Longterm Outcomes of Stent Placement for Hepatic Venous Outflow Obstruction in Adult Liver Transplantation Recipients

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1 ORIGINAL ARTICLE Longterm Outcomes of Stent Placement for Hepatic Venous Outflow Obstruction in Adult Liver Transplantation Recipients Hee Ho Chu, 1 * Nam-Joon Yi, 2 * Hyo-Cheol Kim, 1 Kwang-Woong Lee, 2 Kyung-Suk Suh, 2 Hwan Jun Jae, 1 and Jin Wook Chung 1 Departments of 1 Radiology and 2 Surgery, Seoul National University College of Medicine, Seoul National University Hospital, Seoul, South Korea The purpose of this study was to evaluate the longterm outcomes of stent placement for a hepatic venous outflow obstruction in adult liver transplantation recipients. From June 2002 to March 2014, 23 patients were confirmed to have a hepatic venous outflow obstruction after liver transplantation (18 of 789 living donors [2.3%] and 5 of 449 deceased donors [1.1%]) at our institute. Among these patients, stent placement was needed for 16 stenotic lesions in 15 patients (12 males, 3 females; mean age, 51.7 years). The parameters that were documented retrospectively were technical success, clinical success, complications, recurrence, and the patency of the stent. The technical success rate was 100% (16/16). Clinical success was achieved in 11 of the 15 patients (73.3%). A major complication occurred in only 1 patient a hepatic vein laceration during the navigation of the occluded segment. The median follow-up period was 33.5 months (range, months), and the overall 1-, 3-, and 5-year primary patency rates of the stent were all 93.8%. One case of occlusion of the stent without clinical signs and symptoms was observed 5 days after the initial procedure. In this patient, the stent was recanalized by balloon angioplasty and showed patent lumen for 48 months of the subsequent follow-up period. In conclusion, stent placement is a safe and effective treatment modality with favorable longterm outcomes to treat hepatic venous outflow obstruction in adult liver transplantation recipients. Liver Transplantation AASLD. Received May 26, 2016; accepted July 23, Liver transplantation is now widely accepted as a therapeutic option for the treatment of end-stage liver disease and hepatocellular carcinoma. (1-3) The number of liver transplantations is rapidly expanding with the recent advances in surgical techniques, immunosuppressants, and endovascular interventions. Abbreviations: CT, computed tomography; HBV, hepatitis B virus; HCV, hepatitis C virus; HV, hepatic vein; IVC, inferior vena cava; LDLT, living donor liver transplantation; LHV, left hepatic vein; MHV, middle hepatic vein; RHV, right hepatic vein; RIHV, right inferior hepatic vein; US, ultrasonography. Address reprint requests to Hyo-Cheol Kim, M.D., Ph.D., Department of Radiology, Seoul National University College of Medicine, Seoul National University Hospital, 101 Daehak-ro, Jongno-gu, Seoul , South Korea. Telephone: ; FAX: ; angiointervention@gmail.com 1554 ORIGINAL ARTICLE Vascular complications are life-threatening when they develop after liver transplantation. (4-8) A hepatic venous outflow abnormality is one of the most crucial vascular complications, leading to refractory graft dysfunction from liver congestion and causing graft loss and mortality as high as 17%-24%. (9,10) The incidence of hepatic venous outflow abnormality has been reported to be 0.8%-9.5% after liver transplantation. (5,9,11,12) Primary stent placement is a safe and effective treatment modality to treat a posttransplant hepatic venous outflow abnormality. There are several studies with good short-term to midterm results following primary stent placement with a mean follow-up period of months. (13-16) Ko et al. (5) reported that primary stent placement can be effective for treating an early posttransplant hepatic venous outflow obstruction with acceptable longterm patency (5-year primary patency, 72.4%), and they claimed that the diameter of a stent is an independent factor associated with the patency of

2 LIVER TRANSPLANTATION, Vol. 22, No. 11, 2016 stents. Stent placement for hepatic venous outflow obstruction is still an important issue with a few longterm results. Therefore, we retrospectively evaluated the longterm efficacy and patency of stent placement for hepatic venous outflow obstructions in adult liver transplantation recipients. Patients and Methods PATIENT POPULATION This retrospective study was approved by the institutional review board of our hospital, which permitted informed consent to be waived. From June 2002 to March 2014, 1238 adult patients older than 18 years old underwent liver transplantation at our institute (789 living donor and 449 deceased donor transplantations). Of these patients, 23 (1.9%, 23/1238) patients (18 of 789 [2.3%] living donors and 5 of 449 [1.1%] deceased donor transplantations) were diagnosed with a hepatic venous outflow obstruction by using Doppler ultrasonography (US), computed tomography (CT), and hepatic