Advertisement

Imaging-guided interventions modulating portal venous flow: Evidence and controversies

  • Roberto Cannella
    Affiliations
    Université Paris Cité; AP-HP, Hôpital Beaujon, Service de Radiologie, Clichy; Centre de Recherche sur l'inflammation Inserm, UMR 1149, Paris, France

    Section of Radiology - Department of Biomedicine, Neuroscience and Advanced Diagnostics (BiND), University Hospital “Paolo Giaccone”, Via del Vespro 129, 90127 Palermo, Italy

    Department of Health Promotion Sciences Maternal and Infant Care, Internal Medicine and Medical Specialties, PROMISE, University of Palermo, 90127 Palermo, Italy
    Search for articles by this author
  • Lambros Tselikas
    Affiliations
    Department of Anesthesiology, Surgery and Interventional Radiology, Gustave Roussy, Villejuif, France

    Biotheris, CIC 1428 Inserm, Gustave Roussy, Villejuif, France

    Université Paris – Saclay, Saint Aubin, France
    Search for articles by this author
  • Fréderic Douane
    Affiliations
    Service de Radiologie, CHU Nantes, Nantes, France
    Search for articles by this author
  • François Cauchy
    Affiliations
    Université Paris Cité; AP-HP, Hôpital Beaujon, Service de Chirurgie HBP, Clichy, France
    Search for articles by this author
  • Pierre-Emmanuel Rautou
    Affiliations
    Université Paris Cité, AP-HP, Hôpital Beaujon, Service d'Hépatologie, DMU DIGEST, Centre de Référence des Maladies Vasculaires du Foie, FILFOIE, ERN RARE-LIVER, Centre de Recherche sur l'inflammation Inserm, UMR 1149, Paris, France
    Search for articles by this author
  • Rafael Duran
    Affiliations
    Department of Diagnostic and Interventional Radiology, Centre Hospitalier Universitaire Vaudois (CHUV) and University of Lausanne, Lausanne, Switzerland
    Search for articles by this author
  • Maxime Ronot
    Correspondence
    Corresponding author. Address: Hopital Beaujon, 100 boulevard du Général Leclerc, 92119 Clichy, France; Tel.: +33 1 40 87 55 66, fax: +33 1 40 87 05 48.
    Affiliations
    Université Paris Cité; AP-HP, Hôpital Beaujon, Service de Radiologie, Clichy; Centre de Recherche sur l'inflammation Inserm, UMR 1149, Paris, France
    Search for articles by this author
Open AccessPublished:April 04, 2022DOI:https://doi.org/10.1016/j.jhepr.2022.100484

      Summary

      Portal hypertension is defined by an increase in the portosystemic venous gradient. In most cases, increased resistance to portal blood flow is the initial cause of elevated portal pressure. More than 90% of cases of portal hypertension are estimated to be due to advanced chronic liver disease or cirrhosis. Transjugular intrahepatic portosystemic shunts, a non-pharmacological treatment for portal hypertension, involve the placement of a stent between the portal vein and the hepatic vein or inferior vena cava which helps bypass hepatic resistance. Portal hypertension may also be a result of extrahepatic portal vein thrombosis or compression. In these cases, percutaneous portal vein recanalisation restores portal trunk patency, thus preventing portal hypertension-related complications. Any portal blood flow impairment leads to progressive parenchymal atrophy and triggers hepatic regeneration in preserved areas. This provides the rationale for using portal vein embolisation to modulate hepatic volume in preparation for extended hepatic resection. The aim of this paper is to provide a comprehensive evidence-based review of the rationale for, and outcomes associated with, the main imaging-guided interventions targeting the portal vein, as well as to discuss the main controversies around such approaches.

      Keywords

      Abbreviations:

      ALPPS (associating liver partition and portal vein ligation for staged hepatectomy), BSG (British Society of Gastroenterology), EASL (European Association for the Study of the Liver), FLR (future liver remnant), HE (hepatic encephalopathy), NCBA (N-butyl cyanoacrylate), PH (portal hypertension), PVE (portal vein embolisation), PVR (portal vein recanalisation), RCT (randomised controlled trial), TACE (trans-arterial chemoembolization), TIPS (transjugular intrahepatic portosystemic shunt)
      • There are 3 main clinical indications for TIPS: refractory ascites, secondary prophylaxis of variceal rebleeding in high-risk patients, and uncontrolled variceal haemorrhage.
      • Portal vein recanalisation is performed to treat portal vein thrombosis in liver transplant recipients, and to manage the complications of cavernous transformation, acute thrombosis and portal vein stenosis (due to extrinsic compression or postoperative stenosis).
      • For patients with insufficient future liver remnant, portal vein embolisation can be used to increase the number of candidates amenable to surgical resection and to prevent postoperative complications.
      • Despite progress in the management of patients, controversies remain for several clinical scenarios.
      • Further studies are needed to address specific controversies and to support future evidence-based recommendations.

      Introduction

      The portal vein carries approximately 75% of total liver blood flow, explaining why portal blood flow is so important for sustaining hepatic physiology, or the total volume of functional hepatic parenchyma. Any portal blood flow impairment leads to progressive parenchymal atrophy and triggers a compensatory hepatic regeneration – and therefore volume increase – in preserved areas. This provides a robust rationale for modulating hepatic volume by portal vein occlusion to prepare for extended hepatic resection.
      Portal hypertension (PH) corresponds to an increase in the portosystemic venous gradient as a result of an increase in splanchnic venous pressure.
      • Sanyal A.J.
      • Bosch J.
      • Blei A.
      • Arroyo V.
      Portal hypertension and its complications.
      In most clinical situations, an increase in resistance to portal blood flow – either prehepatic, intrahepatic, or post-hepatic – is the initial cause of elevated portal pressure. More than 90% of PH cases are estimated to be due to advanced chronic liver disease or cirrhosis and the resulting combination of fibrosis deposition, liver parenchymal extinction, and regeneration. When portal pressure is above a certain threshold (>10 mmHg), portosystemic shunts and complications develop, including upper digestive bleeding, ascites, spontaneous bacterial peritonitis, hepatorenal syndrome and hepatic encephalopathy (HE).
      • Garcia-Tsao G.
      • Abraldes J.G.
      • Berzigotti A.
      • Bosch J.
      Portal hypertensive bleeding in cirrhosis: risk stratification, diagnosis, and management: 2016 practice guidance by the American Association for the study of liver diseases.
      Treatment of PH includes a wide spectrum of pharmacological and non-pharmacological options to lower portal pressure. One such option – a so-called transjugular intrahepatic portosystemic shunt (TIPS) – involves the placement of a stent graft in the hepatic parenchyma to create a shunt between the portal vein and the hepatic vein or the inferior vena cava and hence bypass hepatic resistance.
      PH may also be a result of extrahepatic portal vein thrombosis or compression. The development of venous collaterals – e.g. portal cavernous transformation – partially compensates for the decrease in portal blood flow and helps lower splanchnic venous pressure. However, this is usually insufficient over time and patients may experience PH-related complications. The goal of percutaneous portal vein recanalisation (PVR) and stenting is to treat these complications by restoring the patency of the portal venous system.
      The aim of this article is to discuss the 3 main portal vein imaging-guided interventions, namely TIPS, PVR and PVE by providing a comprehensive evidence-based review of the rationale, main technical considerations, evidence of effectiveness and potential complications. The current controversies around these imaging-guided portal venous interventions will also be addressed.

      Transjugular intrahepatic portosystemic shunt

      Rationale and indications

      Careful patient selection is critical before TIPS placement, since the procedure is technically challenging and may result in deterioration of hepatic function and complications in patients with advanced chronic liver disease, which must be considered in relation to the expected clinical benefits of this treatment.
      The American Association for The Study of Liver Disease practice guidelines on the role of TIPS in the management of portal hypertension,
      • Boyer T.D.
      • Haskal Z.J.
      American Association for the Study of Liver Diseases
      The role of Transjugular Intrahepatic Portosystemic Shunt (TIPS) in the management of portal hypertension: update 2009.
      European Association for the Study of Liver (EASL) guidelines for the management of decompensated cirrhosis,
      European Association for the Study of the Liver
      EASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis.
      British Society of Gastroenterology (BSG) TIPS guidelines,
      • Tripathi D.
      • Stanley A.J.
      • Hayes P.C.
      • Travis S.
      • Armstrong M.J.
      • Tsochatzis E.A.
      • et al.
      Transjugular intrahepatic portosystemic stent-shunt in the management of portal hypertension.
      and the Baveno VII consensus update
      • de Franchis R.
      • Bosch J.
      • Garcia-Tsao G.
      • Reiberger T.
      • Ripoll C.
      Baveno VII Faculty
      Baveno VII - renewing consensus in portal hypertension.
      all recommend TIPS as second-line therapy for the complications of PH (Table 1).
      Table 1Indications and contraindications for TIPS according to society guidelines.
      AASLD 2009EASL 2018BSG 2020
      IndicationsEvidence levelIndicationsEvidence/recommendation levelIndicationsEvidence/recommendation level
      Recurrent or refractory ascitesIRecurrent or refractory ascitesI – strong recommendationRecurrent or refracto-ry ascitesHigh evidence, strong recommendation.
      Uncontrolled variceal haemorrhageII-3Hepatic hydrothoraxII-2 – strong recommendationGastro-oesophageal variceal bleeding refractory to endo-scopic and drug therapyModerate evidence, strong recommendation.
      Secondary prevention of variceal haemorrhage after failure of pharmacologic and endoscopic therapyISecondary prophylaxis (early TIPS) of variceal haemorrhage in high-risk patients (Child-Pugh class C with score <14).I – weaker recommendationPre-emptive TIPS (Child-Pugh class C or MELD ≥19)Moderate evidence, weak recommendation.
      Prevention of rebleed-ing from gastric and ectopic varicesII-3Persistent variceal bleeding and early rebleeding (rescue TIPS)I – strong recommendationRebleeding despite optimal therapyLow evidence, strong recommendation.
      Portal hypertension gastropathy with recurrent bleeding despite the use of beta-blockersII-3Portal hypertensive gastropathy, if beta-blockers fail or are not toleratedII-3 – weaker recommendationSecondary prevention of gastric variceal bleedingModerate evidence, weak recommendation.
      Uncontrolled hepatic hydrothoraxII-3Hepatorenal syndromeII-2 – weaker recommendationRefractory bleeding from ectopic varices or portal hypertensive gastropathyLow evidence, weak recommendation.
      Budd-Chiari syndromeII-3Refractory hepatic hydrothoraxModerate evidence, strong recommendation.
      Budd-Chiari syndromeModerate evidence, strong recommendation.
      ContraindicationsContraindicationsContraindications
      Absolute contraindications: primary prevention of variceal bleeding, congestive heart failure, multiple hepatic cysts, uncontrolled systemic infection or sepsis, unrelieved biliary obstruction, severe pulmonary hypertension.

      Relative contraindications: hepa-toma especially if central, obstruction of all hepatic veins, portal vein thrombosis, severe coagulopathy (INR >5), thrombocytopenia of <20,000/cm3, moderate pulmonary hypertension.
      Serum bilirubin >3 mg/dl and a platelet count <75 x109/L, current hepatic encephalopathy grade ≥2 or chronic hepatic encephalopathy, concomitant active infection, progressive renal failure, severe systolic or diastolic dysfunction; pulmonary hypertension.Patients with ascites with bilirubin >50 μm/L and platelets <75×109, pre-existing encephalopathy, active infection, severe cardiac failure or severe pulmonary hypertension; left ventricular dysfunction or severe pulmonary hypertension; significant intrinsic renal disease (stage 4/5).
      Level of evidence: I = randomised controlled trials; II-1 = controlled trials without randomisation; II-2 = controlled trials without randomisation; II-3 = multiple time series, dramatic uncontrolled experiments.
      AASLD, American Association for the Study of Liver Disease; BSG, British Society of Gastroenterology; EASL, European Association for the Study of the Liver; INR, international normalised ratio; MELD, model for end-stage liver disease; TIPS, transjugular intrahepatic portosystemic shunt.
      Refractory ascites is the most common indication for TIPS.
      • Boyer T.D.
      • Haskal Z.J.
      American Association for the Study of Liver Diseases
      The role of Transjugular Intrahepatic Portosystemic Shunt (TIPS) in the management of portal hypertension: update 2009.
      European Association for the Study of the Liver
      EASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis.
      • Tripathi D.
      • Stanley A.J.
      • Hayes P.C.
      • Travis S.
      • Armstrong M.J.
      • Tsochatzis E.A.
      • et al.
      Transjugular intrahepatic portosystemic stent-shunt in the management of portal hypertension.
      • de Franchis R.
      • Bosch J.
      • Garcia-Tsao G.
      • Reiberger T.
      • Ripoll C.
      Baveno VII Faculty
      Baveno VII - renewing consensus in portal hypertension.
      • Biggins S.W.
      • Angeli P.
      • Garcia-Tsao G.
      • Ginès P.
      • Ling S.C.
      • et al.
      Diagnosis, evaluation, and management of ascites, spontaneous bacterial peritonitis and hepatorenal syndrome: 2021 practice guidance by the American Association for the Study of Liver Diseases.
      TIPS is also recommended in patients with variceal bleeding for 3 main reasons: i) rescue therapy (salvage TIPS) in refractory variceal bleeding that does not respond to endoscopic and medical treatment; ii) secondary prevention of rebleeding in high-risk patients after initial endoscopic and pharmacological therapies (pre-emptive TIPS); iii) rebleeding despite optimal secondary prophylaxis.
      • Boyer T.D.
      • Haskal Z.J.
      American Association for the Study of Liver Diseases
      The role of Transjugular Intrahepatic Portosystemic Shunt (TIPS) in the management of portal hypertension: update 2009.
      European Association for the Study of the Liver
      EASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis.
      • Tripathi D.
      • Stanley A.J.
      • Hayes P.C.
      • Travis S.
      • Armstrong M.J.
      • Tsochatzis E.A.
      • et al.
      Transjugular intrahepatic portosystemic stent-shunt in the management of portal hypertension.
      • de Franchis R.
      • Bosch J.
      • Garcia-Tsao G.
      • Reiberger T.
      • Ripoll C.
      Baveno VII Faculty
      Baveno VII - renewing consensus in portal hypertension.
      In particular, pre-emptive TIPS is recommended in patients with Child-Pugh C cirrhosis with a score <14 by EASL guidelines, and Child-Pugh C or model for end-stage liver disease (MELD) score ≥19 by BSG guidelines.
      European Association for the Study of the Liver
      EASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis.
      ,
      • Tripathi D.
      • Stanley A.J.
      • Hayes P.C.
      • Travis S.
      • Armstrong M.J.
      • Tsochatzis E.A.
      • et al.
      Transjugular intrahepatic portosystemic stent-shunt in the management of portal hypertension.
      Furthermore, the Baveno VII consensus on portal hypertension recommend pre-emptive TIPS in patients with Child-Pugh C cirrhosis and a score <14 and or Child-Pugh class B >7 with active bleeding at initial endoscopy or hepatic venous pressure gradient >20 mmHg at the time of haemorrhage.
      • de Franchis R.
      • Bosch J.
      • Garcia-Tsao G.
      • Reiberger T.
      • Ripoll C.
      Baveno VII Faculty
      Baveno VII - renewing consensus in portal hypertension.
      TIPS is currently not recommended for the primary prevention of variceal bleeding since no clinical trials have compared TIPS to other therapies in these patients and because the high rate of HE and known procedural risks could outweigh the risk of variceal haemorrhage in patients without a history of bleeding.
      The indications for TIPS are rapidly being extended to the treatment of symptomatic ectopic varices, hepatic hydrothorax, hepatorenal syndrome, Budd-Chiari syndrome, portal vein thrombosis, and non-cirrhotic PH, although randomised controlled trials (RCTs) are still needed for these indications.
      The contraindications of TIPS are summarised in Table 1. In particular, cardiac dysfunction and severe pulmonary hypertension should be excluded before performing TIPS to avoid cardiac overload from the increase in blood volume in the right atrium.
      • Boyer T.D.
      • Haskal Z.J.
      American Association for the Study of Liver Diseases
      The role of Transjugular Intrahepatic Portosystemic Shunt (TIPS) in the management of portal hypertension: update 2009.
      ,
      • Tripathi D.
      • Stanley A.J.
      • Hayes P.C.
      • Travis S.
      • Armstrong M.J.
      • Tsochatzis E.A.
      • et al.
      Transjugular intrahepatic portosystemic stent-shunt in the management of portal hypertension.
      The patency of the hepatic veins, the inferior vena cava, and the portal vein, as well as anatomical variants, should be evaluated before the procedure, as they are relative contraindications in patients with cirrhosis.

