Clinical Utility of Pulsed Doppler in the Detection of Arterioportal Shunting in Patients with Hepatocellular Carcinoma Zu-Yau Lin, MD, Wen-Yu Chang, MD, MS, Liang-Yen Wang; MD, Wang-Pin Su, MD, Sheng-Nan Lu, MD, MPH, Shinn; Cherng Chen, MD, MS, Wan-Long Chuang, MD, MS, Ming-Yuh Hsieh, MD, Jung-Fa Tsai, MD, D, MedSci
Ninety-seven patients with hepatocellular carcinoma had duplex scanning from the patent or residual portal lumen and comparative angiography. Duplex ·ultrasonography identified five of nine patients with angiographic evidence of arterioportal shunting. Furthermore, Doppler results indicated the presence of the shunt in one patient without angiographic evidence. Duplex scanning from the portal lumen may be useful
A
in the detection of arterioportal shunting. This procedure can be used to evaluate the hemodynamic change of the recipient portal vein under natural physiologic conditions. However, small shunts without hepatofugal portal blood cannot be detected by this procedure. KEY WORDS: Hepatocellular carcinoma; Arterioportal shunting; Ultrasound, Doppler studies.
rterioportal (AP) shunting can occur under a variety of circumstances, and the usual malignant cause of this shunting is hepatocellular carcinoma (HCC). HI, AP shunting in patients with HCC is a cause not only of intrahepatic spread of cancer cells4 but also of portal hypertension .1•8 Preoperative assessment of the portal venous system in patients with HCC is mandatory because large AP shunts are a contraindication to tumor resection.9.1° Furthermore, variceal hemorrhage in patients with HCC and hyperkinetic portal hypertension secondary to AP shunting may be readily and safely controlled by occlusion of the shunting artery.'·8 Therefore, detection of an AP shunt in patients with HCC is of clinical importance. Angiography 4 and dynamic computed tomography 11 are usually used to detect AP shunts. However, both modalities are expensive and angiography also is in-
vasive. Duplex pulsed Doppler ultrasonography is an inexpensive and noninvasive modality that can detect blood flow from small targets in the liver. Several reports have shown that pulsed Doppler ultrasonography could be used to detect AP shunting. 12- 18 The diagnostic criteria for AP shunting from these reports were based mainly on the high-frequency systolic Doppler shifts around the periphery of the tumor, 14 ~ 17 but this diagnostic criterion did not reflect the hemodynamic change in the recipient portal lumen. Only a few reports from a few patients revealed unusual Doppler signals from the portal lumen.1M 3.t 3 The purpose of this prospective study was to investigate the clinical utility of duplex pulsed Doppler ultrasonography in the detection of AP shunting from the portal lumen in patients with HCC.
Received July 23, 1991, from the Department of Internal Medicine, Kaohsiung Medical College Hospital, Taiwan, Republic of China. Revised manuscript accepted for publication January 8, 1992. Address correspondence and reprint requests to Zu·Yau Lin, MD, Department of Internal Medicine.• Kaohsiung Medical College Hos· pita!, No. 100 Shih~Chuan 1st Road, Kaohsiung City 807, Taiwan, ROC.
MATERIALS AND METHODS From August 1989 to May 1990, 97 patients (80 men, 17 women) with HCC seen at our institution underwent duplex pulsed Doppler scanning of the portal
@ 1992 by the American Institute of Ultrasound in Medicine• JUltrasound Med 11 :269- 273, 1992 • 0278-4297/ 92/ $3.50
270
DETECTION OF ARTERIOPORT AL SHUNTING
venous system and comparative angiography. The patients ranged in age from 24 to 80 years. The diagnosis of HCC was made by sonographically guided percu· taneous aspiration cytology or biopsy plus at least one positive result with angiography or a serum alphafetoprotein level of greater than 400 ng/ml. Classification of the type of HCC (diffuse or massive) and the diagnosis of portal venous thrombosis were made by B,mode real-time ultrasonography. 1• .20 Comparative celiac or hepatic arteriography and arterial portography were performed within 2 weeks after Doppler examination. Doppler examination was performed with a 3.75 MHz sector scanner combined with a duplex pulsedwave Doppler system (SSA toOA, Toshiba, Tokyo, japan). The wall filter was set at 100 Hz, and the pulse repetition frequency was 4 KHz. The Doppler gain (set at 2 to 4) and the echo level (set at 6 to 8), which were used to alter the strength of the Doppler signals from the display of the spectral profile, were at their optimum settings to obtain clear outline of flow waves with a minimum of background noise. The depth of the measurement was limited to less than 10 cm to prevent interference by signals of unrelated vessels adjacent to the portal vein because the sonographic beam diverges the farther it is from the transducer.21 All patients were examined in the supine or left decubitus position. The portal venous system was ex; amined regularly from main trunk, left transverse, and umbilical portions to right anterior and posterior branches. B~mode real-time sector imaging was used first to detect any thrombus within the lumen. The Doppler cursor was then manipulated under B-mode real-time sonographic guidance within the lumen (in vessels without thrombus) or within the residual lumen (in partially thrombotic portal veins) to detect the waveform and the direction of the portal blood flow. The sample width was set to encompass the whole patent lumen with care taken not to exceed the margin of the lumen being studied to exclude the possibility of picking up Doppler signals transmitted from adjacent unrelated vessels. The probe was manipulated from every possible direction to obtain Doppler signals from the smallest angle between the Doppler beam and the vessels being studied. Any tubular structure adjacent to the portal vein was also examined to exclude the possibility of interference from adjacent vessels unrelated to the portal vessel. Celiac or hepatic arteriography was performed by the conventional Seldinger technique. The catheter was placed in the common or preferably proper hepatic artery and 40 to 55 ml of 65% meglumine diatrizoate was injected within 5 sec by the automatic injector. For arterial portography, 40 to 45 ml of the contrast medium was injected into the superior mesenteric artery.
