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Treatment of Hepatic Venous Outflow Obstruction after Piggyback Liver Transplantation¹

¹ From the Division of Vascular and Interventional Radiology (S.L.W., D.Y.S., M.K.R., S.T.K., J.K.F., M.D.D.) and Department of Surgery (Transplantation) (S.B.), Stanford University Medical Center, H3646, 300 Pasteur Dr, Stanford, CA 94305-5642. Received February 19, 2004; revision requested April 29; final revision received July 30; accepted September 29. Address correspondence to D.Y.S. (e-mail: dansze{at}stanford.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To evaluate retrospectively the endovascular management of hepatic venous outflow obstruction after piggyback orthotopic liver transplantation.

MATERIALS AND METHODS: The study was performed with the approval and under the guidelines of the institutional review board and complied with the Health Insurance Portability and Accountability Act. Informed consent from patients was not required by the institutional review board for this retrospective study. From 1995 to 2003, 13 patients (eight male, five female), including 12 adults and one adolescent (age range, 14–67 years; median age, 52 years), underwent endovascular treatment of hepatic venous outflow obstruction after piggyback orthotopic liver transplantation. Patients gave informed consent for all procedures. Eleven patients received whole livers, and two received living-related donor right liver lobes. Four underwent repeat piggyback orthotopic liver transplantation prior to intervention. Primary stent placement was performed in 12 patients. One patient refused primary stent placement and chose venoplasty alone, but required a stent 5 months later. Short balloon-expandable stents (mean diameter, 14.6 mm ± 1.1 [standard deviation]) were used to minimize jailing of branch vessels and to resist recoil. Pre- and postprocedural pressure gradients were measured. Follow-up included venography, cross-sectional imaging, and laboratory tests. The Wilcoxon signed rank test or the sign test was performed to compare pre- and postprocedural pressure gradients, body weights, and laboratory values.

RESULTS: Technical success (pressure gradient 3 mm Hg) was achieved in 13 of 13 patients, and clinical success, in 12 of 13. Mean pre- and postprocedural pressure gradients were 13.0 mm Hg ± 1.4 and 0.8 mm Hg ± 0.3. Mean interval from transplantation to intervention was 348 days ± 159. Mean follow-up was 678 days (range, 16–2880 days). Technical success did not result in clinical improvement in one patient. Biopsy demonstrated severe hepatic necrosis, likely from prolonged venous congestion, and the patient required repeat transplantation. Only one patient required reintervention for stent migration, and no other complications occurred. No significant restenosis was encountered after stent placement.

CONCLUSION: Hepatic venous outflow obstruction is an uncommon but potentially fatal complication of piggyback orthotopic liver transplantation. Endovascular treatment with balloon-expandable stents is effective, safe, and apparently durable.

© RSNA, 2005

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
In 1968, Calne and Williams (1) described a method of orthotopic liver transplantation that incorporated preservation of the retrohepatic inferior vena cava (IVC). Over the last several years, increasing international experience and acceptance of the piggyback technique for orthotopic liver transplantation have made it the preferred method for liver transplantation at many institutions, including our own (2). Variations in this technique have led to its popularity, given the increasing number of living donor transplantations and orthotopic liver transplantations in pediatric patients, in whom a size mismatch between the graft and the recipient makes the standard technique challenging. Modern advances in the piggyback technique have shortened the anhepatic phase and obviated venous bypass (2,3). Several investigators (2–6) have shown improved hemodynamic stability, particularly during the anhepatic phase, with lower numbers of technique-related surgical complications and a diminished need for intraoperative blood products with this technique.

A rare but potentially catastrophic complication of piggyback orthotopic liver transplantation is hepatic venous outflow obstruction. Various authors have described an incidence of 1%–7%, with many occurrences in the immediate or early postoperative period (4,7–9). Hepatic venous outflow obstruction typically occurs at the hepatic venous anastomosis with the suprahepatic IVC and may be chronic (10). Manifestation typically occurs with symptoms of hepatic congestion, Budd-Chiari syndrome, and, frequently, IVC obstruction. Short-term results of endovascular treatment of hepatic venous outflow obstruction by using the minimally invasive techniques of venoplasty and balloon-expandable stent placement were previously reported in two patients (11). The purpose of our study was to evaluate retrospectively the endovascular management of hepatic venous outflow obstruction after piggyback orthotopic liver transplantation.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Patient Population and Transplantation Procedures
This retrospective study was performed with the approval of and under the guidelines of the institutional review board and complied with the Health Insurance Portability and Accountability Act. Informed consent from patients was not required by the institutional review board for this retrospective study. Patients gave informed consent for all procedures performed.

From May 1995 through July 2003, 13 patients who had previously undergone piggyback orthotopic liver transplantation underwent treatment for hepatic venous outflow obstruction with endovascular placement of balloon-expandable stents. In 12 patients, transplantation was performed by our institution's liver transplantation team; one patient underwent transplantation at another university medical center and was subsequently transferred to our institution for long-term care. There were eight male patients and five female patients with an age range of 14–67 years and a median age of 52 years. Only one pediatric patient, who was 14 years old but had the body size of an adult, was included. Four of the patients had undergone a second liver transplantation, also performed with a piggyback anastomosis, prior to endovascular intervention. Two of the 13 patients had undergone living donor transplantation of the right hepatic lobe. The remaining 11 patients had undergone cadaveric piggyback orthotopic whole-liver transplantation. Under our institution's liver transplantation team, 352 liver transplantations were performed with the piggyback technique during the study period, including 43 living donor transplantations, 46 cadaveric split or partial orthotopic liver transplantations, and 263 cadaveric orthotopic whole-liver transplantations. Overall incidence of hepatic venous outflow obstruction was 3.4% (12 of 352) after piggyback orthotopic liver transplantation, 4.7% (two of 43) after living donor liver transplantation, and 3.8% (10 of 263) after cadaveric piggyback orthotopic whole-liver transplantation. (The study patient who underwent transplantation surgery at another institution is not included in these statistics.) Pretransplantation liver diseases that necessitated transplantation included hepatitis C (n = 4), hepatitis C–related and alcoholic cirrhosis (n = 2), primary biliary cirrhosis (n = 2), primary sclerosing cholangitis (n = 1), hepatitis B (n = 1), ₁-antitrypsin deficiency (n = 1), and cryptogenic cirrhosis (n = 2).

