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Novel classification of non-malignant portal vein thrombosis: A guide to surgical decision-making during liver transplantation

Published:August 20, 2019DOI:https://doi.org/10.1016/j.jhep.2019.08.012

      Summary

      Non-tumoral portal vein thrombosis (PVT) is present at liver transplantation in 5% to 26% of cirrhotic patients, and the prevalence of complex PVT as defined here (grade 4 Yerdel, and grade 3,4 Jamieson and Charco) has been reported in 0% to 2.2%. Adequate portal inflow is mandatory to ensure graft and patient survival after liver transplantation. With time, the proposed classifications of non-tumoral chronic PVT have evolved from being anatomy-based, to also incorporating functional parameters. However, none of the currently proposed classifications are directed towards decision-making, regarding the choice of inflow to the graft during transplantation and the outcomes thereof. The present scoping review i) addresses the limits of the currently available classifications in terms of surgical decisiveness, ii) clarifies the concept of physiological or non-physiological portal inflow reconstruction, and subsequently, iii) proposes a new classification of non-tumoral PVT in candidates for liver transplantation; to help tailor the surgical strategy to an individual patient, in order to provide portal inflow to the graft together with control of prehepatic portal hypertension whenever feasible.

      Keywords

      Linked Article

      Introduction

      Adequate portal inflow is necessary to ensure graft and patient survival after liver transplantation (LT);
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      thus, coexisting portal vein thrombosis (PVT) was long considered an absolute contraindication for LT due to the high mortality associated with the procedure.
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      where the portal vein trunk was resected en bloc with the thrombus, and porto-portal anastomosis was performed with an interposed cadaveric vein jump graft.
      Though initial studies reported worse post-LT outcomes in patients with PVT compared to those without PVT, most studies published after the year 2000 have reported similar 1-year survival in both groups.
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      However, the vast majority of these studies did not detail post-LT results according to the extent/grade of PVT, which may influence the post-LT outcome to a large extent.
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      In a recent meta-analysis, Zanetto et al.
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      found that postoperative mortality was higher (27%) in patients with grade 4 (Yerdel) PVT in the 10 studies that reported on mortality by grade of PVT. One-year mortality was also higher in patients with complete (42%) compared to partial (22%) PVT in 3 studies. Meanwhile, previous studies have shown that even in higher grades of PVT, if it is possible to achieve a porto-portal anastomosis, there is no major impact on post-LT survival.
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      With time, the proposed classifications of non-tumoral chronic PVT have evolved from being anatomy-based (site and extent), to also incorporating functional parameters (presence of symptomatic portal hypertension [PHT] or a portal cavernoma), which may aid in decision-making with regards to the medical management of these patients (role of transjugular intrahepatic portosystemic shunt [TIPS], variceal ligation, embolisation of spontaneous portosystemic shunts etc.).
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      • et al.
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      None of the 9 currently proposed classifications
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      • Fung J.J.
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      • et al.
      The spectrum of portal vein thrombosis in liver transplantation.
      • Nonami T.
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      The incidence of portal vein thrombosis at liver transplantation.
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      • Echeverri L.
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      • et al.
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      • Gunson B.
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      • Olliff S.
      • Buckels J.
      • et al.
      Portal vein thrombosis in adults undergoing liver transplantation: risk factors, screening, management, and outcome.
      • Jamieson N.V.
      Changing perspectives in portal vein thrombosis and liver transplantation.
      • Charco R.
      • Fuster J.
      • Fondevila C.
      • Ferrer J.
      • Mans E.
      • García-Valdecasas J.C.
      Portal vein thrombosis in liver transplantation.
      • Bauer J.
      • Johnson S.
      • Durham J.
      • Ludkowski M.
      • Trotter J.
      • Bak T.
      • et al.
      The role of TIPS for portal vein patency in liver transplant patients with portal vein thrombosis.
      • Ma J.
      • Yan Z.
      • Luo J.
      • Liu Q.
      • Wang J.
      • Qiu S.
      Rational classification of portal vein thrombosis and its clinical significance.
      are directed towards decision-making, regarding the choice of inflow to the graft during LT. Though the functional classification proposed by Sarin et al.
      • Sarin S.K.
      • Philips C.A.
      • Kamath P.S.
      • Choudhury A.
      • Maruyama H.
      • Nery F.G.
      • et al.
      Toward a comprehensive new classification of portal vein thrombosis in patients with cirrhosis.
      has incorporated thrombus and patient characteristics, it does not allude to the pre-transplant approach towards ensuring portal vein patency for eventual porto-portal anastomoses in these patients.
      Prevalence of non-malignant PVT in cirrhotic patients ranges from 5% to 26% at the time of LT.

      Methods

      This study is a scoping review of the English-language literature on the currently available classifications of PVT (their usefulness and limitations in defining surgical strategy during LT), and methods described for portal inflow to the graft during LT in the case of diffuse PVT (with their associated outcomes). Since the body of evidence on this topic is complex, and suffers from heterogeneity, a precise systematic review is not possible. Also, the surgical options, and an algorithmic approach to surgical management during LT in cases of “complex PVT”, as defined here, have not been comprehensively reviewed before. This review tries to consolidate the current evidence available on the management of diffuse PVT in the liver transplant setting, as well as mapping out the results achieved to date. We have also tried to clarify the concept of physiological vs. non-physiological inflow reconstruction, and proposed a new algorithm for the surgical strategy during transplant, which could provide portal inflow to the graft together with control of prehepatic PHT whenever feasible.

      Current grading systems for non-tumoral PVT and a new proposed classification

      Nine classification systems have been proposed to grade non-tumoral PVT
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      • Philips C.A.
      • Kamath P.S.
      • Choudhury A.
      • Maruyama H.
      • Nery F.G.
      • et al.
      Toward a comprehensive new classification of portal vein thrombosis in patients with cirrhosis.
      • Stieber A.C.
      • Zetti G.
      • Todo S.
      • Tzakis A.G.
      • Fung J.J.
      • Marino I.
      • et al.
      The spectrum of portal vein thrombosis in liver transplantation.
      • Nonami T.
      • Yokoyama I.
      • Iwatsuki S.
      • Starzl T.E.
      The incidence of portal vein thrombosis at liver transplantation.
      • Gayowski T.J.
      • Marino I.R.
      • Doyle H.R.
      • Echeverri L.
      • Mieles L.
      • Todo S.
      • et al.
      A high incidence of native portal vein thrombosis in veterans undergoing liver transplantation.
      • Yerdel M.A.
      • Gunson B.
      • Mirza D.
      • Karayalçin K.
      • Olliff S.
      • Buckels J.
      • et al.
      Portal vein thrombosis in adults undergoing liver transplantation: risk factors, screening, management, and outcome.
      • Jamieson N.V.
      Changing perspectives in portal vein thrombosis and liver transplantation.
      • Charco R.
      • Fuster J.
      • Fondevila C.
      • Ferrer J.
      • Mans E.
      • García-Valdecasas J.C.
      Portal vein thrombosis in liver transplantation.
      • Bauer J.
      • Johnson S.
      • Durham J.
      • Ludkowski M.
      • Trotter J.
      • Bak T.
      • et al.
      The role of TIPS for portal vein patency in liver transplant patients with portal vein thrombosis.
      • Ma J.
      • Yan Z.
      • Luo J.
      • Liu Q.
      • Wang J.
      • Qiu S.
      Rational classification of portal vein thrombosis and its clinical significance.
      (Table S1). All but one
      • Sarin S.K.
      • Philips C.A.
      • Kamath P.S.
      • Choudhury A.
      • Maruyama H.
      • Nery F.G.
      • et al.
      Toward a comprehensive new classification of portal vein thrombosis in patients with cirrhosis.
      include 4 grades, and there is no one grade common to all classification systems. Some include grades pertaining to thrombosis of intrahepatic portal vein branches without portal trunk thrombosis. These grades have limited value, if any, in the setting of LT, because the native liver, together with the thrombosed portal vein branches, will be removed in its entirety during LT. So far, the Yerdel,
      • Yerdel M.A.
      • Gunson B.
      • Mirza D.
      • Karayalçin K.
      • Olliff S.
      • Buckels J.
      • et al.
      Portal vein thrombosis in adults undergoing liver transplantation: risk factors, screening, management, and outcome.
      Jamieson,
      • Jamieson N.V.
      Changing perspectives in portal vein thrombosis and liver transplantation.
      and Charco
      • Charco R.
      • Fuster J.
      • Fondevila C.
      • Ferrer J.
      • Mans E.
      • García-Valdecasas J.C.
      Portal vein thrombosis in liver transplantation.
      grading systems are best at describing a correlation between the extent of thrombosis and surgical management at the time of LT. In Yerdel’s classification,
      • Yerdel M.A.
      • Gunson B.
      • Mirza D.
      • Karayalçin K.
      • Olliff S.
      • Buckels J.
      • et al.
      Portal vein thrombosis in adults undergoing liver transplantation: risk factors, screening, management, and outcome.
      grade 4 PVT denotes complete splanchnic vein thrombosis, including thrombosis of the portal vein and proximal superior mesenteric vein (SMV) and splenic vein. The surgical decisiveness of this classification is limited because it does not consider the coexistence of large spontaneous or surgical shunts that could be used for portal inflow reconstruction. The Jamieson
      • Jamieson N.V.
      Changing perspectives in portal vein thrombosis and liver transplantation.
      and Charco
      • Charco R.
      • Fuster J.
      • Fondevila C.
      • Ferrer J.
      • Mans E.
      • García-Valdecasas J.C.
      Portal vein thrombosis in liver transplantation.
      classification systems aim to define the complete or partial nature of thrombosis, denote the extent of thrombosis along the portal system, and account for the existence of large portosystemic collaterals. In both classification systems, grade 3 is defined as diffuse thrombosis of the splanchnic venous system with large accessible collaterals, whereas grade 4 includes extensive thrombosis of the splanchnic venous system with only fine collaterals. To define the surgical strategy for LT, group Yerdel grade 4 and Jamieson and Charco grades 3 and 4 PVT can be grouped together as “complex PVT” because the technical strategy for portal inflow reconstruction would be similar. In the same vein, we propose to classify less severe PVT (Yerdel grade 1-3 PVT) as “non-complex PVT”. These patients have partial or complete thrombosis limited to the portal vein trunk and/or the very distal part of the splenic vein and/or the SMV. Due to technical improvements, this can be resolved during LT using surgical thrombectomy, with standard porto-portal reconstruction, or an interposition vein graft from the SMV to the graft portal vein. Optimal outcomes with these approaches have been reported extensively and will not be discussed here.
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      The friendly incidental portal vein thrombus in liver transplantation.
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      “Complex PVT” has been defined in the proposed novel classification as grade 4 (Yerdel), and Grades 3 and 4 (Jamieson and Charco’s classifications).