J Ultrasound Med 11:269-273, 1992
RESULTS Twenty-one patients were found to have portal venous thrombosis on B-mode real-time ultrasonography. Seven of them demonstrated AP shunting on arteriography (two cases), duplex scanning (one case), or both (four cases). AP shunting was also shown by arteriography and duplex scanning in three patients without evidence of portal venous thrombosis on B· mode real-time ultrasonography (two by arteriography and one by both arteriography and duplex scanning). None of these three patients had a history of hepatic trauma, operation, or biopsy. The results of duplex scanning from nine patients with AP shunting on arteriography (one diffuse and eight massive HCC) were as follows: four patients demonstrated unidirectional or bidirectional pulsatile waves from the patent lumen near the site of the shunt (Fig. 1), one other patient revealed pulsatile waves from the whole length of the patent left portal venous branch (Fig. 2), and the other four patients did not demonstrate any unusual Doppler signals from the patent lumen. One patient with massive HCC demonstrated left portal venous thrombosis on B-mode real-time ultrasonography but did not have evidence of AP shunting on arteriography. Duplex scanning of this patient demonstrated continuous waves of hepatofugal direction from the residual lumen of the left portal vein, and high-frequency systolic Doppler shifts (>3.5 KHz) from the adjacent hepatic artery (Fig. 3). The Doppler results indicated the presence of AP shunting.
DISCUSSION Detection of AP shunting by Doppler ultrasonography
is based mainly on the high-frequency systolic Doppler
shifts (>3 KHz), which is produced by a large pressure gradient between the artery and the recipient vein15.22 around the periphery of the tumor. 14 - 17 Although Doppler examination using this criterion appears to be more sensitive than angiography in the detection of AP shunts, 1' it cannot be used to assess the hemodynamic change in the portal vein lumen. Detection of an AP shunt by Doppler ultrasonography without simultaneously determining the hemodynamic change in the recipient portal vein lumen will limit the clinical utility of this information. Patients with HCC and AP shunting are particularly likely to bleed from esophagogastric varices.7 Although the simultaneous presence of cirrhosis, portal hypertension, and a portal vein thrombus represents a relative contraindication to hepatic arterial embolization;?:! variceal hemorrhage in patients with HCC complicated by hepatofugal portal blood flow
JUltrasound Med 11:269- 273, 1992
A
LIN ET AL 271
A
B
B Figure 2 Arterioportal shunting in patient with he patocellular carcinoma. A, Doppler scanning demonstrates pulsatile waves from the whole length of the left portal venous branch .. B, Celiac arteriography demonstrates arterioportal shunting (arrcw).
c Figure 1 Hepatocellular carcinoma with right portal venous thrombosis. A, Doppler scanning demonstrates bidirectional pulsatile waves from the patent lumen near the right portal venous thrombus. B, When the Doppler cursor (arrowheads) is moved away from the thrombotic segment, the pulsatile waves change to the portal continuous waves. C, Celiac arteriography demonstrates arterioportal shunting (arrow).
