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Transjugular intrahepatic portosystemic shunting improves splanchnic hemodynamics and renal Na excretion in cirrhosis with refractory ascites
International ELSEVIER
Hepatology Communications 6-(1996)-l -7
Transjugular intrahepatic portosystemic shunting improves splanchnic hemodynamics and renal Na excretion in cirrhosis with refractory ascites Shuichi SezaP,*, Mitsuhiro Terada”, Masayoshi Ito”, Yukihiro Sakurai”, Kazuaki Kamisaka”, Takashi Abeb, Fumiaki Ikegamib, Masanori Hiranoc “Division
of Gastroenterology,
Kanto
bHealth Care Center, ‘Tokyo Metropolitan
NTT Hospital, S-9-22 Higashi-gotanda, Shinagawa-ku, Tokyo 141, Japan Kanto NTT Hospital, Tokyo 141, Japan Police Hospital, Tokyo 102, Japan
Received 17 November 1995; revised 24 July 1996; accepted 1 August 1996
Abstract
To clarify the pathogenesis of ascitesin patientswith liver cirrhosis,we explored the effects of transjugular intrahepatic portosystemicshunting in six cirrhotic patients with refractory ascites.The portal pressuredecreasedfrom 39f 7 cmH,O before treatmentto 32 + 5 cmH,O immediatelyafter the procedure.Liver function transiently deterioratedafter the procedure, but recoveredwithin 1 week. Urinary Na excretion increased1 week after treatment. In five patients, ascitesimproved within 3 weeks.Along with the decreaseof portal congestion, there was an improvementof esophagealvarices, and an increaseof gastric mucosalblood flow, and an inhibition of the renin-angiotensin-aldosterone systemin all of the patientsafter 2-4 weeks.Manageable shunt encephalopathyoccurred in three patients. These findings strongly suggestthe pivotal role of increasedportal pressurein the formation of ascitesin patientswith liver cirrhosis. Keywords:
Portal congestion;Portal pressure;Esophagealvarices; Hepatic encephalopathy
* Corresponding author. Tel.: + 81 3 34486102; fax: + 81 3 34486137. 092%4346/96/$12.00 Copyright 0 1996 Elsevier Science Ireland Ltd. All rights reserved PII SO928-4346(96)003
19-2
2
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
l- 7
1. Introduction Both the ‘underfilling’ and ‘overflow’ theories on the pathogenesis of ascites in liver cirrhosis have been discussed by several researchers, but no definite conclusions have been reached. Since 1993, the effectiveness of transjugular intra-hepatic portosystemic shunting (TIPS) for refractory ascites has been reported in the literature [I -51. The primary purpose of this procedure is to reduce hepatic sinusoidal pressure. Existence of the ‘underfilling’ mechanism [6] based on sinusoidal hypertension would thus be supported by the reduction of ascites in cirrhotic patients after TIPS. In the present study, we performed TIPS in cirrhotic patients with refractory ascites and examined its effects on splanchnic hemodynamics and renal Na excretion as well as on the ascites per se.
