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Jiang
Lin, Xiao-Hai Chen, Kang-Rong Zhou, Zu-Wang Chen, Jian-Hua Wang, Zhi-Ping
Yan, Ping Wang, Department of Radiology, Affiliated Zhongshan
Hospital, Fudan University, Shanghai 200032, China
Correspondence to: Dr. Jiang Lin, Department of Radiology,
Affiliated Zhongshan Hospital, Fudan University, Shanghai 200032,
China. linjiang@zshospital.net
Telephone: +86-21-64041990 Ext 2463
Fax: +86-21-64038472
Received: 2003-04-02
Accepted: 2003-05-11
Abstract
AIM: To evaluate the role of three-dimensional contrast-enhanced
magnetic resonance angiography (3D CE MRA) in the diagnosis of Budd-Chiari
syndrome (BCS).
METHODS:
Twenty-three patients with BCS underwent 3D CE MRA examination, in
which 13 cases were secondary to either hepatocellular carcinoma (11
cases), right adrenal carcinoma (1 case) or thrombophlebitis (1
case) and 10 suffered from primary BCS. The patency of the inferior
vena cava (IVC), hepatic and portal veins as well as the presence of
intra- and extrahepatic collaterals, liver parenchymal abnormalities
and porto-systemic varices were evaluated. Inferior vena cavography
was performed in 10 cases. The diagnosis of IVC obstruction by 3D CE
MRA was compared with that demonstrated by inferior vena cavography.
RESULTS:
The major features of BCS could be clearly displayed on 3D CE MRA.
Positive hepatic venous signs included tumor thrombosis (9 cases),
tumor compression (2 cases), nonvisualization (4 cases) and focal
stenosis (2 cases). Positive IVC findings were noted as severe
stenosis or occlusion (10 cases), tumor invasion (2 cases),
thrombosis (3 cases), thrombophlebitis (1 case) and septum formation
(3 cases). Intrahepatic collaterals were shown in 9 patients, 2 of
them with "spider web" sign. The displayed extrahepatic
collaterals included dilated azygos and hemi-azygos veins (13 cases)
and left renal-inferior phrenic-pericardiophrenic veins (2 cases).
The occlusion of the left intrahepatic portal veins was found in 2
cases. Porto-systemic varices were detected in 10 patients. Liver
parenchymal abnormalities displayed by 3D CE MRA were enlargement of
the caudate lobe (7 cases), heterogenous enhancement (18 cases) and
complicated tumors (13 cases). Compared with the inferior vena
cavography performed in 10 cases, the accuracy of 3D CE MRA was 100
% in the diagnosis of IVC obstruction.
CONCLUSION:
3D CE MRA can display the major features of BCS and provide an
accurate diagnosis.
Lin
J, Chen XH, Zhou KR, Chen ZW, Wang JH, Yan ZP, Wang P. Budd-Chiari
syndrome: Diagnosis with three-dimensional contrast-enhanced
magnetic resonance angiography. World J Gastroenterol
2003; 9(10):2317-2321
http://www.wjgnet.com/1007-9327/9/2317.asp
INTRODUCTION
Budd-Chiari syndrome (BCS) is a rare disease caused by the
obstruction of the hepatic venous outflow or the inferior vena cava
(IVC) above the hepatic vein[1]. It often occurs
secondary to intrinsic vascular thrombosis, hepatic tumor
invasion/compression, or associates with an idiopathic obstructing
membrane[1,2]. The clinical signs of ascites, abdominal
pain and hepatomegaly are the typical triad of BCS. Since these
signs are nonspecific, the clinical diagnosis of this syndrome is
difficult. Conventionally, X-ray angiography and/or liver biopsy are
used to confirm the diagnosis of BCS with the limitation of
invasiveness. Ultrasound (US), computed tomography (CT) and magnetic
resonance imaging (MRI) are the noninvasive imaging techniques
currently used in the evaluation of the patency of hepatic veins,
IVC and portal vein. However, some limitations are also existed in
each of these modalities[2-7].
Three-dimensional
contrast-enhanced magnetic resonance angiography (3D CE MRA) is a
new technique and widely used in the imaging of the arterial system,
portal venous system and central venous system[8-16].
However, to our knowledge, few studies have been reported so far
concerning its use in the diagnosis of BCS[17].
Therefore, this study was conducted to evaluate the usefulness of
this technique in the imaging of BCS and to present various findings
of BCS demonstrated on 3D CE MRA.
