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Efficacy of Balloon-occluded Retrograde Transvenous Obliteration of Large Spontaneous Lienorenal Shunt in Patients with Severe Recurrent Hepatic Encephalopathy with Foam Sclerotherapy: Initial Experience
CLINICAL STUDY
Efficacy of Balloon-occluded Retrograde Transvenous Obliteration of Large Spontaneous Lienorenal Shunt in Patients with Severe Recurrent Hepatic Encephalopathy with Foam Sclerotherapy: Initial Experience Amar Mukund, MD, S. Rajesh, MD, Ankur Arora, MD, DNB, FRCR, Yashwant Patidar, MD, Deepak Jain, FRCR, and Shiv K. Sarin, MD, DM
ABSTRACT Purpose: Balloon-occluded retrograde transvenous obliteration (BRTO) is a widely accepted treatment for gastric varices, but data are limited in regard to its role in the management of hepatic encephalopathy (HE). This study evaluated the efficacy of BRTO with foam sclerotherapy in the management of HE arising as a result of spontaneous large portosystemic shunts. Materials and Methods: Eight sessions of BRTO with sodium tetradecyl sulfate foam were performed in seven patients with cirrhosis complicated by HE. All patients had portosystemic communication (ie, gastro-/lienorenal shunt) on preprocedure computed tomography. Clinical and laboratory parameters including arterial ammonia level were evaluated in all patients before and after the procedure. Results: Technical success rates were 86% (six of seven) for the first BRTO session and 100% (one of one) for the second. Follow-up imaging revealed complete obliteration of the varices in five of seven patients (71%) and partial obliteration in the remaining two. Immediate clinical improvement of HE was observed in six of seven patients (86%), with postprocedural decrease in arterial ammonia levels; one patient showed delayed improvement. Procedure-related complications (eg, abnormal liver function test results, acute kidney injury with leukocytosis) were encountered in two patients. All patients showed clinical and symptomatic improvement at the time of discharge and during a follow-up of 4 months (with visits at 1 mo and 3 mo later). Conclusions: Initial experience suggests that BRTO is an effective procedure in the management of HE arising as a result of large portosystemic shunts.
ABBREVIATIONS BRTO ⫽ balloon-occluded retrograde transvenous obliteration, HE ⫽ hepatic encephalopathy, STS ⫽ sodium tetradecyl sulfate
Hepatic encephalopathy (HE) is an important cause of morbidity in patients with cirrhosis. Encephalopathy in cirrhosis can be of two types: portal systemic encephalop-
From the Departments of Radiology/Interventional Radiology (A.M., S.R., A.A., Y.P., D.J.) and Hepatology (S.K.S.), Institute of Liver and Biliary Sciences, D1, Vasant Kunj, New Delhi 110070, India. Received January 28, 2012; final revision received May 11, 2012; accepted May 14, 2012. Address correspondence to A.M.; E-mail: [email protected] None of the authors have identified a conflict of interest. © SIR, 2012 J Vasc Interv Radiol 2012; 23:1200–1206 http://dx.doi.org/10.1016/j.jvir.2012.05.046
athy and end-stage encephalopathy (1). Portal systemic encephalopathy is caused by shunting of blood flow from supramesenteric veins to systemic veins, leading to high systemic blood ammonia levels (2). Thus occlusion of these shunts helps in counteracting encephalopathy (3). Balloonoccluded retrograde transvenous obliteration (BRTO) is an endovascular interventional procedure originally described for the management of bleeding gastric varices and HE in patients with cirrhosis (4). The technique involves occlusion of the efferent veins of a portosystemic shunt by using a balloon catheter followed by injection of a sclerosing agent (4 – 6). Since the introduction of the technique in the 1990s, several studies have reported satisfactory results of BRTO in the management of bleeding gastric varices, and
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talizations (at least three) were required within the 6-month period before the procedure. They showed a poor response to medical management for encephalopathy consisting of L-ornithine and L-aspartate infusion combined with oral lactulose during inpatient periods and oral lactulose during outpatient periods. During each hospitalization, each patient had grade III HE per West Haven criteria; however, before the procedure, only five patients had grade III HE and the other two had grade II HE. The indications for BRTO in the remaining two patients were acute variceal bleeding and shunt myelopathy; these patients were excluded from the study. Demographic and clinical profiles of the subjects are shown in Table 1. All patients were male, ranging in age from 45 to 67 years (mean, 56 y). The mean diameter of the lienorenal shunt based on preprocedural CT was 15 mm (range, 10 –20 mm).
Procedure Technique Figure 1. Coronal reformatted CT image shows a large gastrorenal shunt (arrowheads) and perigastric varices (arrows).
it is commonly used in Japan (7–11). However, it is still not widely practiced in other countries, and its role in management of HE needs to be validated by larger studies. This retrospective single-center study was done to assess the efficacy of BRTO in the management of HE.
MATERIALS AND METHODS A retrospective analysis was done for all BRTO procedures performed at a single institution from July to December 2011. In view of the retrospective nature of the study, institutional review board approval was not required per our institution’s policy.
