8,573

Simultaneous Combined Transjugular Intrahepatic Portosystemic Shunt and Partial Splenic Embolization for Decompensated Cirrhosis

Wan Yue-Meng, Li-Hong Yang, Ying Xu, Yu-Hua Li, Jing Yang, Jin-Hui Yang, Ying-Chun Li, Song-Wei Li, Gui-Bo Song

Wan Yue-Meng, Li-Hong Yang, Ying Xu, Yu-Hua Li, Jing Yang, Jin-Hui Yang, Department of Hepatology Center, The 2nd Affiliated Hospital of Kunming Medical University, Kunming City, China
Ying-Chun Li, Song-Wei Li, Department of Radiology, Interventional Unit, The 2nd Affiliated Hospital of Kunming Medical University, Kunming City, China
Gui-Bo Song, Department of Clinical Laboratory, The 1st Affiliated Hospital of Kunming Medical University, Kunming City, China
Wan Yue-Meng, and Li-Hong Yang contributed equally to this work

Correspondence to: Jin-Hui Yang, Ying Xu, Professor, Hepatology center of the 2nd Affiliated Hospital of Kunming Medical University, Yunnan Province, China
Email: august19840820@163.com, 1085088967@qq.com
Telephone: +86-0871-6535128
Fax: +86-0871-65361017
Received: November 15, 2015
Revised: January 4, 2016
Accepted: January 8, 2016
Published online: January 17, 2016

ABSTRACT

AIM: To evaluate the efficacy and safety of transjugular intrahepatic portosystemic shunt (TIPS) in combination with partial splenic arterial embolization (PSE) for cirrhotic patients with recurrent variceal bleeding and hypersplenism.

METHODS: Institutional review board approval was obtained; all patients provided informed consent. From January 2010 to December 2014, a total of 141 cirrhotic patients received TIPS alone(group A, n=114) and simultaneous combined TIPS and PSE(group B, n=27) for recurrent variceal bleeding and hypersplenism secondary to portal hypertension. The TIPS was created by using covered stents. All patients underwent embolotherapy via the jugular vein after TIPS implantation. Patients in group B (n=27) received simultaneous PSE after creation of TIPS. Biochemical tests, coagulation function, complete blood cell (CBC) counts, frequencies of recurrent variceal bleeding and hepatic encephalopathy (HE), and survival were evaluated. Model for end stage liver diseases (MELD) scores were calculated.

RESULTS: TIPS creation was successful in all patients. After the treatments, patients in group B had better hepatic synthetic function, increased levels of white blood cells (WBC), platelets (PLT), and hemoglobin(HGB), lower frequency of HE, lower overall and cirrhosis-related mortality than patients in group A (P<0.05), though the two groups had similar recurrent variceal bleeding frequency (P>0.05). Multivariate analysis showed that MELD scores, HE, and group were independent factors for overall and liver-related mortality at month 24 (P<0.05). No severe complications were observed in the two groups.

CONCLUSIONS: Simultaneous combined TIPS and PSE regimen improves hematologic parameters, prevents deterioration of liver function and coagulation function, reduces variceal bleeding and HE, thus reduces mortality.

© 2016 ACT. All rights reserved.

Key words:Transjugular intrahepatic portosystemic shunt(TIPS); Partial splenic embolization(PSE); Decompensated cirrhosis; Portal hypertension

Yue-Meng W, Yang LH, Xu Y, Li YH, Yang J, Yang JH, Li YC, Li SW, Song GB. Simultaneous Combined Transjugular Intrahepatic Portosystemic Shunt and Partial Splenic Embolization for Decompensated Cirrhosis. Journal of Gastroenterology and Hepatology Research 2016; 5(1): 1914-1920 Available from: URL: http://www.ghrnet.org/index.php/joghr/article/view/1573

Abbreviation

TIPS: transjugular intrahepatic portosystemic shunt; PSE: partial splenic embolization; HBV: hepatitis B virus; HCV: hepatitis C virus; ALB: serum albumin; ALT: alanine aminotransferase; AST: aspartate aminotransferase; CHE: cholinesterase; TBIL: total bilirubin; DBIL: direct bilirubin; Cr: creatinine; TC: total cholesterol; PT: prothrombin time; INR: international normalized ratio; WBC: white blood cell; RBC: red blood cell; HGB: hemoglobin; PLT: platelet; CTP: Child-Turcotte-Pugh score; MELD: model for end stage liver disease; HE: hepatic encephalopathy; RR: relative risk; CI: confidence interval; NS: not significant; DSA: digital subtraction angiography.