      Prevalence of complex PVT in patients with cirrhosis at the time of LT

      Published studies (1998–2017, over 2 decades) reporting on the initial diagnosis of PVT, prevalence, and grade of PVT at the time of LT (single centre series only) were reviewed. A total of 28 studies reported on a total of 19,325 cirrhotic patients (Table S2).
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      Portal vein thrombosis in adults undergoing liver transplantation: risk factors, screening, management, and outcome.
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      Liver transplantation in patients with portal vein thrombosis.
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      Thrombendvenectomy for organized portal vein thrombosis at the time of liver transplantation.
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      Comparative analysis of the results of orthotopic liver transplantation in patients with and without portal vein thrombosis.
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      Portal vein thrombosis in patients undergoing orthotopic liver transplantation: intraoperative endovascular radiological procedures.
      • Egawa H.
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      Single center experience of 39 patients with preoperative portal vein thrombosis among 404 adult living donor liver transplantations.
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      Liver transplantation in adult patients with portal vein thrombosis: risk factors, management and outcome.
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      Management of portal vein thrombosis in liver transplantation: influence on morbidity and mortality.
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      The recipient with portal thrombosis and/or previous surgery.
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      Thrombosis confined to the portal vein is not a contraindication for living donor liver transplantation.
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      Liver transplant recipients with portal vein thrombosis: a single center retrospective study.
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      Single-center experience of 253 portal vein thrombosis patients undergoing liver transplantation in China.
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      Pre-existent portal vein thrombosis in liver transplantation: influence of pre-operative disease severity.
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      Portal vein thrombosis and liver transplantation: long term.
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      Prevention and treatment of rethrombosis after liver transplantation with an implantable pump of the portal vein.
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      Outcomes of liver transplantation in candidates with portal vein thrombosis.
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      • Zanello M.
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      • Ercolani G.
      • Cescon M.
      • Del Gaudio M.
      • et al.
      Portal vein thrombosis and liver transplantation: evolution during 10 years of experience at the University of Bologna.
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      • Lim C.
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      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
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      • et al.
      Restoration of portal flow using a pericholedochal varix in adult living donor liver transplantation for patients with total portosplenomesenteric thrombosis.
      • Hibi T.
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      • et al.
      When and why portal vein thrombosis matters in liver transplantation: a critical audit of 174 cases.
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      • et al.
      Prevalence and outcome of portal thrombosis in a cohort of cirrhotic patients undergoing liver transplantation.
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      • Ozer A.
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      • Emiroglu R.
      Liver transplantation in patients with complete portal vein thrombosis: renoportal or varicoportal anastomosis using cryopreserved vein grafts.
      The prevalence of non-tumoral PVT at LT was 5% to 26%, and the prevalence of complex PVT, as defined here, would range from 0% (9/27 analysable series) to 2.2%. The prevalence of non-tumoral PVT at LT may be falsely low because, up until the last decade, many LT teams around the world considered it a contraindication for LT, and hence LT in these patients was refused. In a systematic review of PVT in the transplant population, Rodríguez-Castro et al.
      • Rodríguez-Castro K.I.
      • Porte R.J.
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      analysed 41 studies published from 1986 to 2012 (25,753 patients) and found a 14.6% incidence of Yerdel grade 4 PVT (104/713 PVT cases), representing 2.8% of all LTs. The presence of large usable portosystemic shunts (spontaneous or surgical) was not analysed in either study. Similarly, 2 reviews based on the Organ Procurement and Transplant Network waitlist and first LT found that the prevalence of PVT at LT was between 6.8% and 8.7%.
      • Ghabril M.
      • Agarwal S.
      • Lacerda M.
      • Chalasani N.
      • Kwo P.
      • Tector A.J.
      Portal Vein Thrombosis Is a Risk Factor for Poor Early Outcomes After Liver Transplantation: Analysis of Risk Factors and Outcomes for Portal Vein Thrombosis in Waitlisted Patients.
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      • Perkins J.
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      The grade of PVT and the presence of shunts were not detailed in either review.
      In complex PVT, portal reconstruction can be considered “physiological” when the splanchnic blood is somehow redirected to the graft, thus resolving the pre-existing PHT.

      Definition of physiological vs. non-physiological portal flow reconstruction revisited

      In an audit of 174 cases of non-tumoral PVT at LT, Hibi et al.
      • Hibi T.
      • Nishida S.
      • Levi D.M.
      • Selvaggi G.
      • Tekin A.
      • Fan J.
      • et al.
      When and why portal vein thrombosis matters in liver transplantation: a critical audit of 174 cases.
      defined portal inflow reconstruction as non-physiological when porto-portal anastomosis could not be performed. According to that definition, inflow achieved by renoportal anastomosis (RPA), cavoportal hemitransposition, or portal vein arterialisation (see below) would all be types of non-physiological portal flow reconstruction. They also defined the terms anatomical and non-anatomical to denote the use of interposed grafts for portal inflow reconstruction.
      From a functional standpoint, we propose defining reconstruction of portal flow as physiological when the splanchnic venous blood (all or part of it) can be redirected to the liver graft. Hence, in addition to porto-portal anastomoses, reconstruction of physiological portal inflow is also possible by redirecting the blood flow from a large portosystemic shunt (spontaneous or surgical) to the graft, either by anastomosis of the shunt to the graft portal vein, or anastomosis of the tributary of the inferior vena cava (IVC), which drains this shunt, to the graft portal vein. This dichotomy is important because physiological portal flow reconstruction, as defined by us, should solve the problem of pre-existing prehepatic PHT due to PVT, either immediately or in the short/mid-term after LT. This is contrary to non-physiological portal flow reconstruction in which PHT persists, or even worsens following LT. Furthermore, it could be better to clearly specify whether the reconstruction requires an interposed biological or synthetic graft, rather than using the misleading terms anatomical and non-anatomical to denote this.
      Diligent management of PHT before, and after LT is key.
      Subsequently, we can consider that portal inflow reconstruction for non-complex PVT (as defined above) is always physiological. For patients with complex PVT, the available options for portal inflow reconstructions are dichotomised into physiological or non-physiological as follows.

      Physiological reconstructions

      The prevalence of large spontaneous portosystemic shunts in patients with end-stage liver disease undergoing LT ranges from 20% to 40%.
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      Association Between Portosystemic Shunts and Increased Complications and Mortality in Patients With Cirrhosis.
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      Ligation versus no ligation of spontaneous portosystemic shunts during liver transplantation: Audit of a prospective series of 66 consecutive patients.
      However, the available literature does not clarify the prevalence of large spontaneous portosystemic shunts in patients with complex PVT, which could be used for portal inflow reconstruction.
      Similarly, large collaterals (varices) that could be used for portal inflow in patients with cirrhosis and PHT include gastric (left gastric vein [LGV]), pericholedochal, and rarely dilated right superior colic, ileocolic, gastroepiploic, or the middle colic veins. The prevalence of gastric and pericholedochal varices in cirrhotic patients with significant PHT has been variably reported as 2–70%,
      • Bandali M.F.
      • Mirakhur A.
      • Lee E.W.
      • Ferris M.C.
      • Sadler D.J.
      • Gray R.R.
      • et al.
      Portal hypertension: Imaging of portosystemic collateral pathways and associated image-guided therapy.
      and 23–94%,
      • Palazzo L.
      • Hochain P.
      • Helmer C.
      • Cuillerier E.
      • Landi B.
      • Roseau G.
      • et al.
      Biliary varices on endoscopic ultrasonography: clinical presentation and outcome.
      respectively. However, what percentage of these varices are large enough to serve as an inflow, and their prevalence in patients with complex PVT is not known.

      Patients with a pre-existing portosystemic shunt (surgical or spontaneous)