due to a large AP shunt may be safely controlled by a highly selective therapeutic occlusion of the shunting artery. 8 Furthermore, understanding the probable point
of shunting and the hemodynamics of the recipient portal vein may be used to predict the possible areas of dissemination of cancer cells. Hepatofugal portal blood flow from AP shunting in patients with HCC may have allowed dissemination of cancer cells in the splanchnic area. Hepatic resection in this situation may be meaningless. Therefore, Doppler scanning from the portal lumen is mandatory for the clinical detection of AP shunts by Doppler ultrasonography. Changes in the Doppler signals and in the hemody· namics in the recipient portal vein lumen in patients with AP shunting have been discussed by some au· thors. 12""'13. 18 However, these reports did not apply Dop· pier ultrasonography in a large series of patients to evaluate its clinical utility in the detection of AP shunting from the portal lumen. In the present study, nine of 97 patients demonstrated AP shunting on arteriog-
272
DETECTION OF ARTERIOPORTAL SHUNTING
A
8
c Figure 3 Hepatocellular carcinoma with left portal venous
thrombosis. A, Doppler scanning demonstrates continuous waves of hepatofugal direction from the residual lumen of the left portal vein (arrow). B, Doppler scanning from the adjacent hepatic artery demonstrates high-frequency systolic Doppler shifts (greater than 3.5 KHz) (arrowl1eads). C, There is no evidence of arterioportal shunting on hepatic arteriography.
J Ultrasound Med 11:269- 273, 1992
raphy. Duplex scanning from the patent portal lumen correctly identified five of these nine patients. Among them, only one patient could demonstrate pulsatile waves along the entire length of the left portal branch. In the other four patients pulsatile waves were found only at the site near the shunting. The reason for the difference in Doppler results may be the differing amounts of blood flowing through the shunt. A small volume of arterial blood flowing through the shunt may be able to change the portal continuous waves to pulsatile waves at the site near the shunt. However, it is unable to maintain its pulsatile character at sites away from the shunt because relatively large volumes of confluent portal blood flow reduce the ability to produce pulsatile waves. A large volume of arterial blood flowing through the shunt may overcome the portal blood flow and may even produce retrograde hepatofugal flow in the portal venous system. 8 There· fore, increasing the volume of blood flowing through the shunt can produce detectable pulsatile waves from the recipient portal lumen father away from the shunt area. However, the angiographic features of AP shunting in these five patients were similar. The inconsistency between Doppler and angiographic results may be due to the different procedures employed for these two examinations. Celiac or hepatic arteriography requires injection of contrast material, which is usually performed by an automatic injector over a few seconds and, therefore, leads to a high injection pressure in the artery. Consequently, the results obtained by this procedure do not reflect the patient's natural physiologic condition. 4•18 Duplex scanning, however, does not require the use of contrast material or special preparation of the patient. Thus, the Doppler results reflect the natural physiologic condition. Four patients with angiographic evidence of AP shunting did not demonstrate unusual Doppler signals from the patent portal lumen. The finding of only a small amount of contrast medium in the recipient portal vein on angiography in these patients indicated that a small volume of blood was flowing through the shunt. Duplex scanning failed to detect these shunts because pulsatile character of a low volume of arterial blood cannot be expressed when there is a relatively large volume of portal blood flow. One patient without angiographic evidence of AP shunting had unusual Doppler results that indicated the existence of the shunt. The continuous rather than pulsatile waves from the residual lumen, as seen in this patient, may result from a low rate of blood flow through the shunt, which could not be identified by arteriography; therefore, the pulsatile character was not obvious. Blood flow was hepatofugal because of the total occlusion of the distal portion of the left portal venous branch by the tumor thrombus. In 14 of 21 patients in the present study who had
J Ultrasound Med 11 :269- 273, 1992
portal venous thrombosis on B-mode real-time ultrasonography, AP shunting was not found on arteriography or duplex scanning. Although very small AP shunts may be missed by both arteriography 15 and duplex scanning, our findings indicated that patients with portal venous thrombosis did not necessarily have obvious AP shunting. On the other hand, three patients in the present study without evidence of portal venous thrombosis on B-mode real-time ultrasonography also demonstrated AP shunting on arteriography and duplex scanning. These patients did not undergo hepatic resection or autopsy and, therefore, the real mechanism of shunt formation could not be determined. However, this result indicated that existence of an AP shunt could not be excluded in patients without portal venous thrombosis on B-mode real-time ultrasonography. All patients with HCC should be examined carefully to rule out AP shunting. Recent technological developments in Doppler color flow imaging have made it possible to investigate the vascular stenosis, occlusion, and flow disturbance easily and rapidly.24 Theoretically Doppler color flow imaging will be much easier than duplex ultrasonography in detecting and evaluating the severity of AP shunting. The clinical utility of Doppler color flow imaging for detecting AP shunts remains to be evaluated in a large series of patients with HCC. From the foregoing results, we conclude that duplex scanning from the patent or residual lumen of the portal venous system may be useful in the detection of AP shunting in patients with HCC. This procedure also can indicate hemodynamic changes in the recipient portal venous system. However, small shunts without hepatofugal portal blood flow cannot be detected by this procedure. Simultaneous Doppler scanning from the periphery of the tumor and the tubular structures around the portal venous system may compensate for this limitation.
