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Transjugular Intrahepatic Portosystemic Shunt Placement in Liver Transplant Recipients: Experiences with Pediatric and Adult Patients

¹ Department of Radiology, The University of Chicago Hospitals, 5841 S. Maryland Ave., MC 2026, Chicago, IL 60637.
² Pritzker School of Medicine, The University of Chicago Hospitals, Chicago, IL 60637.
³ Department of Surgery, The University of Chicago Hospitals, Chicago, IL 60637.

Received July 2, 2003; accepted after revision June 30, 2004.

 
Address correspondence to T. G. Van Ha (tgvanha{at}radiology.bsd.uchicago.edu).

Abstract

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OBJECTIVE. The purpose of our study was to evaluate the safety and efficacy of transjugular intrahepatic portosystemic shunts (TIPS) in pediatric and adult liver transplant recipients. A retrospective review of six TIPS placed in six liver transplant recipients—a pediatric patient with a split liver transplant, a pediatric patient with left lateral segment transplant, and four adult patients—was performed.

CONCLUSION. TIPS placement in both pediatric and adult liver transplant recipients is feasible. In liver transplant patients who are recipients of a left lateral segment or a split liver transplant, knowledge of the liver transplant anatomy is critical in the placement of TIPS. TIPS placement is a treatment option and a bridge to retransplantation for patients who have undergone liver transplantation and develop sequelae of portal hypertension.

Introduction

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The insertion of transjugular intrahepatic portosystemic shunts (TIPS) has been shown to be an effective therapy for portal hypertension when conservative medical management has failed. Variceal bleeding not controlled with medical or endoscopic therapy and ascites refractory to frequent paracentesis and diuresis may be alleviated by shunt insertion [1, 2], although definitive therapy for patients with hepatic failure is liver transplantation. TIPS has proved to be a valuable bridge to transplantation. At least one randomized prospective study has also shown a survival advantage for patients with refractory ascites treated with TIPS compared with serial paracenteses [2]. The optimal therapy for a liver transplant recipient who develops portal hypertension is unknown. Two studies have shown that in adult liver transplant recipients who have developed sequelae of portal hypertension, TIPS is feasible and can serve as a bridge to liver retransplantation [3, 4]. This article describes our experience with TIPS placement in both pediatric and adult liver transplant recipients.

Materials and Methods

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This retrospective study was approved by the institutional review board of our hospital. Between January 1990, and January 1999, 212 TIPS procedures were performed at our institution. Six TIPS were placed in six liver transplant recipients, four males and two females, ranging in age from 5 to 67 years old. Indications were refractory ascites (n = 5) and variceal bleeding resistant to endoscopic therapy (n = 1). The time between liver transplantation and TIPS placement ranged from 3 to 113 months. One patient was classified as Child-Pugh class A, one was Child-Pugh class B, and four were Child-Pugh class C (Table 1). Conservative management had failed in all patients with ascites, and medical and endoscopic therapy had failed in the patient with variceal bleeding. Two patients had concomitant thrombocytopenia from hypersplenism. Patients were followed up until retransplantation or death. The total follow-up time was 97 months (mean, 16 months).

The cohort consisted of two pediatric patients and four adult patients. The indications for TIPS placement in the pediatric patients were variceal hemorrhage (patient 1) and ascites (patient 2). Both these patients had transplants that were reduced in size. One patient (patient 1) had a living donor, left lateral segment liver transplant with a hepatic-to-caval anastomosis, and the other patient (patient 2) had a full left lobe liver transplant. Patient 2 also had splenomegaly and thrombocytopenia from hypersplenism. Both pediatric patients had varying degrees of chronic rejection.

In the adults, an 18-year-old man (patient 3), who had received a full liver transplant as an 11-year-old child for hepatic failure due to Wilson's disease, developed portal hypertension and splenomegaly as a result of cirrhosis and fibrosis of the liver transplant. The indication for the TIPS placement in this patient was ascites and thrombocytopenia resulting from hypersplenism from splenomegaly. In all other adult patients, the indication for TIPS was refractory ascites. One patient (patient 4) had mild acute rejection of the allograft that was confirmed by biopsy. Another (patient 5) developed chronic active hepatitis, which was serology negative. The last patient (patient 6) had portal hypertension that was caused by Budd-Chiari syndrome, which was ultimately confirmed at autopsy.