      Technical considerations

      The TIPS procedure is safe when performed by experts. The high reported rate of technical success, which is more than 95%, and the low rate of major intra-procedural complications, correspond to those in experienced tertiary centres.
      • Saad W.E.
      • Darwish W.M.
      • Davies M.G.
      • Kumer S.
      • Anderson C.
      • Waldman D.L.
      • et al.
      Transjugular intrahepatic portosystemic shunts in liver transplant recipients: technical analysis and clinical outcome.
      ,
      • Sarwar A.
      • Zhou L.
      • Novack V.
      • Tapper E.B.
      • Curry M.
      • Malik R.
      • et al.
      Hospital volume and mortality after transjugular intrahepatic portosystemic shunt creation in the United States.
      A detailed description of the TIPS procedure (Fig. 1) has been reported and is not the purpose of this review.
      • Fidelman N.
      • Kwan S.W.
      • LaBerge J.M.
      • Gordon R.L.
      • Ring E.J.
      • Kerlan Jr., R.K.
      The transjugular intrahepatic portosystemic shunt: an update.
      ,
      • Keller F.S.
      • Farsad K.
      • Rösch J.
      The transjugular intrahepatic portosystemic shunt: technique and instruments.
      The exact procedure may vary according to patient characteristics and institutional preferences, with the possibility of using a trans-splenic approach (in patients where the portal vein approach has failed), or a direct intrahepatic portacaval shunt in adjunct or instead of the conventional TIPS technique.
      • Fidelman N.
      • Kwan S.W.
      • LaBerge J.M.
      • Gordon R.L.
      • Ring E.J.
      • Kerlan Jr., R.K.
      The transjugular intrahepatic portosystemic shunt: an update.
      ,
      • Artru F.
      • Moschouri E.
      • Denys A.
      Direct intrahepatic portocaval shunt (DIPS) or transjugular transcaval intrahepatic portosystemic shunt (TTIPS) to treat complications of portal hypertension: indications, technique, and outcomes beyond Budd-Chiari syndrome.
      Initial experiences were also reported with endoscopic puncture of the portal vein for portal venous pressure measurement.
      • Zhang W.
      • Peng C.
      • Zhang S.
      • Huang S.
      • Shen S.
      • Xu G.
      • et al.
      EUS-guided portal pressure gradient measurement in patients with acute or subacute portal hypertension.
      The portosystemic pressure gradient is usually measured before TIPS placement and haemodynamic success is assessed by a reduction in the portosystemic pressure gradient to below 12 mmHg or >20% below baseline.
      • Silva-Junior G.
      • Turon F.
      • Baiges A.
      • Cerda E.
      • García-Criado Á.
      • Blasi A.
      • et al.
      Timing affects measurement of portal pressure gradient after placement of transjugular intrahepatic portosystemic shunts in patients with portal hypertension.
      Different types of stents have been used over time. Expanded polytetrafluoroethylene-covered stents represent the current standard of care and have significantly improved stent patency and lowered the rate of TIPS revisions compared to uncovered stents.
      • Sommer C.M.
      • Gockner T.L.
      • Stampfl U.
      • Bellemann N.
      • Sauer P.
      • Ganten T.
      • et al.
      Technical and clinical outcome of transjugular intrahepatic portosystemic stent shunt: bare metal stents (BMS) versus viatorr stent-grafts (VSG).
      ,
      • Gupta A.C.
      • Wang W.
      • Shah C.
      • Sands M.J.
      • Bullen J.
      • Remer E.M.
      • et al.
      Added value of covered stents in transjugular intrahepatic portosystemic shunt: a large single-center experience.
      Figure thumbnail gr1
      Fig. 161-year-old man with decompensated cirrhosis and refractory ascites undergoing TIPS.
      (A) Angiography shows the middle hepatic vein venogram, (B) catheterisation of the left portal vein, (C) transhepatic portogram with opacification of the associated porto-systemic shunts, (D) insertion of the expandable covered stent graft (Viatorr, Bard), (E) angioplasty of the graft with dilatation at 10 mm, (F) final portogram showing successful TIPS placement. Pre-TIPS portosystemic pressure gradient was 23 mmHg and post-TIPS portosystemic pressure gradient was 5 mmHg. TIPS, transjugular intrahepatic portosystemic shunt.

      Results and evidence

      Most clinical studies and RCTs have focused on 3 main clinical applications of TIPS: refractory ascites, secondary prophylaxis of variceal bleeding, and uncontrolled variceal haemorrhage.

      Ascites

      Recommendations on TIPS for refractory ascites are supported by strong evidence, including 7 prospective RCTs and 7 meta-analyses.
      European Association for the Study of the Liver
      EASL clinical practice guidelines on the management of ascites, spontaneous bacterial peritonitis, and hepatorenal syndrome in cirrhosis.
      ,
      • Madoff D.C.
      • Cornman-Homonoff J.
      • Fortune B.E.
      • Gaba R.C.
      • Lipnik A.J.
      • Yarmohammadi H.
      • et al.
      Management of refractory ascites due to portal hypertension: current status.
      Data consistently report a lower rate of recurrent ascites (42% in the patients treated with TIPS) than in patients managed by repeated large volume paracentesis (89%).
      • Salerno F.
      • Cammà C.
      • Enea M.
      • Rössle M.
      • Wong F.
      Transjugular intrahepatic portosystemic shunt for refractory ascites: a meta-analysis of individual patient data.
      Although large volume paracentesis rapidly relieves abdominal tension, it does not treat the cause, and therefore cannot prevent recurrent ascites, while TIPS lowers elevated sinusoidal pressure, which contributes to the formation of ascites.
      • Madoff D.C.
      • Cornman-Homonoff J.
      • Fortune B.E.
      • Gaba R.C.
      • Lipnik A.J.
      • Yarmohammadi H.
      • et al.
      Management of refractory ascites due to portal hypertension: current status.
      Nevertheless, the improved efficacy of TIPS compared to large volume paracentesis for refractory ascites should be balanced against a higher rate and severity of HE and its possible contraindications in patients with advanced liver disease.
      European Association for the Study of the Liver
      EASL clinical practice guidelines on the management of ascites, spontaneous bacterial peritonitis, and hepatorenal syndrome in cirrhosis.
      Moreover, the real benefit to survival following TIPS for refractory ascites is still a subject of debate and optimal patient selection remains the key to improve survival.
      • Biggins S.W.
      • Angeli P.
      • Garcia-Tsao G.
      • Ginès P.
      • Ling S.C.
      • et al.
      Diagnosis, evaluation, and management of ascites, spontaneous bacterial peritonitis and hepatorenal syndrome: 2021 practice guidance by the American Association for the Study of Liver Diseases.
      Bureau et al. identified platelet count over 75x109/L and bilirubin below 50 μmol/L as predictors of improved survival in patients with refractory ascites treated with TIPS.
      • Bureau C.
      • Métivier S.
      • D'Amico M.
      • Péron J.M.
      • Otal P.
      • Pagan J.C.
      • et al.
      Serum bilirubin and platelet count: a simple predictive model for survival in patients with refractory ascites treated by TIPS.

      Bleeding

      The recommendations for TIPS as salvage therapy in refractory variceal bleeding or in patients with rebleeding have been supported by several prospective studies and meta-analyses.
      • Sauerbruch T.
      • Mengel M.
      • Dollinger M.
      • Zipprich A.
      • Rössle M.
      • Panther E.
      • et al.
      Prevention of rebleeding from esophageal varices in patients with cirrhosis receiving small-diameter stents versus hemodynamically controlled medical therapy.
      ,
      • Holster I.L.
      • Tjwa E.T.
      • Moelker A.
      • Wils A.
      • Hansen B.E.
      • Vermeijden J.R.
      • et al.
      Covered transjugular intrahepatic portosystemic shunt versus endoscopic therapy + β-blocker for prevention of variceal rebleeding.
      In patients with uncontrolled bleeding, the goal of TIPS is to reduce the portosystemic pressure gradient. Several studies have demonstrated the effectiveness of salvage TIPS in patients who do not respond to endoscopic and medical therapies, with a reduction in rebleeding and an improvement in overall survival.
      • Garcia-Tsao G.
      • Abraldes J.G.
      • Berzigotti A.
      • Bosch J.
      Portal hypertensive bleeding in cirrhosis: risk stratification, diagnosis, and management: 2016 practice guidance by the American Association for the study of liver diseases.
      ,
      • Niekamp A.
      • Kuban J.D.
      • Lee S.R.
      • Yevich S.
      • Metwalli Z.
      • McCarthy C.J.
      • et al.
      Transjugular intrahepatic portosystemic shunts reduce variceal bleeding and improve survival in patients with cirrhosis: a population-based analysis.
      Despite successful TIPS placement in controlling bleeding, the survival benefit of salvage TIPS is limited due to the development of complications, with about 13% of patients experiencing early rebleeding
      European Association for the Study of the Liver
      EASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis.
      and 30-day mortality rates as high as 30-44%.
      • Azoulay D.
      • Castaing D.
      • Majno P.
      • Saliba F.
      • Ichaï P.
      • Smail A.
      • et al.
      Salvage transjugular intrahepatic portosystemic shunt for uncontrolled variceal bleeding in patients with decompensated cirrhosis.
      ,
      • Vangeli M.
      • Patch D.
      • Burroughs A.K.
      Salvage tips for uncontrolled variceal bleeding.
      García-Pagán et al.
      • García-Pagán J.C.
      • Caca K.
      • Bureau C.
      • Laleman W.
      • Appenrodt B.
      • Luca A.
      • et al.
      Early use of TIPS in patients with cirrhosis and variceal bleeding.
      published the first multicentre RCT investigating the efficacy of pre-emptive TIPS compared to standard medical and endoscopic therapy. In this study, patients with a high risk of bleeding-related mortality (Child-Pugh C or B with active bleeding at endoscopy) were included. Pre-emptive TIPS was associated with a significant reduction in mortality (1-year survival 86% with early TIPS vs. 61% with standard therapy).
      • García-Pagán J.C.
      • Caca K.
      • Bureau C.
      • Laleman W.
      • Appenrodt B.
      • Luca A.
      • et al.
      Early use of TIPS in patients with cirrhosis and variceal bleeding.
      These results, along with other studies, suggest that pre-emptive TIPS should be considered as a first-line treatment to prevent rebleeding in a specific subset of high-risk patients, although the benefit on overall survival has not yet been demonstrated in patients with advanced cirrhosis.
      • Rudler M.
      • Cluzel P.
      • Corvec T.L.
      • Benosman H.
      • Rousseau G.
      • Poynard T.
      • et al.
      Early-TIPSS placement prevents rebleeding in high-risk patients with variceal bleeding, without improving survival.
      • Bucsics T.
      • Schoder M.
      • Goeschl N.
      • Schwabl P.
      • Mandorfer M.
      • Diermayr M.
      • et al.
      Re-bleeding rates and survival after early transjugular intrahepatic portosystemic shunt (TIPS) in clinical practice.
      • Hernández-Gea V.
      • Procopet B.
      • Giráldez Á.
      • Amitrano L.
      • Villanueva C.
      • Thabut D.
      • et al.
      Preemptive-TIPS improves outcome in high-risk variceal bleeding: an observational study.
      • Dunne P.D.J.
      • Sinha R.
      • Stanley A.J.
      • Lachlan N.
      • Ireland H.
      • Shams A.
      • et al.
      Randomised clinical trial: standard of care versus early-transjugular intrahepatic porto-systemic shunt (TIPSS) in patients with cirrhosis and oesophageal variceal bleeding.
      Acute hepatic decompensation often presents as a result of systemic inflammation.
      • Trebicka J.
      • Fernandez J.
      • Papp M.
      • Caraceni P.
      • Laleman W.
      • Gambino C.
      • et al.
      PREDICT identifies precipitating events associated with the clinical course of acutely decompensated cirrhosis.
      In a large multicentric study, patients with acute-on-chronic liver failure and acute variceal bleeding treated by pre-emptive TIPS had reduced rates of rebleeding and 1-year mortality compared to patients without pre-emptive TIPS.
      • Trebicka J.
      • Gu W.
      • Ibáñez-Samaniego L.
      • Hernández-Gea V.
      • Pitarch C.
      • Garcia E.
      • et al.
      Rebleeding and mortality risk are increased by ACLF but reduced by pre-emptive TIPS.

      Other

      Specific consideration of non-malignant portal vein thrombosis, which is strongly associated with cirrhosis, is important. TIPS can be considered in patients with portal vein thrombosis without recanalisation on anticoagulation or with progressive extension of the thrombosis.
      • de Franchis R.
      • Bosch J.
      • Garcia-Tsao G.
      • Reiberger T.
      • Ripoll C.
      Baveno VII Faculty
      Baveno VII - renewing consensus in portal hypertension.
      Retrospective studies have reported similar technical success and efficacy of TIPS in patients with cirrhosis with and without non-malignant portal vein thrombosis.
      • Luca A.
      • Miraglia R.
      • Caruso S.
      • Milazzo M.
      • Sapere C.
      • Maruzzelli L.
      • et al.
      Short- and long-term effects of the transjugular intrahepatic portosystemic shunt on portal vein thrombosis in patients with cirrhosis.
      • Qi X.
      • He C.
      • Guo W.
      • Yin Z.
      • Wang J.
      • Wang Z.
      • et al.
      Transjugular intrahepatic portosystemic shunt for portal vein thrombosis with variceal bleeding in liver cirrhosis: outcomes and predictors in a prospective cohort study.
      • Lv Y.
      • He C.
      • Wang Z.
      • Guo W.
      • Wang J.
      • Bai W.
      • et al.
      Association of nonmalignant portal vein thrombosis and outcomes after transjugular intrahepatic portosystemic shunt in patients with cirrhosis.
      A large retrospective study found no significant differences in the outcomes of patients with and without pre-existing portal vein thrombosis.
      • Lv Y.
      • He C.
      • Wang Z.
      • Guo W.
      • Wang J.
      • Bai W.
      • et al.
      Association of nonmalignant portal vein thrombosis and outcomes after transjugular intrahepatic portosystemic shunt in patients with cirrhosis.
      Moreover, complete resolution of portal vein thrombosis was observed in 57% of patients, with a low recurrence rate, and a reduction in thrombosis in 30% of cases.
      • Luca A.
      • Miraglia R.
      • Caruso S.
      • Milazzo M.
      • Sapere C.
      • Maruzzelli L.
      • et al.
      Short- and long-term effects of the transjugular intrahepatic portosystemic shunt on portal vein thrombosis in patients with cirrhosis.
      There was no additional benefit to anticoagulation therapies in an RCT after TIPS in patients with portal vein thrombosis.
      • 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.
      Finally, several teams have evaluated the role of TIPS in the prevention of hepatic decompensation following extrahepatic abdominal surgery in patients with cirrhosis, with promising results reported.
      • Fares N.
      • Robic M.A.
      • Péron J.M.
      • Muscari F.
      • Otal P.
      • Suc B.
      • et al.
      Transjugular intrahepatic portosystemic shunt placement before abdominal intervention in cirrhotic patients with portal hypertension: lessons from a pilot study.
      • Lahat E.
      • Lim C.
      • Bhangui P.
      • Fuentes L.
      • Osseis M.
      • Moussallem T.
      • et al.
      Transjugular intrahepatic portosystemic shunt as a bridge to non-hepatic surgery in cirrhotic patients with severe portal hypertension: a systematic review.
      • Tabchouri N.
      • Barbier L.
      • Menahem B.
      • Perarnau J.M.
      • Muscari F.
      • Fares N.
      • et al.
      Original study: transjugular intrahepatic portosystemic shunt as a bridge to abdominal surgery in cirrhotic patients.
      The rationale for preoperative TIPS is to decrease the hepatic venous pressure gradient, which is a known predictor of decompensation after surgery.
      • Reverter E.
      • Cirera I.
      • Albillos A.
      • Debernardi-Venon W.
      • Abraldes J.G.
      • Llop E.
      • et al.
      The prognostic role of hepatic venous pressure gradient in cirrhotic patients undergoing elective extrahepatic surgery.

