craniocaudal direction. The right hepatic vein can also be well depicted on
coronal images because of its parallel orientation to the body axis. However,
the left and middle hepatic veins, which are shorter than the right hepatic
vein, may lead to diagnostic problems particularly if they are compressed by
the distorted liver parenchyma. Thin-caliber but patent hepatic veins that are
obscured in the distorted liver parenchyma may be difficult to visualize. They
can be best identified near the caval confluence.
Sagittal images obtained adjacent to midline seem to be helpful in
displaying the left hepatic vein. Although nonvisualization of hepatic veins
may be suggestive of Budd-Chiari syndrome
(Fig. 4), inadequate time delay
after contrast material administration can be responsible for the
nonvisualization of these veins. Because hepatic circulation is sluggish in
Budd-Chiari syndrome, late venous phase imaging is warranted to visualize the
draining veins on contrast-enhanced MR angiography (Fig.
5A,5B).
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Fig. 4. —Portal venous phase coronal source MR image shows that
hepatic veins (solid arrow), inferior right hepatic vein (open
arrow), and inferior vena cava (arrowhead) are occluded in
32-year-old man with Behçet's symdrome. In this patient, main portal
vein (not shown) was major drainage vein of liver, and predominant parenchymal
supplier was hepatic artery. Note large amount of ascites.
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Fig. 5A. —Contrast-enhanced three-dimensional MR portography performed
in 28-year-old woman with chronic Budd-Chiari syndrome. Coronal source MR
image obtained during early venous phase shows distribution of contrast
material within portal vein radicles. This appearance is due to stasis in
sinusoids and portal venous bed. Contrast material cannot be identified in
hepatic vein (arrow).
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Fig. 5B. —Contrast-enhanced three-dimensional MR portography performed
in 28-year-old woman with chronic Budd-Chiari syndrome. Coronal source MR
image obtained during late venous phase shows enhancement of hepatic vein
(arrow).
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Collateral Veins
MR angiography appears to offer a noninvasive method of evaluating the
intra- and extrahepatic collateral pathways. Identification of intrahepatic
collateral veins (Figs. 6 and
7) is highly suggestive of
Budd-Chiari syndrome [3,
7]. The intrahepatic collateral
vessels divert blood away from the occluded hepatic vein and drain into a
patent hepatic vein or a systemic vein. They can be identified by their
typical tortuous course or curvilinear configuration.
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Fig. 6. —Coronal maximum-intensity-projection image from MR angiogram
shows bridging collaterals (arrowheads) between right hepatic vein
(long arrow) and inferior right hepatic vein (short arrow)
in 25-year-old man in whom Budd-Chiari syndrome developed after surgery for
hydatid disease.
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Fig. 7. —Coronal maximum-intensity-projection image from MR angiogram
shows stenosis (arrow) in inferior right hepatic vein at junction of
inferior vena cava in 45-year-old woman with chronic Budd-Chiari syndrome due
to factor V Leiden mutation. In Budd-Chiari syndrome, main drainage vein of
right lobe is inferior right hepatic vein.
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The sites of extrahepatic collateral veins in Budd-Chiari syndrome are
generally different from those collaterals localized at the portosystemic
communication sites in cirrhosis. Extrahepatic systemic venous collateral
routes in Budd-Chiari syndrome can be evaluated in four groups according to
the classification proposed by Cho et al.
[7]. In Budd-Chiari syndrome,
deep and central tributaries of the systemic circulation (i.e., ascending
lumber veins, vertebral venous plexus, and azygos and hemiazygos veins) are
the most commonly collateralized routes
(Fig. 8). The other collateral
vessels seen in this syndrome are the left renal—hemiazygos pathway
(Fig. 9), inferior
phrenic—pericardiophrenic collaterals
(Fig. 8), and superficial
collaterals of the abdominal wall (Fig.
10). Although collateralized abdominal wall veins are seen even at
physical examination of patients, this finding may not be displayed on MR
angiograms because of the limited size of the selected imaging volume.
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Fig. 8. —Coronal maximum-intensity-projection image from MR angiogram
shows intrahepatic collateral and extrahepatic collateral veins: inferior
right hepatic vein (solid arrow), azygos vein (open arrow),
and left inferior phrenic vein (arrowhead) in 34-year-old man with
chronic Budd-Chiari syndrome.
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Fig. 9. —Coronal oblique maximum-intensity-projection image from MR
angiogram shows communication of left renal vein and hemiazygos vein
(arrow) in 33-year-old man with chronic Budd-Chiari syndrome.
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Fig. 10. —Coronal maximum-intensity-projection image from MR angiogram
reveals abdominal wall collaterals (superficial epigastric veins)
(arrows) ascending laterally before anastomosing with lateral
thoracic vein branches in 36-year-old woman with chronic Budd-Chiari
syndrome.
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Inferior Vena Cava
Contrast-enhanced MR angiography can delineate the inferior vena cava in
great detail throughout its course. In the late venous phases, patency and
structural abnormalities, including a web in the inferior vena cava, can be
shown (Fig. 11). The web has
been shown to be a likely sequela of thrombosis at that level
[1]. It arises from the wall of
the vessel and may obliterate the lumen completely or partially. Thrombosis of
the inferior vena cava (Fig.
12) can be depicted on MR imaging in 27% of patients with
Budd-Chiari syndrome [8].
Stenosis of the inferior vena cava may be associated with external compression
of an enlarged caudate lobe (Fig.
13). The incidence of this pressure effect on the vena cava was
reported to be 23% [8].
