1967, Br. J.

Radiol, 40, 755-759

OCTOBER 1967

Vascular radiology in the Budd-Chiari syndrome

By Louis Kreel, M.R.C.P., F.F.R., James W. Freston, M.D.* and David Clain, M.B., M.R.C.P.f Departments of Radiology and Medicine, Royal Free Hospital, Grays Inn Road, London, W.C.1.
(Received, March, 1967)

Occlusion of the major hepatic veins is uncommon (Sherlock, 1963; Parker, 1959). It produces a wellrecognised clinical syndrome, the main features of which are marked ascites with hepatomegaly and sometimes jaundice, haematemesis and obstruction of the inferior vena cava (Budd, 1845; Chiari, 1899; Parker, 1959). This condition is commonly associated with polycythaemia rubra vera, hypernephroma and tumours of the inferior vena cava. To date no specific radiological signs have been described. In the last year the present authors have examined six cases of hepatic vein thrombosis by hepatic venography and in each a unique pattern was seen. This pattern has not been previously mentioned although this procedure has now been used since 1953 (Tori, 1953). In one case an actual shortlength obstruction to the left hepatic vein was also demonstrated. In addition, the appearances on the inferior vena cavogram and on hepatic arteriography are described, as in these examinations changes were also found, which are suggestive if not diagnostic of this condition. Two illustrative case histories are briefly presented, together with their radiological findings.

hypercellularity of particles with hyperplasia of all formed elements, especially erythrocyte precursors. Serum bilirubin was 5-2 mg per cent (2-2 mg conjugated), alkaline phosphatase 42 K.A. units per 100 ml., aspartic transaminase 37 i.u. per litre, albumin 3-7 g per cent, globulins 4-3 g per cent and prothrombin time 17 seconds (control 13 seconds). Barium swallow showed varices in the distal oesophagus. A film following the injection of contrast medium in the wedged position was obtained (Fig. 1). This showed a fine network pattern resembling a spider's web extending outwards from the catheter and surrounding it. There was no sinusoidal filling as usually occurs in the wedged position (Fig. 2), nor was there any backflow of contrast medium along the hepatic vein which the catheter had entered. No retrograde flow into portal radicals could be seen. An inferior vena cavogram demonstrated a marked regular and smooth narrowing at the upper end of the inferior vena cava. This narrowing was greater from side to side than from back to front and appeared to be due to extrinsic pressure. His condition gradually deteriorated and he lapsed into coma and died in August, 1965. At autopsy the spleen weighed 580 g and was firm. The liver was enlarged (2,065 g) and deep purple. The cut surface showed 6-8 cm areas of intense congestion. Microscopically organised thrombus was seen in medium sized veins, central veins were dilated, and there was prominent central zonal congestion and fibrosis. The findings were characteristic of Budd-Chiari syndrome. The superior segment of the inferior vena cava was narrowed, owing to compression by the enlarged liver.
Case 2