REFERENCES 1. Van Way CW, Crane JM, Ridell DH, et al: Arteriovenous fistula in the portal circulation. Surgery 70:876, 1971 2. ltzchak Y, Adar R, Bogokowski H, et al: lntrahepatic arterial portal communications: Angiographic study. AJR 121:384, 1974 3. Rabinowitz JG, Kinkabwala M, Ulreich S: Macro-regenerating nodule in the cirrhotic liver. AJR 121:401, 1974 4. Okuda K, Musha H, Yamasaki T, et al: Angiographic demonstration of intrahepatk arterio-portal anastomoses in hepatocellular carcinoma. Radiology 122:53, 1977 5. Okuda K, Musha H, Nakajima Y, et al: Frequency of intrahepatic arteriovenous fistula as a sequela to percutaneous needle puncture of the liver. Gastroenterology 74:1204, 1978
LIN ET AL
273
6. Bookstein JJ, Cho KJ, Davis GB, et al: Arterioportal communications: Observations and hypotheses concerning transsinusoidal and transvasal types. Radiology 142:581, 1982 7. Nagasue N, Inokuchi K, Kobayashi M, et al: Hepatoportal arteriovenous fistula in primary carcinoma of the liver. Surg Gynecol Obstet 145:504, 1977 8. Morse SS, Sniderman KW, Galloway S, et al: Hepatoma, arterioportal shunting, and hyperkinetic portal hypertension: Therapeutic embolization. Radiology 155:77, 1985 9. Gammill SL, Takahashi M, Kawanarni M, et al: Hepatic angiography in the selection of patients with hepatoma for hepatic lobectomy. Radiology 101:549, 1971 10. Marks WM, Jacobs RP, Goodman PC, et al: Hepatocellular carcinoma: Clinical and angiographic findings and predictability for surgical resection. AJR 132:7, 1979 11. Nakayama T, Hiyama Y, Ohnishi K, et al: Arterioportal shunts on dynamic computed tomography. AJR 140:953, 1983 12. Lafortune M, Breton G, Charlebois S: Arterioportal fistula demonstrated by pulsed Doppler ultrasonography. J Ultrasound Med 5:105, 1986 13. Ohnishi K, Saito M, Sata S, et al: Clinical utility of pulsed Doppler flowmetry in patients with portal hypertension. Am J Gastroenterol 81:1, 1986 14. Taylor KJW, Ramos I, Morse SS, et al: Focal liver masses: Differential diagnosis with pulsed Doppler US. Radiology 164:643, 1987 15. Taylor KJW, Ramos I, Carter D, et al: Correlation of Doppler US tumor signals with neovascular morphologic features. Radiology 166:57, 1988 16. Yasuhara K, Kimura K, Ohto M, et al: Pulsed Doppler in the diagnosis of small liver tumours. Br J Radio) 61:898, 1988 17. Ohnishi K, Nomura F: Ultrasonic Doppler studies of hepatocellular carcinoma and comparison with other he· patic focal lesions. Gastroenterology 97:1489, 1989 18. Lafortune M, Patriquin H, Bums P: Doppler ultrasound in the evaluation of portal and splanchnic blood flow. Ill Ferrucci JT, Mathieu DG (eds): Advances in Hepatobiliary Radiology. St. Louis, CV Mosby, 1990, p 29 19. Ohto M, Ebara M, Okuda K: Ultrasonography in the diagnosis of hepatic tumor. 111 Okuda K, Ishak KG (eds); Neoplasms of the Liver. Tokyo, Springer-Verlag, 1987, p 251 20. Gansbeke DV, Avni EF, Delcour C, et al: Sonographic features of portal vein thrombosis. AJR 144:749, 1985 21. Kisslo J, Mark DB, Adams D: Pulsed and continuous wave Doppler. In Kisslo J, Adams D, Mark DB (eds): Basic Doppler Echocardiography. New York, Churchill Livingstone, 1986, p 25 22. Bums PN, Gowland MR, Rimmer S: Use of Doppler ultrasound in the detection of changes in the blood flow in tumour circulation in the rabbit. J Physiol 342: 12, 1983 23. Chamsangavej C, Chuang VP, Wallace S, et al: Work in progress: Transcatheter management of primary card· noma of the liver. Radiology 147:51, 1983 24. Merritt CRB: Doppler color flow imaging. J Clin Ultra~ sound 15:591, 1987
Ninety-seven patients with hepatocellular carcinoma had duplex scanning from the patent or residual portal lumen and comparative angiography. Duplex ·ultrasonography identified five of nine patients with angiographic evidence of arterioportal shunting. Furthermore, Doppler results indicated the presence of the shunt in one patient without angiographic evidence. Duplex scanning from the portal lumen may be useful
A
in the detection of arterioportal shunting. This procedure can be used to evaluate the hemodynamic change of the recipient portal vein under natural physiologic conditions. However, small shunts without hepatofugal portal blood cannot be detected by this procedure. KEY WORDS: Hepatocellular carcinoma; Arterioportal shunting; Ultrasound, Doppler studies.