In the 11 cadaveric piggyback orthotopic whole-liver transplantations, the donor suprahepatic IVC was anastomosed to a vascular cuff, which was formed by combining the lumina of multiple recipient hepatic veins. In eight of these 11 cases, the vascular cuff comprised the middle and left hepatic veins, while in the remaining three cases it comprised the right, middle, and left hepatic veins. The IVC was preserved and remained fully patent during all of these procedures.

In the two patients who underwent living donor right hepatic lobe transplantation with the piggyback procedure, small cavotomies were created in the side of the recipient IVC, and the donor right hepatic veins were anastomosed to the recipient IVC in an end-to-side fashion. The recipient's middle and left hepatic vein stumps were oversewn.

Diagnosis of Hepatic Venous Outflow Obstruction
Diagnosis of hepatic venous outflow obstruction was determined from findings at computed tomography (CT), magnetic resonance (MR) imaging, venography, Doppler ultrasonography (US), and/or clinical manifestations. US was performed by using color Doppler and/or power Doppler imaging (Sequoia; Acuson/Siemens Medical Solutions, Malvern, Pa). Biphasic contrast material–enhanced CT examinations were performed with a standard liver protocol and with a single–detector row scanner (HiSpeed CT; GE Medical Systems, Milwaukee, Wis) or a four–detector row scanner (LightSpeed QX/i; GE Medical Systems) in the earlier portion of this study and with an eight–detector row scanner (LightSpeed Ultra; GE Medical Systems) or 16–detector row CT scanner (LightSpeed 16; GE Medical Systems) later in the study. CT section thicknesses were 2.5 mm in the arterial phase and 5.0 mm in the portal venous phase. MR imaging was performed by using a 1.5-T magnet (Signa EchoSpeed; GE Medical Systems) with standard sequences: transverse spoiled gradient-recalled echo, transverse gradient-recalled echo, coronal contrast-enhanced angiography, and transverse contrast-enhanced gradient-recalled echo. All pre- and postprocedural cross-sectional diagnostic imaging studies were prospectively interpreted by attending physicians of the radiology department and reviewed for definitive interpretation by one of the authors (D.Y.S.).

All patients underwent venography with measurement of pressure gradients in the hepatic vein and right atrium. At Doppler US, hepatic venous outflow obstruction was suspected when hepatic venous spectral waveforms were dampened or monophasic (n = 4), when low flow velocity or absence of flow was depicted in the hepatic vein (n = 1), or when stenosis was depicted in the anastomosis of the native hepatic vein to the donor suprahepatic IVC (n = 2). At CT and MR imaging, obstruction was suspected when a stenotic segment in the hepatic venous anastomosis was identified or when little or no contrast was noted in the hepatic vein (n = 2). In addition, early-phase transverse images that showed predominant central enhancement, combined with later images that showed predominant peripheral enhancement, were suspicious for venous outflow obstruction.

In nine of the 13 patients, hepatic venous outflow obstruction was included in the differential diagnosis on the basis of clinical manifestations. Initial manifestations often included abdominal pain, weight gain, ascites, lower-extremity edema, pleural effusion, hepatosplenomegaly, and worsening hepatic function as manifested by increasing serum bilirubin and coagulation parameters and decreasing serum albumin. Eight of the 13 patients underwent transvenous liver biopsy prior to stent placement.

Venography and Stent Placement
Informed consent was obtained from each patient after an explanation of the procedure, objectives, risks, and alternatives. Each patient gave written consent for the off-label use of stents, a practice for which our institutional review board does not require its approval. Eleven procedures were performed by one practitioner (D.Y.S., who completed an interventional radiology fellowship in 1997), and two procedures were performed by another practitioner (M.K.R., who completed the fellowship in 1995). All procedures were performed for the medical care of patients and not for research purposes.

A right internal jugular venous approach was used in 11 patients, a left internal jugular venous approach was used in one patient, and a right femoral venous approach was used in one patient. In nine patients who had lower-extremity edema and/or azotemia, flush venography of the IVC was performed by using a pigtail catheter, and pressure gradients were measured in the infrahepatic IVC and right atrium. In all patients, transplant hepatic veins were selected, and venography was performed by using pigtail catheters. In one patient, traversal of the stenosis required US-guided percutaneous access to the donor right hepatic vein by using a 22-gauge needle and 0.018-inch guidewire, which was then snared in the IVC from the jugular venous access. Pressure gradients were measured in the right atrium and the hepatic vein prior to stent placement. Measurement of each stenotic region was performed at multiple obliquities to ensure the proper stent size. In one especially complex case, intravascular US (Jomed, Rancho Cordova, Calif) was performed to characterize the anastomosis. A single balloon-expandable stainless steel stent was deployed across the strictured region and subsequently dilated with size-appropriate balloons. Stents (Palmaz, Palmaz Genesis XD; Cordis/Johnson & Johnson, Warren, NJ) ranged from 18 to 30 mm in initial length and from 10 to 25 mm in final diameter (mean, 14.6 mm ± 1.1 [standard deviation]). The donor side of the piggyback anastomosis was composed of the donor suprahepatic IVC, and the recipient side of the anastomosis was composed of a single hepatic venous cuff fashioned from two or three recipient hepatic veins, so stent diameters were maximized to match the large normal diameters of these vessels. Postintervention pressure measurements were then obtained in the hepatic vein and right atrium, and pressure gradients were calculated. The average time from transplantation to stent placement was 349 days ± 159 (median, 114 days). Only two patients required stent placement within 30 days of transplantation (on posttransplantation days 3 and 6).

