Vascular and Interventional Radiology Original Research

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1 Vascular and Interventional Radiology Original Research Fanelli et al. Stent-Graft for Hepatic Encephalopathy Vascular and Interventional Radiology Original Research Fabrizio Fanelli 1 Filippo Maria Salvatori 1 Paolo Rabuffi 1 Emanuele Boatta 1 Oliviero Riggio 2 Pierleone Lucatelli 1 Roberto Passariello 1 Fanelli F, Salvatori FM, Rabuffi P, et al. Keywords: covered stent, hepatic encephalopathy, portal hypertension, TIPS, transjugular intrahepatic portosystemic shunt DOI: /AJR Received April 28, 2009; accepted after revision June 12, Vascular and Interventional Radiology Unit, Department of Radiological Sciences, Sapienza University of Rome, Viale Regina Elena, Rome, Italy. Address correspondence to F. Fanelli (fabrizio.fanelli@uniroma1.it). 2 Gastroenterologic Unit, Sapienza University of Rome, Rome, Italy. AJR 2009; 193: X/09/ American Roentgen Ray Society Management of Refractory Hepatic Encephalopathy After Insertion of TIPS: Long-Term Results of Shunt Reduction With Hourglass-Shaped Balloon-Expandable Stent-Graft OBJECTIVE. The purpose of this study was to review the use of an hourglass-shaped expanded polytetrafluoroethylene (eptfe) stent-graft to reduce transjugular intrahepatic portosystemic shunts in patients with hepatic encephalopathy refractory to conventional medical therapy. MATERIALS AND METHODS. From January 2000 through December 2008, 189 transjugular intrahepatic portosystemic shunt procedures were performed with self-expanding stent-grafts. After a mean period of 43.4 ± 57 weeks, hepatic encephalopathy developed in 12 patients and did not respond to conventional medical therapy with lactulose, nonabsorbable antibiotics, and a protein-restricted diet. In all cases, shunt reduction was performed with an hourglass-shaped balloon-expandable eptfe stent-graft inserted into the original shunt. RESULTS. Technically successful shunt reduction with an immediate increase in portosystemic gradient was achieved in all patients. Symptoms of hepatic encephalopathy disappeared a mean of 22.3 hours (range, hours) after the procedure. After a mean followup period of 73.9 ± weeks, no recurrence of hepatic encephalopathy was found. One patient (8.3%) needed dilation of the hourglass-shaped stent-graft after 37 weeks because of recurrence of ascites. At the end of the study, five patients (41.6%) were alive in good clinical condition. Four patients (33.3%) died of cardiovascular failure 1, 2, 24, and 96 weeks after the corrective procedure. Eight months after the reduction procedure, one patient (8.3%) underwent orthotopic liver transplantation, which resulted in clinical improvement. Two patients (16.6%) were lost to follow-up 15.6 and 46.8 weeks after the procedure. CONCLUSION. Shunt reduction with an hourglass-shaped eptfe balloon-expandable stent-graft seems effective in reducing shunt flow and rapidly improving the patient s clinical condition. With this technique, shunt diameter can be modified on the basis of the patient s clinical condition. E stablishment of a transjugular intrahepatic portosystemic shunt (TIPS) has been widely used as an alternative to surgery in the management of complications of portal hypertension [1]. The presence of a TIPS, however, is associated with a high rate of hepatic encephalopathy, ranging from 3% to 35%, especially in cases of a marked decrease in portosystemic gradient [2 4]. Some investigators [5, 6] have attempted to correlate the presence of a small-caliber portosystemic shunt with reduced risk of hepatic encepha lopathy. In general, hepatic encephalopathy can be successfully managed with medical therapy, but if the patient s condition is refractory to conventional medical treatment, the shunt must be occluded or reduced. In an effort to reverse TIPS-induced hepatic encephalopathy, vari- ous strategies of increasing the portosystemic gradient by producing outflow resistance within the shunt have been developed [7 10]. We report the results of our technique of TIPS reduction based on use of an hourglassshaped balloon-expandable expanded polytetrafluoroethylene (eptfe) stent-graft released inside the shunt to reduce blood flow. Materials and Methods We conducted a retrospective analysis of the cases of 189 patients with variceal bleeding, refractory ascites, or Budd-Chiari syndrome who from January 2000 through December 2008 underwent TIPS procedures that included placement of a selfexpanding eptfe stent-graft (Viatorr, W. L. Gore & Associates). After the TIPS procedure, hepatic encephalopathy occurred in 68 of the patients (36%). Twelve patients (five women, seven men; 1696 AJR:193, December 2009

