DOI: 10.1148/radiol.2391050387
(Radiology 2006;239:285-290.)
© RSNA, 2006
Vascular and Interventional Radiology |
Outcome of Percutaneous Transhepatic Venoplasty for Hepatic Venous Outflow Obstruction after Living Donor Liver Transplantation1
Takeshi Kubo, MD,
Toshiya Shibata, MD,
Kyo Itoh, MD,
Yoji Maetani, MD,
Hiroyoshi Isoda, MD,
Masahiro Hiraoka, MD,
Hiroto Egawa, MD,
Koichi Tanaka, MD and
Kaori Togashi, MD
1 From the Departments of Radiology (T.K., T.S., K.I., Y.M., H.I., M.H., K. Togashi) and Transplantation and Immunology (H.E., K. Tanaka), Kyoto University Graduate School of Medicine, 54-Kawaharacho, Shogoin, Sakyoku, Kyoto, 606-8507, Japan. Received March 6, 2005; revision requested April 29; revision received May 20; accepted June 21; final version accepted August 1.
Address correspondence to: T.S. (e-mail: ksj{at}kuhp.kyoto-u.ac.jp).
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ABSTRACT
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Purpose: To evaluate retrospectively the outcome of percutaneous transhepatic venoplasty of hepatic venous outflow obstruction after living donor liver transplantation (LDLT).
Materials and Methods: The institutional Human Subjects Research Review Board approved the interventional protocol and the retrospective study, for which informed consent was not required. Before treatment, informed consent was obtained from the patient or the patient's parents in all cases. Of 26 consecutive patients (nine male, 17 female; median age, 9 years) suspected of having hepatic venous outflow obstruction after LDLT, 20 patients confirmed to have anastomotic outflow stenosis at percutaneous hepatic venography and manometry underwent venoplasty. Pressure gradients before and after venoplasty were evaluated by using a paired t test. Patients in whom obstruction recurred during follow-up were re-treated with venoplasty with or without expandable metallic stents. Patency was analyzed by using Kaplan-Meier analysis.
Results: The initial balloon venoplasty was technically successful in all 20 patients, all of whom had improved clinical findings. The pressure gradient ± standard deviation was reduced from 14.6 mg Hg ± 8.6 to 2.2 mg Hg ± 2.4 (P < .001). Eleven patients had recurrent obstruction and were treated with balloon venoplasty; one of them underwent stent placement, as well as venoplasty. The primary (event-free) patency and 95% confidence interval (CI) at 3, 12, and 60 months after venoplasty were 0.80 (95% CI: 0.62, 0.98), 0.60 (95% CI: 0.38, 0.81), and 0.60 (95% CI: 0.38, 0.81), respectively. The primary assisted patency, maintained with repeated venoplasty and expandable metallic stents, was 1.00 at 60 months.
Conclusion: Percutaneous venoplasty is an effective treatment for hepatic venous outflow obstruction after LDLT.
© RSNA, 2006
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INTRODUCTION
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Liver transplantation is an important option in managing the end stages of liver disease (1,2). Recent improvements in surgical techniques and immunosuppression have contributed to improved posttransplant outcomes. However, a shortage of donors has been one of the major problems in orthotopic liver transplantation (OLT). Living donor liver transplantation (LDLT) has been introduced to solve problems of liver graft shortages (2). Hepatic venous outflow obstruction is a relatively uncommon but important complication after liver transplantation. When outflow obstruction occurs, hepatic congestion can cause massive ascites and hepatic dysfunction. The rate of occurrence of hepatic venous outflow obstruction after OLT is reported to be about 1%, and the rate after LDLT is reported to be about 2%–4% (3,8–10). With the increase in cases of LDLT, management of hepatic venous outflow obstruction has become an important issue (4–7). Thus, the aim of our study was to evaluate retrospectively the outcome of percutaneous transhepatic venoplasty of hepatic venous outflow obstruction after LDLT.
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MATERIALS AND METHODS
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Patients
Between October 1997 and February 2003, 26 consecutive patients (nine male, 17 female; median age, 9 years) clinically suspected of having hepatic venous outflow obstruction were referred to our department of radiology for percutaneous transhepatic procedures. All patients had received left liver grafts from living donors between December 1993 and September 2002 and were suspected of having outflow obstruction because of intractable ascites, abnormal venous flow patterns at Doppler ultrasonography (US), histologic findings suggesting outflow obstruction, or deterioration of liver function not otherwise explained. US findings suggesting outflow obstruction were disappearance of pulsatile hepatic venous flow or flattening of the hepatic venous wave. Liver biopsy findings consistent with hepatic venous outflow obstruction were congestion, hemorrhage, and necrosis around the central veins. Common abnormal laboratory findings included hypoalbuminemia and hyperbilirubinemia.
