What Is the Role of Minimally Invasive Liver Surgery in Treating Patients with Hepatocellular Carcinoma on Cirrhosis?
Abstract
:Simple Summary
Abstract
1. Introduction
2. Natural History of HCC
3. Current Management of HCC
4. Are There New Perspectives in HCC Treatment?
5. Is There a Changing Scenario in the Epidemiology of HCC?
6. Does MILS Improve Post-Resection Outcomes?
7. Does MILS Increase the Indications for Liver Resection?
8. Does MILS Expand the Indications for HCC Ablation?
9. Does MILS Increase the Probability of Primary or Salvage Liver Transplantation?
10. What Is the Role/Position of MILS in the HCC Treatment Algorithm?
11. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Cancer. IAfRo. GLOBOCAN. 2020. Available online: https://gco.iarc.fr/today/online-analysis-multi-bars?v=2020&mode=cancer&mode_population=countries&population=900&populations=900&key=asr&sex=1&cancer=39&type=0&statistic=5&prevalence=0&population_group=0&ages_group%5B%5D=0&ages_group%5B%5D=17&nb_items=10&group_cancer=1&include_nmsc=0&include_nmsc_other=1&type_multiple=%257B%2522inc%2522%253Atrue%252C%2522mort%2522%253Afalse%252C%2522prev%2522%253Afalse%257D&orientation=horizontal&type_sort=0&type_nb_items=%257B%2522top%2522%253Atrue%252C%2522bottom%2522%253Afalse%257D (accessed on 1 January 2024).
- McGlynn, K.A.; Petrick, J.L.; London, W.T. Global Epidemiology of Hepatocellular Carcinoma. Clin. Liver Dis. 2015, 19, 223–238. [Google Scholar] [CrossRef] [PubMed]
- Rahib, L.; Smith, B.D.; Aizenberg, R.; Rosenzweig, A.B.; Fleshman, J.M.; Matrisian, L.M. Projecting Cancer Incidence and Deaths to 2030: The Unexpected Burden of Thyroid, Liver, and Pancreas Cancers in the United States. Cancer Res. 2014, 74, 2913–2921. [Google Scholar] [CrossRef] [PubMed]
- European Association for the Study of the Liver. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J. Hepatol. 2018, 69, 182–236. [Google Scholar] [CrossRef] [PubMed]
- Santambrogio, R.; Vertemati, M.; Barabino, M.; Zappa, M.A. Laparoscopic Microwave Ablation: Which Technologies Improve the Results. Cancers 2023, 15, 1814. [Google Scholar] [CrossRef] [PubMed]
- Zhu, P.; Liao, W.; Zhang, W.G.; Chen, L.; Shu, C.; Zhang, Z.W.; Huang, Z.Y.; Chen, Y.F.; Lau, W.Y.; Zhang, B.X.; et al. A Prospective Study Using Propensity Score Matching to Compare Long-term Survival Outcomes after Robotic-assisted, Laparoscopic, or Open Liver Resection for Patients with BCLC Stage 0-A Hepatocellular Carcinoma. Ann. Surg. 2023, 277, e103–e111. [Google Scholar] [CrossRef] [PubMed]
- El-Gendi, A.; El-Shafei, M.; El-Gendi, S.; Shawky, A. Laparoscopic Versus Open Hepatic Resection for Solitary Hepatocellular Carcinoma Less Than 5 cm in Cirrhotic Patients: A Randomized Controlled Study. J. Laparoendosc. Adv. Surg. Tech. A 2018, 28, 302–310. [Google Scholar] [CrossRef]
- Goh, B.K.P.; Syn, N.; Koh, Y.X.; Teo, J.Y.; Cheow, P.C.; Jeyaraj, P.R.; Chow, P.K.H.; Ooi, L.; Chung, A.Y.F.; Chan, C.Y. Comparison between short and long-term outcomes after minimally invasive versus open primary liver resections for hepatocellular carcinoma: A 1:1 matched analysis. J. Surg. Oncol. 2021, 124, 560–571. [Google Scholar] [CrossRef]
- Llovet, J.M.; Kelley, R.K.; Villanueva, A.; Singal, A.G.; Pikarsky, E.; Roayaie, S.; Lencioni, R.; Koike, K.; Zucman-Rossi, J.; Finn, R.S. Hepatocellular carcinoma. Nat. Rev. Dis. Prim. 2021, 7, 6. [Google Scholar] [CrossRef]