      Left renal vein to graft portal vein anastomosis

      This technique is indicated in patients with a splenorenal shunt (SRS) (spontaneous or surgical): this end-to-end anastomosis between the left renal vein and the graft portal vein (so-called renoportal anastomosis or RPA) drains the splanchnic blood flow to the graft via the left renal vein as illustrated in Fig. 1. Sheil et al.
      • Sheil A.G.
      • Stephen M.S.
      • Chui A.K.
      • Ling J.
      • Bookallil M.J.
      A liver transplantation technique in a patient with a thrombosed portal vein and a functioning renal-lieno shunt.
      described the first case of native left renal vein to graft portal vein anastomosis in a patient with a thrombosed portal vein and a functioning, previously created, surgical end-to-end SRS. Kato et al.
      • Kato T.
      • Levi D.M.
      • DeFaria W.
      • Nishida S.
      • Tzakis A.G.
      Liver transplantation with renoportal anastomosis after distal splenorenal shunt.
      modified this procedure and used an interposition cadaveric vein graft in 5 patients with a patent surgically created distal SRS.
      Figure thumbnail gr1
      Fig. 1Reno-portal anastomosis. This reconstruction is physiological because it directs the large spleno-renal shunt into the graft portal vein via the left renal vein (with interposed vein graft). (A) Before transplantation; (B) After transplantation.
      Table 1 summarises 57 reported cases (1997–2017) of RPA in patients with PVT.
      • Bhangui P.
      • Lim C.
      • Salloum C.
      • Andreani P.
      • Sebbagh M.
      • Hoti E.
      • et al.
      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
      • Hibi T.
      • Nishida S.
      • Levi D.M.
      • Selvaggi G.
      • Tekin A.
      • Fan J.
      • et al.
      When and why portal vein thrombosis matters in liver transplantation: a critical audit of 174 cases.
      • Aktas H.
      • Ozer A.
      • Guner O.S.
      • Gurluler E.
      • Emiroglu R.
      Liver transplantation in patients with complete portal vein thrombosis: renoportal or varicoportal anastomosis using cryopreserved vein grafts.
      • Sheil A.G.
      • Stephen M.S.
      • Chui A.K.
      • Ling J.
      • Bookallil M.J.
      A liver transplantation technique in a patient with a thrombosed portal vein and a functioning renal-lieno shunt.
      • Kato T.
      • Levi D.M.
      • DeFaria W.
      • Nishida S.
      • Tzakis A.G.
      Liver transplantation with renoportal anastomosis after distal splenorenal shunt.
      • Marubashi S.
      • Dono K.
      • Nagano H.
      • Gotoh K.
      • Takahashi H.
      • Hashimoto K.
      • et al.
      Living-donor liver transplantation with renoportal anastomosis for patients with large spontaneous splenorenal shunts.
      • Moon D.B.
      • Lee S.G.
      • Ahn C.S.
      • Kim K.H.
      • Hwang S.
      • Ha T.Y.
      • et al.
      Technical modification of reno-portal anastomosis in living donor liver transplantation for patients with obliterated portal vein and large spontaneous splenorenal shunts.
      • González-Pinto I.M.
      • Miyar A.
      • García-Bernardo C.
      • Vázquez L.
      • Barneo L.
      • Cortés E.
      • et al.
      Renoportal anastomosis as a rescue technique in postoperative portal thrombosis in liver transplantation.
      • Perumalla R.
      • Jamieson N.V.
      • Praseedom R.K.
      Left renal vein as an option for portal inflow in liver transplant recipients with portal vein thrombosis.
      • Moon D.B.
      • Lee S.G.
      • Ahn C.S.
      • Ha T.Y.
      • Park G.C.
      • Yu Y.D.
      Side-to-end renoportal anastomosis using an externally stented polytetrafluoroethylene vascular graft for a patient with a phlebosclerotic portal vein and a large spontaneous splenorenal shunt.
      • Awad N.
      • Horrow M.M.
      • Parsikia A.
      • Brady P.
      • Zaki R.
      • Fishman M.D.
      • et al.
      Perioperative management of spontaneous splenorenal shunts in orthotopic liver transplant patients.
      • Matsumoto Y.
      • Ikegami T.
      • Morita K.
      • Yoshizumi T.
      • Kayashima H.
      • Shirabe K.
      • et al.
      Renoportal anastomosis in right lobe living donor liver transplantation: report of a case.
      • Quintini C.
      • Spaggiari M.
      • Hashimoto K.
      • Aucejo F.
      • Diago T.
      • Fujiki M.
      • et al.
      Safety and effectiveness of renoportal bypass in patients with complete portal vein thrombosis: an analysis of 10 patients.
      • Nazzal M.
      • Sun Y.
      • Okoye O.
      Reno-portal shunt for liver transplant, an alternative inflow for recipients with grade III-IV portal vein thrombosis: Tips for a better outcome.
      • Ozdemir F.
      • Kutluturk K.
      • Barut B.
      • Abbasov P.
      • Kutlu R.
      • Kayaalp C.
      • et al.
      Renoportal anastomosis in living donor liver transplantation with prior proximal splenorenal shunt.
      Thirty-two of these patients had a spontaneous SRS, 13 had a previously created surgical SRS, and in 6 patients, the type of pre-existing shunt (spontaneous or surgical) was not specified. One patient had a pre-existing mesorenal shunt. In 5 cases, RPA was performed in patients without pre-existing SRSs
      • Bhangui P.
      • Lim C.
      • Salloum C.
      • Andreani P.
      • Sebbagh M.
      • Hoti E.
      • et al.
      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
      • Marubashi S.
      • Dono K.
      • Nagano H.
      • Gotoh K.
      • Takahashi H.
      • Hashimoto K.
      • et al.
      Living-donor liver transplantation with renoportal anastomosis for patients with large spontaneous splenorenal shunts.
      (see below, section of non-physiological reconstructions). Considering the analysable data, postoperative variceal bleeding, acute kidney injury, and PVT occurred in 7%, 20%, and 6% of patients, respectively. The postoperative mortality rate was 16% (8/51 analysable cases). Among 51 analysable cases, 41 (81%) patients were alive and well with patent portal flow at the last follow-up visit (2 months to 5 years after surgery).
      Portal reconstruction in complex PVT depends upon the presence of large spontaneous (splenorenal being most common) or previously surgically created portosystemic shunts. Renoportal anastomosis is the reconstruction of choice in case of a pre-existing splenorenal shunt.
      Table 1Reported series of renoportal anastomosis.
      Author, yearrefNPostoperative mortalityPatients alive/ follow-up
      Sheil, 1997
      • Sheil A.G.
      • Stephen M.S.
      • Chui A.K.
      • Ling J.
      • Bookallil M.J.
      A liver transplantation technique in a patient with a thrombosed portal vein and a functioning renal-lieno shunt.
      101/1 (5 years)
      Kato, 2000
      • Kato T.
      • Levi D.M.
      • DeFaria W.
      • Nishida S.
      • Tzakis A.G.
      Liver transplantation with renoportal anastomosis after distal splenorenal shunt.
      514/5 (3–41 months)
      Marubashi, 2005
      • Marubashi S.
      • Dono K.
      • Nagano H.
      • Gotoh K.
      • Takahashi H.
      • Hashimoto K.
      • et al.
      Living-donor liver transplantation with renoportal anastomosis for patients with large spontaneous splenorenal shunts.
      303/3(12–48 months)
      Moon, 2008
      • Moon D.B.
      • Lee S.G.
      • Ahn C.S.
      • Kim K.H.
      • Hwang S.
      • Ha T.Y.
      • et al.
      Technical modification of reno-portal anastomosis in living donor liver transplantation for patients with obliterated portal vein and large spontaneous splenorenal shunts.
      514/5 (1–35 months)
      Gonzalez-Pinto, 2009
      • González-Pinto I.M.
      • Miyar A.
      • García-Bernardo C.
      • Vázquez L.
      • Barneo L.
      • Cortés E.
      • et al.
      Renoportal anastomosis as a rescue technique in postoperative portal thrombosis in liver transplantation.
      101/1 (2 months)
      Perumalla, 2008
      • Perumalla R.
      • Jamieson N.V.
      • Praseedom R.K.
      Left renal vein as an option for portal inflow in liver transplant recipients with portal vein thrombosis.
      101/1 (12 months)
      Bhangui, 201
      • Bhangui P.
      • Lim C.
      • Salloum C.
      • Andreani P.
      • Sebbagh M.
      • Hoti E.
      • et al.
      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
      17611/17 (3–144 months)
      Moon, 2011
      • Moon D.B.
      • Lee S.G.
      • Ahn C.S.
      • Ha T.Y.
      • Park G.C.
      • Yu Y.D.
      Side-to-end renoportal anastomosis using an externally stented polytetrafluoroethylene vascular graft for a patient with a phlebosclerotic portal vein and a large spontaneous splenorenal shunt.
      101/1 (8 months)
      Awad, 2012
      • Awad N.
      • Horrow M.M.
      • Parsikia A.
      • Brady P.
      • Zaki R.
      • Fishman M.D.
      • et al.
      Perioperative management of spontaneous splenorenal shunts in orthotopic liver transplant patients.
      10Yes/1 (N
      Matsumoto, 2013
      • Matsumoto Y.
      • Ikegami T.
      • Morita K.
      • Yoshizumi T.
      • Kayashima H.
      • Shirabe K.
      • et al.
      Renoportal anastomosis in right lobe living donor liver transplantation: report of a case.
      101/1 (4 months)
      Hibi, 2014
      • Hibi T.
      • Nishida S.
      • Levi D.M.
      • Selvaggi G.
      • Tekin A.
      • Fan J.
      • et al.
      When and why portal vein thrombosis matters in liver transplantation: a critical audit of 174 cases.
      6n.a.n.a./6
      Quintini, 2015
      • Quintini C.
      • Spaggiari M.
      • Hashimoto K.
      • Aucejo F.
      • Diago T.
      • Fujiki M.
      • et al.
      Safety and effectiveness of renoportal bypass in patients with complete portal vein thrombosis: an analysis of 10 patients.
      10010/10 (mean: 42.2 ± 21.1 months)
      Aktas, 2017
      • Aktas H.
      • Ozer A.
      • Guner O.S.
      • Gurluler E.
      • Emiroglu R.
      Liver transplantation in patients with complete portal vein thrombosis: renoportal or varicoportal anastomosis using cryopreserved vein grafts.
      202/2 (8–36 months)
      Nazzal, 2017
      • Nazzal M.
      • Sun Y.
      • Okoye O.
      Reno-portal shunt for liver transplant, an alternative inflow for recipients with grade III-IV portal vein thrombosis: Tips for a better outcome.
      211/2 (11 months
      Ozdemir, 2017
      • Ozdemir F.
      • Kutluturk K.
      • Barut B.
      • Abbasov P.
      • Kutlu R.
      • Kayaalp C.
      • et al.
      Renoportal anastomosis in living donor liver transplantation with prior proximal splenorenal shunt.
      110/1
      n.a., not available; N, number of patients.