Introduction

Although transjugular intrahepatic portosystemic shunt (TIPS) has been proved to be an effective treatment for preventing variceal bleeding secondary to portal hypertention in cirrhosis[1,2], the risk of hepatic encephalopathy(HE) greatly increases after TIPS placement, and the risk of recurrent variceal bleeding after TIPS placement remains an issue[1,3]. Risk factors for recurrent bleeding include an insufficient decrease in portosystemic pressure gradient after TIPS creation alone[4].

Partial splenic arterial embolization(PSE), which has been an established interventional approach for portal hypersplenism[5,6], appears to be efficatious to in reducing episodes of variceal bleeding[7,8], improving hematologic parameters[9,10], enhancing hepatic protein synthesis[11], and reducing severity of HE[12]. Therefore, we hypothesized that concomitant PSE can further improve the clinical outcomes of cirrhotic patients who underwent TIPS palcement. The efficacy and safety of this simultaneous combined therapy are discussed below.

Methods

Subjects

This study was approved by our institutional ethics committee. The study protocol conformed to the ethical guidelines of the 2008 Declaration of Helsinki. No potential conflicts of interest were disclosed. Between January 2010 and December 2014, a total of 174 consecutive patients with cirrhosis and gastroesophageal variceal bleeding proved by emergent gastroscopy were identified in this study. In total, we performed TIPS alone in 114 patients (group A, n=114), and simultaneous combined TIPS and PSE in 27 patients (group B, n=27) (Figure 1).

Therapeutic protocol

After their conditions were stabilized by medications, and /or endoscopic band ligation or sclerotherapy, a physician and a consulted interventional radiologist explained the benefits and risks of the procedures to each patient in view of their laboratory tests and computerized tomography portal venography (CTPV) reports, and determined whether a patient would receive either TIPS alone or simultaneous TIPS and PSE after giving informed consent.

Indications for TIPS and PSE in our center were gastroesphogeal variceal bleeding and severe hypersplenism with white blood cell (WBC) counts below 2×109/L or platelet (PLT) counts below 30×109/L secondary to portal hypertension in cirrhosis, respectively. Patients with severe pulmonary hypertension(mean pulmonary artery pressure >45 mmHg) or known cardiac dysfunction such as congestive cardiac failure and severe tricuspid regurgitation[3], severely impaired liver fuction (e.g. total bilirubin above 5mg/dL, INR>2.0,current HE grade 2 or chronic HE), concomitant active infection, progressive renal failure or other hematological diseases leading to thrombocytopenia were considered unfit for this treatment[13].

After receiving TIPS, all patients were given prophylactic low molecular weight heparin 4,100 IU (GSK China investment co., LTD) Qd or Q12h subcutaneously for 5-7 days, thereafter all patients were orally given aspirin (Bayer Schering Pharma AG) 100 mg Qd or clopidogrel (Sanofi Pharma Bristol-Myers Squibb SNC) 75 mg Qd to prevent blockage of the shunt by thrombus. All patients were given oral fructose, intravenous ornithine aspartate as prophylactics for HE.

TIPS procedure

TIPS was carried out by two highly experienced interventional radiologists in our institution according to the method described by Rossle et al[14]. RUPS 100 puncture kit (Cook Inc. Bloomington, IN, USA) and ePTFE-covered stent (Fluency stent graft, 8mm×60mm, Angiomed GmbH Co.subsidiary of C.R. Bard, Inc.)were used in all patients. A stent was inserted between the right hepatic vein and right portal vein depending on anatomical conditions. Dialated collaterals including short gastric vein, gastric coronary vein were embolized with spring coils of varying diameters (35-8/5mm, 35-10/5mm, 35-6/3mm, 35-5/3mm, 35-4/3mm Cook Inc., Bloomington, IN, USA) (Figure 2A).

