PORTAL- VEIN THROMBOSIS: IMAGING FEATURES AND ASSOCIATED ETIOLOGIES

ABSTRACT.-Thrombosis of the portal vein and its splanchnic tributaries is often unsuspected clinically and may be recognized only after imaging studies of the abdomen are performed for other reasons. Radiologists should be aware of the clinical situations that predispose a patient to portal or mesenteric veiu thrombosis and should also be able to recognize the sequelae of chronic thrombosis. Different modalities can be used to image the patient with portal vein thrombosis; each has its strengths and drawbacks. This paper discusses the conditions that predispose to portal and mesenteric vein thrombosis, difkkrentiating intrahepatic portal vein occlusion secondary to liver disease from extrahepatic portal vein occlusion associated with a normal liver. The imaging features of portal vein thrombosis, its associated causes and sequelae will be reviewed as demonstrated on computed tomography (CT), ultrasound, magnetic resonance imaging (MRI), angiography, and plain fihn.

CIJW Probl

Diagn

Radial,

July/August

1992

117

Patricia L. Abbitt, M.D., is an Associate Professor of Radiology at the University of Florida Health Sciences Center, Gainesville, Florida, where she is a member of the Division of Abdominal Imaging. Her areas of interest include ultrasonography, ultrasound-guided interventional procedures in the abdomen, and mammography. Dr. Abbitt received her medical degree from Tufts University School of Medicine, Boston, Massachusetts. She completed a diagnostic radiology residency and fellowship in medical imaging and mammography at the University of Virginia in Charlottesville. She served as an attending physician and Director of Vltrasound in the Radiology Department at the University of Virginia for three years prior to her move to Florida. 118

Cum Probl

Diagn

Radio&

July/August

19Si

PORTAL WEIN THROMBOSIS: IMAGING FEATURES AND ASSOCIATED ETIOLOGIES

INTRODUCTION Thrombosis of the portal vein or its major splanchnic tributaries may present as a catastrophic abdominal event requiring evaluation and intervention. Much more often, however, thrombosis of the major veins of the abdomen occurs so silently as to be unrecognized clinically and is only suspected when abdominal imaging is performed for other clinical reasons. Often the sequelae of portal vein thrombosis are recognized rather than the acute thrombus itself. The predisposing causes of portal and splanchnit vein thrombosis are numerous and often clinically overshadow the development of venous thrombosis. Occlusion of the portal vein may originate in the intrahepatic portions of the portal vein as in the case of hepatocellular disease with cirrhosis. In such a situation, thrombosis of the vein is precipitated by the extreme distortion of anatomy caused by the fibrosis and altered sinusoidal anatomy associated with cirrhosis. Stagnation of blood flow in the portal vein predisposes to thrombosis. The causes of cirrhosis are numerous and include alcoholic liver disease, biliary cirrhosis, and postnecrotic cirrhosis, but all may result in portal vein occlusion. The patient with cirrhosis has another risk factor for developing portal vein occlusion, for such a patient may develop hepatocellular carcinoma within the diseased liver. Hepatocellular carciCurr

t’robl

Diagn

Radio&

July/August

1992

noma is a tumor with a propensity to invade venous structures and propagate within them. Patients with normal livers and no evidence of hepatocellular disease may develop portal and splanchnic vein occlusion. Generally, these patients develop extrahepatic portal vein occlusion related to operative injury of the vein, hypercoagulable states resulting in hypetiscosity, or venous compression secondary to neoplastic or inflammatory masses. Infections in the abdomen which drain into the liver via the portal vein may give rise to septic thrombosis of the portal vein. Acute thrombosis of the portal vein may be detected by computed tomography, ultrasound, magnetic resonance imaging, or angiography by visualization of the clot itself or because of lack of flow within the vein. In situations of chronic portal vein occlusion, the presence of collateral pathways bypassing the occlusion may be the predominant feature, and the portal vein may not be identiilable. In patients with liver disease as their’predisposing cause for thrombosis, the features of liver disease will predominate both clinically and on imaging studies. In patients in whom extrahepatic portal vein occlusion has occurred, the cause of the occlusion may no longer be obvious (e.g., pancreatitis, abdominal infection, or previous surgery), but the sequelae of the occlusion (e.g., collateral pathways) will often be quite obvious. This monograph reviews the anatomy of the portal vein, imaging features of portal vein occlu119

sion as seen by many different modalities, and predisposing conditions, which cause portal vein thrombosis. I hope that this review will aid the radiologist in recognizing this condition which is often undetected clinically.

PORTAL

VEIN EMBRYOLOGY

AND ANATOMY

The portal vein selves as the major nutrient vessel to the liver, supplying approximately 75% of the hepatic blood supply. Its territory of drainage is the gastrointestinal (GII tract, including both the large and small intestines. Embryologically the portal vein derives from the omphalomesenteric veins which transport blood from the yolk sac and the intestines to the liver. During normal development, the omphalic portion of the vein regresses with the disappearance of the yolk sac. As intestinal growth continues, the mesenteric portions persist and become tributaries of the portal vein. In 85% to 93% of patients, the portal vein is formed by the union of the superior mesenteric vein and the splenic vein just posterior to the head of the pancreas at the level of the second lumbar vertebral body. In approximately 10% of patients, the portal vein is formed by the confluence of the superior mesenteric, inferior mesenteric, and splenic veins. The other major tributaries of the portal vein are the short gastric, inferior mesenteric, gastroepiploic, and pancreaticoduodenal veins. The -portal vein averages 7 cm in length and 6.3 + 2.3 mm in diameter. It can reach a diameter of 13 mm in normal individuals performing the Valsalva maneuver.’ At the porta hepatis, the portal vein divides into right and left branches in 74% to 80% of subjects; in 10% it divides into three branches, two going to the right and one to the left lobe of the liver. The right lobar branch receives the cystic vein draining the gallbladder, and the smaller left lobar branch receives the umbilical vein and the associated periumbilical veins. Other modes of division are quite rare with major branching usually occurring just outside the liver. After the portal vein enters the liver, it divides into progressively smaller radicles that run with the hepatic artery branches and biliary ducts, terminating in the sinusoids. The sinusoids, the termination of the portal system, represent the point of origin of the hepatic venules, which eventuallydrain into the inferior vena cava via the hepatic veins. The splenic vein, one of the major tributaries of the portal vein, runs adjacent to the hilum of the lefi

kidney,

an anatomic

the development 1.30

r=lationship

of the spontaneous

that

explains

splenorenal

FIG 1. A large tortuous splenorenal collateral (arrows) is well seen on contrast-enhanced CT in this patient with portal hypertension related to alcoholic liver disease.

shunt in some patients with portal hypertension (Figs 1 and 2). The splenic vein receives branches from the pancreas, stomach, and left colon. The superior mesenteric vein, a sizable tributary of the portal system, is second in diameter to the portal vein. It receives blood from veins of the small intestine, the cecum, and the ascending and transverse colon. Twenty-five percent of the liver’s blood supply enters via the higher pressure arterial system, the

FIG 2. This &year-old girl had liver resection of a hepatoblastoma as an infant and required repeated hospitalization for GI hemorrhage. UItrasound showed no obvious portal vein. In the region of the splenic hilum a large collateral was visualized. The venous phase of the mesenteric arteriogram demonstrates the patients spontaneous splenorenal pathway and no normal portal vein, findings suggestive of chronic portal vein occlusion. Cur-r

Probl

Diagn

Radio&

July/August

1992

remainder through the lower pressure venous system. Increased vascular resistance within the liver, which accompanies cirrhosis, may lead to enlargement of the portal vein and its branches, stagnation of flow, and development of alternate methods of drainage with retrograde flow into normally closed portosystemic collaterals. Usually such collateral pathways are functionless unless there is an increase in portal venous pressure. Several anastomoses may be seen: (1) The gastrocoronary vein is the pathway connecting the short gastric vein to the inferior vena cava. At the gastroesophageal junction this anastomosis can result in esophageal and gastric &rices (Figs 3, 4, and 5). (2) Recanalization of veins adjacent to the fetal umbilical vein or newly developed periumbilical channels to abdominal wall vessels may give rise to the caput medusae (Fig 6). (3) Branches of the inferior mesenteric vein to rectal veins can lead to the formation of large internal hemor-

FIG 4. Thickening of the folds ber of causes including,

of the proximal stomach as in this case, gastric

may have varices.

a num-

rhoids (Fig 7). (4) Retroperitoneal veins may communicate with other retroperitoneal veins. Collaterals around the gallbladder may sometimes be seen (Fig 8).

THE NATURAL HISTORY VEIN THROMBOSIS

OF PORTAL

Venous thrombosis, as stated by Virchow’s law, is promoted by changes in the vessel, particularly endothelial damage, changes in blood composition, and disturbance of blood flow, especially stasis. Thrombosis of the portal vein may involve either the intrahepatic or extrahepatic portions of the

FIG 3.

FIG 5.