2 Stent-Graft for Hepatic Encephalopathy mean age, 57.5 years; range, years) needed reduction of the TIPS because of the onset of severe hepatic encephalopathy refractory to conventional medical therapy with lactulose, nonabsorbable antibiotics, and a protein-restricted diet. TIPS was performed in six cases for recurrent variceal bleeding and in the other six for refractory ascites. One patient had Child-Pugh class A disease; five patients, class B; and six patients, class C disease. All patients were informed of the intended treatment and possible complications, and written consent was obtained before the procedure. The study was approved by the institutional review board. Clinical Data The clinical data on the patients are summarized in Table 1. All procedures were performed with implantation of a 10-mm-diameter self-expanding eptfe stent-graft. The length of the covered portion of the stent-graft varied according to the length of the intrahepatic track. The portosystemic gradient after the initial TIPS procedure decreased from a mean of 22.7 ± 4.7 (SD) mm Hg to 6.0 ± 1.8 mm Hg. The mean portosystemic gradient before reduction of the TIPS was 6.6 ± 2.69 mm Hg (range, 4 13 mm Hg). In three cases (25%), mild hepatic encephalopathy was present before the initial TIPS procedure. Severe hepatic encephalopathy developed in all 12 patients after a mean period of 43.4 ± 57.5 weeks (range, weeks) from the initial TIPS procedure. Encephalopathy was refractory to conventional medical treatment with lactulose, nonabsorbable antibiotics, and a protein-restricted diet (1 g/kg body weight per day). Before and after the TIPS procedure, grade of hepatic encephalopathy (Table 2), Model for End- Stage Liver Disease score, plasma ammonia and bilirubin levels (Table 3), and international normalized ratio were evaluated for all patients. The Trail-Making Test was performed for accurate evaluation of the grade of hepatic encephalopathy. Definitions Severe hepatic encephalopathy was defined as grade II or greater according to the West Haven criteria. Refractory hepatic encephalopathy was considered recurrent or persistent hepatic encephalopathy. Recurrent hepatic encephalopathy was defined as at least three episodes of non-precipitant-induced severe encephalopathy necessitating hospitalization in a 3-month period despite continuous treatment with nonabsorbable disaccharides. Persistent hepatic encephalopathy was defined as the presence of a continuously detectable altered mental state with further episodic deterioration despite protein restriction and treatment with nonabsorbable disaccharides. Technical success of TIPS reduction was defined as an increase in portosystemic gradient after shunt reduction. Patients were considered responders when they had clinically significant relief of hepatic encephalopathy after TIPS reduction. Patients were considered nonresponders when there was no relief of hepatic encephalopathy after TIPS reduction. Refractory bleeding was defined as reappearance of gastrointestinal bleeding after establishment of the TIPS or after TIPS reduction that was unmanageable with conventional therapy. Refractory ascites was defined as reappearance of ascites after establishment of the TIPS or after TIPS reduction that was refractory to conventional therapy. Technique Under sterile conditions, the right internal jugular vein was punctured through an anterior approach with an 18-gauge needle. A 10-French 25-cm-long introducer sheath (Check-Flo, Cook) was advanced into the inferior vena cava close to the hepatic vein. An angled inch hydrophilic guidewire (Radifocus, Terumo) was advanced through the TIPS and into the superior mesenteric or splenic vein. Portography was performed with a 5-French pigtail catheter placed in the portal region, and the portosystemic gradient was measured. Shunt reduction was performed by implantation of an eptfe balloon-expandable stent-graft (Jostent, Abbott) into the shunt. Before insertion, an absorbable 3 0 polyglactin 910 (Vicryl, Ethicon) suture was tied in the middle of a mm balloon catheter (Wanda, Boston Scientific) (Fig. 1A). The central ligature of the balloon allowed dilation of both ends of the stent only, producing an hourglass appearance. The balloon was inflated with saline