PSE procedure

PSE was also carried out by the same interventional radiologists, according to the method described in previous studies[8,15]. During the procedure, a 5.0-F RH or Yashiro catheter (Terumo, Tokyo, Japan) was used to demonstrate the distribution of splenic arteries and collateral circulation routes, and spring coils(18-6/2mm, 18-10/4mm, Cook Inc., Bloomington, IN, USA) were used to embolize branches of the splenic arteries with a splenic infarction ratio set at below 50% (Figure 2B).

Follow-up protocol

All patients were followed up in our center at the 1st month, 4th months, 10th months post-treatment, then at a 6-month interval or any time a patient felt unwell. During each visit, laboratory tests including complete blood count (CBC), lipid metabolism, liver, kidney and blood coagulate functions, levels of HBV-DNA or HCV-RNA, and radiologic examinations including CTPV and Collor Doppler Ultrasound(CDUS) for abdomen and TIPS were performed on each patient.

Statistical analysis

Bivariate analyses of continuous variables were performed using Student’s t-test or the Wilcoxon rank-sum test depending on the distribution. Pearson chi-square test was used for bivariate analyses of dichotomous variables. We also analyzed the overall survival and cirrhosis-related mortality with Kaplan-Meier method and compared difference by log-rank test. We performed univariate and multivariate analyses using a Cox proportional hazard model. All data are expressed as mean ± standard deviation (SD). All p values were two-sided, and a p value of <0.05 was considered to be statistically significant. All statistical analyses were performed using the SPSS package, version 13.0(SPSS Inc., Chicago, IL, USA).

Results

Subjects characteristics

The baseline data, including age, gender, etiology, levels of red blood cell(RBC) counts and hemoglobin(HGB), liver function, coagulation function, Child classification and model for end stage liver disease (MELD) scores, positivities and levels of HBV-DNA and HCV-RNA, were comparable between the two groups (P>0.05), except that patients in group B had significantly lower levels of WBC and PLT(p<0.05). (Table 1).

Changes of laboratory tests

Levels of WBC, HGB, PLT at pretreatment, at the 1st,4th, 10th month, 1.5 years, 2 years posttreatment are shown in Figure 3 a, b, and c. After the procedure, WBC, PLT counts, and HGB in group B increased significantly during the follow-up period compared to pretreatment levels (P<0.05). WBC counts in group B were similar at the 4th month (P>0.05) and higher than that of group A since the 10th month (P<0.05) forwards (Figure 3a). Despite being rising after PSE, PLT counts in group B were lower (P<0.05) than that of group A until 2 years posttreatmen (P>0.05) (Figure 3b). After the procedures, HGB levels significantly increased in both groups(p<0.05), though HGB in group B increased higher that of group A (P<0.05) (Figure 3c).

Laboratory tests, such as alanine aminotransferase (ALT), aspartate aminotransferase (AST), cholinesterase (CHE), creatine (Cr),and levels of HCV-RNA were not significantly different between the two groups or within the two groups compared to pretreatment levels at each follow-up point (P>0.05, Table 2). However, serum albumin (ALB) levels increased significantly (P<0.05)in both groups compared to pretreatment levels, and ALB levels in group B were significantly higher than that in group A at every follow-up point (P<0.05, Table 2). Total cholesterol (TC) was similar between the two groups (P>0.05), while it increased significantly (P<0.05) in group B since the 4th month forwards (Table 2).Total bilirubin(TBIL) increased significantly since the 4th month forwards in group A (P<0.05), but not in group B (P>0.05), and it remained significantly lower (P<0.05) in group B than that in group A since the 1st month forwards (Table 2). Prothrombin time (PT) increased significantly in group A (P<0.05) and it remained significantly higher than that of group B since the 4th month forwards (Table 2), though it increased in group B between the 4th and 10th month posttreatment, but normalized again since 1.5 years forwards. International normalized ratio(INR) in group A also escalated since 1st month (P<0.05) forwards, which remained significantly higher (P<0.05) than that in group B since the 10th month forwards, while it remained not significantly elevated until the 10th month posttreatment in group B (Table 2).

