Beyond the Rex: an innovative meso-intrahepatic portal vein bypass for late-onset extrahepatic portal vein occlusion after living donor liver transplantation

Introduction

Background

Extrahepatic portal vein occlusion (EHPVO) accounts for approximately 20% of portal hypertension in children (1,2). The various causes of portal vein (PV) occlusion include congenital PV hypoplasia, neonatal umbilical vein catheterization, regional trauma related to surgical procedures, tumor, and infection but majority of the cases are idiopathic. Most patients are asymptomatic in earlier stages but may present with splenomegaly, hypersplenism, ascites, impaired somatic growth, life-threatening variceal bleeding, and graft loss if left untreated. Clinically significant symptoms refractory to conservative management warrant surgical intervention (3).

Rationale

There have been significant advancements in medical, endoscopic, radiologic, and surgical interventions for EHPVO and its associated complications (4). The introduction of the mesenteric-to-left portal vein (LPV) bypass or more commonly known as Meso-Rex bypass (MRB) by De Goyet in 1992 for symptomatic post-transplant portal vein thrombosis (PVT) has caused a paradigm shift in the therapeutic approach for EHPVO. Over the years, the MRB has been utilized both in the pediatric and adult population, within and outside the context of liver transplantation (LT) (5,6). Various modifications to the conventional MRB have been described. However, after exhausting all the available conventional treatment strategies and thorough multidisciplinary discussion, the team deemed the MRB may not be safe option for this specific patient.

Objective

In this paper, the authors aimed to demonstrate a novel hybrid mesenteric-to-intrahepatic portal vein bypass (MIPVB) using GORE^® VIABAHN^® for late-onset EHPVO after living donor liver transplantation (LDLT) in a patient with a Rex recess that is not safely accessible due to patient with extensive post-operative adhesions, perihilar collaterals, and cavernous transformation. We present this article in accordance with the SUPER reporting checklist (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-23-616/rc).

Case presentation

The patient is a 22-year-old male who underwent LDLT with a left lateral segment graft for neonatal hepatitis at one year of age. The PV reconstruction was performed using an end-to-end anastomosis of the native PV branch patch to the graft LPV. The perioperative course was unremarkable.

In the interim, the patient experienced several post-transplant complications. A year after LDLT, he was admitted for septic shock secondary to biliary tract infection which was managed conservatively. At 44 months post-transplant, he underwent small bowel resection due to intestinal diffuse large B-cell lymphoma and received adjuvant chemotherapy. To date, there has been no recurrence of the post-transplant lymphoproliferative disorder (PTLD). However, at 13 years post-transplant, he had recurrent variceal bleeding due to portal hypertension from main portal vein (MPV) occlusion. He underwent endoscopic therapy and splenic artery embolization. Additionally, percutaneous transluminal PV stenting was attempted but was unsuccessful due to a long segment occlusion. Portal hypertension decompression surgery was performed wherein an inferior mesenteric vein to femoral vein shunt was made using a 6-mm ringed GORE-TEX^® interposition graft. Unfortunately, there was early shunt thrombosis, hence, partial splenectomy combined with distal splenorenal shunt was done. Similarly, the second shunt procedure failed to achieve long term patency.

Subsequently, he experienced increasing frequency of gastrointestinal bleeding. Capsule endoscopy showed jejunal varices for which hemoclips were applied. However, bleeding recurred despite these interventions. After a comprehensive multidisciplinary team planning, the authors performed an innovative surgical alternative to the MRB in this post-LDLT patient with extensive post-operative adhesions, perihilar collaterals, and cavernous transformation (Figure 1A). Based on preoperative assessment, he was classified as low risk for intraoperative cardiopulmonary complications. Availability of the blood products for possible operating room (OR) use was ensured. The procedure was performed under general anesthesia with the patient in supine position. To the authors’ knowledge, this is the first report on MIPVB using a GORE^® VIABAHN^® as a conduit.