Procedures
All patients underwent contrast-enhanced CT and sonography of the abdomen before TIPS placement. After undergoing general endotracheal anesthesia, patients were prepared and draped in a sterile fashion. We routinely perform TIPS placement under general anesthesia because, in our experience, this is safe and allows better patient monitoring and control, especially in the pediatric population. TIPS were placed via the right internal jugular vein in five patients. A left internal jugular approach was used in one pediatric patient because her right internal jugular vein was occluded. A Rosch-Uchida TIPS set (Cook) was used to access the portal vein from the hepatic vein. This set was used in both the adult and pediatric patients. Although we have used reduced-size TIPS sets successfully for other pediatric patients without transplants, the Rosch-Uchida set was preferred for its improved stiffness. In two patients, one adult and one pediatric, we used a micropuncture wire (Cook) placed in the portal vein under sonographic guidance to help guide the portal vein puncture (Fig. 1). Wallstent (Boston Scientific Vascular) endoprostheses were used to create the shunts. Four patients had one stent placed, and two adult patients required two overlapping stents. Wallstents ranged from 8 to 12 mm in diameter. Angioplasty balloon (Ultrathin, Boston Scientific Vascular) diameters ranged from 6 to 12 mm. In full-liver transplant recipients, all shunts were from the right hepatic vein to the right portal vein (Fig. 1). Sonography was used within 48 hr to determine patency of the TIPS. Serial sonographic examinations were performed to access patency of the shunts. The patients were followed up until retransplantation or death.

View larger version (158K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1. —45-year-old female liver transplant recipient who underwent TIPS for ascites. Portal venogram shows metallic stent (solid arrows) in inferior vena cava placed previously for caval stenosis at surgical anastomosis. Puncture is made from transplanted liver right hepatic vein into right portal vein (open arrow), which is opacified with contrast material. Wire (arrowheads) was placed percutaneously in portal vein under sonographic guidance to help guide transhepatic puncture from hepatic vein.

Results

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TIPS were successfully placed in all six patients. However, one pediatric patient required two procedures on two separate days. The first attempt was unsuccessful because we could not access the portal vein despite numerous punctures from the hepatic vein as a result of difficult anatomy. In addition, the contrast load to the patient was at a maximum. The second, successful attempt was performed with a guidewire placed into the portal vein percutaneously to guide the puncture. The corrected portosystemic gradients ranged from 18 to 25 mm Hg before shunt placement. After shunt placement, the gradients ranged from 4 to 10 mm Hg (Table 2). Doppler sonography performed on all six patients revealed a patent TIPS within 48 hr of the procedure.

Both pediatric patients underwent retransplantations. One of the pediatric patients underwent retransplantation 4 days after the TIPS procedure. During those 4 days, he did not have a recurrence of his ascites. This patient continues to live after his fourth transplant. The second pediatric patient had a patent TIPS shown on sonography at 6 weeks. This patient had no recurrence of varices in the intervening 4 months between TIPS and retransplantation.

In the adult group, three of four patients had resolution or improvement of ascites. Patient 3, an 18-year-old man, is symptom-free at the 22-month follow-up. Ascites resolved in a 59-year-old woman (patient 5), but she died 5 months after TIPS placement from progressive renal and hepatic failure. The corrected portosystemic shunt gradient was 4 mm Hg after shunt placement. After 4 months of doing well, the patient developed worsening liver function with rejection, and she also developed renal failure attributable in part to calcineurin inhibitor nephrotoxicity. A 67-year-old man (patient 4) had improvement in ascites but required two supplemental Denver shunt creations at 9 days and 4 weeks after the procedure for complete control of symptoms. He continued to be symptom-free at 66 months. Patient 6 died of acute liver failure 4 days after the procedure. The hepatic artery was patent, as shown on duplex sonography. This patient had a corrected portosystemic shunt gradient of 7 mm Hg after TIPS placement.

Discussion

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TIPS is an accepted treatment for intractable ascites and variceal hemorrhage refractory to medical and endoscopic therapy in patients with sinusoidal portal hypertension. Two small series have reported TIPS in adult liver transplant recipients [3, 4], and a case report has also been published [5]. LaBerge et al. [1] mentioned two liver transplant recipients who underwent TIPS placement. Hidajat et al. [6] reported one incidental case of TIPS creation in a transplanted liver in their series of 110 patients. Ciccarelli et al. [7] reported a case of early portal vein thrombosis after liver transplantation treated by combining TIPS creation and thrombolysis. A series of pediatric TIPS placements included a liver transplant recipient [8]. Richard et al. [5] reported a case of TIPS placement in a patient who had a liver transplant complicated by Budd-Chiari syndrome. To our knowledge, posttransplantation TIPS has not been extensively reported in pediatric patients. Notably, we found TIPS to be technically feasible in both left lateral segment and split liver transplants.

