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Pictorial Essay
November 2002

Budd-Chiari Syndrome: Evaluation with Multiphase Contrast-Enhanced Three-Dimensional MR Angiography

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].
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.

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).
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).
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.

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).
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.
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).
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).

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.
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.
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.
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.
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.
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.
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.

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.
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.
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).
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.

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.
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.
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.
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.

Footnote

Address correspondence to A. Erden.

References

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Information & Authors

Information

Published In

American Journal of Roentgenology
Pages: 1287 - 1292
PubMed: 12388515

History

Submitted: March 11, 2002
Accepted: May 13, 2002

Authors

Affiliations

Ayşe Erden
Department of Radiology, Ankara University, Medical School, Talatpaşa Bulvari Sihhiye, 06100 Ankara, Turkey.
İlhan Erden
Department of Radiology, Ankara University, Medical School, Talatpaşa Bulvari Sihhiye, 06100 Ankara, Turkey.
Selim Karayalçin
Department of Gastroenterology, Ankara University, Medical School, Sihhiye, 06100 Ankara, Turkey.
Cihan Yurdaydin
Department of Gastroenterology, Ankara University, Medical School, Sihhiye, 06100 Ankara, Turkey.

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