- El-Serag, H.B. Hepatocellular carcinoma. N. Engl. J. Med. 2011, 365, 1118–1127. [Google Scholar] [CrossRef]
- Reig, M.; Forner, A.; Rimola, J.; Ferrer-Fàbrega, J.; Burrel, M.; Garcia-Criado, Á.; Kelley, R.K.; Galle, P.R.; Mazzaferro, V.; Salem, R.; et al. BCLC strategy for prognosis prediction and treatment recommendation: The 2022 update. J. Hepatol. 2022, 76, 681–693. [Google Scholar] [CrossRef]
- Niizeki, T.; Tokunaga, T.; Takami, Y.; Wada, Y.; Harada, M.; Shibata, M.; Nakao, K.; Sasaki, R.; Hirai, F.; Shakado, S.; et al. Comparison of Efficacy and Safety of Atezolizumab Plus Bevacizumab and Lenvatinib as First-Line Therapy for Unresectable Hepatocellular Carcinoma: A Propensity Score Matching Analysis. Target. Oncol. 2022, 17, 643–653. [Google Scholar] [CrossRef]
- Pei, Y.; Li, W.; Wang, Z.; Liu, J. Successful conversion therapy for unresectable hepatocellular carcinoma is getting closer: A systematic review and meta-analysis. Front. Oncol. 2022, 12, 978823. [Google Scholar] [CrossRef]
- Li, W.; Pei, Y.; Wang, Z.; Liu, J. Efficacy of transarterial chemoembolization monotherapy or combination conversion therapy in unresectable hepatocellular carcinoma: A systematic review and meta-analysis. Front. Oncol. 2022, 12, 930868. [Google Scholar] [CrossRef] [PubMed]
- Li, B.; Qiu, J.; Zheng, Y.; Shi, Y.; Zou, R.; He, W.; Yuan, Y.; Zhang, Y.; Wang, C.; Qiu, Z.; et al. Conversion to Resectability Using Transarterial Chemoembolization Combined with Hepatic Arterial Infusion Chemotherapy for Initially Unresectable Hepatocellular Carcinoma. Ann. Surg. Open 2021, 2, e057. [Google Scholar] [CrossRef] [PubMed]
- Li, X.; Chen, J.; Wang, X.; Bai, T.; Lu, S.; Wei, T.; Tang, Z.; Huang, C.; Zhang, B.; Liu, B.; et al. Outcomes and prognostic factors in initially unresectable hepatocellular carcinoma treated using conversion therapy with lenvatinib and TACE plus PD-1 inhibitors. Front. Oncol. 2023, 13, 1110689. [Google Scholar] [CrossRef] [PubMed]
- Lin, K.-Y.; Lin, Z.-W.; Chen, Q.-J.; Luo, L.-P.; Zhang, J.-X.; Chen, J.-H.; Wang, K.; Tai, S.; Zhang, Z.-B.; Wang, S.-F.; et al. Perioperative safety, oncologic outcome, and risk factors of salvage liver resection for initially unresectable hepatocellular carcinoma converted by transarterial chemoembolization plus tyrosine kinase inhibitor and anti-PD-1 antibody: A retrospective mu. Hepatol. Int. 2023, 17, 1477–1489. [Google Scholar] [CrossRef] [PubMed]
- Luo, L.; He, Y.; Zhu, G.; Xiao, Y.; Song, S.; Ge, X.; Wang, T.; Xie, J.; Deng, W.; Hu, Z.; et al. Hepatectomy after Conversion Therapy for Initially Unresectable HCC: What is the Difference? J. Hepatocell. Carcinoma 2022, 9, 1353–1368. [Google Scholar] [CrossRef] [PubMed]
- Zhu, X.-D.; Huang, C.; Shen, Y.-H.; Xu, B.; Ge, N.-L.; Ji, Y.; Qu, X.-D.; Chen, L.; Chen, Y.; Li, M.-L.; et al. Hepatectomy after Conversion Therapy Using Tyrosine Kinase Inhibitors Plus Anti-PD-1 Antibody Therapy for Patients with Unresectable Hepatocellular Carcinoma. Ann. Surg. Oncol. 2023, 30, 2782–2790. [Google Scholar] [CrossRef] [PubMed]
- Cheng, A.L.; Qin, S.; Ikeda, M.; Galle, P.R.; Ducreux, M.; Kim, T.Y.; Lim, H.Y.; Kudo, M.; Breder, V.; Merle, P.; et al. Updated efficacy and safety data from IMbrave150: Atezolizumab plus bevacizumab vs. sorafenib for unresectable hepatocellular carcinoma. J. Hepatol. 2022, 76, 862–873. [Google Scholar] [CrossRef] [PubMed]