Amesur et al. [4] reported a series of 12 adult patients who received a TIPS from 6 months to 13 years after liver transplantation. Six of their patients had TIPS placed for variceal hemorrhage and six patients for ascites. In the patients with refractory variceal bleeding, four did not experience rebleeding, and two had recurrent bleeding within 1 week. Of the former group, two had functional shunts at 3 and 36 months, and two underwent retransplantation at 3 and 7 months. In the patients who had TIPS placement for ascites, two underwent retransplantation at 2 and 6 weeks, with improvement in ascites in the interval. Ascites was in good control in one patient at the 32-month follow-up. One patient died 1 month after TIPS placement after a splenectomy. Two patients died from fulminate hepatic failure within 1 week. The authors concluded that TIPS placement directly contributed to the rapid development of liver failure in those two patients despite uneventful TIPS placements and no sonographic evidence of arterial compromise. These two patients had gradients of 7 and 8 mm Hg after TIPS placement. In our study, the patient who died 4 days after TIPS placement had a gradient of 7 mm Hg. The one who died 5 months after TIPS placement had a final gradient of 4 mm Hg. As suggested by Amesur et al. [4], although gradients in the 6–8 mm Hg range have been reported to completely control ascites, a higher gradient might be needed to avoid acute liver failure in this population [4]. In another article, Lerut et al. [3] reported two patients of eight who died shortly after TIPS placement. Although the final corrected portosystemic gradients of these two patients were not reported, Lerut et al. noted the high incidence of hepatic encephalopathy in this patient population and the subsequent need to have the final gradient high enough to preserve hepatoportal perfusion.

Lerut et al. [3] presented a series of eight adult patients who had TIPS placement after liver transplantation. The indications were refractory ascites (n = 5), hepatic hydrothorax and concomitant ascites (n = 1), bleeding esophageal varices (n = 1), and repeated biliary surgery (n = 1). The authors judged the TIPS results to be successful in three patients, partly successful in three patients, and unfavorable in two patients. Both patients in the unfavorable group had TIPS placed for ascites. One was classified as Child-Pugh class C and the other as Child-Pugh class B. These two patients died shortly after the TIPS placement. One patient died from duodenal ulcer bleeding and necrotic pancreatitis. The other died of liver failure 4 months after TIPS placement. Although their technical success was 100%, Lerut et al. raised the point that TIPS placement could be technically difficult in some patients, particularly those with piggyback, cavocaval anastomoses, because of the difficulty in cannulation of the allograft hepatic and portal veins. Those authors stated that for TIPS placement to be feasible, if the piggyback, cavocaval anastomosis was used, the donor vena cava must encompass the orifices of all hepatic veins. We experience no unexpected difficulties in TIPS placement in the full-liver transplants. However, our patients received the conventional surgical approach with caval replacement. In the two pediatric patients who received reduced-size transplants, we found that cross-sectional imaging, combined with review of surgical techniques used, was essential in guiding the punctures from the hepatic vein to the portal vein (Figs. 2A, 2B, 2C, 2D, 2E, 2F, and 2G). Despite the extensive preprocedural workup, one patient required two procedures for successful shunt insertion. In two cases, we introduced guidewires into the portal vein percutaneously to help guide punctures. Other techniques of portal vein localization can certainly be used, such as CT-guided marking of the portal vein [9], CO₂ wedged hepatic venography [10], or balloon occlusion venography [11]. However, the safety of CO₂ wedged or balloon occlusion hepatic venography in liver transplantation, especially partial transplantation, is not known.

View larger version (114K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —16-year-old girl with left lateral segment transplant undergoing evaluation for TIPS placement. Unenhanced CT scans from superior (A) to inferior (D) show relative position of hepatic vein (solid arrows, A) to portal vein (open arrows, C and D). Arrowhead (B) indicates junction of hepatic vein with inferior vena cava (curved arrow, B).

View larger version (121K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —16-year-old girl with left lateral segment transplant undergoing evaluation for TIPS placement. Unenhanced CT scans from superior (A) to inferior (D) show relative position of hepatic vein (solid arrows, A) to portal vein (open arrows, C and D). Arrowhead (B) indicates junction of hepatic vein with inferior vena cava (curved arrow, B).

View larger version (117K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —16-year-old girl with left lateral segment transplant undergoing evaluation for TIPS placement. Unenhanced CT scans from superior (A) to inferior (D) show relative position of hepatic vein (solid arrows, A) to portal vein (open arrows, C and D). Arrowhead (B) indicates junction of hepatic vein with inferior vena cava (curved arrow, B).

View larger version (117K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D. —16-year-old girl with left lateral segment transplant undergoing evaluation for TIPS placement. Unenhanced CT scans from superior (A) to inferior (D) show relative position of hepatic vein (solid arrows, A) to portal vein (open arrows, C and D). Arrowhead (B) indicates junction of hepatic vein with inferior vena cava (curved arrow, B).

View larger version (191K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2E. —16-year-old girl with left lateral segment transplant undergoing evaluation for TIPS placement. Hepatic venogram shows that hepatic vein is accessed and opacified with contrast material (arrows). Stent (arrowheads) is from previous attempt at TIPS placement at different institution. TIPS was placed after CT scans A–D.