MATERIALS
AND METHODS
Patients
Twenty-three patients with BCS underwent 3D CE MRA. There
were 20 men and 3 women ranging from 26 to 56 years of age (average
age 38 years). In 11 patients, BCS was secondary to the invasion and
occlusion of the hepatic vein and/or IVC by hepatocellular carcinoma
(HCC). In 1 patient, BCS was resulted from tumor invasion of IVC by
right adrenal carcinoma. In 1 patient, IVC obstruction was due to
superior extension of pelvic thrombophlebitis. The above 13 patients
were considered to be secondary BCS. Ten patients had primary BCS
with an unknown origin. The diagnosis of BCS was confirmed by
inferior vena cavography in 10 cases, percutaneous liver biopsy in 2
cases, and surgery in 5 cases. The diagnosis of the remaining 6
cases was confirmed by combined color Doppler sonography and
contrast-enhanced CT.
3D
CE MRA examination
All scans were performed using a 1.5T MR imager (Signa,
General Electric Medical Systems, Milwaukee, WI.) and a body coil.
After the localizing images were obtained, a breathhold T1-weighted
fast multiplanar spoiled gradient-echo(FMPSPGR) sequence (repetition
time/echo time, 150/4.2 msec; flip angle, 90°; field of view, 360
mm; matrix, 128×256; 18 slices; slice thickness, 7.0 mm; gap, 3.0
mm; one signal acquired) and a respiratory-triggered T2-weighted
fast spin-echo sequence (repetition time/echo time, 2800-4200/80
msec; echo train length 8-12, field of view, 360 mm; matrix, 128×256;
18 slices; slice thickness, 7.0 mm; gap, 3.0 mm; 2 signals acquired)
were performed in the liver. For 3D CE MRA, a breath-hold 3D fast
spoiled gradient-echo sequence (repetition time/echo time,
5.2-10.2/1.2-1.9 msec; flip angle, 30° or 45°; field of view,
360-480 mm; matrix, 128×256; imaging volume, 75-168 mm; number of
partitions, 24-30; one signal acquired; and acquisition time, 19-28
sec) was used.
With
T1-weighted and T2-weighted images as reference, the imaging volume
of 3D CE MRA was acquired in a coronal plane to cover the hepatic
veins, IVC, portal veins and collateral vessels. The imaging volume
was determined by a radiologist depending on each patient′s
abnormalities, liver size and ability of breathholding.
A
gadolinium chelate called gadopentetate-dimeglumine (Magnevist;
Schering AG, Berlin, Germany) was used as a contrast material for
all examinations, with a concentration of 0.15 mmol per kilogram of
body weight. In all cases the contrast material was injected by an
experienced MR technician through an antecubital vein with an
injection rate of approximately 3 ml/sec. In 2 patients, however,
due to poor visualization of IVC after injection of the contrast
material into an arm vein, the study was repeated and the contrast
agent was injected via a pedal vein for assessment of IVC. Scanning
was commenced immediately after the injection and repeated three
times with a 6-second delay between each acquisition for patient's
breathing. The first acquisition was the imaging of the arterial
phase, the second acquisition was the portal venous phase for
demonstration of the portal vein and IVC, while the third
acquisition coincided with the image of the late venous phase for
visualization of the hepatic veins. Source images of each
acquisition were reviewed first, and then these images were
reconstructed on a workstation (Advantage windows workstation,
General Electric Medical Systems, Milwaukee, WI) to produce
projectional images like X-ray angiography. Both maximum intensity
projection (MIP) and multiplanar reconstruction (MPR) techniques
were employed to analyze the acquired image.
Image
analysis
3D CE MRA images were reviewed together by two radiologists
unaware of the patients' clinical statuses and other imaging
findings. The patency of the hepatic veins, IVC and portal veins was
assessed. The presence of intra- and extrahepatic collaterals, liver
parenchymal abnormalities and porto-systemic varices were also
noted. Inferior vena cavography was performed in 10 cases. The
diagnosis of IVC obstruction by 3D CE MRA was compared with that
demonstrated by inferior vena cavography.
RESULTS
3D CE MRA findings
Hepatic veins 3D
CE MRA demonstrated tumor thrombosis of two or three hepatic veins
in each of the 9 patients with HCC (Figure 1). The right and middle
hepatic veins were severely compressed and distorted by HCC in 2
patients. Nonvisualization of hepatic veins occurred in 4 patients
with primary BCS. Focal stenosis of the right and middle hepatic
veins near the caval confluence was detected in 2 patients with
primary BCS (Figure 2).
IVC Severe
stenosis or occlusion of the IVC was found in 10 patients (Figure
3), 3 of them were associated with the external compression or
direct invasion of IVC by HCC. Tumor thrombosis was found in 3 cases
with HCC (Figure 1). Direct invasion of IVC by right adrenal tumor
was observed in 1 case. Thrombosis of IVC was shown in 1 patient
with pelvic thrombophlebitis. A septum or obstructing membrane was
demonstrated in the IVC in 3 patients (Figure 4). Localized
dilatation of the distal IVC and renal veins were shown in 2 cases
with IVC obstruction. In 10 patients with inferior vena cavography,
the site and extent of IVC obstruction and distribution of
collaterals presented by 3D CE MRA were in agreement with those by
cavography (Figure 3). The accuracy of 3D CE MRA was 100 % in the
diagnosis of IVC obstruction.