The Human Subjects Research Review Board at our institution approved our interventional protocol and our retrospective study. The board did not require informed consent for our retrospective study. Informed consent regarding percutaneous hepatic venography and possible interventional procedures was obtained from the patient or the patient's parents. All 26 patients underwent percutaneous hepatic venography. The age of the patients ranged from 10 months to 54 years (median, 9 years) (Table). All patients received liver transplant from a relative. In 16 patients lateral segments (Couinaud segments II and III) of the liver were transplanted, and in 10 patients the left lobe (Couinaud segments II, III, and IV) was used as the graft. Two recipients had received left lobe grafts, while the right lobe of their native liver was left in its original location (auxiliary partial OLT). In all patients, the left hepatic vein or common trunk of the left and middle hepatic veins of the graft were anastomosed with the recipient vein. The mode of anastomosis was end to end (a donor hepatic vein to a recipient hepatic vein stem) or end to side (a donor hepatic vein to a side wall of the recipient inferior vena cava (4). The interval between transplantation and percutaneous venography was 19–3115 days (median, 287 days). The percutaneous procedure was performed with general anesthesia in 19 patients (age range, 10 months to 18 years) and with local anesthesia in seven patients (age range, 12–54 years).
Procedures
Three authors (T.K., T.S., and K.I.) with 9, 18, and 20 years of experience in interventional radiology performed the procedures. The left hepatic vein was punctured with an 18-gauge needle (PTCD; Hanako, Saitama, Japan) designed for percutaneous transhepatic biliary drainage. Transhepatic rather than transluminal puncture of the vein was made with a subxiphoid approach and US guidance. After the inner stylet of the needle was withdrawn and a successful puncture was confirmed, a 0.035-inch stiff guidewire (Cook, Bloomington, Ind) was introduced into the hepatic vein by using the outer needle, and a 7-F interventional sheath introducer (Brite tip; Cordis, Roden, the Netherlands) was inserted over the guidewire. Then, digital subtraction angiography of the hepatic vein was performed in posteroanterior and lateral projections.
Passage through the stenotic segment was attempted with a 0.032-inch angled hydrophilic guidewire (Radifocus; Terumo, Tokyo, Japan) and a 5-F catheter with a hockey stick–shaped tip (Cook). After passage of the catheter, venous pressure on both sides of the stenosis was recorded and the pressure gradient across the stricture—that is, between the right atrium and left hepatic vein—was calculated. Patients with a pressure gradient of more than 3 mm Hg were considered to have significant outflow obstruction requiring treatment and were candidates for venoplasty (see Discussion). A percutaneous transluminal angioplasty catheter (Powerflex Plus; Cordis) with a balloon diameter of 6–10 mm and length of 40 mm was used for venoplasty. The diameter of the balloon was matched to that of the vein on the hepatic side of the stenosis. The balloon was placed across the stenosis and was inflated for 60 seconds with an atmospheric pressure of 10 atm. Dilation with the balloon was performed three times, and venography and manometry were repeated to evaluate the effectiveness of venoplasty. At the end of the procedure, the sheath inserted through the hepatic parenchyma was removed. Hemostasis was obtained with manual compression only, without embolization of the transhepatic track. Patients were not heparinized during the procedure. Immediately after the procedure, heparin was used for 2–3 days as a transition to warfarin (Eisai, Tokyo, Japan). Warfarin was administered from the day after the procedure, usually for more than half a year so that international normalized ratio was maintained in a range of 1.5–2.0.
Follow-up Evaluation
Patients were followed up every 1–2 months. Symptoms, laboratory data of liver function, and Doppler US scans of the hepatic vein were routinely evaluated. When symptoms suggesting hepatic venous obstruction recurred or when disappearance of pulsatile hepatic venous flow or flattening of the hepatic venous wave was noted at Doppler US, percutaneous hepatic venography was repeated; balloon venoplasty was performed when stenosis was confirmed. Expandable metallic stent (EMS) placement was performed in selected patients who were not likely to respond favorably to repeated venoplasty. Candidates for EMS placement included patients who had recurrence in less than 3 months after initial intervention and/or needed balloon venoplasty more than twice. These patients were informed of the reason for the EMS recommendation, its expected effectiveness, and possible disadvantages.
The evaluated items were (a) technical success, (b) manometric findings, (c) complications, (d) outcome of venoplasty and recurrence, and (e) patency rate. One author (T.K.) reviewed the patient's medical records retrospectively.
