Advertisement
Research Article| Volume 165, ISSUE 3, P525-533, March 2019

Simultaneous hepatic and portal vein ligation induces rapid liver hypertrophy: A study in pigs

Published:October 25, 2018DOI:https://doi.org/10.1016/j.surg.2018.09.001

      Abstract

      Background

      Liver hypertrophy induced by partial portal vein occlusion (PVL) is accelerated by adding simultaneous parenchymal transection (“ALPPS procedure”). This preclinical experimental study in pigs tests the hypothesis that simultaneous ligation of portal and hepatic veins of the liver also accelerates regeneration by abrogation of porto-portal collaterals without need for operative transection.

      Methods

      A pig model of portal vein occlusion was compared with the novel model of simultaneous portal and hepatic vein occlusion, where major hepatic veins draining the portal vein–deprived lobe were identified with intraoperative ultrasonography and ligated using pledgeted transparenchymal sutures. Kinetic growth was compared, and the portal vein system was then studied after 7 days using epoxy casts of the portal circulation. Portal vein flow and portal pressure were measured, and Ki-67 staining was used to evaluate the proliferative response.

      Results

      Pigs were randomly assigned to portal vein occlusion (n = 8) or simultaneous portal and hepatic vein occlusion (n = 6). Simultaneous portal and hepatic vein occlusion was well tolerated and led to mild cytolysis, with no necrosis in the outflow vein–deprived liver sectors. The portal vein–supplied sector increased by 90 ± 22% (mean ± standard deviation) after simultaneous portal and hepatic vein occlusion compared with 29 ± 18% after PVL (P < .001). Collaterals to the deportalized liver developed after 7 days in both procedures but were markedly reduced in simultaneous portal and hepatic vein occlusion. Ki-67 staining at 7 days was comparable.