- Finn, R.S.; Qin, S.; Ikeda, M.; Galle, P.R.; Ducreux, M.; Kim, T.-Y.; Kudo, M.; Breder, V.; Merle, P.; Kaseb, A.O.; et al. Atezolizumab plus Bevacizumab in Unresectable Hepatocellular Carcinoma. N. Engl. J. Med. 2020, 382, 1894–1905. [Google Scholar] [CrossRef]
- Fulgenzi, C.A.M.; Cheon, J.; D’Alessio, A.; Nishida, N.; Ang, C.; Marron, T.U.; Wu, L.; Saeed, A.; Wietharn, B.; Cammarota, A.; et al. Reproducible safety and efficacy of atezolizumab plus bevacizumab for HCC in clinical practice: Results of the AB-real study. Eur. J. Cancer 2022, 175, 204–213. [Google Scholar] [CrossRef]
- Singal, A.G.; Llovet, J.M.; Yarchoan, M.; Mehta, N.; Heimbach, J.K.; Dawson, L.A.; Jou, J.H.; Kulik, L.M.; Agopian, V.G.; Marrero, J.A.; et al. AASLD Practice Guidance on prevention, diagnosis, and treatment of hepatocellular carcinoma. Hepatology 2023, 78, 1922–1965. [Google Scholar] [CrossRef]
- Qin, S.; Chen, M.; Cheng, A.L.; Kaseb, A.O.; Kudo, M.; Lee, H.C.; Yopp, A.C.; Zhou, J.; Wang, L.; Wen, X.; et al. Atezolizumab plus bevacizumab versus active surveillance in patients with resected or ablated high-risk hepatocellular carcinoma (IMbrave050): A randomised, open-label, multicentre, phase 3 trial. Lancet 2023, 402, 1835–1847. [Google Scholar] [CrossRef]
- Huang, D.Q.; Singal, A.G.; Kono, Y.; Tan, D.J.H.; El-Serag, H.B.; Loomba, R. Changing global epidemiology of liver cancer from 2010 to 2019: NASH is the fastest growing cause of liver cancer. Cell Metab. 2022, 34, 969–977.e962. [Google Scholar] [CrossRef]
- Mathurin, P.; de Zélicourt, M.; Laurendeau, C.; Dhaoui, M.; Kelkouli, N.; Blanc, J.F. Treatment patterns, risk factors and outcomes for patients with newly diagnosed hepatocellular carcinoma in France: A retrospective database analysis. Clin. Res. Hepatol. Gastroenterol. 2023, 47, 102124. [Google Scholar] [CrossRef] [PubMed]
- Myers, S.; Neyroud-Caspar, I.; Spahr, L.; Gkouvatsos, K.; Fournier, E.; Giostra, E.; Magini, G.; Frossard, J.-L.; Bascaron, M.-E.; Vernaz, N.; et al. NAFLD and MAFLD as emerging causes of HCC: A populational study. JHEP Rep. 2021, 3, 100231. [Google Scholar] [CrossRef] [PubMed]
- Younossi, Z.; Stepanova, M.; Ong, J.P.; Jacobson, I.M.; Bugianesi, E.; Duseja, A.; Eguchi, Y.; Wong, V.W.; Negro, F.; Yilmaz, Y.; et al. Nonalcoholic Steatohepatitis Is the Fastest Growing Cause of Hepatocellular Carcinoma in Liver Transplant Candidates. Clin. Gastroenterol. Hepatol. 2019, 17, 748–755.e743. [Google Scholar] [CrossRef] [PubMed]
- Zhang, C.H.; Cheng, Y.; Zhang, S.; Fan, J.; Gao, Q. Changing epidemiology of hepatocellular carcinoma in Asia. Liver Int. 2022, 42, 2029–2041. [Google Scholar] [CrossRef] [PubMed]
- Kim, M.N.; Han, K.; Yoo, J.; Hwang, S.G.; Zhang, X.; Ahn, S.H. Diabetic MAFLD is associated with increased risk of hepatocellular carcinoma and mortality in chronic viral hepatitis patients. Int. J. Cancer 2023, 153, 1448–1458. [Google Scholar] [CrossRef] [PubMed]
- Vitale, A.; Svegliati-Baroni, G.; Ortolani, A.; Cucco, M.; Dalla Riva, G.V.; Giannini, E.G.; Piscaglia, F.; Rapaccini, G.; Di Marco, M.; Caturelli, E.; et al. Epidemiological trends and trajectories of MAFLD-associated hepatocellular carcinoma 2002–2033: The ITA.LI.CA database. Gut 2023, 72, 141–152. [Google Scholar] [CrossRef] [PubMed]