Technical success was defined as successful puncture of the hepatic vein, passage of a catheter over the stenotic segment, and completion of venoplasty with full expansion of the balloon.
Pressure gradient across the stenotic segment before and after venoplasty was calculated to evaluate the effect of venoplasty. The pressure gradient was calculated as the blood pressure in the left hepatic vein minus that in the right atrium, expressed in millimeters of mercury.
Complications related to the procedures were divided into major and minor categories, in accordance with the complication definitions established by the Society of Interventional Radiology (11). A major complication was defined as any complication that required additional hospital stay for the treatment. Major complications occurring after percutaneous transhepatic interventions for hepatic venous outflow obstruction were hemorrhage requiring transfusion or interventional procedures such as transcatheter arterial embolization, thrombosis of hepatic vein, pneumothorax requiring placement of a chest tube, or pleural effusion requiring thoracentesis. A minor complication was defined as a complication that led to no consequence and thus resulted in completion of the planned procedure. Minor complications evaluated were transient hypotension or abdominal pain.
The outcome of initial venoplasty was defined as presence or absence of recurrent obstruction during the follow-up period. For those with recurrent outflow obstruction, dates and types of additional interventional procedures (balloon venoplasty with or without EMS placement) were documented.
Analysis of patency was performed by using the Kaplan-Meier method. Primary patency or event-free patency was defined as the interval between initial venoplasty and the first appearance of outflow compromise that necessitated percutaneous hepatic venography. Primary assisted patency was defined as patency after initial venoplasty until treatment with repeated percutaneous intervention was abandoned. Repeated venoplasty and EMS placement for restenosis are included in the evaluation of primary assisted patency. Secondary patency after intervention was defined as patency after the treatment of thrombosis with thrombolysis and/or mechanical recanalization until all the attempts at maintaining patency were abandoned. Data were evaluated and estimated at the time of patient death, retransplantation, or the end of follow-up.
Statistical Analysis
Statistical analysis of the pressure gradients before and after venoplasty was performed with a paired t test. P < .05 was considered to indicate a significant difference. Data processing and analysis were performed with commercially available software (SPSS for Windows version 9.0, SPSS, Chicago, Ill).
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RESULTS
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Technical Success
Of 26 patients who underwent venography and manometry, 20 patients had a pressure gradient of more than 3 mm Hg across the anastomotic site, and six had a pressure gradient of 3 mm Hg or less with no apparent stenosis noted at hepatic venography. In 20 patients with a pressure gradient of more than 3 mm Hg, percutaneous hepatic venoplasty was successfully performed; the rate of technical success was 100% (Fig 1).
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Figure 1a: Left lobe graft for biliary atresia in a 1-year-old infant. (a) Lateral hepatic venogram shows almost complete blockage (arrow) of hepatic venous outflow. Pressure gradient between right atrium and left hepatic vein, after passing the catheter, was 15 mm Hg. (b) Fluoroscopic lateral view during balloon venoplasty shows full expansion of the balloon. (c) Lateral hepatic venogram after balloon venoplasty shows improved flow into right atrium (*). The pressure gradient disappeared.
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Figure 1b: Left lobe graft for biliary atresia in a 1-year-old infant. (a) Lateral hepatic venogram shows almost complete blockage (arrow) of hepatic venous outflow. Pressure gradient between right atrium and left hepatic vein, after passing the catheter, was 15 mm Hg. (b) Fluoroscopic lateral view during balloon venoplasty shows full expansion of the balloon. (c) Lateral hepatic venogram after balloon venoplasty shows improved flow into right atrium (*). The pressure gradient disappeared.
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Figure 1c: Left lobe graft for biliary atresia in a 1-year-old infant. (a) Lateral hepatic venogram shows almost complete blockage (arrow) of hepatic venous outflow. Pressure gradient between right atrium and left hepatic vein, after passing the catheter, was 15 mm Hg. (b) Fluoroscopic lateral view during balloon venoplasty shows full expansion of the balloon. (c) Lateral hepatic venogram after balloon venoplasty shows improved flow into right atrium (*). The pressure gradient disappeared.
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Manometric Findings
The mean pressure gradient (blood pressure in the left hepatic vein minus that in the right atrium) ± standard deviation was 14.6 mm Hg ± 8.6 (range, 4–33 mm Hg) before venoplasty and 2.2 mm Hg ± 2.4 (range, 0–8 mm Hg) after venoplasty. A significant difference was noted before and after venoplasty (P < .001).
Complications
No major complications occurred during the procedures. As to minor complication, transient hypotension during balloon dilation was seen in two sessions in two patients, who recovered with conservative treatment.