Barium swallow demonstrates woman with portal vein thrombosis ble state (protein S deficiency). Cut-r

Probl

Diagn

Radio!,

July/August

esophageal secondary

1992

varices in young to a hypercoagula-

Extensive collaterals are present around the stomach (arrow) and no identifiable portal vein is seen in this patient with primary biliary cirrhosis being evaluated for possible liver transplantation. 121

A, marked enlargement of the left portal vein was the first observation which led to recognition of recanalization of a paraumbilical collateral. B, C, CT correlates well with the sonogram and reveals the large recanalized collateral, a sign of portal hypertension. In this case, the patients liver disease was secondary to alcohol use

vein and may be due to a number of possible associated etiologies (Table 1). The majority of portal vein thrombi involves obstruction and thrombosis within the sinusoids and intrahepatic portions of the vein in a diseased, cirrhotic liver. In patients with cirrhosis secondary to any cause, features of severe liver disease and portal hypertension will usually be the predominant findings and will predate the development of portal vein thrombosis. In these patients, a small nodular liver with segmental enlargement of the caudate or left lobe, splenomegaly, ascites, “corkscrew” hepatic artery, and collateral formation may be present before portal vein thrombosis occurs (Fig 91. In cirrhosis the fibrotic reaction within the liver and distortion of the hepatic architecture (Figs 10 and 111 may be secondary to a number of toxins, including alcohol; chronic diseases such as hepatitis; or inborn errors of metabolism such as Wilson’s disease or alpha,-antitrypsin disease. Fibrosis and distorted architecture within the liver result in significant resistance to blood flow

FIG 7. Extensive perirectal collaterals are identified in a young man with cavernous transformation of the portal vein, Portal vein thrombosis. was believed secondary to multiple operations as a newborn. 122

from the GI tract into the liver. Collateral pathways, often flowing in a hepatofugal direction, develop over time to establish portosystemic decompression. Blood flow to the liver is maintained although velocity may be signihcantly diminished. Liver disease usually results in portal hypertension with subsequent enlargement of the portal vein. When thrombosis occurs primarily in the extrahepatic portion of the portal vein, it may originate within the main portal vein itself or in one of the mesenteric tributaries that drain into the liver via the portal vein (Fig 12). In such a situation, hepatopedal collaterals often develop because the liver is normal and hepatic blood flow remains intact. Extrahepatic portal vein thrombosis may be secondary to injury or encasement of the vein, congenital abnormalities of the vein, hypercoagulable states, or irritation of the vein due to infections in the abdomen which lead to endophlebitis and thrombosis. Injury to the portal vein may occur secondary to

FAG 8. Collaterals (arrows) around the gallbladder are seen in this patient with previous pancreatitis and portal vein thrombosis. Cum

Probl

Diagn

Kadiol,

July/August

1992

TABLE 1. Etiologies

of Portal

Vein Thrombosis

I. Intrahepatic Thrombosis of Portal Vein A. Hepatocellular Disease 1. Cirrhosis a. Alcoholic cirrhosis b. Postnecmtic cirrhosis c. Bihary cirrhosis d. Pigment cirrhosis associated with hemochmmatosis e. Cirrhosis associated with Wilson’s disease f. Cirrhosis associated with alpha,-antitrypsin disease g. Cardiac cirrhosis h. Cryptogenic cirrhosis 2. Hepatitis (Fulminant) a. Viral b. Drug-induced 3. Budd-Chiari Syndrome B. Neoplasia (Tumor Thrombus) 1. Hepatocellular Carcinoma 2. Metastatic Disease II. Extrahepatic Obstruction of Portal Vein A. Hypercoagulable States 1. Polycythemia vera 2. Myelofibrosis 3. Postsplenectomy 4. Antithrombin III deficiency 5. Protein C deficiency 6. Protein S deficiency B. Injury/Encasement of Portal Vein 1. Injury a. Postsplenectomy b. Liver resection c. Liver transplantation d. Surgery near the portal vein e. Blunt trauma 2. Encasement a. Portal adenopathy b. Pancreatic carcinoma c. Pancreatitis with phlegmonpseudocyst formation C. Inflammatory/Infectious Conditions Draining via the Portal Vein (Endophlebitis) 1. Pancreatitis 2. Appendicitis 3. Cmhn’s disease 4. Ischemic colitis 5. Diverticulitis 6. Cholangitis 7. Cholecystitis 8. Ulcerated gastrointestinal carcinoma 9. OmphalitisAtmbilical catheters D. Congenital Abnormalities of the Portal Vein 1. Portal vein stenosis 2. Portal vein atresia 3. Portal vein agenesis E. Idiopathic

abdominal trauma or iatrogenic injury due to surgery on the liver, pancreas, or other nearby organs. Encasement and compression of the vein occur when masses such as pancreatic carcinoma, pancreatitis with pseudocyst formation, or portal adeCur-r Pmbl

Diagn

Radioi,

July/August

1992

FIG 9. Cirrhotic changes in the liver include an irregular contour, segmental hypertrophy of the left lobe and a corkscrew appearance of the hepatic artery in this patient with alcoholic liver disease and hepatocellular carcinoma.

nopathy develop around the porta hepatis. Congenital abnormalities of the portal vein include portal vein stenosis, portal vein atresia, or agenesis. Such congenital abnormalities are rarely recognized. The etiology of portal vein thrombosis remains unknown in as many as one-half of patients in some studies. The physiology of portal vein thrombosis associated with cirrhosis and hepatocellular disease is very different from obstruction of the extrahepatic portions of the portal vein in a normal liver. In patients with normal liver function, maintenance of liver perfusion is accomplished by establishment of hepatopedal collaterals. This development of large hepatopedal collaterals, so-called cavernous

FIG 10. Gross section and abnormal

of cirrhotic architecture.

liver demonstrates irregular liver contour (Courtesy of David Dolson, M.D.) 123

FIG 11.

FIG 13.

Dense bands of fibrous tissue distort the normal sinusoidal anatomy in this patient with micronodular cirrhosis. (Courtesy of David Dolson, M.D.)

Cavernous transformation of the portal vein is seen as an extensive cluster of periportal collaterals.

transformation of the portal vein, is a distinctive feature in patients with extrahepatic portal venous thrombosis (Figs 13 and 14). The hepatopedal collaterals may terminate in mid-sized intrahepatic portal veins. This situation is more favorable for the patient than portal vein thrombosis secondary to intrahepatic sinusoidal occlusion.’ Clinical management of extrahepatic portal vein thrombosis and a normal liver differs from the management of thrombosis related to cirrhosis. The survival of patients with a normal liver is not limited by the progression of underlying liver disease. In most cases, emphasis is on control of variceal bleeding which may begin at any time from infancy to adulthood and may recur. Concern about progressive liver dysfunction is not usually necessary in such patients.

The development of portal vein thrombosis may be associated clinically with acute worsening of liver function, abdominal pain, new onset ascites, or GI hemorrhage. Often, the onset of portal vein thrombosis is so gradual or indolent that no specific clinical manifestations are initially recognized. In such situations, imaging studies may provide the first clue that portal or mesenteric vein thrombosis has occurred. In patients with severe liver disease and stasis within the portal vein secondary to anatomical distortion in the liver, the development of portal vein thrombosis often elicits little clinical change. An overt decompensation of the patient may not be clinically obvious because the flow within the liver may have been very limited prior to thrombosis of the portal vein. The patient with a normal liver who develops portal vein thrombosis acutely does not have established collateral pathways to divert the blood around the obstructed portal vein. Depending

FIG 12.

FIG 14.

CT shows a focal thrombus (arrow) within the portal vein in this patient with pancreatitis. The liver was unremarkable.

A normal portal vein is not seen; only a cluster of small tortuous vessels is seen in the porta hepatis.

124

Curr

Probl

Diagn

Radio&

July/August

1992

upon the severity and extent of the portal vein thrombus and the rapidity with which collaterals develop, these patients may be acutely ill with deterioration of liver function, hepatosplenomegaly, abdominal pain, ascites formation, splenic or bowel infarction, or GI hemonhage. This acute decompensation is obvious because the collateral pathways that could divert blood around the obstructed portal vein are not well established. It does not take long for the collateral channels to develop. Exactly how long is not known, but individual case reports have illustrated extensive collateral formation within a U-day period? Gastrointestinal hemorrhage and hepatosplenomegaly were the most common clinical presentations reported by Webb and Sherlock3 in a series of patients with extrahepatic portal vein occlusion. These patients were believed to be presenting late in the course of the process. This same observation was made by Rosch and Dotter4 who described cavernous transformation that developed in childhood, but did not become obvious until the teenage years, when splenomegaly or GI hemorrhage occurred. Patients with more acute portal vein occlusion have abdominal pain and new onset ascites Early transient ascites that resolves is a well-known complication of portal vein obstruction. Development of ascites is probably secondary to an acute increase in portal pressure, which diminishes as collaterals develop. Chronic portal vein thrombosis does not often have associated ascites unless other complicating features are present. Patients with portal vein thrombosis may, over time or with treatment, develop signs of recanalization of the portal vein with restoration of flow through the vein. Such patients may have thickening or calcification of the venous wall, but restoration of flow, within a small vein (Fig 15). Sometimes

FIG 15. A, marked function transverse Curr

Probl

and

thickening of the portal vein wall with recanalization recurrent GI hemorrhage. Portal vein thrombosis image in the same patient. Diagn

Radio&

July/August

1992

the portal vein thrombosis is so severe as to cause obliteration of the vein. In such a case, the predominant findings consist of collateral formation and no main portal vein may be identified (Fig 161.

IMAGING THE PATIENT VEIN THROMBOSIS

WITH

PORTAL

If a patient is imaged in the acute stages of portal vein thrombosis, the thrombus may be identified within the portal vein. Often the portal vein is engorged and filled with thrombus (Figs 17 and M), much like deep venous thrombosis of the leg, in which the veins become large, filled with clot, Obviously, noncompressand noncompressible. ibility of the portal vein cannot be assessed during an imaging study. Visualization of the actual clot by ultrasound may not be possible in all cases because acute thrombus is often almost cystic in appearance, with low-level echoes (Fig 19). To verify the presence of portal vein thrombosis by ultrasound, the absence of Doppler flow in the portal vein must be established, or flow around a partially occluding thrombus must be demonstrated. The features of the disease process that predisposed to portal vein thrombosis may predominate on the imaging studies. Typical features of severe hepatocellular disease may be apparent in the patient with cirrhosis (Fig 20). In patients with normal livers and extrahepatic portal vein occlusion, nodal masses, intra-abdominal abscesses, or pancreatitis, all of which are predisposing conditions, may be recognized (Fig 21). Most often portal vein thrombosis is recognized late, weeks to months, or years after it develops. Imaging studies, such as computed tomography (CT), ultrasound, or magnetic resonance imaging (MRI), may show a very small or unidentifiable

of the central lumen is present in this young was believed to be secondary to surgery and

woman recurrent

with normal pancreatitis.

liver

B,

125

FIG 18. Lack acute

FIG 16. Acute portal vein thrombosrs (A), schematically depicted here, engorges the vein. Over time and depending upon the severity and extent of thrombosis, the vein may be obliterated, being replaced by collaterals (B), or recanalized with thickening of the wall or calcification as indicators of previous thrombosis (C).

portal vein with extensive collateral formation. One may also see changes in the vein itself, such as calcification or wall thickening. These accompany recanalization of old thrombus. These patients may be undergoing imaging studies for recurrent GI

of enhancement of the portal vein thrombosis.