Patients and Procedure Indications A total of 11 BRTO sessions were carried out in nine patients with hepatic cirrhosis and portal hypertension. All these patients had portosystemic communication with a caliber greater than 1 cm in the form of a gastro-/lienorenal shunt, which were defined as large portosystemic shunts. These shunts were seen to continue as dilated and tortuous perigastric and lienorenal varices on preprocedural contrast-enhanced computed tomography (CT; Fig 1). All procedures were performed in the interventional wing of the radiology department by A.M. (n ⫽ 10) or D.J. (n ⫽ 1), who have 7 and 9 years of experience in interventional radiology, respectively. Inclusion criteria for the study were (i) cirrhosis with recurrent severe encephalopathy and a documented large portosystemic shunt and (ii) no response to medical management. Patients who did not fulfill these criteria were excluded. Seven of nine patients who underwent BRTO had recurrent severe encephalopathy for which multiple hospi-
The procedure was performed under local anesthesia or conscious sedation. After written informed consent was obtained, the right internal jugular vein (n ⫽ 7) or right common femoral vein (n ⫽ 1) was accessed and a 6-F vascular access sheath (Cook, Bloomington, Indiana) was placed. Subsequently, selective cannulation of the left renal vein was performed with use of a 5-F angiographic catheter (C2; Cook), which was then replaced with a flexible straight or curved sheath (9, 10, or 12 F; 45, 75, or 80 cm length; Flexor Check-Flo Introducer with large valve assembly, Mullin design, and Ansel modification; Cook). After this long sheath had been placed, a 4-F angled or curved glide catheter (MPA/C2 Slip-Cath; Cook) was used to cannulate the shunt. Gradually, the catheter was advanced deep within the varix. Later, the glide catheter was replaced with a balloon catheter over a stiff guide wire (AES; Cook). The size of the balloon was kept 1–2 mm larger than the diameter of the gastro-/lienorenal shunt and varied from 10 to 22 mm. Although the balloon was slightly oversized, complete occlusion of the shunt was confirmed before the sclerosant agent was injected by injecting contrast medium after inflating the balloon. The use of a compliant occlusion balloon would have been appropriate in these cases, but because such balloon catheters were not available, we had to use noncompliant balloon catheters. Rival balloon catheters (Bard Peripheral Vascular, Tempe, Arizona) were used for shunts as large as 10 mm in caliber, and Atlas balloon catheters (Bard Peripheral Vascular) were used for shunts larger than 10 mm. The Rival balloon was preferred because of its better trackability, but it is not available in sizes larger than 10 mm in diameter. The balloon was positioned proximally within the shunt, as the aim of the procedure was to occlude the shunt and prevent portosystemic mixing of blood. The sclerosing agent, in the form of a foam, was then prepared by mixing air, 3% sodium tetradecyl sulphate (STS; SETROL; Samarth Life Sciences, Mumbai, India), and lipiodol in a 3:2:1 ratio. The sclerosing agent was infused with the goal of filling the full extent of varices (Fig 2). The injection endpoint was defined as
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Table 1. Details of Demographic Data, Disease and Treatment Characteristics, and Complications Disease Score Pt. No./Age (y) 1/63 2/67 3/47 4/62 5/60 6/52 7/57
Child-Pugh 6 7 11 11 10 11 12
MELD 13 14 20 12 24 20 17
Etiology of Cirrhosis NASH NASH Hepatitis B Cryptogenic Cryptogenic Alcoholic Alcoholic
STS Volume Used (mL) 14 10 20 16 20 18 18
Observation Period (d) 180 150 150 150 120 120 120
Complications per SIR Criteria None None None Grade D Grade D None None
Hospital Stay (d) 2 3 2 12 8 2 2
All patients were male. MELD ⫽ Model for End-stage Liver Disease, NASH ⫽ nonalcoholic steatohepatitis, STS ⫽ sodium tetradecyl sulfate.
Figure 2. (a) Abdominal radiograph during the procedure displays stasis of sclerosant mixture within the gastrorenal shunt and perigastric varix (arrows). (b) Radiograph at 3-month follow-up shows retained sclerosant mixture within the same varix (arrows).
(i) complete filling of the varix with the sclerosant mixture as seen on fluoroscopy and cone-beam CT (BRANSIST saphire; Shimadzu, Kyoto, Japan) or (ii) administration of the maximum permissible dose of STS (600 mg) per the available literature (12). After infusion of the sclerosing agent, the balloon was kept inflated for 6 hours. During this period, the patient was kept in the angiography suite or in the recovery area beside the angiography suite, and regular monitoring for stasis of the sclerosant mixture was performed every 30 minutes by fluoroscopy. After 6 hours of balloon inflation, contrast venography through the balloon catheter was performed, and lack of contrast opacification coupled with visible stasis of the sclerosant mixture within the varix was considered to represent complete closure of the shunt and varix. In two cases, the procedure was started in the late afternoon, and, because prothrombin time and platelet counts were normal, the check venogram for confirmation of occlusion was attempted at 4 hours, which confirmed closure of the varix. When no contrast agent flow could be demonstrated within the varix with retained sclerosant mixture, the balloon catheter was deflated and removed. Arterial ammonia levels were measured before and
after the procedure (within 24 – 48 h after shunt closure) in all patients, along with detailed clinical and laboratory investigations. These investigations included postprocedural grading of encephalopathy, liver function tests, renal function tests, and complete blood count throughout the hospital stay (Tables 2 and 3). Postprocedural follow-up imaging at 24 – 48 hours was done with fluoroscopy (Fig 2) to assess for stasis of the sclerosant mixture. Thereafter, regular clinical and imaging follow-up was scheduled and consisted of a visit to the follow-up clinic of the hepatologist and multiphasic CT at 1 month and 4 months (Fig 3). Although contrast-enhanced CT is superior to Doppler ultrasound (US) for documenting the closure of varices, we refrained from the use of iodinated contrast media in patients with decreased renal function. In such patients, Doppler US with bowel preparation was performed to look for any evidence of residual or recanalized lieno-/gastrorenal shunt. This was combined with abdominal radiography to document retained lipiodol within the shunt and varix. If slightest of suspicion was raised on Doppler US regarding a residual/recanalized shunt, CT was planned and performed after stabilization of renal function (Fig 4).