In September, 1965 this 46-year-old housewife developed ascites which became refractory to diuretic therapy and 3 1. were removed by paracentesis at another hospital. There was Case 1 In 1962 a 43-year-old male toolmaker experienced inter- no history of previous heart disease, jaundice or excessive mittent right upper quadrant abdominal pain and dizzy alcohol consumption. When first seen in December, 1965 she complained of spells. Facial plethora and a liver edge 3 cm below the right costal margin were noted at another hospital. The haema- tiredness and abdominal tension. There were signs of bi3 lateral pleural effusions. Heart sounds were normal. Gross tocrit was 65 per cent, leucocyte count 15,000 per mm and platelet count 295,000 per mm3. Alkaline phosphatase ascites was present and the liver was tender, firm and enwas 18-2 K.A. units, serum albumin 4-1 g per cent, globu- larged, extending well into the left upper abdomen. The lins 2-7 g per cent and total bilirubin 3-0 mg per cent. spleen was not palpated with certainty. Leg oedema extenPolycythaemia rubra vera was diagnosed and he was treated ded to both knees. Pelvic examination was normal. The with radioactive phosphorus (32P), 6/x.Ci intravenously and haematocrit was 73 per cent, leucocyte count 26,800 per 3 3 venesection. In 1964 he had episodes of thrombophlebitis in mm (neutrophils 23,850), platelet count 290,000 mm and both legs; ankle oedema developed followed by ascites and red cell volume 48 ml./kg. The thrombotest was 12 per cent mild jaundice. He drank little alcohol and there was no past (normal 60-110 per cent). The sternal marrow showed generalised hyperplasia. Neutrophile alkaline phosphatase score history of jaundice. When first seen in 1965 there was facial plethora, num- was 166 (normal 1575). The bilirubin was 1-2 mg per cent, erous spider angiomata, jaundice, prominent collateral veins alkaline phosphatase 18 K.A. units per 100 ml., aspartic over a distended abdomen, ascites and hepatosplenomegaly. transaminase 19 I.U. per litre, albumin 2-6 g per cent, globuThe haematocrit was 59 per cent, leucocyte count 18,000 lins 2-4 g per cent. Urinalysis and barium swallow were norper 3mm3 (11,946 neutrophils), platelet count 388,000 per mal. The wedged hepatic venogram on the right side showed a mm and red cell volume 56-6 ml./kg body weight (normal <40 ml./kg). Sternal marrow aspiration revealed marked small area of the spider's-web pattern together with larger channels which appeared to be collateral hepatic veins (Fig. 3). On the left side an. injection of contrast medium into the hepatic vein demonstrated a definite short-length narrow* Supported by a U.S. Public Health Service fellowship ing through which the catheter had passed. Beyond this (5 F 2 Am.28 215-01) from the Institute of arthritis and there was opacification of a dilated hepatic vein and its metabolic diseases. branches. In the region of the hepatic vein stenosis there t In receipt of a grant from the William Shephard bequest was a leash of surrounding channels indicating the formation of a collateral pathway (Fig. 4). to the Royal Free Hospital. 755

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40, No. 478 Louis Kreel, J. W. Freston and David Clain

METHOD

FIG. 1. Case 1. Wedged hepatic venogram demonstrating the fine spider'sweb network pattern in the liver substance in the area around the catheter. No hepatic or portal veins have been shown and no contrast medium is present in the hepatic vein along which the catheter has passed. This appearance is pathognomonic of the Budd-Chiari syndrome.

By passing an end hole catheter under fluoroscopic control along the brachial vein and thence down the superior vena cava and via the right atrium, one of the hepatic veins can be entered and pressures measured. As the wedged hepatic venous pressure approximates to the portal venous pressure (Myers and Taylor, 1951) one can assess the portal pressure without puncturing the spleen. In addition portal hypertension due to liver cirrhosis can be distinguished from that due to extra-hepatic vein occlusion such as occurs in thrombosis of the portal vein. In assessing the "wedged hepatic venous pressure" it is imperative that the catheter has been truly wedged and criteria for this have been laid down (Paton, Reynolds and Sherlock, 1953). A rapid and effective method is to inject a small amount of contrast medium (5-10 ml. of 45% Hypaque) down the catheter and take a film immediately thereafter (Reynolds, Redeker and Geller, 1960). This shows a characteristic pattern of hepatic sinusoidal filling with variable retrograde filling of portal veins (Fig. 2). Occasionally parallel hepatic veins are also shown, but if the catheter is properly wedged there will be no flow of contrast medium visible around the catheter back along the hepatic vein which was entered. The appearances of a normal wedged hepatic venogram are similar to those produced on a simple test

FIG. 2. FIG. 3. Case 2. FIG. 2. Normal wedged hepatic venogram. (A) Wedged hepatic catheter, (B) Normal sinusoidal liver pattern, (c) Retrograde filling of portal veins. FIG. 3. Wedged hepatic venogram in the right lobe of the liver. A coarse network pattern with filling of collateral veins has been demonstrated.

756

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1967

Vascular Radiology in the Budd-Chiari Syndrome

FIG. 4. Case 2, FIG. 5. FIG. 4. The hepatic catheter has passed through a stenosis (at arrow) of the main left hepatic vein which is demonstrated by the injection of contrast medium. The dilated hepatic veins proximal to the stenosis are shown and the collateral hepatic venous circulation is demonstrated around the site of the stenosis. FIG. 5. Coarse network pattern seen in the Budd-Chiari syndrome. This is due to collateral venous filling in the presence of a blocked hepatic vein.