Follow-up and Analysis
After stent deployment and hepatic venography, technical success was evaluated on the basis of resolution of the venographic stenosis, pace of blood flow, and a clinically important reduction in pressure gradient to 3 mm Hg or less (12). Doppler US was performed within 24 hours after stent placement. Subsequent follow-up was performed at approximately 3-month intervals, primarily with Doppler US; however, CT, MR imaging, and venography also were performed if posttransplantation complications were suspected. Laboratory follow-up analyses were performed according to the standard protocol of the liver transplantation service, and all patients underwent postprocedural evaluation at 1 month after intervention. The clinical follow-up interval was decided on an individual basis by the hepatologist but typically was every 1–3 months for 1 year after stent placement.

The outcome of the procedure was evaluated retrospectively with regard to technical success, clinical improvement, major procedure-related complications, and recurrence of hepatic venous outflow obstruction. Technical success was defined by resolution of stenosis on the venogram, a normal velocity of blood flow through the anastomosis, and a postprocedural pressure gradient of 3 mm Hg or less. The velocity of blood flow was judged and pre- and postprocedural pressure gradients were measured by one of two interventional radiologists (D.Y.S., M.K.R.).

Clinical improvement was assessed by the patients, transplantation surgeons, hepatologists, and interventional radiologists with an evaluation of signs and symptoms, including abdominal pain, ascites, lower-extremity edema, and pleural effusion. Assessment was largely subjective, but body weight was measured to determine the presence of diuresis and resolution of ascites, pleural effusion, and edema. Clinical improvement was also determined with 1-month follow-up laboratory evaluation. Changes in serum albumin, aspartate aminotransferase, alanine aminotransferase, total bilirubin, creatinine, and alkaline phosphatase levels, in prothrombin time, and in patient weight were calculated at the 1-month postprocedural follow-up examination (S.L.W.).

Major procedure-related complications were defined as those directly related to the stent placement, including stent migration, visceral or vascular injury secondary to the procedure, unintended location of stent deployment, or any complications necessitating reintervention or prolonged hospital stay or resulting in permanent morbidity or death. Recurrence was defined as redemonstration of US, venographic, CT, or MR imaging findings or recurrence of clinical symptoms suggestive of hepatic venous outflow obstruction, confirmed by an increased pressure gradient (>3 mm Hg) at the time of venography.

Statistical Analysis
Where symmetry assumptions were borne out by the data, the Wilcoxon signed rank test was performed to evaluate differences in pre- and postprocedural body weights, as well as hepatic laboratory values including serum albumin, total bilirubin, and prothrombin time. Where symmetry assumptions were not met, the sign test was performed to evaluate differences in pre- and postprocedural pressure gradients and levels of aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, and serum creatinine. Results were also stratified by age and sex by using a Spearman (ordinal correlation coefficient) test for age and a Mann-Whitney U test for sex. Statistical analysis was performed by our departmental statistician with software (SPSS, version 11.0; SPSS, Chicago, Ill). P values less than .05 were considered to indicate a statistically significant difference, while those between .05 and .10 were considered to indicate a difference with marginal significance.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Technical Success and Clinical Improvement
Technical success was achieved in all 13 patients (100%) (Fig 1). Clinical improvement was noted in 12 (92%) of 13 patients. The mean change in pressure gradient across the stenosis was –12.2 mm Hg ± 1.5 (P < .001) (Table). Female patients demonstrated a larger decrease in pressure gradient than did male patients (–15.6 vs –8.6 mm Hg, P = .019). No other parameters differed between the sexes. Tissue specimens from biopsies performed at the time of stent placement were interpreted by the pathologists as indicative of centrilobular congestion (n = 2), regions of ischemia and necrosis (n = 1), large duct obstruction (n = 1), acute rejection (n = 3), and chronic rejection (n = 1).

View larger version (128K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. Images in 52-year-old woman 191 days after second piggyback transplantation for primary biliary cirrhosis with ascites and poor liver function. (a) Transverse contrast-enhanced CT scan obtained in venous phase at level of hepatic venous confluence shows lack of enhancement of parenchyma and hepatic veins (arrowheads) because of venous obstruction, with avid filling of gastroesophageal varices (arrow). (b) Anteroposterior right hepatic venogram shows venous engorgement and stasis, with occlusion of anastomosis by 10-F sheath (arrow).(c) Fluoroscopic image shows balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) deployed over 12-mm-diameter balloon centered in stenosis. (d) Repeat venogram demonstrates resolution of engorgement, stasis, and stenosis. The pressure gradient decreased from 23 to 0 mm Hg. (e) Follow-up transverse CT scan 723 days after stent placement shows resolution of congestion and ascites and decreased variceal enhancement.

View larger version (125K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. Images in 52-year-old woman 191 days after second piggyback transplantation for primary biliary cirrhosis with ascites and poor liver function. (a) Transverse contrast-enhanced CT scan obtained in venous phase at level of hepatic venous confluence shows lack of enhancement of parenchyma and hepatic veins (arrowheads) because of venous obstruction, with avid filling of gastroesophageal varices (arrow). (b) Anteroposterior right hepatic venogram shows venous engorgement and stasis, with occlusion of anastomosis by 10-F sheath (arrow).(c) Fluoroscopic image shows balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) deployed over 12-mm-diameter balloon centered in stenosis. (d) Repeat venogram demonstrates resolution of engorgement, stasis, and stenosis. The pressure gradient decreased from 23 to 0 mm Hg. (e) Follow-up transverse CT scan 723 days after stent placement shows resolution of congestion and ascites and decreased variceal enhancement.