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Table 2. Laboratory Test Results before and after Treatment Total Bilirubin (mg/dL)
Serum Albumin (g/dL)
INR*
Serum Creatinine (mg/dL)
Postprocedure Postprocedure Postprocedure Postprocedure Pt. No. Preprocedure 2 d 1 mo 4 mo Preprocedure 2 d 1 mo 4 mo Preprocedure 2 d 1 mo 4 mo Preprocedure 2 d 1 mo 4 mo 1 2.5 2.2 2.3 1.8 3.1 2.3 3.1 3.0 1.2 1.4 1.2 1.0 0.8 0.8 0.6 0.8 2 2.1 2.7 1.8 2.0 2.9 2.0 2.8 3.0 1.1 1.0 1.1 1.0 0.4 0.1 0.2 0.1 3 1.2 1.1 1.4 0.9 2.5 1.2 2.1 2.8 1.3 1.8 1.4 1.6 1.1 1.2 1.0 0.8 4 3.1 5.4 2.8 3.8 2.4 1.5 2.0 2.1 1.7 2.9 1.8 2.4 0.7 1.6 1.0 0.8 5 1.4 6.7 2.3 1.8 2.3 2.2 2.2 2.4 1.4 1.6 1.4 1.2 0.8 1.4 0.9 1.0 6 4.2 4.1 3.9 3.0 2.9 3.0 3.1 3.4 1.4 1.2 1.0 1.1 0.9 0.7 0.7 0.9 7 4.4 4.7 4.0 3.8 3.0 2.7 2.4 3.0 1.9 2.2 2.8 2.4 0.8 0.9 0.6 0.4 INR ⫽ international normalized ratio.
Table 3. Plasma Ammonia Levels and Hepatic Encephalopathy Grades before and after Treatment Plasma Ammonia (g/dL)
Hepatic Encephalopathy Grade† After Procedure
Pt. No. 1 2 3 4 5 6 7
Before Procedure 147 244 301 184 166 180 139
After Procedure* 86 73 97 78 143 123 87
Shunt Occlusion Complete Complete Complete Partial Complete Partial Complete
Before Procedure II II III III III III III
24 – 48 h I I I I III II I
1 mo Resolved Resolved Resolved Resolved I I Resolved
4 mo Resolved Resolved Resolved Resolved I Resolved Resolved
* At 24 – 48 h after the procedure. † Per West Haven criteria.
Statistical Analysis Statistical analysis was performed by using a paired t test for arterial ammonia levels before and after the procedure in each patient. A P value lower than .05 was considered statistically significant. Commercially available software (SPSS version 17; SPSS, Chicago, Illinois) was used to perform calculations.
RESULTS Technical Success BRTO was performed once in each of six patients and twice in one patient. Technical success rates were 86% (six of sessions) for the first session and 100% (one of one) for the second. The only case of failure was secondary to inability to catheterize and occlude the shunt as a result of extreme tortuosity of the varix. The procedure was performed successfully the next day with the use of a Flexor Check-Flo introducer with an Ansel modification in place of the Flexor Check-Flo introducer with a Mullin design. Two patients had only partial obliteration of the lienorenal shunt as a result of exceedingly tortuous varices of varying caliber,
which possibly led to ineffective occlusion of the varix by the balloon catheter, resulting in partial runoff of the sclerosant mixture. Procedure times ranged from 45 to 120 minutes, with 15– 40 minutes of fluoroscopy time required to cannulate the shunt and reach deep within the varix to place the balloon, depending on the tortuosity of the varices. Thereafter, the balloon was kept inflated for the next 4 – 6 hours. The injected dose of STS ranged from 300 to 600 mg (mean, 480 mg). The mean total volume of STS was 16 mL (range, 10 –20 mL; Table 1), and that of the sclerosing mixture (ie, foam) used was 56 mL (range, 35–70 mL). Technical success was defined as successful administration of sclerosing agent within the shunt and associated varix after placement of the occlusion balloon within the shunt, leading to closure of the varix.
Follow-up Clinical and radiologic follow-up was available for all patients. Follow-up imaging revealed complete obliteration of varix in five of the seven patients, whereas incomplete closure of the shunt was seen in two (Table 3) with partial
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hypernatremia, acute kidney injury, and leukocytosis after the procedure, which was managed with free water replacement, terlipressin, and antibiotic therapy.
DISCUSSION
Figure 3. Coronal reformatted postprocedural (1 mo) CT image shows obliteration of shunt with retained sclerosing agent within the shunt and varix (arrows).
obliteration (approximately 75%) on follow-up imaging at 1 month (Fig 4). Clinically, there was remarkable improvement in the symptoms of HE within 24 – 48 hours of the procedure in all but one patient (decreased grade of encephalopathy; Table 3). However, this patient showed significant clinical improvement in terms of features of HE as well as arterial ammonia levels at 1 month and subsequently at 3 months. Arterial ammonia levels decreased from 220 g/dL ⫾ 81 to 108 g/dL ⫾ 35 (Table 3), which was statistically significant (P ⬍ .05). Even in patients with only partial obliteration of the shunt, the clinical results were comparable to those in the rest of the patients. BRTO did not show any significant effect on liver and kidney functions, including serum bilirubin, albumin, and creatinine levels, and prothrombin time (Table 2), except in two cases that showed immediate postprocedural deterioration in liver and kidney functions.
