Role of temporary portosystemic surgical shunt during liver resection to prevent a post-resection small for size-like syndrome

Abstract

Liver resection stands as the gold-standard therapeutic approach for selected cases of hepatocellular carcinoma (HCC). The extent of resectable parenchyma hinges upon the underlying liver function and its regenerative potential. Consequently, cirrhosis may impede access to potentially curative interventions for HCC arising within this context. Cirrhotic patients undergoing liver resection face heightened susceptibility to post-hepatectomy liver failure (PHLF). The clinical profile of PHLF bears a resemblance to a well-documented syndrome within the liver transplant (LT) domain: Small-for-size syndrome (SFSS), a form of graft failure observed in the postoperative phase following LT with undersized or partial organs. Management of SFSS targets mitigating the overflow syndrome, achievable through diverse portal diversion techniques. Portal vein flow diversion encompasses procedures redirecting a variable proportion of portal vein flow towards systemic circulation. Consequently, derivative procedures aim to directly alleviate portal hypertension. Side-to-side portocaval shunts emerge as the most straightforward and efficacious means of decompressing the portal system. Furthermore, they afford flow calibration to diminish the incidence and severity of steal syndrome and hepatic encephalopathy, without compromising efficacy or hepatic function. Translating insights gleaned from LT complexities involving SFSS to liver resection, strategies involving portal flow diversion warrant consideration in efforts to forestall PHLF. This approach aims to extend the frontiers of liver surgery, broadening access to hepatectomy with curative intent, either as a standalone intervention or as part of a comprehensive treatment regimen where LT serves as a secondary option.

Keywords

Portosystemic shunts / liver resection / cirrhosis / post-hepatectomy liver failure / small-for-size

References

[1] European association for the Study of the Liver. EASL clinical practice guidelines: management of hepatocellular carcinoma.J Hepatol2018;69:182-236

[2] Cillo U.Liver resection is a therapeutic option for highly selected BCLC C patients in the context of an expert multidisciplinary setting.Dig Liver Dis2013;45:460-1.

[3] Ray S,Golhar A.Post hepatectomy liver failure - A comprehensive review of current concepts and controversies.Ann Med Surg2018;34:4-10 PMCID:PMC6120608

[4] Glanemann M,Nussler AK,Neuhaus P.Hyperperfusion syndrome in small-for-size livers.Eur Surg Res2005;37:335-41.

[5] Troisi R,de Hemptinne B.Small-for-size syndrome: what is the problem?.Liver Transpl2003;9:S1.

[6] Ueno S,Kurita K,Aikou T.Effect of prior portosystemic shunt on early hepatic hemodynamics and sinusoids following 84% hepatectomy in dogs.Res Exp Med1995;195:1-8.

[7] García-Valdecasas JC,Charco R.Changes in portal vein flow after adult living-donor liver transplantation: does it influence postoperative liver function?.Liver Transpl2003;9:564-9.

[8] Eguchi S,Sugiyama N,Furui J.Relationship between portal venous flow and liver regeneration in patients after living donor right-lobe liver transplantation.Liver Transpl2003;9:547-51.

[9] Marubashi S,Nagano H.Effect of portal hemodynamics on liver regeneration studied in a novel portohepatic shunt rat model.Surgery2004;136:1028-37.

[10] Sato Y,Tsukada K.Acute portal hypertension reflecting shear stress as a trigger of liver regeneration following partial hepatectomy.Surg Today1997;27:518-26.

[11] Rocheleau B,Houle R,Bilodeau M.Hepatic artery buffer response following left portal vein ligation: its role in liver tissue homeostasis.Am J Physiol1999;277:G1000-7.

[12] Lautt WW.Regulatory processes interacting to maintain hepatic blood flow constancy: Vascular compliance, hepatic arterial buffer response, hepatorenal reflex, liver regeneration, escape from vasoconstriction.Hepatol Res2007;37:891-903. PMCID:PMC2981600

[13] Lautt WW.The 1995 Ciba-Geigy Award Lecture. Intrinsic regulation of hepatic blood flow.Can J Physiol Pharmacol1996;74:223-33.

[14] Gülberg V,Rössle M.Hepatic arterial buffer response in patients with advanced cirrhosis.Hepatology2002;35:630-4.

[15] Ezzat WR.Hepatic arterial pressure-flow autoregulation is adenosine mediated.Am J Physiol1987;252:H836-45.