Figure
1 Source image
of three-dimensional contrast-enhanced magnetic resonance
angiography shows tumor thrombosis of the right hepatic vein (short
arrow) and inferior vena cava (long arrow). A hypointense
hepatocellular carcinoma (arrowhead) is shown simultaneously.
Figure 2 A:
Axial reconstruction of three-dimensional contrast-enhanced magnetic
resonance angiography demonstrates focal stenosis of right and
middle hepatic veins (arrow heads). Intrahepatic collateral between
right hepatic vein and subcapsular vein is also demonstrated
(arrow). B: Coronal
reconstruction reveals fine collaterals between hepatic veins
(arrows), resembling a "spider web".
Intra-and
extrahepatic collaterals 3D
CE MRA revealed fine venous collaterals between the right hepatic
veins and subcapsular veins, and between the right, middle and left
hepatic veins in 2 patients with focal hepatic vein stenosis,
appearing as the typical "spider web" sign (Figure 2B).
Large and tortuous veins between enlarged right inferior accessory
hepatic veins and right main hepatic veins were identified in 3
patients with IVC occlusion (Figure 3B). Various extrahepatic
collaterals were found in the abdominal wall, peritoneal and
retroperitoneal areas. Prominent azygos and hemiazygos veins were
demonstrated in 13 patients. The left renal-inferior
phrenic-pericardiophrenic collaterals were displayed in 2 patients
(Figure 5).
Portal veins and porto-systemic varices
The portal veins were found patent in all observed patients
except 2 whose left intrahepatic portal veins were occluded (Figure
6). Gastroesophageal/esophageal varices and spontaneous spleno-renal
shunts were identified in 8 and 2 patients respectively.
Liver parenchyma An
enlarged caudate lobe was found in 7 patients. Heterogenous liver
enhancement was observed in 18 cases (Figure 6). HCC, which showed
hyperintensity in arterial phase and hypointensity in portal venous
phase, was found in 13 patients (Figure 1). In 2 of them, the tumor
was developed after the primary BCS formation, because these two
patients underwent long-term follow-up studies and the initial
imaging findings indicated no intrahepatic tumors.
Figure
3 A:
Source image depicts occlusion of the inferior vena cava(arrowhead).
B: Maximum intensity
projection of three-dimensional contrast-enhanced magnetic resonance
angiography depicts tortuous intrahepatic collaterals (arrows)
between right inferior accessory hepatic vein and right main hepatic
vein. C: Inferior
vena cavography confirms the occlusion of the inferior vena cava
(arrowhead) and the intrahepatic collaterals (arrow).
Figure 4
Three-dimensional contrast-enhanced magnetic resonance
angiography identifies a septum (arrowheads) in the inferior vena
cava.
Figure 5
Three-dimensional contrast-enhanced magnetic resonance
angiography detects occlusion of the inferior vena cava(white
arrowheads), prominent left renal-inferior phrenic-pericardiophrenic
collaterals (arrows) and esophageal varix(black arrowhead).
Figure 6
Three-dimensional contrast-enhanced magnetic resonance
angiography demonstrates occlusion of the left portal vein
(arrowhead) and heterogeneous enhancement pattern of the liver
(arrows).
DISCUSSION
BCS is difficult to be diagnosed clinically. However, accurate
and early diagnosis is important for its treatment. Radiologic
assessment is an important step for its diagnosis. Diagnosis by US
was noninvasive, relatively inexpensive and readily available, but
its accuracy was limited by operator's experience, poor acoustic
window, inaccessible anatomic structure and body forms[1,3,7].
Contrast-enhanced CT was readily available too, but it used ionizing
radiation and required intravenous administration of a large amount
of iodinated contrast material with the risk of nephrotoxicity and
possible allergic reactions[1,5,6]. X-ray angiography was
the reference criteria for the evaluation of BCS, due to its superb
spatial resolution[1,3], but it was invasive and
uncomfortable. Like CT, it also involved radiation and use of
iodinated contrast material. Disadvantages also included high cost,
requirement of operator's expertise (especially for hepatic
venography), and associated complications such as hemorrhage. MRI
and non-enhanced magnetic resonance angiography (MRA) with
time-of-flight (TOF) and phase-contrast (PC) techniques were other
non-invasive means for demonstrating the hepatic venous system, but
were limited by long acquisition time, motion and flow artifacts,
and saturation effects[2,4,18-21].