venography. A hepatic venous outflow abnormality was suspected when a Doppler US examination showed no detectable flow signal, a persistent monophasic waveform, a slow flow of less than 10 cm/second, or a reverse flow direction. If patients were highly suspected of having a hepatic venous outflow abnormality on a Doppler US examination, a CT scan was performed. A hepatic venous outflow abnormality was diagnosed when a CT scan showed nonopacified hepatic veins (HVs), focal luminal narrowing >70% of the adjacent normal hepatic venous diameter, or a geographic low attenuation area in the liver in the clinical setting of hepatic congestion: ascites, pleural effusion, elevated liver enzyme, or abnormal findings on an immediate postoperative Doppler US examination. A hepatic venous outflow *These authors contributed equally to this work. Copyright VC 2016 by the American Association for the Study of Liver Diseases. View this article online at wileyonlinelibrary.com. DOI /lt Potential conflict of interest: Nothing to report. FIG. 1. A flowchart that shows the incidence of hepatic venous outflow obstruction and the management process in adult liver transplantation recipients. abnormality was confirmed by hepatic venography, and we defined significant hepatic venous outflow stenosis when the pressure gradient between the HV and the inferior vena cava (IVC) was > 5 mm Hg or when the lumen of the HV was compromised by more than 70% compared with the distal part of the HV. The 23 patients with a confirmed hepatic venous outflow obstruction were initially treated by percutaneous transluminal angioplasty in 10 patients and by primary stent placement in 13 patients. Two patients underwent percutaneous endovascular stent placement for recurrent hepatic venous outflow obstruction after percutaneous transluminal angioplasty (Fig. 1). The 15 patients who underwent percutaneous endovascular stent placement for treating hepatic venous outflow abnormalities were included in this study. The median time period between the liver transplantation and the stent placement was 59 days (range, days). The baseline characteristics of these patients are summarized in Table 1. SURGICAL HEPATIC VENOUS ANASTOMOSIS In the recipients, the native liver was removed preserving the vena cava and without venovenous bypass. In the deceased donor liver transplantations, both conventional piggyback end-to-end reconstruction and side-to-side IVC reconstruction were used according ORIGINAL ARTICLE 1555

3 LIVER TRANSPLANTATION, November 2016 TABLE 1. Baseline Characteristics of the 15 Patients Characteristics Values Sex, male:female 12:3 Age, years, range (mean, ) Causes of underlying liver disease HBV 13 HCV 1 Alcohol 1 Donor types Living 12 Deceased donor 3 Graft types Whole 3 Right lobe 10 Left lobe 1 Left lobe auxiliary partial 1 Interval between transplantation and stent placement, days, range (median, ) Preprocedure Doppler US findings (n 5 16) Nondetectable flow 4 Persistent monophasic waveform 11 Reverse flow direction 1 Preprocedure CT findings (n 5 16) Nonopacified HVs 6 Focal HV luminal narrowing greater than 50% 10 Geographic low attenuation in hepatic parenchyma 11 Clinical symptom or sign Ascites or pleural effusion 6 Abnormal liver enzymes 8 None* 1 Involved HVs (n 5 16) RHV 5 LHV 2 MHV 7 RIHV 2 *These patients showed nondetectable flow in MHV on immediate postoperative Doppler US. to the individual condition. In the living donor liver transplantations (LDLTs), end-to-end HV reconstruction was used in the usual manner. (17) In the deceased donor liver transplantations with end-to-end venous reconstruction, the end of the graft IVC was directly anastomosed to the common orifice of the recipient s HVs using a 4-0 Prolene running suture technique. In the deceased donor liver transplantations with side-to-side IVC reconstruction, ellipsoid openings were made on both the recipient s and donor s graft IVCs, and the IVCs were directly anastomosed using a 5-0 Prolene running suture technique. In the LDLTs, the recipient s HV stump was extended to the IVC for size matching after the recipient s IVC clamp, and the graft HV was directly anastomosed to the recipient s HV orifice using either a 4-0 or 5-0 Prolene running suture technique. STENT PLACEMENT A total of 16 stent placements in 15 patients were conducted by 2 experienced interventional radiologists (H.C.K. and H.J.J.). Under local anesthesia, a selective hepatic venography and a stent placement were performed in the right internal jugular vein (n 5 13), the right femoral vein (n 5 1), and the cooperation of the right internal jugular vein and the transhepatic access (n 5 1). The transhepatic approach is rarely considered at our institute to minimize damage to the transplanted liver. A inch hydrophilic guide wire (Terumo, Tokyo, Japan) and a 5-Fr cobra catheter (Cook, Bloomington, IN) were used to select each HV. After the hepatic venography, the pressure gradient across the anastomosis was obtained in most patients except those with