[16] Demetris AJ,Eghtesad B.Pathophysiologic observations and histopathologic recognition of the portal hyperperfusion or small-for-size syndrome.J Surg Pathol2006;30:986-93.

[17] Man K,Ng IO.Liver transplantation in rats using small-for-size grafts: a study of hemodynamic and morphological changes.Arch Surg2001;136:280-5.

[18] Man K,Lo CM.Graft injury in relation to graft size in right lobe live donor liver transplantation: a study of hepatic sinusoidal injury in correlation with portal hemodynamics and intragraft gene expression.Ann Surg2003;237:256-64. PMCID:PMC1522144

[19] Clavien PA,DeOliveira ML.Strategies for safer liver surgery and partial liver transplantation.N Engl J Med2007;356:1545-59.

[20] Zhou Z,Lin N.Associating liver partition and portal vein ligation for staged hepatectomy versus conventional two-stage hepatectomy: a systematic review and meta-analysis.World J Surg Oncol2017;15:227. PMCID:PMC5738171

[21] Lang H.ALPPS - Beneficial or detrimental?.Surg Oncol2020;33:249-53

[22] Kawaguchi Y,Vauthey JN.Dealing with an insufficient future liver remnant: Portal vein embolization and two-stage hepatectomy.J Surg Oncol2019;119:594-603. PMCID:PMC6422720

[23] Simoneau E,Shaheen M.Portal vein embolization and its effect on tumour progression for colorectal cancer liver metastases.Br J Surg2015;102:1240-9.

[24] Schnitzbauer AA,Goessmann H.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 Surg2012;255:405-14

[25] Schadde E,Slankamenac K.ALPPS offers a better chance of complete resection in patients with primarily unresectable liver tumors compared with conventional-staged hepatectomies: results of a multicenter analysis.World J Surg2014;38:1510-9.

[26] Aloia TA.Associating liver partition and portal vein ligation for staged hepatectomy (ALPPS): what is gained and what is lost?.Ann Surg2012;256:e9; author reply e16-9.

[27] D'Haese JG,Weniger M.Should ALPPS be used for liver resection in intermediate-stage HCC?.Ann Surg Oncol2016;23:1335-43.

[28] Oldhafer KJ,Jenner RM,Stavrou GA.ALPPS for patients with colorectal liver metastases: effective liver hypertrophy, but early tumor recurrence.World J Surg2014;38:1504-9.

[29] Chia DKA,Loh SEK,Madhavan K.ALPPS for hepatocellular carcinoma is associated with decreased liver remnant growth.J Gastrointest Surg2018;22:973-80.

[30] Schadde E,Robles-Campos R.ALPPS Registry GroupEarly survival and safety of ALPPS: first report of the international ALPPS registry.Ann Surg2014;260:829-36; discussion 836-8

[31] Chan ACY,Dai JWC.Impact of split completeness on future liver remnant hypertrophy in associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) in hepatocellular carcinoma: complete-ALPPS versus partial-ALPPS.Surgery2017;161:357-64.

[32] Vennarecci G,Tudisco A.The ALPPS procedure: hepatocellular carcinoma as a main indication. An Italian single-center experience.Updates Surg2019;71:67-75.

[33] Kiuchi T,Uryuhara K. Impact of graft size mismatching on graft prognosis in liver transplantation from living donors. Available from: http://journals.lww.com/00007890-199901270-00024 [Last accessed on 12 Mar 2024]

[34] Xu HS,Jones RS.Study of donor-recipient liver size match for transplantation.Ann Surg1994;219:46-50. PMCID:PMC1243089

[35] Sugawara Y,Takayama T.Small-for-size grafts in living-related liver transplantation.J Am Coll Surg2001;192:510-3.

[36] Wang HS,Enomoto Y.Excessive portal flow causes graft failure in extremely small-for-size liver transplantation in pigs.World J Gastroenterol2005;11:6954-9. PMCID:PMC4717037

[37] Hibi T.Small-for-size syndrome in LT.Clin Liver Dis2017;10:93-6 PMCID:PMC6499227

[38] Nardo B,Puviani L.Portal vein arterialization in a patient with acute liver failure.Transplantation2005;79:851-2.

[39] Fan YD,Van Huysse J,De Hemptinne B.Effects of portal vein arterialization on liver regeneration after partial hepatectomy in the rat.Liver Transpl2002;8:146-52.