Figure 1 Preoperative, intraoperative, postoperative imaging studies, and intraoperative findings. (A) Preoperative CTA showing prominent perihilar collaterals and cavernous transformation (yellow arrows). (B) Larger collateral of SMV (yellow arrows). (C) Gelsoft™ Plus interposition graft (yellow arrow) punctured for venogram and endovascular thrombectomy, covered self-expandable metal stent (GORE^®VIABAHN^®) (yellow arrowheads). (D) Intraoperative portal venogram showing engorged SMV collateral-bare metal stent (white arrowhead)-Gelsoft™ Plus (white arrow)-GORE^®VIABAHN^® graft (yellow arrowheads)-intrahepatic portal vein (yellow arrow). (E) CTA at day 8 after MIPVB showing the Gelsoft™ Plus (yellow arrow)-GORE^®VIABAHN^® graft (yellow arrowheads) and patent intrahepatic PV (white arrows). (F) Venogram via jejunal vein catheter prior to removal on day 14 after MIPVB (yellow arrowheads); coils from previous attempt at PV stenting (white arrow). (G) CTA at 10 months after MIPVB showing patent MIPVB (yellow arrowheads) and regression of perihilar collaterals (yellow arrows). (H) Doppler ultrasonography at 19 months after MIPVB showing patent intrahepatic portal vein with normal flow and waveform. CTA, computed tomography angiography; SMV, superior mesenteric vein; MIPVB, meso-intrahepatic portal vein bypass; PV, portal vein.

All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for publication of this article and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Preoperative preparations and requirements

The procedure was performed at the Kaohsiung Chang Gung Memorial Hospital LT OR suite. In addition to the basic LT surgical instruments, the following equipment, supplies, and drug were prepared for the procedure; C-arm machine for the portography, GORE^® VIABAHN^® covered stent (13 mm × 100 mm), Gelsoft™ Plus graft (10 mm diameter, Terumo^®), Luminexx^® bare metal stent (12 mm × 60 mm, Bard Medical), AngioJet™ ZelanteDVT™ console and catheter (8 Fr, 6 mm × 105 cm, Boston Scientific), Fogarty^® catheter (3 Fr), intraoperative Doppler ultrasound (DUS), urokinase (240 kU via jejunal vein catheter). The multidisciplinary team was comprised of 3 transplant surgeons, 1 cardiovascular surgeon, 2 interventional radiologists, 2 anesthesiologists, 1 nurse anesthetist, 1 circulating nurse, 2 scrub nurses, 1 radiologic technologist. The roles of personnel directly involved in the procedure per se will be described in the surgical technique segment.

Step-by-step description

Extensive and dense adhesions were encountered by the transplant surgeons upon entering the abdomen through the previous incision. The liver graft showed no gross signs of cirrhosis. Multiple engorged mesenteric veins of the jejunal Roux-Y limb up to 5 mm in diameter were noted. Portal venogram was carried out by the interventional radiologists to serve as a roadmap, identify preferential flow and collaterals, and evaluate the shunt patency. The initial portogram revealed significant portosystemic shunting with a large superior mesenteric vein (SMV) collateral (>8 mm) and MPV occlusion with extensive adhesions, perihilar collaterals, and cavernous transformation. The largest SMV collateral vein was isolated to be used as the inflow for the bypass conduit (Figure 1B).

The radiologists did ultrasound-guided transhepatic puncture through the transection surface of segment 3 and cannulation of the umbilical portion of the LPV. A 13 mm × 100 mm covered stent (GORE^® VIABAHN^®) was deployed with the distal end inside the umbilical portion of the LPV and the proximal end connected to and deployed within a 10-mm diameter Gelsoft™ Plus (Terumo^®) graft. The proximal Gelsoft™ Plus graft was tunneled through the transverse mesocolon and an end-to-end anastomosis of the large SMV collateral to the Gelsoft™ Plus graft was done by the transplant surgeons using 6-0 Prolene^® continuous suture. On the other hand, the proximal end of the GORE^® VIABAHN^® had a 2-cm overlap with the Gelsoft™ Plus upon which, 2 fixation stitches using Prolene^® 6-0 were placed. The 2 synthetic grafts had a snug and secure fit at the overlapped portion.