2. Patients and methods This prospective study was performed in six patients with cirrhosis and ascites that could not be controlled by bed rest, a low-Na diet, restriction of water intake, albumin infusion, and diuretics given according to Quiroga’s criteria [3]. Two of them received the lower dose set by the criteria due to elevated creatinine levels, and so did the other four due to the presence of hyperkalemia and mastitis. The average diuretic doses are given in Table 1. There were three men and three women with a mean age of 62 years. The severity of cirrhosis was classified according to Child’s classification; all six patients were in class C. Pugh’s score was 11 in two patients; ten in one patient and nine in three patients. The control group comprised eight patients (4 men and 4 women with a mean age of 60 years) who were all in Child’s class C and did not undergo TIPS. A Riisch-Uchida Transjugular Liver Access Set (Hirata, Osaka, Japan) was employed for the procedure, using five Z stents (1 cm in diameter) and one Wall type stent (0.8 cm). The study protocol was approved by the ethics committee of our hospital and conformed to the guidelines of the Declaration of Helsinki. All the patients were informed of the details of the procedure and gave written consent. Liver function was assessed periodically before and after the procedure. The portal venous pressure was also measured before and after TIPS. After the Table 1 Clinical data before the treatment Furocemide (mg/day) Spironolactone (mg/day) Urine volume (mg/day) Urinary Na excretion (mEq/day] Bilirubin (mg/dl) Albumin (g/dl) PT (%) BUN (mg/dl)
92 k 142 + 562 k 36& 1.6 k 2.7 + 56 + 33 *
5 32 91 13 0.4 0.5 9 5
S. Sezai et al. 1 International
Hepaiology
Communications
6 (1996)
I- 7
3
improvement of ascites, duplex sonography (Toshiba SSA-260A, Tokyo, Japan) was performed with a phased-array transducer. The angle between the Doppler beam and the longitudinal axis of the vessels was maintained at less than 60”. The congestive index (CI) was calculated from the ratio between the cross sectional area and the blood flow velocity (V,,,, of the portal vein [7]). Since it was impossible to measure these two parameters before TIPS because of the presence of ascites, measurement was done as soon as the ascites had resolved. The changes of urinary Na excretion as well as those of the plasma renin activity and plasma aldosterone concentration were measured. The F-factor of esophageal varices was. evaluated according to the diagnostic criteria of the Japanese Research Society for Portal Hypertension [8] both 2 weeks before and 2-4 weeks after TIPS. Gastric mucosal blood flow was measured with a laser Doppler flowmeter (Periflux PF-3, Stockholm, Sweden). Results are shown as the mean + S.E. Paired and unpaired students’ t-tests were used to compare the two groups, and analysis of variance was used for multiple sets of data. A P value less than 0.05 was considered to indicate statistical significance.
3. Results The serum GPT level was maximal at 24 h after TIPS and returned to baseline by 7 days after the procedure (Fig. 1). The cholesterol and cholinesterase levels were lowest at 1 week after TIPS and gradually returned to baseline thereafter. In the five patients we could follow, urinary Na excretion began to increase gradually about 1 week after TIPS (Fig. 2). After the procedure, the diuretic dosage was reduced in all patients depending on the persistence of ascites. Disappearance of ascites was confirmed by ultrasonography within 7 days in two patients, after 16 days in three patients, and after 3 months in one patient. In the patient with the slowest improvement, urinary Na excretion returned to the normal range after 4 weeks. Plasma renin and aldosterone levels were reduced after TIPS. The serum creatinine in two patients with preoperative levels of 2 mg/dl was normalized on days 21 and 24 after TIPS respectively. Portal venous pressure decreased from 39 f 3 cmH,O to 32 + 2 cmH,O (P < 0.01). I’,,,, was higher in the TIPS patients than in the control group (17.8 f 1.7 cm/s vs. 8.1 + 2.4, P -c 0.01). The CI was significantly lower than in the control group (0.08 + 0.01 vs. 0.19 f 0.06, P < 0.01). The F-factor of esophageal varices was improved in all of the patients undergoing TIPS and gastric mucosal blood flow was significantly increased (P < 0.01, Table 2). The serum ammonia level was also elevated in all patients (Fig. 3), and required to start medication such as lactulose and amino acid infusion.
