Eur Radiol DOI 10.1007/s00330-015-3777-1

INTERVENTIONAL

Percutaneous transhepatic balloon-assisted transjugular intrahepatic portosystemic shunt for chronic, totally occluded, portal vein thrombosis with symptomatic portal hypertension: procedure technique, safety, and clinical applications Yong Chen 1 & Peng Ye 1 & Yanhao Li 1 & Shuoyi Ma 1 & Jianbo Zhao 1 & Qingle Zeng 1

Received: 16 October 2014 / Revised: 6 February 2015 / Accepted: 7 April 2015 # European Society of Radiology 2015

Abstract Objectives To introduce a modified transjugular intrahepatic portosystemic shunt (TIPS) procedure, percutaneous transhepatic balloon-assisted TIPS (BA-TIPS), and to evaluate its feasibility and efficacy in patients with chronic totally occluded portal vein thrombosis (CTO-PVT) with symptomatic portal hypertension. Methods Eighteen patients (12 men, six women; mean age 49 years [range, 34–68 years]) with CTO-PVT with symptomatic portal hypertension undergoing BA-TIPS between July 2011 and June 2014 were enrolled in this retrospective study. Rates of technical success, efficacy, and complications were evaluated, and pre- and post-procedure portosystemic gradients compared. Clinical follow-up and periodic assessment of TIPS for patency were performed. Results BA-TIPS was successful in fourteen patients and converted to open portosystemic shunt placement in four. Mean portosystemic pressure gradient fell from 24.1±2.3 mmHg to

12.1±3.5 mmHg after BA-TIPS (P<0.01). No procedurerelated complications were observed. During a median follow up of 16 months (range, 3–41 months), there was one death from hepatocellular carcinoma, one death from severe heart disease, and shunt dysfunction 16 months after BA-TIPS in one patient. Shunt patency was maintained in the remaining patients without symptoms of recurrence. Conclusions BA-TIPS is feasible, safe, and effective for CTO-PVT with symptomatic portal hypertension. Key Points • Transjugular intrahepatic portosystemic shunt is an important treatment for portal vein thrombosis (PVT). • TIPS is challenging for patients with chronic totally occluded portal vein thrombosis (CTO-PVT). • The use of a balloon increased the technical success of portal puncture. • Balloon-assisted TIPS (BA-TIPS) is feasible, safe, and effective for CTO-PVT.

* Yong Chen [email protected]

Keywords Portosystemic shunt, transjugular intrahepatic . Balloon . Hypertension, portal . Thrombosis . Portal vein, cavernous transformation of

Peng Ye [email protected] Yanhao Li [email protected] Shuoyi Ma [email protected] Jianbo Zhao [email protected] Qingle Zeng [email protected] 1

Department of Interventional Radiology, Nanfang Hospital, Southern Medical University, 1838, North Guangzhou Avenue, Guangzhou City, Guangdong Province, China

Abbreviations BA-TIPS Balloon-assisted transjugular intrahepatic portosystemic shunt CTO-PVT Chronic totally occluded portal vein thrombosis MPV Main portal vein PV Portal vein SMV Superior mesenteric vein SV Splenic vein

Eur Radiol

Introduction Portal vein thrombosis (PVT) is a pre-hepatic cause of symptomatic portal hypertension. Its prevalence varies from 6 to 17 % in cirrhotic patients [1–3], and it is even more common in patients with local risk factors, including decompensated cirrhosis and a history of abdominal surgery [4]. The clinical presentations of PVT are acute and chronic: two stages of the same disease that differ in their management. For patients with acute PVT, anticoagulation therapy is recommended to prevent further thrombosis and to promote recanalization of the obstructed veins. More and more studies on chronic PVT have shown, however, that a transjugular intrahepatic shunt (TIPS) is technically feasible and effective in recanalization of the portal vein. Rates of technical success have been reported in a range of 75–100 % in non-selected patients. However, in patients with chronic totally occluded (CTO)-PVT, the technical difficulty associated with accessing a totally occluded portal vein and passing the wire across the occluded segment via the transjugular route increases the difficulty of the standard TIPS procedure. Thus, creation of the shunt may fail when a transjugular approach alone is used. Studies have reported that technical success is associated with the degree of occlusion of the main portal vein (MPV) [5], and cavernous transformation may also increase the technical difficulty. In an attempt to overcome these difficulties and to improve the technical success of TIPS, we have developed a balloonassisted TIPS (BA-TIPS) procedure, which is a modified TIPS technique in which a balloon is used to re-canalize the occluded portal vein and as a target for portal puncture through a combined transhepatic and transjugular approach. Here, we describe the BA-TIPS procedure and evaluate its efficacy and safety in patients with CTO-PVT with symptomatic portal hypertension.

