duplex ultrasonography as a noninvasive technique forassessing portal hemodynamics

Duplex Uitrasonography as a Noninvasive Technique for Assessing Portal Hemodynamics

Claire F. Ozaki, MD, Joseph C. Anderson, MD, Robert P. Ueberman, MD, and Layton F. Rikkers, MD, Omaha, Nebraska

Preservation of portal blood flow is important for maintaining hepatic physiologic characteristics in patients with portal hypertension. When portal flow is diverted by nonselective shunting procedures, hepatic function deteriorates and encephalopathy is frequent. Therefore, recently described operations for variceal hemorrhage have been designed to maintain hepatic portal perfusion. The operation that most consistently achieves this objective is the distal splenorenal shunt described by Warren and colleagues [1]. Sclerotherapy, another commonly used therapeutic option for bleeding esophageal varices, also preserves portal blood flow by obliter- ating varices without altering portal pressure or liver perfusion [2,3].

Measurement of portal blood flow has been ac- complished by several techniques including radio- colloid clearance, indicator dilution, iodized oil (Li- piodol | droplet velocity, and visceral angiography [4-7]. These methods are complex, invasive, and often imprecise. Even angiography, which is the present clinical standard for evaluation of hepatic hemodynamic function, provides only qualitative information regarding portal flow and is also invasive. Recently, duplex ultrasonography (real-time B-scan imaging and pulsed Doppler ultrasonography) has been applied to evaluation of portal hemodynamics [8]. This technique provides quantitative analysis of portal flow and is noninvasive, rela- tively inexpensive, and portable.

Three clinical studies were designed to evaluate duplex ultrasonographic analysis of portal physiologic characteristics. Initially, duplex ultrasonographic measurements of portal flow were compared in control subjects and in patients with portal hypertension. Then, the accuracy of duplex ultrasonography was assessed by comparison with angiography. Finally, patients with portal hypertension

From the Departments of Surgery and Radiology, University of Nebraska Medical Center. Omaha, Nebraska. Supported in part by Public Health Service Grant 5 RO1 DK35168 from the National Institutes of Health, Bethesda, Maryland,

Requests for reprints should be addressed to Claire F. Ozaki, MD, Department of Surgery, University of Nebraska Medical Center, 42nd and Dewey Avenue, Omaha, Nebraska 68105.

Presented at the 28th Annual Meeting of the Society for Surgery of the Alimentary Tract, Chicago, Illinois, May 12 and 13, 1987.

were studied before and after distal splenorenal shunting to determine the effect of this operation on hepatic portal perfusion.

Material and Methods An Advanced Technology Laboratories Mark 500|

pulsed duplex ultrasonographic scanner was used to evaluate portal vein anatomy and Doppler flow parameters. Patients were fasted overnight before the study. Portal vein diameter and the angle between the Dopple r beam and the long axis of the portal vein were measured from a B-scan image showing beam direction with the portal vein in its long axis. An anterior subcostal approach, which provides optimal visualization of the portal vein walls, was used since it allows axial resolution for a more accurate diameter measurement. Portal vein diameter was measured at a location 1 to 2 cm proximal to its bifurcation.

Doppler signals were obtained from a sample volume located at the center of the portal vein. The lateral inter- costal approach used minimized the angle between the long axis of the portal vein and the ultrasonic beam to allow a maximal Doppler shift frequency. Direction of flow was determined by a positive (hepatopetal) or nega- tive (reversed flow) deflection of the Doppler shift frequency tracing. Fast Fourier Doppler frequency spectral analysis of portal flow was printed on translucent film. Then, maximum Doppler frequency was digitized over two cardiac cycles using an Apple II+ | microcomputer and a digitizer pad.

Hemodynamic calculations were performed using the following equations: flow velocity (V) = (Af X c)/(2fo X cos 0) and flow volume (O) = (V • ~ • d2)/4, where c indicates velocity of the ultrasonic beam in soft tissues (154,000 cm/second), fo indicates ultrasonic frequency (3 MHz), Af indicates maximum Doppler shift frequency averaged over two cardiac cycles, d indicates portal vein diameter, and ~ indicates angle of insonation.