rterioportal (AP) shunting can occur under a variety of circumstances, and the usual malignant cause of this shunting is hepatocellular carcinoma (HCC). HI, AP shunting in patients with HCC is a cause not only of intrahepatic spread of cancer cells4 but also of portal hypertension .1•8 Preoperative assessment of the portal venous system in patients with HCC is mandatory because large AP shunts are a contraindication to tumor resection.9.1° Furthermore, variceal hemorrhage in patients with HCC and hyperkinetic portal hypertension secondary to AP shunting may be readily and safely controlled by occlusion of the shunting artery.'·8 Therefore, detection of an AP shunt in patients with HCC is of clinical importance. Angiography 4 and dynamic computed tomography 11 are usually used to detect AP shunts. However, both modalities are expensive and angiography also is in-
vasive. Duplex pulsed Doppler ultrasonography is an inexpensive and noninvasive modality that can detect blood flow from small targets in the liver. Several reports have shown that pulsed Doppler ultrasonography could be used to detect AP shunting. 12- 18 The diagnostic criteria for AP shunting from these reports were based mainly on the high-frequency systolic Doppler shifts around the periphery of the tumor, 14 ~ 17 but this diagnostic criterion did not reflect the hemodynamic change in the recipient portal lumen. Only a few reports from a few patients revealed unusual Doppler signals from the portal lumen.1M 3.t 3 The purpose of this prospective study was to investigate the clinical utility of duplex pulsed Doppler ultrasonography in the detection of AP shunting from the portal lumen in patients with HCC.
Received July 23, 1991, from the Department of Internal Medicine, Kaohsiung Medical College Hospital, Taiwan, Republic of China. Revised manuscript accepted for publication January 8, 1992. Address correspondence and reprint requests to Zu·Yau Lin, MD, Department of Internal Medicine.• Kaohsiung Medical College Hos· pita!, No. 100 Shih~Chuan 1st Road, Kaohsiung City 807, Taiwan, ROC.
MATERIALS AND METHODS From August 1989 to May 1990, 97 patients (80 men, 17 women) with HCC seen at our institution underwent duplex pulsed Doppler scanning of the portal
@ 1992 by the American Institute of Ultrasound in Medicine• JUltrasound Med 11 :269- 273, 1992 • 0278-4297/ 92/ $3.50
270
DETECTION OF ARTERIOPORT AL SHUNTING
venous system and comparative angiography. The patients ranged in age from 24 to 80 years. The diagnosis of HCC was made by sonographically guided percu· taneous aspiration cytology or biopsy plus at least one positive result with angiography or a serum alphafetoprotein level of greater than 400 ng/ml. Classification of the type of HCC (diffuse or massive) and the diagnosis of portal venous thrombosis were made by B,mode real-time ultrasonography. 1• .20 Comparative celiac or hepatic arteriography and arterial portography were performed within 2 weeks after Doppler examination. Doppler examination was performed with a 3.75 MHz sector scanner combined with a duplex pulsedwave Doppler system (SSA toOA, Toshiba, Tokyo, japan). The wall filter was set at 100 Hz, and the pulse repetition frequency was 4 KHz. The Doppler gain (set at 2 to 4) and the echo level (set at 6 to 8), which were used to alter the strength of the Doppler signals from the display of the spectral profile, were at their optimum settings to obtain clear outline of flow waves with a minimum of background noise. The depth of the measurement was limited to less than 10 cm to prevent interference by signals of unrelated vessels adjacent to the portal vein because the sonographic beam diverges the farther it is from the transducer.21 All patients were examined in the supine or left decubitus position. The portal venous system was ex; amined regularly from main trunk, left transverse, and umbilical portions to right anterior and posterior branches. B~mode real-time sector imaging was used first to detect any thrombus within the lumen. The Doppler cursor was then manipulated under B-mode real-time sonographic guidance within the lumen (in vessels without thrombus) or within the residual lumen (in partially thrombotic portal veins) to detect the waveform and the direction of the portal blood flow. The sample width was set to encompass the whole patent lumen with care taken not to exceed the margin of the lumen being studied to exclude the possibility of picking up Doppler signals transmitted from adjacent unrelated vessels. The probe was manipulated from every possible direction to obtain Doppler signals from the smallest angle between the Doppler beam and the vessels being studied. Any tubular structure adjacent to the portal vein was also examined to exclude the possibility of interference from adjacent vessels unrelated to the portal vessel. Celiac or hepatic arteriography was performed by the conventional Seldinger technique. The catheter was placed in the common or preferably proper hepatic artery and 40 to 55 ml of 65% meglumine diatrizoate was injected within 5 sec by the automatic injector. For arterial portography, 40 to 45 ml of the contrast medium was injected into the superior mesenteric artery.
