Abstract
Background
The presence of clinically significant portal hypertension (CSPH) remains a relative contraindication to liver resection for patients with resectable hepatocellular carcinoma (HCC). The goal of this study was to explore whether a laparoscopic approach could extend the indications for hepatectomy to patients with PH.
Method
Patients who underwent laparoscopic liver resection (LLR) from February 2016 to September 2019 performed by a single medical team were included in this study. We analyzed the surgical and oncological outcomes between groups with and without CSPH before and after propensity score matching (PSM).
Result
We enrolled 156 patients divided into two groups according to the presence (CSPH, n = 26) or absence (non-CSPH, n = 130) of CSPH. CSPH group was associated with more clinical signs of liver dysfunction (p < 0.05). After PSM (n = 48 patients), the CSPH group tended to have a longer postoperative hospital stay (p = 0.054); however, there was no difference in operation time (p = 0.329), blood loss volume (p = 0.392), transfusion rates (p = 0.701), rate of conversion to open surgery (p = 0.666), surgical margin (p = 0.306), surgical mortality (n = 0), or comprehensive complication index (p = 0.844) between the two groups. The median follow-up time for the entire cohort was 19.6 months (range 0.2–40.6 months). The 3-year overall survival rate was 62.9% in the CSPH group and 84.3% in the non-CSPH group (p = 0.1090), and results were similar after PSM (p = 0.5734).
Conclusions
LLR is safe and feasible for HCC with PH. The introduction of minimally invasive surgery, represented by LLR, can appropriately expand the indications for hepatectomy.
Similar content being viewed by others
Abbreviations
- HCC:
-
Hepatocellular carcinoma
- CSPH:
-
Clinically significant portal hypertension
- LLR:
-
Laparoscopic liver resection
- PSM:
-
Propensity score matched
- HBV:
-
Hepatitis B virus
- BCLC:
-
Barcelona Clinic Liver Cancer
- RFA:
-
Radiofrequency ablation
- RFS:
-
Recurrence-free survival
- OS:
-
Overall survival
- BMI:
-
Body mass index
- ASA:
-
American Society of Anesthesiologists
- ICG-R15:
-
Indocyanine green retention rate at 15 min
- HVPG:
-
Hepatic venous pressure gradient
- CCI:
-
Comprehensive complication index
- AST:
-
Aspartate aminotransferase
- ALT:
-
Alanine aminotransferase
- INR:
-
International normalized ratio
- IQR:
-
Interquartile range
References
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424
Grazi GL, Ercolani G, Pierangeli F, Del Gaudio M, Cescon M, Cavallari A, Mazziotti A (2001) Improved results of liver resection for hepatocellular carcinoma on cirrhosis give the procedure added value. Ann Surg 234:71–78
EASL Clinical Practice Guidelines (2018) Management of hepatocellular carcinoma. J Hepatol 69:182–236
Zhu RX, Seto WK, Lai CL, Yuen MF (2016) Epidemiology of hepatocellular carcinoma in the Asia-pacific region. Gut Liver 10:332–339
Hackl C, Schlitt HJ, Renner P, Lang SA (2016) Liver surgery in cirrhosis and portal hypertension. World J Gastroenterol 22:2725–2735
Llovet JM, Bru C, Bruix J (1999) Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 19:329–338
Forner A, Reig ME, de Lope CR, Bruix J (2010) Current strategy for staging and treatment: the BCLC update and future prospects. Semin Liver Dis 30:61–74
Tian G, Yang S, Yuan J, Threapleton D, Zhao Q, Chen F, Cao H, Jiang T, Li L (2018) Comparative efficacy of treatment strategies for hepatocellular carcinoma: systematic review and network meta-analysis. BMJ Open 8:e021269
Kawano Y, Sasaki A, Kai S, Endo Y, Iwaki K, Uchida H, Shibata K, Ohta M, Kitano S (2008) Short- and long-term outcomes after hepatic resection for hepatocellular carcinoma with concomitant esophageal varices in patients with cirrhosis. Ann Surg Oncol 15:1670–1676
Cucchetti A, Ercolani G, Vivarelli M, Cescon M, Ravaioli M, Ramacciato G, Grazi GL, Pinna AD (2009) Is portal hypertension a contraindication to hepatic resection? Ann Surg 250:922–928
Giannini EG, Savarino V, Farinati F, Ciccarese F, Rapaccini G, Marco MD, Benvegnu L, Zoli M, Borzio F, Caturelli E, Chiaramonte M, Trevisani F (2013) Influence of clinically significant portal hypertension on survival after hepatic resection for hepatocellular carcinoma in cirrhotic patients. Liver Int 33:1594–1600