[40] Ito T,Yamamoto H.Changes in portal venous pressure in the early phase after living donor liver transplantation: pathogenesis and clinical implications.Transplantation2003;75:1313-7.

[41] Lo CM,Fan ST.Portal hyperperfusion injury as the cause of primary nonfunction in a small-for-size liver graft-successful treatment with splenic artery ligation.Liver Transpl2003;9:626-8.

[42] Yan L,Chen Z.Small-for-size syndrome secondary to outflow block of the segments V and VIII anastomoses--successful treatment with trans-splenic artery embolization: a case report.Transplant Proc2007;39:1699-703.

[43] Abdalla EK,Doherty D,Vauthey JN.Extended hepatectomy in patients with hepatobiliary malignancies with and without preoperative portal vein embolization.Arch Surg2002;137:675-80; discussion 680

[44] Adam R,Bismuth H.Partial portacaval shunt: renaissance of an old concept.Surgery1992;111:610-6.

[45] Batignani G,Rega L.Small diameter H-graft porta-caval shunt performed at different stages of liver disease.Hepatobiliary Pancreat Dis Int2004;3:516-21.

[46] Hu HJ,Li JS,Chai ZP.Small-diameter prosthetic H-graft portacaval shunts in the treatment of portal hypertension.Chin Med J2004;117:195-8.

[47] Del Guercio LR,Kazarian KK.A shunt equation for estimating the splenic component of portal hypertension.Am J Surg1978;135:70-5.

[48] Sax FL.Bleeding esophageal varices.Surg Clin North Am1981;61:209-19.

[49] Brand M,Ede CJ.Surgical portosystemic shunts versus transjugular intrahepatic portosystemic shunt for variceal haemorrhage in people with cirrhosis.Cochrane Database Syst Rev2018;10:CD001023. PMCID:PMC6516991

[50] European Association for the Study of the LiverEASL Clinical Practice Guidelines for the management of patients with decompensated cirrhosis.J Hepatol2018;69:406-60

[51] Starzl TE,Francavilla A.The Eck fistula in animals and humans.Curr Probl Surg1983;20:687-752 PMCID:PMC3154772

[52] Rosemurgy AS.Management of variceal hemorrhage.Curr Probl Surg2003;40:263-343.

[53] Wolff M,Textor J.[Surgery for portal hypertension and transjugular intrahepatic portosystemic shunts in Germany: results of a national survey].Chirurg1999;70:447-52.

[54] Mitra SK,Narasimhan KL.Side-to-side lienorenal shunt without splenectomy in noncirrhotic portal hypertension in children.J Pediatr Surg1993;28:398-401; discussion 401

[55] Mercado MA,Guillén-Navarro E.Small-diameter mesocaval shunts: a 10-year evaluation.J Gastrointest Surg2000;4:453-7.

[56] Glowka TR,Manekeller S.Update on shunt surgery.Visc Med2020;36:206-11 PMCID:PMC7383297

[57] di Francesco F,de Ville de Goyet J.Meso-rex bypass--a procedure to cure prehepatic portal hypertension: the insight and the inside.J Am Coll Surg2014;218:e23-36

[58] Wolff M.Surgical treatment of portal hypertension.Zentralbl Chir2005;130:238-45.

[59] Henderson JM,Kutner MH.DIVERT Study GroupDistal splenorenal shunt versus transjugular intrahepatic portal systematic shunt for variceal bleeding: a randomized trial.Gastroenterology2006;130:1643-51.

[60] Khaitiyar JS,Prasad N,Daruwala DK.Transjugular intrahepatic portosystemic shunt versus distal splenorenal shunt--a comparative study.Hepatogastroenterology2020;47:492-7.

[61] Lee M,Chung YE.Portal venous perfusion steal causing graft dysfunction after orthotopic liver transplantation: serial imaging findings in a successfully treated patient.Ultrasonography2016;35:78-82. PMCID:PMC4701369

[62] Lee SG,Ahn CS.Ligation of left renal vein for large spontaneous splenorenal shunt to prevent portal flow steal in adult living donor liver transplantation.Transpl Int2007;20:45-50.

[63] Castillo-Suescun F,Hidalgo E.Hemodynamic consequences of spontaneous splenorenal shunts in deceased donor liver transplantation.Liver Transpl2011;17:891-5.