Complications and Hospital Stay Median hospital stay was 2 days (range, 2–12 d; Table 1). Complications were observed in 29% of patients (n ⫽ 2; Table 1). One of these was a 62-year-old man with cryptogenic cirrhosis complicated by portal hypertension and ascites. He had a history of multiple (n ⫽ 6 –7) episodes of encephalopathy in the previous 1 year requiring multiple hospital admissions. Also significant was the history of left-sided hemiparesis (right basal ganglia hemorrhage) 3 months before BRTO. After the procedure, this patient developed gradual deterioration of hepatic and renal functions, with increasing total leucocyte count. He was administered antibiotic therapy and albumin and recovered gradually in 4 –5 days. He later showed improvement in symptoms of HE on follow-up. Another patient developed
HE is a neuropsychiatric disorder characterized by altered level of consciousness, irritability, inverted sleep/wake pattern, and fluctuating neurologic signs. Important factors in its pathogenesis are severe hepatic dysfunction and shunting of portal venous blood into the systemic circulation so that toxic substances absorbed from the intestine are not detoxified by the liver, leading to metabolic abnormalities in brain. Ammonia is the substance most often incriminated in the pathogenesis of encephalopathy (2). Many, but not all, patients with HE have elevated blood ammonia levels, and recovery from encephalopathy is often accompanied by declining blood ammonia levels (2). The diagnosis of HE is usually one of exclusion. There are no specific diagnostic liver function test abnormalities, although an elevated arterial ammonia level in the appropriate clinical setting is highly suggestive of the diagnosis (2). Severe HE can adversely affect the patient’s quality of life, and its early recognition and management is important (13). In cases that are refractory to medical treatment, BRTO of spontaneous portosystemic shunt is an alternative. BRTO was first described by Kanagawa et al (4) as an endovascular interventional procedure for control of bleeding varices. In recent years, BRTO has been preferred over surgical treatment as a therapy for chronic recurrent HE on account of its reliability and minimal invasiveness (14 –21). The goal of BRTO is to close a large shunt between the portal and systemic circulation. It involves use of an appropriately sized balloon catheter into the efferent vein of a large spontaneous portosystemic shunt to occlude it. After blockade of blood flow is confirmed by injection of contrast media, a sclerosing agent is hand-injected slowly under fluoroscopic guidance. The amount of sclerosing agent needed varies according to the diameter and length of the varix. Detergent-based chemicals in liquid or foam forms have been used as sclerosing agents (22,23). The sclerosing agent used in the present study was STS foam. STS is an anionic surfactant available as a sterile nonpyrogenic solution for intravenous use as a sclerosing agent. Its action is on the lipid molecules in the endothelium, causing intimal inflammation and thrombus formation (22,23). This usually occludes the injected vein. Subsequent formation of fibrous tissue results in partial or complete obliteration of the vein (24). The present study shows that BRTO with STS foam is an effective procedure for obliteration of gastro-/lienorenal shunts with a remarkably good success rate (87%), resulting in significant improvement in the clinical symptoms of HE in these patients. These shunt closure results are in concordance with the observations of Sabri et al (12), who reported a success rate of 91% in their study. Even in patients
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Figure 4. (arrows).
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(a, b) Coronal reformatted pre- and postprocedural contrast-enhanced CT images show partial obliteration of shunt
with partial obliteration of varices, the clinical results were highly satisfactory. Obliteration of major spontaneous portosystemic shunt by BRTO increases portal hepatic blood flow, resulting in improvement in hepatic function and enhanced ammonia detoxification by liver (18,25,26). Although this has been attributed to be the major factor contributing to the therapeutic effect of BRTO on HE, elevation of portal venous pressure can aggravate complications of portal hypertension, including worsening of esophageal varices, ascites, splenomegaly, and gallbladder wall edema (27,28). The present study demonstrates that BRTO had no significant long-term effects on liver or renal function in a small population. The incidence of complications in the present study was 29% (two of seven patients). Both patients began to experience acute renal dysfunction within 48 hours of the procedure. In addition, they also developed fever with increasing leucocyte counts, consistent with bacteremia, which resolved with antibiotic therapy. This is in agreement with the report of Sabri et al (12), who observed a complication rate of 14%, which included portal vein thrombosis caused by sclerosant agent leakage and transient bacteremia. However, in the present study, no overt complications related to leakage of sclerosing agent were seen. The reason for deterioration of hepatic function in one patients is unknown. Although the results of the present study appear promising, the retrospective nature, combined with a small sample size, limited follow-up, and lack of postprocedural portal pressure measurements and endoscopic findings, are some limitations. Long-term follow-up is needed to document the incidence of relapse in the study population and the effect of BRTO on esophageal variceal status and ascites. In conclusion, although the long-term outcome and complications remain to be seen, our initial experience with BRTO of lienorenal shunt, whether complete or partial,
suggests good clinical outcomes in terms of chronic recurrent HE.
REFERENCES 1. Sherlock S. Hepatic cirrhosis. Diseases of the liver and biliary system (eighth edition). London: Blackwell, 1989; 410 – 424. 2. Chung RT, Podolsky DK. Cirrhosis and its complications. In: Kasper DL, Braunwald E, Fauci AS, Hauser SL, Longo DL, Jameson JL. Harrison’s principles of internal medicine, 16th ed. New York: McGraw-Hill, 2005; 1867–1869. 3. Kato T, Uematu T, Nishigaki Y, et al: Therapeutic effect of balloonoccluded retrograde transvenous obliteration on portal-systemic encephalopathy in patients with liver cirrhosis. Intern Med 2001; 40:688 – 691. 4. Kanagawa H, Mima S, Kouyama H, Gotoh K, Uchida T, Okuda K. Treatment of gastric fundal varices by balloon-occluded retrograde transvenous obliteration. J Gastroenterol Hepatol 1996; 11:51–58. 5. Chikamori F, Shibuya S, Takase Y, Ozaki A, Fukao K. Transjugular retrograde obliteration for gastric varices. Abdom Imaging 1996; 21:299 – 303. 6. Hiraga N, Aikata H, Takaki S, et al. The long-term outcome of patients with bleeding gastric varices after balloon-occluded retrograde transvenous obliteration. J Gastroenterol 2007; 42:663– 672. 7. Kawanaka H, Ohta M, Hashizume M, et al. Portosystemic encephalopathy treated with balloon-occluded retrograde transvenous obliteration. Am J Gastroenterol 1995; 90:508 –510. 8. Hirota S, Matsumoto S, Tomita M, Sako M, Kono M. Retrograde transvenous obliteration of gastric varices. Radiology 1999; 211:349 –356. 9. Koito K, Namieno T, Nagakawa T, Morita K. Balloon-occluded retrograde transvenous obliteration for gastric varices with lienorenal or gastrocaval collaterals. AJR Am J Roentgenol 1996; 167:1317–1320. 10. Hayashi S, Saeki S, Hosoi H, et al. A clinical and portal hemodynamic analysis for obliteration of gastric-renal shunt communicated with gastric fundal varices. Jpn J Gastroenterol 1998; 95:755–763. 11. Matsumoto A, Hamamoto N, Nomura T, et al. Balloon-occluded transvenous retrograde obliteration of high risk gastric fundal varices. Am J Gastroenterol 1999; 94:643– 649. 12. Sabri SS, Swee W, Turba UC, et al. Bleeding gastric varices obliteration with balloon-occluded retrograde transvenous obliteration using sodium tetradecyl sulfate foam. J Vasc Interv Radiol 2011; 22:309 –316. 13. Takashimizu S, Watanabe N, Kojima S, et al. Efficacy of balloon occluded retrograde transvenous obliteration (B-RTO) performed in a patient with primary biliary cirrhosis with severe recurrent hepatic encephalopathy due to splenorenal shunt. Tokai J Exp Clin Med 2007; 32:70 –74.