Visceral angiography was performed on patients fasted overnight. Portal vein diameter was measured on the venous phase of the selective superior mesenteric anglo- gram at a point 1 to 2 cm proximal to the bifurcation of the portal vein (as by duplex ultrasonography). A 30 percent magnification error was subtracted from the actual measurements. Portal perfusion grade, a qualitative grading system of portal blood flow, was also determined from the

70 The American Journal of Surgery

Duplex Ul t rasonography and Portal Hemodynamics

TABLE I Portal Hemodynamic Variables Measured by Duplex Ultrasonography in Patients With and Without Portal Hypertension (PH) (mean -I- standard error of the mean)

Control PH Group Parameters (n -- 22) (n = 29) p value

Portal vein diameter 9.95 -I- 0.33 10.08 -I- 0.49 NS (mm)

Velocity (cm/s) 18.99 -I- 0.86 6.21 + 1,60 <0.001 Volume (ml/min) 874 -4- 44 450 -I- 86 <0.001

NS = not significant.

venous phase of the superior mesenteric angiogram [9]. Portal perfusion grades were defined as 1, good hepatopetal portal flow with clear visualization of intrahepatic portal branching; 2, fair portal flow with poorly visualized intrahepatic portal branching; 3, opacification of only the main portal vein; and 4, no visualization of the portal vein. When the portal vein was not opacified on superior rues- enteric angiogram, selective hepatic arterial injection was performed. A portal perfusion grade of 5 was defined as portal vein filling after hepatic arterial injection, indicat- ing retrograde flow in the portal vein.

Duplex ultrasonographic portal vein analysis was performed on 29 adult patients with portal hypertension and 22 adult control subjects. Liver disease and portal hypertension were documented by liver biopsy or endoscopic identification of esophageal varices. The portal hypertension group included 16 patients with alcoholic cirrhosis and 13 patients with nonalcoholic liver disease. Duplex ultrasonography was performed before any therapy (shunt or sclerotherapy) for portal hypertension. Control studies were obtained from adult patients with no history of liver disease and normal liver function during abdomi- nal ultrasonography for evaluation of an unrelated problem.

A total of 34 visceral angiograms were performed on 22 patients with portal hypertension, 15 of whom had alcoholic cirrhosis and 7, nonalcoholic cirrhosis. All patients had had at least one documented episode of hemorrhage from esophageal varices. Twelve studies were performed after patients had undergone a portasystemic shunt pro- cedure (a distal splenorenal shunt in 10 and an interposi- tion shunt in 2). Duplex ultrasonography was performed within 3 days of angiography.

Ten patients with portal hypertension (seven with alcoholic cirrhosis and three with nonalcoholic cirrhosis) were evaluated by duplex ultrasonography before and after distal splenorenal shunting. Preoperative portal flow studies were obtained within 1 month of operation. Du- plex ultrasonography was repeated in the early postoperative period i to 3 months after distal splenorenal shunt in all 10 patients and 1 year after operation in 5 patients.

Significant differences between the portal hypertension and control groups were determined by the Student's unpaired t test. The extent of concordance between duplex ultrasonography and angiography was assessed by

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linear regression and Pearson's correlation coefficient. Differences between preoperative and postoperative studies were analyzed by the Student's paired t test.

Resul ts

Portal vein diameter, flow velocity, and volume were compared in the control and portal hyperten- sive groups (Table I, Figure 1). No differences were noted in portal vein diameter between the two groups. In contrast, mean flow velocity and volume were significantly decreased in patients with portal hypertension compared with control subjects. A wide range of flow velocities was recorded in each group, with considerable overlap of the groups. However, 18 patients with portal hypertension (62 percent) had portal flow velocities less than 500 ml/min, the lowest portal flow velocity in the control group. Five patients with portal hypertension (17 percent) had spontaneous reversal of portal blood flow. Portal flow was not significantly different in patients with nonalcoholic cirrhosis (484 • 147 ml/min) and patients with alcoholic cirrhosis (423 • 104 ml/min; p value not significant) (Table I).

