Advertisement

Safety of laparoscopic hepatectomy in patients with hepatocellular carcinoma and portal hypertension: interim analysis of an open prospective study

  • Chetana Lim
  • Michael Osseis
  • Eylon Lahat
  • Alexandre Doussot
  • Dobromir Sotirov
  • Francois Hemery
  • Marc Lantéri-Minet
  • Cyrille Feray
  • Chady Salloum
  • Daniel Azoulay
Research Article
  • 8 Downloads

Abstract

Background

The laparoscopic approach might increase the number of cirrhotic patients with hepatocellular carcinoma (HCC) indicated for liver resection, otherwise contraindicated due to portal hypertension. The goal of this study was to confirm the safety of laparoscopic liver resection (LLR) in patients with portal hypertension.

Methods

This prospective, single-center, open study (ClinicalTrials.gov ID: NCT02145013) included all consecutive cirrhotic patients who underwent LLR for HCC from 2014 to 2017. Short-term outcomes were compared between patients with and without clinically significant portal hypertension (CSPH, defined by hepatic venous pressure gradient ≥ 10 mmHg).

Results

The study population included 45 patients, comprising 27 patients (60%) in the no CSPH group and 18 patients (40%) in the CSPH group. All planned procedures could be performed. The two groups did not differ in the extent of resection, transfusion, duration of clamping, and need for conversion. Overall, the 90-day mortality and severe morbidity rates were nil. Moderate morbidity was significantly higher in the CSPH group (39 vs. 4%, p = 0.01); however, the two groups did not differ in the rate of unresolved liver decompensation. Intensive care unit and hospital stays were significantly longer in the CSPH group. At 2 years, overall survival was 77% in the no CSPH group and 100% in the CSPH group (p = 0.17), and recurrence-free survival was 55% in the no CSPH group and 79% in the CSPH group (p = 0.10).

Conclusion

LLR is safe in BCLC 0-A patients with CSPH, with no mortality and good short-term outcomes. Re-evaluation of the BCLC guidelines is needed.

Keywords

Liver resection Hepatocellular carcinoma Laparoscopic Clinically significant portal hypertension Hepatic venous pressure gradient 

Notes

Compliance with Ethical Standards

Disclosures

Dr. Chetana Lim, Dr. Michael Osseis, Dr. Eylon Lahat, Dr. Alexandre Doussot, Dr. Dobromir Sotirov, Dr. Francois Hemery, Dr. Marc Lantéri-Minet, Pr. Cyrille Feray, Dr. Chady Salloum, and Pr. Daniel Azoulay have no conflicts of interest or financial ties to disclose.