HBV-DNA in both groups decreased significantly since the initiation of antiviral therapy (P<0.05), and remained negative since the 4th month posttreatment in all HBV infected patients (Table 2).

Variceal bleeding and HE

Episodes of variceal bleeding in both groups reduced significantly (P<0.05) from 5.06±2.22 to 0.076±0.18 episodes per year in group A, and from 4.88±1.96 to 0.063±0.18 in group B (Figuer 4a). HE increased significantly in group A from 0.18±0.392 to 1.42±0.71 episodes per year (P<0.001), but it remained similar in group B from 0.13±0.35 to 0.38±0.52 episodes per year (P>0.05, Figure 4b).

Predictive factors for mortality

In univariate analysis, pretreatment MELD score(P=0.000), HE (P=0.000) were found to be significantly associated with overall and cirrhosis-related mortality (Table 3). In multivariate analysis, pretreatment MELD scores (P=0.000), HE (P<0.01) and group (P<0.05) were found to be independently associated with overall and cirrhosis-related mortality at month 24 (Table 3).

Overall mortality and cirrhosis-related mortality

By month 24, a total of 26 patients died of progression of hepatic cancer (n=5), sepsis (n=2), HE (n=5), hepatorenal syndrome (n=4), and liver failure (n=10), with 25 patients in group A and 1 in group B (P=0.028, Table 4). The one-year and 2-year overall survival rates were 93% and 78% in group A, 100% and 96% in group B. The mean overall survival time (SD) was 22.4 (0.38) months [95% Confidence Interval (CI): 21.6-23.1] in group A and 24.0 (0.02) months (95% CI: 23.9-24.0) in group B (P=0.032, log-rank test, Figure 5A). When only cirrhosis-related mortality was considered, mean survival time(SD) remained significantly longer in group B (Figure 5B, p = 0.042 by log-rank test).

Complications related to the interventional radiology technique

Almost all patients experienced nausea, dizziness after TIPS placement, however, severe complications such as gallbladder perforation, intraperitoneal haemorrhage, portal vein to bile duct fistula, localized collection between the gallbladder and the liver, pneumothorax, and neck haematoma, as reported in previous studies[16,17], were not observed. Following PSE, 18 patients (66.7%) had mild fever( not above 38.5℃), abdominal pain and vomiting. No patients suffered splenic abscess, splenic rupture,pneumonia, refractory ascites, pleural effusions and gastrointestinal bleeding, as reported in previous studies[18,19]. Patients in group B had similar hospital stays to that of group A (P>0.05, Table 4) in spite of additional intervention.

Discussion

Portal hypertension is the most common complication of chronic liver disease. It is responsible for the development of gastroesophageal varices, ascites, hepatorenal syndrome, bacterial infection, HE and hypersplenism, which are the main causes for the morbidity and mortality of liver cirrhosis[20].

TIPS has been well documented in the treatment of esophagogastric variceal bleeding due to portal hypertension in cirrhosis[3,21]. Consistent with these studies, variceal bleeding in our study decreased significantly in all patients receiving TIPS. Despite PSE being reported as efficacious in reducing variceal bleeding[8] by reducing portal venous flow and pressure, combined therapy using TIPS and PSE in our study did not achieve significantly more reduced variceal bleeding compared to that of patients receiving TIPS alone, which might be related to the already very low bleeding frequencies obtained by creation of TIPS.

HE is a very common complication in patients after TIPS procedure. 20-31% of the patients who undergo a TIPS procedure would demonstrate new or worsening incidence of HE after TIPS[1].Consistent with this report, patients receiving TIPS alone in our study had significantly elevated frequencies of HE. Hiroshi Yoshida et al[12] reported that PSE following obliteration of portal-systemic shunt reduces serum ammonia levels, and improves portal systemic encephalopathy, which might explain the result observed in our study that HE in group B did not worsen significantly, and was significantly lower than that of group A.