Coelho FF, Kruger JA, Fonseca GM, Araujo RL, Jeismann VB, Perini MV, Lupinacci RM, Cecconello I, Herman P (2016) Laparoscopic liver resection: experience based guidelines. World J Gastrointest Surg 8:5–26
Abraldes JG, Araujo IK, Turon F, Berzigotti A (2012) Diagnosing and monitoring cirrhosis: liver biopsy, hepatic venous pressure gradient and elastography. Gastroenterol Hepatol 35:488–495
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 26:348–362
Berzigotti A, Reig M, Abraldes JG, Bosch J, Bruix J (2015) Portal hypertension and the outcome of surgery for hepatocellular carcinoma in compensated cirrhosis: a systematic review and meta-analysis. Hepatology 61:526–536
Bruix J, Sherman M (2005) Management of hepatocellular carcinoma. Hepatology 42:1208–1236
de Franchis R, Dell'Era A, Primignani M (2008) Diagnosis and monitoring of portal hypertension. Dig Liver Dis 40:312–317
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 250:825–830
Makuuchi M, Hasegawa H, Yamazaki S (1985) Ultrasonically guided subsegmentectomy. Surg Gynecol Obstet 161:346–350
Couinaud C (1954) Anatomic principles of left and right regulated hepatectomy: technics. J Chir (Paris) 70:933–966
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 828–829
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 240:205–213
Clavien PA, Vetter D, Staiger RD, Slankamenac K, Mehra T, Graf R, Puhan MA (2017) The comprehensive complication index (CCI(R)): added value and clinical perspectives 3 years "down the line". Ann Surg 265:1045–1050
Kawamura H, Kamiyama T, Nakagawa T, Nakanishi K, Yokoo H, Tahara M, Kamachi H, Toi H, Matsushita M, Todo S (2008) Preoperative evaluation of hepatic functional reserve by converted ICGR15 calculated from Tc-GSA scintigraphy. J Gastroenterol Hepatol 23:1235–1241
Takasaki K, Kobayashi S, Tanaka S, Saito A, Yamamoto M, Hanyu F (1990) Highly anatomically systematized hepatic resection with Glissonean sheath code transection at the hepatic hilus. Int Surg 75:73–77
Cai J, Zheng J, Xie Y, Kirih MA, Jiang G, Liang Y, Liang X (2020) A novel simple intra-corporeal Pringle maneuver for laparoscopic hemihepatectomy: how we do it. Surg Endosc 34:2807
Sala M, Fuster J, Llovet JM, Navasa M, Solé M, Varela M, Pons F, Rimola A, García-Valdecasas JC, Brú C, Bruix J (2004) High pathological risk of recurrence after surgical resection for hepatocellular carcinoma: an indication for salvage liver transplantation. Liver Transpl 10:1294–1300
Worhunsky DJ, Dua MM, Tran TB, Siu B, Poultsides GA, Norton JA, Visser BC (2016) Laparoscopic hepatectomy in cirrhotics: safe if you adjust technique. Surg Endosc 30:4307–4314
Molina V, Sampson-Davila J, Ferrer J, Fondevila C, Diaz Del Gobbo R, Calatayud D, Bruix J, Garcia-Valdecasas JC, Fuster J (2018) Benefits of laparoscopic liver resection in patients with hepatocellular carcinoma and portal hypertension: a case-matched study. Surg Endosc 32:2345–2354
Lim C, Osseis M, Lahat E, Doussot A, Sotirov D, Hemery F, Lanteri-Minet M, Feray C, Salloum C, Azoulay D (2019) Safety of laparoscopic hepatectomy in patients with hepatocellular carcinoma and portal hypertension: interim analysis of an open prospective study. Surg Endosc 33:811–820
Austin PC (2011) An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivariate Behav Res 46:399–424
Cipriani F, Fantini C, Ratti F, Lauro R, Tranchart H, Halls M, Scuderi V, Barkhatov L, Edwin B, Troisi RI, Dagher I, Reggiani P, Belli G, Aldrighetti L, Abu HM (2018) Laparoscopic liver resections for hepatocellular carcinoma. Can we extend the surgical indication in cirrhotic patients? Surg Endosc 32:617–626
Harada N, Maeda T, Yoshizumi T, Ikeda T, Kayashima H, Ikegami T, Harimoto N, Takaki S, Maehara Y (2016) Laparoscopic liver resection is a feasible treatment for patients with hepatocellular carcinoma and portal hypertension. Anticancer Res 36:3489–3497
Santambrogio R, Kluger MD, Costa M, Belli A, Barabino M, Laurent A, Opocher E, Azoulay D, Cherqui D (2013) Hepatic resection for hepatocellular carcinoma in patients with Child-Pugh's A cirrhosis: is clinical evidence of portal hypertension a contraindication? HPB (Oxford) 15:78–84
EASL-EORTC clinical practice guidelines (2012) Management of hepatocellular carcinoma. J Hepatol 56:908–943
Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022
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 111:1018–1022