3D
CE MRA is a recently developed, non-invasive, fast and easy to be
performed technique, which is capable of depicting vascular anatomy
in multiple projections. It involves no radiation. With this
technique, the imaging of the hepatic veins, IVC and portal veins is
accomplished with only one injection of contrast material and short
breath holding. It requires only a peripheral venous injection of a
small amount of gadolinium, which is much safer than iodine-based
contrast material. By using gadolinium to shorten the T1 value of
the blood, it overcomes flow artifacts and saturation effects in TOF
and PC. Moreover, it permits assessment of liver parenchyma and
extravascular abnormalities during investigation of the vascular
system[12,15,17]. So 3D CE MRA has many advantages over
the currently more conventional methods for imaging the BCS.
According
to our study, 3D CE MRA was able to demonstrate the patency of the
hepatic veins, IVC and portal veins. It could show intra- and
extrahepatic collaterals as well as porto-systemic varices caused by
cirrhosis. 3D CE MRA could distinguish extravascular compression
from intravascular thrombosis, detect liver abnormalities and
evaluate the extent of the disease. By means of only one
examination, 3D CE MRA provided all these crucial information for
accurate diagnosis of BCS and for possible surgical or
interventional managements, such as porto-caval shunt, liver
transplantation, transjugular intrahepatic porto-systemic shunt (TIPSS),
percutaneous transluminal angioplasty (PTA) and stent placement[22-27].
Among
13 patients of secondary BCS, tumor thrombosis, external compression
and direct invasion of hepatic veins and/or IVC by tumors were the
main causes of this disease. Through demonstration of intra- and
extrahepatic disorders and the involved blood vessels, 3D CE MRA
could disclose the etiology of BCS. For patients with primary BCS,
nonvisualization, focal stenosis of the hepatic veins, occlusion or
a septum formed in IVC were the most common findings on 3D CE MRA,
as have been reported by Miller et al[5] with CT
and MRI techniques. Compared with vena cavography, 3D CE MRA was 100
% accurate in diagnosis of IVC obstruction. On the basis of this
study and Erden's report[17], 3D CE MRA could replace
inferior vena cavography for diagnosing IVC obstruction.
3D
CE MRA could evaluate the intra- and extrahepatic collateral
pathways. Identification of intrahepatic collateral veins is highly
suggestive of BCS[6,17,28]. The intrahepatic collateral
veins divert blood away from the stenotic or occluded hepatic vein
and into a patent hepatic vein or a systemic vein. According to
Cho's report[6], intrahepatic collaterals were poorly
defined on contrast-enhanced CT. In this study, 3D CE MRA found
these collateral veins in 2 patients with stenosis of the hepatic
veins. On 3D CE MRA, they were identified either by typical
"spider web" sign or by large connecting veins between
accessory and main hepatic veins. The dilated azygos and hemiazygos
veins were the most commonly collateralized extrahepatic routes
shown in this study. The infrequent left renal-inferior
phrenic-pericardiophrenic collaterals were also seen on 3D CE MRA.
Our
study indicated that a strong point of 3D CE MRA was to display the
portal venous system simultaneously with hepatic veins and IVC.
Obstruction or increased pressure in hepatic veins resulted in
portal hypertension and portal flow stasis, which might further
cause porto-systemic varices and portal vein thrombosis.
Complications of portal hypertension were fatal in more than 50 % of
BCS patients[27]. Thus the accurate delineation of the
abnormalities of the portal vein, and the anatomic relationship
between portal vein, hepatic veins and IVC were very important,
particularly when preparing the treatment with porto-caval shunt or
TIPSS[22-24,27]. In this study, 3D CE MRA showed the
ability to provide all these relevant information.
Hypertrophy
of the caudate lobe was found on 3D CE MRA. This was related to
independent blood supply and drainage of this lobe. Heterogeneous
enhancement pattern observed by 3D CE MRA has been already known
from studies on contrast-enhanced CT[1]. It reflected the
hemodynamic disturbance in the liver with BCS. 3D CE MRA found 2
patients with primary BCS developed HCC during a long-term follow-up
period. The development of HCC in patients with chronic BCS has been
reported in the literature[29]. According to that report,
many factors, such as chronic viral infection or cirrhosis might
play a role in the development of this malignancy.
Our
study had two limitations. Firstly, a detailed comparison between 3D
CE MRA and X-ray angiography was not performed, because none of our
patients underwent hepatic venography and only some had inferior
vena cavography. But 3D CE MRA could demonstrate various findings of
BCS, which might provide clues to the correct diagnosis. Secondly,
the opacification of IVC, after injection of contrast material into
an arm vein, was inadequate in 2 patients with severe cirrhosis,
portal hypertension and edema. We speculated this was due to the
dilution of the contrast material in the porto-systemic collaterals,
enlarged spleens and increased extracellular fluid. In these
circumstances, the IVC could be enhanced properly by injecting
contrast material into a pedal vein.
In
conclusion, 3D CE MRA can display various features of BCS and
provide an accurate diagnosis.
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Edited
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