References

  1. 1.
    EASL-EORTC (2012) EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56:908–943CrossRefGoogle Scholar
  2. 2.
    Faitot F, Allard MA, Pittau G, Ciacio O, Adam R, Castaing D, Cunha AS, Pelletier G, Cherqui D, Samuel D, Vibert E (2015) Impact of clinically evident portal hypertension on the course of hepatocellular carcinoma in patients listed for liver transplantation. Hepatology 62:179–187CrossRefPubMedGoogle Scholar
  3. 3.
    Boleslawski E, Petrovai G, Truant S, Dharancy S, Duhamel A, Salleron J, Deltenre P, Lebuffe G, Mathurin P, Pruvot FR (2012) Hepatic venous pressure gradient in the assessment of portal hypertension before liver resection in patients with cirrhosis. Br J Surg 99:855–863CrossRefPubMedGoogle Scholar
  4. 4.
    Bruix J, Castells A, Bosch J, Feu F, Fuster J, Garcia-Pagan JC, Visa J, Bru C, Rodes J (1996) Surgical resection of hepatocellular carcinoma in cirrhotic patients: prognostic value of preoperative portal pressure. Gastroenterology 111:1018–1022CrossRefPubMedGoogle Scholar
  5. 5.
    Cucchetti A, Cescon M, Golfieri R, Piscaglia F, Renzulli M, Neri F, Cappelli A, Mazzotti F, Mosconi C, Colecchia A, Ercolani G, Pinna AD (2015) Hepatic venous pressure gradient in the preoperative assessment of patients with resectable hepatocellular carcinoma. J Hepatol 64:79–86CrossRefPubMedGoogle Scholar
  6. 6.
    Lim C, Salloum C, Osseis M, Lahat E, Gomez-Gavara C, Compagnon P, Luciani A, Feray C, Azoulay D (2017) Short-term outcomes following hepatectomy for hepatocellular carcinoma within and beyond the BCLC guidelines: a prospective study. HPB (Oxford).  https://doi.org/10.1016/j.hpb.2017.08.027 Google Scholar
  7. 7.
    Llovet JM, Bru C, Bruix J (1999) Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 19:329–338CrossRefPubMedGoogle Scholar
  8. 8.
    Molina V, Sampson-Davila J, Ferrer J, Fondevila C, Diaz Del Gobbo R, Calatayud D, Bruix J, Garcia-Valdecasas JC, Fuster J (2017) Benefits of laparoscopic liver resection in patients with hepatocellular carcinoma and portal hypertension: a case-matched study. Surg Endosc.  https://doi.org/10.1007/s00464-017-5930-1 Google Scholar
  9. 9.
    Stremitzer S, Tamandl D, Kaczirek K, Maresch J, Abbasov B, Payer BA, Ferlitsch A, Gruenberger T (2011) Value of hepatic venous pressure gradient measurement before liver resection for hepatocellular carcinoma. Br J Surg 98:1752–1758CrossRefPubMedGoogle Scholar
  10. 10.
    Truant S, Bouras AF, Hebbar M, Boleslawski E, Fromont G, Dharancy S, Leteurtre E, Zerbib P, Pruvot FR (2011) Laparoscopic resection vs. open liver resection for peripheral hepatocellular carcinoma in patients with chronic liver disease: a case-matched study. Surg Endosc 25:3668–3677CrossRefPubMedGoogle Scholar
  11. 11.
    Berzigotti A, Reig M, Abraldes JG, Bosch J, Bruix J (2014) Portal hypertension and the outcome of surgery for hepatocellular carcinoma in compensated cirrhosis: a systematic review and meta-analysis. Hepatology 61:526–536CrossRefGoogle Scholar
  12. 12.
    Choi SB, Kim HJ, Song TJ, Ahn HS, Choi SY (2014) Influence of clinically significant portal hypertension on surgical outcomes and survival following hepatectomy for hepatocellular carcinoma: a systematic review and meta-analysis. J Hepatobiliary Pancreat Sci 21:639–647CrossRefPubMedGoogle Scholar
  13. 13.
    Tang YH, Zhu WJ, Wen TF (2014) Influence of clinically significant portal hypertension on hepatectomy for hepatocellular carcinoma: a meta-analysis. Asian Pac J Cancer Prev 15:1649–1654CrossRefPubMedGoogle Scholar
  14. 14.
    Jiang B, Yan X, Zhang JH (2018) Meta-analysis of laparoscopic versus open liver resection for hepatocellular carcinoma. Hepatol Res.  https://doi.org/10.1111/hepr.13061 Google Scholar
  15. 15.
    Xiong JJ, Altaf K, Javed MA, Huang W, Mukherjee R, Mai G, Sutton R, Liu XB, Hu WM (2012) Meta-analysis of laparoscopic vs open liver resection for hepatocellular carcinoma. World J Gastroenterol 18:6657–6668CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Memeo R, de’Angelis N, Compagnon P, Salloum C, Cherqui D, Laurent A, Azoulay D (2014) Laparoscopic vs. open liver resection for hepatocellular carcinoma of cirrhotic liver: a case-control study. World J Surg 38:2919–2926CrossRefPubMedGoogle Scholar