solution to verify the correct position of the suture line and dilatation of both ends only (Fig. 1B). The balloon-expandable device is large (diameter, 6 12 mm; length, 38 mm) and has an unmounted sandwich design that includes a thin layer of eptfe between two stainless-steel (316L) stents and is manually crimped on the central portion of the balloon. The hourglass-shaped expandable stent-graft mounted on the balloon catheter was inserted into the sheath with the balloon completely deflated and was advanced into the self-expanding stentgraft used for the TIPS until the desired position was reached, generally in the middle of the covered TABLE 1: Clinical Data on Patients With Hepatic Encephalopathy Refractory to Conventional Medical Therapy Patient Age (y) Sex Disease Child-Pugh Class Indication for TIPS Dimensions of TIPS Portosystemic Gradient Grade of Hepatic Stent-Graft (mm) (mm Hg) Encephalopathy Diameter Length a Before TIPS Before TIPS After TIPS 1 68 M Alcoholic cirrhosis B Refractory ascites F HCV A Variceal bleeding F HCV C Refractory ascites F Alcoholic cirrhosis C Refractory ascites M HCV C Variceal bleeding I II M Alcoholic cirrhosis C Refractory ascites F HCV, HCC B Variceal bleeding I II F HBV B Refractory ascites M HCV, HCC C Variceal bleeding I II M HCV, HCC B Variceal bleeding M HBV B Refractory ascites M Alcoholic cirrhosis C Variceal bleeding Note TIPS = transjugular intrahepatic portosystemic shunt, HCV = hepatitis C virus infection, HBV = hepatitis B virus infection, HCC = hepatocellular carcinoma. a Length of covered portion of stent-graft. 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3 Fanelli et al. TABLE 2: Classification of Hepatic Encephalopathy Related Symptoms According to the West Haven Criteria Grade Symptoms 0 Lack of detectable changes in personality or behavior Asterixis absent I Trivial lack of awareness Shortened attention span Impaired addition or subtraction Hypersomnia, insomnia, or inversion of sleep pattern Euphoria or depression Asterixis detectable II Lethargy or apathy Disorientation Inappropriate behavior Slurred speech Obvious asterixis III Gross disorientation Bizarre behavior Semistupor to stupor Asterixis generally absent IV Coma portion. With an inflator device, the balloon was dilated up to its nominal pressure rate (8 atm [811 kpa]). The proximal and distal portions of the balloon were completely dilated up to 10 mm; the central portion was only partially expanded because of the presence of the suture line. After removal of the 10-mm balloon, a 5-mm balloon catheter was inserted to dilate the middle portion of the stentgraft. A venogram was obtained to analyze the residual flow inside the shunt, and the portosystemic gradient was measured (Fig. 2). The hourglassshaped stent-graft was dilated to increase the portosystemic gradient according to the patient s clinical condition. If the portosystemic gradient was too high, the middle portion of the shunt was further dilated with a larger balloon (6 8 mm). During the follow-up period, patients were evaluated by the same medical team who conducted the clinical assessment. Upper endoscopy was performed only on patients treated for variceal bleeding. Color Doppler ultrasound examinations were performed the day after and 3, 6, and 12 months after the TIPS reduction procedure. Results All the reduction procedures were performed successfully with correct deployment of the hourglass-shaped balloon-expandable stent-graft inside the self-expanding stentgraft without procedural complications. Immediate technical success, represented by increased portosystemic gradient with increased outflow resistance, was achieved in all cases. A marked decrease in flow within the shunt (from 85 to 25 cm/s at color Doppler ultrasound examination) with an increase in mean portosystemic gradient from 6.6 mm Hg (range, 4 13 mm Hg) to 15.1 mm Hg (range, mm Hg) occurred immediately after the TIPS reduction procedure. A 5-mm dilatation of the middle portion of the hourglass-shaped stent-graft was sufficient to increase the portosystemic gradient in two cases (16.6%), and in nine patients (75%), 6-mm dilation was necessary. In one case (8.3%), the hourglass-shaped balloonexpandable stent-graft was dilated to 7 mm. After TIPS reduction, grade of hepatic encephalopathy decreased substantially, and symptoms were relieved (Table 3) within a mean of 22.3 hours (range, hours). Plasma ammonia level decreased in all cases. The mean value before TIPS reduction was ± 81.7 μg/100 ml (range, g/100 TABLE 3: Laboratory Values and Clinical Status of Patients With Refractory Hepatic Encephalopathy Before and After Reduction of Transjugular Intrahepatic Portosystemic Shunt (TIPS) Patient No. Plasma Ammonia (µg/100 ml) Total Bilirubin (mg/dl) Model for End-Stage Liver Disease Score Hepatic Encephalopathy Grade Before TIPS After TIPS Before TIPS After TIPS Before TIPS After TIPS Before TIPS After TIPS III IV I III I II IV III II III II III III III I II III II I IV II 1698 AJR:193, December 2009