4. Discussion
Generally, TIPS is indicated for cirrhotic patients with esophageal varices that are resistant to scierotherapy and there have only been a few prospective studies of
4
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
1- 7
W)
Fig. 1. Changes of liver function parameters after TIPS: the serum GPT level was markedly elevated at 24 h after TIPS. Cholinesterase (ChE) and Cholesterol (Cho) levels were lowest 1 week after TIPS and then returned gradually to baseline.
its use for refractory ascites [l-3]. The present results indicated the effectiveness of TIPS for this condition. The serum GPT level was elevated temporarily following TIPS, and parameters of hepatic synthetic function reached a minimum 1 week later. This temporary worsening of liver function might have been due to procedural invasion, as has also been reported elsewhere [2,5,9]. The formation of ascites should be primarily related to increased sinusoidal pressure according to the ‘underfilling’ theory. Our results confirmed the relationship between a decrease of the sinusoidal pressure and increased urinary Na excretion, with an increase of Na excretion and a decline of renin-aldosterone activity being seen after TIPS. In contrast, the ‘overflow’ theory regards accelerated renal Na reabsorption as an initial event in the formation of ascites [lo] Increased cardiac output and low systemic venous resistance characterize patients with advanced cirrhosis [3,4,11,12]. One report has described deterioration of the hyperdynamic state after TIPS, resulting in heart failure [4]. However, Mprller et al. [ll] assessed the volume of the cardiac cavities and confirmed a decrease of right heart blood volume in cirrhosis by magnetic resonance imaging. Considering their results, the ‘underfilled’ right heart could be improved by TIPS. Furthermore serum renin-aldosterone activity should be suppressed in the ‘overflow’ state. However, we found the inhibition of this system only
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
I ~7
Fig. 2. Changes of plasma renin and aldosterone and urinary Na excretion after TIPS: plasma renin and aldosterone activities after TIPS in the four patients assessed. In contrast, urinary Na excretion increased.
after TIPS along with the lessening of ascites. Somberg [2] and Quiroga et al. [3] have presented semilar findings of increased urinary Na excretion and decreased renin-aldosterone activity. Our study showed that TIPS relieved portal congestion, increased gastric mucosal flow, and improved esophageal varices and renal function. According to Azoulay et al. the portal pressure was reduced immediately after TIPS, continued to decline gradually, and reached a plateau about 1 month later [4]. Thus, by diverting the enlarged splanchnic blood pool into the systemic Table 2 Effect of TIPS on esophageal varices and gastric mucosal blood flow (GMBF) Esophageal varices
GMBF (V) Pre-TIPS Case Case Case Case
1 2 3 4
2.2 2.3 2.2
Case 5
0.8 2.0
Case 6 Mean i. S.E.
1.5 1.8 kO.3
*P 0.01 vs. pre-TIPS value.
Post-TIPS 2.8 3.8 3.0 2.1 2.0 3.0 2.9 + 0.3*
Pre-TIPS
Post-TIPS
F3 F2 F,
F2 F, Fo
F2 F3
FO F2
6
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
I- 7
13th : .--: : : : :
I , -1w
I 0
I lw
Time I I I 2w 3w 4w
Fig. 3. Serum ammonia and shunt encephalopathy after TIPS: the serum ammonia level increased in all six patients. Shunt encephalopathy (arrows) occurred in three patients on days 13, 16, and 26 after the procedure.
circulation, TIPS may increase cardiac preload and result in an increase of effective organ perfusion. However, shunt encephalopathy developed almost simultaneously with the improvement of hemodynamics. In previous studies, this complication has been found to occur over a wide range from less than IO-75% [2,9,13]. Our rather high incidence of this complication (50%) might have been due to the fact that our patients were all in child’s class C, juding from the risk factors described in previous reports.
References [l] Ferral H, Bjarnason H, Wegryn SA, et al. Refractory ascites: early experience in treatment with transjugular intrahepatic portosystemic shunt. Radiology 1993; 189: 795-801. [2] Somberg KA, Lake JR, Tomlanovich SJ, et al. Transjugular intrahepatic portosystemic shunts for refractory ascites: assessment of clinical and hormonal response and renal function. Hepatology 1995; 21: 7099716. [3] Quiroga J, Sangro B, Nunez M, et al. Transjugular intra-hepatic portal systemic shunt in the treatment of refractory ascites: effect on clinical, renal, humoral, and hemodynamic parameters. Hepatology 1995; 21: 986-994. [4] Azoulay D, Castang D, Dennison A, et al. Transjugular intrahepatic portosystemic shunt worsens the hyperdynamic circulatory state of the cirrhotic patient: preliminary report of a prospective study. Hepatology 1994; 19: 129-132.