Previous studies[6,19] demonstrated that WBC and PLT counts after PSE increased significantly than those before PSE. Consistent with these findings, patients receiving TIPS and PSE in our study had significantly increased WBC and PLT counts. Our study also showed increased levels of HGB in both groups, with patients receiving combined therapy of TIPS and PSE having higher HGB levels, which may be related to reduced blood loss obtained by TIPS and reduced intrasplenic destruction of RBC obtained by PSE. Bernd Saugel et al[22] reported that the TIPS procedure led to a significant increase in serum bilirubin level, ALT and AST levels, and INR level as well. Earlier studies[23,24] reported that TIPS can result in a deterioration of the liver function in the form of elevation of bilirubin, ALT and AST, probably due to reduction of hepatic blood flow and sinusoidal blood flow resulting from diversion of portal blood through a TIPS, which is even more obvious in patients with advanced liver disease due to incomplete hepatic artery buffer response[25]. Compatible with these studies, our study showed that TBIL, PT, INR, and ALT and AST levels had significantly increased after TIPS in group A, but ALT and AST levels normalized by the 1st month posttreatment. Previous study[11] demonstrated that PSE has beneficial effects on liver function, enhancing hepatic protin synthesis capacity. The mechanism of improved liver function following PSE could be attributed to hemodynamic changes after PSE, which reduces portal venous flow, leading to a compensatory increase of blood flow in hepatic artery and superior mesenteric artery and vein[26,27]. This hemodynamic change may result in more nutritious blood flow to the liver, and may improve liver function and induce liver regeneration in cirrhotics[28,29]. Thus, we speculate that reduced HE may also be related to improved liver function following hemodynamic change brought on by PSE.

Regarding the effects of TIPS on survival, previous studies showed conflicting results. In two studies[30,31], survival was found to be higher after TIPS, while two other studies failed to show any difference[32,33]. Garcı´a-Paga´n et al[2] reported that early ePTFE-covered TIPS in highly selected patients with cirrhosis and acute variceal bleeding was associated with significant reductions in treatment failure and mortality. Our study demonstrated that combined therapy using TIPS and PSE was also associated with significant reductions in overall and cirrhosis-related mortality compared to TIPS alone, which may be attributed to reduced HE, improved liver function following combined PSE.

Michael Malinchoc et al[34] reported that serum concentrations of bilirubin and Cr, INR, and the cause of the underlying liver disease were predictors of survival in patients undergoing elective TIPS, either for prevention of variceal rebleeding or for treatment of refractory ascites. In our study, Cox proportional-hazards regression showed that pretreatment MELD score, HE and group were independent predictors for cirrhosis-related mortality.

Our study was a retrospective study and had a few limitations. First, the number of patients in group B was relatively small. Second, the treatment assignment was not done by randomization,which seems impossible in real clinical practice,since TIPS is a very costly and complicated procedure and addition of PSE increases the cost and risk. Thus, there were some differences in the baseline characteristics of patients in two groups.

In conclusion, our study showed that simultaneous combined TIPS and PSE regimen improves hematologic parameters, prevents deterioration of liver function and coagulation function, reduces variceal bleeding and HE, thus reduces mortality.

CONFLICT OF INTERESTS

The authors declare that they do not have conflict of interests.

REFERENCES

1Boyer TD, Haskal ZJ. The role of transjugular intrahepatic portosystemic shunt (TIPS) in the management of portal hypertension: update 2009. Hepatology 2010; 51: 306.

2García-Pagán JC, Caca K, Bureau C, Laleman W, Appenrodt B, Luca A, Abraldes JG, Nevens F, Vinel JP, Mössner J, Bosch J; Early TIPS (Transjugular Intrahepatic Portosystemic Shunt) Cooperative Study Group. Early use of TIPS in patients with cirrhosis and variceal bleeding. N Engl J Med 2010; 362(25): 2370–2379.

3Boyer TD, Haskal ZJ. The role of transjugular intrahepatic portosystemic shunt in the management of portal hypertension. Hepatology 2005; 41: 386–400.

4Patel N. Transjugular intrahepatic portosystemic shunt. In: Patel NH, Haskal ZJ, Kerlan RK Jr, eds. Portal hypertension diagnosis and intervention. 2nd ed. Fairfax, Va: Society of Cardiovascular and Interventional Radiology 2001; 31-36.