portal

vein

in this

patient

is seen

in

hemorrhage, abdominal pain, or follow-up of previously recognized abnormalities (e.g., pancreatitis). In such patients, it is important that the radiologist recognize the fact that portal or mesenteric vein thrombosis has occurred, report the sequelae of that observation, such as splenomegaly or collateral formation, and speculate about any possible associated causes. Patients may develop portal vein thrombosis as a result of tumor invasion of the portal vein, most notably hepatocellular carcinoma. Usually, a mass lesion within the liver can be imaged in this setting (Fig 22). Changes of cirrhosis are often associated with the mass, as cirrhotics run an increased risk of heDatocellular carcinoma. These natients may decompensate clinically when tumor invasion of the portal vein occurs. Clinical decompensation is dependent upon hepatic function and relative blood flow via the portal vein prior to tumor invasion. 1

COMPUTED

FIG 17. Portal vein thrombosis ages The portal vein also present. 126

(arrows) is readily is completely filled

seen on gray-scale with material. Ascites

imis

TOMOGRAPHY

Dynamic postcontrast computed tomography allows portal vein thrombosis to be identified with ease and confidence in most cases. In portal vein thrombosis identified by CT, the lumen of the thrombosed vein does not enhance as do other nearby vascular structures (Figs 23 and 24). In some cases, CT demonstrates periportal enhancement, believed to be secondary to proliferation of the vasa vasorum of the portal vein. Some authors have suggested that this feature does not occur Curr

Probl

Diap

Radio&

July/August

1992

FIG 19. A, this middle-aged performance Thrombosis

man with a myeloproliferativC? of an ultrasound. No thrombus was was confirmed by MRI

disorder identified

required a splenectomy. The onset of ascites in the mortal vein. B, no flow was identifiable

after in the

splenectomy portal vein

led to the by Doppler.

immediately after thrombosis, but rather represents a feature of longstanding thrombus. Hammerman et al5 report that periportal contrast enhancement can be seen without portal vein occlusion, is a nonspecific finding, and should not be confused with portal vein thrombosis. Sometimes CT shows transient inhomogeneous enhancement of the nearby hepatic tissue when portal vein thrombosis is present. Computed tomography also allows more complete visualization of collaterals than does sonography. Thrombosis of the splenic and mesenteric veins can be more easily identified by CT than by sonography (Figs 25 and 26). Sometimes, when portal or mesenteric thrombosis is acute and severe, mesenteric stranding and bowel wall thickening related to venous engorgement can be appreciated (Fig 27). Splenic infarction may be noted.

In patients with hepatocellular carcinoma and portal vein thrombosis secondary to tumor invasion, an ill-defined low-density mass that often appears infiltrative is identified, sometimes within an obviously cirrhotic liver (Fig 28). The portal vein is often engorged as a result of tumor invasion. Although unenhanced CT scans are not generally helpful in delineating portal vein thrombosis, they can demonstrate high-density thrombus which might be secondary to recent 0nset.l’ 6 The high attenuation of a thrombus is caused by the high protein content in concentrated red blood cells6 Most new thrombi are rich in red blood cells trapped in fibrin. Artifacts from surgical clips’ can make it difficult to visualize the porta hepatis and may make recognition of portal vein thrombosis difficult. Possible mistakes in evaluating the porta hepatis by CT include mistaking a thrombosed portal vein for a di-

FIG 20.

FIG 21.

This 48-year-old woman with primary biliary cirrhosis had massive ascites, a very small irregular liver and a small, chronically occluded portal vein (arrow). The patient did not survive liver transplantation.

This patient had a history of islet cell tumor of the pancreas with a large calcified pancreatic mass (arrowhead). Collateral formation and thrombosis of the portal vein secondary to encasement and compression by the mass (arrow) are identified.

Curr

Probl

Diagn

Radial,

July/August

1992

127

FIG 24. This young woman required prolonged hospitalization after cholecystectomy and severe pancreatitis., Fatty infiltration of the liver and portal vein thrombosis (arrows) are easily seen on CT.

FIG 22. Extensive low-density tumor mass is seen within the liver with associated thrombosis of the main portal vein (arrow) in this patient with heoatocellular carcinoma.

lated bile duct; mistaking an engorged thrombosed superior or inferior mesenteric vein for a pancreatic pseudocyst (Fig 29); or interpreting multiple intrahepatic stones as a calciilc portal vein thrombus.8 In many cases, the CT features of portal vein thrombosis are straightforward, but because there are so many possible manifestations of portal vein thrombosis, misinterpretation can result. Chronic portal vein occlusion may cause obliteration of the vein or thickening of its wall with a

small lumen (Fig 30). Portal collaterals and an increase in the size of the hepatic artery may be seen due to increased liver blood flow through the hepatic artery. ULTRASOUND The thrombosed portal vein often contains intraluminal echoes that obliterate the normally echo-free lumen of the vessel (Fig 31). The echogenicity of the thrombus is often similar to that of the liver. Thrombus which is very new (hours to a few days) may be essentially anechoic. The thrombus may not be visualized, but a flow void will be detected on duplex or color flow scanning (Fig 32).’ As fibrosis develops, the thrombus becomes more echogenic.

FIG 23. Four weeks prior to this examination this patient was treated for appendicitis complicated by abscess formation in the right lower quadrant. The development of epigastric pain led to the CT which showed thrombus within the main portal vein. The liver appears normal.

12.6

FIG 25. Partially occluding thrombus (arrow) within the superior mesenteric vein is easily seen by CT.

Curr

Probl

Oiagn

Radio&

July/August

1992

FIG 28. Extension of thrombosis into the superior and inferior mesenteric veins (arrows) is demonstrated in this patient.

Often, the lumen of the portal vein is enlarged as it is filled with clot. The normal resting diameter of approximately 6 mm may become as large as 13 mm with expiration or the Valsalva maneuver. In patients with portal hypertension, diameters greater than 13 mm are characteristic. In acute or subacute portal vein thrombosis the vein is distended, whereas the vein may be normal size or smaller if the occlusion is chronic. Thrombosed veins do not change in size with respiration. In some cases, enlargement and tortuosity of the hepatic artery and the presence of collaterals may be identified. In cases of hepatocellular carcinoma with tumor invasion of the portal vein, abnormal

FIG 27. Extensive mesenteric stranding with bowel wall thickening is visualized in this patient with severe splanchnic thrombosis. The patient did not survive this illness.

Curr

Probl

Diagn

Radio/,

JulylAugust

1992

FIG 28. Large low-density mass in the liver and failure of the portal vein to enhance are consistent with hepatocellular carcinoma and portal vein invasion.

echotexture of the liver may be seen (Fig 331. Sometimes a well-defined mass can often be identified. The sonographic appearance of the thrombus alone does not allow differentiation of bland thrombus from tumor thrombus (Fig 341. Sonography is ‘particularly limited in obese patients, patients with extensive bowel gas, and patients in whom the thrombus is echo poor unless

FIG 28. This patient, an 18-year-old man, underwent multiple abdominal operations as an infant and, as a young adult, had recurrent bouts of GI bleeding. He was referred for workup of a suspected pancreatic mass. CT shows the pancreatic mass to be an engorged, thrombus-filled confluence of the superior mesenteric and splenic veins.

129

FIG 32. FIG 30. A markedly attenuated portal vein with wall irregularities (arrow) is seen in this patient with recanalization of the portal vein after thrombosis.

Doppler evaluation is undertaken. Thrombosis of the vessels can be confirmed by a lack of Doppler signal from the central lumen of the vessel. Usually portal vein flow in healthy subjects shows a low, continuous hepatopedal pattern with mild respiratory variations. In patients with cavernous transformation and extensive collaterals around the portal vein, the operator must be careful not to mistake one of the large hepatopedal collaterals for the thrombosed or obliterated portal vein (Fig 35 and Color Fig 1). The addition of color Doppler facilitates detec-

One day after liver transplantation, this young girl experienced severe allograft dysfunction. Although no thrombus could be seen sonograohically, no flow was obtainable by Doppler. This finding was confirmed angiographically.

tion of vessels that could be missed by gray scale or conventional Doppler (Color Figs 2 and 3).’ Color Doppler provides information regarding flow direction and patterns of turbulence at real-time sonography. With color Doppler, portal vein thrombosis is diagnosed when no intravascular flow is detected, despite an adequate scan angle and adequate ac-

FIG 31.

FIG 33.

Evaluation of this candidate for possible liver transplantation demonstrated portal vein thrombosis. Complete thrombosis of the main portal vein is seen here, together with ascites and irregularity of the liver consistent with cirrhosis.

Large echogenic mass in the right lobe of the liver and obliteration of portal and hepatic vein structures allowed the diagnosis of hepatocellular carcinoma to be made in this young man with chronic active heoatitis.

130

Curr

Probl

Diagn

Radioi,

July/August

1992

FIG 34. A, so-called hepatization of the portal vein is &en at ultrasound. Bland thrombus as in this case cannot be differentiated thrombus by its appearance alone. Recognition of a mass in the liver and portal vein thrombosis may suggest portal vein tumor. 8, marked engorgement of the vein was seen in this patient with hepatocellular carcinoma with portal vein invasion.

cess. Usually flow is identifiable in other smaller vessels at the same depth and angle. Flow around a partially occluding thrombus can be seen as well. Color Doppler is superior to gray scale and spectral Doppler imaging in evaluating patients with partially occluded vessels.’ The thrombus can be identified by showing flow around it. The presence of intraluminal echoes is not considered diagnostic, but rather provides supporting evidence of thrombus. Abnormal flow direction can be detected when flow is hepatofugal or bidirectional. For evaluating flow direction, low pulse repetition frequency is optimal, but can result in abasing and mimic flow reversal. Doppler sonography can assess direction of flow and flow rates, but cannot evaluate pressures. Color Doppler offers significant advantages over other, more invasive modalities such as angiography and even over conventional spectral Doppler.’