      Complications and dysfunction

      Major procedure-related complications have been reported to occur in between 4% and 20% of cases.
      • Geeroms B.
      • Laleman W.
      • Laenen A.
      • Heye S.
      • Verslype C.
      • van der Merwe S.
      • et al.
      Expanded polytetrafluoroethylene-covered stent-grafts for transjugular intrahepatic portosystemic shunts in cirrhotic patients: long-term patency and clinical outcome results.
      The most frequent intra-procedural complications include capsular perforation with intraperitoneal haemorrhage, segmental liver ischaemia, hepatic failure, haemobilia, and other biliary complications.
      • Gaba R.C.
      • Khiatani V.L.
      • Knuttinen M.G.
      • Omene B.O.
      • Carrillo T.C.
      • Bui J.T.
      • et al.
      Comprehensive review of TIPS technical complications and how to avoid them.
      The main concerns after TIPS placement are the development of HE, cardiac dysfunction, and early stent dysfunction. HE is the most common complication after TIPS and is the leading cause of early hospital readmission (∼27–48% at 30 days).
      • Vozzo C.F.
      • Singh T.
      • Bullen J.
      • Sarvepalli S.
      • McCullough A.
      • Kapoor B.
      Hospital readmission following transjugular intrahepatic portosystemic shunt: a 14-year single-center experience.
      ,
      • Sarwar A.
      • Weinstein J.L.
      • Novack V.
      • Chakrala N.
      • Tapper E.B.
      • Malik R.
      • et al.
      Causes and rates of 30-day readmissions after transjugular intrahepatic portosystemic shunts.
      New episodes of HE occur in ∼18–40% of patients, while worsening of pre-TIPS HE is reported in ∼50% of patients.
      • Vozzo C.F.
      • Singh T.
      • Bullen J.
      • Sarvepalli S.
      • McCullough A.
      • Kapoor B.
      Hospital readmission following transjugular intrahepatic portosystemic shunt: a 14-year single-center experience.
      • Sarwar A.
      • Weinstein J.L.
      • Novack V.
      • Chakrala N.
      • Tapper E.B.
      • Malik R.
      • et al.
      Causes and rates of 30-day readmissions after transjugular intrahepatic portosystemic shunts.
      • Coronado W.M.
      • Ju C.
      • Bullen J.
      • Kapoor B.
      Predictors of occurrence and risk of hepatic encephalopathy after TIPS creation: a 15-year experience.
      • Khan A.
      • Maheshwari S.
      • Gupta K.
      • Naseem K.
      • Chowdry M.
      • Singh S.
      Rate, reasons, predictors, and burden of readmissions after transjugular intrahepatic portosystemic shunt placement.
      • Bureau C.
      • Thabut D.
      • Jezequel C.
      • Archambeaud I.
      • D'Alteroche L.
      • Dharancy S.
      • et al.
      The use of rifaximin in the prevention of overt hepatic encephalopathy after transjugular intrahepatic portosystemic shunt : a randomized controlled trial.
      Refractory HE can require TIPS reduction or occlusion to control the symptoms of this complication.
      • Pereira K.
      • Carrion A.F.
      • Salsamendi J.
      • Doshi M.
      • Baker R.
      • Kably I.
      Endovascular management of refractory hepatic encephalopathy complication of transjugular intrahepatic portosystemic shunt (TIPS): comprehensive review and clinical practice algorithm.
      Several predictive factors have been associated with the risk and prognosis of HE after TIPS, including a prior history of HE, age, Child-Pugh and MELD scores, the presence of other portosystemic shunts, high portosystemic pressure gradient reduction, and stents without controlled expansion.
      • Coronado W.M.
      • Ju C.
      • Bullen J.
      • Kapoor B.
      Predictors of occurrence and risk of hepatic encephalopathy after TIPS creation: a 15-year experience.
      ,
      • Borentain P.
      • Soussan J.
      • Resseguier N.
      • Botta-Fridlund D.
      • Dufour J.C.
      • Gérolami R.
      • et al.
      The presence of spontaneous portosystemic shunts increases the risk of complications after transjugular intrahepatic portosystemic shunt (TIPS) placement.
      A recent multicentre analysis of 1,871 patients has proposed the FIPS (Freiburg index of post-TIPS survival) score based on age, bilirubin, albumin, and creatinine to predict patients with a worse prognosis after elective TIPS.
      • Bettinger D.
      • Sturm L.
      • Pfaff L.
      • Hahn F.
      • Kloeckner R.
      • Volkwein L.
      • et al.
      Refining prediction of survival after TIPS with the novel Freiburg index of post-TIPS survival.
      A different study identified sarcopenia as an independent predictor of acute-on-chronic liver failure and death after TIPS.
      • Praktiknjo M.
      • Clees C.
      • Pigliacelli A.
      • Fischer S.
      • Jansen C.
      • Lehmann J.
      • et al.
      Sarcopenia is associated with development of acute-on-chronic liver failure in decompensated liver cirrhosis receiving transjugular intrahepatic portosystemic shunt.
      Cardiac dysfunction has been reported in ∼20% of patients after TIPS and was associated with cardiac parameters measured before TIPS.
      • Billey C.
      • Billet S.
      • Robic M.A.
      • Cognet T.
      • Guillaume M.
      • Vinel J.P.
      • et al.
      A prospective study identifying predictive factors of cardiac decompensation after transjugular intrahepatic portosystemic shunt: the toulouse algorithm.
      Stent stenosis or occlusion are the most common cause of TIPS dysfunction, often requiring strict surveillance and leading to a high frequency of revisions. Doppler ultrasound with measurement of flow velocities is the primary method of assessment of TIPS stenosis and occlusion during follow-up. The patency of expanded polytetrafluoroethylene-covered stents is improved and reaches more than 90% at 1 year and 80% at 5 years, thus significantly reducing the need for TIPS revisions.
      • Geeroms B.
      • Laleman W.
      • Laenen A.
      • Heye S.
      • Verslype C.
      • van der Merwe S.
      • et al.
      Expanded polytetrafluoroethylene-covered stent-grafts for transjugular intrahepatic portosystemic shunts in cirrhotic patients: long-term patency and clinical outcome results.
      In a multicentre RCT, the 2-year rate of stent dysfunction was 44% and 63% (p = 0.032) for covered and bare stents, respectively, with no differences in complications or patient survival.
      • Perarnau J.M.
      • Le Gouge A.
      • Nicolas C.
      • d'Alteroche L.
      • Borentain P.
      • Saliba F.
      • et al.
      Covered vs.. uncovered stents for transjugular intrahepatic portosystemic shunt: a randomized controlled trial.

      Controversies

      Bleeding of other porto-systemic shunts (ectopic varices)

      Endoscopic or medical treatment is often ineffective in patients with bleeding ectopic varices.
      • Saad W.E.
      • Lippert A.
      • Saad N.E.
      • Caldwell S.
      Ectopic varices: anatomical classification, hemodynamic classification, and hemodynamic-based management.
      Theoretically, TIPS could be used to reduce portosystemic pressure and the risk of rebleeding. Nevertheless, the value of TIPS in the treatment of ectopic varices is uncertain because rebleeding is frequent despite normalisation of the portosystemic pressure gradient. Moreover, the best available knowledge is based on small observational studies.
      • Vidal V.
      • Joly L.
      • Perreault P.
      • Bouchard L.
      • Lafortune M.
      • Pomier-Layrargues G.
      Usefulness of transjugular intrahepatic portosystemic shunt in the management of bleeding ectopic varices in cirrhotic patients.
      • Vangeli M.
      • Patch D.
      • Terreni N.
      • Tibballs J.
      • Watkinson A.
      • Davies N.
      • et al.
      Bleeding ectopic varices--treatment with transjugular intrahepatic porto-systemic shunt (TIPS) and embolisation.
      • Oey R.C.
      • de Wit K.
      • Moelker A.
      • Atalik T.
      • van Delden O.M.
      • Maleux G.
      • et al.
      Variable efficacy of TIPSS in the management of ectopic variceal bleeding: a multicentre retrospective study.
      • Deipolyi A.R.
      • Kalva S.P.
      • Oklu R.
      • Walker T.G.
      • Wicky S.
      • Ganguli S.
      Reduction in portal venous pressure by transjugular intrahepatic portosystemic shunt for treatment of hemorrhagic stomal varices.
      Despite good technical success (90%), a high early rebleeding rate (42%) was reported in patients without concomitant ectopic variceal embolisation.
      • Vangeli M.
      • Patch D.
      • Terreni N.
      • Tibballs J.
      • Watkinson A.
      • Davies N.
      • et al.
      Bleeding ectopic varices--treatment with transjugular intrahepatic porto-systemic shunt (TIPS) and embolisation.
      A retrospective study in 53 patients with ectopic varices from 3 tertiary centres reported a rebleeding rate of 23% at 1 year and 32% at 5 years after TIPS.
      • Oey R.C.
      • de Wit K.
      • Moelker A.
      • Atalik T.
      • van Delden O.M.
      • Maleux G.
      • et al.
      Variable efficacy of TIPSS in the management of ectopic variceal bleeding: a multicentre retrospective study.
      Deipolyi et al.
      • Deipolyi A.R.
      • Kalva S.P.
      • Oklu R.
      • Walker T.G.
      • Wicky S.
      • Ganguli S.
      Reduction in portal venous pressure by transjugular intrahepatic portosystemic shunt for treatment of hemorrhagic stomal varices.
      described 10 patients with stomal variceal bleeding treated with TIPS (in combination with embolisation in 5) resulting in recurrent bleeding in 4 cases. A meta-analysis in patients with gastric bleeding concluded that TIPS was associated with a lower risk of rebleeding (hazard ratio 0.35; p = 0.004) than endoscopic variceal sclerotherapy.
      • Bai M.
      • Qi X.S.
      • Yang Z.P.
      • Wu K.C.
      • Fan D.M.
      • Han G.H.
      EVS vs. TIPS shunt for gastric variceal bleeding in patients with cirrhosis: a meta-analysis.

      Pre-emptive TIPS in Child-Pugh B patients

      The potential benefits of pre-emptive TIPS are still controversial in Child-Pugh B patients with active bleeding at endoscopy, and other patients who do not meet the high-risk criteria, as survival benefits reported in this subset of patients were not clear.
      • Bucsics T.
      • Schoder M.
      • Goeschl N.
      • Schwabl P.
      • Mandorfer M.
      • Diermayr M.
      • et al.
      Re-bleeding rates and survival after early transjugular intrahepatic portosystemic shunt (TIPS) in clinical practice.
      ,
      • Hernández-Gea V.
      • Procopet B.
      • Giráldez Á.
      • Amitrano L.
      • Villanueva C.
      • Thabut D.
      • et al.
      Preemptive-TIPS improves outcome in high-risk variceal bleeding: an observational study.
      ,
      • Lv Y.
      • Zuo L.
      • Zhu X.
      • Zhao J.
      • Xue H.
      • Jiang Z.
      • et al.
      Identifying optimal candidates for early TIPS among patients with cirrhosis and acute variceal bleeding: a multicentre observational study.
      Although a large observational study
      • Hernández-Gea V.
      • Procopet B.
      • Giráldez Á.
      • Amitrano L.
      • Villanueva C.
      • Thabut D.
      • et al.
      Preemptive-TIPS improves outcome in high-risk variceal bleeding: an observational study.
      reported that pre-emptive TIPS led to no improvement in mortality in Child-Pugh B patients with active bleeding, a recent meta-analysis
      • Nicoară-Farcău O.
      • Han G.
      • Rudler M.
      • Angrisani D.
      • Monescillo A.
      • Torres F.
      • et al.
      Effects of early placement of transjugular portosystemic shunts in patients with high-risk acute variceal bleeding: a meta-analysis of individual patient data.
      comparing individual patient data reported a significant benefit in bleeding control and 1-year survival with pre-emptive TIPS compared to medical and endoscopic therapies in both Child-Pugh C and Child-Pugh B patients with active bleeding. In particular, pre-emptive TIPS significantly improved survival in patients with Child-Pugh B >7, while the prognosis did not change in those with Child-Pugh B7.
      • Nicoară-Farcău O.
      • Han G.
      • Rudler M.
      • Angrisani D.
      • Monescillo A.
      • Torres F.
      • et al.
      Effects of early placement of transjugular portosystemic shunts in patients with high-risk acute variceal bleeding: a meta-analysis of individual patient data.
      Finally, while pre-emptive TIPS has been shown to be effective in selected patients, it is not systemically used in real life practice. Although approximately 35% of patients with variceal bleeding are potentially eligible for pre-emptive TIPS, access to the procedure remains limited to about 7% of patients in referral centres, mainly due to the absence of dedicated interventional radiologists in non-referral institutions.
      • Thabut D.
      • Pauwels A.
      • Carbonell N.
      • Remy A.J.
      • Nahon P.
      • Causse X.
      • et al.
      Cirrhotic patients with portal hypertension-related bleeding and an indication for early-TIPS: a large multicentre audit with real-life results.