Materials and methods Patients This study was approved by the ethics committee of our hospital. Between July 2012 and June 2014, 18 consecutive patients with CTO-PVT with symptomatic portal hypertension were treated in our hospital. The study population comprised 12 men and six women with an age range of 34–68 years (mean, 49 years). Clinical characteristics on presentation and the vessel involved are presented in Table 1. Indications for TIPS placement were elective control of variceal bleeding in patients having failed endoscopic and medical therapy and refractory ascites. Patients were treated after providing informed consent.

Chronic PVT was diagnosed based on clinical and imaging findings. Presenting symptoms of portal hypertension included variceal re-bleeding and ascites. Computed tomography (CT) and digital subtraction angiography were used to evaluate the extent of thrombosis and degree of obstruction and cavernous transformation. Exclusion criteria included (1) no detectable portal remnant, or a fibrotic cord replacing the MPV; (2) extensive PVT without an appropriate landing zone at the distal end of the portal vein (PV) or superior mesenteric vein (SMV); and (3) evidence of hepatocellular carcinoma. The study was approved by the ethics committee of our hospital. All patients had recurrent variceal bleeding that had not responded to endoscopic therapy, and patients 2 and 7 had medically intractable ascites. Liver disease was classified according to the Child-Pugh classification system. Four patients had class A cirrhosis, 13 had class B cirrhosis, and one had class C cirrhosis. Seventeen patients had hepatitis B cirrhosis and one had cirrhosis of unknown origin. Twelve patients had a history of splenectomy for portal hypertension complicated by variceal bleeding. The degree of thrombosis within the MPV was classified simply as partial or complete thrombus. There is a clear distinction between the two on CT and angiography, as has been previously described [6]. Cavernous transformation was defined as the presence of numerous collateral veins bypassing the occluded PV of the patent segmental vessel. Complete thrombus with cavernous transformation was confirmed by CT and angiography in nine patients.

Procedure Transhepatic approach Under fluoroscopic guidance, a 6-Fr introducer (SKATER® Introducer Set; Medical Device Technologies, Inc. [DBA Angiotech], Lausanne, Switzerland) was introduced at the intersection of the intercostal space and the mid-axillary line and advanced into the liver. Suction was applied to the sheath as it was slowly withdrawn. When blood was aspirated, contrast medium was injected to determine which vascular structure had been entered. If a peripheral portal vein branch was visualized, a 6-Fr sheath (Terumo Corporation, Tokyo, Japan) was advanced to the obstructed segment. A torque-control guide wire (Terumo) was rotated with gentle forward pressure and dragged along the surface of the vein at the point of obstruction. After the guide wire and catheter were manipulated across the obstructed portal vein segment into the SMV or SV, angiography was performed and portal pressure values were recorded. Balloon angioplasty of the occluded lumen with a 6-mm balloon (POWERFLEX® P3 PTA Dilatation Catheter; Cordis Corporation, Bridgewater, NJ, USA) was performed and the thrombus aspirated to re-canalize the portal

Eur Radiol Table 1 No.

Clinical characteristics

Age/sex

Clinical presentation

Aetiology of cirrhosis

Variceal rebleeding

Ascites

Splenectomy

Age before thrombus (months)

Extent of thrombosis PV

SMV

Child-Pugh

1 2 3 4 5 6 7 8 9 10 11 12 13 14

42/M 68/F 43/M 45/M 47/F 55/M 60/M 34/F 51/M 53/M 37/F 48/M 56/M 55/M

+ + + + + + + + + + + + + +

+ + -

HBV HBV HBV HBV Unknown HBV HBV HBV HBV HBV HBV HBV HBV HBV

+ + + + + + + + + +

43 24 12 32 18 96 27 16 27 32

Totala Totala Totala Totala Totala Totala Totala Totala Totala Totala Totala Totala Totala Totala

+ + + + + + + + + + +

B A B C B A B B B B B B B A

15 16 17 18

61/M 38/F 52/M 49/F

+ + + +

-

HBV HBV HBV HBV

+ + -

6 10 16

Totala Totala Totala Totala

+ + +

B B A B

HBV hepatitis B virus, NA not applicable, PBC primary biliary cirrhosis, PG pressure gradient, PV portal vein, SMV superior mesenteric vein a

With cavernomas

vein. Follow-up angiography was performed to assess the degree of stenosis reduction and the presence or absence of thrombus.

the guide wire was then manipulated into the vein lumen. After the ruptured balloon was removed, a standard TIPS procedure was performed.