[64] Rosemurgy AS,Clark WC,Zervos EE.H-graft portacaval shunts versus TIPS: ten-year follow-up of a randomized trial with comparison to predicted survivals.Ann Surg2005;241:238-46. PMCID:PMC1356908

[65] Rosemurgy AS,Teta AF,Ross SB.Prosthetic H-graft portacaval shunts vs transjugular intrahepatic portasystemic stent shunts: 18-year follow-up of a randomized trial.J Am Coll Surg2012;214:445-53; discussion 453

[66] Llovet JM,Bruix J.Prognosis of hepatocellular carcinoma: the BCLC staging classification.Semin Liver Dis1999;19:329-38.

[67] Vitale A,Zanus G.Barcelona clinic liver cancer staging and transplant survival benefit for patients with hepatocellular carcinoma: a multicentre, cohort study.Lancet Oncol2011;12:654-62

[68] Zhang ZY,Zhang EL,Chen XP.Resection might be a meaningful choice for hepatocellular carcinoma with portal vein thrombosis: A systematic review and meta-analysis.Medicine2019;98:e18362. PMCID:PMC6922393

[69] Sangiovanni A,Iavarone M.Multimodality treatment of hepatocellular carcinoma: How field practice complies with international recommendations.Liver Int2018;38:1624-34.

[70] Wehling C,Olkus A.Treatment stage migration and treatment sequences in patients with hepatocellular carcinoma: drawbacks and opportunities.J Cancer Res Clin Oncol2021;147:2471-81 PMCID:PMC8236446

[71] Marrero JA,Sirlin CB.Diagnosis, staging, and management of hepatocellular carcinoma: 2018 practice guidance by the american association for the study of liver diseases.Hepatology2018;68:723-50.

[72] Vitale A,Pawlik TM.The concept of therapeutic hierarchy for patients with hepatocellular carcinoma: A multicenter cohort study.Liver Int2019;39:1478-89.

[73] Vitale A,Iavarone M.HCC Special Interest Group of the Italian Association for the Study of the LiverPersonalised management of patients with hepatocellular carcinoma: a multiparametric therapeutic hierarchy concept.Lancet Oncol2023;24:e312-22.

[74] Roayaie S,Tabrizian P.The role of hepatic resection in the treatment of hepatocellular cancer.Hepatology2015;62:440-51.

[75] Mazzaferro V,Doci R.Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis.N Engl J Med1996;334:693-9.

[76] Duvoux C,Decaens T.Liver Transplantation French Study GroupLiver transplantation for hepatocellular carcinoma: a model including α-fetoprotein improves the performance of Milan criteria.Gastroenterology2012;143:986-94.e3; quiz e14

[77] Toso C,Wei A.Total tumor volume predicts risk of recurrence following liver transplantation in patients with hepatocellular carcinoma.Liver Transpl2008;14:1107-15.

[78] Lee SG,Moon DB.Expanded indication criteria of living donor liver transplantation for hepatocellular carcinoma at one large-volume center.Liver Transpl2008;14:935-45.

[79] Mazzaferro V,Zhou J.Metroticket 2.0 model for analysis of competing risks of death after liver transplantation for hepatocellular carcinoma.Gastroenterology2018;154:128-39

[80] Cillo U,Polacco M.Liver transplantation for hepatocellular carcinoma through the lens of transplant benefit.Hepatology2017;65:1741-8

[81] Ishizawa T,Aoki T.Neither multiple tumors nor portal hypertension are surgical contraindications for hepatocellular carcinoma.Gastroenterology2008;134:1908-16.

[82] Zhong JH,Gong WF.Hepatic resection associated with good survival for selected patients with intermediate and advanced-stage hepatocellular carcinoma.Ann Surg2014;260:329-40.

[83] Cucchetti A,Vivarelli M.Is portal hypertension a contraindication to hepatic resection?.Ann Surg2009;250:922-8.

[84] Azoulay D,Casellas-Robert M.Liver resection for hepatocellular carcinoma in patients with clinically significant portal hypertension.JHEP Rep2021;3:100190 PMCID:PMC7689549

[85] Citterio D,Sposito C,Bhoori S.Hierarchic interaction of factors associated with liver decompensation after resection for hepatocellular carcinoma.JAMA Surg2016;151:846-53.

