Applied Radiology

Dr. Zimmerman and Dr. Grant are from the UCLA Medical Center/West Los Angeles VAMC; Dr. Lu is from the UCLA Medical Center; Dr. Farooki is from the Ohio State University School of Medicine; Dr. Melany is from Cedars-Sinai Medical Center; and Dr. Duerinckx is from the University of Texas, Southwestern-Dallas VAMC.

Diseases of the hepatic vasculature may be diagnosed by observing intrinsic abnormalities of the vessels, and, frequently, hepatic or extrahepatic anatomic abnormalities that may underlie or be a consequence of the vascular disorder. Doppler sonography provides a combination of hemodynamic and anatomic information, and is therefore an excellent modality for evaluation of these clinical problems. The Doppler evaluation of the liver should include a thorough evaluation of the liver parenchyma and other relevant intra-abdominal structures. This article will review technical issues relevant to Doppler ultrasound, and describe the Doppler sonographic features of normal hepatic vessels, disorders involving the hepatic vasculature.

Technical issues

There are several forms of Doppler sonography, including color Doppler sonography (CDS), pulsed or spectral Doppler, and power Doppler. CDS measures the mean Doppler frequency shift of blood flow by color coding the information and superimposing it on a gray-scale image. CDS provides a global depiction of flow, allowing large regions to be surveyed rapidly, and facilitating placement of a sample volume for spectral analysis.

Pulsed or spectral Doppler is obtained by positioning a sample volume in a vessel visualized on gray-scale or CDS image, and a spectrum, or graph of velocities from within the sample volume, is plotted as a function of time. The operator estimates the Doppler angle with the assumption that flow direction is parallel to the vessel wall, and this value is used to calculate flow velocity. The resulting spectrum allows assessment of flow velocity and waveform morphology, both of which provide information about regional hemodynamics.

Vascular impedance or resistance is measured using several indices, the most common being the resistance index (RI):

RI = PSV - EDV

PSV

where PSV is peak systolic velocity and EDV is end diastolic velocity. The RI is a function of multiple factors, but is primarily related to the resistance of the distal, receiving vascular bed. The morphology of the waveform, such as the slope of the systolic upstroke, can also indicate the presence of a proximal flow restricting lesion. ^1,2

Power Doppler (energy map) measures and displays the power (or amplitude) of Doppler signal, which is primarily a reflection of the quantity of blood present, rather than its velocity (as in CDS). As this technique is highly sensitive to flow, it is best suited for determination of whether or not flow is present. In contrast to CDS, flow direction and velocity information are not provided.

Doppler of normal hepatic vessels

The pulsed Doppler spectrum of the normal hepatic artery is characterized by pulsatile, low-resistance flow, with a broad systolic peak, abundant antegrade flow in diastole, and spectral broadening (figure 1A). The continuous, low-resistance flow is typical for parenchymal organs (such as the kidneys, spleen, pancreas, or brain) that have a continuous, high oxygen demand. The normal portal vein flow direction is toward the liver (antegrade, hepatopedal), and the Doppler spectrum has continuous, non-pulsatile flow with minor fluctuations due to respiratory and cardiac activity (figure 1B). The normal hepatic vein has a complex triphasic waveform, due to pulsatility from the right atrium, respiration, and changing abdominal pressure. There are two phases of flow toward the heart (during right atrial filling) and one phase of flow away from the heart (during right atrial systole) (figure 1C). ³

Disorders of the hepatic vasculature: Hepatic artery

In cirrhosis, the hepatic artery may become enlarged, with increased flow, presumably as a homeostatic mechanism to maintain hepatic perfusion in response to decreased portal venous flow to the liver. Doppler sonography reveals enlarged, tortuous hepatic arteries with high velocity flow, which may be manifest by aliasing on color Doppler. Other conditions that may cause hepatic artery enlargement include intrahepatic arteriovenous shunting (vascular neoplasms), hereditary hemorrhagic telangectasia, and chronic active hepatitis. ⁴