Transjugular approach

Stent implantation

The right internal jugular vein was accessed, and a 10-Fr ring transjugular intrahepatic access set (Arrow International, Reading, PA, USA) was advanced into the inferior vena cava. The middle or right hepatic vein was then selectively catheterized, and hepatic venography was obtained. Using a transhepatic approach, the balloon (POWERFLEX® P3; Cordis Corp.) was positioned at the site of bifurcation of the right and left portal veins and inflated with contrast medium to 80 % of its volume. Under fluoroscopic guidance, with the contrast-filled balloon as a target and using a transjugular approach, a 16-gauge Colapinto needle (optimed Medizinische Instrumente GmbH, Ettlingen, Germany) was used to puncture the balloon. The curve of the puncture needle could be adjusted based on the position of the balloon in the anteroposterior and oblique projections. Once the balloon had been successfully punctured, its rupture and extravasated contrast medium were observed. Following balloon rupture, the guide wire was easily advanced through the needle into the SMV or SV. If it entered the balloon, the guide wire and balloon could be advanced into the MPV or SMV together, and

Via a jugular approach, the liver parenchymal tract and the occluded segment of portal vein were dilated with a 6-mm balloon (POWERFLEX® P3; Cordis Corp.). A 10-Fr transjugular sheath was then negotiated into the portal vein. The thrombus was aspirated using an 8- or 9-Fr main portal artery guiding catheter (VISTA BRITE TIP®; Cordis Corp.) to evacuate the portal vein clot and restore patency. To create the shunt, two or more stent grafts (FLUENCY® Plus Vascular Stent Graft; C. R. Bard Angiomed GmbH & Co., Karlsruhe, Germany) were deployed from the uppermost patent segment of the SMV or SV through the parenchymal tract and into the lumen of the hepatic vein–inferior vena cava confluence. (The use of GORE® VIATORR® TIPS Endoprosthesis has not been approved by China Food and Drug Administration.) If necessary, an additional bare metal stent (E •Luminexx ® Vascular Stent; C. R. Bard Angiomed GmbH & Co.) was placed overlapping the previous one. Pre- and post-procedure portosystemic gradients were compared using a paired-samples t test. Final portography was obtained and portal pressure gradient was determined. If portal blood flow

Eur Radiol

could not be completely established, catheter-directed thrombolysis was performed. The parenchymal liver tract was embolised with Gelfoam® (Pfizer/Pharmacia and Upjohn Co., Kalamazoo, MI, USA), and the sheath for jugular access was removed at the completion of the procedure. Postoperatively, patients were administered lowmolecular-weight heparin 4,100 IU injected subcutaneously every 12 h for 3 days, and received anticoagulation therapy with warfarin sodium for at least 6 months, titrated to an international normalized ratio of up to two times the upper limit of normal, to prevent shunt dysfunction. Intravenous ornithine aspartate 2.5 g was administered once per day for 5 days as prophylaxis against encephalopathy. Follow-up All patients were followed up at 1, 3, 6, and 12 months postoperatively. The follow-up protocol included assessment of recurrent bleeding, regular blood tests, and coagulation studies as well as colour Doppler ultrasound (diameter and flow velocity of the portal vein and shunt) and CT.

Results BA-TIPS procedures were performed successfully in 14 of 18 patients (Fig. 1). In four patients, the procedure was converted to open portosystemic shunt placement after failed percutaneous transhepatic puncture of the portal vein. Details of procedures and follow-up are summarized in Table 2. Mean postBA-TIPS gradient was significantly lower than pre-BA-TIPS gradient (P<0.01). No procedure-related complications such as abdominal haemorrhage, haemobilia, or stent malposition were observed. One patient developed hepatic encephalopathy after the procedure but soon recovered with conservative medical management. During the median follow-up of 16 months (range, 3– 41 months), patient 3 was found to have hepatocellular carcinoma 11 months after the procedure and died within 5 months, patient 7 died of severe heart disease, and patient 2 experienced shunt dysfunction 16 months after BA-TIPS and underwent TIPS revision with stent grafts. All remaining patients demonstrated maintenance of shunt patency without symptoms of recurrence.