View larger version (136K): [in this window] [in a new window] [Download PPT slide]   Figure 1c. Images in 52-year-old woman 191 days after second piggyback transplantation for primary biliary cirrhosis with ascites and poor liver function. (a) Transverse contrast-enhanced CT scan obtained in venous phase at level of hepatic venous confluence shows lack of enhancement of parenchyma and hepatic veins (arrowheads) because of venous obstruction, with avid filling of gastroesophageal varices (arrow). (b) Anteroposterior right hepatic venogram shows venous engorgement and stasis, with occlusion of anastomosis by 10-F sheath (arrow).(c) Fluoroscopic image shows balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) deployed over 12-mm-diameter balloon centered in stenosis. (d) Repeat venogram demonstrates resolution of engorgement, stasis, and stenosis. The pressure gradient decreased from 23 to 0 mm Hg. (e) Follow-up transverse CT scan 723 days after stent placement shows resolution of congestion and ascites and decreased variceal enhancement.

View larger version (141K): [in this window] [in a new window] [Download PPT slide]   Figure 1d. Images in 52-year-old woman 191 days after second piggyback transplantation for primary biliary cirrhosis with ascites and poor liver function. (a) Transverse contrast-enhanced CT scan obtained in venous phase at level of hepatic venous confluence shows lack of enhancement of parenchyma and hepatic veins (arrowheads) because of venous obstruction, with avid filling of gastroesophageal varices (arrow). (b) Anteroposterior right hepatic venogram shows venous engorgement and stasis, with occlusion of anastomosis by 10-F sheath (arrow).(c) Fluoroscopic image shows balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) deployed over 12-mm-diameter balloon centered in stenosis. (d) Repeat venogram demonstrates resolution of engorgement, stasis, and stenosis. The pressure gradient decreased from 23 to 0 mm Hg. (e) Follow-up transverse CT scan 723 days after stent placement shows resolution of congestion and ascites and decreased variceal enhancement.

View larger version (116K): [in this window] [in a new window] [Download PPT slide]   Figure 1e. Images in 52-year-old woman 191 days after second piggyback transplantation for primary biliary cirrhosis with ascites and poor liver function. (a) Transverse contrast-enhanced CT scan obtained in venous phase at level of hepatic venous confluence shows lack of enhancement of parenchyma and hepatic veins (arrowheads) because of venous obstruction, with avid filling of gastroesophageal varices (arrow). (b) Anteroposterior right hepatic venogram shows venous engorgement and stasis, with occlusion of anastomosis by 10-F sheath (arrow).(c) Fluoroscopic image shows balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) deployed over 12-mm-diameter balloon centered in stenosis. (d) Repeat venogram demonstrates resolution of engorgement, stasis, and stenosis. The pressure gradient decreased from 23 to 0 mm Hg. (e) Follow-up transverse CT scan 723 days after stent placement shows resolution of congestion and ascites and decreased variceal enhancement.

In the patient in whom clinical improvement was not achieved, the preprocedural pressure gradient was 10 mm Hg and the postprocedural gradient was 0 mm Hg. This patient required placement of a stent in the hepatic vein approximately 1 month after receiving a right hepatic lobe graft from a living donor. Pre- and postprocedural biopsies in this patient demonstrated confluent regions of severe central hepatic necrosis, which had resulted in bile duct necrosis. The severe ischemic changes were surmised to be secondary to the hepatic venous outflow obstruction and subsequent infarction. This patient's immediate postoperative course was also complicated by upper gastrointestinal tract bleeding, which required embolization, as well as by sepsis and renal failure, which complicated and delayed the diagnosis of hepatic venous outflow obstruction. The patient ultimately required repeat transplantation 2 months after receiving the initial transplant.

Causes of Obstruction
The cause of the venous outflow obstruction, given the delayed onset, was presumed to be intimal hyperplasia and fibrosis in 11 of 13 patients. This diagnosis was based on the venographic, US, and CT characteristics of obstruction. In two of these 11 patients, calcification was seen in the stenotic anastomosis, a finding that supported a determination of fibrosis as the cause. The other two patients required intervention at the 3rd and 6th postoperative days after transplantation, respectively, suggesting a positional origin of obstruction (from torsion, kinking, or compression) (Fig 2).

View larger version (60K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. US images in 26-year-old man 6 days after second piggyback transplantation following liver transplant rejection and chronic hepatitis B with ascites and pleural effusion. (a) Oblique coronal color Doppler US image of right hepatic vein shows high-grade anastomotic stenosis (arrow) with monophasic color Doppler waveform that indicates low flow velocity. (b–f) Intravascular US images. Left: Cross-sectional image. Right: Composite longitudinal image oriented with liver (arrow in b) at top and with right atrium (arrowhead in b) at bottom of image. (b) Engorged intrahepatic branches of hepatic veins (*). (c) Tapered lumen of donor IVC. (d) Tight anastomotic stricture (#). (e) Redundant tissue near suture line (arrowheads). (f) Normal recipient IVC. (g) After placement of a stent (Palmaz Genesis XD 1910; Cordis/Johnson & Johnson) dilated to 18 mm diameter, the pressure gradient was reduced from 14 to 3 mm Hg. Oblique coronal color Doppler US image obtained at follow-up shows resolution of stenosis and appearance of normal multiphasic waveform reflecting pulsatility of right heart and augmentation due to respiration, and an approximately fourfold increase in flow.