It depicts blood flow direction easily and may detect collaterals more readily than conventional gray scale images. Color Doppler can facilitate recognition of recanalization of a paraumbilical vein, an observation which connotes portal hypertension. This pathway is normally obliterated shortly after birth. In cases of portal hypertension, it provides communication between the left portal vein and the superficial epigastric veins. Recognition of this “protective” pathway may be helpful in avoiding injury to patients scheduled for lapamtomy or laparoscopy. Patency of the main portal vein is virtually assured when there is recanalization of a paraumbilical vein, and blood flow direction is IYequently hepatofugal (Fig 36). Very low flow states which can be present after liver transplantation may mimic portal vein thrombosis and may necessitate a contrast study to insure patency. Very low flow can mimic anechoic clot. MAGNETIC

FIG 35. Cavernous

transformation

Cum

Diagn

Probl

Radiol,

of the portal

July/August

vein seen

1992

on CT

from tumor invasion by

RESONANCE IMAGING

Magnetic resonance imaging is another modality that can be used to evaluate the patency of the portal vein and its major tributaries. Generally, rapidly flowing blood creates a signal void within the vessel on Tl- and T2-weighted spin-echo images. This finding is seen because stimulated protons have left the sample volume prior to emitting an echo. Slow flow within the portal vein can produce a bright intraluminal signal, most pronounced when partial saturation sequences and short TR times are used.” Moreover, increased signal is seen when slowly moving blood is imaged, especially in the second echo image. This feature is secondary to a spin-rephasing effect.

131

COLOR FIG 1. Large hepatopedal collaterals seen with color Doppler may be misinterpreted as the portal vein, which has been obliterated.

It is often difficult to differentiate slow flow in patients with portal hypertension from actual portal vein occlusion if spin-echo images alone are used. Signal secondary to slow flow should increase in intensity from the first to the second spin-echo sequence.ll Although this increase may be dithcult to appreciate by visual inspection alone, calculated T2 values can be used to differentiate slow Bow tiom thrombosis. Use of a third echo image may also helpl’ to differentiate slow Bow from thrombosis. Acute portal vein thrombosis (less than 5 weeks old) is hyperintense relative to nearby liver on TIweighted images and becomes even brighter on T2-weighted images (Fig 37). In a study of 14 patients with portal vein thrombosis, Zirinsky et al?3 showed that older thrombus (more than 2 months old) is still hyperintense to liver, but only on T2weighted images (Fig 38). The loss of hyperintensity on n-weighted images may be secondary to fibrinization, lysis, and organization which occur in a chronic thrombus. A recent study by Silverman et al.1’ suggested that gradient-echo sequences may be an adjunct to spin-echo techniques for evaluating the portal venous system with MRI. Gradient-echo scans permit excellent visualization of the portal system because, in normal patients, there is intense intraluminal signal which allows ready identification of the main vein and its 132

COLOR flG 2. Color flow evaluation of the portal vein facilitates detection of normal flow.

COLOR FIG 3. Extensive pelvic collaterals are easily seen in this young woman with portal vein occlusion. Curr

Probl

Diagn

Radial,

July/August

1992

-

-FIG 36. A, B, recanalization of a paraumbilical vein allows recognition of severe srtuation the left portal vein is often large with he:atofugal flow,

tributaries and provides contrast with surrounding tissue. Acquisition times from gradient-echo sequences are decreased, reducing motion artifacts. Because normal flow in the portal vein is identified by a very bright signal on gradient-echo sequences, a partial thrombus or a completely occluded vein is relatively easy to identity using this technique. While thrombus identified on spinecho techniques appears as a region of high signal intensity, it is seen as an area of decreased signal intensity on gradient-echo images. The high intensity signal in vessels on gradientecho sequences is subject to artifacts that can be recognized by the experienced. Frequently there are linear or curvilinear artifacts that can be interpreted as thrombus. Correlation with other sequences may be necessary to exclude thrombus. Gradient-echo imaging is less degraded by motion artifact but provides poorer contrast between tumor masses and other normal tissues. For this reason, routine spin-echo sequences should still be obtained. Tumor can present an extremely variable appearance on gradient-echo images, making it

portal

hypertension

requiring

collateral

pathway

formation.

In this

difficult to recognize. Tumor thrombus can also be quite variable on such sequences.11 Sometimes the main portal vein or one of its tributaries cannot be identified, and numerous collaterals can be seen. Recognition of collateral pathways is easy on gradient-echo sequences. The high intensity signal obtained by gradientecho sequences is well suited for angiographic evaluation of blood vessels (Fig 39). Encasement, obstruction, and collateralization can be imaged in this manner. The angiographic displays are, however, prone to artifacts which may be resolved by referring to standard axial gradient-echo images. Magnetic resonance angiograms can be created by processing a series of flow-compensated gradient-echo images.14 Flow velocity can be determined with a bolus-tracking method. Magnetic resonance angiography can be used to provide functional information regarding the portal venous system, as well as a three-dimensional display of the anatomy.14 To identify whether thrombus in the portal vein was tumoral or bland in character, Hricak et al.‘l

FIG 37. A, B, T2-weighted images (2000/90) at 1 .O Tesla vena cava and aorta, and high signal consistent the thrombosed vein (arrows).

Cur-r

Probl

Dia.&y

Radio/,

July/August

1992

in this young with extensive

man with polycythemia vera show splenomegaly, signal void in the inferior thrombosis of the portal vein, The hepatic artery can be seen anterior to

133

FIG 38. A, Tl-weighted

images (450/30) and (B) T2-weighted images (2500/90) at 1 .O Tesla demonstrate old thrombus in a patient several months after splenectomy for a myeloproliferative disorder. Tl-weighted images, somewhat hampered by motion artifact, reveal the portal vein to be lower in signal intensity than nearby liver. T2-weighted images show the portal vein to be markedly hyperintense to nearby liver. With normal portal vein flow, signal void should have been recognized.

noted that the signal intensity of at least a portion of the thrombus was similar to a tumor mass in the liver on both the first and second spin-echo images (Figs 40 and 41). Magnetic resonance imaging is probably comparable to contrast-enhanced CT for evaluation of portal vein thrombus and may be better if surgical clips, which may provoke CT artifact, are present. Collateral vessels may be more easily seen on MEU than on CT.” Magnetic resonance imaging is considered reliable in identifying the major abdominal

veins. Therefore, nonvisualization of the portal vein and the presence of collaterals should lead one to suspect an absent or thrombosed vein. Levy and Newhouse*’ described 100% specificity using spin-echo techniques in nine patients with portal vein thrombosis. Persistent signal at the same location in the vessel on multiple sequences and no evidence of entry-slice phenomena, evenecho rephasing, or nonvisualization of the portal vein with collateral formation were believed to be diagnostic of portal vein thrombosis.

ANGIOGRA?‘HY

FIG 39. Two-dimensional MR angiogram based on coronal gradient-echo images shows extensive collateralization, narrowing of the inferior vena cava and no hepatic vein flow in this young woman with an &year-history of Budd-Chiari syndrome, complicated by portal vein thrombosis. Note the tangle of vessels in the porta hepatis. 134

Angiography, although invasive, continues to be employed to evaluate the status of the portal venous system. Patency of vessels, vascular pressures, collateral flow pathways, nonoccluding thrombus (Fig 42) and direction of flow can all be identified by angiography. Angiography cannot assess blood flow rates. It may be used to evaluate the portal system although CT, ultrasound, and MRI provide increasingly important noninvasive ways to study this system. The femoral artery approach is generally preferable for percutaneous catheterization although the axillary artery on the left can be used. Local complications uith the axillary approach are more likely, and when the axillary approach is used the procedure becomes more difficult technically. Umbilical vein cutdowns, percutaneous puncture of the spleen with angiography, and transhepatic puncture may all be used as part of the evaluation of the portal venous system. Indications for such invasive approaches are becoming more limited.16 Curr

Probl

Diagn

Radio/,

July/August

1992

FIG 40. A, CT reveals Tesla tumor

low density show signal intensity involvement.

mass in the right lobe oPthe liver and suggests portal vein within the portal vein confirming thrombosis. Inhomogeneity

Superior mesenteric or celiac arterial angiography requires large doses of intravascular contrast and prolonged filming to adequately visualize the portal system. The use of digital vascular systems may permit significant reduction in contrast doses and film timing. Venous opacification can be optimized by the use of vasodilators. Vasodilators used in angiography include tolazoline (Priscoline), prostaglandin E and FZu, papaverine, bradykinin, and glucagon.16 Use of vasodilators causes rapid arterial flow and promotes prompt, dense venous opacification of subsequently injected contrast agents. Varices are seen on the venous phase of the arteriogram. Newer nonionic and low osmolar ionic contrast agents cause less dilution and may enhance portal opacification. Vasodilators are not used in the presence of active or recent hemorrhage. Direct splenic puncture allows dense opaciiication of the portal venous system, but it represents a much more traumatic procedure with splenic laceration, fracture, or bleeding possible conse-

FIG 41. A, in a similar

occlusion. B, Tl -weighted of the liver is also noted,

Probl

Diagn

Radiol,

July/August

1992

(300/20) consistent

at 1 .O wrth

quences. This procedure is rarely used today, having been replaced by less traumatic procedures. Hepatic venous catheterization allows measurements of venous pressures to be obtained and demonstrates parenchymal stain by introducing contrast into the hepatic and portal veins. In portal vein thrombosis, hepatic venous wedge pressures are usually normal to subnormal. Transhepatic catheterization of the portal vein can be used to embolize varices but is not usually employed unless other measures have failed. Obviously, the portal vein must be open to perform such a procedure. The thrombosis which is initiated to obliterate varices may propagate to involve the portal vein and its tributaries. The development of portal vein thrombosis is the most serious complication of transhepatic obliteration of varices. In one series, one of 19 patients developed this complication;l” in a series reported by Widrich et alI7 it arose in 5 of 60 patients. Portal vein thrombosis proved fatal in some patients, but was only incidentally discovered at angiography in oth-

patient, CT showed low density within the liver. B, proton-density images (1800/45) liver and thrombosis of a similar signal intensity within the portal vein. The hepatic artery (arrow) signal void. Curr

images a finding

show anterior

extensive abnormality within the to the portal vein demonstrates

135

FIG 42. The venous phase of a superior mesenteric artery injection shows a partially occluding thrombus in the portal vein (arrow).