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
l-7
I
[5] Martin M, Zajko FAB, Orons PD, et al. Transjugular intrahepatic portosysternic shunt in the management of variceal bleeding: indications and clinical results. Surgery 1993; 114: 719-727. [6] Epstein M. Decreased sodium homeostasis in cirrhosis. Gastroenterology 1979; 76: 622-635. [7] Moriyasu F, Nishida 0, Ban N, et al. ‘Congestive Index’ of the portal vein. Am J Roentgenology 1986; 146: 7355739. [8] Japanese Research Society for Portal Hypertension. The general rules for recording endoscopic findings on esophageal varcies. Jpn J Surg 1980; 10: 84487. [9] Laberge JM, Ring EJ, Gordon RL, et al. Creation of transjugular intrahepatic portosystemic shunts with wall stent endoprosthesis: results in 100 patients. Radiology 1993; 187: 413-420. [lo] Lieberman FL, Denison EK, Reynolds TB, et al. The relationship of plasma volume, portal hypertension, ascites, and renal sodium retention in cirrhosis: the ‘overflow’ theory of ascites formation. Ann NY Acad Sci 1970; 170: 202-206. [11] Moller S. Ssndergaard L, Mogelvang J, et al. Decreased right heart blood volume determined by magnetic resonance imaging: evidence of central underfilling in cirrhosis. Hepatology 1995; 22: 412- 478. [12] Wong F, Liu P, Tobe S, et al. Central blood volume in cirrhosis-measurement with radionuclide angiography. Hepatology 1994; 19: 312-321. [13] Rossle M, Haag K, Ochs A, et al. The transjugular intrahepatic portosystemic stent-shunt procedure for variceal bleeding. New Eng J Med 1994: 330: 165- 171.
Hepatology Communications 6-(1996)-l -7
Transjugular intrahepatic portosystemic shunting improves splanchnic hemodynamics and renal Na excretion in cirrhosis with refractory ascites Shuichi SezaP,*, Mitsuhiro Terada”, Masayoshi Ito”, Yukihiro Sakurai”, Kazuaki Kamisaka”, Takashi Abeb, Fumiaki Ikegamib, Masanori Hiranoc “Division
of Gastroenterology,
Kanto
bHealth Care Center, ‘Tokyo Metropolitan
NTT Hospital, S-9-22 Higashi-gotanda, Shinagawa-ku, Tokyo 141, Japan Kanto NTT Hospital, Tokyo 141, Japan Police Hospital, Tokyo 102, Japan
Received 17 November 1995; revised 24 July 1996; accepted 1 August 1996
Abstract
To clarify the pathogenesis of ascitesin patientswith liver cirrhosis,we explored the effects of transjugular intrahepatic portosystemicshunting in six cirrhotic patients with refractory ascites.The portal pressuredecreasedfrom 39f 7 cmH,O before treatmentto 32 + 5 cmH,O immediatelyafter the procedure.Liver function transiently deterioratedafter the procedure, but recoveredwithin 1 week. Urinary Na excretion increased1 week after treatment. In five patients, ascitesimproved within 3 weeks.Along with the decreaseof portal congestion, there was an improvementof esophagealvarices, and an increaseof gastric mucosalblood flow, and an inhibition of the renin-angiotensin-aldosterone systemin all of the patientsafter 2-4 weeks.Manageable shunt encephalopathyoccurred in three patients. These findings strongly suggestthe pivotal role of increasedportal pressurein the formation of ascitesin patientswith liver cirrhosis. Keywords:
Portal congestion;Portal pressure;Esophagealvarices; Hepatic encephalopathy
* Corresponding author. Tel.: + 81 3 34486102; fax: + 81 3 34486137. 092%4346/96/$12.00 Copyright 0 1996 Elsevier Science Ireland Ltd. All rights reserved PII SO928-4346(96)003
19-2
2
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
l- 7
1. Introduction Both the ‘underfilling’ and ‘overflow’ theories on the pathogenesis of ascites in liver cirrhosis have been discussed by several researchers, but no definite conclusions have been reached. Since 1993, the effectiveness of transjugular intra-hepatic portosystemic shunting (TIPS) for refractory ascites has been reported in the literature [I -51. The primary purpose of this procedure is to reduce hepatic sinusoidal pressure. Existence of the ‘underfilling’ mechanism [6] based on sinusoidal hypertension would thus be supported by the reduction of ascites in cirrhotic patients after TIPS. In the present study, we performed TIPS in cirrhotic patients with refractory ascites and examined its effects on splanchnic hemodynamics and renal Na excretion as well as on the ascites per se.