- Piscaglia, F.; Svegliati-Baroni, G.; Barchetti, A.; Pecorelli, A.; Marinelli, S.; Tiribelli, C.; Bellentani, S. Clinical patterns of hepatocellular carcinoma in nonalcoholic fatty liver disease: A multicenter prospective study. Hepatology 2016, 63, 827–838. [Google Scholar] [CrossRef] [PubMed]
- Tariciotti, L.; D’Ugo, S.; Manzia, T.M.; Tognoni, V.; Sica, G.; Gentileschi, P.; Tisone, G. Combined liver transplantation and sleeve gastrectomy for end-stage liver disease in a bariatric patient: First European case-report. Int. J. Surg. Case Rep. 2016, 28, 38–41. [Google Scholar] [CrossRef]
- Conci, S.; Cipriani, F.; Donadon, M.; Marchitelli, I.; Ardito, F.; Famularo, S.; Perri, P.; Iaria, M.; Ansaloni, L.; Zanello, M.; et al. Hepatectomy for Metabolic Associated Fatty Liver Disease (MAFLD) related HCC: Propensity case-matched analysis with viral- and alcohol-related HCC. Eur. J. Surg. Oncol. 2022, 48, 103–112. [Google Scholar] [CrossRef]
- Koh, Y.X.; Tan, H.J.; Liew, Y.X.; Syn, N.; Teo, J.Y.; Lee, S.Y.; Goh, B.K.P.; Goh, G.B.B.; Chan, C.Y. Liver Resection for Nonalcoholic Fatty Liver Disease-Associated Hepatocellular Carcinoma. J. Am. Coll. Surg. 2019, 229, 467–478.e461. [Google Scholar] [CrossRef] [PubMed]
- Tan, D.J.H.; Ng, C.H.; Lin, S.Y.; Pan, X.H.; Tay, P.; Lim, W.H.; Teng, M.; Syn, N.; Lim, G.; Yong, J.N.; et al. Clinical characteristics, surveillance, treatment allocation, and outcomes of non-alcoholic fatty liver disease-related hepatocellular carcinoma: A systematic review and meta-analysis. Lancet Oncol. 2022, 23, 521–530. [Google Scholar] [CrossRef]
- Kanwal, F.; Kramer, J.R.; Mapakshi, S.; Natarajan, Y.; Chayanupatkul, M.; Richardson, P.A.; Li, L.; Desiderio, R.; Thrift, A.P.; Asch, S.M.; et al. Risk of Hepatocellular Cancer in Patients with Non-Alcoholic Fatty Liver Disease. Gastroenterology 2018, 155, 1828–1837.e1822. [Google Scholar] [CrossRef] [PubMed]
- Hanif, H.; Ali, M.J.; Susheela, A.T.; Khan, I.W.; Luna-Cuadros, M.A.; Khan, M.M.; Lau, D.T. Update on the applications and limitations of alpha-fetoprotein for hepatocellular carcinoma. World J. Gastroenterol. 2022, 28, 216–229. [Google Scholar] [CrossRef]
- Ahn, J.C.; Teng, P.C.; Chen, P.J.; Posadas, E.; Tseng, H.R.; Lu, S.C.; Yang, J.D. Detection of Circulating Tumor Cells and Their Implications as a Biomarker for Diagnosis, Prognostication, and Therapeutic Monitoring in Hepatocellular Carcinoma. Hepatology 2021, 73, 422–436. [Google Scholar] [CrossRef]
- Endo, Y.; Moazzam, Z.; Woldesenbet, S.; Lima, H.A.; Alaimo, L.; Munir, M.M.; Shaikh, C.F.; Yang, J.; Azap, L.; Katayama, E.; et al. Hospital Volume and Textbook Outcomes in Minimally Invasive Hepatectomy for Hepatocellular Carcinoma. J. Gastrointest. Surg. 2023, 27, 956–964. [Google Scholar] [CrossRef]
- Pu, J.L.; Xu, X.; Chen, L.L.; Li, C.; Jia, H.D.; Fan, Z.Q.; Li, J.D.; Guan, M.C.; Liang, Y.J.; Zhou, Y.H.; et al. Postoperative infectious complications following laparoscopic versus open hepatectomy for hepatocellular carcinoma: A multicenter propensity score analysis of 3876 patients. Int. J. Surg. 2023, 109, 2267–2275. [Google Scholar] [CrossRef]
- Sotiropoulos, G.C.; Prodromidou, A.; Kostakis, I.D.; Machairas, N. Meta-analysis of laparoscopic vs open liver resection for hepatocellular carcinoma. Updates Surg. 2017, 69, 291–311. [Google Scholar] [CrossRef]