5Sangro B1, Bilbao I, Herrero I, Corella C, Longo J, Beloqui O, Ruiz J, Zozaya JM, Quiroga J, Prieto J. Partial splenic embolization for the treatment of hypersplenism in cirrhosis. Hepatology 1993; 18: 309–14.

6He XH, Gu JJ, Li WT, Peng WJ, Li GD, Wang SP, Xu LC, Ji J. Comparison of total splenic artery embolization and partial splenic embolization for hypersplenism. World J Gastroenterol 2012; 18(24): 3138-3144.

7Liu Q, Song Y, Xu X, Jin Z, Duan W, Zhou N. Management of Bleeding Gastric Varices in Patients with Sinistral Portal Hypertension. Dig Dis Sci 2014; 59: 1625–1629.

8Senthilkumar Sankararaman, Sujithra Velayuthan, Romulo Vea, John Herbst. Severe gastric variceal bleeding successfully treated by emergency splenic artery embolization. Pediatrics International 2013; 55: e42–e45.

9N’Kontchou G1, Seror O, Bourcier V, Mohand D, Ajavon Y, Castera L, Grando-Lemaire V, Ganne-Carrie N, Sellier N, Trinchet JC, Beaugrand M. Partial splenic embolization in patients with cirrhosis: efficacy, tolerance and long-term outcome in 32 patients. Eur J Gastroenterol Hepatol 2005; 17: 179-84.

10Halle´n M, Forsberg AM, Alwmark A. Partial splenic embolization: long-term outcome. Langenbecks Arch Surg 2003; 387:421-6.

11Takashi Tajiri, Masahiko Onda,Hiroshi Yoshida, Yasuhiro Mamada. long-term hematological and biochemical effects of parial splenic embolization in hepatic cirrhosis. Hepatogastroenterology 2002; 49: 1445-1448.

12Hiroshi Yoshida,Yasuhiro Mamada, Nobuhiko Taniai, Kazuhito Yamamoto, et al. Long term results of partial splenic artery embolization as supplemental treatment for portosystemic encephalopathy. Am J Gastroenterol 2005; 100: 43-47.

13Krajina A, Hulek P, Fejfar T, Valek V. Quality improvement guidelines for Transjugular Intrahepatic Portosystemic Shunt (TIPS). Cardiovasc Intervent Radiol 2012; 35(6): 1295-1300.

14Ochs A, Rössle M, Haag K, Hauenstein KH, Deibert P, Siegerstetter V, Huonker M, Langer M, Blum HE. The transjugular intrahepatic portosystemic stent-shunt procedure for variceal bleeding. N Engl J Med 1994; 330: 165-71.

15Secil Omer,Octavian Zara, Claudia Iacobescu, Ion Dina. Partial Splenic Embolization for Hypersplenism in Cirrhotic Patients. A Case Series. J Gastrointestin Liver Dis 2014; 23: 215-218.

16Murphy KD, Shirodkar NP, Joiner DR, Adrian EA. Portal vein bifurcation and its relevance to transjugular intrahepatic portosystemic shunts. J Interv Radiol 1998; 13: 83–88.

17Rossle M, Siegerstetter V, Huber M, Ochs A. The first decade of the transjugular intrahepatic portosystemic shunt (TIPS): state of the art. Liver 1998; 18: 73–89.

18Hayashi H, Beppu T, Okabe K, Masuda T, Okabe H, Baba H. Risk factors for complications after partial splenic emboliza¬tion for liver cirrhosis. Br J Surg 2008; 95: 744-750.

19Zhu K, Meng X, Qian J, Huang M, Li Z, Guan S, Jiang Z, Shan H. Partial splenic embolization for hypersplenism in cirrhosis: a long-term outcome in 62 patients. Dig Liver Dis 2009; 41: 411-416.

20Bernhard Angermayr. Transjugular intrahepatic portosystemic shunt-current status in 2011. Acta Gastroenterol Belg 2011; 74: 553-559.