      Embolisation of associated varices

      Embolisation of varices has become a treatment option for gastroesophageal varices in patients who are not eligible for TIPS.
      • Kim C.Y.
      • Pinchot J.W.
      • Ahmed O.
      • Braun A.R.
      • Cash B.D.
      • et al.
      Expert Panel on Interventional Radiology
      ACR appropriateness criteria® radiologic management of gastric varices.
      Balloon-occluded retrograde transvenous obliteration has been performed in patients with bleeding from high-flow gastric varices.
      • Liu J.
      • Yang C.
      • Huang S.
      • Zhou C.
      • Shi Q.
      • Qian K.
      • et al.
      The combination of balloon-assisted antegrade transvenous obliteration and transjugular intrahepatic portosystemic shunt for the management of cardiofundal varices hemorrhage.
      The procedure has been associated with a lower rate of rebleeding and HE compared to TIPS for the management of gastric varices.
      • Paleti S.
      • Nutalapati V.
      • Fathallah J.
      • Jeepalyam S.
      • Rustagi T.
      Balloon-occluded retrograde transvenous obliteration (BRTO) versus transjugular intrahepatic portosystemic shunt (TIPS) for treatment of gastric varices because of portal hypertension: a systematic review and meta-analysis.
      The use of concomitant TIPS and embolisation is controversial. On one hand, variceal embolisation could help reduce the risk of rebleeding in patients with TIPS. On the other hand, closing variceal shunts could worsen the portosystemic pressure gradient.
      • Saad W.E.
      Combining transjugular intrahepatic portosystemic shunt with balloon-occluded retrograde transvenous obliteration or augmenting TIPS with variceal embolization for the management of gastric varices: an evolving middle ground?.
      In the absence of clear recommendations, some authors have proposed embolisation if persistent variceal flow is observed on portography after TIPS, but in most cases the decision is made on a case-by-case basis.
      • Saad W.E.
      Combining transjugular intrahepatic portosystemic shunt with balloon-occluded retrograde transvenous obliteration or augmenting TIPS with variceal embolization for the management of gastric varices: an evolving middle ground?.
      • Loffroy R.
      • Favelier S.
      • Pottecher P.
      • Estivalet L.
      • Genson P.Y.
      • Gehin S.
      • et al.
      Transjugular intrahepatic portosystemic shunt for acute variceal gastrointestinal bleeding: indications, techniques and outcomes.
      • Yu J.
      • Wang X.
      • Jiang M.
      • Ma H.
      • Zhou Z.
      • Yang L.
      • et al.
      Comparison of transjugular intrahepatic portosystemic shunt (TIPS) alone and combined with embolisation for the management of cardiofundal varices: a retrospective study.
      In one RCT, Chen et al.
      • Chen S.
      • Li X.
      • Wei B.
      • Tong H.
      • Zhang M.G.
      • Huang Z.Y.
      • et al.
      Recurrent variceal bleeding and shunt patency: prospective randomized controlled trial of transjugular intrahepatic portosystemic shunt alone or combined with coronary vein embolization.
      showed that the 6-month rate of recurrent variceal bleeding was lower in patients with TIPS and concomitant left gastric vein embolisation than with TIPS alone, but cumulative recurrence did not differ at 3 years. A meta-analysis (6 studies, 770 patients) reported that TIPS combined with variceal embolisation led to a significantly lower rebleeding rate, while no differences were observed in the occurrence of HE or shunt dysfunction compared to patients with TIPS alone.
      • Qi X.
      • Liu L.
      • Bai M.
      • Chen H.
      • Wang J.
      • Yang Z.
      • et al.
      Transjugular intrahepatic portosystemic shunt in combination with or without variceal embolization for the prevention of variceal rebleeding: a meta-analysis.
      The benefit of partial splenic embolisation in combination with TIPS remains to be established. While it can reduce the splenic flow and portosystemic gradient, current studies did not report a survival benefit with combined TIPS and splenic embolisation.
      • Kim C.Y.
      • Pinchot J.W.
      • Ahmed O.
      • Braun A.R.
      • Cash B.D.
      • et al.
      Expert Panel on Interventional Radiology
      ACR appropriateness criteria® radiologic management of gastric varices.
      ,
      • Wan Y.M.
      • Li Y.H.
      • Xu Z.Y.
      • Wu H.M.
      • Wu X.N.
      • Xu Y.
      Comparison of TIPS alone and combined with partial splenic embolization (PSE) for the management of variceal bleeding.
      ,
      • Li Y.H.
      • Wu J.F.
      • Wu H.M.
      • Wu X.N.
      • Xu Y.
      • Wan Y.M.
      The effect of transjugular intrahepatic portosystemic shunt plus partial splenic embolization for the treatment of patients with recurrent variceal bleeding.

      Targeted porto-systemic gradient and stent size

      TIPS size and the portosystemic gradient are strongly associated with the control of PH-related complications and the occurrence of post-TIPS HE. A reduction in the portosystemic pressure gradient to <12 mmHg or >20% of the pre-TIPS grade has consistently been shown to be an optimal target value that is associated with a lower risk of rebleeding or ascites. This is consistent with the fact that PH-related complications almost always occur in patients with a portosystemic pressure gradient >12 mmHg following TIPS.
      • Bosch J.
      Small diameter shunts should lead to safe expansion of the use of TIPS.
      However, the optimal endpoint for the portosystemic pressure gradient is still a matter of debate. A reduction of the portosystemic pressure gradient to <10 mmHg has been associated with an increased risk of HE, suggesting that the optimal window for TIPS is narrow (from 10 to 12 mmHg).
      • Bosch J.
      Small diameter shunts should lead to safe expansion of the use of TIPS.
      ,
      • Chung H.H.
      • Razavi M.K.
      • Sze D.Y.
      • Frisoli J.K.
      • Kee S.T.
      • Dake M.D.
      • et al.
      Portosystemic pressure gradient during transjugular intrahepatic portosystemic shunt with Viatorr stent graft: what is the critical low threshold to avoid medically uncontrolled low pressure gradient related complications?.
      The timing of portosystemic pressure measurements is controversial because early measurements performed immediately after TIPS may be affected by haemodynamic conditions and general anaesthesia, and may not be consistent with long-term portosystemic pressure measurements.
      • Silva-Junior G.
      • Turon F.
      • Baiges A.
      • Cerda E.
      • García-Criado Á.
      • Blasi A.
      • et al.
      Timing affects measurement of portal pressure gradient after placement of transjugular intrahepatic portosystemic shunts in patients with portal hypertension.
      Repeated portosystemic pressure measurements should be considered at 24 hours after the procedure to have reliable values that correlate with clinical outcomes.
      • Silva-Junior G.
      • Turon F.
      • Baiges A.
      • Cerda E.
      • García-Criado Á.
      • Blasi A.
      • et al.
      Timing affects measurement of portal pressure gradient after placement of transjugular intrahepatic portosystemic shunts in patients with portal hypertension.
      The results of the use of small-diameter stents (8 mm) to reduce the rate of post-TIPS HE are contradictory. In an RCT by Riggio et al.
      • Riggio O.
      • Ridola L.
      • Angeloni S.
      • Cerini F.
      • Pasquale C.
      • Attili A.F.
      • et al.
      Clinical efficacy of transjugular intrahepatic portosystemic shunt created with covered stents with different diameters: results of a randomized controlled trial.
      8-mm stent TIPS resulted in a significantly higher portosystemic pressure gradient and higher rate of persistent ascites than 10-mm stents, but there were no differences in the occurrence of HE or in survival. These results were similar to those of another study by Miraglia et al.
      • Miraglia R.
      • Maruzzelli L.
      • Tuzzolino F.
      • Petridis I.
      • D'Amico M.
      • Luca A.
      Transjugular intrahepatic portosystemic shunts in patients with cirrhosis with refractory ascites: comparison of clinical outcomes by using 8- and 10-mm PTFE-covered stents.
      that evaluated a larger cohort of patients with refractory ascites. On the other hand, Trebicka et al.
      • Trebicka J.
      • Bastgen D.
      • Byrtus J.
      • Praktiknjo M.
      • Terstiegen S.
      • Meyer C.
      • et al.
      Smaller-diameter covered transjugular intrahepatic portosystemic shunt stents are associated with increased survival.
      found that 8-mm stents were associated with significantly longer survival, while Luo et al.
      • Luo X.
      • Wang X.
      • Zhu Y.
      • Xi X.
      • Zhao Y.
      • Yang J.
      • et al.
      Clinical efficacy of transjugular intrahepatic portosystemic shunt created with expanded polytetrafluoroethylene-covered stent-grafts: 8-mm versus 10-mm.
      reported a lower rate of HE in patients receiving 8-mm stents.
      A recent meta-analysis of 5 studies concluded that patients treated with 8-mm covered stents have a higher 1-year and 3-year overall survival, a lower rate of HE, and no difference in rebleeding rate, compared to those treated with 10-mm stents.
      • Huang Z.
      • Yao Q.
      • Zhu J.
      • He Y.
      • Chen Y.
      • Wu F.
      • et al.
      Efficacy and safety of transjugular intrahepatic portosystemic shunt (TIPS) created using covered stents of different diameters: a systematic review and meta-analysis.
      The study by Praktiknjo et al.
      • Praktiknjo M.
      • Abu-Omar J.
      • Chang J.
      • Thomas D.
      • Jansen C.
      • Kupczyk P.
      • et al.
      Controlled underdilation using novel VIATORR® controlled expansion stents improves survival after transjugular intrahepatic portosystemic shunt implantation.
      reported improved 1-year survival and a reduced rate of shunt-related complications in patients treated with underdilated controlled expansion stent grafts, which maintain a stable 8-mm expansion, compared to underdilated VIATORR® TIPS stent grafts.

      Non-cirrhotic patients

      Despite the absence of cirrhosis or other causes of chronic liver disease, the complications of non-cirrhotic PH are similar, including variceal haemorrhage, ascites, and portal vein thrombosis. The efficacy and safety of TIPS in patients with non-cirrhotic PH is not established, as only a few observational studies have been published to date. In a multicentre study by Bissonnette et al.
      • Bissonnette J.
      • Garcia-Pagán J.C.
      • Albillos A.
      • Turon F.
      • Ferreira C.
      • Tellez L.
      • et al.
      Role of the transjugular intrahepatic portosystemic shunt in the management of severe complications of portal hypertension in idiopathic noncirrhotic portal hypertension.
      including 47 patients with idiopathic non-cirrhotic PH, variceal rebleeding and HE occurred in 28% and 34% of patients after TIPS, respectively. Significant extrahepatic comorbidities and elevated serum creatinine negatively influenced survival (27% mortality after TIPS during follow-up).
      • Bissonnette J.
      • Garcia-Pagán J.C.
      • Albillos A.
      • Turon F.
      • Ferreira C.
      • Tellez L.
      • et al.
      Role of the transjugular intrahepatic portosystemic shunt in the management of severe complications of portal hypertension in idiopathic noncirrhotic portal hypertension.
      The results of TIPS in patients with non-cirrhotic portal cavernous transformation have been reported in a few case series.
      • Luo X.
      • Nie L.
      • Zhou B.
      • Yao D.
      • Ma H.
      • Jiang M.
      • et al.
      Transjugular intrahepatic portosystemic shunt for the treatment of portal hypertension in noncirrhotic patients with portal cavernoma.
      • Fanelli F.
      • Angeloni S.
      • Salvatori F.M.
      • Marzano C.
      • Boatta E.
      • Merli M.
      • et al.
      Transjugular intrahepatic portosystemic shunt with expanded-polytetrafuoroethylene-covered stents in non-cirrhotic patients with portal cavernoma.
      • Qi X.
      • Han G.
      • Yin Z.
      • He C.
      • Wang J.
      • Guo W.
      • et al.
      Transjugular intrahepatic portosystemic shunt for portal cavernoma with symptomatic portal hypertension in non-cirrhotic patients.
      In a study by Fanelli et al. in 13 patients, TIPS implantation was successful in 10 (83%) patients with portal cavernoma without cirrhosis, leading to a significant reduction in the portosystemic pressure gradient.
      • Fanelli F.
      • Angeloni S.
      • Salvatori F.M.
      • Marzano C.
      • Boatta E.
      • Merli M.
      • et al.
      Transjugular intrahepatic portosystemic shunt with expanded-polytetrafuoroethylene-covered stents in non-cirrhotic patients with portal cavernoma.
      However, the success rate of TIPS was only 35% in another series of 20 patients.
      • Qi X.
      • Han G.
      • Yin Z.
      • He C.
      • Wang J.
      • Guo W.
      • et al.
      Transjugular intrahepatic portosystemic shunt for portal cavernoma with symptomatic portal hypertension in non-cirrhotic patients.
      In a recent study on 39 patients with cavernous transformation of the portal vein, symptom improvement was observed in 87% of patients with an overall TIPS patency of 81% at 36 months.
      • Knight G.M.
      • Clark J.
      • Boike J.R.
      • Maddur H.
      • Ganger D.R.
      • Talwar A.
      • et al.
      TIPS for adults without cirrhosis with chronic mesenteric venous thrombosis and EHPVO refractory to standard-of-care therapy.

      Portal vein recanalisation

      Rationale and indications

      Patients with portal vein occlusion or stenosis may develop venous collaterals and be at risk of life-threatening bleeding or ascites due to prehepatic PH. The rationale for PVR is to restore the physiological portal venous flow and to prevent bleeding from ectopic collaterals. The main indications for PVR are portal vein thrombosis in liver transplant recipients, the management of complications of chronic portal vein thrombosis with cavernous transformation (e.g., portal hypertension with bleeding and ascites, cholangiopathy) (Fig. 2) and acute thrombosis (e.g. bowel ischaemia), and portal vein stenosis due to extrinsic compression or postoperative stenosis.
      Figure thumbnail gr2
      Fig. 219-year-old man with chronic portal vein thrombosis and cavernous transformation undergoing portal vein recanalisation.
      (A) Pre-procedural contrast-enhanced CT shows cavernous transformation of the main portal vein. Recanalisation procedure consisting of (B) catheterisation of the segment IV portal vein branch, (C) catheterisation of the portal vein and superior mesenteric vein through the portal cavernoma, (D) stent placement, (E) dilatation of the stent at 10 mm, and (F) final portogram.

      Technical considerations

      Various endovascular approaches have been attempted for PVR, including transhepatic, transjugular intrahepatic, or trans-splenic approaches.
      • Yadav A.
      • Gangwani G.
      • Mishra N.
      • Gupta A.
      Percutaneous transhepatic approach for recanalization of superior mesenteric and portal vein in a patient with pancreatic neuroendocrine tumor presenting with bleeding duodenal varices: a brief case report.
      In patients with portal vein thrombosis, local mechanical thrombectomy combined with pharmacological thrombolysis may be attempted to restore normal blood flow. Mechanical thrombectomy may be performed with balloon angioplasty, device-assisted thrombectomy, or sheath-directed thrombus aspiration.
      • Rodrigues S.G.
      • Maurer M.H.
      • Baumgartner I.
      • De Gottardi A.
      • Berzigotti A.
      Imaging and minimally invasive endovascular therapy in the management of portal vein thrombosis.
      Uncovered self-expandable metallic stents may be used for long-term patency of the portal vein after the procedure, especially in patients with adjacent compressing masses. Overall, the reported technical success is 87–95% in large retrospective series.
      • Marot A.
      • Barbosa J.V.
      • Duran R.
      • Deltenre P.
      • Denys A.
      Percutaneous portal vein recanalization using self-expandable nitinol stents in patients with non-cirrhotic non-tumoral portal vein occlusion.
      ,
      • Kim K.R.
      • Ko G.Y.
      • Sung K.B.
      • Yoon H.K.
      Percutaneous transhepatic stent placement in the management of portal venous stenosis after curative surgery for pancreatic and biliary neoplasms.

      Results and evidence

      Most of the current evidence on PVR is based on case reports or small case series. Oral anticoagulant therapies are the first-line treatment in patients with portal vein thrombosis, while endovascular therapies and PVR may be attempted if medical treatment fails.
      • Valla D.C.
      Recent developments in the field of vascular liver diseases.
      It should be noted that the small number of patients in those retrospective studies and the lack of randomised controls prevent us from drawing strong evidence-based conclusions on the role of PVR.
      In liver transplant recipients complicated by portal vein stenosis, PVR with balloon angioplasty and stent placement has been shown to be an acceptable and safe procedure. A patency rate of 82% and 68% has been reported 5 and 10 years after balloon angioplasty, respectively, with a patency rate of 100% after stent placement in post-transplant portal vein stenosis.
      • Kim K.S.
      • Kim J.M.
      • Lee J.S.
      • Choi G.S.
      • Cho J.W.
      • Lee S.K.
      Stent insertion and balloon angioplasty for portal vein stenosis after liver transplantation: long-term follow-up results.
      Primary stent placement was also shown to have a significantly higher success rate than balloon angioplasty (97–100% vs. 67–69%) in a recent meta-analysis.
      • Sare A.
      • Chandra V.
      • Shanmugasundaram S.
      • Shukla P.A.
      • Kumar A.
      Safety and efficacy of endovascular treatment of portal vein stenosis in liver transplant recipients: a systematic review.
      Clinical improvement was reported in 92% of patients with chronic portal vein thrombosis and cavernous transformation of the portal vein following mechanical thrombectomy combined with pharmacological thrombolysis via an intrahepatic portosystemic approach.
      • Luo J.
      • Yan Z.
      • Wang J.
      • Liu Q.
      • Qu X.
      Endovascular treatment for nonacute symptomatic portal venous thrombosis through intrahepatic portosystemic shunt approach.
      While the recanalisation rate was only 40% in patients with acute portal vein thrombosis, this remains higher than medical therapy alone.
      • Hall T.C.
      • Garcea G.
      • Metcalfe M.
      • Bilku D.
      • Dennison A.R.
      Management of acute non-cirrhotic and non-malignant portal vein thrombosis: a systematic review.
      ,
      • Rössle M.
      • Bettinger D.
      • Trebicka J.
      • Klinger C.
      • Praktiknjo M.
      • Sturm L.
      • et al.
      A prospective, multicentre study in acute non-cirrhotic, non-malignant portal vein thrombosis: comparison of medical and interventional treatment.
      PVR with stent placement has also been used in patients with extrinsic obstruction caused by either inflammatory conditions or malignant tumours.
      • Kim K.R.
      • Ko G.Y.
      • Sung K.B.
      • Yoon H.K.
      Percutaneous transhepatic stent placement in the management of portal venous stenosis after curative surgery for pancreatic and biliary neoplasms.
      ,
      • Woodrum D.A.
      • Bjarnason H.
      • Andrews J.C.
      Portal vein venoplasty and stent placement in the nontransplant population.
      ,
      • Hasegawa T.
      • Yamakado K.
      • Takaki H.
      • Nakatsuka A.
      • Uraki J.
      • Yamanaka T.
      • et al.
      Portal venous stent placement for malignant portal venous stenosis or occlusion: who benefits?.
      Kim et al.
      • Kim K.R.
      • Ko G.Y.
      • Sung K.B.
      • Yoon H.K.
      Percutaneous transhepatic stent placement in the management of portal venous stenosis after curative surgery for pancreatic and biliary neoplasms.
      performed PVR in patients with extrahepatic portal vein obstruction for biliary or pancreatic neoplasms, with a mean patency of 30 and 21 months after stent placement in patients with benign and malignant stenosis, respectively.