      Conclusion

      This study in pigs found that simultaneous portal and hepatic vein occlusion led to rapid hypertrophy without necrosis of the deportalized liver. The findings suggest that the use of simultaneous portal and hepatic vein occlusion accelerates liver hypertrophy for extended liver resections and should be evaluated further.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Surgery
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Abdalla EK
        • Noun R
        • Belghiti J
        Hepatic vascular occlusion: which technique?.
        Surg Clin North Am. 2004; 84: 563-585
        • Kianmanesh R
        • Farges O
        • Abdalla EK
        • Sauvanet A
        • Ruszniewski P
        • Belghiti J
        Right portal vein ligation: a new planned two-step all-surgical approach for complete resection of primary gastrointestinal tumors with multiple bilateral liver metastases.
        J Am Coll Surg. 2003; 197: 164-170
        • Vauthey JN
        • Mizuno T
        Portal vein embolization: tailoring, optimizing, and quantifying an invaluable procedure in hepatic surgery.
        Ann Surg Oncol. 2017; 24: 1456-1458
        • Schnitzbauer AA
        • Lang SA
        • Goessmann H
        • Nadalin S
        • Baumgart J
        • Farkas SA
        • 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.
        Ann Surg. 2012; 255: 405-414
        • Deal RA
        • Fredericks C
        • Williams L
        • Olthof PB
        • Dirscherl K
        • Keutgen X
        • et al.
        Rapid liver hypertrophy after portal vein occlusion correlates with the degree of collaterization between lobes: a study in pigs.
        J Gastrointest Surg. 2017; (in press)
        • Kilkenny C
        • Altman DG
        Improving bioscience research reporting: ARRIVE-ing at a solution.
        Lab Anim. 2010; 44: 377-378
        • Deal R
        • Frederiks C
        • Williams L
        • Olthof PB
        • Dirscherl K
        • Keutgen X
        • et al.
        Rapid liver hypertrophy after portal vein occlusion correlates with the degree of collateralization between lobes: a study in pigs.
        J Gastrointest Surg. 2017; 22: 203-213
        • Schadde E
        • Tsatsaris C
        • Swiderska-Syn M
        • Breitenstein S
        • Urner M
        • Schimmer R
        • et al.
        Hypoxia of the growing liver accelerates regeneration.
        Surgery. 2017; 163: 666-679
        • Francavilla A
        • Azzarone A
        • Carrieri G
        • Scotti-Foglieni C
        • Zeng QH
        • Cillo U
        • et al.
        Effect on the canine Eck fistula liver of intraportal TGF-beta alone or with hepatic growth factors.
        Hepatology. 1992; 16: 1267-1270
        • Hwang S
        • Ha TY
        • Ko GY
        • Kwon DI
        • Song GW
        • Jung DH
        • et al.
        Preoperative sequential portal and hepatic vein embolization in patients with hepatobiliary malignancy.
        World J Surg. 2015; 39: 2990-2998
        • Hwang S
        • Lee SG
        • Ko GY
        • Kim BS
        • Sung KB
        • Kim MH
        • et al.
        Sequential preoperative ipsilateral hepatic vein embolization after portal vein embolization to induce further liver regeneration in patients with hepatobiliary malignancy.
        Ann Surg. 2009; 249: 608-616
        • 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.
        Eur Radiol. 2017; 27: 3343-3352
        • Guiu B
        • Chevallier P
        • Denys A
        • Delhom E
        • Pierredon-Foulongne MA
        • Rouanet P
        • et al.
        Simultaneous trans-hepatic portal and hepatic vein embolization before major hepatectomy: the liver venous deprivation technique.
        Eur Radiol. 2016; 26: 4259-4267
        • van Lienden KP
        • van den Esschert JW
        • Rietkerk M
        • Heger M
        • Roelofs JJ
        • Lameris JS
        • et al.
        Short-term effects of combined hepatic vein embolization and portal vein embolization for the induction of liver regeneration in a rabbit model.
        J Vasc Intervent Radiol. 2012; 23: 962-967
        • Huisman F
        • van Lienden KP
        • Damude S
        • Hoekstra LT
        • van Gulik TM
        A review of animal models for portal vein embolization.
        J Surg Res. 2014; 191: 179-188
        • de Santibanes E
        • Clavien PA
        Playing Play-Doh to prevent postoperative liver failure: the "ALPPS" approach.
        Ann Surg. 2012; 255: 415-417
        • Schadde E
        • Malago M
        • Hernandez-Alejandro R
        • Li J
        • Abdalla E
        • Ardiles V
        • et al.
        Monosegment ALPPS hepatectomy: extending resectability by rapid hypertrophy.
        Surgery. 2015; 157: 676-689
        • Aloia TA
        • Vauthey JN
        Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): what is gained and what is lost?.
        Ann Surg. 2012; 256 (author reply e16-9): e9
        • Dokmak S
        • Belghiti J
        Which limits to the "ALPPS" approach?.
        Ann Surg. 2012; 256 (author reply e16-7): e6
        • Belghiti J
        • Dokmak S
        • Schadde E
        ALPPS: Innovation for innovation's sake.
        Surgery. 2016; 159: 1287-1288
        • Schadde E
        • Ardiles V
        • Robles-Campos R
        • Malago M
        • Machado M
        • Hernandez-Alejandro R
        • et al.
        Early survival and safety of ALPPS: first report of the International ALPPS Registry.
        Ann Surg. 2014; 260 (discussion 36-8): 829-836
        • Schadde E
        • Raptis DA
        • Schnitzbauer AA
        • Ardiles V
        • Tschuor C
        • Lesurtel M
        • et al.
        Prediction of mortality after ALPPS Stage-1: an analysis of 320 patients from the international ALPPS registry.
        Ann Surg. 2015; 262: 780-786
        • Linecker M
        • Bjornsson B
        • Stavrou GA
        • Oldhafer KJ
        • Lurje G
        • Neumann U
        • et al.
        Risk adjustment in ALPPS is associated with a dramatic decrease in early mortality and morbidity.
        Ann Surg. 2017; 266: 779-786
        • Sandstrom P
        • Rosok BI
        • Sparrelid E
        • Larsen PN
        • Larsson AL
        • Lindell G
        • et al.
        ALPPS improves resectability compared with conventional two-stage hepatectomy in patients with advanced colorectal liver metastasis: results from a Scandinavian multicenter randomized controlled trial (LIGRO Trial).
        Ann Surg. 2018; 267: 833-840
        • Truant S
        • Baillet C
        • Deshorgue AC
        • Leteurtre E
        • Hebbar M
        • Ernst O
        • et al.
        Drop of total liver function in the interstages of the new associating liver partition and portal vein ligation for staged hepatectomy technique: analysis of the "auxiliary liver" by HIDA scintigraphy.
        Ann Surg. 2016; 263: e33-e34
        • Matsuo K
        • Hiroshima Y
        • Yamazaki K
        • Kasahara K
        • Kikuchi Y
        • Kawaguchi D
        • et al.
        Immaturity of bile canalicular-ductule networks in the future liver remnant while associating liver partition and portal vein occlusion for staged hepatectomy (ALPPS).
        Ann Surg Oncol. 2017; 24: 2456-2464
        • Matsuo K
        • Murakami T
        • Kawaguchi D
        • Hiroshima Y
        • Koda K
        • Yamazaki K
        • et al.
        Histologic features after surgery associating liver partition and portal vein ligation for staged hepatectomy versus those after hepatectomy with portal vein embolization.
        Surgery. 2016; 159: 1289-1298
        • Olthof PB
        • Tomassini F
        • Huespe P
        • Truant S
        • Pruvot FR
        • Troisi R
        • et al.
        Hepatobiliary scintigraphy to evaluate liver function in ALPPS - liver volume overestimates liver function.
        Surgery. 2017; 162: 775-783
        • Olthof PB
        • Schadde E
        • van Lienden KP
        • Heger M
        • de Bruin K
        • Verheij J
        • et al.
        Hepatic parenchymal transection increases liver volume but not function after portal vein embolization in rabbits.
        Surgery. 2017; 162: 732-741
        • Denys AL
        • Abehsera M
        • Sauvanet A
        • Sibert A
        • Belghiti J
        • Menu Y
        Failure of right portal vein ligation to induce left lobe hypertrophy due to intrahepatic portoportal collaterals: successful treatment with portal vein embolization.
        AJR Am J Roentgenol. 1999; 173: 633-635
        • van Lienden KP
        • Hoekstra LT
        • Bennink RJ
        • van Gulik TM
        Intrahepatic left to right portoportal venous collateral vascular formation in patients undergoing right portal vein ligation.
        Cardiovasc Interven Radiol. 2013; 36: 1572-1579
        • Rous P
        • Larimore LD
        Relation of the portal blood to liver maintenance: a demonstration of liver atrophy conditional on compensation.
        J Exp Med. 1920; 31: 609-632