Portal vein diameters measured by duplex ultrasonography (10.44 • 0.40 ram) and by angiography (10.25 • 0.39 ram) were closely related (correlation coefficient 0.53, p <0.005) (Figure 2). Both portal flow velocity and volume by duplex ultrasonography correlated inversely with angiographic portal perfusion grade and duplex ultrasonography was 100 percent accurate in detecting reversed (hepatofugal) portal flow (Table II, Figure 3).

No significant changes in portal vein diameter were detected in the 10 patients studied with duplex ultrasonography before and after distal splenorenal shunt (Table III). However, a greater than 50 per-

Volume 155, January 1988 71

Ozaki et al

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cent decrease in mean portal flow velocity and volume was noted by duplex ultrasonography after distal splenorenal shunt and reversal of portal blood flow occurred in two patients in the early postoperative period (Table III, Figure 4). In contrast, preoperative and postoperative angiographic portal perfusion grades, which were available for 9 of the 10 patients, revealed no significant alteration in portal flow (preoperative value 2.11 • 0.78 and postoperative value 2.67 • 1.22; p value not significant). Two of the three patients with nonalcoholic liver disease maintained portal perfusion postoperatively. The third patient had partial portal vein thrombosis preoperatively which progressed to complete occlu- sion after distal splenorenal shunting.

Five of these patients were restudied 1 year after operation and four of the five, all with alcoholic cirrhosis, were noted to have hepatofugal portal flow. Two of these patients had had hepatopetal flow on the early postoperative study. Portal vein diameter significantly decreased at 1 year (7.80 • 0.73 mm) compared with preoperative diameter (11.13 • 0.62 mm, p <0.01).

Comments Although duplex ultrasonography has been pur-

ported to be an accurate technique for measurement of portal blood flow, its validity has not been documented in clinical studies [8]. Animal investigations have shown that duplex ultrasonographic portal flow values are similar to those obtained by electro-

TABLE II Comparison of Angiographic Portal Perfusion Grade (PPG), Portal Flow Velocity, and Volume Measured by Duplex Ultrasonography

PPG Velocity (cm/s) Volume (ml/min)

1 (n = 6) 12.65 4- 1.96 887 4- 237 2(n = 11) 8.14 4- 0.94 475 4-71 3 (n = 9) 7.51 -I- 1.16 335 -I- 87 4 (n = 2) 2.55 4- 2.55 205 4- 205 5 (n = 4) --12.85 4- 2.10 - 487 4- 106

magnetic flowmeter and by transit time ultrasonic blood flowmetry [10,11]. The only clinical study comparing duplex ultrasonography with another blood flow measurement technique utilized iodized oil droplet velocity [12]. No study has yet objective- ly compared visceral angiography (the present clinical standard for assessing portal hemodynamics) to duplex ultrasonography.

A major objective of the present investigation was to compare quantitative estimation of portal blood flow by duplex ultrasonography to qualitative grading of flow by angiography. Since portal vein diameter is a key variable in calculating duplex ultrasonographic flow, measurements of this parameter by ultrasonography and angiography were also compared. Although mean portal vein diameter was similar using the two techniques, significant varia- tion, probably due to errors inherent in both methods, occurred (Figure 2). Accurate measurement of diameter by duplex ultrasonography is dependent on the angle of insonation, which should be as close to 90 degrees as possible, and angiographic estimation of portal vein diameter is complicated by a variable magnification error [13].