4 Stent-Graft for Hepatic Encephalopathy ml), and the mean value after TIPS reduction was ± μg/100 ml (range, g/100 ml). Clinical responses and final outcomes after shunt reduction are summarized in Table 4. After a mean follow-up period of 73.9 ± weeks (range, weeks), six patients (50%) were alive and in good clinical condition. Four patients (33.3%) died of cardiac or multiorgan failure 1, 2, 24, and 96 weeks after shunt reduction. One patient A A B Fig. 1 Materials used for reduction of transjugular intrahepatic portosystemic shunt. A, Photograph shows 3 0 absorbable suture line tied in middle of mm balloon for expansion of two ends of stent but not central portion. Balloon is inflated with saline solution to verify correct position of suture line. B, Photograph shows large (diameter, 6 12 mm; length, 38 mm) hourglass-shaped balloon-expandable expanded polytetrafluoroethylene stent-graft manually crimped on balloon catheter. When balloon is completely dilated, proximal and distal ends of stent-graft are fully expanded up to 10 mm, and central portion of stent-graft is only partially dilated, producing hourglass shape. However, middle portion of stent-graft should be progressively dilatated with larger balloon according to patient s clinical condition. (8.3%) (patient 4) underwent orthotopic liver transplantation 8 months after reduction and was in improved clinical condition and without signs of hepatic encephalopathy or recurrence of ascites. Two patients (16.6%) (patients 8 and 10) were lost to the follow-up after 46.8 and 15.6 weeks, respectively, but no signs of hepatic encephalopathy, refractory ascites, or rebleeding were reported at the last follow-up evaluation. In patient 3, the reduced 6-mm shunt was dilated to 7 mm because of the onset of ascites 8 months after reduction; the symptoms resolved completely without evidence of hepatic encephalopathy. Discussion TIPS is generally considered a less morbid procedure than surgical shunting in the management of complications of portal hypertension. The technique, however, has not eradicated the consequences of portosystemic shunting, such as hepatic encephalopathy. The Fig year-old man (patient 5) with transjugular intrahepatic portosystemic shunt (TIPS) for variceal bleeding. TIPS resulted in high flow within shunt and marked reduction of portosystemic gradient (6 mm Hg). Five days after TIPS procedure, grade III hepatic encephalopathy refractory to conventional medical therapy developed. A, Venogram obtained at end of TIPS procedure shows correctly deployed mm self-expanding stent-graft covering all of intrahepatic track from portal vein to junction of inferior vena cava. B, Venogram obtained after TIPS reduction in which 38-mm-long hourglass-shaped balloon-expandable stent-graft was released inside shunt shows middle portion of shunt dilated to 7 mm. C, Venogram obtained at end of reduction procedure shows marked reduction of flow inside shunt due to outflow resistance. Increased portosystemic gradient (16 mm Hg) was immediately recorded. B C AJR:193, December

5 Fanelli et al. TABLE 4: Clinical Response and Characteristics After Reduction of Transjugular Intrahepatic Portosystemic Shunt (TIPS) Patient Interval Between TIPS and Reduction (wk) Hepatic Encephalopathy Grade presence of the shunt alters hepatic hemodynamics and increases the bioavailability of intestinally derived agents, such as ammonium, increasing the risk of hepatic encephalopathy and liver dysfunction [11 13]. A varying incidence of hepatic encephalopathy after TIPS procedures (3 35%) has been reported [14 19]. Several factors predictive of the development of post-tips encephalopathy have been suggested, such as nonalcoholic causes of cirrhosis with hypoalbuminemia, Child-Pugh class B or C disease, previous episodes of encephalopathy, a high degree of reduction of the portosystemic gradient, and large shunt diameter [20]. Kochar et al. [21], however, reported that older age should