I

em.17.18 Another complication of transhepatic embolization of varices, hemoperitoneum secondary to the liver puncture, is seen less frequently with occlusion of the needle tract. Fever, ascitic leak, or hematoma formation may also complicate transhepatic embolization.

PLAIN

FILM

Radiographs of the abdomen generally play a small part in detecting or assessing portal vein thrombosis. Calcification seen within the portal vein on plain film has been described (Fig 431.l” ” Generally, the calcification is either within the thrombus or the wall of the portal vein. The course and pattern of branching, with involvement of major tributaries, allow portal vein calcifications to be correctly identified. The portal vein begins at the junction of the superior mesenteric and splenic veins just anterior to the inferior vena cava and to the right of the vertebral body of Ll or LZ. The main vein extends 7 to 8 cm in a relatively straight or slightly curved path posterior to the descending duodenum. The main vein bifurcates into right and left branches which enter the right and left lobes of the liver. Calcifications of the portal vein can be either overlooked or mistaken for artifact or foreign body. Cross-sectional imaging with CT or ultrasound may be necessaty to establish the calcification’s position within the vein (Fig 44). In one study of neonates with calcification of the portal vein seen radiographically,” three of the six infants had chromosomal abnormalities and three had physical anomalies, including low set ears and cardiac abnormalities. None had primary hepatic or portal disease. These findings substantiated an earlier report by Blanc et al.‘l who had 136

FIG 43. Calcifications within the portal vein are seen on plain films. Notice the oblique course of the main portal vein as it enters the liver.

noted calcifications in the portal vein in infants with congenital anomalies. Portal venous air may also be seen on plain film in the setting of pylophlebitis, a condition in which infectious material drains via the portal vein into the liver. Usually patients with portal air are .

IfIG 44. This patient, who had acute portal vein thrombosis 18 months earlier, developed calcifications (arrows) within the main portal vein.

Cur-r Probl

Diagn

Radio&

July/August

1992

extremely ill and are often septic or hypotensive. If the patient survives, portal vein thrombosis may develop. NUCLEAR MEDICINE Some studies22-28 have suggested that nuclear medicine can be used to assess the arterial and portal components of hepatic blood flow and the effects of drugs or surgery on the arterial-portal ratio. Manifestations of hepatocellular disease such as small liver, irregular, radionuclide uptake, splenomegaly, and colloid shift are often seen with nuclear medicine imaging. ASSOCIATED ETIOLOGIES VEIN THROMBOSIS ZNTRAHEPATZC THROMBOSIS

OF PORTAL OF PORTAL VEIN

Hepatocellular Disease (Cirrhosis) Cirrhosis is a predisposing factor to portal vein thrombosis in that it obstructs venous flow at the sinusoidal or intrahepatic postsinusoidal level (Fig 45). The fibrosis and distortion of the normal hepatic architecture characteristic of cirrhosis cause stagnation of venous flow and may eventually give rise to thrombosis (Fig 46). In Western adults, alco-

FIG 45. Changes of cirrhosis with marked irregularity of the liver surface and segmental hypertrophy may be seen in patients with intrahepatic portal occlusion secondary to distortion and obliteration of the veins within the liver. A hepatocellular carcinoma may become superimposed upon cirrhosis. This malignancy often arises in the cirrhotic liver and tends to invade the portal vein in the involved segment of liver.

Curr

Probl

Diagn

Rxiiol,

July/August

1992

FIG 46. Gross section of macronodular cirrhotic liver demonstrates marked irregularity of liver surface as well as distortion of the architecture secondary to fibrosis. Extrahepatic portal vein thrombosis is seen (arrow). The thrombus has propagated from its intrahepatic origin into the extrahepatic portion of the vein

hol abuse is probably the most common cause of liver disease and cirrhosis associated with portal vein thrombosis. In children, cirrhosis is often related to errors of metabolism such as tyrosinosis or Wilson’s disease, viral hepatitis, or cystic fibrosis. In very young children, neonatal hepatitis and biliary atresia are usually the predisposing factors in the development of cirrhosis. The exact incidence of portal vein thrombosis secondary to cirrhosis is unclear, and series have cited a wide range of incidence (from cl% to 64% )? Autopsy studies have estimated that as many as 20% of patients with Laennec’s cirrhosis have portal vein thrombosis.30 The presence of portal vein thrombosis has presented a formidable technical challenge to surgeons performing orthotopic liver transplantation for liver failure. In the past, a known preexisting thrombosis of the portal vein with or without involvement of its tributaries was a relative contraindication to liver transplantation. (Fig 471. In a large series of patients (1,585 patients) undergoing liver transplantation at the University of Pittsburgh, 2.1% were discovered to have preexisting portal vein thrombosis.31 In a study from Japan in 1984,2s 708 consecutive patients with unequivocal cirrhosis underwent transhepatic portography or superior mesenteric arterial portography. Excluding two patients in whom portal vein thrombosis was believed to be secondary to splenectomy, only four patients were demonstrated to have portal vein thrombosis. This study indicates a calculated incidence of portal vein thrombosis of 0.5% to 3% in cirrhotic patients

137

duce hepatic vein occlusion. Venous occlusion of the liver may be related to chemotherapeutic agents or is an unusual response to a parasitic infestation such as malaria. Acute reversal of blood flow within the portal vein is noted on imaging studies of patients with Budd-Chiari syndrome. Stagnation of flow predisposes to portal vein occlusion (Fig 481. Histopathologically, the venous outtlow obstruction causes sinusoidal dilatation with congestion and eventual fibrosis. The fibrosis within the sinusoidal bed can lead to eventual resistance to inflow and thrombosis of the portal vein system. Collateralization around the obstructed hepatic outflow will develop . FIG 47. This cirrhotic patient was being evaluated for liver transplantation. Computed tomography demonstrates massive ascites and tangle of vessels (arrow) instead of an identifiable portal vein.

without splenectomy. Whether the cause of cirrhosis, chronic hepatitis in Japan or alcoholic liver disease in the West, affects the incidence of portal vein thrombosis is unknown. Increasingly sophisticated surgical techniques and grafting procedures have allowed treatment of portal and splanchnic vein thrombosis so that even patients with extensive splanchnic thromboIn sis can be candidates for liver transplantation. is expected, situations in which such thrombosis long segments of donor iliac vein may be harvested to provide bypass graft material to use if necessary.32

Budd-Chiari

Thrombus

Hepatocellular carHepatoceNular Carcinoma.cinoma is one of the most common malignancies worldwide. It is especially frequent in East Asia and South Africa. Most patients have postnecrotic cirrhosis of the liver secondary to hepatitis B exposure. In the West, hepatocellular carcinoma also arises most often within the cirrhotic liver, usually secondary to alcohol abuse. Approximately onehalf of cases of hepatocellular carcinoma in the United States arise in patients with preexisting cirrhosis.34 Symptoms of hepatocellular carcinoma may include pain, jaundice, deterioration of liver function, or an acute abdomen with hemoperitoneum secondary to tumor rupture. If symptoms are sec-

Syndrome

Portal vein thrombosis may occur in as many as 20% of patients with Budd-Chiari syndrome.33 Budd-Chiari, a rare condition, is an obstruction of the hepatic venous outflow manifested by abdominal pain, severe ascites, and hepatomegaly. Imaging studies show hepatomegaly, often with marked enlargement of the caudate lobe. This selective enlargement results from the fact that the caudate drains directly into the inferior vena cava rather than via the hepatic veins. Often the cause of the Budd-Chiari syndrome is unknown, but when known, the etiologies are similar to those of primary portal vein thrombosis. Hypercoagulable states, neoplasms, trauma, congenital abnormalities and certain medications such as birth control pills predispose to the development of Budd-Chiari syndrome. The hypercoagulability state induced by oral contraceptives is not as apt to produce portal vein thrombosis as it is to pro-

138

Tumor

FIG 48. Portal vein occlusion was present Budd-Chiari syndrome secondary varices (arrowheads) and several are identified (Large arrow).

Curr

Probl

in this patient with a history of to birth control pills. lntrahepatic collaterals at the porta hepatis

Oiagn

R&id,

July/August

1992

FIG 49. A, this young man with chronic hepatitis presented with acute decompensation of liver function. Computed tomography shows a large, low-density mass in the right lobe of the liver w&h thrombosis of the portal vein; B, invasion of the inferior vena cava (arrow) and the right hepatic vein has occurred. C, scans into the chest show multiple pulmonary metastases.

ondary to the neoplasm, the disease is usually quite advanced. The prognosis for patients with hepatocellular carcinoma is dismal; median survival time is 1 to 6 months in untreated patients. Surgical therapy offers the only chance for either long-term cure or palliation in patients with hepatocellular carcinoma. Ringe et al.35 treated 198 patients with hepatocellular carcinoma, fibrolamellar carcinoma, or mixed hepatocholangiocellular carcinoma using either partial hepatectomy or liver transplantation. Survival rates at five years were 35.8% after liver resection and 15.2% after transplantation. Factors significantly improving long-term outcome in these patients included absence of vascular invasion and absence of portal vein thrombosis. All forms of hepatocellular carcinoma, whether unifocal, diffusely infiltrative, or multifocal, have a strong propensity to invade vascular structures (Figs 49 and 50). Sometimes the intravascular tumor thrombus extends in a snake-like fashion in the portal vein or its branches in a hepatofugal di-

rection. Shimokawa et al.36 found pathologically that 70% of 113 hepatocellular carcinomas had portal vein thrombus and that 13% had hepatic vein thrombus. Albacete et al. found the extrahepatic portal vein to be involved in 32% of cases.37 The tumor invades the veins of the involved hepatic segment. (Fig 51). The presence of tumor thrombus in the main trunk or major branches of the portal vein involved by hepatocellular carcinoma usually indicates a poor prognosis.’ Liver MetastasesInvasion and involvement of the portal vein by tumor thrombus in patients with hepatocellular carcinoma is well recognized. Its reported incidence is 26% to 36% by diagnostic tests and 70% in autopsy series.38’ 3s Portal vein thrombosis secondary to liver metastases is generally believed to be rare. This general principle leads most diagnosticians to a presumption of hepatocellular carcinoma if a mass lesion in the liver is seen with associated portal vein thrombosis on imaging studies. Autopsy studies suggest a 5% incidence of portal

FIG 50. A, this patient with alcoholic liver disease had a rapidly climbing alpha-fetoprotein level. Computed tomography appearing liver with a low-density mass in the left lobe. B, C, CT performed in the venous phase after celiac artery vein occlusion involving the left branch of the portal vein secondary to tumor invasion.