View larger version (102K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. US images in 26-year-old man 6 days after second piggyback transplantation following liver transplant rejection and chronic hepatitis B with ascites and pleural effusion. (a) Oblique coronal color Doppler US image of right hepatic vein shows high-grade anastomotic stenosis (arrow) with monophasic color Doppler waveform that indicates low flow velocity. (b–f) Intravascular US images. Left: Cross-sectional image. Right: Composite longitudinal image oriented with liver (arrow in b) at top and with right atrium (arrowhead in b) at bottom of image. (b) Engorged intrahepatic branches of hepatic veins (*). (c) Tapered lumen of donor IVC. (d) Tight anastomotic stricture (#). (e) Redundant tissue near suture line (arrowheads). (f) Normal recipient IVC. (g) After placement of a stent (Palmaz Genesis XD 1910; Cordis/Johnson & Johnson) dilated to 18 mm diameter, the pressure gradient was reduced from 14 to 3 mm Hg. Oblique coronal color Doppler US image obtained at follow-up shows resolution of stenosis and appearance of normal multiphasic waveform reflecting pulsatility of right heart and augmentation due to respiration, and an approximately fourfold increase in flow.

View larger version (113K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. US images in 26-year-old man 6 days after second piggyback transplantation following liver transplant rejection and chronic hepatitis B with ascites and pleural effusion. (a) Oblique coronal color Doppler US image of right hepatic vein shows high-grade anastomotic stenosis (arrow) with monophasic color Doppler waveform that indicates low flow velocity. (b–f) Intravascular US images. Left: Cross-sectional image. Right: Composite longitudinal image oriented with liver (arrow in b) at top and with right atrium (arrowhead in b) at bottom of image. (b) Engorged intrahepatic branches of hepatic veins (*). (c) Tapered lumen of donor IVC. (d) Tight anastomotic stricture (#). (e) Redundant tissue near suture line (arrowheads). (f) Normal recipient IVC. (g) After placement of a stent (Palmaz Genesis XD 1910; Cordis/Johnson & Johnson) dilated to 18 mm diameter, the pressure gradient was reduced from 14 to 3 mm Hg. Oblique coronal color Doppler US image obtained at follow-up shows resolution of stenosis and appearance of normal multiphasic waveform reflecting pulsatility of right heart and augmentation due to respiration, and an approximately fourfold increase in flow.

View larger version (114K): [in this window] [in a new window] [Download PPT slide]   Figure 2d. US images in 26-year-old man 6 days after second piggyback transplantation following liver transplant rejection and chronic hepatitis B with ascites and pleural effusion. (a) Oblique coronal color Doppler US image of right hepatic vein shows high-grade anastomotic stenosis (arrow) with monophasic color Doppler waveform that indicates low flow velocity. (b–f) Intravascular US images. Left: Cross-sectional image. Right: Composite longitudinal image oriented with liver (arrow in b) at top and with right atrium (arrowhead in b) at bottom of image. (b) Engorged intrahepatic branches of hepatic veins (*). (c) Tapered lumen of donor IVC. (d) Tight anastomotic stricture (#). (e) Redundant tissue near suture line (arrowheads). (f) Normal recipient IVC. (g) After placement of a stent (Palmaz Genesis XD 1910; Cordis/Johnson & Johnson) dilated to 18 mm diameter, the pressure gradient was reduced from 14 to 3 mm Hg. Oblique coronal color Doppler US image obtained at follow-up shows resolution of stenosis and appearance of normal multiphasic waveform reflecting pulsatility of right heart and augmentation due to respiration, and an approximately fourfold increase in flow.

View larger version (114K): [in this window] [in a new window] [Download PPT slide]   Figure 2e. US images in 26-year-old man 6 days after second piggyback transplantation following liver transplant rejection and chronic hepatitis B with ascites and pleural effusion. (a) Oblique coronal color Doppler US image of right hepatic vein shows high-grade anastomotic stenosis (arrow) with monophasic color Doppler waveform that indicates low flow velocity. (b–f) Intravascular US images. Left: Cross-sectional image. Right: Composite longitudinal image oriented with liver (arrow in b) at top and with right atrium (arrowhead in b) at bottom of image. (b) Engorged intrahepatic branches of hepatic veins (*). (c) Tapered lumen of donor IVC. (d) Tight anastomotic stricture (#). (e) Redundant tissue near suture line (arrowheads). (f) Normal recipient IVC. (g) After placement of a stent (Palmaz Genesis XD 1910; Cordis/Johnson & Johnson) dilated to 18 mm diameter, the pressure gradient was reduced from 14 to 3 mm Hg. Oblique coronal color Doppler US image obtained at follow-up shows resolution of stenosis and appearance of normal multiphasic waveform reflecting pulsatility of right heart and augmentation due to respiration, and an approximately fourfold increase in flow.

View larger version (116K): [in this window] [in a new window] [Download PPT slide]   Figure 2f. US images in 26-year-old man 6 days after second piggyback transplantation following liver transplant rejection and chronic hepatitis B with ascites and pleural effusion. (a) Oblique coronal color Doppler US image of right hepatic vein shows high-grade anastomotic stenosis (arrow) with monophasic color Doppler waveform that indicates low flow velocity. (b–f) Intravascular US images. Left: Cross-sectional image. Right: Composite longitudinal image oriented with liver (arrow in b) at top and with right atrium (arrowhead in b) at bottom of image. (b) Engorged intrahepatic branches of hepatic veins (*). (c) Tapered lumen of donor IVC. (d) Tight anastomotic stricture (#). (e) Redundant tissue near suture line (arrowheads). (f) Normal recipient IVC. (g) After placement of a stent (Palmaz Genesis XD 1910; Cordis/Johnson & Johnson) dilated to 18 mm diameter, the pressure gradient was reduced from 14 to 3 mm Hg. Oblique coronal color Doppler US image obtained at follow-up shows resolution of stenosis and appearance of normal multiphasic waveform reflecting pulsatility of right heart and augmentation due to respiration, and an approximately fourfold increase in flow.