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14. Fukuda T, Hirota S, Sugimura K. Long-term results of balloon-occluded retrograde transvenous obliteration for the treatment of gastric varices and hepatic encephalopathy. J Vasc Interv Radiol 2001; 12:327–336. 15. Sherif SH, Robert SS, J. Michael H, et al. Reversal of hepatic encephalopathy after occlusion of total portosystemic shunts. Am J Surg 1981; 142:285–289. 16. Kato T, Uematu T, Nishigaki Y, et al. Therapeutic effect of balloonoccluded retrograde transvenous obliteration on portal-systemic encephalopathy in patients with liver cirrhosis. Intern Med 2001; 40:688 – 691. 17. Cardoso J, Gautreau C, Jeyaraji PR, et al. Augmentation of portal blood flow improves function of human cirrhotic liver. Hepatology 1994; 19: 375–380. 18. Miyamoto Y, Oho K, Kumamoto M, et al. Balloon-occluded retrograde transvenous obliteration improves liver function in patients with cirrhosis and portal hypertension. J Gastroenterol Hepatol 2003; 18:934 –942. 19. Hashimoto N, Akahoshi T, Shoji T, et al. Successful treatment for hepatic encephalopathy aggravated by portal vein thrombosis with balloon-occluded retrograde transvenous obliteration. Case Rep Gastroenterol 2011; 5:366 –371. 20. Hiraoka A, Kurose K, Hamada M, et al. Hepatic encephalopathy due to intrahepatic portosystemic venous shunt successfully treated by interventional radiology. Intern Med 2005; 44:212–216. 21. Tanaka O, Ishihara K, Oyamada H, et al. Successful portal-systemic shunt occlusion with balloon-occluded retrograde transvenous oblitera-
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Efficacy of Balloon-occluded Retrograde Transvenous Obliteration of Large Spontaneous Lienorenal Shunt in Patients with Severe Recurrent Hepatic Encephalopathy with Foam Sclerotherapy: Initial Experience Amar Mukund, MD, S. Rajesh, MD, Ankur Arora, MD, DNB, FRCR, Yashwant Patidar, MD, Deepak Jain, FRCR, and Shiv K. Sarin, MD, DM
ABSTRACT Purpose: Balloon-occluded retrograde transvenous obliteration (BRTO) is a widely accepted treatment for gastric varices, but data are limited in regard to its role in the management of hepatic encephalopathy (HE). This study evaluated the efficacy of BRTO with foam sclerotherapy in the management of HE arising as a result of spontaneous large portosystemic shunts. Materials and Methods: Eight sessions of BRTO with sodium tetradecyl sulfate foam were performed in seven patients with cirrhosis complicated by HE. All patients had portosystemic communication (ie, gastro-/lienorenal shunt) on preprocedure computed tomography. Clinical and laboratory parameters including arterial ammonia level were evaluated in all patients before and after the procedure. Results: Technical success rates were 86% (six of seven) for the first BRTO session and 100% (one of one) for the second. Follow-up imaging revealed complete obliteration of the varices in five of seven patients (71%) and partial obliteration in the remaining two. Immediate clinical improvement of HE was observed in six of seven patients (86%), with postprocedural decrease in arterial ammonia levels; one patient showed delayed improvement. Procedure-related complications (eg, abnormal liver function test results, acute kidney injury with leukocytosis) were encountered in two patients. All patients showed clinical and symptomatic improvement at the time of discharge and during a follow-up of 4 months (with visits at 1 mo and 3 mo later). Conclusions: Initial experience suggests that BRTO is an effective procedure in the management of HE arising as a result of large portosystemic shunts.
ABBREVIATIONS BRTO ⫽ balloon-occluded retrograde transvenous obliteration, HE ⫽ hepatic encephalopathy, STS ⫽ sodium tetradecyl sulfate
Hepatic encephalopathy (HE) is an important cause of morbidity in patients with cirrhosis. Encephalopathy in cirrhosis can be of two types: portal systemic encephalop-
From the Departments of Radiology/Interventional Radiology (A.M., S.R., A.A., Y.P., D.J.) and Hepatology (S.K.S.), Institute of Liver and Biliary Sciences, D1, Vasant Kunj, New Delhi 110070, India. Received January 28, 2012; final revision received May 11, 2012; accepted May 14, 2012. Address correspondence to A.M.; E-mail: [email protected] None of the authors have identified a conflict of interest. © SIR, 2012 J Vasc Interv Radiol 2012; 23:1200–1206 http://dx.doi.org/10.1016/j.jvir.2012.05.046
athy and end-stage encephalopathy (1). Portal systemic encephalopathy is caused by shunting of blood flow from supramesenteric veins to systemic veins, leading to high systemic blood ammonia levels (2). Thus occlusion of these shunts helps in counteracting encephalopathy (3). Balloonoccluded retrograde transvenous obliteration (BRTO) is an endovascular interventional procedure originally described for the management of bleeding gastric varices and HE in patients with cirrhosis (4). The technique involves occlusion of the efferent veins of a portosystemic shunt by using a balloon catheter followed by injection of a sclerosing agent (4 – 6). Since the introduction of the technique in the 1990s, several studies have reported satisfactory results of BRTO in the management of bleeding gastric varices, and
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talizations (at least three) were required within the 6-month period before the procedure. They showed a poor response to medical management for encephalopathy consisting of L-ornithine and L-aspartate infusion combined with oral lactulose during inpatient periods and oral lactulose during outpatient periods. During each hospitalization, each patient had grade III HE per West Haven criteria; however, before the procedure, only five patients had grade III HE and the other two had grade II HE. The indications for BRTO in the remaining two patients were acute variceal bleeding and shunt myelopathy; these patients were excluded from the study. Demographic and clinical profiles of the subjects are shown in Table 1. All patients were male, ranging in age from 45 to 67 years (mean, 56 y). The mean diameter of the lienorenal shunt based on preprocedural CT was 15 mm (range, 10 –20 mm).