      Complications and dysfunction

      The possible complications following PVR include portal vein restenosis and thrombosis. Life-threatening bleeding and other complications such as hepatic abscesses and subcapsular haemorrhage are rare.
      • Luo J.
      • Yan Z.
      • Wang J.
      • Liu Q.
      • Qu X.
      Endovascular treatment for nonacute symptomatic portal venous thrombosis through intrahepatic portosystemic shunt approach.

      Controversies

      Association with TIPS

      The association of TIPS with PVR (PVR-TIPS) is controversial.
      • Thornburg B.
      • Desai K.
      • Hickey R.
      • Kulik L.
      • Ganger D.
      • Baker T.
      • et al.
      Portal vein recanalization and transjugular intrahepatic portosystemic shunt creation for chronic portal vein thrombosis: technical considerations.
      Even though TIPS may not reduce portal pressure in case of prehepatic PH without hepatic alterations, the combination of TIPS and PVR has been proposed to maintain portal vein patency in case of a persistently high portosystemic gradient after recanalisation.
      • Rosenqvist K.
      • Eriksson L.G.
      • Rorsman F.
      • Sangfelt P.
      • Nyman R.
      Endovascular treatment of acute and chronic portal vein thrombosis in patients with cirrhotic and non-cirrhotic liver.
      Currently, there are only a few series on the clinical values of PVR-TIPS.
      • 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.
      ,
      • Barbier C.E.
      • Rorsman F.
      • Eriksson L.G.
      • Sangfelt P.
      • Sheikhi R.
      • Vessby J.
      • et al.
      Placement of a transjugular intrahepatic portosystemic shunt in addition to recanalization of acute and chronic portomesenteric vein occlusions - a retrospective evaluation.
      Barbier et al.
      • Barbier C.E.
      • Rorsman F.
      • Eriksson L.G.
      • Sangfelt P.
      • Sheikhi R.
      • Vessby J.
      • et al.
      Placement of a transjugular intrahepatic portosystemic shunt in addition to recanalization of acute and chronic portomesenteric vein occlusions - a retrospective evaluation.
      have reported a success rate of 85–100% with PVR-TIPS, although several interventions were required in patients with acute thrombosis, and the recurrence rate in patients with chronic thrombosis was 53%. Habib et al.
      • Habib A.
      • Desai K.
      • Hickey R.
      • Thornburg B.
      • Vouche M.
      • Vogelzang R.L.
      • et al.
      Portal vein recanalization-transjugularintrahepatic portosystemic shunt using the transsplenic approach to achieve transplant candidacy in patients with chronic portal vein thrombosis.
      assessed the ability of PVR-TIPS to re-establish portal vein flow in transplant candidates with portal vein thrombosis. Despite the technical success, only 3/11 patients were finally transplanted in that study.
      • Habib A.
      • Desai K.
      • Hickey R.
      • Thornburg B.
      • Vouche M.
      • Vogelzang R.L.
      • et al.
      Portal vein recanalization-transjugularintrahepatic portosystemic shunt using the transsplenic approach to achieve transplant candidacy in patients with chronic portal vein thrombosis.
      In a cohort of 61 liver transplantation candidates, PVR-TIPS patency was 92% at 19 months, recurrent thrombosis only occurred in 8% of patients, but only 39% of patients were finally transplanted.
      • 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.
      Thus, improved survival and the added value of PVR-TIPS compared to other therapies has not been clearly established. Finally, there is no standard portal pressure gradient cut-off for optimal patient selection for the combined PVR-TIPS procedure.

      Portal vein embolisation

      Rationale and indications

      Postoperative liver failure is a severe complication after major hepatectomy and is associated with high morbidity and mortality. Preoperative PVE can be performed as a volume modulation procedure in patients with an insufficient future liver remnant (FLR) both to increase the number of candidates for surgical resection and to prevent postoperative complications. PVE promotes hypertrophy by redirecting portal venous flow to the non-embolised liver, increasing the ratio between the expected FLR and total liver volume. The main clinical indication for PVE is major hepatectomy in patients with malignant liver lesions and insufficient FLR (Fig. 3). PVE is generally indicated when the FLR is ≤20–−25% in a healthy liver, ≤30–35% in patients with chronic liver disease but without cirrhosis (non-alcoholic fatty liver disease, chemotherapy-associated steatohepatitis, cholangitis) or reduced liver function, and ≤40% in cirrhosis or non-alcoholic steatohepatitis.
      • Vauthey J.N.
      • Dixon E.
      • Abdalla E.K.
      • Helton W.S.
      • Pawlik T.M.
      • Taouli B.
      • et al.
      Pretreatment assessment of hepatocellular carcinoma: expert consensus statement.
      Figure thumbnail gr3
      Fig. 366-year-old man with cirrhosis secondary to non-alcoholic fatty liver disease complicated by hepatocellular carcinoma.
      (A) Preoperative contrast-enhanced CT shows a 6 cm hepatocellular carcinoma. The future liver remnant was 27%. (B) Angiography shows right portogram after ipsilateral canalisation of the portal vein. Embolisation was performed with a mixture of N-butyl cyanoacrylate and lipiodol. One small anterior branch was coil embolised to avoid embolisation material migration (C) Cone beam CT angiography after portal vein embolisation shows embolic agents in the right portal vein. (D) Contrast-enhanced CT 6 weeks after portal vein embolisation shows relative hypertrophy of the left liver. The future liver remnant increased to 41%. Patients underwent successful right hepatectomy.

      Technical considerations

      Technical aspects of this procedure have been extensively described in prior studies.
      • Denys A.
      • Prior J.
      • Bize P.
      • Duran R.
      • De Baere T.
      • Halkic N.
      • et al.
      Portal vein embolization: what do we know?.
      ,
      • Downing T.M.
      • Khan S.N.
      • Zvavanjanja R.C.
      • Bhatti Z.
      • Pillai A.K.
      • Kee S.T.
      Portal venous interventions: how to recognize, avoid, or get out of trouble in transjugular intrahepatic portosystemic shunt (TIPS), balloon occlusion sclerosis (ie, BRTO), and portal vein embolization (PVE).
      Overall, the reported technical success has been reported to be between 80–100%.
      • van Lienden K.P.
      • van den Esschert J.W.
      • de Graaf W.
      • Bipat S.
      • Lameris J.S.
      • van Gulik T.M.
      • et al.
      Portal vein embolization before liver resection: a systematic review.
      Briefly, PVE can be performed by a percutaneous transhepatic contralateral approach with ultrasound-guided access to the portal vein via the FLR, a transhepatic ipsilateral approach via the future resected liver, or a trans-ileocolic venous approach.
      • Downing T.M.
      • Khan S.N.
      • Zvavanjanja R.C.
      • Bhatti Z.
      • Pillai A.K.
      • Kee S.T.
      Portal venous interventions: how to recognize, avoid, or get out of trouble in transjugular intrahepatic portosystemic shunt (TIPS), balloon occlusion sclerosis (ie, BRTO), and portal vein embolization (PVE).
      The approach depends on the patients’ anatomy and the radiologist’s preference, and in relation to the possible risks of FLR injury with the contralateral approach. Numerous embolic agents can be used. Their impact on FLR hypertrophy is discussed below.
      Although biliary drainage may be needed in patients with obstructive jaundice and hepatobiliary malignancies requiring preoperative PVE, there are no clear recommendations in the literature supporting routine preoperative biliary drainage in these patients, even in the presence of jaundice. One study has shown that the hypertrophy ratio was significantly higher when selective drainage of the FLR was performed instead of total liver drainage.
      • Ishizawa T.
      • Hasegawa K.
      • Sano K.
      • Imamura H.
      • Kokudo N.
      • Makuuchi M.
      Selective versus total biliary drainage for obstructive jaundice caused by a hepatobiliary malignancy.
      A recent meta-analysis has shown that FLR drainage has now become an accepted practice,
      • Hameed A.
      • Pang T.
      • Chiou J.
      • Pleass H.
      • Lam V.
      • Hollands M.
      • et al.
      Percutaneous vs.. endoscopic pre-operative biliary drainage in hilar cholangiocarcinoma - a systematic review and meta-analysis.
      which makes sense because obstructive jaundice reduces compensatory hypertrophy of the liver. Nevertheless, in patients with FLR drainage and with worsening jaundice or cholangitis, additional drainage of the future resected liver did not decrease FLR ratios or the hypertrophy ratio after PVE.
      • Miura S.
      • Kanno A.
      • Fukase K.
      • Tanaka Y.
      • Matsumoto R.
      • Nabeshima T.
      • et al.
      Preoperative biliary drainage of the hepatic lobe to be resected does not affect liver hypertrophy after percutaneous transhepatic portal vein embolization.

      Results and evidence

      PVE can induce 35–50% FLR hypertrophy, with no difference in the rates of hypertrophy, morbidity or mortality compared to portal vein ligation.
      • Isfordink C.J.
      • Samim M.
      • Braat M.N.G.J.A.
      • Almalki A.M.
      • Hagendoorn J.
      • Borel Rinkes I.H.M.
      • et al.
      Portal vein ligation versus portal vein embolization for induction of hypertrophy of the future liver remnant: a systematic review and meta-analysis.
      PVE is the treatment of choice in patients who do not require 2-stage hepatectomy. However, the rate of FLR hypertrophy is lower than following the associated liver partition and portal vein ligation for staged hepatectomy (ALPPS) procedure (+48–90% between stage 1 & 2).
      • Schnitzbauer A.A.
      • Lang S.A.
      • Goessmann H.
      • Nadalin S.
      • Baumgart J.
      • Farkas S.A.
      • et al.
      Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings.
      • Truant S.
      • Scatton O.
      • Dokmak S.
      • Regimbeau J.M.
      • Lucidi V.
      • Laurent A.
      • et al.
      Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): impact of the inter-stages course on morbi-mortality and implications for management.
      • Buac S.
      • Schadde E.
      • Schnitzbauer A.A.
      • Vogt K.
      • Hernandez-Alejandro R.
      The many faces of ALPPS: surgical indications and techniques among surgeons collaborating in the international registry.
      In the latter, parenchymal transection and hepatic vein ligation further induce FLR hypertrophy.
      • Schnitzbauer A.A.
      • Lang S.A.
      • Goessmann H.
      • Nadalin S.
      • Baumgart J.
      • Farkas S.A.
      • et al.
      Right portal vein ligation combined with in situ splitting induces rapid left lateral liver lobe hypertrophy enabling 2-staged extended right hepatic resection in small-for-size settings.
      • Truant S.
      • Scatton O.
      • Dokmak S.
      • Regimbeau J.M.
      • Lucidi V.
      • Laurent A.
      • et al.
      Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): impact of the inter-stages course on morbi-mortality and implications for management.
      • Buac S.
      • Schadde E.
      • Schnitzbauer A.A.
      • Vogt K.
      • Hernandez-Alejandro R.
      The many faces of ALPPS: surgical indications and techniques among surgeons collaborating in the international registry.
      ALPPS is also associated with a higher rate of completion of second stage hepatectomy than conventional 2-stage hepatectomy with PVE or ligation. However, ALPPS is also clearly associated with significantly higher periprocedural morbidity and mortality.
      • Eshmuminov D.
      • Raptis D.A.
      • Linecker M.
      • Wirsching A.
      • Lesurtel M.
      • Clavien P.A.
      Meta-analysis of associating liver partition with portal vein ligation and portal vein occlusion for two-stage hepatectomy.
      Thus, ALPPS should be considered as an alternative option during the first stage in patients requiring conventional 2-stage hepatectomies with resection in the FLR or in patients requiring 1-stage hepatectomy with insufficient hypertrophy following PVE.
      Curative-intent surgical resection is successful in 67–90% of patients who undergo preoperative PVE.
      • Shindoh J.
      • Tzeng C.W.
      • Aloia T.A.
      • Curley S.A.
      • Huang S.Y.
      • Mahvash A.
      • et al.
      Safety and efficacy of portal vein embolization before planned major or extended hepatectomy: an institutional experience of 358 patients.
      • Glantzounis G.K.
      • Tokidis E.
      • Basourakos S.P.
      • Ntzani E.E.
      • Lianos G.D.
      • Pentheroudakis G.
      The role of portal vein embolization in the surgical management of primary hepatobiliary cancers. A systematic review.
      • Ironside N.
      • Bell R.
      • Bartlett A.
      • McCall J.
      • Powell J.
      • Pandanaboyana S.
      Systematic review of perioperative and survival outcomes of liver resections with and without preoperative portal vein embolization for colorectal metastases.
      • Shindoh J.
      • Tzeng C.W.
      • Aloia T.A.
      • Curley S.A.
      • Zimmitti G.
      • Wei S.H.
      • et al.
      Portal vein embolization improves rate of resection of extensive colorectal liver metastases without worsening survival.
      This is important since patients who undergo preoperative PVE and extended hepatectomy have been shown to have a better prognosis that those who do not undergo curative-intent surgery.
      • Shindoh J.
      • Tzeng C.W.
      • Aloia T.A.
      • Curley S.A.
      • Zimmitti G.
      • Wei S.H.
      • et al.
      Portal vein embolization improves rate of resection of extensive colorectal liver metastases without worsening survival.
      Drop-out is mainly due to tumour progression and not to insufficient FLR hypertrophy.
      PVE can be associated with transarterial therapies (i.e. transarterial chemoembolisation [TACE]) to obtain greater preoperative disease control and lower the risk of tumour progression. While concomitant occlusion of both arterial and portal flow may increase patient morbidity, several retrospective studies have suggested that sequential TACE and PVE may lead to a higher rate of tumour necrosis, increased hypertrophy of FLR, and longer overall survival compared to PVE alone in patients with hepatocellular carcinoma.
      • Glantzounis G.K.
      • Tokidis E.
      • Basourakos S.P.
      • Ntzani E.E.
      • Lianos G.D.
      • Pentheroudakis G.
      The role of portal vein embolization in the surgical management of primary hepatobiliary cancers. A systematic review.
      ,
      • Ogata S.
      • Belghiti J.
      • Farges O.
      • Varma D.
      • Sibert A.
      • Vilgrain V.
      Sequential arterial and portal vein embolizations before right hepatectomy in patients with cirrhosis and hepatocellular carcinoma.
      • Yoo H.
      • Kim J.H.
      • Ko G.Y.
      • Kim K.W.
      • Gwon D.I.
      • Lee S.G.
      • et al.
      Sequential transcatheter arterial chemoembolization and portal vein embolization versus portal vein embolization only before major hepatectomy for patients with hepatocellular carcinoma.
      • Ronot M.
      • Cauchy F.
      • Gregoli B.
      • Breguet R.
      • Allaham W.
      • Paradis V.
      • et al.
      Sequential transarterial chemoembolization and portal vein embolization before resection is a valid oncological strategy for unilobar hepatocellular carcinoma regardless of the tumor burden.
      In a recent study, radioembolisation with Yttrium-90 (when performing radiation lobectomy) has been proposed as an alternative to PVE in patients with hepatocellular carcinoma, resulting in better hypertrophy and tumour control
      • Bekki Y.
      • Marti J.
      • Toshima T.
      • Lewis S.
      • Kamath A.
      • Argiriadi P.
      • et al.
      A comparative study of portal vein embolization versus radiation lobectomy with Yttrium-90 micropheres in preparation for liver resection for initially unresectable hepatocellular carcinoma.
      but not increased resection rates. Furthermore, a case-controlled series showed that radioembolisation induced significantly less FLR hypertrophy than PVE in patients with secondary liver tumours.
      • Garlipp B.
      • de Baere T.
      • Damm R.
      • Irmscher R.
      • van Buskirk M.
      • Stübs P.
      • et al.
      Left-liver hypertrophy after therapeutic right-liver radioembolization is substantial but less than after portal vein embolization.