21Garcia-Tsao G, Sanyal AJ, Grace ND, Carey W; Practice Guidelines Committee of the American Association for the Study of Liver Diseases; Practice Parameters Committee of the American College of Gastroenterology. Prevention and management of gastroesophageal varices and variceal hemorrhage in cirrhosis. Hepatology 2007; 46(3): 922–938.

22Saugel B, Phillip V, Gaa J, Berger H, Lersch C, Schultheiss C, Thies P, Schneider H, Höllthaler J, Herrmann A, Schmid RM, Huber W. Advanced Hemodynamic Monitoring before and after Transjugular Intrahepatic Portosystemic Shunt:Implications for Selection of Patients—A Prospective Study. Radiology 2012; 262(1): 343-351.

23Jalan R, Gooday R, O’Carroll RE, Redhead DN, Elton RA, Hayes PC. A prospective evaluation of changes in neuropsychological and liver function tests following transjugular intrahepatic portosystemic stent-shunt. J Hepatol 1995; 23: 697–705.

24Lotterer E, Wengert A, Fleig WE. Transjugular intrahepatic portosystemic shunt: short-term and long-term effects on hepatic and systemic hemodynamics in patients with cirrhosis. Hepatology 1999; 29: 632-639.

25Gulberg V, Haag K, Rossle M, Gerbes AL. Hepatic arterial buffer response in patients with advanced cirrhosis. Hepatology 2002; 35: 630–634.

26Nishida O, Moriyasu F, Nakamuru T, Ban N, Tamada T, Kawasaki T, Uchino H. Interrelationship between splenic and superior mesenteric venous circulation manifested by transient splenic arterial occlusion using a balloon catheter. Hepatology 1987; 7: 442-446.

27Porter BA, Frey CF, Link DP, Lantz BMT, Pimstone NR. Splenic embolization monitored by video dilution technique. AJR Am J Roentgenol 1983; 41: 1063-1065.

28Hidaka H,Kokubu S,Saigenji K,Isobe Y,Maeda T. Restoration of thrombopoietin producion after partial splenic embolization leads to resolution of thrombocytopenia in liver cirrhosis. Hepatol Res 2002; 23: 265-273.

29Quanda Liu, Kuansheng Ma, Yang Song, Ningxin Zhou, and Zhenping He. Two-year follow-up of splenic radiofrequency ablation in patients with cirrhotic hypersplenism: Does increased hepatic arterial flow induce liver regeneration? Surgery 2008; 143: 509-18.

30Rossle M, Ochs A, Gulberg V, Siegerstetter V, Holl J, Deibert P, Olschewski M, Reiser M, Gerbes AL. A comparison of paracentesis and transjugular intrahepatic portosystemic shunting in patients with ascites. N Engl J Med 2000; 342: 1701-1707.

31Salerno F, Merli M, Riggio O, Cazzaniga M, Valeriano V, Pozzi M, Nicolini A, Salvatori F. Randomized controlled study of TIPS versus paracentesis plus albumin in cirrhosis with severe ascites. Hepatology 2004; 40: 629–635.

32Escorsell A, Bañares R, García-Pagán JC, Gilabert R, Moitinho E, Piqueras B, Bru C, Echenagusia A, Granados A, Bosch J. TIPS versus drug therapy in preventing variceal rebleeding in advanced cirrhosis: a randomized controlled trial. Hepatology 2002; 35: 385-392.

33Sanyal AJ, Genning C, Reddy KR, Wong F, Kowdley KV, Benner K, McCashland T; North American Study for the Treatment of Refractory Ascites Group. The North American study for the treatment of refractory ascites. Gastroenterology 2003; 124: 634-641.

34Malinchoc M, Kamath PS, Gordon FD, Peine CJ, Rank J, ter Borg PC. A Model to Predict Poor Survival in Patients Undergoing Transjugular Intrahepatic Portosystemic Shunts. Hepatology 2000; 31(4): 864-871.

Peer reviewer:Akira Yagi, PhD, Emeritus Professor, Fukuyama University, Japan.

Refbacks

  • There are currently no refbacks.


Creative Commons License
This work is licensed under a Creative Commons Attribution 3.0 License.