thrombotic hepatic venous occlusion or those who had severe stenosis that was difficult to negotiate. Fifteen self-expandable stents with a diameter of 7-14 mm and a length of mm (Zilver; Cook Medical Inc., Bloomington, IN) and 1 balloon expandable stent with a diameter of 7 mm and a length of 15 mm (Palmaz Genesis; Cordis, Miami, FL) were used. In 2 patients, 1 session of balloon angioplasty following stent placement was performed because of recurrent stenosis after the balloon angioplasty. After the stent placement, a postprocedural hepatic venography and manometry were conducted to determine the technical success of each procedure. Heparin was administered to patients during the procedure using 50 IU/kg of heparin, and the heparin was stopped after the procedure. Low-dose aspirin (2-3 mg/kg/day) was administered for 1-2 years after the stent placement. FOLLOW-UP AND DEFINITIONS After the stent placement, a follow-up Doppler US examination, CT scan, and laboratory examination were generally conducted every 1-3 months for the first year and then at 3-6-month intervals. A Doppler US examination was conducted by a radiologist at our institute. Patient symptoms and biochemical data, including serum aspirate aminotransferase, alanine aminotransferase, and bilirubin, were assessed on a daily basis until a patient was discharged, and the patient would then be randomly assessed every 3-6 months at the transplant outpatient clinic. A radiologist (H.H.C.) retrospectively reviewed and documented technical success, clinical success, recurrence, and stent patency ORIGINAL ARTICLE

4 LIVER TRANSPLANTATION, Vol. 22, No. 11, 2016 Technical success was achieved when a pressure gradient across the stenosis was 5mm Hg on a postprocedural manometry or when the stenosis was <20% on a postprocedural venography. (5) Clinical success was judged as an amelioration of presenting signs and symptoms, and the recovery of liver function with improvement of follow-up Doppler US and CT findings: a biphasic or triphasic waveform on a Doppler US examination and the disappearance of a geographic low attenuation area in the liver on a CT scan. Recurrence was defined as a relapse of clinical signs and symptoms or liver function deterioration associated with a hepatic venous outflow abnormality. Stent patency was defined as a biphasic or triphasic waveform on a follow-up Doppler US examination or the well enhancement of an inserted stent lumen without HV stenosis >50% of the stent diameter on a follow-up CT scan. If the stent-inserted HV was suspected of having stenosis or occlusion on follow-up Doppler US and CT (no detectable flow signal or monophasic waveform on Doppler, >50% of in-stent stenosis, or no enhancement of stented HV on CT) and/or clinical signs/symptoms related with hepatic venous outflow abnormality recurred, hepatic venography was performed to evaluate the stent patency. The primary patency of the stent placement (intervention-free survival) was defined as the duration of time from the initial stent placement to any intervention designed to maintain or reestablish patency or the last time of identification of patency on a Doppler US examination, CT scan, or hepatic venography. (18,19) Complications were classified as either major or minor according to the guidelines of the Society of Interventional Radiology Standards of Practice Committee. (20) A major complication was defined as an event that increased the level of care needed by a patient or lengthened a patient s hospital stay and that resulted in permanent adverse sequelae or death. A minor complication was defined as an event that required no therapy or nominal therapy, including overnight admission for only observation. STATISTICAL ANALYSIS Changes in the laboratory findings and pressure gradient between the preprocedural and postprocedural period were compared using the Wilcoxon signed-rank test. The Kaplan-Meier method was used to analyze the cumulative patency rate of the inserted HV stent. In the calculation of the stent patency period, patients were censored if cessation of stent patency did not occur during a patient s life. A P value < 0.05 was considered to be statistically significant. All analyses were conducted with SPSS software, version 22.0 (SPSS, Chicago, IL). Results TECHNICAL SUCCESS Successful stent placement was achieved in 16 anastomoses in 15 patients (there were 2 anastomoses in 1 patient; Table 2). Technical success was obtained in all 16 stent placements (100%). In 2 patients, a balloon angioplasty was initially performed to treat a hepatic venous outflow abnormality, and the following stent placement was performed because of recurrence. The duration between the initial balloon angioplasty and the following stent placement was 8 and 21 days, respectively. The pressure gradient was measured in 15 anastomoses. The preprocedural and postprocedural pressure gradients across stenoses were mm Hg (range, 5-29 mm Hg) and mm Hg (range, 0-6 mm Hg), respectively (P < 0.001; Fig. 2). CLINICAL SUCCESS