      Complications

      Severe procedural complications have been reported in 3–16% of patients following PVE.
      • Hameed A.
      • Pang T.
      • Chiou J.
      • Pleass H.
      • Lam V.
      • Hollands M.
      • et al.
      Percutaneous vs.. endoscopic pre-operative biliary drainage in hilar cholangiocarcinoma - a systematic review and meta-analysis.
      ,
      • Shindoh J.
      • Tzeng C.W.
      • Aloia T.A.
      • Curley S.A.
      • Huang S.Y.
      • Mahvash A.
      • et al.
      Safety and efficacy of portal vein embolization before planned major or extended hepatectomy: an institutional experience of 358 patients.
      ,
      • Di Stefano D.R.
      • de Baere T.
      • Denys A.
      • Hakime A.
      • Gorin G.
      • Gillet M.
      • et al.
      Preoperative percutaneous portal vein embolization: evaluation of adverse events in 188 patients.
      ,
      • Yeom Y.K.
      • Shin J.H.
      Complications of portal vein embolization: evaluation on cross-sectional imaging.
      Portal vein thrombosis in the proximal or contralateral portal vein and unwanted embolisation material extending into the FLR portal branches are the most severe complications and can jeopardise FLR hypertrophy.
      • Yeom Y.K.
      • Shin J.H.
      Complications of portal vein embolization: evaluation on cross-sectional imaging.
      Other minor complications include abscesses (especially in the presence of dilated intrahepatic bile ducts), bilomas, haematomas, and hepatic insufficiency.
      • Yeom Y.K.
      • Shin J.H.
      Complications of portal vein embolization: evaluation on cross-sectional imaging.

      Controversies

      Embolisation agents

      There is no consensus on the best embolic agent for FLR hypertrophy. Several embolic agents have been used, including N-butyl cyanoacrylate (NBCA), gelatin sponge, coils, ethanol, nitinol plugs, or a combination of these materials. In clinical practice, the choice of the embolic agent is mainly based on the operators’ experience, availability, and cost. There are very few retrospective comparisons of embolic agents and some results are contradictory.
      • Guiu B.
      • Bize P.
      • Gunthern D.
      • Demartines N.
      • Halkic N.
      • Denys A.
      Portal vein embolization before right hepatectomy: improved results using n-butyl-cyanoacrylate compared to microparticles plus coils.
      ,
      • Dhaliwal S.K.
      • Annamalai G.
      • Gafoor N.
      • Pugash R.
      • Dey C.
      • David E.N.
      Portal vein embolization: correlation of future liver remnant hypertrophy to type of embolic agent used.
      In the study by Jaberi et al.,
      • Jaberi A.
      • Toor S.S.
      • Rajan D.K.
      • Mironov O.
      • Kachura J.R.
      • Cleary S.P.
      • et al.
      Comparison of clinical outcomes following glue versus polyvinyl alcohol portal vein embolization for hypertrophy of the future liver remnant prior to right hepatectomy.
      NBCA combined with an amplatzer vascular plug resulted in a higher rate of FLR hypertrophy than polyvinyl alcohol and coils, although no differences were observed in the surgical outcomes or the rate of complications. In a retrospective analysis, Sugawara et al.
      • Sugawara S.
      • Arai Y.
      • Sone M.
      • Nara S.
      • Kishi Y.
      • Esaki M.
      • et al.
      Retrospective comparative study of absolute ethanol with N-Butyl-2-Cyanoacrylate in percutaneous portal vein embolization.
      reported that PVE with ethanol significantly increased the non-embolised liver volume compared to NBCA, but a recent systematic review concluded that NBCA provided greater FLR hypertrophy, with no difference in the rate of complications.
      • Ali A.
      • Ahle M.
      • Björnsson B.
      • Sandström P.
      Portal vein embolization with N-butyl cyanoacrylate glue is superior to other materials: a systematic review and meta-analysis.
      A recent RCT showed that PVE with NCBA plus iodised oil resulted in faster and greater FLR hypertrophy than PVE with PVA particles plus coils (57% vs. 37% respectively, at 28 days, p <0.001).
      • Luz J.H.M.
      • Veloso Gomes F.
      • Costa N.V.
      • Vasco I.
      • Coimbra E.
      • Luz P.M.
      • et al.
      BestFLR trial: liver regeneration at CT before major hepatectomies for liver cancer-A randomized controlled trial comparing portal vein embolization with N-butyl-cyanoacrylate plus iodized oil versus polyvinyl alcohol particles plus coils.
      However, this was not associated with a significantly higher rate of surgical resection (80% vs. 77%, respectively, p = 0.75) or a statistically significant better postoperative outcome (liver failure in 13% vs. 27%, respectively, p = 0.27).
      • Luz J.H.M.
      • Veloso Gomes F.
      • Costa N.V.
      • Vasco I.
      • Coimbra E.
      • Luz P.M.
      • et al.
      BestFLR trial: liver regeneration at CT before major hepatectomies for liver cancer-A randomized controlled trial comparing portal vein embolization with N-butyl-cyanoacrylate plus iodized oil versus polyvinyl alcohol particles plus coils.

      Factors affecting hepatic regeneration

      Inadequate FLR hypertrophy, which occurs in 10–20% of patients, is a major cause of unresectability after PVE. While hypertrophy occurs at a slower rate in fibrotic or cirrhotic livers, the rate of FLR hypertrophy is not significantly affected by the quality of the hepatic parenchyma. It has been suggested that several factors may hinder hepatic regeneration and FLR hypertrophy.
      • Malinowski M.
      • Stary V.
      • Lock J.F.
      • Schulz A.
      • Jara M.
      • Seehofer D.
      • et al.
      Factors influencing hypertrophy of the left lateral liver lobe after portal vein embolization.
      In particular, the potentially deleterious effect of neoadjuvant chemotherapy on FLR hypertrophy remains unclear.
      • Fischer C.
      • Melstrom L.G.
      • Arnaoutakis D.
      • Jarnagin W.
      • Brown K.
      • D'Angelica M.
      • et al.
      Chemotherapy after portal vein embolization to protect against tumor growth during liver hypertrophy before hepatectomy.
      Since angiogenesis may play a crucial role in hepatic regeneration, the effect of antiangiogenic therapies may play a role. Hypertrophy rates at 4 weeks were comparable in patients who did or did not receive bevacizumab,
      • Zorzi D.
      • Chun Y.S.
      • Madoff D.C.
      • Abdalla E.K.
      • Vauthey J.N.
      Chemotherapy with bevacizumab does not affect liver regeneration after portal vein embolization in the treatment of colorectal liver metastases.
      while another study
      • Aussilhou B.
      • Dokmak S.
      • Faivre S.
      • Paradis V.
      • Vilgrain V.
      • Belghiti J.
      Preoperative liver hypertrophy induced by portal flow occlusion before major hepatic resection for colorectal metastases can be impaired by bevacizumab.
      showed that the rate was lower in patients treated with bevacizumab compared to chemotherapy without bevacizumab.

      Associated hepatic vein embolisation

      Hepatic vein(s) embolisation performed either subsequently or concomitantly (also known as liver venous deprivation, or as simultaneous radiological portohepatic vein embolisation, RASPE) to PVE is another strategy to further increase parenchymal hypertrophy in patients with insufficient FLR.
      • Guiu B.
      • Chevallier P.
      • Denys A.
      • Delhom E.
      • Pierredon-Foulongne M.A.
      • Rouanet P.
      • et al.
      Simultaneous trans-hepatic portal and hepatic vein embolization before major hepatectomy: the liver venous deprivation technique.
      ,
      • Laurent C.
      • Fernandez B.
      • Marichez A.
      • Adam J.P.
      • Papadopoulos P.
      • Lapuyade B.
      • et al.
      Radiological simultaneous portohepatic vein embolization (RASPE) before major hepatectomy: a better way to optimize liver hypertrophy compared to portal vein embolization.
      Retrospective studies have reported that the combined embolisation of the portal and hepatic veins leads to greater hypertrophy compared to PVE alone.
      • Laurent C.
      • Fernandez B.
      • Marichez A.
      • Adam J.P.
      • Papadopoulos P.
      • Lapuyade B.
      • et al.
      Radiological simultaneous portohepatic vein embolization (RASPE) before major hepatectomy: a better way to optimize liver hypertrophy compared to portal vein embolization.
      • Hocquelet A.
      • Sotiriadis C.
      • Duran R.
      • Guiu B.
      • Yamaguchi T.
      • Halkic N.
      • et al.
      Preoperative portal vein embolization alone with biliary drainage compared to a combination of simultaneous portal vein, right hepatic vein embolization and biliary drainage in Klatskin tumor.
      • Kobayashi K.
      • Yamaguchi T.
      • Denys A.
      • Perron L.
      • Halkic N.
      • Demartines N.
      • et al.
      Liver venous deprivation compared to portal vein embolization to induce hypertrophy of the future liver remnant before major hepatectomy: a single center experience.
      • Le Roy B.
      • Gallon A.
      • Cauchy F.
      • Pereira B.
      • Gagnière J.
      • Lambert C.
      • et al.
      Combined biembolization induces higher hypertrophy than portal vein embolization before major liver resection.
      In a meta-analysis by Esposito et al.,
      • Esposito F.
      • Lim C.
      • Lahat E.
      • Shwaartz C.
      • Eshkenazy R.
      • Salloum C.
      • et al.
      Combined hepatic and portal vein embolization as preparation for major hepatectomy: a systematic review.
      the increase in FLR was 33–63% and was significantly higher when hepatic vein embolisation and PVE were performed simultaneously, rather than sequentially (54% vs. 44%, p = 0.008). The added value of embolisation of both the right and middle hepatic veins vs. the right hepatic vein alone in addition to PVE must still be assessed. Substantial hypertrophy of segment IV can be observed when the right hepatic vein is targeted. This could be an obstacle in patients requiring right hepatectomy extended to segment IV. In this setting, embolisation of both the right and middle hepatic veins or just the middle hepatic vein could be considered in association with PVE.
      • Guiu B.
      • Quenet F.
      • Escal L.
      • Bibeau F.
      • Piron L.
      • Rouanet P.
      • et al.
      Extended liver venous deprivation before major hepatectomy induces marked and very rapid increase in future liver remnant function.
      ,
      • Khayat S.
      • Cassese G.
      • Quenet F.
      • Cassinotto C.
      • Assenat E.
      • Navarro F.
      • et al.
      Oncological outcomes after liver venous deprivation for colorectal liver metastases: a single center experience.
      Despite promising results, the results of RCTs are awaited to compare the 2 approaches and the added value of combined embolisation on patient outcome must be evaluated in large cohorts.
      • Deshayes E.
      • Piron L.
      • Bouvier A.
      • Lapuyade B.
      • Lermite E.
      • Vervueren L.
      • et al.
      Study protocol of the HYPER-LIV01 trial: a multicenter phase II, prospective and randomized study comparing simultaneous portal and hepatic vein embolization to portal vein embolization for hypertrophy of the future liver remnant before major hepatectomy for colo-rectal liver metastases.
      In particular, this interventional procedure should also be compared to ALPPS for 2-stage hepatectomy because it could decrease morbidity but achieve similar hypertrophy. Finally, variations in liver function should be assessed, as FLR function can improve more significantly and faster than volume.
      • Piron L.
      • Deshayes E.
      • Cassinotto C.
      • Quenet F.
      • Panaro F.
      • Hermida M.
      • et al.
      Deportalization, venous congestion, venous deprivation: serial measurements of volumes and functions on morphofunctional 99mTc-mebrofenin SPECT-CT.
      ,
      • Guiu B.
      • Quenet F.
      • Panaro F.
      • Piron L.
      • Cassinotto C.
      • Herrerro A.
      • et al.
      Liver venous deprivation versus portal vein embolization before major hepatectomy: future liver remnant volumetric and functional changes.

      Segment IV embolisation

      PVE has been extended to segment IV in patients undergoing right hepatectomy extended to segment IV. The main advantage of this type of PVE is significantly higher hypertrophy of the left lateral segment compared to right PVE alone.
      • Kishi Y.
      • Madoff D.C.
      • Abdalla E.K.
      • Palavecino M.
      • Ribero D.
      • Chun Y.S.
      • et al.
      Is embolization of segment 4 portal veins before extended right hepatectomy justified?.
      ,
      • Björnsson B.
      • Hasselgren K.
      • Røsok B.
      • Larsen P.N.
      • Urdzik J.
      • Schultz N.A.
      • et al.
      Segment 4 occlusion in portal vein embolization increase future liver remnant hypertrophy - a Scandinavian cohort study.
      Segment IV embolisation is technically difficult because of the risk of unwanted reflux of embolic material and of accidental occlusion of the left portal vein branches which could affect FLR hypertrophy. This explains why most segment IV embolisations are performed with coils. There are no studies on differences in the subsequent resection rate in patients undergoing PVE extended to segment IV or not.
      • Kishi Y.
      • Madoff D.C.
      • Abdalla E.K.
      • Palavecino M.
      • Ribero D.
      • Chun Y.S.
      • et al.
      Is embolization of segment 4 portal veins before extended right hepatectomy justified?.
      ,
      • Björnsson B.
      • Hasselgren K.
      • Røsok B.
      • Larsen P.N.
      • Urdzik J.
      • Schultz N.A.
      • et al.
      Segment 4 occlusion in portal vein embolization increase future liver remnant hypertrophy - a Scandinavian cohort study.
      Moreover, improvement in postoperative complications and survival have not been clearly assessed.
      • Ito J.
      • Komada T.
      • Suzuki K.
      • Matsushima M.
      • Nakatochi M.
      • Kobayashi Y.
      • et al.
      Evaluation of segment 4 portal vein embolization added to right portal vein for right hepatic trisectionectomy: a retrospective propensity score-matched study.
      In the study by Hammond et al.,
      • Hammond C.J.
      • Ali S.
      • Haq H.
      • Luo L.
      • Wyatt J.I.
      • Toogood G.J.
      • et al.
      Segment 2/3 hypertrophy is greater when right portal vein embolisation is extended to segment 4 in patients with colorectal liver metastases: a retrospective cohort study.
      post-surgical survival did not differ between patients with and without segment IV-extended PVE.