Procedure Technique Figure 1. Coronal reformatted CT image shows a large gastrorenal shunt (arrowheads) and perigastric varices (arrows).
it is commonly used in Japan (7–11). However, it is still not widely practiced in other countries, and its role in management of HE needs to be validated by larger studies. This retrospective single-center study was done to assess the efficacy of BRTO in the management of HE.
MATERIALS AND METHODS A retrospective analysis was done for all BRTO procedures performed at a single institution from July to December 2011. In view of the retrospective nature of the study, institutional review board approval was not required per our institution’s policy.
Patients and Procedure Indications A total of 11 BRTO sessions were carried out in nine patients with hepatic cirrhosis and portal hypertension. All these patients had portosystemic communication with a caliber greater than 1 cm in the form of a gastro-/lienorenal shunt, which were defined as large portosystemic shunts. These shunts were seen to continue as dilated and tortuous perigastric and lienorenal varices on preprocedural contrast-enhanced computed tomography (CT; Fig 1). All procedures were performed in the interventional wing of the radiology department by A.M. (n ⫽ 10) or D.J. (n ⫽ 1), who have 7 and 9 years of experience in interventional radiology, respectively. Inclusion criteria for the study were (i) cirrhosis with recurrent severe encephalopathy and a documented large portosystemic shunt and (ii) no response to medical management. Patients who did not fulfill these criteria were excluded. Seven of nine patients who underwent BRTO had recurrent severe encephalopathy for which multiple hospi-
The procedure was performed under local anesthesia or conscious sedation. After written informed consent was obtained, the right internal jugular vein (n ⫽ 7) or right common femoral vein (n ⫽ 1) was accessed and a 6-F vascular access sheath (Cook, Bloomington, Indiana) was placed. Subsequently, selective cannulation of the left renal vein was performed with use of a 5-F angiographic catheter (C2; Cook), which was then replaced with a flexible straight or curved sheath (9, 10, or 12 F; 45, 75, or 80 cm length; Flexor Check-Flo Introducer with large valve assembly, Mullin design, and Ansel modification; Cook). After this long sheath had been placed, a 4-F angled or curved glide catheter (MPA/C2 Slip-Cath; Cook) was used to cannulate the shunt. Gradually, the catheter was advanced deep within the varix. Later, the glide catheter was replaced with a balloon catheter over a stiff guide wire (AES; Cook). The size of the balloon was kept 1–2 mm larger than the diameter of the gastro-/lienorenal shunt and varied from 10 to 22 mm. Although the balloon was slightly oversized, complete occlusion of the shunt was confirmed before the sclerosant agent was injected by injecting contrast medium after inflating the balloon. The use of a compliant occlusion balloon would have been appropriate in these cases, but because such balloon catheters were not available, we had to use noncompliant balloon catheters. Rival balloon catheters (Bard Peripheral Vascular, Tempe, Arizona) were used for shunts as large as 10 mm in caliber, and Atlas balloon catheters (Bard Peripheral Vascular) were used for shunts larger than 10 mm. The Rival balloon was preferred because of its better trackability, but it is not available in sizes larger than 10 mm in diameter. The balloon was positioned proximally within the shunt, as the aim of the procedure was to occlude the shunt and prevent portosystemic mixing of blood. The sclerosing agent, in the form of a foam, was then prepared by mixing air, 3% sodium tetradecyl sulphate (STS; SETROL; Samarth Life Sciences, Mumbai, India), and lipiodol in a 3:2:1 ratio. The sclerosing agent was infused with the goal of filling the full extent of varices (Fig 2). The injection endpoint was defined as
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Table 1. Details of Demographic Data, Disease and Treatment Characteristics, and Complications Disease Score Pt. No./Age (y) 1/63 2/67 3/47 4/62 5/60 6/52 7/57
Child-Pugh 6 7 11 11 10 11 12
MELD 13 14 20 12 24 20 17
Etiology of Cirrhosis NASH NASH Hepatitis B Cryptogenic Cryptogenic Alcoholic Alcoholic
STS Volume Used (mL) 14 10 20 16 20 18 18
Observation Period (d) 180 150 150 150 120 120 120
Complications per SIR Criteria None None None Grade D Grade D None None
Hospital Stay (d) 2 3 2 12 8 2 2
All patients were male. MELD ⫽ Model for End-stage Liver Disease, NASH ⫽ nonalcoholic steatohepatitis, STS ⫽ sodium tetradecyl sulfate.
Figure 2. (a) Abdominal radiograph during the procedure displays stasis of sclerosant mixture within the gastrorenal shunt and perigastric varix (arrows). (b) Radiograph at 3-month follow-up shows retained sclerosant mixture within the same varix (arrows).
