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AJR 2001; 176:909-912
© American Roentgen Ray Society

Doppler Sonography of Hepatic Arterial Blood Flow Velocity After Percutaneous Transhepatic Portal Vein Embolization

Yasushi Kito1, Masato Nagino and Yuji Nimura

1 All authors: First Department of Surgey, Nagoya University School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya 466-8550, Japan.

Received August 24, 2000; accepted after revision September 26, 2000.

 
Supported in part by a Grant-in-Aid for General Scientific Research (09671298 to M. Nagino) from the Ministry of Education, Science and Culture, Japan, and grants from the Uehara Memorial Foundation (Y. Nimura).

Address correspondence to Y. Nimura.


Abstract
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 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
OBJECTIVE. This study was conducted to elucidate the changes in hepatic arterial blood flow after portal vein embolization.

SUBJECTS AND METHODS. We prospectively measured the flow velocity and resistive index of the common, right, and left hepatic arteries, using Doppler sonography, in 21 patients who underwent embolization of the right portal vein. The measurements were performed before and 1, 3, 5, 7, and 14 days after embolization. We assessed the changes in liver volume with a volumetric study using CT.

RESULTS. After embolization, flow velocity in the common hepatic artery increased significantly (p < 0.0001). Flow velocity in the right hepatic artery also increased significantly (p < 0.0001), with a significant decrease in resistive index (p < 0.0001). The flow velocity and resistive index of the left hepatic artery were unchanged. The increase in flow velocity in the right hepatic artery significantly correlated with that in the common hepatic artery (r = 0.514, p < 0.05). The calculated volume of the embolized right hepatic lobe significantly (p < 0.0001) decreased, from 685 ± 32 cm3 before embolization to 568 ± 28 cm3 after embolization. The atrophy rate of the right hepatic lobe significantly correlated with the increase in flow velocity in the right hepatic artery (r = 0.700, p < 0.0005).

CONCLUSION. Portal vein embolization induces an increase in hepatic arterial blood flow velocity in the embolized hepatic segments, resulting from an increase in common hepatic arterial flow, but not from a steal phenomenon due to decreased hepatic arterial blood flow in the nonembolized hepatic segments. This observation may be explained by the simple mechanical effect of interposing a slower flowing stream (portal flow) in the path of a faster flowing stream (arterial flow).


Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
The liver is the most richly vascularized organ in the body. It constitutes only 2.5% of body weight but receives 25% of the cardiac output. In addition, the liver is a unique organ because of its dual blood supply. The normal liver receives approximately 80% of its blood supply from the portal vein and 20% from the hepatic artery. These two blood sources are structurally and functionally different. Portal blood flow in a healthy individual is determined simply by the net outflow of the extrahepatic splanchnic organs. If portal blood flow is compromised, hepatic arterial blood flow increases to maintain total hepatic blood flow constant [1,2,3,4,5,6]. This arterial compensation has been known to occur after reduction of segmental portal blood flow [7, 8].

Percutaneous transhepatic portal vein embolization (PTPE) has become important in preparation for extensive liver resection [9,10,11,12,13,14,15,16]; it has the potential to prevent liver failure after hepatectomy and, in turn, to increase the safety of liver resection. We previously reported radiologic visualization of an immediate increase in hepatic arterial blood flow in the embolized hepatic segments after PTPE on CT arteriography [17]. However, to our knowledge, no report has clearly documented a quantitative evaluation of the arterial compensation after termination of segmental portal blood flow in humans.

In this study, we prospectively measured hepatic arterial—blood flow velocity using color Doppler sonography to quantitatively assess the time course of changes in hepatic arterial blood flow velocity after PTPE.


Subjects and Methods
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 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
This study involved 21 patients who underwent PTPE as part of their presurgical treatment for a planned extensive liver resection at our institution. The subjects consisted of 13 men and eight women, with a mean age of 63.0 ± 2.2 years (range, 44-78 years). There were 14 patients with hilar cholangiocarcinoma and seven with advanced gallbladder carcinoma. No patient was cirrhotic. Fifteen patients were jaundiced on admission, but neither jaundice nor cholangitis was present at the time of PTPE because the patients had undergone percutaneous transhepatic biliary drainage. Because advanced carcinomas often separate the intrahepatic bile ducts into several units, 11 of the 15 patients received multiple biliary drainage to drain the entire biliary system [18, 19]. Consequently, in our series, the effect of intrahepatic segmental biliary obstruction on lobar blood flow imbalance was negligible. We performed arteriography before PTPE and confirmed a "textbook" distribution of the hepatic artery; the right and left hepatic arteries arose from the proper hepatic artery originating from the common hepatic artery in all patients. We also confirmed no stenosis of the hepatic arteries in all patients. Written informed consent for participation was obtained from each patient before enrollment in the study, which was approved by the human research review committee at our institution.