2. Patients and methods This prospective study was performed in six patients with cirrhosis and ascites that could not be controlled by bed rest, a low-Na diet, restriction of water intake, albumin infusion, and diuretics given according to Quiroga’s criteria [3]. Two of them received the lower dose set by the criteria due to elevated creatinine levels, and so did the other four due to the presence of hyperkalemia and mastitis. The average diuretic doses are given in Table 1. There were three men and three women with a mean age of 62 years. The severity of cirrhosis was classified according to Child’s classification; all six patients were in class C. Pugh’s score was 11 in two patients; ten in one patient and nine in three patients. The control group comprised eight patients (4 men and 4 women with a mean age of 60 years) who were all in Child’s class C and did not undergo TIPS. A Riisch-Uchida Transjugular Liver Access Set (Hirata, Osaka, Japan) was employed for the procedure, using five Z stents (1 cm in diameter) and one Wall type stent (0.8 cm). The study protocol was approved by the ethics committee of our hospital and conformed to the guidelines of the Declaration of Helsinki. All the patients were informed of the details of the procedure and gave written consent. Liver function was assessed periodically before and after the procedure. The portal venous pressure was also measured before and after TIPS. After the Table 1 Clinical data before the treatment Furocemide (mg/day) Spironolactone (mg/day) Urine volume (mg/day) Urinary Na excretion (mEq/day] Bilirubin (mg/dl) Albumin (g/dl) PT (%) BUN (mg/dl)
92 k 142 + 562 k 36& 1.6 k 2.7 + 56 + 33 *
5 32 91 13 0.4 0.5 9 5
S. Sezai et al. 1 International
Hepaiology
Communications
6 (1996)
I- 7
3
improvement of ascites, duplex sonography (Toshiba SSA-260A, Tokyo, Japan) was performed with a phased-array transducer. The angle between the Doppler beam and the longitudinal axis of the vessels was maintained at less than 60”. The congestive index (CI) was calculated from the ratio between the cross sectional area and the blood flow velocity (V,,,, of the portal vein [7]). Since it was impossible to measure these two parameters before TIPS because of the presence of ascites, measurement was done as soon as the ascites had resolved. The changes of urinary Na excretion as well as those of the plasma renin activity and plasma aldosterone concentration were measured. The F-factor of esophageal varices was. evaluated according to the diagnostic criteria of the Japanese Research Society for Portal Hypertension [8] both 2 weeks before and 2-4 weeks after TIPS. Gastric mucosal blood flow was measured with a laser Doppler flowmeter (Periflux PF-3, Stockholm, Sweden). Results are shown as the mean + S.E. Paired and unpaired students’ t-tests were used to compare the two groups, and analysis of variance was used for multiple sets of data. A P value less than 0.05 was considered to indicate statistical significance.