      Large left gastric vein to portal vein anastomosis

      Czerniak et al.
      • Czerniak A.
      • Badger I.
      • Sherlock D.
      • Buckels J.
      Orthotopic liver transplantation in a patient with thrombosis of the hepatic portal and superior mesenteric veins.
      first reported on anastomosis of a large LGV functioning as a spontaneous portosystemic shunt to the graft portal vein (so-called coronary-portal anastomosis) in a patient with complete PVT (Fig. 2). Table 2 summarises the 37 reported cases (1990–2018) of LGV to portal anastomosis.
      • Stieber A.C.
      • Zetti G.
      • Todo S.
      • Tzakis A.G.
      • Fung J.J.
      • Marino I.
      • et al.
      The spectrum of portal vein thrombosis in liver transplantation.
      • Orlando G.
      • De Luca L.
      • Toti L.
      • Zazza S.
      • Angelico M.
      • Casciani C.U.
      • et al.
      Liver transplantation in the presence of portal vein thrombosis: report from a single center.
      • Lladó L.
      • Fabregat J.
      • Castellote J.
      • Ramos E.
      • Torras J.
      • Jorba R.
      • et al.
      Management of portal vein thrombosis in liver transplantation: influence on morbidity and mortality.
      • Pan C.
      • Shi Y.
      • Zhang J.J.
      • Deng Y.L.
      • Zheng H.
      • Zhu Z.J.
      • et al.
      Single-center experience of 253 portal vein thrombosis patients undergoing liver transplantation in China.
      • Ramos A.P.
      • Reigada C.P.
      • Ataíde E.C.
      • Almeida J.R.
      • Cardoso A.R.
      • Caruy C.A.
      • et al.
      Portal vein thrombosis and liver transplantation: long term.
      • Ravaioli M.
      • Zanello M.
      • Grazi G.L.
      • Ercolani G.
      • Cescon M.
      • Del Gaudio M.
      • et al.
      Portal vein thrombosis and liver transplantation: evolution during 10 years of experience at the University of Bologna.
      • Kim J.D.
      • Choi D.L.
      • Han Y.S.
      An early single-center experience of portal vein thrombosis in living donor liver transplantation: clinical feature, management and outcome.
      • Hibi T.
      • Nishida S.
      • Levi D.M.
      • Selvaggi G.
      • Tekin A.
      • Fan J.
      • et al.
      When and why portal vein thrombosis matters in liver transplantation: a critical audit of 174 cases.
      • Simón-Talero M.
      • Roccarina D.
      • Martínez J.
      • Lampichler K.
      • Baiges A.
      • Low G.
      • et al.
      Association Between Portosystemic Shunts and Increased Complications and Mortality in Patients With Cirrhosis.
      • Czerniak A.
      • Badger I.
      • Sherlock D.
      • Buckels J.
      Orthotopic liver transplantation in a patient with thrombosis of the hepatic portal and superior mesenteric veins.
      • Maluf D.
      • Shim I.
      • Posner M.
      • Cotterell A.H.
      • Fisher R.A.
      Salvage procedure for unexpected portal vein thrombosis in living donor liver transplantation.
      • Wu T.H.
      • Chou H.S.
      • Pan K.T.
      • Lee C.S.
      • Wu T.J.
      • Chu S.Y.
      • et al.
      Application of cryopreserved vein grafts as a conduit between the coronary vein and liver graft to reconstruct portal flow in adult living liver transplantation.
      • Alexopoulos S.P.
      • Thomas E.
      • Berry E.
      • Whang G.
      • Matsuoka L.
      The portal vein-variceal anastomosis: an important technique for establishing portal vein inflow.
      • Wang Z.
      • Yang L.
      Gastric coronary vein to portal vein reconstruction in liver transplant: case report.
      • Teixeira U.F.
      • Machry M.C.
      • Goldoni M.B.
      • Kruse C.
      • Diedrich J.A.
      • Rodrigues P.D.
      • et al.
      Use of Left Gastric Vein as an Alternative for Portal Flow Reconstruction in Liver Transplantation.
      • Safwan M.
      • Nagai S.
      • Abouljoud M.S.
      Portal Vein Inflow From Enlarged Coronary Vein in Liver Transplantation: Surgical Approach and Technical Tips: A Case Report.
      All reports were single case reports or small case series (median number of cases per publication = 2) without details regarding the postoperative morbidity. The postoperative mortality (in papers mentioning this outcome) was nil. Long-term results were available in 24 patients, and 22 (92%) patients were reported to be alive and well with a patent portal reconstruction at the last follow-up visit.
      Figure thumbnail gr2
      Fig. 2Coronary-portal anastomosis. This reconstruction is physiological because it directs the large left gastric vein (coronary vein) into the graft portal vein (with interposed vein graft). (A) Initial control in the recipient; (B) After reconstruction of portal inflow.
      Table 2Reported cases of use of left gastric vein for portal vein inflow in complex PVT.
      Author, yearrefNOutcome (shunt patency, patient last follow-up status, duration)
      Czerniak, 1990
      • Czerniak A.
      • Badger I.
      • Sherlock D.
      • Buckels J.
      Orthotopic liver transplantation in a patient with thrombosis of the hepatic portal and superior mesenteric veins.
      1Patent, well, 3 months
      Stieber, 1991
      • Stieber A.C.
      • Zetti G.
      • Todo S.
      • Tzakis A.G.
      • Fung J.J.
      • Marino I.
      • et al.
      The spectrum of portal vein thrombosis in liver transplantation.
      1Patent, well, 6 years
      Orlando, 2004
      • Orlando G.
      • De Luca L.
      • Toti L.
      • Zazza S.
      • Angelico M.
      • Casciani C.U.
      • et al.
      Liver transplantation in the presence of portal vein thrombosis: report from a single center.
      2n.a.
      Maluf, 2006
      • Maluf D.
      • Shim I.
      • Posner M.
      • Cotterell A.H.
      • Fisher R.A.
      Salvage procedure for unexpected portal vein thrombosis in living donor liver transplantation.
      1Patent, well, 24 months
      Llado, 2007
      • Lladó L.
      • Fabregat J.
      • Castellote J.
      • Ramos E.
      • Torras J.
      • Jorba R.
      • et al.
      Management of portal vein thrombosis in liver transplantation: influence on morbidity and mortality.
      5n.a.
      Pan, 2009
      • Pan C.
      • Shi Y.
      • Zhang J.J.
      • Deng Y.L.
      • Zheng H.
      • Zhu Z.J.
      • et al.
      Single-center experience of 253 portal vein thrombosis patients undergoing liver transplantation in China.
      4n.a.
      Wu, 2009
      • Wu T.H.
      • Chou H.S.
      • Pan K.T.
      • Lee C.S.
      • Wu T.J.
      • Chu S.Y.
      • et al.
      Application of cryopreserved vein grafts as a conduit between the coronary vein and liver graft to reconstruct portal flow in adult living liver transplantation.
      3Patent, well, 21, 36, 36 months after LT
      Ramos, 2010
      • Ramos A.P.
      • Reigada C.P.
      • Ataíde E.C.
      • Almeida J.R.
      • Cardoso A.R.
      • Caruy C.A.
      • et al.
      Portal vein thrombosis and liver transplantation: long term.
      1n.a.
      Kim, 2011
      • Kim J.D.
      • Choi D.L.
      • Han Y.S.
      An early single-center experience of portal vein thrombosis in living donor liver transplantation: clinical feature, management and outcome.
      3Shunt patent, long term in 2, thrombosed in 1 patient, all patients well at last follow up
      Ravaioli, 2011
      • Ravaioli M.
      • Zanello M.
      • Grazi G.L.
      • Ercolani G.
      • Cescon M.
      • Del Gaudio M.
      • et al.
      Portal vein thrombosis and liver transplantation: evolution during 10 years of experience at the University of Bologna.
      3n.a., 1 patient died, 2 alive at last follow-up
      Hibi, 2014
      • Hibi T.
      • Nishida S.
      • Levi D.M.
      • Selvaggi G.
      • Tekin A.
      • Fan J.
      • et al.
      When and why portal vein thrombosis matters in liver transplantation: a critical audit of 174 cases.
      1n.a.
      Alexopoulos, 2014
      • Alexopoulos S.P.
      • Thomas E.
      • Berry E.
      • Whang G.
      • Matsuoka L.
      The portal vein-variceal anastomosis: an important technique for establishing portal vein inflow.
      5All shunts patent (1 after surgical revision), all patients well, median follow up 2.3 years
      Wang, 2014
      • Wang Z.
      • Yang L.
      Gastric coronary vein to portal vein reconstruction in liver transplant: case report.
      1Patent, well, 1 year
      Teixeira, 2016
      • Teixeira U.F.
      • Machry M.C.
      • Goldoni M.B.
      • Kruse C.
      • Diedrich J.A.
      • Rodrigues P.D.
      • et al.
      Use of Left Gastric Vein as an Alternative for Portal Flow Reconstruction in Liver Transplantation.
      2Patent, well, 5 years, 1 month
      Safwan, 2016
      • Safwan M.
      • Nagai S.
      • Abouljoud M.S.
      Portal Vein Inflow From Enlarged Coronary Vein in Liver Transplantation: Surgical Approach and Technical Tips: A Case Report.
      1Patent, well, 3 months
      Gomez Gavara, 2018
      • Gomez Gavara C.
      • Bhangui P.
      • Salloum C.
      • Osseis M.
      • Esposito F.
      • Moussallem T.
      • et al.
      Ligation versus no ligation of spontaneous portosystemic shunts during liver transplantation: Audit of a prospective series of 66 consecutive patients.
      3Patent and well at 1, 2, 2 years
      n.a., not available; PVT, portal vein thrombosis; N, number of patients.