PTPE was performed 2-3 weeks before liver resection, according to a previously reported method [11, 12, 14, 15]. Briefly, with fluoroscopic control, a 5.5-French triple-lumen balloon catheter was advanced into the target portal vein through a 6-French catheter sheath introduced by sonographically guided puncture of the anterior branch of the right portal vein. We used fibrin glue (Bolheal; Fujisawa Pharmaceutical, Tokyo, Japan) mixed with iodized oil (Lipiodol; Kodama Pharmaceutical, Tokyo, Japan) as the embolic material. The right portal vein was embolized in all patients.

We measured hepatic arterial—blood flow velocity before and 1, 3, 5, 7, and 14 days after PTPE, using a color Doppler sonography instrument (Logic 500 MD; General Electric Yokogawa Medical Systems, Tokyo, Japan) with a convex-array transducer operating at 5.0 MHz in imaging mode and 3.3 MHz in Doppler mode. All measurements were taken with patients fasting overnight, at rest, and during a 5- to 8-sec breath-hold in the supine position. At least two measurements per session were obtained, and the mean value was calculated. The common hepatic artery was examined near the origin arising from the celiac artery with a transverse scan. The right hepatic artery was examined near the bifuraction of the anterior and posterior branches with a right intercostal scan. The left hepatic artery was examined at the level of the umbilical portion of the left portal vein with a transverse scan. Mean flow velocity was automatically calculated with the Doppler unit from the average Doppler spectrum over approximately two cardiac cycles. The angle of incidence of the Doppler sonography beam to all vessels was kept within 60° to minimize intrinsic errors. The resistive index (RI) in each hepatic artery was calculated according to the following formula: RI = (peak systolic velocity — end diastolic velocity) / peak systolic velocity. In addition, the increase in flow velocity in each vessel was defined as the velocity on day 1 after embolization divided by the velocity before embolization.

CT of the liver was used for volume determination before and 14.2 ± 0.7 days after PTPE. CT at 1-cm intervals from the dome to the most inferior part of the liver was performed with enhancement by an IV bolus injection of contrast medium. The volumetric measurement was performed according to a previously reported method [20]. Liver function parameters, such as the serum total bilirubin, aspartate transaminase, and alanine transaminase concentrations, were examined regularly before and after PTPE, with a standard laboratory method.

Results were expressed as means ± standard error. Statistical analysis was performed with the Wilcoxon's signed rank test. Simple linear regression analysis by the least-squares method was also used. A level of p less than 0.05 was considered statistically significant.


Results
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 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
All PTPEs were performed without any complications. Serum aspartate transaminase and alanine transaminase concentrations were elevated slightly after embolization but returned to baseline levels within 1 week. Serum total bilirubin concentrations remained near levels obtained before embolization. Histologic examination of the resected specimens revealed that no infarction due to PTPE developed in the embolized hepatic segments in all patients.

The blood flow velocity in each vessels was successfully measured in all examinations. In all patients the right portal vein remained completely embolized, without recanalization, during the period studied. The flow velocity in the common hepatic artery significantly increased (p < 0.0001), from 50.5 ± 3.4 cm/sec before embolization to 74.8 ± 6.5 cm/sec 1 day after embolization. This increase was followed by a mild decrease, but the velocity remained significantly elevated until day 14 after embolization (Fig. 1). The RI of this artery was unchanged during the period studied (Fig. 2). The flow velocity in the right hepatic artery significantly increased (p < 0.0001), from 34.8 ± 3.7 cm/sec before embolization to 70.4 ± 5.6 cm/sec 1 day after embolization. The velocity decreased 3 days after embolization but remained significantly elevated until day 14 after embolization (Fig. 1). The RI of the right hepatic artery significantly decreased (p < 0.0001), from 0.69 ± 0.01 before embolization to 0.60 ± 0.02 1 day after embolization, and remained decreased until day 14 after embolization (Fig. 2). The flow velocity in the left hepatic artery slightly decreased, from 27.9 ± 2.2 cm/sec before embolization to 23.4 ± 1.8 cm/sec 1 day after embolization, but this change was not statistically significant. The velocity remained constant until day 14 after embolization (Fig. 1). The RI of the left hepatic artery was unchanged during the period studied (Fig. 2).



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  		Fig. 1. —Line graph shows changes in arterial blood flow velocity after portal vein embolization. Values are expressed as mean with standard error (vertical bars). {circ} = common hepatic artery, [UNK] = right hepatic artery, {triangleup} = left hepatic artery, * = p < 0.05, ** = p < 0.01, {dagger} = p < 0.0001 versus value before embolization (by Wilcoxon's signed rank test).

 


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  		Fig. 2. —Line graph shows changes in arterial resistive index after portal vein embolization. Values are expressed as mean with standard error (vertical bars). {circ} = common hepatic artery, [UNK] = right hepatic artery, {triangleup} = left hepatic artery, * = p < 0.05, ** = p < 0.01, {dagger} = p < 0.0001 versus value before embolization (by Wilcoxon's signed rank test).