Jaeck D, Bachellier P, Oussoultzoglou E, Weber JC, Wolf P (2004) Surgical resection of hepatocellular carcinoma. Post-operative outcome and long-term results in Europe: an overview. Liver Transpl 10:S58–S63
Shen YN, Tang TY, Yao WY, Guo CX, Yi Z, Song W, Liang TB, Bai XL (2019) A nomogram for prediction of posthepatectomy liver failure in patients with hepatocellular carcinoma: a retrospective study. Medicine (Baltimore) 98:e18490
Capussotti L, Ferrero A, Vigano L, Muratore A, Polastri R, Bouzari H (2006) Portal hypertension: contraindication to liver surgery? World J Surg 30:992–999
Peng W, Li JW, Zhang XY, Li C, Wen TF, Yan LN, Yang JY (2019) A novel model for predicting posthepatectomy liver failure in patients with hepatocellular carcinoma. PLoS ONE 14:e0219219
Gaillard M, Tranchart H, Dagher I (2014) Laparoscopic liver resections for hepatocellular carcinoma: current role and limitations. World J Gastroenterol 20:4892–4899
Llovet JM, Fuster J, Bruix J (1999) Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology 30:1434–1440
Koniaris LG, Levi DM, Pedroso FE, Franceschi D, Tzakis AG, Santamaria-Barria JA, Tang J, Anderson M, Misra S, Solomon NL, Jin X, DiPasco PJ, Byrne MM, Zimmers TA (2011) Is surgical resection superior to transplantation in the treatment of hepatocellular carcinoma? Ann Surg 254:527–537 discussion 53–528
Adam R, Bhangui P, Vibert E, Azoulay D, Pelletier G, Duclos-Vallee JC, Samuel D, Guettier C, Castaing D (2012) Resection or transplantation for early hepatocellular carcinoma in a cirrhotic liver: does size define the best oncological strategy? Ann Surg 256:883–891
Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, Sugawara Y, Minagawa M, Takayama T, Kawasaki S, Makuuchi M (2003) Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 38:200–207
Vigano L, Laurenzi A, Solbiati L, Procopio F, Cherqui D, Torzilli G (2018) Open liver resection, laparoscopic liver resection, and percutaneous thermal ablation for patients with solitary small hepatocellular carcinoma (≤30 mm): review of the literature and proposal for a therapeutic strategy. Dig Surg 35:359–371
Belli A, Cioffi L, Russo G, Belli G (2015) Liver resection for hepatocellular carcinoma in patients with portal hypertension: the role of laparoscopy. Hepatobil Surg Nutr 4:417–421
Kanazawa A, Tsukamoto T, Shimizu S, Kodai S, Yamazoe S, Yamamoto S, Kubo S (2013) Impact of laparoscopic liver resection for hepatocellular carcinoma with F4-liver cirrhosis. Surg Endosc 27:2592–2597
Cheung TT, Dai WC, Tsang SH, Chan AC, Chok KS, Chan SC, Lo CM (2016) Pure laparoscopic hepatectomy versus open hepatectomy for hepatocellular carcinoma in 110 patients with liver cirrhosis: a propensity analysis at a single center. Ann Surg 264:612–620
Cai J, Zheng J, Xie Y, Kirih MA, Tao L, Liang X (2019) Laparoscopic repeat hepatectomy for treating recurrent liver cancer. J Minim Access Surg. https://doi.org/10.4103/jmas.JMAS_187_19
Lee KF, Wong J, Cheung SYS, Chong CCN, Hui JWY, Leung VYF, Yu SCH, Lai PBS (2018) Does intermittent pringle maneuver increase postoperative complications after hepatectomy for hepatocellular carcinoma? A randomized controlled trial. World J Surg 42:3302–3311
Zhang F, Yan J, Feng XB, Xia F, Li XW, Ma KS, Bie P (2015) Efficiency and safety of radiofrequency-assisted hepatectomy for hepatocellular carcinoma with cirrhosis: a single-center retrospective cohort study. World J Gastroenterol 21:10159–10165
Acknowledgement
We thank Jane Charbonneau, DVM, from Liwen Bianji, Edanz Group China (www.liwenbianji.cn/ac) for editing the English text of a draft of this manuscript.
Funding
This study was supported by the National Natural Science Foundation of China (Grant No. 81827804) and the Zhejiang Major Medical Science and Technology Plan supported by National Health Commission of China (Grant No. WKJ-ZJ-2030).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosures
Xiao Liang, Junhao Zheng, Xu Feng, Yuelong Liang, Jingwei Cai, Zhaoqi Shi, Mubarak Ali Kirih, and Liye Tao have no conflict of interest or financial ties to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zheng, J., Feng, X., Liang, Y. et al. Safety and feasibility of laparoscopic liver resection for hepatocellular carcinoma with clinically significant portal hypertension: a propensity score-matched study. Surg Endosc 35, 3267–3278 (2021). https://doi.org/10.1007/s00464-020-07763-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00464-020-07763-6