      Large pericholedochal varix to portal vein anastomosis

      In some cases of complex PVT, a large pericholedochal varix running anterolateral to the main bile duct is the only portal inflow to the liver.
      • Spira R.
      • Widrich W.C.
      • Keusch K.D.
      • Jackson B.T.
      • Katzman H.E.
      • Coello A.A.
      Bile duct varices.
      • Couinaud C.
      The parabiliary venous system.
      Hiatt et al.
      • Hiatt J.R.
      • Quinones-Baldrich W.J.
      • Ramming K.P.
      • Lois J.F.
      • Busuttil R.W.
      Bile duct varices. An alternative to portoportal anastomosis in liver transplantation.
      first reported the use of a pericholedochal varix as portal inflow to the graft.
      In this technique, an end-to-end anastomosis is constructed between the graft portal vein and varix (Fig. 3). In this setting, a Roux-en-Y hepaticojejunostomy is logical because of the risk of injury to the sole portal flow available.
      Figure thumbnail gr3
      Fig. 3Pericholedochal varix to portal vein anastomosis. This reconstruction is physiological because it directs the large pericholedochal varix to the graft portal vein. (A) Before transplantation; (B) After transplantation.
      Eleven cases (1986–2017) of pericholedochal varix to portal vein anastomosis have been reported in patients with complex PVT
      • Moon D.B.
      • Lee S.G.
      • Ahn C.S.
      • Hwang S.
      • Kim K.H.
      • Ha T.Y.
      • et al.
      Restoration of portal flow using a pericholedochal varix in adult living donor liver transplantation for patients with total portosplenomesenteric thrombosis.
      • Cherqui D.
      • Duvoux C.
      • Rahmouni A.
      • Rotman N.
      • Dhumeaux D.
      • Julien M.
      • et al.
      Orthotopic liver transplantation in the presence of partial or total portal vein thrombosis: problems in diagnosis and management.
      • Kniepeiss D.
      • Müller H.
      • Wagner D.
      • Iberer F.
      • Tscheliessnigg K.H.
      Management of complications after varicoportal anastomosis in liver transplantation.
      • Lee S.
      • Kim D.J.
      • Kim I.G.
      • Jeon J.Y.
      • Jung J.P.
      • Choi G.S.
      • et al.
      Use of pericholedochal plexus for portal flow reconstruction in diffuse portal vein thrombosis: case report.
      • Kim J.D.
      • Choi D.L.
      • Han Y.S.
      The paracholedochal vein: a feasible option as portal inflow in living donor liver transplantation.
      • Bharathy K.G.
      • Sasturkar S.V.
      • Sinha P.K.
      • Kumar S.
      • Pamecha V.
      Portal Inflow in Extensive Portomesenteric Thrombosis: Using the Pericholedochal Varix in Living Donor Liver Transplantation.
      • Yu Y.D.
      • Kim D.S.
      • Han J.H.
      • Yoon Y.I.
      Successful Treatment of a Patient With Diffuse Portosplenomesenteric Thrombosis Using a Pericholedochal Varix for Portal Flow Reconstruction During Deceased Donor Liver Transplantation: A Case Report.
      (Table 3). Postoperative mortality was nil and postoperative morbidity could not be clarified. With a follow-up ranging from 12 to 92 months, 9/10 (90%) patients were reported as well with a patent portal reconstruction.
      Table 3Reported cases of use of pericholedochal varix to graft portal vein anastomosis.
      Author, yearrefNPVT GradeBiliary reconstructionOutcome
      Hiatt, 1986
      • Hiatt J.R.
      • Quinones-Baldrich W.J.
      • Ramming K.P.
      • Lois J.F.
      • Busuttil R.W.
      Bile duct varices. An alternative to portoportal anastomosis in liver transplantation.
      1Yerdel 4Duct to ductPatent and well, 12 months
      Santoni, 1990
      • Santoni P.
      • Johanet H.
      • Pras-Jude N.
      • Houssin D.
      • Chapuis Y.
      Orthotopic liver transplantation in patients with complete obliteration of the portal vein.
      1Diffusen.a.Died 12 months, patent
      Cherqui, 1993
      • Cherqui D.
      • Duvoux C.
      • Rahmouni A.
      • Rotman N.
      • Dhumeaux D.
      • Julien M.
      • et al.
      Orthotopic liver transplantation in the presence of partial or total portal vein thrombosis: problems in diagnosis and management.
      1Diffusen.a.n.a.
      Kniepeiss, 2011
      • Kniepeiss D.
      • Müller H.
      • Wagner D.
      • Iberer F.
      • Tscheliessnigg K.H.
      Management of complications after varicoportal anastomosis in liver transplantation.
      1Diffusen.a.Patent and well, 6 months
      Lee, 2014
      • Lee S.
      • Kim D.J.
      • Kim I.G.
      • Jeon J.Y.
      • Jung J.P.
      • Choi G.S.
      • et al.
      Use of pericholedochal plexus for portal flow reconstruction in diffuse portal vein thrombosis: case report.
      1Yerdel 4n.a.Patent and well, 24 months
      Kim, 2014
      • Kim J.D.
      • Choi D.L.
      • Han Y.S.
      The paracholedochal vein: a feasible option as portal inflow in living donor liver transplantation.
      2Yerdel 4Roux-en-YPatent and well, 22, 21 months
      Moon, 2014
      • Moon D.B.
      • Lee S.G.
      • Ahn C.S.
      • Hwang S.
      • Kim K.H.
      • Ha T.Y.
      • et al.
      Restoration of portal flow using a pericholedochal varix in adult living donor liver transplantation for patients with total portosplenomesenteric thrombosis.
      2Diffusen.a.Patent and well, 44, 92 months
      Bharathy, 2017
      • Bharathy K.G.
      • Sasturkar S.V.
      • Sinha P.K.
      • Kumar S.
      • Pamecha V.
      Portal Inflow in Extensive Portomesenteric Thrombosis: Using the Pericholedochal Varix in Living Donor Liver Transplantation.
      1DiffuseRoux-en-YPatent and well, 39 months
      Yu, 2017
      • Yu Y.D.
      • Kim D.S.
      • Han J.H.
      • Yoon Y.I.
      Successful Treatment of a Patient With Diffuse Portosplenomesenteric Thrombosis Using a Pericholedochal Varix for Portal Flow Reconstruction During Deceased Donor Liver Transplantation: A Case Report.
      1DiffuseRoux-en-YPatent and well, (stent), 9 months
      n.a., not available; PVT, portal vein thrombosis; N, number of patients.

      Use of other varices or pre-existing shunts

      Other varices have been used to reconstruct the portal inflow to the graft, including the right superior colic vein,
      • Cherqui D.
      • Duvoux C.
      • Rahmouni A.
      • Rotman N.
      • Dhumeaux D.
      • Julien M.
      • et al.
      Orthotopic liver transplantation in the presence of partial or total portal vein thrombosis: problems in diagnosis and management.
      ileocolic vein,
      • Langnas A.N.
      • Marujo W.C.
      • Stratta R.J.
      • Wood R.P.
      • Ranjan D.
      • Ozaki C.
      • et al.
      A selective approach to preexisting portal vein thrombosis in patients with liver transplantation.
      gastroepiploic vein,
      • Davidson B.R.
      • Gibson M.
      • Dick R.
      • Burroughs A.
      • Rolles K.
      Incidence, risk factors, management and outcome of portal vein abnormalities at orthotopic liver transplantation.
      or the middle colic vein.
      • Rudroff C.
      • Scheele J.
      The middle colic vein: an alternative source of portal inflow in orthotopic liver transplantation complicated by portal vein thrombosis.
      The surgical technique is similar to that described for LGV to donor portal vein anastomosis.
      Similarly, in the case of pre-existing spontaneous mesenterico-iliac or surgically created mesocaval shunts that cannot be dismantled, cavoportal hemitransposition (see below for the technical aspects) may be a good option.
      • Memeo R.
      • Salloum C.
      • Subar D.
      • De'angelis N.
      • Zantidenas D.
      • Compagnon P.
      • et al.
      Transformation of cavoportal inflow to renoportal inflow to the graft during liver transplantation for stage IV portal vein thrombosis.
      The latter may still qualify as a physiological inflow because cavoportal hemitransposition drains the portal flow via the IVC to the graft (Fig. 4). However, this latter point is still debatable, as this reconstruction may still be considered non-physiological as some of these patients continue to have persistent PHT, leading to bleeding complications and requiring surgical and/or endoscopic interventions even in the long-term.
      Figure thumbnail gr4
      Fig. 4Cavo-portal anastomosis after graft implantation. (A) With division of the vena cava (the whole caval flow is directed to the graft); (B) Without calibration of the inferior vena cava; (C) With calibration of the inferior vena cava (part of the caval flow is directed to the graft). In case of a mesocaval shunt that cannot be dismantled (as illustrated here), these reconstructions are physiological. Otherwise, these reconstructions are non-physiological.
      The reported postoperative mortality of different physiological reconstructions detailed above is very heterogeneous, primarily because of the data being derived from single case reports, or a small case series, and also due to variable follow-up durations. The reported postoperative mortality in the RPA group was 19%, and 0% in the LGV and pericholedochal varices groups (Table 1, Table 2, Table 3). However, there could be a significant reporting bias, especially in the review based on case reports, because there is always a tendency to report successful cases, and not the ones in which the patients did not survive after attempts at such procedures for portal inflow.
      There are indeed some rare situations where anastomosis between the mesenteric and gonadal vein, followed by RPA are performed for portal inflow. The question remains whether the PHT, which can be documented in the form of collaterals by imaging or by repeat endoscopy, actually resolves in the long run in such cases. If the PHT resolves, only then can this reconstruction be considered truly physiological.

      Patients with complex PVT with no pre-existing shunts

      Other options of physiological reconstruction in the absence of pre-existing shunts or large varices

      A rare situation is the presence of a patent mid-portion of the splenic vein without a large usable portosystemic shunt. In this situation, it is possible to achieve a physiological portal reconstruction as follows: a latero-lateral splenorenal anastomosis is performed (with an interposed vein, artery, or synthetic graft). Then, end-to-end RPA as described above is performed. One such case was performed at our centre (unpublished). Potentially, the same strategy could be used by anastomosing a large inferior mesenteric vein to the left gonadal vein
      • Kim H.B.
      • Pomposelli J.J.
      • Lillehei C.W.
      • Jenkins R.L.
      • Jonas M.M.
      • Krawczuk L.E.
      • et al.
      Mesogonadal shunts for extrahepatic portal vein thrombosis and variceal hemorrhage.
      or left renal vein,
      • Yamamoto S.
      • Sato Y.
      • Nakatsuka H.
      • Oya H.
      • Kobayashi T.
      • Hatakeyama K.
      Beneficial effect of partial portal decompression using the inferior mesenteric vein for intractable gastroesophageal variceal bleeding in patients with liver cirrhosis.
      followed by RPA or, for that matter, any other large collateral to the IVC
      • Hau H.M.
      • Fellmer P.
      • Schoenberg M.B.
      • Schmelzle M.
      • Morgul M.H.
      • Krenzien F.
      • et al.
      The collateral caval shunt as an alternative to classical shunt procedures in patients with recurrent duodenal varices and extrahepatic portal vein thrombosis.
      followed by cavoportal anastomosis (CPA). Ultimately, this would amount to a physiological portal inflow to the graft.
      In patients with complex PVT, a thorough evaluation of the choices for portal inflow should be performed well in advance of LT, whenever possible.
      In the presence of a patent proximal splenic vein (in the splenic hilum) without a large usable shunt, the concept of heterotopic LT in the splenic fossa is an option.
      • Muscari F.
      • Suc B.
      • Fourtanier G.
      • Escat J.
      Liver transplantation in the presence of a non-functional portal vein: an original technique.
      This was recently reported by our team during retransplantation of a patient with complex PVT.
      • Azoulay D.
      • Lahat E.
      • Salloum C.
      • Compagnon P.
      • Feray C.
      Heterotopic liver retransplantation for impossible former graft explantation.
      Regarding the surgical approach used during recipient hepatectomy in patients with diffuse PVT, Lerut et al.
      • Lerut J.P.
      • Mazza D.
      • van Leeuw V.
      • Laterre P.F.
      • Donataccio M.
      • de Ville de Goyet J.
      • et al.
      Adult liver transplantation and abnormalities of splanchnic veins: experience in 53 patients.
      proposed that the extent of thrombosis and quality of the vessel wall should determine the use of a hilar or infracolic approach to the portomesenteric system. The latter is preferred, especially if the portal vein is reduced to a fibrotic vessel remnant, or if inflammatory portal vein changes are present. Additionally, in the presence of portal phlebitis, a jump graft from the SMV may be preferable as a primary approach, even in grade 3 (Yerdel) PVT, rather than an attempt to dissect out and perform an anastomosis using the portal vein.