Unfortunately, intrahepatic PVT occurred during the procedure which was initially managed with endovascular local infusion of urokinase 240 kU and thrombectomy using a 3 Fr Fogarty^® catheter was performed by the cardiovascular surgeon (Figure 1C). To prevent angulation, the radiologists deployed a 12 mm × 60 mm Luminexx^® bare metal stent at the anastomosis of Gelsoft™ Plus-SMV collateral (Figure 1D). Due to the persistence of intrahepatic PV and interposition graft thrombosis, the cardiovascular surgeon performed thrombectomy using AngioJet™ ZelanteDVT™ catheter (8 Fr, 6 mm × 105 cm, Boston). Approximately 190 mL of blood clots was aspirated and repeat venogram showed disappearance of thrombus (Figure 1D). Intraoperative DUS confirmed patency and good flow to the LPV. The jejunal vein catheter was tunneled percutaneously for continuous local infusion of heparin postoperatively. The operative time was 8 hours.

Postoperative considerations and tasks

Given the occurrence of intraoperative thrombosis, local infusion of heparin was given via jejunal vein catheter that was inserted for intraoperative venography. Continuous infusion was started after creation of the shunt with 50 IU/kg/day. The dose was adjusted accordingly to maintain an international normalized ratio (INR) of 1.5–2.0× and signs of bleeding were closely monitored. The heparin infusion was maintained for 2 weeks. After computed tomography angiography (CTA), DUS, and portogram via the jejunal vein catheter confirmed patency of the conduit, the catheter was removed (Figure 1E,1F). The patient was then maintained on dabigatran 110 mg twice daily. The patient was on monthly follow-up for the first 3 months then every 3 months thereafter. Complete blood count, coagulation parameters, and liver function tests were checked on every follow-up. DUS was performed every 3 months. The patient was advised to consult immediately if with signs of bleeding such as hematochezia or melena.

Since the procedure, the patient has been readmitted for three times, the earliest was at seven months after the operation. The frequency and severity of the bleeding episodes were much less compared to prior to the bypass procedure. On the second readmission, red blood cell scan, enteroscopy, and colonoscopy showed no active bleeding. The latest CTA performed at 10 months showed patency of the intrahepatic PV and interposition graft as well as regression of perihilar collaterals (Figure 1G). DUS at 19 months showed patent intrahepatic PV with normal flow and waveform (Figure 1H). His liver function remains normal at 21 months after the procedure.

Tips and pearls

A multidisciplinary team approach is essential in this procedure. Preoperative CT angiography, intraoperative portogram, and DUS are extremely important in identification of the most suitable PV inflow as well as in the determination of the presence of collaterals/shunts that may need to be ligated. Heparin administration just prior to initiating the stent procedure should be ensured to reduce the risk of intraoperative thrombotic events.

Some may suggest adding a small diameter transjugular intrahepatic portosystemic shunt (TIPS) to the shunt to improve outflow. These maneuvers may be required if outflow remains suboptimal or with high intrahepatic vascular resistance due to parenchymal disorder. If that is the case, retransplantation is indicated because shunting cannot improve liver metabolic and synthetic function. In this patient with normal liver parenchymal function and outflow, TIPS and re-transplantation were not considered.

The authors would also like to emphasize the indication for using of GORE^® VIABAHN^®, an expandable polytetrafluoroethylene (PTFE) covered stent instead of expandable bare metallic stent. In this case, the shunt is an interposition graft from extrahepatic SMV collateral vein to intrahepatic PV, so a covered stent is required. An expandable bare metallic stent would be more suitable for intra-luminal shunting.

Discussion

Surgical highlights

EHPVO after LT develops in approximately 8.7% of pediatric patients. The authors have previously reported that post-LDLT PVT occurred more frequently among biliary atresia (BA) compared to non-BA patients (7.6% vs. 3.7%) (7). It is more commonly seen in partial compared to whole-sized liver grafts (3). Thrombectomy and balloon angioplasty with or without stents are treatment options for post-transplant PVT but these may not always be feasible as seen in this case. Among the surgical options, there has been increasing utilization of the MRB, as it not only decreases PV pressure but also restores physiologic blood flow to the liver (8).

Several authors have described the numerous benefits of the meso-portal bypass which incudes normalization of coagulation parameter and improvement in neurocognitive function (9). Furthermore, previous reports have shown that MRB can also reverse hyperammonemia, hepatopulmonary syndrome, and encephalopathy, and improve somatic growth as well (8,10).

Alternative conduits and inflows for the MRB have been previously reported but all of these still utilize the Rex recess to access the LPV. However, in certain patients, this landmark is not always readily accessible. Hence, there is a need to develop techniques to overcome this limitation.