Contrast-enhanced three-dimensional MR angiograms may replace the biplane
inferior vena cavograms to rule out the compression of the caudate lobe as a
cause of caval stenosis. This method offers the advantage over conventional
cavography of enabling assessment of the nature of the obstruction (intrinsic
or extrinsic in origin) at the same time as the surrounding soft-tissue
anatomy. Contrast-enhanced MR angiography can also show both proximal and
distal parts of the obstructive lesion.
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Fig. 11. —Coronal maximum-intensity-projection image obtained from
contrast-enhanced three-dimensional MR angiogram shows web (arrow) in
inferior vena cava in 34-year-old-man with chronic Budd-Chiari syndrome. Web
appears to be thin curvilinear membrane located perpendicular to long axis of
inferior vena cava.
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Fig. 12. —Coronal source MR image reveals segmental obstruction of
inferior vena cava in 36-year-old woman with chronic Budd-Chiari syndrome.
Note hypointense cordlike structure at location of inferior vena cava
(arrows).
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Fig. 13. —Coronal late venous phase maximum-intensity-projection MR
image shows narrowing of inferior vena cava due to compression of enlarged
caudate lobe in 28-year-old woman with acute Budd-Chiari syndrome. Note normal
enhancement of this lobe compared with remainder of hepatic parenchyma.
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Changes in Liver Parenchyma
In Budd-Chiari syndrome, the most striking and common change in hepatic
configuration is hypertrophy of the caudate lobe
(Fig. 14). Hypertrophy is
found in 82-91% of all cases
[3,
8,
9] and is related to
independent drainage of this lobe. In the acute stage, the liver may be
globally enlarged owing to vascular congestion
[8,
9]. In the chronic stage,
atrophy of the right lobe of the liver, hypertrophy of the left lobe,
irregularities of liver contours, and presence of regenerative nodules are
prominent features [9].
Nodularities of the hepatic surface may show the progression to cirrhosis.
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Fig. 14. —Portal venous phase coronal maximum-intensity-projection MR
image reveals normally enhancing hypertrophic caudate lobe in 28-year-old
woman with acute Budd-Chiari syndrome. Note hypoperfusion of other segments.
PV = portal vein, SV = splenic vein, SMV = superior mesenteric vein.
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Regional enhancement differences that reflect the hemodynamic disturbance
in the liver in patients with Budd-Chiari syndrome have been already known
from observations on contrastenhanced CT
[9]. Nonenhancement is an
indicator of hypoperfusion, and hypoperfused regions are prone to severe
damage due to anoxia.
Normal or increased enhancement of the caudate lobe (Figs.
13 and
14) is usually seen in acute
forms of Budd-Chiari syndrome because the caudate lobe has separate venous
drainage from the remainder of the liver
[10]. Rarely, subcapsular
enhancement is shown in patients with acute symptoms
(Fig. 15). The reason for
peripheral hepatic enhancement in these patients is probably related to the
independent drainage of the subcapsular regions through their own capsular
veins. A patchy pattern of hepatic enhancement
(Fig. 5) is thought to be
produced by regional stagnation of portal flow
[8]. In some patients with
chronic disease, the signal intensity difference between the peripheral and
central liver is minimal [10].
Thus, a number of features on MR angiography are valuable in understanding the
effect of Budd-Chiari syndrome on the overall function of the liver.
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Fig. 15. —Coronal maximum-intensity-projection image obtained during
portal venous phase of MR angiogram shows subcapsular contrast enhancement
(arrows) in 29-year-old man with acute Budd-Chiari syndrome.
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References
- Dilawari JB, Bambery P, Chawla Y, et al. Hepatic outflow
obstruction (Budd-Chiari syndrome): experience with 177 patients and a review
of the literature. Medicine (Baltimore)
1994;73:21
-36[Medline]
- Murata S, Hai Y, Asato M, et al. Effect of temporary occlusion of
the hepatic vein on dual blood supply in the liver: evaluation with spiral CT.
Radiology
1995;197:351
-356[Abstract/Free Full Text]
- Kim TK, Chung JW, Han JK, Kim AY, Park JH, Choi BI. Hepatic changes
in benign obstruction of the hepatic inferior vena cava: CT findings.
AJR
1999;173:1235
-1242[Abstract/Free Full Text]
- Okuda H, Yamagata H, Obata H, et al. Epidemiological and clinical
features of Budd-Chiari syndrome in Japan. J Hepatol
1995;22:1
-9[Medline]
- Hawighorst H, Schoenberg SO, Knopp MV, Essig M, Miltner P, van
Kaick G. Hepatic lesions: morphologic and functional characterization with
multiphase breath-hold 3D gadolinium-enhanced MR angiography—initial
results. Radiology
1999;210:89
-96[Abstract/Free Full Text]
- Vogelzang RL, Anschuetz SL, Gore RM. Budd-Chiari syndrome: CT
observations. Radiology
1987;163:329
-333[Abstract/Free Full Text]
- Cho O-K, Koo J-H, Kim Y-S, Rhim H-C, Koh B-H, Seo H-S. Collateral
pathways in Budd-Chiari syndrome: CT and venographic correlation.
AJR
1996;167:1163
-1167[Free Full Text]
- Soyer P, Rabenandrasana A, Barge J, et al. MRI of Budd-Chiari
syndrome. Abdom Imaging
1994;19:325
-329[Medline]
- Mathieu D, Vasile N, Menu Y, Van Beers B, Lorphelin JM, Pringot J.
Budd-Chiari syndrome: dynamic CT. Radiology
1987;165:409
-413[Abstract/Free Full Text]
- Noone TC, Semelka RC, Siegelman ES, Balci NC, Hussain SPN, Mitchel
DG. Budd-Chiari syndrome: spectrum of appearances of acute, subacute, and
chronic disease with magnetic resonance imaging. J Magn Reson
Imaging 2000;11:44
-50[Medline]
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Introduction
Changes in Vascular System