(i) complete filling of the varix with the sclerosant mixture as seen on fluoroscopy and cone-beam CT (BRANSIST saphire; Shimadzu, Kyoto, Japan) or (ii) administration of the maximum permissible dose of STS (600 mg) per the available literature (12). After infusion of the sclerosing agent, the balloon was kept inflated for 6 hours. During this period, the patient was kept in the angiography suite or in the recovery area beside the angiography suite, and regular monitoring for stasis of the sclerosant mixture was performed every 30 minutes by fluoroscopy. After 6 hours of balloon inflation, contrast venography through the balloon catheter was performed, and lack of contrast opacification coupled with visible stasis of the sclerosant mixture within the varix was considered to represent complete closure of the shunt and varix. In two cases, the procedure was started in the late afternoon, and, because prothrombin time and platelet counts were normal, the check venogram for confirmation of occlusion was attempted at 4 hours, which confirmed closure of the varix. When no contrast agent flow could be demonstrated within the varix with retained sclerosant mixture, the balloon catheter was deflated and removed. Arterial ammonia levels were measured before and
after the procedure (within 24 – 48 h after shunt closure) in all patients, along with detailed clinical and laboratory investigations. These investigations included postprocedural grading of encephalopathy, liver function tests, renal function tests, and complete blood count throughout the hospital stay (Tables 2 and 3). Postprocedural follow-up imaging at 24 – 48 hours was done with fluoroscopy (Fig 2) to assess for stasis of the sclerosant mixture. Thereafter, regular clinical and imaging follow-up was scheduled and consisted of a visit to the follow-up clinic of the hepatologist and multiphasic CT at 1 month and 4 months (Fig 3). Although contrast-enhanced CT is superior to Doppler ultrasound (US) for documenting the closure of varices, we refrained from the use of iodinated contrast media in patients with decreased renal function. In such patients, Doppler US with bowel preparation was performed to look for any evidence of residual or recanalized lieno-/gastrorenal shunt. This was combined with abdominal radiography to document retained lipiodol within the shunt and varix. If slightest of suspicion was raised on Doppler US regarding a residual/recanalized shunt, CT was planned and performed after stabilization of renal function (Fig 4).
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Table 2. Laboratory Test Results before and after Treatment Total Bilirubin (mg/dL)
Serum Albumin (g/dL)
INR*
Serum Creatinine (mg/dL)
Postprocedure Postprocedure Postprocedure Postprocedure Pt. No. Preprocedure 2 d 1 mo 4 mo Preprocedure 2 d 1 mo 4 mo Preprocedure 2 d 1 mo 4 mo Preprocedure 2 d 1 mo 4 mo 1 2.5 2.2 2.3 1.8 3.1 2.3 3.1 3.0 1.2 1.4 1.2 1.0 0.8 0.8 0.6 0.8 2 2.1 2.7 1.8 2.0 2.9 2.0 2.8 3.0 1.1 1.0 1.1 1.0 0.4 0.1 0.2 0.1 3 1.2 1.1 1.4 0.9 2.5 1.2 2.1 2.8 1.3 1.8 1.4 1.6 1.1 1.2 1.0 0.8 4 3.1 5.4 2.8 3.8 2.4 1.5 2.0 2.1 1.7 2.9 1.8 2.4 0.7 1.6 1.0 0.8 5 1.4 6.7 2.3 1.8 2.3 2.2 2.2 2.4 1.4 1.6 1.4 1.2 0.8 1.4 0.9 1.0 6 4.2 4.1 3.9 3.0 2.9 3.0 3.1 3.4 1.4 1.2 1.0 1.1 0.9 0.7 0.7 0.9 7 4.4 4.7 4.0 3.8 3.0 2.7 2.4 3.0 1.9 2.2 2.8 2.4 0.8 0.9 0.6 0.4 INR ⫽ international normalized ratio.
Table 3. Plasma Ammonia Levels and Hepatic Encephalopathy Grades before and after Treatment Plasma Ammonia (g/dL)
Hepatic Encephalopathy Grade† After Procedure
Pt. No. 1 2 3 4 5 6 7
Before Procedure 147 244 301 184 166 180 139
After Procedure* 86 73 97 78 143 123 87
Shunt Occlusion Complete Complete Complete Partial Complete Partial Complete
Before Procedure II II III III III III III
24 – 48 h I I I I III II I
1 mo Resolved Resolved Resolved Resolved I I Resolved
4 mo Resolved Resolved Resolved Resolved I Resolved Resolved
* At 24 – 48 h after the procedure. † Per West Haven criteria.
Statistical Analysis Statistical analysis was performed by using a paired t test for arterial ammonia levels before and after the procedure in each patient. A P value lower than .05 was considered statistically significant. Commercially available software (SPSS version 17; SPSS, Chicago, Illinois) was used to perform calculations.
RESULTS Technical Success BRTO was performed once in each of six patients and twice in one patient. Technical success rates were 86% (six of sessions) for the first session and 100% (one of one) for the second. The only case of failure was secondary to inability to catheterize and occlude the shunt as a result of extreme tortuosity of the varix. The procedure was performed successfully the next day with the use of a Flexor Check-Flo introducer with an Ansel modification in place of the Flexor Check-Flo introducer with a Mullin design. Two patients had only partial obliteration of the lienorenal shunt as a result of exceedingly tortuous varices of varying caliber,
which possibly led to ineffective occlusion of the varix by the balloon catheter, resulting in partial runoff of the sclerosant mixture. Procedure times ranged from 45 to 120 minutes, with 15– 40 minutes of fluoroscopy time required to cannulate the shunt and reach deep within the varix to place the balloon, depending on the tortuosity of the varices. Thereafter, the balloon was kept inflated for the next 4 – 6 hours. The injected dose of STS ranged from 300 to 600 mg (mean, 480 mg). The mean total volume of STS was 16 mL (range, 10 –20 mL; Table 1), and that of the sclerosing mixture (ie, foam) used was 56 mL (range, 35–70 mL). Technical success was defined as successful administration of sclerosing agent within the shunt and associated varix after placement of the occlusion balloon within the shunt, leading to closure of the varix.
Follow-up Clinical and radiologic follow-up was available for all patients. Follow-up imaging revealed complete obliteration of varix in five of the seven patients, whereas incomplete closure of the shunt was seen in two (Table 3) with partial
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hypernatremia, acute kidney injury, and leukocytosis after the procedure, which was managed with free water replacement, terlipressin, and antibiotic therapy.