injection film to establish the presence of true wedging of the catheter. More extensive filling of the hepatic vasculature can be obtained, however, by using larger quantities (20-30 ml. of 45% Hypaque) of contrast medium (Fig. 2). This produces little discomfort in the patient and no detectable change in liver function tests or histological changes in experimental animals. Occasionally in liver cirrhosis, because of intrahepatic shunting, nearly the whole intrahepatic portal venous system may be filled.
DISCUSSION

hepatic arteriography or splenoportography, in which examinations we have had a considerable experience. Occlusion of hepatic veins may affect the whole liver or only part of the liver, and the actual occlusion may be incomplete or complete. In the latter case the hepatic vein radicles may contain thrombus extending back into the liver substance. The specific patterns associated with wedged hepatic venography will only occur if the catheter tip enters a blocked hepatic vein. Hepatic venogram If in the presence of a blocked hepatic vein a venogram is performed it may show one of the following appearances. Firstly, spreading out from the catheter tip in an area varying from 1 0 x 1 0 cm to 2 X 3 cm there is a "spider's-web" network pattern (Fig. 1) which surrounds the catheter. The strands of contrast medium making up this spider's-web network pattern are well defined and not at all like the fine sinusoidal pattern of the normal liver or the coarse, granular pattern of post-necrotic cirrhosis. No normal hepatic veins running parallel to the catheter are shown. There may be slight filling of venous radicles in the region of the injection but this is only minimal. The second type of pattern occurs where occlusion of the hepatic veins is incomplete and one sees a coarse network of hepatic veins in the surrounding liver substance. But these hepatic veins do not run

Since the first report on the use of this method for the visualisation of the vasculature of the liver, numerous abnormal patterns have been noted (Tori, 1964). Tumours of the liver, both hepatoma and secondary deposits, as well as regenerating nodules of post-necrotic cirrhosis, have been shown by this method. It has also been used in demonstrating hydatid cysts. In post-necrotic cirrhosis of the liver a coarse nodular pattern is present and occasionally in cirrhosis of the liver the collateral venous circulation by the gastric and oesophageal plexuses has also been demonstrated when other methods, such as spleno-portography, have failed (Schlant, Galambos, Shuford, Rawls, Winter and Edwards, 1963). However, in none of the reports on the use of wedged hepatic venography has the value of this method in the Budd-Chiari syndrome been discussed, nor has any specific radiological pattern been described. Nor has a similar pattern been seen on

757

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40, No. 478 Louis Kreel, J. W. Freston and David Clain phatic flow as measured at the thoracic duct (Grossi, 1966), and dilated lymphatic spaces have been shown in the liver in experimental animals as well as markedly dilated surface lymphatics having been demonstrated at post-mortem in cases of BuddChiari syndrome. In the late stage a "sugar icing" thick white membrane is produced on the liver surface. However, interconnections between the hepatic veins and lymphatic system have not been demonstrated by this investigation. The inferior vena cavogram Two distinct patterns have been noted in these six cases. In one there were irregular intrinsic filling defects at the upper end of the inferior vena cava just proximal to the position of entry of the hepatic vein. These were interpreted as representing extension of the thrombus into the upper end of the inferior vena cava. This process may become more extensive and produce complete occlusion. This also occurred in one case. In four of the six cases there was a distinct smooth long length narrowing of the upper end of the inferior vena cava, more marked from side to side than from back to front (Figs. 6A and 6B). The appearances of this indicated a uniform compression of the inferior vena cava which was due to the swollen

in the normal position or direction (Fig. 5). These appear to be collateral hepatic veins which are seen to arch outwards from the catheter tip, and then come together again nearer the site of entry of the hepatic vein into the inferior vena cava. The obstruction of an individual hepatic vein may be incomplete forming a stricture, and this gives rise to the third type of pattern associated with the Budd-Chiari syndrome. If the catheter passes through this stricture (Fig. 4) and the hepatic veins beyond are still patent, these patent hepatic veins and the stricture will be demonstrated (Case 2). In this particular case the left lobe of the liver showed this appearance, while hepatic veins in the right lobe of the liver were completely occluded and showed the spider's-web network pattern (Fig. 3). The very fine spider's-web network pattern does not correspond to the normal or abnormal sinusoidal pattern, to the fine arborisation seen on the splenoportogram, nor to the fine arborisation seen on the hepatic arteriogram. As the larger hepatic veins are blocked, the contrast thus penetrates into the finest venous radicles giving rise to the particular pattern mentioned. Where collateral hepatic veins are still patent, these will be filled giving the second type of pattern mentioned. Hepatic vein occlusion leads to increased lym-

6. (A) Frontal view of inferior vena cavogram. There is marked side to side compression of the upper part of the inferior vena cava. This is due to the marked swelling of the liver substance which occurs in the Budd-Chiari syndrome. (B) Lateral view of the inferior vena cava showing a normal antero-posterior diameter.
FIG.