A hepatic artery aneurysm or pseudoaneurysm may result from atherosclerosis, infection, trauma, pancreatitis, and vasculitis. Doppler evaluation reveals a cystic lesion containing turbulent, arterial flow. ⁵ Hereditary hemorrhagic telangiectasia (HHT) is an autosomal dominant disorder characterized by telangiectasias; arteriovenous malformations (AVM); and aneurysms of the skin, mucosa, and vessels of the lung, liver, and central nervous system (CNS). Doppler reveals large tortuous feeding arteries with high velocity, aliased flow, multiple dilated vessels representing AVMs, and large draining veins (figure 2). On gray-scale imaging, the liver may have areas of fatty change and fibrosis, though it is controversial whether HHT results in cirrhosis. ⁴ A hepatic artery-portal vein fistula may form from biopsy and trauma, with Doppler findings of turbulent, high-velocity, low-resistance flow in the hepatic artery, a CDS "bruit" (random assignment of color in perivascular soft tissue due to tissue vibration from high-velocity flow), and arterialized, frequently retrograde, flow in the portal vein. ³

Hepatic arterial liver transplant complications

The hepatic artery is the sole vascular supply to the biliary tree in a liver transplant, and consequently hepatic artery stenosis (HAS) and hepatic artery thrombosis (HAT) can cause graft failure and biliary necrosis. Doppler evaluation includes direct evaluation of the hepatic artery, as well as assessment of the intrahepatic arterial waveform morphology, which can suggest abnormalities in the hepatic artery itself. Direct criteria for HAS (>50%) include a focal velocity increase (>200 cm/sec) with associated turbulence (figure 3A). The criterion for HAT is a lack of Doppler detectable intrahepatic arterial flow. The addition of criteria that evaluate the morphology of the intrahepatic arterial waveform raise the sensitivity for detection of hepatic artery compromise (HAT or HAS) to a very high level (97%). ⁶ The criteria are a low resistive index (< 0.5) and/or a systolic acceleration time >0.8 sec (figure 3B). In order to avoid false positive diagnoses, it should be noted that a low resistive index may be present in a normal transplant intraoperatively or in the early post-transplantation period. Gray scale findings that may be associated with arterial compromise include biliary dilatation (due to stricture), infarction, and biloma. ⁷

Portal vein

Portal vein thrombosis (PVT) has multiple etiologies, including cirrhosis, hypercoagulable states, surgery, intraperitoneal inflammatory processes such as pancreatitis and appendicitis, and malignancy (hepatocellular or pancreatic carcinoma and liver metastases). The Doppler ultrasound criteria are absence of Doppler detectable flow and echo-genic thrombus and enlargement of the vein on gray scale. ^3,4 Whenever a Doppler diagnosis of vascular occlusion is invoked, it is essential to ensure that this is not due to technical factors. Optimizing the angle of insonation, pulse repetition frequency, and wall filter are important. Additionally, patent vessels at similar depth with comparable velocity can serve as an internal standard to confirm adequacy of technique. Since very slow flow, which is often present in cirrhosis, may be undetectable by Doppler and result in a false positive, the diagnosis of thrombosis should be confirmed by an alternative modality, unless definite vein expansion and echogenic clot are present. Gray scale imaging alone may yield a false negative due to anechoic acute clot, and a false positive due to high echogenicity of slowly flowing blood related to RBC Rouleaux formation. If portal vein thrombosis is chronic and persistent, the vein may become fibrotic, and collateral vessels in the porta hepatis may develop, resulting in cavernous transformation of the portal vein. The Doppler ultrasound findings include echogenic or nonvisualized portal vein, which is replaced by a network of tortuous vessels containing low velocity venous signal. ^3-5