be considered the main factor predictive of hepatic encephalopathy. The incidence and severity of hepatic encephalopathy are higher during the first month after a TIPS procedure and decrease progressively because the diameter of the shunt tends to decrease spontaneously. This theory is confirmed by the increase in portosystemic gradient index and reduction in ammonia levels during the follow-up period [22], especially in patients treated with bare stents. Hepatic encephalopathy usually can be controlled with conventional medical therapy with lactulose, nonabsorbable antibiotics, and an appropriate protein-restricted diet (1 g/kg body weight per day) [22]. In the treatment of patients whose condition is refractory to medical therapy, different methods Balloon Dilatation Diameter (mm) Portosystemic Gradient (mm Hg) Before Reduction After Reduction Follow-Up Period (wk) Outcome III IV Dead of cardiovascular failure III Alive, episodes of ascites and hepatic encephalopathy I II Alive, dilation to 7 mm 32 wk after reduction for recurrence of ascites IV Alive, orthotopic liver transplantation 8 mo after reduction III Dead of cardiovascular failure II III Alive II III Dead of cardiovascular failure III Lost to follow-up III Alive II III Lost to follow-up II Dead of cardiovascular failure IV Alive based on partial or complete occlusion of the shunt have been adopted to control the portosystemic shunt overflow that can occur after establishment of a TIPS. Rose and Katz [1] reported on their experience with nonabsorbable materials that definitively occluded the shunt. The technique, however, is associated with a high risk of variceal rebleeding consequent to an irreversible increase in portal pressure. Shunt occlusion also can be performed with an occlusion balloon inflated inside the shunt for at least 12 hours. Portal thrombosis and variceal rebleeding can occur, however, as reported by Kerlan et al. [23] and Haskal et al. [24]. Kochar et al. [21] described 29 cases of shunt occlusion with an inferior vena caval filter with or without coil embolization. A high incidence of procedure-related complications after shunt occlusion, however, such as portal and mesenteric venous thrombosis with intestinal infarction, has been observed. From the data available, partial occlusion of a TIPS appears to be more attractive than complete occlusion because partial occlusion allows reversal of flow-related complications and control of portal hypertension. Some authors [7 10] have reported on their experience with partial reduction of the shunt lumen with bare stents. The efficacy of this technique is not immediate because time is required for complete thrombosis outside the stent and consequent reduction of shunt flow. Haskal and Middlebrook [8] constrained a stent (Wallstent, Boston Scientific) using a 3 0 silk suture to produce an hourglass shape with a constraining diameter of 5 mm. Those authors attributed the reduction in blood flow through the stent to increased friction and turbulence caused by the interposed stent meshes. Additional embolization of the dead space surrounding the narrowed portion of a stent with the aim of complete and rapid reduction of blood flow was described by Gerbes et al. [7] in After injection of an embolic emulsion (Ethibloc, Ethicon) into the dead space, the portosystemic gradient increased rapidly from 10 to 23 mm Hg and shunt flow velocity decreased from 85 to 25 cm/s. Other embolic agents, such as Gianturco-Anderson-Wallace coils, have been used to completely fill the dead space. Results of some studies [2, 10, 25 30] suggest reducing a TIPS with stents covered with various materials. A polyethylene terephthalate covered self-expanding nitinol stent especially designed for TIPS reduction was used by Hauenstein et al. [12] in The procedure, however, was unsuccessful in three of six patients treated for liver failure. Lack of thrombosis around the stent, which led to treatment failure, occurred in patients with severe coagulopathy. Madoff et al. [2] in 2004 described the use of constrained stent-grafts (Wallgraft, Boston Scientific) to treat six patients. Clinical improvement was achieved within 72 hours AJR:193, December 2009