The four prerequisites for a MIPVB include: (I) no irreversible intrinsic liver disease, (II) patent intrahepatic PV and outflow system, (III) sufficient venous inflow from the mesenteric circulation, (IV) absence of untreatable hypercoagulable state (10).

A thorough preoperative evaluation to determine the feasibility of the bypass is necessary and it is achieved with imaging studies such as DUS, CT angiography, magnetic resonance imaging (MRI), retrograde portal venography (1). In addition to the imaging studies, routine blood test, liver function tests, and coagulation studies are done to exclude intrinsic liver disease and to rule out presence of hypercoagulable states. A liver biopsy is also recommended to exclude intrinsic liver disease (3,10,11).

In the technique described in this paper, the intrahepatic PV of the left liver graft was accessed by puncture at the transection surface of segment 3 and not via the Rex recess. A fully covered expandable stent (GORE^® VIABAHN^®) was then deployed as conduit to a Gelsoft™ Plus graft and SMV collateral.

Strengths and limitations

This new approach avoids the risks associated with isolation of the vein over an area with extensive adhesions, prominent perihilar collaterals, and cavernous transformation.

The MIPVB is an innovative technique to address EHPVO especially in patients with a Rex recess that is not safely accessible and with symptoms that are refractory to conventional surgical strategies. Furthermore, it is potentially useful for the right liver graft as well. Like in other procedures that utilize stents and synthetic vascular grafts that requires postoperative anticoagulation, patients are closely monitored for bleeding and thrombosis.

Comparison with other surgical techniques and researches

Modifications to the classic MRB technique employ either the use of alternative conduits or inflows (12,13). Despite several reports on acceptable patency of the MRB, the choice for the best conduit is still controversial (12). One author reported that the patency of Rex bypass using the internal jugular vein was superior to other conduits. Alternatively, a Gore-Tex^® conduit can be used, albeit with a reported higher risk of bypass thrombosis (4). Another author described their successful experience with Gore-Tex^® with a shunt patency of 2.5 years at the time of their report (14). Concerns regarding the use of PTFE in the portal system include: risk of thrombosis due to low flow, the risk of infection, and risk of fistula formation or erosion into adjacent structures (15).

The MRB, conventional or modified, utilizes the Rex recess which limits its utility for the right liver graft. Long et al. mentioned that the greatest challenge for a right sided bypass is the isolation of the right PV and MPV without interruption of extensive collaterals in the right pedicle and hepatoduodenal ligament (12). Since the authors’ approach uses a puncture method to access the intrahepatic PV, without the need for actual exposure of the vein, it is potentially useful for the right liver graft as well.

Implications and actions recommended

There is still no consensus regarding the post-operative anticoagulation after MRB but most centers give anticoagulant for at least 6 months to avoid stent thrombosis (16). For this case, the patient will be maintained on anticoagulant as long as possible given that there are no associated complications. This patient already underwent multiple procedures to address the EHPVO-related complications and failure of this most recent bypass procedure might lead to re-transplantation which would be unfavorable for this patient given his previous history of PTLD. Furthermore, the availability of an alternative treatment for this patient’s recurrent variceal bleeding obviates the need for re-transplantation especially at this time with normal liver function.

Based on this experience in post-transplant EHPVO, the authors still recommend percutaneous thrombectomy with or without PV stenting as first line intervention but if not feasible, the patient should be evaluated for an MRB without delay as recommended by current treatment guidelines for EHPVO.

Conclusions

MIPVB creation following liver transplant is a technically challenging procedure but with a multidisciplinary team approach, meticulous preoperative planning, and close follow-up, the authors have demonstrated that it is a safe and feasible option for patients with late-onset EHPVO after LT.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the SUPER reporting checklist. Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-23-616/rc

Peer Review File: Available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-23-616/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://hbsn.amegroups.com/article/view/10.21037/hbsn-23-616/coif). C.L.C. serves as an unpaid editorial board member of Hepatobiliary Surgery and Nutrition. The other authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the Helsinki Declaration (as revised in 2013). Written informed consent was obtained from the patient for publication of this article and accompanying images. A copy of the written consent is available for review by the editorial office of this journal.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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