Neoplastic portal vein thrombosis can be diagnosed with high specificity by the presence of pulsatile intrathrombus flow (hepatopedal or hepatofugal) with different waveform morphology from the hepatic artery and a nonthrombosed portion of the portal vein (figure 4). These findings are virtually diagnostic of tumor thrombus, and are due to flow in tumor neovascularity, analogous to the angiographic "thread and streaks" sign. Rarely, bland thrombus can appear to contain pulsatile flow, if the vein already contains pulsatile flow from another etiology, and a recanalized portion of thrombus is insonated. Continuous intrathrombus flow may be present in bland or tumor thrombus. ⁸

Portal venous hypertension

Portal venous hypertension is due to venous obstruction, which can occur at the pre-, intra-, or posthepatic levels. In North America, the most common causes are cirrhosis (intrahepatic) and portal vein thrombosis (prehepatic). The Doppler ultrasound diagnosis of portal hypertension is made by evaluating portal vein flow characteristics and size; and secondary signs, such as portosystemic collateral vessels, splenomegaly, and ascites. Portal vein flow may be bi-directional in moderate, and reversed (hepatofugal or retrograde) in severe portal hypertension (figure 5A). The prevalence of retrograde portal vein flow in cirrhotic patients is <10%. ^9,10 The pulsed Doppler waveform contour may be altered in portal hypertension. As portal hypertension develops, the mild fluctuations present in the normal venous waveform diminish, and the waveform may become monophasic. The size of the portal vein may be increased, with a portal vein diameter of >1.3 cm being 100% specific for portal hypertension, though this finding is present in only 75% of cases. The lower sensitivity is likely due to decreased portal vein size as portosystemic collaterals increase. The velocity of portal venous flow tends to decrease in portal hypertension, though using this as a criterion is difficult, as velocities vary in a given individual related to postprandial state, respiration, and position, and there is overlap between normal and abnormal. The tendencies of enlarged portal vein size and reduced flow velocity in portal hypertension are represented in the "congestive index," which is the ratio of the area of the portal vein divided by the flow velocity (ratio >0.13 cm/sec is 67% sensitive for portal hypertension). A gray scale finding related to the vasculature is the loss of portal, splenic, and mesenteric vein caliper variation with respiration. In normal individuals, the portal venous system distends with deep inspiration due to diaphragmatic descent and compression of hepatic venous flow. A subnormal (<20%) increase in portal vein diameter with deep inspiration is 81% sensitive and 100% specific for portal hypertension.

Collateral vessels can be visualized with ultrasound in 88% of patients with portal hypertension. The most important portosystemic collaterals (varices) are the coronary veins with associated esophageal varices, and the paraumbilical vein (figures 5B and C). Additional grayscale findings are the superior mesenteric vein being larger than the portal vein, splenomegaly, ascites, and changes in hepatic morphology compatible with cirrhosis (figure 5). ^{3-5, 11-13}

Portal vein in cardiac disease

The portal vein waveform may be pulsatile in patients with congestive heart failure or tricuspid regurgitation, probably due to the fluid wave being transmitted through dilated sinusoids. Doppler findings include waveform pulsatility, with a greater than 2/3 change from peak to minimal velocity, and, frequently, reversal of flow during the cardiac cycle (figure 6). ^3,5 Other causes of pulsatile portal vein are hepatic artery to portal vein fistula, cirrhosis (due to arteriovenous shunting), and portal to hepatic vein fistula.

Portal vein stenosis

Portal vein stenosis occurs as a complication of liver transplantation. Ultrasound findings include narrowing of the vein, poststenotic dilatation, and focal aliasing on CDS with a focal velocity increase on spectral doppler (three- to fourfold increase compared to prestenotic segment). ⁷

Portal vein aneurysm is a rare entity, with congenital or acquired (portal hypertension and possibly pancreatitis) etiologies. The Doppler ultrasound finding is that of a anechoic, cystic lesion in communication with the portal vein containing turbulent venous flow (figure 7). ³