      Tumour growth induced by PVE

      Tumour progression is a major concern following PVE and it has been reported to be the main cause of dropout (accounting for unresectability in around two-thirds of patients after PVE).
      • Ironside N.
      • Bell R.
      • Bartlett A.
      • McCall J.
      • Powell J.
      • Pandanaboyana S.
      Systematic review of perioperative and survival outcomes of liver resections with and without preoperative portal vein embolization for colorectal metastases.
      ,
      • Alvarez F.A.
      • Castaing D.
      • Figueroa R.
      • Allard M.A.
      • Golse N.
      • Pittau G.
      • et al.
      Natural history of portal vein embolization before liver resection: a 23-year analysis of intention-to-treat results.
      ,
      • Loveday B.P.T.
      • Jaberi A.
      • Moulton C.A.
      • Wei A.C.
      • Gallinger S.
      • Beecroft R.
      • et al.
      Effect of portal vein embolization on treatment plan prior to major hepatectomy for hepatocellular carcinoma.
      The evidence of the effect of PVE on tumour growth is conflicting, and the possible effect on tumours in the embolised and non-embolised livers should be considered separately. Several studies have reported increased tumour growth in the embolised liver and the possible mechanisms for tumour growth are still under investigation.
      • Lim C.
      • Cauchy F.
      • Azoulay D.
      • Farges O.
      • Ronot M.
      • Pocard M.
      Tumour progression and liver regeneration--insights from animal models.
      Simoneau et al.
      • Simoneau E.
      • Aljiffry M.
      • Salman A.
      • Abualhassan N.
      • Cabrera T.
      • Valenti D.
      • et al.
      Portal vein embolization stimulates tumour growth in patients with colorectal cancer liver metastases.
      observed a high rate of tumour progression and increased tumour volume after PVE in 77% of patients with colorectal liver metastases treated with chemotherapy +/- bevacizumab. In patients with hepatocellular carcinoma, Loveday et al.
      • Loveday B.P.T.
      • Jaberi A.
      • Moulton C.A.
      • Wei A.C.
      • Gallinger S.
      • Beecroft R.
      • et al.
      Effect of portal vein embolization on treatment plan prior to major hepatectomy for hepatocellular carcinoma.
      reported an increase in tumour volume in 25 out of 31 patients leading to a change in treatment plan in approximately a quarter of patients. However, the effect of tumour progression after PVE on long-term patient outcome is a subject of debate. In a recent study, disease progression after PVE did not affect long-term overall survival in patients with hepatocellular carcinoma, even though the increase in tumour burden was significantly associated with shorter disease-free survival.
      • Imai K.
      • Yamashita Y.I.
      • Nakao Y.
      • Uemura N.
      • Kitamura F.
      • Miyata T.
      • et al.
      Is disease progression a contraindication for the strategy of portal vein embolization followed by hepatectomy for hepatocellular carcinoma?.
      In colorectal liver metastases, a meta-analysis
      • Giglio M.C.
      • Giakoustidis A.
      • Draz A.
      • Jawad Z.A.R.
      • Pai M.
      • Habib N.A.
      • et al.
      Oncological outcomes of major liver resection following portal vein embolization: a systematic review and meta-analysis.
      concluded that PVE did not negatively affect progression-free survival or overall survival.
      Tumour growth in the non-embolised lobe is more of a concern because it could prevent curative-intent surgery and influence patient prognosis, especially in case of the occurrence of new lesions in the non-embolised liver. In patients with bilobar tumours, retrospective studies showed no differences in the tumour progression rate in embolised and non-embolised livers.
      • Pommier R.
      • Ronot M.
      • Cauchy F.
      • Gaujoux S.
      • Fuks D.
      • Faivre S.
      • et al.
      Colorectal liver metastases growth in the embolized and non-embolized liver after portal vein embolization: influence of initial response to induction chemotherapy.
      ,
      • Spelt L.
      • Sparrelid E.
      • Isaksson B.
      • Andersson R.G.
      • Sturesson C.
      Tumour growth after portal vein embolization with pre-procedural chemotherapy for colorectal liver metastases.
      Studies have addressed the effect of chemotherapy on tumour progression after PVE.
      • Fischer C.
      • Melstrom L.G.
      • Arnaoutakis D.
      • Jarnagin W.
      • Brown K.
      • D'Angelica M.
      • et al.
      Chemotherapy after portal vein embolization to protect against tumor growth during liver hypertrophy before hepatectomy.
      The proportion of hepatic resection after PVE was comparable in patients with and without chemotherapy, but the PVE with chemotherapy group had a lower rate of progression (18.9% vs. 34.2%; p = 0.03) and better 5-year survival (49% vs. 24%; p = 0.006).
      • Fischer C.
      • Melstrom L.G.
      • Arnaoutakis D.
      • Jarnagin W.
      • Brown K.
      • D'Angelica M.
      • et al.
      Chemotherapy after portal vein embolization to protect against tumor growth during liver hypertrophy before hepatectomy.

      Conclusion

      Image-guided interventions involving the portal vein positively influence the management and outcomes of patients with portal hypertension or hepatic tumours. Significant progress has been made, in particular regarding the standardisation of techniques and patient selection. Nevertheless, certain controversies remain and need to be evaluated in further studies.

      Financial support

      The authors received no financial support to produce this manu-script.

      Authors’ contributions

      Conceptualization: LT, RD, MR. Methodology: RC, LT, RD, MR. Supervision: FD, FC, PER, MR. Validation: LT, FD, FC, PER, RD. Writing – original draft: RC. Writing – review & editing: All Authors.

      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.

      Supplementary data

      The following are the supplementary data to this article:

      References

        • Sanyal A.J.
        • Bosch J.
        • Blei A.
        • Arroyo V.
        Portal hypertension and its complications.
        Gastroenterology. 2008; 134: 1715-1728https://doi.org/10.1053/j.gastro.2008.03.007
        • Garcia-Tsao G.
        • Abraldes J.G.
        • Berzigotti A.
        • Bosch J.
        Portal hypertensive bleeding in cirrhosis: risk stratification, diagnosis, and management: 2016 practice guidance by the American Association for the study of liver diseases.
        Hepatology. 2017; 65: 310-335https://doi.org/10.1002/hep.28906
        • Boyer T.D.
        • Haskal Z.J.
        • American Association for the Study of Liver Diseases
        The role of Transjugular Intrahepatic Portosystemic Shunt (TIPS) in the management of portal hypertension: update 2009.
        Hepatology. 2010; 51: 306https://doi.org/10.1002/hep.23383
        • European Association for the Study of the Liver
        EASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis.
        J Hepatol. 2018; 69: 406-460https://doi.org/10.1016/j.jhep.2018.03.024
        • Tripathi D.
        • Stanley A.J.
        • Hayes P.C.
        • Travis S.
        • Armstrong M.J.
        • Tsochatzis E.A.
        • et al.
        Transjugular intrahepatic portosystemic stent-shunt in the management of portal hypertension.
        Gut. 2020; 69: 1173-1192https://doi.org/10.1136/gutjnl-2019-320221
        • de Franchis R.
        • Bosch J.
        • Garcia-Tsao G.
        • Reiberger T.
        • Ripoll C.
        • Baveno VII Faculty
        Baveno VII - renewing consensus in portal hypertension.
        J Hepatol. 2021; https://doi.org/10.1016/j.jhep.2021.12.022
        • Biggins S.W.
        • Angeli P.
        • Garcia-Tsao G.
        • Ginès P.
        • Ling S.C.
        • et al.
        Diagnosis, evaluation, and management of ascites, spontaneous bacterial peritonitis and hepatorenal syndrome: 2021 practice guidance by the American Association for the Study of Liver Diseases.
        Hepatology. 2021; 74: 1014-1048https://doi.org/10.1002/hep.31884
        • Saad W.E.
        • Darwish W.M.
        • Davies M.G.
        • Kumer S.
        • Anderson C.
        • Waldman D.L.
        • et al.
        Transjugular intrahepatic portosystemic shunts in liver transplant recipients: technical analysis and clinical outcome.
        AJR Am J Roentgenol. 2013; 200: 210-218https://doi.org/10.2214/AJR.11.7653
        • Sarwar A.
        • Zhou L.
        • Novack V.
        • Tapper E.B.
        • Curry M.
        • Malik R.
        • et al.
        Hospital volume and mortality after transjugular intrahepatic portosystemic shunt creation in the United States.
        Hepatology. 2018; 67: 690-699https://doi.org/10.1002/hep.29354
        • Fidelman N.
        • Kwan S.W.
        • LaBerge J.M.
        • Gordon R.L.
        • Ring E.J.
        • Kerlan Jr., R.K.
        The transjugular intrahepatic portosystemic shunt: an update.
        AJR Am J Roentgenol. 2012; 199: 746-755https://doi.org/10.2214/AJR.12.9101
        • Keller F.S.
        • Farsad K.
        • Rösch J.
        The transjugular intrahepatic portosystemic shunt: technique and instruments.
        Tech Vasc Interv Radiol. 2016; 19: 2-9https://doi.org/10.1053/j.tvir.2016.01.001
        • Artru F.
        • Moschouri E.
        • Denys A.
        Direct intrahepatic portocaval shunt (DIPS) or transjugular transcaval intrahepatic portosystemic shunt (TTIPS) to treat complications of portal hypertension: indications, technique, and outcomes beyond Budd-Chiari syndrome.
        Clin Res Hepatol Gastroenterol. 2022; : 101858https://doi.org/10.1016/j.clinre.2022.101858
        • Zhang W.
        • Peng C.
        • Zhang S.
        • Huang S.
        • Shen S.
        • Xu G.
        • et al.
        EUS-guided portal pressure gradient measurement in patients with acute or subacute portal hypertension.
        Gastrointest Endosc. 2021; 93: 565-572https://doi.org/10.1016/j.gie.2020.06.065
        • Silva-Junior G.
        • Turon F.
        • Baiges A.
        • Cerda E.
        • García-Criado Á.
        • Blasi A.
        • et al.
        Timing affects measurement of portal pressure gradient after placement of transjugular intrahepatic portosystemic shunts in patients with portal hypertension.
        Gastroenterology. 2017; 152: 1358-1365https://doi.org/10.1053/j.gastro.2017.01.011
        • Sommer C.M.
        • Gockner T.L.
        • Stampfl U.
        • Bellemann N.
        • Sauer P.
        • Ganten T.
        • et al.
        Technical and clinical outcome of transjugular intrahepatic portosystemic stent shunt: bare metal stents (BMS) versus viatorr stent-grafts (VSG).
        Eur J Radiol. 2012; 81: 2273-2280https://doi.org/10.1016/j.ejrad.2011.06.037
        • Gupta A.C.
        • Wang W.
        • Shah C.
        • Sands M.J.
        • Bullen J.
        • Remer E.M.
        • et al.
        Added value of covered stents in transjugular intrahepatic portosystemic shunt: a large single-center experience.
        Cardiovasc Intervent Radiol. 2017; 40: 1723-1731https://doi.org/10.1007/s00270-017-1694-1
        • European Association for the Study of the Liver
        EASL clinical practice guidelines on the management of ascites, spontaneous bacterial peritonitis, and hepatorenal syndrome in cirrhosis.
        J Hepatol. 2010; 53: 397-417https://doi.org/10.1016/j.jhep.2010.05.004
        • Madoff D.C.
        • Cornman-Homonoff J.
        • Fortune B.E.
        • Gaba R.C.
        • Lipnik A.J.
        • Yarmohammadi H.
        • et al.
        Management of refractory ascites due to portal hypertension: current status.
        Radiology. 2021; 298: 493-504https://doi.org/10.1148/radiol.2021201960
        • Salerno F.
        • Cammà C.
        • Enea M.
        • Rössle M.
        • Wong F.
        Transjugular intrahepatic portosystemic shunt for refractory ascites: a meta-analysis of individual patient data.
        Gastroenterology. 2007; 133: 825-834https://doi.org/10.1053/j.gastro.2007.06.020
        • Bureau C.
        • Métivier S.
        • D'Amico M.
        • Péron J.M.
        • Otal P.
        • Pagan J.C.
        • et al.
        Serum bilirubin and platelet count: a simple predictive model for survival in patients with refractory ascites treated by TIPS.
        J Hepatol. 2011; 54: 901-907https://doi.org/10.1016/j.jhep.2010.08.025
        • Sauerbruch T.
        • Mengel M.
        • Dollinger M.
        • Zipprich A.
        • Rössle M.
        • Panther E.
        • et al.
        Prevention of rebleeding from esophageal varices in patients with cirrhosis receiving small-diameter stents versus hemodynamically controlled medical therapy.
        Gastroenterology. 2015; 149: 660-668.e1https://doi.org/10.1053/j.gastro.2015.05.011
        • Holster I.L.
        • Tjwa E.T.
        • Moelker A.
        • Wils A.
        • Hansen B.E.
        • Vermeijden J.R.
        • et al.
        Covered transjugular intrahepatic portosystemic shunt versus endoscopic therapy + β-blocker for prevention of variceal rebleeding.
        Hepatology. 2016; 63: 581-589https://doi.org/10.1002/hep.28318
        • Niekamp A.
        • Kuban J.D.
        • Lee S.R.
        • Yevich S.
        • Metwalli Z.
        • McCarthy C.J.
        • et al.
        Transjugular intrahepatic portosystemic shunts reduce variceal bleeding and improve survival in patients with cirrhosis: a population-based analysis.
        J Vasc Interv Radiol. 2020; 31: 1382-1391.e2https://doi.org/10.1016/j.jvir.2020.06.005
        • Azoulay D.
        • Castaing D.
        • Majno P.
        • Saliba F.
        • Ichaï P.
        • Smail A.
        • et al.
        Salvage transjugular intrahepatic portosystemic shunt for uncontrolled variceal bleeding in patients with decompensated cirrhosis.
        J Hepatol. 2001; 35: 590-597https://doi.org/10.1016/s0168-8278(01)00185-4
        • Vangeli M.
        • Patch D.
        • Burroughs A.K.
        Salvage tips for uncontrolled variceal bleeding.
        J Hepatol. 2002; 37: 703-704https://doi.org/10.1016/s0168-8278(02)00321-5
        • García-Pagán J.C.
        • Caca K.
        • Bureau C.
        • Laleman W.
        • Appenrodt B.
        • Luca A.
        • et al.
        Early use of TIPS in patients with cirrhosis and variceal bleeding.
        N Engl J Med. 2010; 362: 2370-2379https://doi.org/10.1056/NEJMoa0910102
        • Rudler M.
        • Cluzel P.
        • Corvec T.L.
        • Benosman H.
        • Rousseau G.
        • Poynard T.
        • et al.
        Early-TIPSS placement prevents rebleeding in high-risk patients with variceal bleeding, without improving survival.
        Aliment Pharmacol Ther. 2014; 40: 1074-1080https://doi.org/10.1111/apt.12934
        • Bucsics T.
        • Schoder M.
        • Goeschl N.
        • Schwabl P.
        • Mandorfer M.
        • Diermayr M.
        • et al.
        Re-bleeding rates and survival after early transjugular intrahepatic portosystemic shunt (TIPS) in clinical practice.
        Dig Liver Dis. 2017; 49: 1360-1367https://doi.org/10.1016/j.dld.2017.08.002
        • Hernández-Gea V.
        • Procopet B.
        • Giráldez Á.
        • Amitrano L.
        • Villanueva C.
        • Thabut D.
        • et al.
        Preemptive-TIPS improves outcome in high-risk variceal bleeding: an observational study.
        Hepatology. 2019; 69: 282-293https://doi.org/10.1002/hep.30182
        • Dunne P.D.J.
        • Sinha R.
        • Stanley A.J.
        • Lachlan N.
        • Ireland H.
        • Shams A.
        • et al.
        Randomised clinical trial: standard of care versus early-transjugular intrahepatic porto-systemic shunt (TIPSS) in patients with cirrhosis and oesophageal variceal bleeding.
        Aliment Pharmacol Ther. 2020; 52: 98-106https://doi.org/10.1111/apt.15797
        • Trebicka J.
        • Fernandez J.
        • Papp M.
        • Caraceni P.
        • Laleman W.
        • Gambino C.
        • et al.
        PREDICT identifies precipitating events associated with the clinical course of acutely decompensated cirrhosis.
        J Hepatol. 2021; 74: 1097-1108https://doi.org/10.1016/j.jhep.2020.11.019
        • Trebicka J.
        • Gu W.
        • Ibáñez-Samaniego L.
        • Hernández-Gea V.
        • Pitarch C.
        • Garcia E.
        • et al.
        Rebleeding and mortality risk are increased by ACLF but reduced by pre-emptive TIPS.
        J Hepatol. 2020; 73: 1082-1091https://doi.org/10.1016/j.jhep.2020.04.024
        • Luca A.
        • Miraglia R.
        • Caruso S.
        • Milazzo M.
        • Sapere C.
        • Maruzzelli L.
        • et al.
        Short- and long-term effects of the transjugular intrahepatic portosystemic shunt on portal vein thrombosis in patients with cirrhosis.
        Gut. 2011; 60: 846-852https://doi.org/10.1136/gut.2010.228023
        • Qi X.
        • He C.
        • Guo W.
        • Yin Z.
        • Wang J.
        • Wang Z.
        • et al.
        Transjugular intrahepatic portosystemic shunt for portal vein thrombosis with variceal bleeding in liver cirrhosis: outcomes and predictors in a prospective cohort study.
        Liver Int. 2016; 36: 667-676https://doi.org/10.1111/liv.12929
        • Lv Y.
        • He C.
        • Wang Z.
        • Guo W.
        • Wang J.
        • Bai W.
        • et al.
        Association of nonmalignant portal vein thrombosis and outcomes after transjugular intrahepatic portosystemic shunt in patients with cirrhosis.
        Radiology. 2017; 285: 999-1010https://doi.org/10.1148/radiol.2017162266
        • 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.
        Radiology. 2016; 279: 943-951https://doi.org/10.1148/radiol.2015150369
        • Fares N.
        • Robic M.A.
        • Péron J.M.
        • Muscari F.
        • Otal P.
        • Suc B.
        • et al.
        Transjugular intrahepatic portosystemic shunt placement before abdominal intervention in cirrhotic patients with portal hypertension: lessons from a pilot study.
        Eur J Gastroenterol Hepatol. 2018; 30: 21-26https://doi.org/10.1097/MEG.0000000000000990
        • Lahat E.
        • Lim C.
        • Bhangui P.
        • Fuentes L.
        • Osseis M.
        • Moussallem T.
        • et al.
        Transjugular intrahepatic portosystemic shunt as a bridge to non-hepatic surgery in cirrhotic patients with severe portal hypertension: a systematic review.
        HPB (Oxford). 2018; 20: 101-109https://doi.org/10.1016/j.hpb.2017.09.006
        • Tabchouri N.
        • Barbier L.
        • Menahem B.
        • Perarnau J.M.
        • Muscari F.
        • Fares N.
        • et al.
        Original study: transjugular intrahepatic portosystemic shunt as a bridge to abdominal surgery in cirrhotic patients.
        J Gastrointest Surg. 2019; 23: 2383-2390https://doi.org/10.1007/s11605-018-4053-x
        • Reverter E.
        • Cirera I.
        • Albillos A.
        • Debernardi-Venon W.
        • Abraldes J.G.
        • Llop E.
        • et al.
        The prognostic role of hepatic venous pressure gradient in cirrhotic patients undergoing elective extrahepatic surgery.
        J Hepatol. 2019; 71: 942-950https://doi.org/10.1016/j.jhep.2019.07.007
        • Geeroms B.
        • Laleman W.
        • Laenen A.
        • Heye S.
        • Verslype C.
        • van der Merwe S.
        • et al.
        Expanded polytetrafluoroethylene-covered stent-grafts for transjugular intrahepatic portosystemic shunts in cirrhotic patients: long-term patency and clinical outcome results.
        Eur Radiol. 2017; 27: 1795-1803https://doi.org/10.1007/s00330-016-4570-5
        • Gaba R.C.
        • Khiatani V.L.
        • Knuttinen M.G.
        • Omene B.O.
        • Carrillo T.C.
        • Bui J.T.
        • et al.
        Comprehensive review of TIPS technical complications and how to avoid them.
        AJR Am J Roentgenol. 2011; 196: 675-685https://doi.org/10.2214/AJR.10.4819
        • Vozzo C.F.
        • Singh T.
        • Bullen J.
        • Sarvepalli S.
        • McCullough A.
        • Kapoor B.
        Hospital readmission following transjugular intrahepatic portosystemic shunt: a 14-year single-center experience.
        Gastroenterol Rep (Oxf). 2019; 8: 98-103https://doi.org/10.1093/gastro/goz062
        • Sarwar A.
        • Weinstein J.L.
        • Novack V.
        • Chakrala N.
        • Tapper E.B.
        • Malik R.
        • et al.
        Causes and rates of 30-day readmissions after transjugular intrahepatic portosystemic shunts.
        AJR Am J Roentgenol. 2020; 215: 235-241https://doi.org/10.2214/AJR.19.21732
        • Coronado W.M.
        • Ju C.
        • Bullen J.
        • Kapoor B.
        Predictors of occurrence and risk of hepatic encephalopathy after TIPS creation: a 15-year experience.
        Cardiovasc Intervent Radiol. 2020; 43: 1156-1164https://doi.org/10.1007/s00270-020-02512-7
        • Khan A.
        • Maheshwari S.
        • Gupta K.
        • Naseem K.
        • Chowdry M.
        • Singh S.
        Rate, reasons, predictors, and burden of readmissions after transjugular intrahepatic portosystemic shunt placement.
        J Gastroenterol Hepatol. 2021; 36: 775-781https://doi.org/10.1111/jgh.15194
        • Bureau C.
        • Thabut D.
        • Jezequel C.
        • Archambeaud I.
        • D'Alteroche L.
        • Dharancy S.
        • et al.
        The use of rifaximin in the prevention of overt hepatic encephalopathy after transjugular intrahepatic portosystemic shunt : a randomized controlled trial.
        Ann Intern Med. 2021; 174: 633-640https://doi.org/10.7326/M20-0202
        • Pereira K.
        • Carrion A.F.
        • Salsamendi J.
        • Doshi M.
        • Baker R.
        • Kably I.
        Endovascular management of refractory hepatic encephalopathy complication of transjugular intrahepatic portosystemic shunt (TIPS): comprehensive review and clinical practice algorithm.
        Cardiovasc Intervent Radiol. 2016; 39: 170-182https://doi.org/10.1007/s00270-015-1197-x
        • Borentain P.
        • Soussan J.
        • Resseguier N.
        • Botta-Fridlund D.
        • Dufour J.C.
        • Gérolami R.
        • et al.
        The presence of spontaneous portosystemic shunts increases the risk of complications after transjugular intrahepatic portosystemic shunt (TIPS) placement.
        Diagn Interv Imaging. 2016; 97: 643-650https://doi.org/10.1016/j.diii.2016.02.004
        • Bettinger D.
        • Sturm L.
        • Pfaff L.
        • Hahn F.
        • Kloeckner R.
        • Volkwein L.
        • et al.
        Refining prediction of survival after TIPS with the novel Freiburg index of post-TIPS survival.
        J Hepatol. 2021; 74: 1362-1372https://doi.org/10.1016/j.jhep.2021.01.023
        • Praktiknjo M.
        • Clees C.
        • Pigliacelli A.
        • Fischer S.
        • Jansen C.
        • Lehmann J.
        • et al.
        Sarcopenia is associated with development of acute-on-chronic liver failure in decompensated liver cirrhosis receiving transjugular intrahepatic portosystemic shunt.
        Clin Transl Gastroenterol. 2019; 10e00025https://doi.org/10.14309/ctg.0000000000000025
        • Billey C.
        • Billet S.
        • Robic M.A.
        • Cognet T.
        • Guillaume M.
        • Vinel J.P.
        • et al.
        A prospective study identifying predictive factors of cardiac decompensation after transjugular intrahepatic portosystemic shunt: the toulouse algorithm.
        Hepatology. 2019; 70: 1928-1941https://doi.org/10.1002/hep.30934
        • Perarnau J.M.
        • Le Gouge A.
        • Nicolas C.
        • d'Alteroche L.
        • Borentain P.
        • Saliba F.
        • et al.
        Covered vs.. uncovered stents for transjugular intrahepatic portosystemic shunt: a randomized controlled trial.
        J Hepatol. 2014; 60: 962-968https://doi.org/10.1016/j.jhep.2014.01.015
        • Saad W.E.
        • Lippert A.
        • Saad N.E.
        • Caldwell S.
        Ectopic varices: anatomical classification, hemodynamic classification, and hemodynamic-based management.
        Tech Vasc Interv Radiol. 2013; 16: 158-175https://doi.org/10.1053/j.tvir.2013.02.004
        • Vidal V.
        • Joly L.
        • Perreault P.
        • Bouchard L.
        • Lafortune M.
        • Pomier-Layrargues G.
        Usefulness of transjugular intrahepatic portosystemic shunt in the management of bleeding ectopic varices in cirrhotic patients.
        Cardiovasc Intervent Radiol. 2006; 29: 216-219https://doi.org/10.1007/s00270-004-0346-4
        • Vangeli M.
        • Patch D.
        • Terreni N.
        • Tibballs J.
        • Watkinson A.
        • Davies N.
        • et al.
        Bleeding ectopic varices--treatment with transjugular intrahepatic porto-systemic shunt (TIPS) and embolisation.
        J Hepatol. 2004; 41: 560-566https://doi.org/10.1016/j.jhep.2004.06.024
        • Oey R.C.
        • de Wit K.
        • Moelker A.
        • Atalik T.
        • van Delden O.M.
        • Maleux G.
        • et al.
        Variable efficacy of TIPSS in the management of ectopic variceal bleeding: a multicentre retrospective study.
        Aliment Pharmacol Ther. 2018; 48: 975-983https://doi.org/10.1111/apt.14947
        • Deipolyi A.R.
        • Kalva S.P.
        • Oklu R.
        • Walker T.G.
        • Wicky S.
        • Ganguli S.
        Reduction in portal venous pressure by transjugular intrahepatic portosystemic shunt for treatment of hemorrhagic stomal varices.
        AJR Am J Roentgenol. 2014; 203: 668-673https://doi.org/10.2214/AJR.13.12211
        • Bai M.
        • Qi X.S.
        • Yang Z.P.
        • Wu K.C.
        • Fan D.M.
        • Han G.H.
        EVS vs. TIPS shunt for gastric variceal bleeding in patients with cirrhosis: a meta-analysis.
        World J Gastrointest Pharmacol Ther. 2014; 5: 97-104https://doi.org/10.4292/wjgpt.v5.i2.97
        • Lv Y.
        • Zuo L.
        • Zhu X.
        • Zhao J.
        • Xue H.
        • Jiang Z.
        • et al.
        Identifying optimal candidates for early TIPS among patients with cirrhosis and acute variceal bleeding: a multicentre observational study.
        Gut. 2019; 68: 1297-1310https://doi.org/10.1136/gutjnl-2018-317057
        • Nicoară-Farcău O.
        • Han G.
        • Rudler M.
        • Angrisani D.
        • Monescillo A.
        • Torres F.
        • et al.
        Effects of early placement of transjugular portosystemic shunts in patients with high-risk acute variceal bleeding: a meta-analysis of individual patient data.
        Gastroenterology. 2021; 160: 193-205.e10https://doi.org/10.1053/j.gastro.2020.09.026
        • Thabut D.
        • Pauwels A.
        • Carbonell N.
        • Remy A.J.
        • Nahon P.
        • Causse X.
        • et al.
        Cirrhotic patients with portal hypertension-related bleeding and an indication for early-TIPS: a large multicentre audit with real-life results.
        J Hepatol. 2017; 68: 73-81https://doi.org/10.1016/j.jhep.2017.09.002
        • Kim C.Y.
        • Pinchot J.W.
        • Ahmed O.
        • Braun A.R.
        • Cash B.D.
        • et al.
        • Expert Panel on Interventional Radiology
        ACR appropriateness criteria® radiologic management of gastric varices.
        J Am Coll Radiol. 2020; 17: S239-S254https://doi.org/10.1016/j.jacr.2020.01.017
        • Liu J.
        • Yang C.
        • Huang S.
        • Zhou C.
        • Shi Q.
        • Qian K.
        • et al.
        The combination of balloon-assisted antegrade transvenous obliteration and transjugular intrahepatic portosystemic shunt for the management of cardiofundal varices hemorrhage.
        Eur J Gastroenterol Hepatol. 2020; 32: 656-662https://doi.org/10.1097/MEG.0000000000001705
        • Paleti S.
        • Nutalapati V.
        • Fathallah J.
        • Jeepalyam S.
        • Rustagi T.
        Balloon-occluded retrograde transvenous obliteration (BRTO) versus transjugular intrahepatic portosystemic shunt (TIPS) for treatment of gastric varices because of portal hypertension: a systematic review and meta-analysis.
        J Clin Gastroenterol. 2020; 54: 655-660https://doi.org/10.1097/MCG.0000000000001275
        • Saad W.E.
        Combining transjugular intrahepatic portosystemic shunt with balloon-occluded retrograde transvenous obliteration or augmenting TIPS with variceal embolization for the management of gastric varices: an evolving middle ground?.
        Semin Intervent Radiol. 2014; 31: 266-268https://doi.org/10.1055/s-0034-1382796
        • Loffroy R.
        • Favelier S.
        • Pottecher P.
        • Estivalet L.
        • Genson P.Y.
        • Gehin S.
        • et al.
        Transjugular intrahepatic portosystemic shunt for acute variceal gastrointestinal bleeding: indications, techniques and outcomes.
        Diagn Interv Imaging. 2015; 96: 745-755https://doi.org/10.1016/j.diii.2015.05.005
        • Yu J.
        • Wang X.
        • Jiang M.
        • Ma H.
        • Zhou Z.
        • Yang L.
        • et al.
        Comparison of transjugular intrahepatic portosystemic shunt (TIPS) alone and combined with embolisation for the management of cardiofundal varices: a retrospective study.
        Eur Radiol. 2019; 29: 699-706https://doi.org/10.1007/s00330-018-5645-2
        • Chen S.
        • Li X.
        • Wei B.
        • Tong H.
        • Zhang M.G.
        • Huang Z.Y.
        • et al.
        Recurrent variceal bleeding and shunt patency: prospective randomized controlled trial of transjugular intrahepatic portosystemic shunt alone or combined with coronary vein embolization.
        Radiology. 2013; 268: 900-906https://doi.org/10.1148/radiol.13120800
        • Qi X.
        • Liu L.
        • Bai M.
        • Chen H.
        • Wang J.
        • Yang Z.
        • et al.
        Transjugular intrahepatic portosystemic shunt in combination with or without variceal embolization for the prevention of variceal rebleeding: a meta-analysis.
        J Gastroenterol Hepatol. 2014; 29: 688-696https://doi.org/10.1111/jgh.12391
        • Wan Y.M.
        • Li Y.H.
        • Xu Z.Y.
        • Wu H.M.
        • Wu X.N.
        • Xu Y.
        Comparison of TIPS alone and combined with partial splenic embolization (PSE) for the management of variceal bleeding.
        Eur Radiol. 2019; 29: 5032-5041https://doi.org/10.1007/s00330-019-06046-6
        • Li Y.H.
        • Wu J.F.
        • Wu H.M.
        • Wu X.N.
        • Xu Y.
        • Wan Y.M.
        The effect of transjugular intrahepatic portosystemic shunt plus partial splenic embolization for the treatment of patients with recurrent variceal bleeding.
        Acad Radiol. 2020; 27: 323-331https://doi.org/10.1016/j.acra.2019.04.013