      Combined liver and multivisceral transplantation

      The first case of a successful multivisceral transplant (MVT) in a patient with complete thrombosis of the portomesenteric system due to protein C deficiency was reported by Florman et al. in 2002.
      • Florman S.S.
      • Fishbein T.M.
      • Schiano T.
      • Letizia A.
      • Fennelly E.
      • DeSancho M.
      Multivisceral transplantation for portal hypertension and diffuse mesenteric thrombosis caused by protein C deficiency.
      In this case, liver function was normal and there were no signs of PHT before or after MVT.
      Tremendous progress has been made in the field of MVT in the last decade; some expert centres have reported good results with MVT in LT recipients with diffuse PVT, in whom no other option is available to establish mesenteric drainage and physiological portal inflow to the graft
      • Florman S.S.
      • Fishbein T.M.
      • Schiano T.
      • Letizia A.
      • Fennelly E.
      • DeSancho M.
      Multivisceral transplantation for portal hypertension and diffuse mesenteric thrombosis caused by protein C deficiency.
      • Vianna R.M.
      • Mangus R.S.
      • Chandrashekhar K.
      • Fridell J.A.
      • Beduschi T.
      • Tector A.J.
      Multivisceral transplantation for diffuse portomesenteric thrombosis.
      (Table 4). In the largest series published by Vianna et al.,
      • Vianna R.M.
      • Mangus R.S.
      • Chandrashekhar K.
      • Fridell J.A.
      • Beduschi T.
      • Tector A.J.
      Multivisceral transplantation for diffuse portomesenteric thrombosis.
      relatively good long-term survival was reported in 25 patients with diffuse PVT who underwent MVT (patient and graft survival were 80%, 72%, and 72% at 1, 3, and 5 years, respectively). However, 7 patients (28%) died at a median of 5 months (range, 1–22 months) and surgical complications were encountered in 14 patients (56%).
      Table 4Reported cases of multivisceral transplantation for PVT.
      Author, yearrefNDiseaseComplicationsOutcome
      Florman, 2002
      • Florman S.S.
      • Fishbein T.M.
      • Schiano T.
      • Letizia A.
      • Fennelly E.
      • DeSancho M.
      Multivisceral transplantation for portal hypertension and diffuse mesenteric thrombosis caused by protein C deficiency.
      1Protein C deficiency without cirrhosisAcute rejectionPatent PV, well at 17 months
      Vianna, 2015
      • Vianna R.M.
      • Mangus R.S.
      • Chandrashekhar K.
      • Fridell J.A.
      • Beduschi T.
      • Tector A.J.
      Multivisceral transplantation for diffuse portomesenteric thrombosis.
      25Morbidity = 57%Mortality = 28%, patient and graft survival: 80%, 72%, and 72% at 1, 3, and 5 years
      Meira Filho, 2015
      • Abu-Elmagd K.M.
      • Kosmach-Park B.
      • Costa G.
      • Zenati M.
      • Martin L.
      • Koritsky D.A.
      • et al.
      Long-term survival, nutritional autonomy, and quality of life after intestinal and multivisceral transplantation.
      2Cryptogenic cirrhosisIschaemic cholangiopathyDied of infection at 8 months
      NASH cirrhosisGraft vs. host diseaseDied of graft vs. host disease at 34 days
      Ceulemans, 2015
      • Grant D.
      • Abu-Elmagd K.
      • Mazariegos G.
      • Vianna R.
      • Langnas A.
      • Mangus R.
      • et al.
      Intestinal transplant registry report: global activity and trends.
      3Antiphospholipid syndrome, no cirrhosisRemaining left colon ischaemia, rejection, aspergillosis1 died, 2 survived, 7 and 7 months
      Neuroendocrine tumour, no cirrhosisResection of distal ileum, acute rejection
      Alcoholic cirrhosisMycotic aneurysm
      NASH, non-alcoholic steatohepatitis; PVT, portal vein thrombosis; N, number of patients.
      Pooled data shows 5-year survival rates for MVT (5-year actuarial patient and graft survival 60% and 50%, respectively), and intestinal transplant (actuarial patient survival rates are 76% and 56% at 1 and 5 years, respectively), are indeed improving over time.
      • Abu-Elmagd K.M.
      • Kosmach-Park B.
      • Costa G.
      • Zenati M.
      • Martin L.
      • Koritsky D.A.
      • et al.
      Long-term survival, nutritional autonomy, and quality of life after intestinal and multivisceral transplantation.
      • Grant D.
      • Abu-Elmagd K.
      • Mazariegos G.
      • Vianna R.
      • Langnas A.
      • Mangus R.
      • et al.
      Intestinal transplant registry report: global activity and trends.
      Notably, in addition to total hepatectomy, MVT requires massive evisceration (of the stomach, pancreaticoduodenal complex, spleen, small intestine, and portion of the large intestine) to place the multivisceral graft. The intestinal component of the MVT is also associated with additional risks of rejection, chronic diarrhoea, and graft versus host disease.
      MVT is theoretically the ideal treatment in complex PVT with no pre-existing portacaval shunt (spontaneous or surgical) but is still limited to highly specialised centres.

      Non-physiological reconstructions

      These reconstructions pertain to patients with complex PVT and no large accessible portosystemic shunt (spontaneous or surgical).

      Cavoportal anastomosis (cavoportal hemitransposition)

      The use of CPA in patients with diffuse PVT was first described by Tzakis in 1998.
      • Tzakis A.G.
      • Kirkegaard P.
      • Pinna A.D.
      • Jovine E.
      • Misiakos E.P.
      • Maziotti A.
      • et al.
      Liver transplantation with cavoportal hemitransposition in the presence of diffuse portal vein thrombosis.
      Fig. 4 illustrates the various techniques used to establish caval inflow to the graft.
      A total of 28 series have described CPA in 86 adult patients (89 procedures) for grade 4 PVT as defined by Yerdel (Table S3).
      • Bertelli R.
      • Nardo B.
      • Montalti R.
      • Beltempo P.
      • Puviani L.
      • Cavallari A.
      Liver transplantation in recipients with portal vein thrombosis: experience of a single transplant center.
      • Egawa H.
      • Tanaka K.
      • Kasahara M.
      • Takada Y.
      • Oike F.
      • Ogawa K.
      • et al.
      Single center experience of 39 patients with preoperative portal vein thrombosis among 404 adult living donor liver transplantations.
      • Lladó L.
      • Fabregat J.
      • Castellote J.
      • Ramos E.
      • Torras J.
      • Jorba R.
      • et al.
      Management of portal vein thrombosis in liver transplantation: influence on morbidity and mortality.
      • Tao Y.F.
      • Teng F.
      • Wang Z.X.
      • Guo W.Y.
      • Shi X.M.
      • Wang G.H.
      • et al.
      Liver transplant recipients with portal vein thrombosis: a single center retrospective study.
      • Pan C.
      • Shi Y.
      • Zhang J.J.
      • Deng Y.L.
      • Zheng H.
      • Zhu Z.J.
      • et al.
      Single-center experience of 253 portal vein thrombosis patients undergoing liver transplantation in China.
      • Suarez Artacho G.
      • Barrera Pulido L.
      • Alamo Martinez J.M.
      • Serrano Diez-Canedo J.
      • Bernal Bellido C.
      • Marín Gomez L.M.
      • et al.
      Outcomes of liver transplantation in candidates with portal vein thrombosis.
      • Ravaioli M.
      • Zanello M.
      • Grazi G.L.
      • Ercolani G.
      • Cescon M.
      • Del Gaudio M.
      • et al.
      Portal vein thrombosis and liver transplantation: evolution during 10 years of experience at the University of Bologna.
      • Bhangui P.
      • Lim C.
      • Salloum C.
      • Andreani P.
      • Sebbagh M.
      • Hoti E.
      • et al.
      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
      • Tzakis A.G.
      • Kirkegaard P.
      • Pinna A.D.
      • Jovine E.
      • Misiakos E.P.
      • Maziotti A.
      • et al.
      Liver transplantation with cavoportal hemitransposition in the presence of diffuse portal vein thrombosis.
      • Pinna A.D.
      • Nery J.
      • Kato T.
      • Levi D.
      • Nishida S.
      • Tzakis A.G.
      Liver transplant with portocaval hemitransposition: experience at the University of Miami.
      • Selvaggi G.
      • Weppler D.
      • Nishida S.
      • Moon J.
      • Levi D.
      • Kato T.
      • et al.
      Ten-year experience in porto-caval hemitransposition for liver transplantation in the presence of portal vein thrombosis.
      • Olausson M.
      • Norrby J.
      • Mjörnstedt L.
      • Liden H.
      • Friman S.
      Liver transplantation using cavoportal hemitransposition a life-saving procedure in the presence of extensive portal vein thrombosis.
      • Norrby J.
      • Mjörnstedt L.
      • Liden H.
      • Friman S.
      • Olausson M.
      Liver transplantation using cavoportal hemitransposition: a possibility in the presence of extensive portal vein thrombosis.
      • Santaniello W.
      • Ceriello A.
      • Defez M.
      • Maida P.
      • Monti G.N.
      • Sicoli F.
      • et al.
      Liver transplant with cavoportal hemitransposition for portal and mesenteric thrombosis: case report.
      • Weeks S.M.
      • Alexander J.R.
      • Sandhu J.
      • Mauro M.A.
      • Fair J.H.
      • Jaques P.F.
      Mechanic and pharmacologic treatment of a saddle embolus to the portal vein after liver transplantation and portocaval hemitransposition.
      • Shrotri M.
      • Sudhindran S.
      • Gibbs P.
      • Watson C.J.
      • Alexander G.J.
      • Gimson A.E.
      • et al.
      Case report of cavoportal hemitransposition for diffuse portal vein thrombosis in liver transplantation.
      • Gerunda G.E.
      • Merenda R.
      • Neri D.
      • Angeli P.
      • Barbazza F.
      • Valmasoni M.
      • et al.
      Cavoportal hemitransposition: a successful way to overcome the problem of total portosplenomesenteric thrombosis in liver transplantation.
      • Urbani L.
      • Cioni R.
      • Catalano G.
      • Iaria G.
      • Bindi L.
      • Biancofiore G.
      • et al.
      Cavoportal hemitransposition: patient selection criteria and outcome.
      • Varma C.R.
      • Mistry B.M.
      • Glockner J.F.
      • Solomon H.
      • Garvin P.J.
      Cavoportal hemitransposition in liver transplantation.
      • Bakthavatsalam R.
      • Marsh C.L.
      • Perkins J.D.
      • Levy A.E.
      • Healey P.J.
      • Kuhr C.S.
      Rescue of acute portal vein thrombosis after liver transplantation using a cavoportal shunt at retransplantation.
      • Kumar N.
      • Atkison P.
      • Fortier M.V.
      • et al.
      Cavoportal transposition for portal vein thrombosis in a pediatric living-related liver transplantation.
      • Kumar N.
      • Atkison P.
      • Fortier M.V.
      • Grant D.R.
      • Wall W.J.
      Liver transplantation using cavoportal transposition: an effective treatment in patients with complete splanchnic venous thrombosis.
      • Yan M.L.
      • Zeng Y.
      • Li B.
      • Xu M.Q.
      • Wen T.F.
      • Wang W.T.
      • et al.
      Postoperative complications after liver transplantation with cavoportal hemitransposition.
      • Ho M.C.
      • Hu R.H.
      • Lai H.S.
      • Yang P.M.
      • Lai M.Y.
      • Lee P.H.
      Liver transplantation in a patient with diffuse portal venous system thrombosis.
      • Wang C.
      • Zhang T.
      • Song S.
      • Xiu D.
      • Jiang B.
      Liver transplant with portocaval hemitransposition: blood supply with only hepatic artery is possible?.
      • Li F.G.
      • Yan L.N.
      • Wang W.T.
      Extensive thrombosis of the portal vein and vena cava after orthotopic liver transplantation with cavoportal hemitransposition: a case report.
      • Campsen J.
      • Kam I.
      Combined piggyback technique and cavoportal hemitransposition for liver transplant.
      • Shi Z.
      • Yan L.
      • Wen T.
      • Chen Z.
      Cavoportal hemitransposition in an adult-to-adult, living-donor liver transplantation.
      • Srivastava M.
      • Kumaran V.
      • Nundy S.
      • Mehta N.
      Successful living donor liver transplantation with cavoportal hemitransposition in diffuse portomesenteric thrombosis.
      • Gao P.J.
      • Zhu J.Y.
      • Li G.M.
      • Leng X.S.
      Liver transplantation for the patients with end stage liver disease and portal vein thrombosis.
      • Bernardos A.
      • Serrano J.
      • Gomez M.A.
      • Garcia I.
      • Tamayo M.J.
      • Pareja F.
      • et al.
      Portal vein thrombosis: an emergency solution for blood flow in liver transplantation.
      Not all series reported complete information regarding the technique, incidence of complications, morbidity and long-term outcomes following CPA. Among those in which details were available, 46 (68%) procedures were performed with termino-terminal CPA, whereas 22 (32%) were termino-lateral CPA with ligation of the retrohepatic IVC. Eight (12%) patients (among those in whom details were available) were reported to have developed PVT, and 11 (16%) had cavomesenteric thrombosis post-CPA. This high incidence of cavomesenteric and portal thrombosis might be related to slower caval flow entirely directed into the graft. A total of 30–50% of patients have been reported to develop intra-abdominal bleeding after cavoportal hemitransposition. Endoscopic sclerotherapy or band ligation for bleeding oesophageal varices, laparotomy for control of intra-abdominal bleeding, gastric devascularisation, and splenectomy have all been reported for the control of post-CPA bleeding in these patients.
      • Bhangui P.
      • Lim C.
      • Salloum C.
      • Andreani P.
      • Sebbagh M.
      • Hoti E.
      • et al.
      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
      • Lupascu C.
      • Darius T.
      • Goffette P.
      • Lerut J.
      Systemic Venous Inflow to the Liver Allograft to Overcome Diffuse Splanchnic Venous Thrombosis.
      • Lai Q.
      • Spoletini G.
      • Pinheiro R.S.
      • Melandro F.
      • Guglielmo N.
      • Lerut J.
      From portal to splanchnic venous thrombosis: What surgeons should bear in mind.
      Most recipients had ascites after LT (which resolved spontaneously in most). Thirteen patients died during the postoperative period (15%), including 2 of pulmonary embolism, and 48 (63%) were reported to be alive at the last follow-up visit in these series. However, the reported follow-up was short in most series, except for the series by Selvaggi et al.
      • Selvaggi G.
      • Weppler D.
      • Nishida S.
      • Moon J.
      • Levi D.
      • Kato T.
      • et al.
      Ten-year experience in porto-caval hemitransposition for liver transplantation in the presence of portal vein thrombosis.
      (3 days–10 years).
      Cavoportal anastomosis is the reconstruction of choice in case of portocaval shunt that cannot be dismantled.