J Ultrasound Med 11:269-273, 1992
RESULTS Twenty-one patients were found to have portal venous thrombosis on B-mode real-time ultrasonography. Seven of them demonstrated AP shunting on arteriography (two cases), duplex scanning (one case), or both (four cases). AP shunting was also shown by arteriography and duplex scanning in three patients without evidence of portal venous thrombosis on B· mode real-time ultrasonography (two by arteriography and one by both arteriography and duplex scanning). None of these three patients had a history of hepatic trauma, operation, or biopsy. The results of duplex scanning from nine patients with AP shunting on arteriography (one diffuse and eight massive HCC) were as follows: four patients demonstrated unidirectional or bidirectional pulsatile waves from the patent lumen near the site of the shunt (Fig. 1), one other patient revealed pulsatile waves from the whole length of the patent left portal venous branch (Fig. 2), and the other four patients did not demonstrate any unusual Doppler signals from the patent lumen. One patient with massive HCC demonstrated left portal venous thrombosis on B-mode real-time ultrasonography but did not have evidence of AP shunting on arteriography. Duplex scanning of this patient demonstrated continuous waves of hepatofugal direction from the residual lumen of the left portal vein, and high-frequency systolic Doppler shifts (>3.5 KHz) from the adjacent hepatic artery (Fig. 3). The Doppler results indicated the presence of AP shunting.
DISCUSSION Detection of AP shunting by Doppler ultrasonography
is based mainly on the high-frequency systolic Doppler
shifts (>3 KHz), which is produced by a large pressure gradient between the artery and the recipient vein15.22 around the periphery of the tumor. 14 - 17 Although Doppler examination using this criterion appears to be more sensitive than angiography in the detection of AP shunts, 1' it cannot be used to assess the hemodynamic change in the portal vein lumen. Detection of an AP shunt by Doppler ultrasonography without simultaneously determining the hemodynamic change in the recipient portal vein lumen will limit the clinical utility of this information. Patients with HCC and AP shunting are particularly likely to bleed from esophagogastric varices.7 Although the simultaneous presence of cirrhosis, portal hypertension, and a portal vein thrombus represents a relative contraindication to hepatic arterial embolization;?:! variceal hemorrhage in patients with HCC complicated by hepatofugal portal blood flow
JUltrasound Med 11:269- 273, 1992
A
LIN ET AL 271
A
B
B Figure 2 Arterioportal shunting in patient with he patocellular carcinoma. A, Doppler scanning demonstrates pulsatile waves from the whole length of the left portal venous branch .. B, Celiac arteriography demonstrates arterioportal shunting (arrcw).
c Figure 1 Hepatocellular carcinoma with right portal venous thrombosis. A, Doppler scanning demonstrates bidirectional pulsatile waves from the patent lumen near the right portal venous thrombus. B, When the Doppler cursor (arrowheads) is moved away from the thrombotic segment, the pulsatile waves change to the portal continuous waves. C, Celiac arteriography demonstrates arterioportal shunting (arrow).