View larger version (66K): [in this window] [in a new window] [Download PPT slide]   Figure 2g. US images in 26-year-old man 6 days after second piggyback transplantation following liver transplant rejection and chronic hepatitis B with ascites and pleural effusion. (a) Oblique coronal color Doppler US image of right hepatic vein shows high-grade anastomotic stenosis (arrow) with monophasic color Doppler waveform that indicates low flow velocity. (b–f) Intravascular US images. Left: Cross-sectional image. Right: Composite longitudinal image oriented with liver (arrow in b) at top and with right atrium (arrowhead in b) at bottom of image. (b) Engorged intrahepatic branches of hepatic veins (*). (c) Tapered lumen of donor IVC. (d) Tight anastomotic stricture (#). (e) Redundant tissue near suture line (arrowheads). (f) Normal recipient IVC. (g) After placement of a stent (Palmaz Genesis XD 1910; Cordis/Johnson & Johnson) dilated to 18 mm diameter, the pressure gradient was reduced from 14 to 3 mm Hg. Oblique coronal color Doppler US image obtained at follow-up shows resolution of stenosis and appearance of normal multiphasic waveform reflecting pulsatility of right heart and augmentation due to respiration, and an approximately fourfold increase in flow.

View larger version (129K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Left anterior oblique venograms (45° angle) in 60-year-old man 1108 days after piggyback transplantation for chronic hepatitis C and cirrhosis with massive ascites. (a) View of IVC shows long and tapered stenosis (arrow) suggestive of external compression from congested liver. Because the anastomosis could not be crossed in a direction retrograde to the jugular venous access, percutaneous US-guided access to the right hepatic vein was obtained by using a 22-gauge needle. (b) Percutaneous hepatic venogram helps to confirm near-occlusion at the anastomosis (arrow) and stasis of flow. (c) Fluoroscopic image shows 0.018-inch nitinol guidewire (Microvena, White Bear Lake, Minn) passed through the anastomosis and snared in the IVC (Amplatz gooseneck snare; Microvena). (d) Completion venogram shows deployment of balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) via jugular vein. After dilation of the stent to 12 mm, the 14 mm Hg pressure gradient was eliminated and rapid flow was achieved. Follow-up US examination 64 days later (not shown) demonstrated resolution of ascites and no evidence of residual IVC stenosis.

View larger version (126K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Left anterior oblique venograms (45° angle) in 60-year-old man 1108 days after piggyback transplantation for chronic hepatitis C and cirrhosis with massive ascites. (a) View of IVC shows long and tapered stenosis (arrow) suggestive of external compression from congested liver. Because the anastomosis could not be crossed in a direction retrograde to the jugular venous access, percutaneous US-guided access to the right hepatic vein was obtained by using a 22-gauge needle. (b) Percutaneous hepatic venogram helps to confirm near-occlusion at the anastomosis (arrow) and stasis of flow. (c) Fluoroscopic image shows 0.018-inch nitinol guidewire (Microvena, White Bear Lake, Minn) passed through the anastomosis and snared in the IVC (Amplatz gooseneck snare; Microvena). (d) Completion venogram shows deployment of balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) via jugular vein. After dilation of the stent to 12 mm, the 14 mm Hg pressure gradient was eliminated and rapid flow was achieved. Follow-up US examination 64 days later (not shown) demonstrated resolution of ascites and no evidence of residual IVC stenosis.

View larger version (124K): [in this window] [in a new window] [Download PPT slide]   Figure 3c. Left anterior oblique venograms (45° angle) in 60-year-old man 1108 days after piggyback transplantation for chronic hepatitis C and cirrhosis with massive ascites. (a) View of IVC shows long and tapered stenosis (arrow) suggestive of external compression from congested liver. Because the anastomosis could not be crossed in a direction retrograde to the jugular venous access, percutaneous US-guided access to the right hepatic vein was obtained by using a 22-gauge needle. (b) Percutaneous hepatic venogram helps to confirm near-occlusion at the anastomosis (arrow) and stasis of flow. (c) Fluoroscopic image shows 0.018-inch nitinol guidewire (Microvena, White Bear Lake, Minn) passed through the anastomosis and snared in the IVC (Amplatz gooseneck snare; Microvena). (d) Completion venogram shows deployment of balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) via jugular vein. After dilation of the stent to 12 mm, the 14 mm Hg pressure gradient was eliminated and rapid flow was achieved. Follow-up US examination 64 days later (not shown) demonstrated resolution of ascites and no evidence of residual IVC stenosis.

View larger version (134K): [in this window] [in a new window] [Download PPT slide]   Figure 3d. Left anterior oblique venograms (45° angle) in 60-year-old man 1108 days after piggyback transplantation for chronic hepatitis C and cirrhosis with massive ascites. (a) View of IVC shows long and tapered stenosis (arrow) suggestive of external compression from congested liver. Because the anastomosis could not be crossed in a direction retrograde to the jugular venous access, percutaneous US-guided access to the right hepatic vein was obtained by using a 22-gauge needle. (b) Percutaneous hepatic venogram helps to confirm near-occlusion at the anastomosis (arrow) and stasis of flow. (c) Fluoroscopic image shows 0.018-inch nitinol guidewire (Microvena, White Bear Lake, Minn) passed through the anastomosis and snared in the IVC (Amplatz gooseneck snare; Microvena). (d) Completion venogram shows deployment of balloon-expandable stent (Palmaz 188; Cordis/Johnson & Johnson) via jugular vein. After dilation of the stent to 12 mm, the 14 mm Hg pressure gradient was eliminated and rapid flow was achieved. Follow-up US examination 64 days later (not shown) demonstrated resolution of ascites and no evidence of residual IVC stenosis.