      Renoportal anastomosis

      We consider that RPA (in the absence of large retroperitoneal or renoportal collaterals) can better ensure portal perfusion at a flow rate matching the portal vein than CPA, while providing optimal coaxiality and congruence of the anastomosed vessels, and preserving retrohepatic IVC flow.
      • Bhangui P.
      • Lim C.
      • Salloum C.
      • Andreani P.
      • Sebbagh M.
      • Hoti E.
      • et al.
      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
      Furthermore, an RPA can obviate or reduce the specific and frequent complications associated with CPA, such as lower torso oedema, pulmonary embolism, and deep vein thrombosis. Due to the so-called siphon effect, it can also be hypothesised that over a period of time, the splanchnic blood flow with high-pressure will be redirected to the low-pressure caval system via the RPA, thus decompressing the portal system and resolving some persistent PHT after this non-physiological establishment of portal flow.
      • Orozco H.
      • Takahashi T.
      • Mercado M.A.
      • Gonzalez-Lopez-Lira A.
      • Hernandez-Ortiz J.
      Intermittent changes in portal venous flow in relation with spleno-pancreatic collaterals–“the pancreatic siphon”–after a selective shunt in a patient with idiopathic portal hypertension: case report.
      • Slater R.R.
      • Jabbour N.
      • Abbass A.A.
      • Patil V.
      • Hundley J.
      • Kazimi M.
      • et al.
      Left renal vein ligation: a technique to mitigate low portal flow from splenic vein siphon during liver transplantation.
      However, the siphon effect, described in selective portacaval shunts, remains to be demonstrated in the LT setting.

      Portal vein arterialisation

      In the setting of PVT, PVA can be utilised in 2 ways: either arterialisation of a portal reconstruction to augment portal vein flow (where native physiological portal vein flow is also present), or arterialisation of the portal vein without any portal flow from the native system (salvage technique in complex PVT). Fourteen cases of salvage PVA have been reported in the literature. Nine of these procedures were performed for primary complex PVT, and 5 were performed for diffuse PVT after LT.
      • Erhard J.
      • Lange R.
      • Giebler R.
      • Rauen U.
      • de Groot H.
      • Eigler F.W.
      Arterialization of the portal vein in orthotopic and auxiliary liver transplantation.
      • Aspinall R.J.
      • Seery J.P.
      • Taylor-Robinson S.D.
      • Habib N.
      Comments on “arterialization of the portal vein in orthotopic and auxiliary liver transplantation”.
      • Neelamekam T.K.
      • Geoghegan J.G.
      • Curry M.
      • Hegarty J.E.
      • Traynor O.
      • McEntee G.P.
      Delayed correction of portal hypertension after portal vein conduit arterialization in liver transplantation.
      • Stange B.
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      PVA actually represents a non-physiological vascular perfusion of the liver, which is deprived of hepatotrophic splanchnic-derived factors. In addition, “over-arterialisation” can result in liver fibrosis and aneurysmal dilatation of intrahepatic portal branches.

      Peri-transplantation medical management of patients with complex PVT

      In the setting of LT in patients with PVT, the following 3 major perioperative questions need to be addressed: i) How to prevent the progression from non-complex to complex PVT? ii) How to treat pre- and (possible) post-LT residual PHT? and, iii) How to prevent inflow thrombosis of the reconstructed portal vein after LT?
      Up to 31% of patients who are found to have PVT at the time of LT, had PVT at the time of initial listing. This underlines the importance of screening for PVT in cirrhotic patients and potential candidates for LT, as well as the importance of administering anticoagulants to prevent progression to complex PVT.
      • Loffredo L.
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      • Farcomeni A.
      • Violi F.
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      The dose of anticoagulants should be modified as the patient moves up the waiting list. In patients in whom anticoagulant use is contraindicated, or PVT progresses while on anticoagulants, a TIPS may be attempted
      • Loffredo L.
      • Pastori D.
      • Farcomeni A.
      • Violi F.
      Effects of anticoagulants in patients with cirrhosis and portal vein thrombosis: a systematic review and meta-analysis.
      • Wang Z.
      • Jiang M.S.
      • Zhang H.L.
      • Weng N.N.
      • Luo X.F.
      • Li X.
      • et al.
      Is post-TIPS anticoagulation therapy necessary in patients with cirrhosis and portal vein thrombosis? A randomized controlled trial.
      • Senzolo M.
      • Tibbals J.
      • Cholongitas E.
      • Triantos C.K.
      • Burroughs A.K.
      • Patch D.
      Transjugular intrahepatic portosystemic shunt for portal vein thrombosis with and without cavernous transformation.
      • Salem R.
      • Vouche M.
      • Baker T.
      • Herrero J.I.
      • Caicedo J.C.
      • Fryer J.
      • et al.
      Pretransplant portal vein recanalization-transjugular intrahepatic portosystemic shunt in patients with complete obliterative portal vein thrombosis.
      with the same objective i.e. to prevent thrombus progression and/or promote recanalisation of the portal vein to allow for standard porto-portal reconstruction at the time of transplant. As proposed in the EASL Clinical Practice Guidelines, TIPS may be considered early in patients with grade 3 (Yerdel) PVT, since it is unlikely that TIPS will be feasible if the PVT progresses to grade 4.
      • European Association for the Study of the Liver
      EASL Clinical Practice Guidelines: Vascular diseases of the liver.
      Notably, in the only relevant series of pre-LT portal vein recanalisation by TIPS, none of the 61 reported patients had complex PVT as defined here.
      • Thornburg B.
      • Desai K.
      • Hickey R.
      • Hohlastos E.
      • Kulik L.
      • Ganger D.
      • et al.
      Pretransplantation Portal Vein Recanalization and Transjugular Intrahepatic Portosystemic Shunt Creation for Chronic Portal Vein Thrombosis: Final Analysis of a 61-Patient Cohort.
      Anticoagulation should be applied after LT to prevent thrombosis of the portal reconstruction.
      In patients with a history of variceal bleeding or in those with grade 3 varices, a protocol of aggressive variceal eradication by endoscopic variceal ligation or sclerotherapy is indicated during the waiting period for LT.
      • Kniepeiss D.
      • Müller H.
      • Wagner D.
      • Iberer F.
      • Tscheliessnigg K.H.
      Management of complications after varicoportal anastomosis in liver transplantation.
      The embolisation of large spontaneous portosystemic shunts for refractory hepatic encephalopathy
      • Laleman W.
      • Simon-Talero M.
      • Maleux G.
      • Perez M.
      • Ameloot K.
      • Soriano G.
      • et al.
      EASL-CLIF-Consortium. Embolization of large spontaneous portosystemic shunts for refractory hepatic encephalopathy: a multicenter survey on safety and efficacy.
      should be avoided in patients listed for transplantation, as such an intervention might take away the last possibility of providing allograft vascularisation as described above. Finally, long-term warfarin treatment has been proposed to prevent post-LT PVT, particularly for patients with non-physiological portal inflow reconstruction, as well as patients with documented hypercoagulable states.
      • Bhangui P.
      • Lim C.
      • Salloum C.
      • Andreani P.
      • Sebbagh M.
      • Hoti E.
      • et al.
      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
      • Hibi T.
      • Nishida S.
      • Levi D.M.
      • Selvaggi G.
      • Tekin A.
      • Fan J.
      • et al.
      When and why portal vein thrombosis matters in liver transplantation: a critical audit of 174 cases.
      Anticoagulation does tend to make follow-up in post-LT patients complex, due to drug-drug interactions (including with immunosuppression) and interference with surgical or endoscopic interventions (if required or during biopsies). Lerut et al.
      • Lerut J.P.
      • Mazza D.
      • van Leeuw V.
      • Laterre P.F.
      • Donataccio M.
      • de Ville de Goyet J.
      • et al.
      Adult liver transplantation and abnormalities of splanchnic veins: experience in 53 patients.
      previously pointed out that anticoagulation may not be necessary in all patients after LT, but probably should be reserved for those patients in whom a complete thrombectomy could not be achieved during LT, or in whom early post-LT PVT develops. In patients with a hypercoagulable state or a metabolic defect, there may not be a need for anticoagulation after LT, as the new liver will immediately correct the situation.