6 Stent-Graft for Hepatic Encephalopathy Polyethylene terephthalate stents, however, produced a thrombogenic and inflammatory response that led to precocious occlusion of the shunt. Jaquier et al. [25] suggested using a 10-mm covered stent (Wallgraft) pushed coaxially through a previously deployed 6-mm biliary endoprosthesis (Wallstent Unistep) and held in the shunt with an opposing wire against the internal wall of the TIPS. A high risk of stent migration associated with use of the 6-mm biliary endoprosthesis devices, however, should be taken into consideration. In addition, the polyethylene terephthalate lining is associated with high thrombotic risk [2]. Cox et al. [26] described a TIPS reduction technique based on use of a mm self-expandable covered stent (Wallgraft). They placed a 5 0 polypropylene purse-string suture in the middle portion of the stent-graft. The stent-graft was tied down over an inflated 6-mm balloon placed alongside the partially deployed covered stent device. The balloon was deflated and removed, resulting in luminal constriction at the midportion of the stent-graft. The use of eptfe-covered stent-grafts seems effective, as reported by Quaretti et al. [27], Maleux et al. [28, 29], and Weintraub et al. [30]. All of those authors described cases of hepatic encephalopathy after TIPS that resolved with reduction of the shunt lumen with an hourglass-shaped stent-graft [22, 28, 30] or a parallel technique [29]. Quaretti et al. [27] performed shunt reduction by inserting a 48-mm-long balloon-expandable stentgraft (Jostent) through a jugular approach. The stent-graft was mounted on a mm balloon catheter and advanced through a 12-French sheath into the shunt. The sheath was retrieved only from the distal part of the stent-graft to allow dilation of only the distal portion. The proximal portion of the stent-graft was dilated with the mm balloon while the central portion was dilated with a 7-mm balloon, giving the stent an hourglass shape. Weintraub et al. [30] reported on an experience with an adjustable PTFE reducing stent based on a mm biliary endoprosthesis (Wallstent) constrained by a 39-mm balloon-expandable stent-graft (Advanta, Atrium Medical). Our technique of TIPS reduction based on use of a balloon-expandable eptfe stent-graft has the following advantages. The eptfe graft immediately excludes flow outside the reducing stent. It is not necessary, therefore, to wait for thrombus formation around the stenotic area. Use of a stent-graft favors immediate improvement in liver perfusion. Only one stent-graft is necessary, reducing the risks and the costs of the procedure. The suture line is placed on the balloon and not on the stent-graft. In combination with use of a balloon-expandable stent, this aspect of the technique allows progressive dilation of the shunt according to the needs of the patient. An excessive increase in portosystemic gradient can be easily managed with stepwise expansion of the narrowed segment. Like that proposed by Weintraub et al. [30], our technique allows progressive modification of shunt caliber according to the clinical condition of the patient. Moreover, use of one stent rather than two makes this technique easier and less expensive than other procedures. In our experience, all 12 cases of hepatic encephalopathy refractory to conventional medical therapy after establishment of a TIPS were successfully managed by reduction of the shunt lumen with a commercially available eptfe balloon-expandable stentgraft placed in an hourglass configuration inside the self-expanding stent-graft that had been inserted for the TIPS. The presence of the hourglass-shaped stent-graft causes an immediate reduction in flow in the TIPS and a rapid increase in portosystemic gradient that relieves the hepatic encephalopathy. Hepatic encephalopathy is a challenge to conservative management. Use of a balloonexpandable eptfe-covered stent-graft for shunt reduction seems valid for decreasing shunt flow to bring about rapid improvement in the patient s clinical condition. The most important advantage of our technique is the ability to adjust to the patient s clinical condition by progressively increasing the caliber of the shunt with a single stent-graft. Additional studies are needed to evaluate the use of adaptable-caliber stent-grafts that can be fitted to the patient s clinical condition, reducing the need for repeated intervention. References 1. Rose SE, Katz MD. Intentional occlusion of a transjugular intrahepatic portosystemic shunt. Cardiovasc Intervent Radiol 1995; 18: Madoff DC, Wallace MJ, Ahrar K, Saxon RR. TIPS-related hepatic encephalopathy: management options with novel endovascular techniques. RadioGraphics 2004; 24: Rösch J, Keller FS. 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