3. Results The serum GPT level was maximal at 24 h after TIPS and returned to baseline by 7 days after the procedure (Fig. 1). The cholesterol and cholinesterase levels were lowest at 1 week after TIPS and gradually returned to baseline thereafter. In the five patients we could follow, urinary Na excretion began to increase gradually about 1 week after TIPS (Fig. 2). After the procedure, the diuretic dosage was reduced in all patients depending on the persistence of ascites. Disappearance of ascites was confirmed by ultrasonography within 7 days in two patients, after 16 days in three patients, and after 3 months in one patient. In the patient with the slowest improvement, urinary Na excretion returned to the normal range after 4 weeks. Plasma renin and aldosterone levels were reduced after TIPS. The serum creatinine in two patients with preoperative levels of 2 mg/dl was normalized on days 21 and 24 after TIPS respectively. Portal venous pressure decreased from 39 f 3 cmH,O to 32 + 2 cmH,O (P < 0.01). I’,,,, was higher in the TIPS patients than in the control group (17.8 f 1.7 cm/s vs. 8.1 + 2.4, P -c 0.01). The CI was significantly lower than in the control group (0.08 + 0.01 vs. 0.19 f 0.06, P < 0.01). The F-factor of esophageal varices was improved in all of the patients undergoing TIPS and gastric mucosal blood flow was significantly increased (P < 0.01, Table 2). The serum ammonia level was also elevated in all patients (Fig. 3), and required to start medication such as lactulose and amino acid infusion.
4. Discussion
Generally, TIPS is indicated for cirrhotic patients with esophageal varices that are resistant to scierotherapy and there have only been a few prospective studies of
4
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
1- 7
W)
Fig. 1. Changes of liver function parameters after TIPS: the serum GPT level was markedly elevated at 24 h after TIPS. Cholinesterase (ChE) and Cholesterol (Cho) levels were lowest 1 week after TIPS and then returned gradually to baseline.
its use for refractory ascites [l-3]. The present results indicated the effectiveness of TIPS for this condition. The serum GPT level was elevated temporarily following TIPS, and parameters of hepatic synthetic function reached a minimum 1 week later. This temporary worsening of liver function might have been due to procedural invasion, as has also been reported elsewhere [2,5,9]. The formation of ascites should be primarily related to increased sinusoidal pressure according to the ‘underfilling’ theory. Our results confirmed the relationship between a decrease of the sinusoidal pressure and increased urinary Na excretion, with an increase of Na excretion and a decline of renin-aldosterone activity being seen after TIPS. In contrast, the ‘overflow’ theory regards accelerated renal Na reabsorption as an initial event in the formation of ascites [lo] Increased cardiac output and low systemic venous resistance characterize patients with advanced cirrhosis [3,4,11,12]. One report has described deterioration of the hyperdynamic state after TIPS, resulting in heart failure [4]. However, Mprller et al. [ll] assessed the volume of the cardiac cavities and confirmed a decrease of right heart blood volume in cirrhosis by magnetic resonance imaging. Considering their results, the ‘underfilled’ right heart could be improved by TIPS. Furthermore serum renin-aldosterone activity should be suppressed in the ‘overflow’ state. However, we found the inhibition of this system only
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
I ~7
Fig. 2. Changes of plasma renin and aldosterone and urinary Na excretion after TIPS: plasma renin and aldosterone activities after TIPS in the four patients assessed. In contrast, urinary Na excretion increased.
after TIPS along with the lessening of ascites. Somberg [2] and Quiroga et al. [3] have presented semilar findings of increased urinary Na excretion and decreased renin-aldosterone activity. Our study showed that TIPS relieved portal congestion, increased gastric mucosal flow, and improved esophageal varices and renal function. According to Azoulay et al. the portal pressure was reduced immediately after TIPS, continued to decline gradually, and reached a plateau about 1 month later [4]. Thus, by diverting the enlarged splanchnic blood pool into the systemic Table 2 Effect of TIPS on esophageal varices and gastric mucosal blood flow (GMBF) Esophageal varices
GMBF (V) Pre-TIPS Case Case Case Case
1 2 3 4
2.2 2.3 2.2
Case 5
0.8 2.0
Case 6 Mean i. S.E.