View larger version (163K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2F. —16-year-old girl with left lateral segment transplant undergoing evaluation for TIPS placement. Portal venogram shows that portal vein is accessed from hepatic vein. Portal vein is opacified (arrows).

View larger version (144K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2G. —16-year-old girl with left lateral segment transplant undergoing evaluation for TIPS placement. Shuntogram shows that TIPS shunt is in place (arrows) and is patent as seen by flow of contrast material.

The role of TIPS in patients with portal hypertension continues to evolve. Numerous studies have attempted to define criteria predictive of long-term success. In general, patient outcome is influenced by a variety of factors; and predictably, patients with more advanced liver failure and increased comorbidities fare worse than those with less severe hepatic dysfunction. Patients treated for variceal hemorrhage are usually separated from those with refractory ascites because the degree of liver dysfunction commonly varies substantially between groups. Several investigators have noted that in patients with refractory ascites, renal (serum creatinine > 2.0 mg/dL) and hepatic (serum bilirubin > 3.0 mg/dL) dysfunction portends a poor outcome [1, 2, 12]. In our group, one patient (patient 5) who died 5 months after the procedure was classified as Child class C and had a bilirubin level of 4.0 mg/dL and a creatinine level of 2.6 mg/dL. She died of progressive hepatic and renal failure. In contrast, our two adult patients (patients 3 and 4), alive at follow-up at 22 and 66 months with no recurrence of ascites, had bilirubin levels less than 2.0 mg/dL and serum creatinine levels of 0.9 mg/dL and 2.3 mg/dL, respectively (Table 2).

All our patients were receiving calcineurin inhibitors. Typically, we monitored for nephrotoxicity closely immediately after the procedure: daily at first, then weekly, then monthly. If there was clinical suspicion for nephrotoxicity, then patients were closely evaluated. Calcineurin inhibitors reduce allograft rejection and improve patient survival. However, the nephrotoxicity of these agents may adversely affect allograft and patient survival [13]. The medical management of a liver transplant recipient who undergoes TIPS creation is complex because the clinical pharmacokinetics of drug therapy is altered by the shunt through the liver. In particular, titration of calcineurin inhibitors such as cyclosporin and tacrolimus is problematic because of their narrow therapeutic indexes. If blood levels are too low, the allograft is threatened by rejection; if levels are too high, nephrotoxicity ensues. Superimposed hepatic or renal dysfunction serves to further complicate the issue and exacerbate this problem. Typically, trough levels are used to guide therapy. In addition, in patients who have hepatic failure, the hepatic artery examination, usually initially by duplex sonography, must be performed to rule out stenosis or occlusion.

The role of TIPS in the transplant population is largely undefined. Given the lack of experience, conservative rather than liberal application of the procedure is the rule [3, 4]. This selection bias may negatively affect early attempts, particularly if the procedure is reserved for patients with no other options and is used as a last resort. Experience in patients with native livers has shown that TIPS is predestined to fail in this subgroup of patients [1, 2, 14, 15]. Newer and unproven therapies tend to be initially used in patients with no other options. With respect to TIPS creation, critically ill patients fare much poorer than their counterparts. Specifically, as noted previously, comorbidity—including coagulopathy, renal insufficiency, and hepatic insufficiency—and urgent TIPS placement have been correlated with early mortality [14, 15]. In patients with ascites, TIPS placement appears superior to repeated large-volume paracenteses. However, the survival advantage appears most pronounced in patients with less severe disease [2]. In the three small reported series to date [3, 4], including this one, the 30-day mortality of all patients is 19% (5/26), which is similar to results in most series with TIPS in patients with native livers [1, 2]. Although TIPS may predispose to rapid, fulminant hepatic failure in transplant recipients, this risk does not appear to be greatly exaggerated compared with patients with native livers.

We conclude that placement of TIPS in liver transplant recipients is feasible, especially in orthotopic liver transplants with conventional caval replacement. In pediatric patients with reduced-size transplants, TIPS placement is also possible, although knowledge of the transplant anatomy is critical. We found in one of the pediatric patients and an adult patient, additional sonographically guided, percutaneous placement of a guidewire into the portal vein helped guide the punctures from the hepatic vein. However, we perform this extra maneuver only as needed. TIPS in transplant recipients can be used to treat sequelae of portal hypertension and to serve as a bridge to retransplantation. This patient population might require a higher final corrected portosystemic gradient to have adequate hepatoportal perfusion in order to avoid acute hepatic failure. In patients whose liver transplantation is complicated by rejection, management is made more difficult by the altered metabolism of antirejection drugs in the presence of a TIPS and a failing liver.

References

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This Article Abstract Figures Only Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Van Ha, T. G. Articles by Leef, J. Search for Related Content PubMed PubMed Citation Articles by Van Ha, T. G. Articles by Leef, J. Social Bookmarking                      What's this? Hotlight (NEW!) What's Hotlight?