Clinical success was achieved in 11 of the 15 patients (73.3%) who had ascites, pleural effusion, or abnormal liver enzymes. Four patients with clinical failure died months after the procedure. Even though the inserted stent showed patent hepatic venous outflow on the follow-up studies, the patients died because of either hepatic failure due to acute rejection (n 5 1), primary graft nonfunction of unknown origin (n 5 1), or recurrence of hepatocellular carcinoma with rapid progression (n 5 2). All 11 patients with clinical success were still alive months (range, months) following stent placement. A major procedure-related complication occurred in only 1 patient. A HV laceration and contrast leakage developed during the navigation of the occluded segment. A balloon tamponade was immediately performed for several minutes with close monitoring of the patient s vital signs. Fortunately, a tiny laceration of the HV was repaired without active bleeding during the procedure, and the patient did not need surgical repair. ORIGINAL ARTICLE 1557

5 LIVER TRANSPLANTATION, November 2016 TABLE 2. Outcomes of the 16 Stent Placement Procedures for Hepatic Venous Outflow Obstruction Pressure Gradient, mm Hg Follow-up, Months Survival Patency Pre Post Stenting Vein Stent Size, mm (Diameter 3 Length) Prestenting Angioplasty Graft Types Patient Number Age Sex 1 52 Male Whole None MHV 12 6 Patent 80 Alive 2 48 Male Right None MHV 16 3 Patent 20 Alive 3 45 Male Right None MHV 29 3 Patent 0.5 Death 4 52 Male Right None MHV 21 2 Occlusion 48 Alive 5 55 Male Left auxiliary partial None LHV 20 3 Patent Alive 6 62 Female Right None MHV 16 4 Patent 6.2 Death 7 56 Male Right None RHV Patent 58 Alive 8 50 Female Right None RIHV 13 4 Patent 19.4 Alive 9 40 Male Right None MHV 17 4 Patent 74.7 Alive Male Right None MHV 14 3 Patent 61.3 Alive Male Right None RHV 5 0 Patent 66 Alive Male Left 1 session LHV 7 1 Patent 5.2 Death Female Whole 1 session RHV 7 0 Patent 36.9 Alive Male Whole None RHV 11 0 Patent 9.1 Death Male Right None RHV 13 2 Patent 29.7 Alive 53 Male Right None RIHV 10 5 Patent 30.1 Alive STENT PATENCY The cumulative primary patency rates of the 16 stents for hepatic venous outflow obstruction after liver transplantation are shown in Fig. 3. The median follow-up period was 33.5 months (range, months), and the overall 1-, 3-, and 5-year primary patency rates were all 93.8%. Six (40%) patients had 5-year followup in this study. Occlusion of the stent developed in only 1 patient (patient number 4 in Table 2). The occlusion was observed during a follow-up Doppler US examination 5 days after the initial procedure, and the occlusion presented without clinical signs and symptoms. In this patient, a stent with a diameter of 8 mm and a length of 40 mm was inserted in the middle hepatic vein (MHV), and the pressure gradient across the stenosis was decreased from 21 to 2 mm Hg on the preprocedural and postprocedural manometries, respectively. One session of balloon angioplasty was performed for the recanalization of the inserted stent, and the stent showed a patent lumen for 50.6 months of the subsequent follow-up period. Including this patient, the secondary patency rate was 100% throughout the follow-up period. The primary patency rates of stents had no statistical difference according to the findings of preprocedural Doppler and CT (nondetectable flow versus detectable flow; P ), and time interval between transplantation and stent placement (<4 weeks versus > 4 weeks; P ). Discussion A hepatic venous outflow obstruction is a relatively rare but life-threatening complication of liver transplantation. The reported incidence of hepatic venous outflow obstruction following liver transplantation ranges from 0.8% to 9.5%. (5,9,11,12) Recently, the number of LDLTs is rapidly increasing, and the incidence of hepatic venous outflow obstruction is not infrequent after an LDLT because of the necessity of multiple hepatic venous anastomoses in this procedure. Early diagnosis and adequate treatment of a hepatic venous outflow obstruction is important for good graft function and patient survival. Endovascular treatment, including percutaneous balloon angioplasty and stent placement, for hepatic venous obstruction is generally accepted to be a useful treatment modality for vascular complications after liver transplantation. (5,6,16,21-23) Kubo et al. (23) performed endovascular treatments for 20 patients with hepatic venous outflow obstruction after liver transplantation ORIGINAL ARTICLE