A highly significant inverse relationship was noted when duplex ultrasonographic flow was compared with angiographic portal perfusion grade. Du- plex ultrasound flows varied over a wide range within each portal perfusion grade, but closer correlation may be difficult to achieve since portal perfusion grading is itself qualitative and imprecise. Di- rection of portal flow was always accurately assessed by duplex ultrasonography. Therefore, duplex ultrasonography appears to be at least as accurate as angiography and is an acceptable alternative for the longitudinal assessment of portal blood flow clini- cally.

Although duplex ultrasonographic and anglographic assessments of portal flow were highly correlated, the quantitative accuracy of duplex ultrasonography has not been confirmed by this study. There are many potential errors inherent in the duplex ultrasound technique [13]. First, vessel area is calculated from its diameter and assumes that the vessel is circular, which may not always be the case


Duplex Ultrasonography and Portal Hemodynamics

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Figure 3; Comparison of anglographic portal perfuslon grade and portal blood flow volume measured by duplex ultrasonography (correlation coefficient 0.75, p <0.001).

[14]. Second, several methods, none of which are accurate in all situations, can be used to determine flow [13]. The technique used in the present study assumes the velocity profile within the portal vein to be flat, that is, the velocity is the same at any point within the vessel lumen (plug flow). Although this is the simplest method, the actual velocity profile in most vessels probably falls somewhere between the flat profile and the classic parabolic profile. In addition, since actual velocity profile is dynamic, none of these methods will always be accurate [6]. Finally, the accuracy of many aspects Of the duplex ultrasound technique, such as measurement of portal vein diameter and the angle of insonation, depend to a large degree on the person performing the study.

It is likely that error is minimized when duplex ultrasound stUdies are performed in a standardized method by the same ultrasonographer using the same equipment. Such an approach may result in consistency of error which allows meaningful comparison of data among patients within the same institution and especially serial determinations in the same patient, even though the absolute values may not be quantitatively accurate. A standardized method was used in the present study to estimate portal flow in patients with and without portal hy= pertension, Significant differences in portal blood flow were demonstrated between both the portal hypertension and the control groups. Although there was considerable overlap of the two groups,

TABLE III Porta l H e m o d y n a m i c V a r i a b l e s B e f o r e and Af te r Dista l S p l e n o r e n a l Shunt on D u p l e x U l t r a s o n o g r a p h y

Parameters

Time Period Early

Preop Postop p value

Portal vein diameter (mm)

Velocity (cm/s) Volume (ml/min)

11.13 -4- 0.63 10.33 4- 0.55 NS

9.79 4- 1.35 4.89 4- 1.31 <0.002 643 4- 152 247 4- 68 <0.02

NS -- not significant.

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only patients with portal hypertension had portal flows of less than 500 ml/min. Despite differences in technique and duplex ultrasound equipment among institutions; portal flow analysis has yielded similar results. Mean portal flow volume in control popula- tions has been reported as 952 • 273 ml/min and 889 • 284 ml/min compared with 874 • 207 ml/min in the present investigation (values expressed as mean • standard deviation) [10,15].

Another important finding in this study is that portal flow decreased by more than 50 percent in the early postoperative interval after the distal splenorenal shunt. Although the absolute quantitative ac: curacy of duplex ultrasonography can be ques- tioned, as previously discussed, serial determina- t ions in the same p a t i e n t by the same ultrasonographer should provide consistency of error, making this relative change in flow a meaningful observation. Most distal splenorenal shunt series


Ozaki et al

have reported preservation of hepatic portal perfusion on early postoperative angiography in 80 percent to 90 percent of patients [2,3,16]. Studies in which angiographic flow was qualitatively graded revealed similar preoperative and postoperative portal perfusion grades [3,16].

Although only one of five patients evaluated at 1 year had evidence of prograde portal flow in this series, the late postoperative Study group is biased by inclusion of the only two patients who had reversal of flow on the early postoperative duplex ultrasound study. Distal splenorenal shunt series utilizing angiographic assessment of portal flow have shown preservation of hepatic portal perfusion in approximately 50 percent of patients at 1 year after operation [2,3].