[86] Polacco M,Valmasoni M.Liver resection associated with mini porto-caval shunt as salvage treatment in patients with progression of hepatocellular carcinoma before liver transplantation: a case report.Transplant Proc2010;42:1378-80.

[87] Gil A,Hernández-Lizoain JL.The role of transjugular intrahepatic portosystemic shunt prior to abdominal tumoral surgery in cirrhotic patients with portal hypertension.Eur J Surg Oncol2004;30:46-52.

[88] Schwartz SI.Biliary tract surgery and cirrhosis: a critical combination.Surgery1981;90:577-83.

[89] Garrison RN,Howard DA.Clarification of risk factors for abdominal operations in patients with hepatic cirrhosis.Ann Surg1984;199:648-55. PMCID:PMC1353440

[90] Rajesh S,Philips CA.Transjugular intrahepatic portosystemic shunt in cirrhosis: An exhaustive critical update.World J Gastroenterol2020;26:5561-96 PMCID:PMC7545393

[91] Liu J,Bethea ED,Yamada K.Transjugular intrahepatic portosystemic shunt placement for portal hypertension: meta-analysis of safety and efficacy of 8 mm vs. 10 mm stents.Gastroenterol Res Pract2020;2020:9149065. PMCID:PMC7586157

[92] Vizzutti F,Arena U.Transjugular intrahepatic portosystemic shunt (TIPS): current indications and strategies to improve the outcomes.Intern Emerg Med2020;15:37-48

[93] Menahem B,Desjouis A,Lebreton G.Transjugular intrahepatic portosystemic shunt placement increases feasibility of colorectal surgery in cirrhotic patients with severe portal hypertension.Dig Liver Dis2015;47:81-4.

[94] Nacif LS,Sartori VF.Intraoperative surgical portosystemic shunt in liver transplantation: systematic review and meta-analysis.Ann Transplant2018;23:721-32. PMCID:PMC6248172

[95] Tabchouri N,Menahem B.Original study: transjugular intrahepatic portosystemic shunt as a bridge to abdominal surgery in cirrhotic patients.J Gastrointest Surg2019;23:2383-90.

[96] Pizanias M,Prassas E,Prachalias A.Surgical portosystemic shunts to facilitate major intrabdominal surgery.Hepatobiliary Pancreat Dis Int2019;18:488-90.

[97] Sen I,Kärkkäinen JM.Current indications and long-term outcomes of surgical portosystemic shunts in adults.J Gastrointest Surg2021;25:1437-44.

[98] Lahat E,Bhangui P.Transjugular intrahepatic portosystemic shunt as a bridge to non-hepatic surgery in cirrhotic patients with severe portal hypertension: a systematic review.HPB2018;20:101-9.

[99] Pierce DS,Nirula R.Cost-effective analysis of transjugular intrahepatic portosystemic shunt versus surgical portacaval shunt for variceal bleeding in early cirrhosis.Am Surg2011;77:169-73.

[100] Sliwinski S,Mader C,Bechstein W.Liver resection after transjugular portosystemic stent shunt (TIPSS).Z Gastroenterol2023;61:390-3.

[101] Guglielmi A,Conci S,Iacono C.How much remnant is enough in liver resection?.Dig Surg2012;29:6-17.

[102] Gotohda N,Geller DA.Expert consensus guidelines: how to safely perform minimally invasive anatomic liver resection.J Hepatobiliary Pancreat Sci2022;29:16-32.

[103] Xing L,Kan JL.Clinical outcome of open surgery versus laparoscopic surgery for cirrhotic hepatocellular carcinoma patients: a meta-analysis.Eur J Gastroenterol Hepatol2020;32:239-45.

[104] Ciria R,Ocaña S.A Systematic Review and Meta-Analysis Comparing the Short- and Long-Term Outcomes for Laparoscopic and Open Liver Resections for hepatocellular carcinoma: updated results from the european guidelines meeting on laparoscopic liver surgery, southampton, UK, 2017.Ann Surg Oncol2019;26:252-63.

[105] Takada Y,Ishikawa Y.End-to-side portocaval shunting for a small-for-size graft in living donor liver transplantation.Liver Transpl2004;10:807-10.

[106] Capussotti L,Polastri R,Galatola G.Liver function and encephalopathy after partial vs direct side-to-side portacaval shunt: a prospective randomized clinical trial.Surgery2000;127:614-21.