Helical flow in portal vein

Helical flow is a spiral flow pattern around the long axis of the vein, as opposed to laminar flow. Helical flow is normally seen in smoothly curving vessels. The CDS appearance is alternating bands of red and blue, either orthogonal or parallel to the long axis of the vessel. On spectral Doppler, the direction of flow will vary with the location of the sample volume. Helical flow in the portal vein is seen in 2% of patients without hepatic disease, 20% of patients with end-stage liver disease, immediately after normal transjugular intrahepatic portosystemic shunt (TIPS) and liver transplantation, portal vein stenosis, and in neoplastic narrowing of the portal vein. ¹⁴

A portal vein-hepatic vein fistula is rare, and is manifest on ultrasound as flow containing cystic spaces in the liver, and pulsatile portal vein flow, possibly with a triphasic waveform. ³

Hepatic veins

Budd-Chiari syndrome (BCS) refers to group of conditions resulting in hepatic venous obstruction at the level of the large hepatic veins or the suprahepatic inferior vena cava. With the usual route of egress of blood from liver blocked, collateral routes develop. The majority (50% to 75%) of cases is idiopathic, with other etiologies including webs (uncommon in North America and Europe, common in Japan and India), tumor, coagulation diathesis, and trauma. Doppler findings include absent, reversed, dampened, or turbulent flow in the hepatic veins or inferior vena cava (figure 8), intrahepatic collateral vessels, portal vein flow reversal, slow flow, or thrombosis (20%), absent or abnormal junction hepatic vein with inferior vena cava, direct visualization of thrombus or web, vein wall thickening and irregularity, and vein stenosis with proximal dilatation. Since the caudate lobe drains directly into the inferior vena cava, this lobe is usually not involved. Liver parenchymal and extrahepatic gray scale findings may include parenchymal heterogeneity and hepatomegaly, ascites, and decreased echogenicity of affected regions in the acute phase; and enlargement of the caudate and atrophy of the right lobe, ascites, and splenomegaly in the subacute to chronic phase. ^3-5

Hepatic veno-occlusive disease (VOD) is characterized by occlusion of small centrilobular veins with no involvement of the major hepatic veins. The etiology of this entity is radiation and chemotherapy in bone marrow transplant patients, and bush tea (alkaloid) consumption in Jamaica. Ultrasound diagnosis of this disease is difficult, as the main hepatic veins and inferior vena cava are usually normal. The portal vein may have reversed or "to and fro" flow. In the proper clinical setting, rapid development of reversed portal vein flow or gallbladder wall thickening may be suggestive of the diagnosis. ⁴

Hepatic vein "shielding"

Dampening of the normal triphasic hepatic venous waveform may result when the vein is "shielded" from the hemodynamic effects of the right atrium and thorax. This may occur in the setting of cirrhosis, where it is probably due to a decrease in compliance of the hepatic vein wall from the abnormal liver parenchyma. The shielding effect can also result from venous obstruction, either intrinsic (partial thrombus, Budd Chiari syndrome) or extrinsic (mass). The spectral Doppler findings are dampened waveform with decreased amplitude of oscillations, loss of reversal phase, or completely flat waveform (figure 9). ⁴

Transjugular intrahepatic portosystemic shunts

TIPS is a common procedure for the treatment of portal hypertension and bleeding gastroesophageal varices, and consists of an expandable wire mesh stent that connects a hepatic to a portal vein branch. The Doppler findings in a normal TIPS are high velocity (usually 100 to 200 cm/sec) continuous, minimally pulsatile flow with spectral broadening. The flow direction in the portal vein branches is often toward the stent. Since there is a wide range of velocities in normal, patent stents, a baseline study is recommended to facilitate interpretation of subsequent evaluations. Complications of TIPS include stent stenosis, thrombosis, and hepatic vein stenosis, usually due to pseudointimal hyperplasia. The ultrasound criteria of stent stenosis include a focal velocity increase at the site of stenosis and/or low velocity flow in the nonstenosed portion of the stent and main portal vein, with precise quantitative criteria varying in the literature. ¹⁵ Stent occlusion is diagnosed by a lack of Doppler detectable flow in the stent. Other indicators of stent malfunction are change in portal vein branch flow direction from toward to away from the stent, reversal of flow in hepatic vein (hepatic vein stenosis), and reappearance of collaterals and ascites. ^12,15 AR