Summary Duplex Ultrasonography was evaluated as a non-

invasive, quantitative technique of assessing portal hemodynamic characteristics. Portal blood flow measured by duplex ultrasonography was significantly decreased in patients with portal hypertension (450 • 86 ml/min) compared with control subjects (874 4- 44 ml/min; p <0.001). Quantitative assessment of portal blood flow by duplex ultrasound correlated with qualitative portal perfusion grading by angiography, and direction of flow was always accurately determined by duplex ultrasonography. Although the angiographic portal perfusion grade did not change significantly in the early postoperative period after distal splenorenal shunting, a decrease in mean portal blood flow of more than 50 percent was documented by duplex ultrasonography. Duplex ultrasonography appears to be at least as accurate as angiography and is an acceptable alternative to this more invasive technique for the longitudinal assessment of portal blood flow.

References 1. Warren WD, Salam AA, Hutson D, Zeppa R. Selective dista!

splenorenal shunt: technique and results of operation. Arch Surg 1974; 108: 306-14.

2. Warren WD, Henderson JM, Millikan WJ, et al. Distal splenorenal shunt versus endoscopic sc!erotherapy for long-term management of variceal bleeding. Ann Surg 1986; 203: 454-62.

3. Rikker s LF, Burnett DA, Volentine GD, Buchi KN, Cormier HA. Shunt surgery versus endoscop!c sclerotherapy for long- term treatment of vai'iceal bleeding: early results of a randomize d trial. Ann Surg 1987; 206: 261-9.

4. Rikkers LF, Miller F, Nelson JA, Christian P, Coleman RE. Radiocol!oid estimation of hepatic portal perfusion. J Surg Res 1980; 29: 293-301.

5. Huet PM, Lavoie P, Viallet A. Simultaneous estimation of hepatic and portal blood flows by an indicator dilution technique. J Lab Clin Med 1973; 82: 836-46.

6. Sovak M, Soulen RL, Reichle FA. Blood flow in th e human portal vein: a cineradiographic method using particulate contrast medium. Radiology 1971; 99: 531-6.

7. Viamonte M Jr, Warren WD, Fomon JJ, Martinez LO. Angio-

graphic investigations in portal hypertension. Surg Gynecol Obstet 1970; 130: 37-53.

8. Gill RW. Pulsed doppler with B-mode imaging for quantitative blood flow measUrement. Ultrasound Med Biol 1979; 5: 223-5.

9. Nordlinger BM, Nordlinger DF, Fulenwider JT, et aL Angiogra- phy in portal hypertension: clinical significance in surgery. Am J Surg 1980; 139: 132-41.

10. Moriyasu F, Ban N, Nishida O, et al. Clinical application of an ultrasonic duplex system in the quantitative measurement of portal blood flow. J Clin Ultrasound 1986; 14: 579-88.

11. Ohnishi K, Sait0 M, Sato S, et al. Portal hemodynamics in idiopathic portal hypertension (Banti's syndrome): comparison with chronic persistent hepatitis and normal subjects. Gastroenterology 1987; 92: 751-8.

12. Ohnishi K, Saito M, Koen H, Nakayama T, Nomura F, Okuda K. Pulsed Doppler flow a s a criterion of portal venous velocity: comparison with cineangiograPhic measurementS. Radiol- ogy 1985; 154: 495-8.

13. Gill RW. Measurement of blood flow by ultrasound: accuracy and sources of error. Ultrasound Med BioI 1985; 11: 625- 41.

14. Ackroyd N, Gill R, Griffiths K, Kossoff G, Reeve T. Duplex scanning of the portal vein and portasystemic shunts. Sur- gery 1986; 99: 591-7.

15. Burns P, Taylor K, Blei AT. Doppler flowmetry and portal hypertension (editorial). Gastroenterology 1987; 92: 824- 6.

16. Rikkers LF, Miller FJ, Christian P. Effect of portasYstemic shunt operations on hepatic portal perfusion. Am J Surg 1982; 141: 166-74.