Outcome of Venoplasty and Recurrence
Clinical signs of outflow obstruction improved in all 20 patients who underwent venoplasty. Eleven patients showed no evidence of recurrent outflow obstruction after the initial venoplasty; follow-up in these patients ranged from 20 to 334 weeks (median, 129 weeks). Nine patients had recurrent outflow obstruction 2–306 weeks (median, 13 weeks) after the initial venoplasty; all were treated with balloon venoplasty again. Of the nine patients, four with early recurrence (<3 months) or multiple recurrences were believed to be candidates for EMS placement. However, three did not undergo EMS placement because the family refused it or the surgeon did not agree with this approach. Thus, eight patients were treated with venoplasty only, and one patient with early recurrence 7 weeks after the initial venoplasty underwent venoplasty followed by EMS placement (Fig 2). The number of sessions of venoplasty ranged from 1 to 4 (mean, 1.7) in each patient.
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Figure 2a: Liver graft because of Byler disease in an 8-year-old boy who underwent successful percutaneous venoplasty 7 weeks earlier. (a) Lateral hepatic venogram shows severe recurrent outflow blockage (arrow) of hepatic venous flow. Pressure gradient between right atrium and left hepatic vein was 12 mm Hg. (b) Fluoroscopic lateral view during balloon venoplasty shows full expansion of the balloon. (c) Lateral hepatic venogram after venoplasty and deployment of EMS demonstrates improved flow into right atrium (*). Pressure gradient was reduced to 4 mm Hg. During 133-week follow-up, no recurrence was noted.
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Figure 2b: Liver graft because of Byler disease in an 8-year-old boy who underwent successful percutaneous venoplasty 7 weeks earlier. (a) Lateral hepatic venogram shows severe recurrent outflow blockage (arrow) of hepatic venous flow. Pressure gradient between right atrium and left hepatic vein was 12 mm Hg. (b) Fluoroscopic lateral view during balloon venoplasty shows full expansion of the balloon. (c) Lateral hepatic venogram after venoplasty and deployment of EMS demonstrates improved flow into right atrium (*). Pressure gradient was reduced to 4 mm Hg. During 133-week follow-up, no recurrence was noted.
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Figure 2c: Liver graft because of Byler disease in an 8-year-old boy who underwent successful percutaneous venoplasty 7 weeks earlier. (a) Lateral hepatic venogram shows severe recurrent outflow blockage (arrow) of hepatic venous flow. Pressure gradient between right atrium and left hepatic vein was 12 mm Hg. (b) Fluoroscopic lateral view during balloon venoplasty shows full expansion of the balloon. (c) Lateral hepatic venogram after venoplasty and deployment of EMS demonstrates improved flow into right atrium (*). Pressure gradient was reduced to 4 mm Hg. During 133-week follow-up, no recurrence was noted.
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Patency Rate
The primary patency rates (Fig 3) and 95% confidence intervals (CIs) at 3, 6, 12, and 60 months after venoplasty were 0.80 (95% CI: 0.62, 0.98), 0.65 (95% CI: 0.44, 0.86), 0.60 (95% CI: 0.38, 0.81), and 0.60 (95% CI: 0.38, 0.81), respectively. The primary assisted and secondary patency rates were 1.00 throughout the follow-up period.
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Figure 3: Kaplan-Meier curve shows the patencies after initial transhepatic venoplasty. Dotted and solid lines indicate primary and primary assisted patency, respectively. Vertical lines on solid and dotted lines indicate censored observations.
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DISCUSSION
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The frequency of hepatic venous outflow obstruction after LDLT is about 2%–4% (3–6). The higher rates of occurrence of venous outflow obstruction in LDLT than in OLT may be attributed to a small anastomotic orifice and growth of the graft in LDLT. In OLT with whole-liver grafts, the retrohepatic inferior vena cava of the recipient is replaced with a donor inferior vena cava, while in LDLT the donor left hepatic vein is anastomosed to the hepatic vein or inferior vena cava of the recipient. In addition, partial liver grafts usually grow considerably after transplantation, so the hepatic venous outlet might be compromised because of distortions of the outlet, such as stretching or twisting.
Diagnosis of outflow obstruction in our study was made with a pressure gradient across the anastomotic site. Ducerf et al (12) measured the pressure gradient across the caval anastomosis between the right atrium and hepatic vein in 40 patients after OLT. A mean pressure gradient was less than 3 mm Hg (0.75 mm Hg ± 0.49 and 2.06 mm Hg ± 0.85 for two anastomosis techniques). A pressure gradient of 3 mm Hg or less between the right atrium and the hepatic vein might not be pathologic and probably represents the physiologic difference between intrathoracic and intraperitoneal pressure. Conversely, if the pressure gradient is greater than 3 mm Hg, there might be an additional increase of pressure at the site of anastomosis that is reversible with venoplasty. In previous reports (13,14), the pressure gradient was reduced to 3 mm Hg or less after treatment with metallic stents in all patients. Therefore, it seems reasonable to treat patients with a pressure gradient of more than 3 mm Hg between the hepatic vein and the right atrium, especially in patients clinically suspected of having hepatic venous obstruction.