 

The increase in flow velocity in the right hepatic artery significantly correlated with that in the common hepatic artery (r = 0.514, p < 0.05) (Fig. 3). The calculated volume of the embolized right hepatic lobe significantly decreased (p < 0.0001), from 685 ± 32 cm3 before embolization to 568 ± 28 cm3 after embolization. The atrophy rate of the right hepatic lobe, expressed as (preembolization volume — postembolization volume) / day, significantly correlated with the increase in flow velocity of the right hepatic artery (r = 0.700, p < 0.0005) (Fig. 4). There was no significantly correlation between hepatic functional parameters and the flow velocity change in any vessel.



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  		Fig. 3. —Scatterplot shows correlation between increases in flow velocity in right and common hepatic arteries. Increase in flow velocity was defined as velocity on day 1 after embolization divided by velocity before embolization. y = 0.708 + 1.006x (r = 0.514, p < 0.05).

 


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  		Fig. 4. —Scatterplot shows correlation between atrophy rate of right hepatic lobe and increase in flow velocity in right hepatic artery. Increase in flow velocity was defined as velocity on day 1 after embolization divided by velocity before embolization. y = 0.157 + 3.761x (r = 0.700, p < 0.0005).

 


Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
Doppler sonography has prompted noninvasive and physiologic studies of hepatic hemodynamics. An excellent correlation between Doppler blood flow measurements and the values obtained with electromagnetic flowmetry indicates the accuracy and clinical use of Doppler estimation [21]. Some authors previously reported difficulty in obtaining a Doppler signal from the hepatic artery because of its tortuosity and relatively small caliber [22]. However, recent improvements in Doppler systems have made it possible to visualize the hepatic artery clearly. In this study, a skilled sonographer measured flow velocity with a single modern instrument, minimizing interobserver and interequipment variability [23].

We radiologically showed an immediate increase in hepatic arterial blood flow in the embolized hepatic segments after PTPE [17]. This increase could be explained by two hypotheses. First, total hepatic arterial blood flow might increase, resulting in a constant rate of arterial flow in the nonembolized segments. Second, total hepatic arterial blood flow might remain constant, with the increased arterial flow in the embolized segments attributable to a decrease in flow in the nonembolized segments (steal phenomenon). The current study clearly resolves this issue; the flow velocity in the common and right hepatic arteries increased after right portal vein embolization. The increases in the flow velocity in these two arteries correlated with each other, and the flow velocity in the left hepatic artery was almost constant. These observations strongly support the former of these two hypotheses.

RI is widely used to evaluate arterial vascular resistance [24, 25]. Platt et al. [26] reported a decrease in the hepatic arterial RI in patients with acute portal vein obstruction due to thrombosis. All patients with a hepatic arterial RI of 0.5 or less had acute portal vein obstruction. Our finding that the right hepatic arterial RI significantly decreased after right portal vein embolization is compatible with these prior results.

Several routes exist for communication between the portal vein and the hepatic artery, including transsinusoidal, transvasal, and transplexal routes [27, 28]. At least 30% of the hepatic arterial blood is estimated to be shunted into the portal vein before the arterial blood reaches the sinusoids [29]. Ternberg and Butcher [1] concluded that the relationship between the portal vein and the hepatic artery could be explained as the simple mechanical effect of interposing a slower flowing stream in the path of a faster flowing stream. Specifically, decreasing the amount of slow flow (portal blood flow) is equivalent to the removal of an impedance, and the rate of faster flow (arterial flow) should therefore increase. This theory would predict an immediate decrease in the right hepatic arterial RI followed by an increase in the right hepatic arterial blood flow after right portal vein embolization.

It is well known that portal venous flow, but not hepatic arterial flow, is the major driving force for the development of atrophy and hypertrophy complex of the liver [30, 31]. In a previous study using Doppler sonography, Goto et al. [32] have shown that the hypertrophy rate of the left hepatic lobe after right portal vein embolization closely correlates with the extent of the increase in the portal flow velocity at the umbilical portion. The current study showed that the atrophy rate of the right hepatic lobe after right portal vein embolization significantly correlated with the increase in flow velocity in the right hepatic artery. This observation appears counterintuitive but can be explained by the "stream" theory mentioned previously [1]. The increase in flow velocity in the right hepatic artery is caused by a decrease in the RI. According to the stream theory, the extent of the decrease in the RI is proportional to the extent of the decrease in the amount of right portal blood flow, which acts as an impedance. In other words, the greater right portal blood flow is before embolization, the more the right hepatic arterial flow increases after embolization, and the more the right lobe becomes atrophied.

In conclusion, PTPE induces an increase in hepatic arterial blood flow velocity in the embolized hepatic segments. This change results from an increase in the common hepatic arterial blood flow but not from a steal phenomenon due to a decrease in hepatic arterial blood flow in the nonembolized hepatic segments, although the possibility of a steal occurring in some situations is not completely excluded.


References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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