Discussion I. James Sarfeh (Irvine, CA): Dr. Ozaki, we have also

had some preliminary experience with the duplex scanner. Based on our observations, I have two questions for you. I am astounded by the remarkably different results obtained when the angle of resonance is even slightly altered. Have you gone to the laboratory to determine if this problem can be resolved by standardizing the methods? You have reported that the mea n portal vein diameter is approximately 10 mm. Our own previous studies, as well as those of Nordlinger, have found the mean portal vein diameter in patient s with portal hypertension to be almost twice the size yo u reported. Since this measurement is critical to the derivation of portal flow and volume, it is important that we understand the differences between Your data and ours. if methods can be standard = ized, duplex scanning may well become a state Of the art approach to delineating portalhemodynamic characteristics.

Carlos A. Pellegrini (San Francisco, CA): Dr. Ozaki, you compared duplex ultrasonographic measurements with angiographic determination. I do not think the angiogram is an accurate enough method to determine direction O f portal blood flow; I wonder about your choice of this method. I was surprised to see that you compared the more accurate method to the less accurate one. You also showed that there was a reversal Of portal blood flow after the dista ! splenorenal shunt in a number of patients. Can you speculate as to why this happened in these patients? Are these patients experiencing conversion to a functional side-to-side portacaval shunt?


Duplex Ultrasonography and Portal Hemodynamics

Josef Fischer (Cincinnati, OH): This is an interesting technique, because it is noninvasive, and I think with proper refinement it can be very accurate. My prejudice is that quality as well as quantity of portal flow may be importantl that is, where the blood comes from. One of the issues is what happens to pancreatic blood with its possible trophic effect? Dr. Ozaki, do you think that this par- ticular technique can be modified to predict not only quantity but the direction of the flow from certain compo- nents of the portal circulation? Such measurements may explain some of the discrepancies of hepatic failure after different types of shunts, although your data about drop off in portal flow is probably quite correct.

Claire F, Ozaki, (closing): Dr. Sarfeh, we have performed some preliminary experiments utilizing a phan- tom model that simulates a vessel in soft tissue. We have found some discrepancy in the values obtained when the angle of insonation is altered. The smallest angle appears to provide the most accurate data. Therefore, in performing these studies we try to utilize the smallest possible angle of insonation. We have also begun experiments in a porcine model to further verify the accuracy of this technique. Regarding portal vein diameter , we measure it distally rather than near the superior mesenteric and splenic vein junction. We have found that the distal porta ! vein is approximately 25 percent smaller than the proximal portal vein. When the magnification error of 30 per-

cent is subtracted to allow Comparison of the angiographic measurement to duplex ultrasonography, the average diameter was approximately 10 mm.

Dr. Pellegrini, we compared duple x ultrasonography to angiography because angiography is the method most commonly used to evaluate portal perfusion in the clinical setting. In our late postoperative evaluations, we did see a number of patients with reversal of portal flow. Long- term preservation of portal flow is dependent on two elements: the degree Of separation of the gastrosplenic and portal and mesenteric venous circulations at operation and the cause of the liver disease. Although we performed complete collateral ligation, splenopancreatic dis- connection, as described by Dr. Warren and associates, was not carried out. In addition, patients with alcoholic cirrhosis are more likely to lose portal blood flow after distal splenorenal shunting, and Our study group had a large proportion of patients with alcoholic cirrhosis. Only five patients were studied in the late postoperative period, so the small size of this study group precludes any meaningful interpretation regarding long-term preservation of portal flow after the distal splenorenal shunt.

Dr. Fischer, most of the veins draining into the portal system are not well visualized by duplex ultrasonography. The reason portal vein diameter is measured distally is that the liver provides an excellent window for visualization of the portal vein. The proximal portal vein is often obscured by air within the bowel.


duplex ultrasonography as a noninvasive technique forassessing portal hemodynamics

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