Hepatic venous outflow obstruction immediately after transplantation is a surgical emergency, and reoperation is usually necessary for correction (4,15). On the other hand, late-onset hepatic venous outflow obstruction can cause insidious deterioration of liver function, and surgical correction is usually difficult because fibrotic changes develop around the anastomotic site. Thus interventional procedures are preferred to surgical venoplasty in that situation (9,16,17). For hepatic venous outflow obstruction after OLT from a cadaveric donor, anastomotic stenosis in the inferior vena cava has been treated with balloon venoplasty and EMS placement (18–20). For hepatic venous outflow obstruction after LDLT, balloon venoplasty with or without EMS placement has been used for treatment (8–10). Ko et al (10) reported on 27 patients who received percutaneous interventional treatment for hepatic venous outflow obstruction and advocated the use of EMS in this condition. However, we do not advocate the use of EMS as an initial treatment for three reasons.
First, if primary stent placement is performed routinely, a number of patients may undergo unnecessary EMS placement. In our study, long-term follow-up showed effectiveness of percutaneous intervention in the treatment of hepatic venous outflow obstruction. Both primary assisted patency and secondary patency at 60 months after the initial venoplasty were 1.00; therefore, all patients can be treated with percutaneous intervention. The primary patency remained as high as 0.60 at 60 months; therefore, many patients had patent outflow with one-session venoplasty only. Although recurrent outflow obstructions were frequent in the first 6 months, far fewer patients had recurrence after 6 months. Second, our patients were mostly infants or children. Long-term patency of EMS for decades is unknown. Moreover, when a patient with a transplant grows, the size of the graft hepatic vein may not match the size of the implanted EMS. Third, retransplantation is possible. If primary disease relapses or progressive rejection occurs, retransplantation should be considered. At retransplantation, the presence of EMS in the wall of the suprahepatic inferior vena cava would be technically a challenge for surgeons. Although some patients who undergo multiple interventions might also benefit from EMS placement, our strategy for treating venous outflow obstruction is to attempt venoplasty first; if outflow obstruction recurs, we usually perform additional venoplasty and then consider EMS placement.
In our study, a transhepatic approach to the hepatic vein was used in all cases. Venoplasty can also be performed with a percutaneous transluminal approach, that is, with a transjugular or transfemoral approach (10). Both transhepatic and transluminal approaches are technically easy. However, negotiation of stenotic segments seems to be much easier with a transhepatic approach because passage through the stenosis is much more straightforward with the transhepatic approach than with the transluminal approach. Easier negotiation through the stenosis leads to shorter procedure time and less exposure of the patient to ionizing radiation. This is especially important for infant patients. Injury to the hepatic parenchyma might be a theoretical disadvantage of the transhepatic approach. However, in this study, complications such as hemorrhage were not caused by a direct puncture of the liver.
There were limitations in our study. The number of our patients (n = 24) might not have been enough to evaluate the complications of percutaneous transhepatic interventional procedures, and further clinical studies are needed to establish the safety of the procedures by comparing the transluminal approach. Although only one patient underwent EMS placement, the long-term outcome between venoplasty with and that without EMS placement should be compared in the future.
In conclusion, balloon venoplasty was safe and effective for venous outflow obstruction after LDLT, while some refractory cases might benefit from EMS placement. Percutaneous transhepatic interventional procedures should be considered in patients with venous outflow obstruction after LDLT.
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ADVANCE IN KNOWLEDGE
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- Percutaneous venoplasty is an effective treatment for hepatic venous outflow obstruction after living donor liver transplantation.
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FOOTNOTES
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Abbreviations: CI = confidence interval • EMS = expandable metallic stent • LDLT = living donor liver transplantation • OLT = orthotopic liver transplantation
Author contributions: Guarantors of integrity of entire study, T.K., T.S., K.I.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, T.K., T.S., K.I., H.I., K. Togashi; clinical studies, T.K., T.S., K.I., Y.M., H.E., K. Tanaka; statistical analysis, T.S., Y.M.; and manuscript editing, H.I., M.H., H.E., K. Tanaka, K. Togashi
Authors stated no financial relationship to disclose.
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ABSTRACT
INTRODUCTION