One patient underwent venoplasty alone for focal stenosis at 99 days after transplantation, having refused primary stent placement on the advice of the transplantation surgeon at the outside hospital where he received the transplant. The patient's symptoms did not resolve, and he required stent placement 2 months later. The patient responded well, and CT and US images obtained at the 10-month follow-up evaluation showed normal flow through the stent and complete resolution of ascites.

Another patient underwent successful hepatic venous anastomosis stent place-ment on postoperative day 191, with subsequent resolution of the venous pressure gradient. However, on the 1st day after stent placement, follow-up US images demonstrated a previously undetected extrahepatic portal vein stenosis at the anastomosis with a peak flow velocity of 200 cm/sec. With measurement via a transhepatic route, a 23 mm Hg pressure gradient was found in the anastomosis, and a 12 x 40-mm self-expanding stent (Smart; Cordis/Johnson & Johnson) was successfully placed in the lesion. The patient did well, and both the portal and hepatic venous stents remained widely patent 16 months later.

Follow-up US, CT, MR imaging, and venography demonstrated a patent stent in the hepatic vein, with no evidence of recurrent hepatic venous outflow obstruction, in the 12 patients who did not undergo a second transplantation. Routine follow-up Doppler US images obtained 26 months after hepatic vein stent placement in one patient showed increased hepatic venous flow velocity with monophasic spectral waveforms. Selective hepatic venography was subsequently performed, and venograms demonstrated no evidence of stasis, collateral blood vessels, or restenosis. No trans-anastomotic pressure gradients were found, and no reintervention was performed.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 
Hepatic venous outflow obstruction is a rare complication of liver transplantation. Large-scale retrospective studies of piggyback orthotopic liver transplantation have demonstrated a higher incidence of hepatic venous outflow obstruction in piggyback liver transplants (4,9). For piggyback orthotopic whole-liver transplantation, the incidence of hepatic venous outflow obstruction ranges from 1.5% to 2.5% (4,9); moreover, hepatic venous outflow obstruction was noted to be associated with a 24% mortality rate (9). Several possible causes have been suggested for hepatic venous outflow obstruction in piggyback orthotopic liver transplantations. Possible causes in the immediate posttransplantation period include direct compression of the vein by a graft that is too large, twisting of the venous anastomosis when a graft that is too small slides out of place, excessively tight sutures, and venous congestion of the graft with resultant extrinsic compression of the venous anastomosis (4,9,13). Late posttransplantation hepatic venous outflow obstruction is likely secondary to intimal hyperplasia and fibrotic change at the site of anastomosis. In a retrospective study of 1674 piggyback orthotopic liver transplantations, Parrilla et al (4) noted that the incidence of hepatic venous outflow obstruction was significantly lower (0.28% vs 1.6%) when the patch of the suprahepatic veins was composed of three (right, middle, and left) vessels instead of the traditional two (middle and left). A prospective study by Ducerf et al (12) (n = 20) showed that the incidence of a pressure gradient of more than 3 mm Hg across the two-vessel venous cuff anastomosis 3 months after transplantation was 10%. This increased incidence with a two-vessel cuff was surmised to be due to the decreased diameter of the anastomosis and a resultant increase in the possibility of graft mobility (4). The incidence of hepatic venous outflow obstruction after cadaveric piggyback orthotopic whole-liver transplantation at our institution was 10 (3.8%) of 263. Of the 11 patients who underwent endovascular treatment for hepatic venous outflow obstruction, eight had a two-vessel vascular cuff anastomosis, while three patients had a three-vessel vascular cuff.

Published reports of hepatic venous outflow obstruction in living donor grafts and split-liver cadaveric grafts in pediatric patients indicate a higher incidence (ranging from 2% to 9%) with these procedures than with whole-liver transplantation (7,14–16). This is not surprising, given the shorter vascular pedicles, smaller anastomosis diameter, and potential for a size mismatch in children. An increased incidence of hepatic venous outflow obstruction in living donor liver left lobe transplants has been reported, compared with that in right lobe grafts (5.8% vs 0.8%). This difference has been attributed to increased anatomic variation of the left hepatic vein and to the technical challenges presented by the angle and size of the reconstruction (14,17). Our experience with living donor liver transplants in adults is similar, with incidence of hepatic venous outflow obstruction in two (4.7%) of 43 patients.

The use of venoplasty and stent placement is well described in portal venous and IVC stenoses in patients after orthotopic liver transplantation (7,18–22). Venoplasty and stent placement in hepatic venous anastomosis have not been as well described. Seven case reports and two case series have been published regarding venoplasty and stent placement in hepatic venous anastomosis in the posttransplantation liver (7,8,11,16,20,21). Buell et al (7) described their experience with these procedures in 12 of 325 pediatric patients, most of whom had received split-liver or reduced-size grafts. Ko et al (16) detailed their experience with 27 of 313 patients who underwent living donor liver transplantation, seven of whom were pediatric patients. Egawa et al (8) published three case reports of pediatric patients who had received living donor liver transplants. Our study primarily involved piggyback cadaveric whole-liver transplants in adults and an adult-sized pediatric patient.