Curr

Pmbl

Diagn

Radio&

July/August

1992

shows a cirrhoticinjection shows portal

139

EXTRAHEPATIC PORTAL VEIN

OCCLUSION

OF THE

Encasement or compression of or injury to the portal vein outside of a normal liver may lead to thrombosis, which is often followed by significant collateralization around the porta hepatis (Fig 52). Stasis and hypercoagulable states, as well as inflammatory changes, also predispose to extrahepatic occlusion. Pancreatitis and intra-abdominal inflammatory processes may contribute to portal vein stasis and thrombosis. Hypercoagulable FIG 51. Tumor

fills this

endothelial-lined

space

within

the liver.

vein thrombosis with liver metastases; a prospective study horn Montreal by Atri et al?’ suggested an 8% incidence of portal vein thrombosis related to metastatic involvement of the liver. This study suggested that portal vein thrombosis generally occurred in patients with numerous or diffuse deposits of metastatic disease, rather than with a small burden of disease. No collateral veins were detected in their cases of portal vein thrombosis, perhaps due to the relatively short time course of thrombosis. The suspected mechanism of portal vein thrombosis is thought to be encasement of and stasis within the vein rather than frank tumor invasion as is seen with hepatocellular carcinoma. Heaston et a13’ at M. D. Anderson Cancer Center in Houston, Texas, studied 12 patients with metastatic involvement of the liver and portal vein abnormalities seen at angiography. Tumor thrombus was present in the portal vein in two patients with metastases. Interestingly, one of the metastases with tumor thrombus in the portal vein was a deposit of renal cell carcinoma, another malignancy similar to hepatocellular carcinoma, with a propensity to invade veins. Tumor thrombus within the portal vein receives its blood supply primarily from the hepatic artery with some contribution from the vasa vasorum of the portal vein. Obstruction of the portal vein related to metastatic disease can occur from either intrinsic or extrinsic blockage of the vein or its branches.3s Intrinsic occlusion usually involves metastases from tumors of the GI tract which embolize to the liver via the portal vein. Extrinsic occlusion of the portal vein usually occurs secondary to metastases (e.g., breast and lung carcinoma) which are transported by the systemic circulation and reach the liver via the hepatic artery. Encasement and compression of the main portal vein and its branches can then result in thrombosis. 140

States

Myeloproliferative Disorders.-The chronic myeloproliferative disorders (particularly untreated polycythemia Vera and myelofibrosisl have long been associated with venous thrombosis. Some 75% of patients with polycythemia Vera or myelofibrosis who require surgery develop postoperative thrombotic complications.40 Because the portal vein transports blood at a relatively low flow rate between two venous circulations, it is susceptible to thrombosis in situations of hypercoagulability (Figs 53 and 54). The exact cause of portal vein thrombosis associated with polycythemia Vera is unclear. The elevated packed cell volume and elevated blood viscosity create an environment in which portal vein thrombosis easily occurs. Encasement and compression of the portal vein by extramedullary hematopoietic tissue could predispose a patient to thrombosis. Elevated levels of platelets are present with myeloproliferative disorders. Long-term anticoagulation and prophylaxis with aspirin are used

FIG 52. Extrahepatic portal vein occlusion arises in the setting of a normal liver with injury, stasis, or encasement of the portal system or its tributaries. Curr

Probl

Diagn

Radiol,

July/August

1992

FIG 53. A, B, contrast-enhanced well as extensive

portal

CT scans of a young man with polycythemia and splanchnic vein thrombosis (arrowheads).

to combat the effects of the numerous platelets and minimize the risk of thrombosis. Evaluation of patients to exclude hypercoagulable states (e.g., myeloproliferative disorders and enzymatic deficiencies) should be considered if portal or mesenteric venous thrombosis is encountered without obvious cause. On the other hand, patients with known myeloproliferative conditions might be evaluated to exclude unsuspected portal and splanchnic thrombosis.

Afrer SpZenecforny.-The thrombocytosis that occurs after splenectomy for any cause may result in portal vein thrombosis.41 Platelet counts within the normal range (140,000 to 440,000 per mm31 preoperatively can be expected to increase 30% to 100% after splenectomy, peaking 7 to 20 days after surgery.4Z Sometimes platelet counts become

FIG 54. Ultrasound of the portal region in a middle-aged man with polycythemia vera demonstrates thickening of the wall of the portal vein consistent with previous thrombosis and recanalization. This patient was hospitalized for deep venous thrombosis of his thigh, also secondary to his hypercoagulable state. Curr

Probl

Diagn

Radial,

July/August

1992

vera demonstrate

splenomegaly

with areas

of infarctron

(arrow),

as

significantly elevated (e.g., 600,000 to 800,000 per mm31 creating a hypercoagulable state. Postsplenectomy thrombocytosis was first described in 1923, and authors4’, 43 have recognized that this is not a benign condition. It can lead to significant sequelae such as thrombophlebitis of the lower extremities, portal and mesenteric venous occlusion, pulmonary embolism, and possibly death. Boxer et al.& and Salter and Sherlock4’ found that when splenectomy was performed because the patient had a myeloproliferative disorder such as myelofibrosis or polycythemia Vera, there was clearly an increased risk for thromboembolic events. A comparable risk was not present when splenectomy was performed after trauma or incidentally at surgery. Other authors4’, 46, 47 have also suggested that patients undergoing splenectomy for hematologic disorders incur a disproportionate risk of portal and mesenteric vein thrombosis as compared with other complications. Portal vein thrombosis may occur in the immediate postoperative period or several years after surgery. Clinically, portal vein thrombosis after splenectomy can present as a catastrophic illness leading to death, or it may have relatively few symptoms. Abdominal pain, nausea, vomiting, low-grade fever, development of ascites, and edema may be accompanied by an ileus pattern on radiographs. Mortality is high and approaches 20% if the condition is untreated.41 The diagnosis is frequently not recognized until autopsy. Prolonged unexplained febrile events after splenectomy may suggest portal vein thrombosis. Platelet function abnormalities may be more important than elevated numbers of platelets in causing thromboembolic complications. Blood cell deformability is decreased and blood viscosity 141

rises after splenectomy as we11.41 Stasis in the remnant of an enlarged splenic vein may also predispose to thrombosis. If a patient has preexisting splenomegaly and hyperqplenism, the splenic vein may have reached a diameter of 3 to 4 cm. Thrombosis can form on the injured endothelium, especially if platelet abnormalities are present. Ligation of the splenic vein at its junction with the inferior mesenteric vein may prevent formation of a diverticulum where thrombus can occur. Treatment including anticoagulation, antiplatelet therapy, or chemotherapy to prevent thrombocytosis4’ has been used. Because portal vein thrombosis can occur months or years after splenectomy, long-term treatment may need to be contemplated.

activity of antithrombin III, a globulin produced by the liver. Other conditions in which antithrombin III activity is diminished are cirrhosis and hepatitis. Patients who have had myocardial infarction and those receiving estrogen-containing progestational agents5’ are also at risk. Thrombotic episodes usually occur in adulthood in patients with antithrombin III deficiency. Approximately 90% of cases involve leg or iliac vein thrombosis. Mesenteric vein thrombosis occurred therapy should be underin 8.3%.53 Prophylactic taken in patients with known antithrombin III deficiency who are having elective surgery or after childbirth when the risks of thrombotic complications are increased.51

Enzymatic Deficiencies.-PmrmN C DEFXIENCZY. -Protein C deficiency is an inherited condition in which patients tend to develop superficial and deep venous thrombosis of the extremities, pulemboli, and splanchnic venous thrombomon sis 48~ This tendency to venous thrombosis is secondary to a deficiency of an anticoagulant enzyme (protein Cl that inactivates certain coagulation cofactors and stimulates fibrinolysis. Although this may be a hereditary condition, protein C deficiency may also be seen in patients with liver disease. When related to liver disease, deficiency of protein C is usually secondary to diminished protein synthesis. Patients with protein C deficiency are treated with long-term anticoagulation. In patients in whom portal vein thrombosis is identified without obvious cause, protein C activity should be assayed to establish whether or not a deficiency exists.48

Injury/Encasement

PROTEIN S DEFICIENCY.-Protein S is a vitamin K-dependent protein that inhibits blood clotting by serving as a cofactor to activated protein C. Severe recurrent venous thrombosis may result in patients deficient in protein S because of inability to regulate intravascular clot formation.50 ANTITHROMBIN III DErtcim,cy.-Antithrombin III deficiency is another inherited condition, transmitted as an autosomal dominant trait, which is associated with thrombophlebitis and pulmonary embolism? Gruenberg et a15’ and other authors52’53 have suggested that patients with *primary” or unexplained portal and mesenteric vein thrombosis should be tested to determine whether an inherited antithrombin III deficiency exists that accounts for their thrombotic tendency. Patients with inherited antithrombin III deficiency have a 50% reduction in the normal level of 142

of the Portal Vein

Periportal Masses or PancreatitkDamage to the portal vein may occur whenever surgery is performed in the region of the liver, pancreas, or gallbladder. Such damage would predispose to thrombosis. Blunt abdominal trauma could also result in thrombosis. Encasement of the portal vein by nodal masses or the presence of inflammatory processes in the pancreas can cause compression of the vein and stasis leading to thrombosis. Granulomatous conditions including tuberculosis or sarcoidosis can produce nodal masses that can cause portal vein compression.30’ 54 Portal Vein Thrombosis