  17. 17.
    Morise Z, Ciria R, Cherqui D, Chen KH, Belli G, Wakabayashi G (2015) Can we expand the indications for laparoscopic liver resection? A systematic review and meta-analysis of laparoscopic liver resection for patients with hepatocellular carcinoma and chronic liver disease. J Hepatobiliary Pancreat Sci 22:342–352CrossRefPubMedGoogle Scholar
  18. 18.
    Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Bosch J, Abraldes JG, Berzigotti A, Garcia-Pagan JC (2009) The clinical use of HVPG measurements in chronic liver disease. Nat Rev Gastroenterol Hepatol 6:573–582CrossRefPubMedGoogle Scholar
  20. 20.
    Bosch J, Garcia-Pagan JC, Berzigotti A, Abraldes JG (2006) Measurement of portal pressure and its role in the management of chronic liver disease. Semin Liver Dis 26:348–362CrossRefPubMedGoogle Scholar
  21. 21.
    Forner A, Reig M, Bruix J (2018) Hepatocellular carcinoma. Lancet.  https://doi.org/10.1016/S0140-6736(18)30010-2 PubMedGoogle Scholar
  22. 22.
    Buell JF, Cherqui D, Geller DA, O’Rourke N, Iannitti D, Dagher I, Koffron AJ, Thomas M, Gayet B, Han HS, Wakabayashi G, Belli G, Kaneko H, Ker CG, Scatton O, Laurent A, Abdalla EK, Chaudhury P, Dutson E, Gamblin C, D’Angelica M, Nagorney D, Testa G, Labow D, Manas D, Poon RT, Nelson H, Martin R, Clary B, Pinson WC, Martinie J, Vauthey JN, Goldstein R, Roayaie S, Barlet D, Espat J, Abecassis M, Rees M, Fong Y, McMasters KM, Broelsch C, Busuttil R, Belghiti J, Strasberg S, Chari RS (2009) The international position on laparoscopic liver surgery: the Louisville Statement, 2008. Ann Surg 250:825–830CrossRefPubMedGoogle Scholar
  23. 23.
    Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS, Asbun H, O’Rourke N, Tanabe M, Koffron AJ, Tsung A, Soubrane O, Machado MA, Gayet B, Troisi RI, Pessaux P, Van Dam RM, Scatton O, Abu Hilal M, Belli G, Kwon CH, Edwin B, Choi GH, Aldrighetti LA, Cai X, Cleary S, Chen KH, Schon MR, Sugioka A, Tang CN, Herman P, Pekolj J, Chen XP, Dagher I, Jarnagin W, Yamamoto M, Strong R, Jagannath P, Lo CM, Clavien PA, Kokudo N, Barkun J, Strasberg SM (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261:619–629PubMedGoogle Scholar
  24. 24.
    de Haas RJ, Lim C, Bhangui P, Salloum C, Compagnon P, Feray C, Calderaro J, Luciani A, Azoulay D (2017) Curative salvage liver transplantation in patients with cirrhosis and hepatocellular carcinoma: an intention-to-treat analysis. Hepatology 67:204–215CrossRefPubMedGoogle Scholar
  25. 25.
    Lim C, Shinkawa H, Hasegawa K, Bhangui P, Salloum C, Gomez Gavara C, Lahat E, Omichi K, Arita J, Sakamoto Y, Compagnon P, Feray C, Kokudo N, Azoulay D (2017) Salvage liver transplantation or repeat hepatectomy for recurrent hepatocellular carcinoma: an intent-to-treat analysis. Liver Transpl 23:1553–1563CrossRefPubMedGoogle Scholar
  26. 26.
    de’Angelis N, Eshkenazy R, Brunetti F, Valente R, Costa M, Disabato M, Salloum C, Compagnon P, Laurent A, Azoulay D (2014) Laparoscopic versus open resection for colorectal liver metastases: a single-center study with propensity score analysis. J Laparoendosc Adv Surg Tech A 25:12–20CrossRefPubMedGoogle Scholar
  27. 27.
    de’Angelis N, Memeo R, Calderaro J, Felli E, Salloum C, Compagnon P, Luciani A, Laurent A, Cherqui D, Azoulay D (2014) Open and laparoscopic resection of hepatocellular adenoma: trends over 23 years at a specialist hepatobiliary unit. HPB (Oxford) 16:783–788CrossRefGoogle Scholar
  28. 28.
    Salloum C, Lim C, Azoulay D (2015) Robot-assisted laparoscopic left lateral sectionectomy for benign and malignant liver tumors. J Visc Surg 152:373–378CrossRefPubMedGoogle Scholar
  29. 29.
    Salloum C, Lim C, Lahat E, Gavara CG, Levesque E, Compagnon P, Azoulay D (2016) Robotic-assisted versus laparoscopic left lateral sectionectomy: analysis of surgical outcomes and costs by a propensity score matched cohort study. World J Surg 41:516–524CrossRefGoogle Scholar
  30. 30.
    Salloum C, Subar D, Memeo R, Tayar C, Laurent A, Malek A, Azoulay D (2014) Laparoscopic robotic liver surgery: the Henri Mondor initial experience of 20 cases. J Robot Surg 8:119–124CrossRefPubMedGoogle Scholar
  31. 31.