      Discussion

      Based on the available knowledge and our own experience,
      • Bhangui P.
      • Lim C.
      • Salloum C.
      • Andreani P.
      • Sebbagh M.
      • Hoti E.
      • et al.
      Caval inflow to the graft for liver transplantation in patients with diffuse portal vein thrombosis: a 12-year experience.
      • Simón-Talero M.
      • Roccarina D.
      • Martínez J.
      • Lampichler K.
      • Baiges A.
      • Low G.
      • et al.
      Association Between Portosystemic Shunts and Increased Complications and Mortality in Patients With Cirrhosis.
      • Gomez Gavara C.
      • Bhangui P.
      • Salloum C.
      • Osseis M.
      • Esposito F.
      • Moussallem T.
      • et al.
      Ligation versus no ligation of spontaneous portosystemic shunts during liver transplantation: Audit of a prospective series of 66 consecutive patients.
      a new and simple classification system has been proposed which could serve as a guide to multidisciplinary decision-making before and during LT in patients with diffuse PVT, something that is lacking in the existing classification systems. This classification, which is relatively unique because of its incorporation of stage-based management recommendations, dichotomises PVT into non-complex or complex PVT. Further, the portal inflow reconstruction can be classified as physiological or non-physiological, based on whether it addresses the pre-existing prehepatic PHT from a functional/haemodynamic standpoint. The inflow could be considered physiological when the splanchnic blood flow can be redirected to the liver (both in non-complex and complex PVT), and non-physiological if the prehepatic PHT persists even after LT due to the absence of any spontaneous or surgically created portosystemic shunt redirected to the graft. In cases of complex PVT, a large shunt (spontaneous or surgical), if available, could help achieve a physiological portal inflow, thus helping to ameliorate and correct prehepatic PHT in the short/mid-term after LT. An algorithm is proposed for portal inflow reconstruction during LT in patients with PVT (Fig. 5).
      Figure thumbnail gr5
      Fig. 5Proposed algorithm for the management of non-malignant portal vein thrombosis in the setting of liver transplantation.
      While, in some transplant units, LT is contraindicated in patients with complex PVT and no accessible large portosystemic shunt,
      • Golse N.
      • Bucur P.O.
      • Faitot F.
      • Bekheit M.
      • Pittau G.
      • Ciacio O.
      • et al.
      Spontaneous Splenorenal Shunt in Liver Transplantation: Results of Left Renal Vein Ligation Versus Renoportal Anastomosis.
      it would be preferable to resort to non-physiological reconstruction on a case-by-case basis. MVT should be limited to highly specialised units.
      Some areas of uncertainty remain in the field of LT in patients with complex PVT. These include: the unknown proportion of patients with complex PVT excluded from LT at the time of evaluation; the exact influence of complex PVT and/or persistent PHT on short and long-term patient and graft survival after LT
      • Ghabril M.
      • Agarwal S.
      • Lacerda M.
      • Chalasani N.
      • Kwo P.
      • Tector A.J.
      Portal Vein Thrombosis Is a Risk Factor for Poor Early Outcomes After Liver Transplantation: Analysis of Risk Factors and Outcomes for Portal Vein Thrombosis in Waitlisted Patients.
      ; the impact on outcomes of the donor characteristics
      • Stine J.G.
      • Argo C.K.
      • Pelletier S.J.
      • Maluf D.G.
      • Northup P.G.
      Liver transplant recipients with portal vein thrombosis receiving an organ from a high-risk donor are at an increased risk for graft loss due to hepatic artery thrombosis.
      and of the actual portal vein flow.
      • Draoua M.
      • Titze N.
      • Gupta A.
      • Fernandez H.T.
      • Ramsay M.
      • Saracino G.
      • et al.
      Significance of measured intraoperative portal vein flows after thrombendovenectomy in deceased donor liver transplantations with portal vein thrombosis.
      Sufficient long-term results (at 5 years) of LT for complex PVT in large series are awaited to justify the procedure in the ongoing era of worsening organ shortage.
      Another question that arises is whether, given the worse post-transplant outcomes in patients with complex PVT compared to those with less severe PVT (grade 1/2 Yerdel)
      • Zanetto A.
      • Rodriguez-Kastro K.I.
      • Germani G.
      • Ferrarese A.
      • Cillo U.
      • Burra P.
      • et al.
      Mortality in liver transplant recipients with portal vein thrombosis - an updated meta-analysis.
      , the latter patients should be prioritised for liver allocation, before they progress to complex PVT. In their study evaluating a survival benefit based system for allocating deceased-donor livers to chronic liver failure patients, Schaubel et al.
      • Schaubel D.E.
      • Guidinger M.K.
      • Biggins S.W.
      • Kalbfleisch J.D.
      • Pomfret E.A.
      • Sharma P.
      • et al.
      Survival benefit-based deceased-donor liver allocation.
      found that the presence of PVT was one of the major factors that influenced outcomes of LT (hazard ratio 1.32), and should thus be considered when assessing transplant benefit in organ allocation. Some studies have shown that a policy initiative for early access to deceased donor LT in patients with PVT with both, a very low (<12)
      • Englesbe M.J.
      • Schaubel D.E.
      • Cai S.
      • Guidinger M.K.
      • Merion R.M.
      Portal vein thrombosis and liver transplant survival benefit.
      or very high model for end-stage liver disease (MELD) score (>30)
      • Steggerda J.A.
      • Kim I.K.
      • Todo T.
      • Malinoski D.
      • Klein A.S.
      • Bloom M.B.
      Liver Transplant Survival Index for Patients with Model for End-Stage Liver Disease Score ≥ 35: Modeling Risk and Adjusting Expectations in the Share 35 Era.
      may not be appropriate in terms of transplant benefit. However, decompensated cirrhotic patients with PVT may benefit from having an LT before they reach an MELD score of 30.
      • Kaltenborn A.
      • Hartmann C.
      • Salinas R.
      • Ramackers W.
      • Kleine M.
      • Vondran F.W.
      • et al.
      Risk factors for short- and long-term mortality in liver transplant recipients with MELD score ≥30.
      It is well known that higher mortality in high MELD score patients with complex PVT is not related per se to the PVT grade, but more to the degree of sickness, and medical and surgical (more blood loss during transplant) complications that arise as a result.
      In the living donor (LDLT) setting however, the principles may be different. It is of primary importance to respect the risk-benefit equipoise in the LDLT setting – donor safety is of prime importance. However, in experienced centres, where donor morbidity is very low,
      • Moon D.B.
      • Lee S.G.
      • Hwang S.
      • Kim K.H.
      • Ahn C.S.
      • Ha T.Y.
      • et al.
      More than 300 consecutive living donor liver transplants a year at a single center.
      it may be reasonable to consider decompensated cirrhotics with PVT grade 1-3 (Yerdel) for an early LDLT,
      • Moon D.B.
      • Lee S.G.
      • Ahn C.S.
      • Hwang S.
      • Kim K.H.
      • Ha T.Y.
      • et al.
      Section 6. Management of extensive nontumorous portal vein thrombosis in adult living donor liver transplantation.
      because technical issues are known to make LDLT in complex PVT difficult, and outcomes significantly worse.
      • Kadry Z.
      • Selzner N.
      • Handschin A.
      • Müllhaupt B.
      • Renner E.L.
      • Clavien P.A.
      Living donor liver transplantation in patients with portal vein thrombosis: a survey and review of technical issues.
      • Egawa H.
      • Tanaka K.
      • Kasahara M.
      • Takada Y.
      • Oike F.
      • Ogawa K.
      • et al.
      Single center experience of 39 patients with preoperative portal vein thrombosis among 404 adult living donor liver transplantations.
      Overall, the concept of transplant benefit could guide prioritisation of patients with PVT for LT.
      In conclusion, although challenging, good outcomes are possible in patients with complex PVT if the appropriate surgical technique is chosen to ensure portal inflow and resolution of PHT after LT. We believe our proposed classification of PVT in candidates for LT will help clinicians tailor the surgical strategy to an individual patient, in order to provide portal inflow to the graft, together with control of prehepatic PHT whenever feasible. In addition, it could improve teaching and research in the field through comprehensive description for cohort selection and analyses, as well as helping to predict outcomes of LT (especially with respect to vascular complications) in a subset of patients with the most severe forms of PVT.

      Financial support

      The authors received no financial support to produce this manuscript.

      Conflict of interest

      The authors declare no conflicts of interest that pertain to this work.
      Please refer to the accompanying ICMJE disclosure forms for further details.

      Authors’ contributions

      Study concept and design: CL, CS, DA. Acquisition of data; analysis and interpretation of data: PB, CL, CS, EL, DA. Drafting of the manuscript: PB, CL, DA. Critical revision of the manuscript for important intellectual content: CS, ELe, El, CF. Final approval of the manuscript: PB, CL, ELe, CS, EL, CF, DA.

      Supplementary data

      The following are the Supplementary data to this article:

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