Afer

Liver Transplanta-

tion.-Transplantation of the human liver remains a difficult surgical endeavor. Vascular complications of the graft, including hepatic artery and portal vein thrombosis, pose significant risks of graft loss and patient death. Surgical teams from Pittsburgh and Dallas55’ 56 have reported the incidence of postoperative portal vein thrombosis at 2% and 1% in liver transplant patients. Situations that seem to predispose to postoperative portal vein thrombosis in transplant patients include a previous portosystemic shunt, portal vein thrombosis which existed before transplantation, and previous splenectomy. The reduced blood flow through the portal vein in patients with previous splenectomy and a preexisting portosystemic shunt is believed to be the predisposing cause of postoperative portal vein thrombosis.57 The clinical presentation in patients who develop portal vein thrombosis after liver transplantation often consists of allograft dysfunction, which may become severe enough to lead to fulminant hepatic failure. Liberal use of screening ulCurr

Probl

Diagn

Radio&

July/August

1992

trasound studies as described by Langnas et al.57 at Nebraska may demonstrate portal vein thrombosis before it becomes clinically obvious. Usually portal vein thrombosis complicating liver transplantation occurs soon after surgery with a range, in the study of Langnas et al.57 of 1 to 15 days and a mean of 5 days. Early diagnosis is considered critical for allograft salvage. Surgery is the therapy of choice for portal vein thrombosis in these patients with thrombectomy alone being adequate in some patients. Take-down of previously placed portosystemic shunts, thrombectomy followed by retransplantatio~ or thrombectomy with venous grafts are additional alternatives . Although thrombosis may develop at the venous surgical anastomosis of the portal vein, destruction of the vasculature at the hepatic sinusoidal level may contribute to the development of portal vein thrombosis. This type of injury is believed to be secondary to the length of preservation time and also, perhaps, to the specific preservation solution used57 during organ harvest and to transport time. In children, the majority of patients who developed portal vein thrombosis after liver transplantation had very small or hypoplastic portal veins at the time of surgery. Most of these children suffered from biliary atresia.57 In adults, postprocedure portal venous thrombosis seems to be related most often to inadequate venous inflow to maintain vascular patency as seen in patients with previous portosystemic shunts or splenectomy. Takedown of shunts and ligation of large collaterals aid in improving portal vein patency. Sometimes nonoperative management af portal vein thrombosis in the liver transplant patient is acceptable.57 The decision to treat patients medically is based on the severity of the graft dysfunc-

Pylephlebitis Suppurative phlebitis of the portal vein (pylophlebitis) is unusual but may be the sequela of appendicitis, cholecystitis, pancreatitis, inflammatory bowel disease, or other intra-abdominal infections that drain via the portal vein. In children or teenagers, thrombosis of the portal vein in the absence of liver disease is unusual. Inflammatory or infectious processes in the abdomen may lead to portal vein thrombosis while the liver remains normal. Because appendicitis is the most common cause of an acute abdomen in a child, portal vein thrombosis secondary to complicated appendicitis and pylephlebitis may be encountered. The more usual complications of appendicitis in a child are peritonitis and subsequent abdominal or pelvic abscesses.58 Pylephlebitis may cause the portal vein to carry infected material to the liver, resulting in abscess in the liver or thrombosis of the portal vein (Fig 55). Before antibiotics were developed, complicated appendicitis, resulting in portal vein pylephlebitis and liver abscess, was frequently lethal. This sequence of events (e.g., appendicitis + liver abscess) was the most common cause of liver abscess in children.58 Liver abscesses seen today are more often secondary to amebic infection or ascending cholangitis.58 If portal vein thrombosis occurs acutely, as in pylephlebitis, there may be severe clinical findings,

FIG 55. A, 5, a large low-density

vein

of the portal Cur-r Probl

vein Oiagn

mass in the right lobe of the liver and portal in this teenage patient who had suffered complications Radio&

July/August

1992

tion; the time interval between the diagnosis and the transplant procedure; evidence and extent of necrosis on liver biopsy; and presence of sepsis, coagulopathy, or encephalopathy, all signs of liver dysfunction. Late development of portal vein thrombosis may be managed nonoperatively if graft dysfunction is not present or severe.

thrombosis of appendicitis.

represented (Courtesy

a liver abscess and thrombophlebitis of Chris Sistrom, M.D.) 143

with abdominal pain and rapid development of problems related to portal hypertension: splenomegaly, variceal hemorrhage, or venous engorgement of the GI tract. Patients with pylephlebitis may have hepatomegaly (50% 1. One-third of patients are jaundiced. Splenomegaly is not present initially, but develops in as many as 25% of patients. Usually patients demonstrate leukocytosis, but abnormal liver function tests are present in only one-quarter of cases. Mortality approaches 50% .5s If thrombosis is gradual or incomplete, the clinical manifestations of portal hypertension may be indolent; they are not clinically obvious for a time and a more insidious course follows. Because there may be a great deal of time between the inciting event (i.e., appendicitis or other abdominal process) and the manifestations of occult portal hypertension (i.e., GI hemorrhage), the connection between the two events may not be obvious.30 The initiating event may be mild or transient, and imaging studies may provide the first clue that portal vein thrombosis has occurred. Imaging studies may show collaterals or splenomegaly and no residual portal vein. Portal vein thrombosis secondary to pylephlebitis represents a presinusoidal obstruction related to infection and inflammation in the portal venous system. Infections from a variety of disease processes in the abdomen could give rise to this complication: Crohn’s disease, diverticular disease, ischemic colitis, or ulcerating carcinoma, as well as complicated appendicitis. Any breach of the GI mucosal integrity could seed the portal system.

In newborns, phlebitis of the umbilical vein can propagate into the portal system. This complication is especially prevalent if an umbilical catheter is used (Fig 56). LarrocheGo found that 40% of neonates with umbilical vein catheters had developed portal vein thrombosis after 48 hours and 100% had thrombosis after 3 days. Presumably, sequelae are uncommon since Thompson et a161 found no cases of portal vein occlusion in 470 neonates who had had umbilical vein catheterization. The presence of gas within the portal vein, detected on plain films, ultrasound, CT or angiography, confirms the diagnosis of pylephlebitis (Fig 57). The additional observation of thrombus within the portal vein suggests septic thrombus. The presence of portal vein thrombosis in a child without significant liver disease requires an inquiry into possible causes; intra-abdominal infection may be the culprit.

Congenital

Abnormalities

of the Portal Vein

Congenital abnormalities of the portal vein include atresia or stenosis. These abnormalities are rarely recognized, but may be the underlying problem in children noted to have cavernous transformation of the portal vein without an obvious cause or explainable predisposing condition. Congenital stenosis is characterized by intimal thickening which may affect either the small intrahepatic vessels or the main vein.

Idiopathic Portal vein thrombosis has been considered idiopathic in as many as 50% of patients who have no recognizable predisposing condition (Fig 58). Certainly, the lack of clinical features of portal vein thrombosis and therefore the failure to recognize it may make identification of the underlying cause, which may have resolved, difficult. In addition, myeloproliferative disorders or enzymatic deficiencies which can be subclinical or in early stages should be considered in patients with unexplained portal vein thrombosis. Unexplained portal or splanchnic thrombosis may be secondary to a previously unrecognized clotting abnormality.

MANAGEMENT Clinical management and therapy for patients with portal vein thrombosis depend in large meaCalcification of the portal vein (arrow) is identified on CT and was sure upon the clinical setting in which the thromalso seen sonographically in this infant who had had an umbilical the age of the thrombus, and venous catheter in the neonatal period. Imaging was performed to ‘bosis is discovered, the severity or extent of the thrombosis. Portal vein evaluate persistent liver function abnormalities.

144

Curr

Probl

Diagn

Radio&

July/August

1992

FIG 57. Extensive gas in the portal venous system was death in this patient with ischemia and infarction

detected of bowel.

prior

to

thrombosis which is discovered when a patient is imaged for recurrent GI hemorrhage may be chronic and relatively compensated, and not amenable to anticoagulation. Thrombosis of the portal vein in the period after liver transplantation may require immediate surgery with thrombectomy or retransplantation. When portal vein thrombosis is discovered in the acute stage, antiplatelet therapy, anticoagulation, thrombolytic therapy, or chemotherapy4’ may be employed to aid in recanalization of the portal vein and diminish significantly elevated platelet counts. Therapy is especially useful if the thrombosis is secondary to hypercoagulability related to a myelopmliferative disorder. Patients who develop portal vein thrombosis as a complication

of liver transplantation often undergo additional surgery with thrombectomy, grafting, or retransplantation, although anticoagulation and supportive therapy may be employed if the thrombosis is not extensive and the allograft is not threatened. Patients with chronic portal vein thrombosis either with or without associated liver disease may have recurrent bouts of GI hemorrhage from varices. Control of these recurrent episodes of variceal hemorrhage becomes the dominant issue and may be accomplished via intravenous vasopressin infusion, sclerotherapy of the varices, or balloon tamponade. Transhepatic obliteration of varices can only be performed if the portal vein is not completely obstructed because the catheter must cannulate the portal vein. Surgically placed or percutaneously performed shunt procedures can decompress the collateral pathways sufficiently to diminish the occurrence of GI hemorrhage. Surgery may represent a formidable procedure and lead to life-threatening hemorrhage in the face of extensive collateral pathways.

SUMMARY

Recognition of the various imaging features and predisposing causes of portal and mesenteric vein thrombosis allows a clinical condition that may have severe recurring sequelae to be identified. Often the radiologist is the first to suspect that portal vein thrombosis has occurred.

ACKNOWLEDGEMENTS

The author wishes to thank Dr. Curtis Sutton for organizational assistance and Ms. Linda Pigott for preparation of manuscript.

FIQ SB. A, B, cavernous and no obvious

Cum

fmid

LMagn

transformation predisposing

Radid,

of the portal vein with large, tortuous reason for splanchnic thrombosis.