Discussion CTO-PVT is characterized by complete occlusion of the MPV, with a network of hepatopetal collateral veins and no blood flow. The management of CTO-PVT is challenging not only during surgery and liver transplantation, but also during nonsurgical creation of a TIPS. Complete PV occlusion had been

considered a contraindication for TIPS because of the associated low technical success rate, ranging from 0 to 57.1 % [5, 7–9]. CTO-PVT increases the technical difficulty of the procedure. As thrombosis increases over time in patients with chronic PVT, the occluded portal vein shrinks and cavernous transformation occurs [10], preventing access to the portal vein via the standard transjugular approach. Several variations in the technique have therefore been developed to improve the technical success rate in these patients. Studies have demonstrated that the technical success rate of TIPS creation via combined approaches in patients with CTOPVT may be higher than with the transjugular approach alone [7]. A combination of the transjugular plus transhepatic or trans-splenic approaches is an example [5, 11]. The transhepatic or trans-splenic approach allows recanalization of the occluded portal with the use of some combination of angioplasty, mechanical thrombectomy, and thrombolysis. In some cases in this study, however, angiography showed that even after balloon dilation and thrombus aspiration, the portal blood flow was only partially restored, and so the occluded shrunken lumen could not be completely reopened. Therefore, portal puncture via a transjugular approach was difficult. Chen and Soares [12] and Jourabchi et al. [13] reported successful management of patients with complete PV occlusion and cavernous transformation using a combined transhepatic and transjugular approach for TIPS creation, and were successful in puncturing the inflated balloon in the occluded portal vein after multiple unsuccessful attempts to access the portal vein via the transjugular approach alone. The use of a balloon had not been initially planned in their procedures. In our study (a larger case series), BA-TIPS was intentionally used in the management of patients with CTO-PVT. The success rate of BA-TIPS in patients with CTO-PVT was 77.8 % (14/18 patients), which was better than that reported in previous studies. Thus it was shown that BA-TIPS could increase the rate of technical success of the TIPS procedure in patients with CTO-PVT. This success may be attributed to the following factors. First, it is helpful to re-canalize the MPV by means of balloon angioplasty and thrombus aspiration. Blood flow can then be partially restored, and the transjugular catheter and guide wire can pass through the occluded segment with little resistance. Second, with the balloon inflated to enlarge the occluded and shrunken lumen of the portal vein, the likelihood of technical success of the portal puncture increases. We demonstrated that when the balloon was inflated to 80 % of its volume, the tip of the puncture needle had better contact with the surface of the balloon. We therefore recommend inflating the balloon to 80 % of its volume with contrast medium. To prevent the balloon from slipping when punctured, it should be located at the portal bifurcation, where its position is relatively fixed by the hepatic parenchyma. The presence of the balloon in the PV makes it easier to approach the target. The compliant indentation of the balloon and its

Eur Radiol Fig. 1 A 47-year-old woman with Child-Pugh class B cirrhosis and variceal re-bleeding. (a) CT image demonstrates CTO-PVT (black arrow) and cavernous transformation (white arrow). (b) Transhepatic portography demonstrates complete occlusion of the portal vein with cavernous transformation. The portosystemic gradient is 23.5 mmHg. (c) Balloon angioplasty of the occluded lumen with a 6-mm angioplasty balloon catheter. (d) Follow-up angiography shows portal blood flow could not be well established. (e) A needle is used to puncture the balloon via a transjugular approach. Rupture of the balloon and extravasated contrast medium was seen. (f) Venogram obtained after TIPS creation demonstrates patency of the SMV, PV, and TIPS. The final portosystemic gradient is 11.8 mmHg. (g) One year after the procedure, CT image demonstrates a patent shunt. CTO-PVT chronic totally occlusive portal vein thrombosis, PV portal vein, SMV superior mesenteric vein, TIPS transjugular intrahepatic portosystemic shunt

Eur Radiol Table 2

Procedure details and outcomes

No. Procedure time (min) Exposure Radiation doses PG pre-TIPS PG post-TIPS Procedure-related Outcome time (min) (mGy) (mmHg) (mmHg) Complication

Follow-up (months)