    Inoue Y, Suzuki Y, Fujii K, Kawaguchi N, Ishii M, Masubuchi S, Yamamoto M, Hirokawa F, Hayashi M, Uchiyama K (2017) Laparoscopic hepatic resection using extracorporeal Pringle maneuver. J Laparoendosc Adv Surg Tech A 28:452–458Google Scholar
  32. 32.
    Patriti A, Ceccarelli G, Bartoli A, Casciola L (2011) Extracorporeal Pringle maneuver in robot-assisted liver surgery. Surg Laparosc Endosc Percutaneous Tech 21:e242–e244CrossRefGoogle Scholar
  33. 33.
    Balzan S, Belghiti J, Farges O, Ogata S, Sauvanet A, Delefosse D, Durand F (2005) The “50–50 criteria” on postoperative day 5: an accurate predictor of liver failure and death after hepatectomy. Ann Surg 242:824–828 discussion 828–9CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Lim C, Audureau E, Salloum C, Levesque E, Lahat E, Merle JC, Compagnon P, Dhonneur G, Feray C, Azoulay D (2016) Acute kidney injury following hepatectomy for hepatocellular carcinoma: incidence, risk factors and prognostic value. HPB (Oxford) 18:540–548CrossRefGoogle Scholar
  35. 35.
    Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Edmondson HA, Steiner PE (1954) Primary carcinoma of the liver: a study of 100 cases among 48,900 necropsies. Cancer 7:462–503CrossRefPubMedGoogle Scholar
  37. 37.
    Sala M, Fuster J, Llovet JM, Navasa M, Sole M, Varela M, Pons F, Rimola A, Garcia-Valdecasas JC, Bru C, Bruix J (2004) High pathological risk of recurrence after surgical resection for hepatocellular carcinoma: an indication for salvage liver transplantation. Liver Transpl 10:1294–1300CrossRefPubMedGoogle Scholar
  38. 38.
    Ferrer-Fabrega J, Forner A, Liccioni A, Miquel R, Molina V, Navasa M, Fondevila C, Garcia-Valdecasas JC, Bruix J, Fuster J (2015) Prospective validation of ab initio liver transplantation in hepatocellular carcinoma upon detection of risk factors for recurrence after resection. Hepatology 63:839–849CrossRefGoogle Scholar
  39. 39.
    Benchimol EI, Langan S, Guttmann A (2012) Call to RECORD: the need for complete reporting of research using routinely collected health data. J Clin Epidemiol 66:703–705CrossRefPubMedGoogle Scholar
  40. 40.
    Llop E, Berzigotti A, Reig M, Erice E, Reverter E, Seijo S, Abraldes JG, Bruix J, Bosch J, Garcia-Pagan JC (2011) Assessment of portal hypertension by transient elastography in patients with compensated cirrhosis and potentially resectable liver tumors. J Hepatol 56:103–108CrossRefPubMedGoogle Scholar
  41. 41.
    Llovet JM, Fuster J, Bruix J (1999) Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology 30:1434–1440CrossRefPubMedGoogle Scholar
  42. 42.
    Han HS, Shehta A, Ahn S, Yoon YS, Cho JY, Choi Y (2015) Laparoscopic versus open liver resection for hepatocellular carcinoma: case-matched study with propensity score matching. J Hepatol 63:643–650CrossRefPubMedGoogle Scholar
  43. 43.
    Tajiri K, Shimizu Y (2014) Liver physiology and liver diseases in the elderly. World J Gastroenterol 19:8459–8467CrossRefGoogle Scholar
  44. 44.
    Shaya FT, Breunig IM, Seal B, Mullins CD, Chirikov VV, Hanna N (2013) Comparative and cost effectiveness of treatment modalities for hepatocellular carcinoma in SEER-Medicare. Pharmacoeconomics 32:63–74CrossRefGoogle Scholar
  45. 45.
    Roayaie S, Jibara G, Tabrizian P, Park JW, Yang J, Yan L, Schwartz M, Han G, Izzo F, Chen M, Blanc JF, Johnson P, Kudo M, Roberts LR, Sherman M (2015) The role of hepatic resection in the treatment of hepatocellular cancer. Hepatology 62:440–451CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Chetana Lim
    • 1
  • Michael Osseis
    • 1
  • Eylon Lahat
    • 1
  • Alexandre Doussot
    • 1
    • 2
  • Dobromir Sotirov
    • 1
  • Francois Hemery
    • 3
  • Marc Lantéri-Minet
    • 4
  • Cyrille Feray
    • 5
  • Chady Salloum
    • 1
  • Daniel Azoulay
    • 1
    • 6
    • 7
  1. 1.Department of Hepatobiliary and Pancreatic Surgery and Liver TransplantationHenri Mondor HospitalCréteilFrance
  2. 2.Department of Hepatobiliary and Pancreatic Surgery and Liver TransplantationBesançonFrance
  3. 3.Medical Informatics DepartmentHenri Mondor HospitalCréteilFrance
  4. 4.Department of Anesthesia and Liver Intensive Care UnitHenri Mondor HospitalCréteilFrance
  5. 5.Department of HepatologyHenri Mondor HospitalCréteilFrance
  6. 6.Université Paris-Est UPECCréteilFrance
  7. 7.INSERM, U955CréteilFrance

Personalised recommendations