due to a large AP shunt may be safely controlled by a highly selective therapeutic occlusion of the shunting artery. 8 Furthermore, understanding the probable point
of shunting and the hemodynamics of the recipient portal vein may be used to predict the possible areas of dissemination of cancer cells. Hepatofugal portal blood flow from AP shunting in patients with HCC may have allowed dissemination of cancer cells in the splanchnic area. Hepatic resection in this situation may be meaningless. Therefore, Doppler scanning from the portal lumen is mandatory for the clinical detection of AP shunts by Doppler ultrasonography. Changes in the Doppler signals and in the hemody· namics in the recipient portal vein lumen in patients with AP shunting have been discussed by some au· thors. 12""'13. 18 However, these reports did not apply Dop· pier ultrasonography in a large series of patients to evaluate its clinical utility in the detection of AP shunting from the portal lumen. In the present study, nine of 97 patients demonstrated AP shunting on arteriog-
272
DETECTION OF ARTERIOPORTAL SHUNTING
A
8
c Figure 3 Hepatocellular carcinoma with left portal venous
thrombosis. A, Doppler scanning demonstrates continuous waves of hepatofugal direction from the residual lumen of the left portal vein (arrow). B, Doppler scanning from the adjacent hepatic artery demonstrates high-frequency systolic Doppler shifts (greater than 3.5 KHz) (arrowl1eads). C, There is no evidence of arterioportal shunting on hepatic arteriography.
J Ultrasound Med 11:269- 273, 1992
raphy. Duplex scanning from the patent portal lumen correctly identified five of these nine patients. Among them, only one patient could demonstrate pulsatile waves along the entire length of the left portal branch. In the other four patients pulsatile waves were found only at the site near the shunting. The reason for the difference in Doppler results may be the differing amounts of blood flowing through the shunt. A small volume of arterial blood flowing through the shunt may be able to change the portal continuous waves to pulsatile waves at the site near the shunt. However, it is unable to maintain its pulsatile character at sites away from the shunt because relatively large volumes of confluent portal blood flow reduce the ability to produce pulsatile waves. A large volume of arterial blood flowing through the shunt may overcome the portal blood flow and may even produce retrograde hepatofugal flow in the portal venous system. 8 There· fore, increasing the volume of blood flowing through the shunt can produce detectable pulsatile waves from the recipient portal lumen father away from the shunt area. However, the angiographic features of AP shunting in these five patients were similar. The inconsistency between Doppler and angiographic results may be due to the different procedures employed for these two examinations. Celiac or hepatic arteriography requires injection of contrast material, which is usually performed by an automatic injector over a few seconds and, therefore, leads to a high injection pressure in the artery. Consequently, the results obtained by this procedure do not reflect the patient's natural physiologic condition. 4•18 Duplex scanning, however, does not require the use of contrast material or special preparation of the patient. Thus, the Doppler results reflect the natural physiologic condition. Four patients with angiographic evidence of AP shunting did not demonstrate unusual Doppler signals from the patent portal lumen. The finding of only a small amount of contrast medium in the recipient portal vein on angiography in these patients indicated that a small volume of blood was flowing through the shunt. Duplex scanning failed to detect these shunts because pulsatile character of a low volume of arterial blood cannot be expressed when there is a relatively large volume of portal blood flow. One patient without angiographic evidence of AP shunting had unusual Doppler results that indicated the existence of the shunt. The continuous rather than pulsatile waves from the residual lumen, as seen in this patient, may result from a low rate of blood flow through the shunt, which could not be identified by arteriography; therefore, the pulsatile character was not obvious. Blood flow was hepatofugal because of the total occlusion of the distal portion of the left portal venous branch by the tumor thrombus. In 14 of 21 patients in the present study who had
J Ultrasound Med 11 :269- 273, 1992
portal venous thrombosis on B-mode real-time ultrasonography, AP shunting was not found on arteriography or duplex scanning. Although very small AP shunts may be missed by both arteriography 15 and duplex scanning, our findings indicated that patients with portal venous thrombosis did not necessarily have obvious AP shunting. On the other hand, three patients in the present study without evidence of portal venous thrombosis on B-mode real-time ultrasonography also demonstrated AP shunting on arteriography and duplex scanning. These patients did not undergo hepatic resection or autopsy and, therefore, the real mechanism of shunt formation could not be determined. However, this result indicated that existence of an AP shunt could not be excluded in patients without portal venous thrombosis on B-mode real-time ultrasonography. All patients with HCC should be examined carefully to rule out AP shunting. Recent technological developments in Doppler color flow imaging have made it possible to investigate the vascular stenosis, occlusion, and flow disturbance easily and rapidly.24 Theoretically Doppler color flow imaging will be much easier than duplex ultrasonography in detecting and evaluating the severity of AP shunting. The clinical utility of Doppler color flow imaging for detecting AP shunts remains to be evaluated in a large series of patients with HCC. From the foregoing results, we conclude that duplex scanning from the patent or residual lumen of the portal venous system may be useful in the detection of AP shunting in patients with HCC. This procedure also can indicate hemodynamic changes in the recipient portal venous system. However, small shunts without hepatofugal portal blood flow cannot be detected by this procedure. Simultaneous Doppler scanning from the periphery of the tumor and the tubular structures around the portal venous system may compensate for this limitation.