1.5 1.8 kO.3
*P 0.01 vs. pre-TIPS value.
Post-TIPS 2.8 3.8 3.0 2.1 2.0 3.0 2.9 + 0.3*
Pre-TIPS
Post-TIPS
F3 F2 F,
F2 F, Fo
F2 F3
FO F2
6
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
I- 7
13th : .--: : : : :
I , -1w
I 0
I lw
Time I I I 2w 3w 4w
Fig. 3. Serum ammonia and shunt encephalopathy after TIPS: the serum ammonia level increased in all six patients. Shunt encephalopathy (arrows) occurred in three patients on days 13, 16, and 26 after the procedure.
circulation, TIPS may increase cardiac preload and result in an increase of effective organ perfusion. However, shunt encephalopathy developed almost simultaneously with the improvement of hemodynamics. In previous studies, this complication has been found to occur over a wide range from less than IO-75% [2,9,13]. Our rather high incidence of this complication (50%) might have been due to the fact that our patients were all in child’s class C, juding from the risk factors described in previous reports.
References [l] Ferral H, Bjarnason H, Wegryn SA, et al. Refractory ascites: early experience in treatment with transjugular intrahepatic portosystemic shunt. Radiology 1993; 189: 795-801. [2] Somberg KA, Lake JR, Tomlanovich SJ, et al. Transjugular intrahepatic portosystemic shunts for refractory ascites: assessment of clinical and hormonal response and renal function. Hepatology 1995; 21: 7099716. [3] Quiroga J, Sangro B, Nunez M, et al. Transjugular intra-hepatic portal systemic shunt in the treatment of refractory ascites: effect on clinical, renal, humoral, and hemodynamic parameters. Hepatology 1995; 21: 986-994. [4] Azoulay D, Castang D, Dennison A, et al. Transjugular intrahepatic portosystemic shunt worsens the hyperdynamic circulatory state of the cirrhotic patient: preliminary report of a prospective study. Hepatology 1994; 19: 129-132.
S. Sezai et al. / International
Hepatology
Communications
6 (1996)
l-7
I
[5] Martin M, Zajko FAB, Orons PD, et al. Transjugular intrahepatic portosysternic shunt in the management of variceal bleeding: indications and clinical results. Surgery 1993; 114: 719-727. [6] Epstein M. Decreased sodium homeostasis in cirrhosis. Gastroenterology 1979; 76: 622-635. [7] Moriyasu F, Nishida 0, Ban N, et al. ‘Congestive Index’ of the portal vein. Am J Roentgenology 1986; 146: 7355739. [8] Japanese Research Society for Portal Hypertension. The general rules for recording endoscopic findings on esophageal varcies. Jpn J Surg 1980; 10: 84487. [9] Laberge JM, Ring EJ, Gordon RL, et al. Creation of transjugular intrahepatic portosystemic shunts with wall stent endoprosthesis: results in 100 patients. Radiology 1993; 187: 413-420. [lo] Lieberman FL, Denison EK, Reynolds TB, et al. The relationship of plasma volume, portal hypertension, ascites, and renal sodium retention in cirrhosis: the ‘overflow’ theory of ascites formation. Ann NY Acad Sci 1970; 170: 202-206. [11] Moller S. Ssndergaard L, Mogelvang J, et al. Decreased right heart blood volume determined by magnetic resonance imaging: evidence of central underfilling in cirrhosis. Hepatology 1995; 22: 412- 478. [12] Wong F, Liu P, Tobe S, et al. Central blood volume in cirrhosis-measurement with radionuclide angiography. Hepatology 1994; 19: 312-321. [13] Rossle M, Haag K, Ochs A, et al. The transjugular intrahepatic portosystemic stent-shunt procedure for variceal bleeding. New Eng J Med 1994: 330: 165- 171.