DISCUSSION
Figure 3. Coronal reformatted postprocedural (1 mo) CT image shows obliteration of shunt with retained sclerosing agent within the shunt and varix (arrows).
obliteration (approximately 75%) on follow-up imaging at 1 month (Fig 4). Clinically, there was remarkable improvement in the symptoms of HE within 24 – 48 hours of the procedure in all but one patient (decreased grade of encephalopathy; Table 3). However, this patient showed significant clinical improvement in terms of features of HE as well as arterial ammonia levels at 1 month and subsequently at 3 months. Arterial ammonia levels decreased from 220 g/dL ⫾ 81 to 108 g/dL ⫾ 35 (Table 3), which was statistically significant (P ⬍ .05). Even in patients with only partial obliteration of the shunt, the clinical results were comparable to those in the rest of the patients. BRTO did not show any significant effect on liver and kidney functions, including serum bilirubin, albumin, and creatinine levels, and prothrombin time (Table 2), except in two cases that showed immediate postprocedural deterioration in liver and kidney functions.
Complications and Hospital Stay Median hospital stay was 2 days (range, 2–12 d; Table 1). Complications were observed in 29% of patients (n ⫽ 2; Table 1). One of these was a 62-year-old man with cryptogenic cirrhosis complicated by portal hypertension and ascites. He had a history of multiple (n ⫽ 6 –7) episodes of encephalopathy in the previous 1 year requiring multiple hospital admissions. Also significant was the history of left-sided hemiparesis (right basal ganglia hemorrhage) 3 months before BRTO. After the procedure, this patient developed gradual deterioration of hepatic and renal functions, with increasing total leucocyte count. He was administered antibiotic therapy and albumin and recovered gradually in 4 –5 days. He later showed improvement in symptoms of HE on follow-up. Another patient developed
HE is a neuropsychiatric disorder characterized by altered level of consciousness, irritability, inverted sleep/wake pattern, and fluctuating neurologic signs. Important factors in its pathogenesis are severe hepatic dysfunction and shunting of portal venous blood into the systemic circulation so that toxic substances absorbed from the intestine are not detoxified by the liver, leading to metabolic abnormalities in brain. Ammonia is the substance most often incriminated in the pathogenesis of encephalopathy (2). Many, but not all, patients with HE have elevated blood ammonia levels, and recovery from encephalopathy is often accompanied by declining blood ammonia levels (2). The diagnosis of HE is usually one of exclusion. There are no specific diagnostic liver function test abnormalities, although an elevated arterial ammonia level in the appropriate clinical setting is highly suggestive of the diagnosis (2). Severe HE can adversely affect the patient’s quality of life, and its early recognition and management is important (13). In cases that are refractory to medical treatment, BRTO of spontaneous portosystemic shunt is an alternative. BRTO was first described by Kanagawa et al (4) as an endovascular interventional procedure for control of bleeding varices. In recent years, BRTO has been preferred over surgical treatment as a therapy for chronic recurrent HE on account of its reliability and minimal invasiveness (14 –21). The goal of BRTO is to close a large shunt between the portal and systemic circulation. It involves use of an appropriately sized balloon catheter into the efferent vein of a large spontaneous portosystemic shunt to occlude it. After blockade of blood flow is confirmed by injection of contrast media, a sclerosing agent is hand-injected slowly under fluoroscopic guidance. The amount of sclerosing agent needed varies according to the diameter and length of the varix. Detergent-based chemicals in liquid or foam forms have been used as sclerosing agents (22,23). The sclerosing agent used in the present study was STS foam. STS is an anionic surfactant available as a sterile nonpyrogenic solution for intravenous use as a sclerosing agent. Its action is on the lipid molecules in the endothelium, causing intimal inflammation and thrombus formation (22,23). This usually occludes the injected vein. Subsequent formation of fibrous tissue results in partial or complete obliteration of the vein (24). The present study shows that BRTO with STS foam is an effective procedure for obliteration of gastro-/lienorenal shunts with a remarkably good success rate (87%), resulting in significant improvement in the clinical symptoms of HE in these patients. These shunt closure results are in concordance with the observations of Sabri et al (12), who reported a success rate of 91% in their study. Even in patients
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Figure 4. (arrows).
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(a, b) Coronal reformatted pre- and postprocedural contrast-enhanced CT images show partial obliteration of shunt
with partial obliteration of varices, the clinical results were highly satisfactory. Obliteration of major spontaneous portosystemic shunt by BRTO increases portal hepatic blood flow, resulting in improvement in hepatic function and enhanced ammonia detoxification by liver (18,25,26). Although this has been attributed to be the major factor contributing to the therapeutic effect of BRTO on HE, elevation of portal venous pressure can aggravate complications of portal hypertension, including worsening of esophageal varices, ascites, splenomegaly, and gallbladder wall edema (27,28). The present study demonstrates that BRTO had no significant long-term effects on liver or renal function in a small population. The incidence of complications in the present study was 29% (two of seven patients). Both patients began to experience acute renal dysfunction within 48 hours of the procedure. In addition, they also developed fever with increasing leucocyte counts, consistent with bacteremia, which resolved with antibiotic therapy. This is in agreement with the report of Sabri et al (12), who observed a complication rate of 14%, which included portal vein thrombosis caused by sclerosant agent leakage and transient bacteremia. However, in the present study, no overt complications related to leakage of sclerosing agent were seen. The reason for deterioration of hepatic function in one patients is unknown. Although the results of the present study appear promising, the retrospective nature, combined with a small sample size, limited follow-up, and lack of postprocedural portal pressure measurements and endoscopic findings, are some limitations. Long-term follow-up is needed to document the incidence of relapse in the study population and the effect of BRTO on esophageal variceal status and ascites. In conclusion, although the long-term outcome and complications remain to be seen, our initial experience with BRTO of lienorenal shunt, whether complete or partial,
suggests good clinical outcomes in terms of chronic recurrent HE.
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