J&y/August

1992

hepatopedal

collaterals

is identified

in this patient

with a normal

liver

146

REFERENCES

1. Albertyn LE: Case report: Acute portal vein thrombosis. Clin Radio1 1987; 38:645-648. 2. Belli L, Romani F, Rio10 F, et al: Thrombosis of portal vein in absence of hepatic disease. Surg Gynecol Obstet 1989;169:46-49. 3. Webb LI, Sherlock S: The aetiology, presentation and natural history of extra-hepatic portal venous obstruction.QuartJ Med 1979;48:627-639. 4. Riisch J, Dotter CT: Extrabepatic portal obstruction in childhood and its angiographic diagnosis. AJR 1971; 112:143-149. 5. Hammerman AM, Kotner LM Jr, Doyle TB: Periportal contrast enhancement on CT scans of the liver. AJR 1991;156:313-315. 6. Mori H, Hayashi K, Uetani M, et al: High-attenuation recent thrombus of the portal vein: CT demonstration and clinical significance. Radiology 1987; 163:353-356. 7. Miller VE, Berland LL: Pulsed Doppler duplex sonography and CT of portal vein thrombosis. AJR 1985;

23. Fleming JS, Humphries NLM, Karran SJ, et al: In vivo assessment of hepatic-arterial and portal-venous components of liver perfusion: Concise communication. J NuclMed 1981;22:18-21. 24. Wraight EP, Barber RW, Ritxon A: A relative hepatic arterial and portal flow in liver scintigraphy. Nucl Med Commun 1982;3273-279. 25. Biersack HJ, Tortes J, Thelen M, et al: Determination of liver and spleen perfusion by quantitative sequential scintigraphy: Results in normal subjects and in patients with portal hypertension. Clin Nucl Med 1981; 6218-220. 26.

27.

28.

145:73-76. 8.

9. 10. 11. 12.

13. 14. 15. 16. 17. 18. 19. 20. 21. 22.

146

Martin K, Balfe DM, Lee JKT. Computed tomography of portal vein thrombosis: Unusual appearances and pitfalls in diagnosis. J Comput Assist Tomogr 1989; 13:811-816. Ralls PW: Color Doppler sonography of the hepatic artery and portal venous system. AJR 1990; 1.55517-525. Bradley WG Jr, Waluch V: Blood flow: Magnetic resonance imaging. Radiology 1985; 154:443-450. Hricak H, Ampam E, Fisher MR, et al: Abdominal venous system: Assessment using MR. Radiology 1985; 156:415-422. Silverman PM, Patt RH, Garra BS, et al: MR imaging of the portal venous system: Value of gradient-echo imaging as an adjunct to spin-echo imaging. AJR 1991; 157:297-302. Zirinsky K, Mark&z JA, Rubenstein WA, et al: MR imaging of portal venous thrombosis: Correlation with CT and sonography. AJR 1988; 150283-288. Edelman RR, Zhao B, Liu C, et al: MR angiography and dynamic flow evaluation of the portal venous system. AJR 1989;153:755-760. Levy HM, Newhouse JH: MR imaging of portal vein thrombosis. AIR 1988;151283-286. Johnsrude IS, Jackson DC, Dunnich NR: A Practical Approach to Angiography, ed 2. Boston, Little, Bmwn and Co, 1987, pp 335, 361-370. Widrich WC, Robbins AH, Nabseth CD: Transhepatic embolization of varices. Cardiovasc Zntervent Radio1 1980; 3298-303. Widrich WC, Johnson WC, Robbins AH, et al: Transhepatic Variceal Occlusion. New York, Academic Press. Baker SR, Broker MH, Charnsangavej C, et al: Calcification in the portal vein wall. Radiology 1984; 152:lS. Friedman AP, Hailer JO, Boyer B, et al: Calcified portal vein thmmboemboli in infants: Radiography and ultrasonography. Z%adiology 1981; 140:381-382. Blanc WA, Berdon WE, Baker DH, et al: Calcified portal vein thmmboemboli in newborn and stillborn infants. Radiology 1967; 88287-292. Fleming JS, Ackery DM, Walmsley BH, et al: Scintigraphic estimation of arterial and portal blood supplies to the liver. J Nucl Med 1983; 24:1108-1113.

29.

30.

31. 32. 33. 34.

35.

36.

37.

Sarper R, Fajman WA, Rypins EB, et al: A noninvasive method for measuring portal venous/total hepatic blood flow by hepatosplenic radionuclide angiography. Radiology 1981;141:179-184. Sarper R, Tarcan YA: An improved method of estimating the portal venous fraction of total hepatic blood flow from computerized radionuclide angiography. Radiology 1983; 147559-562. Juni JE, Gross MD, Meyers IJ, et al: Quantitative analysis of hepatic artery and portal vein blood flow by deconvolutional analysis. Eur J Nucl Med 1985; llA9. Okuda K, Ohnishi K, Kimura K, et al: Incidence of portal vein thrombosis in liver cirrhosis. An angiographic study in 708 patients. Gastroenterology 1985; 89279-286. Scully RE, Mark EJ, McNeely WF, et al: A 15-year-old boy with fever of unknown origin, severe anemia, and portal-vein thrombosis. Case records of the Massachusetts General Hospital. N Engl J Med 1991; 324:1.575-1584. Stieber AC, Zetti G, Todo S, et al: The spectrum of portal vein thrombosis in liver transplantation. Ann Surg 1991;213:199-206. Tzakis A, Todo S, Steiber A, et al: Venous jump grafts for liver transplantation in patients with portal vein thrombosis. Transplantation 1989; 48530-531. Vogelzang RL, Anschuetz SL, Gore RM: Budd-Chiari syndrome: CT observations. Radiology 1987; 163:329-333. Lawson TL, Lincoln LB, Foley DW: Malignant neoplasms of the pancreas, liver and biliary tract, in Bragg DG, Rubin P, Youker JE teds): Oncologic Imaging. New York, Pergamon Press, Inc, 1985, pp 316-325. Ringe B, Pichlmayr R, Wittekind C, et al: Surgical treatment of hepatocellular carcinoma: Experience with liver resection and transplantation in 198 patients. WorldJSurg 1991;15270-285. Shimokawa Y, Kubo Y, Arishima T, et al: Studies on primary liver carcinoma. 1. Clinico-pathological characteristics of gross anatomy of hepatocellular carcinoma according to the Nokashima-Okuda classification. Acta HepatoZJap 1975;16:752-762. Albacete RA, Matthews MJ, Saini N: Portal vein thmmboses in malignant hepatoma. Ann Intern Med 1967; 67:337-

348.

Atri M, de Stempel J, Bret PM, et al: Incidence of portal vein thrombosis complicating liver metastasis as detected by duplex ultrasound. J Ultrasound Med 1990; 9285-289. 39. Heaston DK, Chuang VP, Wallace S, et al: Metastatic hepatic neoplasms: Angiographic features of portal vein involvement. AZR 1981; 136:897-900.

38.

Curr

Probl

Diagn

Radio&

July/August 1992

40. Boughton BJ. Hepatic and portal vein thrombosis: EMJ 1991; 302:192- 193. 41. Kowal-Vern A, Radhakrishnan J, Goldman J, et al: Mesenteric and portal vein thrombosis after splenectomy for autoimmune hemolytic anemia. J Clin Gastroenterol 1988; 10:108-110. 42. Balz J, Minton JP: Mesenteric thrombosis following splenectomy. Ann Surg 1975; 181:326-128. 43. Broe PJ, Conley CL, Cameron JL: Thrombosis of the portal vein following splenectomy for myeloid metaplasia. Surg Gynecol Obstet 1981; 152:488-492. 44. Boxer MA, Braun J, Ellman L: Thromboembolic risk of postsplenectomy thrombocytosis. Arch Surg 1978; 113:808. 45. Salter PP, Sherlock EC: Splenectomy, thrombocytosis and venous thrombosis. Am Surg 1957;‘23:549. 46. Bull SM, Zikria BA, Ferrer JM: Mesenteric venous thrombosis following splenectomy: Report of two cases. Ann Surg 1965; 162:938. 47. Gordon DH, Schatlher D, Bennett JM, et al: Postsplenectomy thrombocytosis. Arch Surg 1978; 113:713. 48. Orozco H, Guraieb E, Takahashi T, et al: Deficiency of protein C in patients with portal vein thrombosis. Hepatology 1988; 8:1110-1111. 49. Valla D, Denninger M-H, Delvigne J-M, et al: Portal vein thrombosis with ruptured esophageal varices as presenting manifestation of hereditary protein C deficiency. Gut 1988; 29:856-859. 50. Comp PC, Esmon CT: Recurrent venous thmmboembolism in patients with a partial deficiency of protein S. N Engl J Med 1984; 311:1525-1528. 51. Gruenberg JC, Smallridge RC, Rosenberg RD: Inherited antithmmbin-III deficiency causing mesenteric venous infarction: A new clinical entity. Ann Surg 1975; 181:791-794.

Curr Pmbl Diagn Radial, July/August 1992

52. Collins GJ Jr, Zuck TF, Zajtchuk R, et al: Hypercoagulability in mesenteric venous occlusion. Report of two cases. Am J Surg 1976; 132:390-391. 53. Maung R, Kelly JK, Schneider MP, et al: Mesenteric venous thrombosis due to antithmmbin III deficiency. Arch Path01 Lab Med 1988; 112:37-39. 54. Ruttenberg D, Graham MD, Burns D, et al: Abdominal tuberculosis-A cause of portal vein thrombosis and portal hypertension. Digest Dia Sci 1991; 36:112-115. 55. Lerut J, Tzaks AG, Bmn K, et al: Complications of venous reconstruction in human orthotopic ‘liver tntnsplantation. Ann Surg 1987; 205:404-414. 56. Sayage LH, Husberg BS, Klintmalm GB, et al: Vascular complications in adult liver transplant patients. Value of postoperative Doppler ultrasound screening and the surgical management of hepatic arterial thrombosis. C/in Transpl 1989; 3:344-348. 57. Langnas AN, Marujo W, Stratta RJ, et al: Vascular complications after orthotopic liver transplantation. Am .I Surg

1991;161:76-83.

Slovis TL, Haller JO, Cohen HL, et al: Complicated appendiceal inflammatory disease in children: pylephlebitis and liver abscess. Radiology 1989; 171:823-825. 59. Babcock DS: Ultrasound diagnosis of portal vein thmmbosis as a complication of appendicitis. AJR 1979; 133:317-319. 60. Larmche J-CI: Incidents et accidents au tours du cathBterisme ombilical artlriel et veineux. Etude anatomique. Ar Fr Pediatr 1969; 26:1065- 1083. 61. Thompson EN, Sherlock S: The aetiology of portal vein thrombosis with particular reference to the mle of infection and exchange transfusion. Quart J Med 1964; 33:387-389. 58.

147