758

OCTOBER 1967

Vascular Radiology in the Budd-Chiari Syndrome liver substance produced in the earlier stages of this disease. These signs at the inferior vena cava are not considered diagnostic, but do aid in interpretation of the pathological processes occurring in this condition. Hepatic arteriogram The hepatic arteriogram was performed in two cases to exclude a possible localised hepatic lesion, such as a tumour as the cause of the Budd-Chiari syndrome. In both these cases the hepatic arteries were markedly narrowed and bowed although no definite local tumour could be distinguished, and none was found at autopsy. This narrowing and bowing of the hepatic arteries was interpreted as being due to the markedly swollen liver substance. In one case there was a large internal branch of the hepatic artery (Fig. 7) which was somewhat dilated and then supplied the left lobe of the liver. The appearances are such that they could be interpreted as multiple non-vascular rounded lesions (Fig. 8), but this was not substantiated at post-mortem. Attention is therefore drawn to this type of "pseudotumour" appearance on the hepatic arteriogram in the Budd-Chiari syndrome.
ACKNOWLEDGMENTS

The illustrations were prepared by Mr. Gibson and the Staff of the Photographic Department of the Royal Free Hospital.
ABSTRACT

In six cases of Budd-Chiari syndrome, wedged hepatic venography and inferior vena cavography were performed, and hepatic arteriography was carried out in two of these cases. Specific patterns on the wedged hepatic venogram seen only in this condition are described. Narrowing of the upper end of the inferior vena cava is demonstrated radiographically in this condition. This may be associated with intrinsic filling defects thought to be due to thrombus formation in the upper end of the inferior vena cava. On hepatic arteriography there is marked narrowing of the vessels and these appear bowed. The spider's-web network pattern as well as actual occlusion of a hepatic vein, is considered to be pathognomic of the Budd-Chiari syndrome. REFERENCES BUDD, G., 1845, Disease of the Liver (John Churchill, London). CHIARI, H., 1899, Beitr. path. Anat., 26, 1. GROSSI, C. E., 1966, Archs. Surg., 92, 333.
MYERS, J. D., and TAYLOR, W. J., 1951, J. Clin. Invest.,

30, 662.
PARKER, R. G. F., 1959, Medecine, 38, 369.
PATON, A., REYNOLDS, T. B., and SHERLOCK, S., 1953,

Lancet, 1, 918.
REYNOLDS, T. B., REDEKER, A. G., and GELLER, H. M., 1960,

Gastroenterology, 38, 799.

SCHLANT, R. C , GALAMBOS, J. T., SHUFORD, W. H., RAWLS, W. J., WINTER, T. S., and EDWARDS, F. K., 1963, Am.

It gives us pleasure to thank Professor S. Sherlock under whose care these patients were admitted, for her co-operation, advice and encouragement in the preparation of this paper.

J. Med., 35, 343. SHERLOCK, S., 1963, Diseases of the Liver and Biliary System. 3rd edn. (Blackwell Scientific Publications, Oxford.) TORI, G., 1953, Ada radiol., 39, 89; 1955, Scientia med., 4, 306; 1964, in Vascular Roentgenology, Eds. R. A. Schobinger, and F. F. Ruzicka (Collier-Macmillan).

FIG. 7. FIG. 8. FIG. 7. Frontal view of coeliac axis arteriogram. The hepatic arteries are stretched and bowed particularly the main right hepatic artery. In the liver substance near the hilar region it is tortuous and a little dilated. It then supplies the left lobe of the liver where the stretching and bowing can again be seen. The spleen is moderately enlarged but the arterial pattern to the spleen is essentially normal.

FIG. 8. Oblique view of the coeliac axis arteriogram. The stretching and bowing of the intra-hepatic arteries are more obvious on this view. This produces a "pseudo-tumour" effect. 759