The question of whether to treat hepatic venous outflow obstruction in this patient population with venoplasty alone or with metallic stent placement remains controversial. Among all the previously described cases of hepatic venous outflow obstruction in both adult and pediatric patients with a living donor liver transplant or piggyback orthotopic liver transplant (7,8,11,14,16,20), 15 patients were treated with venoplasty alone. Six (40%) of those 15, however, required reintervention with repeat venoplasty (n = 3), stent placement (n = 2), or surgical repositioning (n = 1). Given the established long-term durability of metallic stents in large veins and our early experience (10,11,23), we chose to place a stent in the lesion in nearly all cases. In one case, in which the patient, on the advice of an outside transplantation surgeon, insisted on venoplasty alone, the hepatic venous outflow obstruction recurred, and the patient underwent stent placement 5 months later.

Ko et al (16) described their experience with self-expanding stents in living donor liver transplant recipients (n = 27), in only 73% of whom clinical success was achieved. Because of the fibrotic nature of the lesions and the marked tissue recoil after venoplasty, we chose to use balloon-expandable stents. These stents have superior radial hoop strength and offer stronger resistance to compressive forces than do self-expanding stents (24). The hoop strength of medium-sized balloon-expandable stents (18.8 N/cm ± 1.2) is significantly greater than the radial resistive force of self-expanding stents (0.39 N/cm ± 0.03). Although the mechanics involved in the testing of these stents is inherently different, the force required to alter the shape of a balloon-expandable stent is an order of magnitude higher than that required to compress a self-expanding stent (24).

In the current study, technical success was achieved in 13 of 13 patients, and clinical improvement was achieved in 12 (92%). Patient survival during the follow-up period was 100% (13 of 13), and graft survival was 92% (12 of 13). Patient body weight, serum albumin level, prothrombin time, and aspartate aminotransferase level were shown to improve at 30 days after hepatic vein stent placement. In four (31%) of the 13 patients in this study, narrowing of the IVC also was demonstrated at angiography and hepatic vein stent placement. This narrowing appeared to be due to external compression, probably from the edematous transplanted liver. In the first case, stent placement was successful in both the IVC and the hepatic venous anastomosis (11); however, future cases were allowed to resolve with gradual relief of hepatic congestion over time. Follow-up imaging showed resolution of the IVC narrowing in all cases. Given these results, it appears most prudent to observe concurrent IVC stenoses in the setting of hepatic venous outflow obstruction, and forgo placement of a permanent device that could complicate future interventions or surgery.

Interestingly, our patients had a paradoxical increase in alkaline phosphatase level (83.7 IU/L ± 53.4), a finding that was marginally significant (P < .092). An increased alkaline phosphatase level was seen in 10 of 13 patients. Increased alkaline phosphatase is usually attributed to cholestasis but may also be caused by viral infection (from Epstein-Barr virus, toxoplasmosis, cytomegalovirus, and others), osteoblastic activity, and pancreatitis. Multiple forms of alkaline phosphatase may be present in the serum, and the standard laboratory test does not differentiate the four isoenzymes that occur in liver, bone, kidney, placenta, and intestine. Several factors may account for an increase in serum alkaline phosphatase in liver transplant recipients. Rejection could result in cholestasis, and in several of our patients (n = 5), pre- and posttreatment biopsies demonstrated acute and chronic rejection. Increased serum levels of alkaline phosphatase may also be iatrogenic, since immunosuppressive agents including azathioprine, cyclosporine, and glucocorticoids have been associated with increased alkaline phosphatase from liver toxicity and/or changes in bone metabolism (25–27). In many of our study patients, rejection of the transplant was suspected, and these patients were given higher doses of immunosuppressive agents, which may have led to delayed and prolonged increases in the serum alkaline phosphatase level, from either hepatic or bone sources or both. Electrophoresis could be performed in future patients to determine the specific alkaline phosphatase isoenzyme present.

The limitations of this study included its retrospective single-arm design and the small number of subjects, particularly of subjects who were in the immediate postoperative period. Because of the success of endovascular repair, no surgical revision of hepatic venous outflow obstruction was performed during the period of this study, and a comparative study therefore was not possible.

In summary, endovascular stent placement for hepatic venous outflow obstruction in piggyback orthotopic liver transplants offers a substantially less invasive alternative to open surgical revision. Although early treatment of hepatic venous outflow obstruction (within 1 week after transplantation) has primarily involved open surgery, our limited experience with two cases of early hepatic venous outflow obstruction with fresh anastomoses suggests that stent placement may be safe and effective even across anastomoses held intact solely by fresh sutures. Similarly, endovascular treatment for delayed hepatic venous outflow obstruction has been proved effective and safe. Only one complication occurred, a delayed stent migration that was possibly related to angulation at the time of stent deployment with a femoral venous approach. Successful endovascular treatment requires timely diagnosis, since prolonged severe hepatic venous outflow obstruction can result in venous infarction and graft loss. Late diagnosis and treatment resulted in the only clinical failure in our series and ultimately led to repeat transplantation. Endovascular treatment of hepatic venous outflow obstruction in piggyback orthotopic liver transplants by using balloon-expandable stents appears to be effective, safe, and durable, and this has become the standard of care in our transplantation service.

	FOOTNOTES

 

Abbreviations: IVC = inferior vena cava

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, S.L.W., D.Y.S.; study concepts, S.L.W., D.Y.S., S.B., M.D.D.; study design, S.L.W., D.Y.S., M.D.D.; literature research, S.L.W., D.Y.S., S.B.; clinical studies, all authors; data acquisition, S.L.W., D.Y.S., J.K.F.; data analysis/interpretation, S.L.W., D.Y.S.; statistical analysis, S.L.W.; manuscript definition of intellectual content, S.L.W., D.Y.S., M.D.D.; manuscript preparation, editing, revision/review, and final version approval, S.L.W., D.Y.S.

	References

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION References

 

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