6 LIVER TRANSPLANTATION, Vol. 22, No. 11, 2016 FIG. 2. Images of a 52-year-old man (patient number 1) who underwent a stent placement for MHV stenosis at 119 days after a deceased donor liver transplantation. (A) A color Doppler US image shows no detectable flow signal at the MHV (arrow), which suggests a hepatic venous outflow obstruction. (B) A transverse contrast-enhanced CT scan obtained in the venous phase that shows a lack of enhancement in both the LHV (arrow) and the MHV (arrowhead) with geographic hepatic parenchymal low attenuation (stars). (C) An anteroposterior middle hepatic venography that shows focal tight stenosis (arrow) at the anastomosis of the MHV to the IVC and numerous collateral vessels. (D) A hepatic venography after the deployment of a stent in the MHV demonstrates the metallic stent (14 mm 3 40 mm) in the MHV without residual stenosis (arrow). The pressure gradient was decreased from 12 to 6 mm Hg. (E) A follow-up transverse CT scan 285 days after stent placement that shows a patent stent (arrow) with the resolution of hepatic parenchymal congestion. ORIGINAL ARTICLE 1559

7 LIVER TRANSPLANTATION, November 2016 FIG. 3. Cumulative primary patency of 16 stents for a hepatic venous outflow obstruction after liver transplantation. An initial balloon venoplasty was technically successful in all patients (technical success rate: 100%), who had improved clinical findings (clinical success rate: 100%). However, 11 (55%) patients had a recurrent obstruction and were treated with either balloon angioplasty or stent placement. The primary patency rates were 80%, 60%, and 60% at 3, 12, and 60 months after venoplasty, respectively, which is suggestive of a high rate of reintervention. Ko et al. (5) performed primary stent placement for early posttransplant hepatic venous outflow obstruction and achieved favorable longterm patency; overall, the 1-, 3-, and 5-year primary patency rates were 82.3%, 75.0%, and 72.4%, respectively. Our results support that stent placement for hepatic venous outflow obstruction in adult liver transplantation recipients is a safe and effective therapeutic option with favorable longterm outcomes. The efficacy parameters of this procedure show excellent results for both technical and clinical success (100.0% and 73.3%, respectively) with a low recurrence rate (6.2%). Therefore, stent placement for hepatic venous outflow obstruction after liver transplantation can be the primary treatment modality because this procedure provides excellent clinical success and longterm patency. The selection of the type and size of stent for each case and careful deployment are important for obtaining a desirable result. Both self-expandable and balloon-expandable stents are good choices and adequate options. A balloon-expandable stent has a more radial stiffness than a self-expandable stent, offering a greater resistance to external pressure, and can be better for the management of fibrotic vascular stenosis. (24) On the other hand, a self-expandable stent has no radial strength limitation, can elastically recover even after being completely flattened or crushed, and has better radial compliance than a balloon-expandable stent. A self-expandable stent becomes part of the anatomy and acts in harmony with native vessels. (25) Wang et al. (12) used short balloon-expandable stents (mean diameter, 14.6 mm 6 1.1; length range, mm) for treating hepatic venous outflow obstructions after liver transplantations, and no significant restenosis was encountered after stent placement (100%, 13 of 13). Ko et al. (5) described their experience with self-expandable stents (diameter range, 6-14 mm; length range, mm) in LDLT recipients (170 anastomoses in 107 patients), in which a 72.4% 5-year primary patency rate was achieved. They showed that the diameter of stents was an independent factor associated with the patency of stents (P ). (5) In the current study, we used short self-expandable stents (diameter range, 7-14 mm; length, 4 cm or shorter in all patients except 1) and achieved 1-, 3-, and 5-year primary patency rates of all 93.8%. The type and size of the stent that allows the best longterm patency has not yet been clearly demonstrated. Although the selection of the type and size of a stent needs to be based on an individual interventional radiologist s experiences and skills, we assume that a selfexpandable stent with relatively large diameter and short length can ensure better longterm patency for treating a hepatic venous outflow obstruction in adult liver transplantation recipients. In LDLTs, when placing an endovascular stent to treat a hepatic venous outflow obstruction, steps should be taken to avoid compromising other hepatic venous drainage. In left lobe grafts, a hepatic venoplasty consisting of the left hepatic vein (LHV) and adjacent veins, such as the left superior vein, MHV, or segment III vein, can be performed to create a single wide orifice without compromising outflow for anastomosis with the recipient s vena cava. (26) For this reason, we considered percutaneous balloon angioplasty to be an appropriate first-line treatment modality in left lobe graft recipients and stent placement to be appropriate for carefully selected cases. We performed stent placement for a hepatic venous outflow obstruction in 2 patients with left lobe grafts, 1 patient with primary stent placement, and 1 patient with recurrence after a percutaneous balloon angioplasty ORIGINAL ARTICLE

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