REFERENCES 1. Van Way CW, Crane JM, Ridell DH, et al: Arteriovenous fistula in the portal circulation. Surgery 70:876, 1971 2. ltzchak Y, Adar R, Bogokowski H, et al: lntrahepatic arterial portal communications: Angiographic study. AJR 121:384, 1974 3. Rabinowitz JG, Kinkabwala M, Ulreich S: Macro-regenerating nodule in the cirrhotic liver. AJR 121:401, 1974 4. Okuda K, Musha H, Yamasaki T, et al: Angiographic demonstration of intrahepatk arterio-portal anastomoses in hepatocellular carcinoma. Radiology 122:53, 1977 5. Okuda K, Musha H, Nakajima Y, et al: Frequency of intrahepatic arteriovenous fistula as a sequela to percutaneous needle puncture of the liver. Gastroenterology 74:1204, 1978
LIN ET AL
273
6. Bookstein JJ, Cho KJ, Davis GB, et al: Arterioportal communications: Observations and hypotheses concerning transsinusoidal and transvasal types. Radiology 142:581, 1982 7. Nagasue N, Inokuchi K, Kobayashi M, et al: Hepatoportal arteriovenous fistula in primary carcinoma of the liver. Surg Gynecol Obstet 145:504, 1977 8. Morse SS, Sniderman KW, Galloway S, et al: Hepatoma, arterioportal shunting, and hyperkinetic portal hypertension: Therapeutic embolization. Radiology 155:77, 1985 9. Gammill SL, Takahashi M, Kawanarni M, et al: Hepatic angiography in the selection of patients with hepatoma for hepatic lobectomy. Radiology 101:549, 1971 10. Marks WM, Jacobs RP, Goodman PC, et al: Hepatocellular carcinoma: Clinical and angiographic findings and predictability for surgical resection. AJR 132:7, 1979 11. Nakayama T, Hiyama Y, Ohnishi K, et al: Arterioportal shunts on dynamic computed tomography. AJR 140:953, 1983 12. Lafortune M, Breton G, Charlebois S: Arterioportal fistula demonstrated by pulsed Doppler ultrasonography. J Ultrasound Med 5:105, 1986 13. Ohnishi K, Saito M, Sata S, et al: Clinical utility of pulsed Doppler flowmetry in patients with portal hypertension. Am J Gastroenterol 81:1, 1986 14. Taylor KJW, Ramos I, Morse SS, et al: Focal liver masses: Differential diagnosis with pulsed Doppler US. Radiology 164:643, 1987 15. Taylor KJW, Ramos I, Carter D, et al: Correlation of Doppler US tumor signals with neovascular morphologic features. Radiology 166:57, 1988 16. Yasuhara K, Kimura K, Ohto M, et al: Pulsed Doppler in the diagnosis of small liver tumours. Br J Radio) 61:898, 1988 17. Ohnishi K, Nomura F: Ultrasonic Doppler studies of hepatocellular carcinoma and comparison with other he· patic focal lesions. Gastroenterology 97:1489, 1989 18. Lafortune M, Patriquin H, Bums P: Doppler ultrasound in the evaluation of portal and splanchnic blood flow. Ill Ferrucci JT, Mathieu DG (eds): Advances in Hepatobiliary Radiology. St. Louis, CV Mosby, 1990, p 29 19. Ohto M, Ebara M, Okuda K: Ultrasonography in the diagnosis of hepatic tumor. 111 Okuda K, Ishak KG (eds); Neoplasms of the Liver. Tokyo, Springer-Verlag, 1987, p 251 20. Gansbeke DV, Avni EF, Delcour C, et al: Sonographic features of portal vein thrombosis. AJR 144:749, 1985 21. Kisslo J, Mark DB, Adams D: Pulsed and continuous wave Doppler. In Kisslo J, Adams D, Mark DB (eds): Basic Doppler Echocardiography. New York, Churchill Livingstone, 1986, p 25 22. Bums PN, Gowland MR, Rimmer S: Use of Doppler ultrasound in the detection of changes in the blood flow in tumour circulation in the rabbit. J Physiol 342: 12, 1983 23. Chamsangavej C, Chuang VP, Wallace S, et al: Work in progress: Transcatheter management of primary card· noma of the liver. Radiology 147:51, 1983 24. Merritt CRB: Doppler color flow imaging. J Clin Ultra~ sound 15:591, 1987