References

1. Burns PN: Interpreting and analyzing the Doppler examination. In: Taylor KJW, Burns PN, Wells PNT (eds): Clinical Applications of Doppler Ultrasound, 2nd ed, pp 55-98. New York, Raven Press, 1995.

2. Burns PN: Doppler artifacts. In: Taylor KJW, Burns PN, Wells PNT (eds): Clinical Applications of Doppler Ultrasound, 2nd ed, pp 99-108. New York, Raven Press, 1995.

3. Grant EG: Color doppler imaging of the vessels of the liver. In: Wilson SR, Charboneau JW, Leopold GR (eds): Ultrasound Categorical Course Syllabus, pp 133-142, Leesburg, VA, American Roentgen Ray Society, 1993.

4. Jeffrey RB, Ralls PW: Sonography of the Abdomen, pp 150-171. New York, Raven Press, 1995.

5. Gore RM: Vascular disorders of the liver and splanchnic circulation. In: Gore RM, Levine MS, Laufer I (eds): Textbook of Gastrointestinal Radiology, vol 2, pp 2018-2050. Philadelphia, WB Saunders, 1994.

6. Dodd GD III, Memel DS, Zajko AB, et al: Hepatic artery stenosis and thrombosis in transplant recipients: Doppler diagnosis with resistive index and systolic acceleration time. Radiology 192:657-661, 1994.

7. Dodd GD III: Sonographic diagnosis of vascular complications of hepatic and renal transplantation. In: Wilson SR, Charboneau JW, Leopold GR (eds): Ultrasound Categorical Course Syllabus, pp 301-308. Leesburg, VA, American Roentgen Ray Society, 1993.

8. Dodd GD III, Memel DS, Baron RB, et al: Portal vein thrombosis in patients with cirrhosis: Does sonographic detection of intrathrombus flow allow differentiation of benign and malignant thrombus? AJR Am J Roentgenol 165:573-577, 1995.

9. Gaiani S, Bolondi L, Li Bassi S, et al: Prevalence of spontaneous hepatofugal portal flow in liver cirrhosis. Clinical and endoscopic correlation in 228 patients. Gastroenterology 100:160-167, 1991.

10. Kawasaki T, Moriyasu F, Nishida O, et al: Analysis of hepatofugal flow in portal venous system using ultrasonic Doppler duplex system. Am J Gastroenterol 84:937-941, 1989.

11. Gore RM: Diffuse liver disease. In: Gore RM, Levine MS, Laufer I (eds): Textbook of Gastrointestinal Radiology, vol 2, pp 1968-2011. Philadelphia, WB Saunders, 1994.

12. Withers CE, Wilson SR: The liver. In: Rumack CM, Wilson SR, Charboneau JW (eds): Diagnostic Ultrasound, 2nd ed, Vol 1, pp 87-154. St Louis, Mosby, 1998.

13. Venbrux AC, Friedman AC: Diffuse hepatocellular diseases, portal hypertension, and vascular diseases. In: Friedman AC, Dachman AH (eds): Radiology of the Liver, Biliary Tract, and Pancreas, pp 49-168. St Louis, Mosby, 1994.

14. Rosenthal SJ, Harrison LA, Kirkman GB, et al: Doppler US of helical flow in the portal vein. Radiographics 15:1103-1111, 1995.

15. Kanterman RY, Darcy MD, Middleton WD, et al: Doppler sonography findings associated with transjugular intrahepatic portosystemic shunt malfunction. AJR Am J Roentgenol 168:467-472, 1997.