1 2 3 4

135 155 113 123

38.5 42.5 25.6 31.8

651.32 695.74 445.63 514.71

23.5 22.8 28.0 26.5

15.4 5.2 17.7 14.7

-

Asymptomatic Asymptomatic Tumor progression Asymptomatic

41 37 16 31

5 6 7 8 9 10 11 12 13 14 15 16 17 18

121 143 130 168 NA 138 NA 136 126 155 133 NA 128 NA

28.7 36.3 34.3 43.2 NA 41.4 NA 43.4 28.9 48.5 31.8 NA 26.7 NA

523.82 672.76 653.23 637.73 NA 601.38 NA 631.35 553.32 685.44 544.21 NA 562.12 NA

23.5 21.3 24.3 27.2 NA 24.8 NA 23.4 21.3 20.8 27.1 NA 23.4 NA

11.8 8.1 12.5 12.5 NA 13.6 NA 13.5 11.4 6.2 13.7 NA 12.8 NA

NA NA NA NA

Asymptomatic Asymptomatic Asymptomatic Asymptomatic Surgery Asymptomatic Surgery Asymptomatic Asymptomatic Asymptomatic Asymptomatic Surgery Asymptomatic Surgery

26 23 10 13 12 12 10 9 9 7 6 4 3 3

NA not applicable, No. number, PG pressure gradient, TIPS transjugular intrahepatic portosystemic shunt

subsequent rupture provide excellent confirmation of PV access. Surgical management of PVT primarily involves surgical thrombectomy, ligation of the varices with or without splenectomy, portosystemic shunt surgery, and liver transplantation. In cirrhotic patients with complete and extended PVT, however, many of these approaches are not suitable and/or feasible in view of the relatively high morbidity rate and high risk of late rebleeding due to reappearance of the varices [14]. Recent consensus has determined that PVT is no longer a contraindication to liver transplantation. Although several centres have reported satisfactory long-term outcome, liver transplantation candidates with PVT, especially patients with more than 50 % portal vein occlusion, are more prone to developing severe perioperative complications and have a high mortality rate and reduced long-term survival [15, 16]. Vianna et al. reported 1- and 3-year survival rates of 80 % and 72 %, respectively. However, the procedure carried a complication rate of 56 %, with half of the patients requiring surgical re-exploration [16]. All patients in our study were asymptomatic, and the primary patency was maintained in 13 of 14 patients during a median follow-up of 16 months. Satisfactory short-term outcome was achieved in this study, but the long-term outcome is still unclear. There were no operative deaths in our group. Intraabdominal haemorrhage, hepatic capsule perforation, and stent malpositioning, which are potential procedure-related complications of TIPS, were not observed in the present study.

The incidence of shunt dysfunction or hepatic encephalopathy after completion of the TIPS procedure in our study was similar to that of previous studies (7–32 % and 0–50 %, respectively) [17]. We have questioned whether the incidence of pulmonary embolism would increase after TIPS creation in patients with PVT. To the best of our knowledge, the incidence in our study was consistent with what has been reported in previous studies [5, 18], i.e., that there was no clinical evidence of pulmonary embolism after TIPS placement. This study has some limitations. First, creation of a portosystemic shunt may fail in patients with a fibrotic cord replacing the MPVor with no detectable intrahepatic branches of the portal vein. In this study, four patients who were found to have no detectable intrahepatic branches of the portal vein underwent surgical portosystemic shunt after failed portal vein access. In patients for whom recanalization of the portal vein is not possible, portal decompression by TIPS creation to the dilated veins of a cavernous transformation may be an alternative solution. Wils et al. [19] reported a small case series in which TIPS was used for portal decompression. It is important to note that the collaterals need to be suitably wide for TIPS placement, and that the high-pressure collaterals should communicate with the varices. Second, there is a high risk of haemorrhage associated with the use of thrombolysis in patients with poor drug excretion due to liver failure. Finally, we had a small study group and a short follow-up period. Therefore, a trial using a larger group and long-term follow-up is needed to confirm the safety and efficacy of BA-TIPS.

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In conclusion, BA-TIPS is a feasible, safe, effective treatment for CTO-PVT with symptomatic portal hypertension. BA-TIPS may increase the rate of technical success of the TIPS procedure in patients with CTO-PVT. Acknowledgments The scientific guarantor of this publication is Yong Chen. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. This study has received funding from the Science and Te c h n o l o g y P l a n n i n g P r o j e c t o f G u a n g d o n g P r o v i n c e (2012B010200027) and the Key Technologies R&D Program of Guangzhou (201300000199). No complex statistical methods were necessary for this paper. Institutional review board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. Some study subjects were previously reported by Stephen Chen (J Vasc Interv Radiol 14: 513-514) and N. Jourabchi et al. (Case Rep Radiol 2013: 635391). Methodology: retrospective, performed at one institution.

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