- Wang, S.; Ye, G.; Wang, J.; Xu, S.; Ye, Q.; Ye, H. Laparoscopic versus open liver resection for hepatocellular carcinoma in elderly patients: A systematic review and meta-analysis of propensity score-matched studies. Front. Oncol. 2022, 12, 939877. [Google Scholar] [CrossRef]
- Giuliante, F.; Ratti, F.; Panettieri, E.; Mazzaferro, V.; Guglielmi, A.; Ettorre, G.M.; Gruttadauria, S.; Di Benedetto, F.; Cillo, U.; De Carlis, L.; et al. Short and long-term outcomes after minimally invasive liver resection for single small hepatocellular carcinoma: An analysis of 714 patients from the IGoMILS (Italian group of minimally invasive liver surgery) registry. HPB 2023, 25, 674–683. [Google Scholar] [CrossRef] [PubMed]
- Lippert, T.; Lim-Dy, A.; Sucandy, I. The future of minimally invasive liver resection for hepatocellular carcinoma BCLC stage 0-A. Hepatobiliary Surg. Nutr. 2023, 12, 601–603. [Google Scholar] [CrossRef] [PubMed]
- Di Benedetto, F.; Magistri, P.; Di Sandro, S.; Sposito, C.; Oberkofler, C.; Brandon, E.; Samstein, B.; Guidetti, C.; Papageorgiou, A.; Frassoni, S.; et al. Safety and Efficacy of Robotic vs Open Liver Resection for Hepatocellular Carcinoma. JAMA Surg. 2023, 158, 46–54. [Google Scholar] [CrossRef] [PubMed]
- Angelico, R.; Siragusa, L.; Serenari, M.; Scalera, I.; Kauffman, E.; Lai, Q.; Vitale, A. Rescue liver transplantation after post-hepatectomy acute liver failure: A systematic review and pooled analysis. Transplant. Rev. 2023, 37, 100773. [Google Scholar] [CrossRef] [PubMed]
- Kato, Y.; Sugioka, A.; Kojima, M.; Mii, S.; Uchida, Y.; Iwama, H.; Mizumoto, T.; Takahara, T.; Uyama, I. Minimally Invasive Anatomic Liver Resection for Hepatocellular Carcinoma Using the Extrahepatic Glissonian Approach: Surgical Techniques and Comparison of Outcomes with the Open Approach and between the Laparoscopic and Robotic Approaches. Cancers 2023, 15, 2219. [Google Scholar] [CrossRef] [PubMed]
- Cheung, T.T.; Dai, W.C.; Tsang, S.H.; Chan, A.C.; Chok, K.S.; Chan, S.C.; Lo, C.M. Pure Laparoscopic Hepatectomy Versus Open Hepatectomy for Hepatocellular Carcinoma in 110 Patients with Liver Cirrhosis: A Propensity Analysis at a Single Center. Ann. Surg. 2016, 264, 612–620. [Google Scholar] [CrossRef]
- Kaibori, M.; Yoshii, K.; Umeda, Y.; Yagi, T.; Okabayashi, T.; Sui, K.; Mori, A.; Hamaguchi, Y.; Kajiyama, K.; Hokuto, D.; et al. Surgical Outcomes of Laparoscopic versus Open Hepatectomy for Left Hepatocellular Carcinoma: Propensity Score Analyses Using Retrospective Japanese and Korean Individual Patient Data. Liver Cancer 2023, 12, 32–43. [Google Scholar] [CrossRef]
- Goh, E.L.; Chidambaram, S.; Ma, S. Laparoscopic vs open hepatectomy for hepatocellular carcinoma in patients with cirrhosis: A meta-analysis of the long-term survival outcomes. Int. J. Surg. 2018, 50, 35–42. [Google Scholar] [CrossRef]
- Jiang, S.; Wang, Z.; Ou, M.; Pang, Q.; Fan, D.; Cui, P. Laparoscopic Versus Open Hepatectomy in Short- and Long-Term Outcomes of the Hepatocellular Carcinoma Patients with Cirrhosis: A Systematic Review and Meta-Analysis. J. Laparoendosc. Adv. Surg. Tech. A 2019, 29, 643–654. [Google Scholar] [CrossRef] [PubMed]
- Kabir, T.; Tan, Z.Z.; Syn, N.L.; Wu, E.; Lin, J.D.; Zhao, J.J.; Tan, A.Y.H.; Hui, Y.; Kam, J.H.; Goh, B.K.P. Laparoscopic versus open resection of hepatocellular carcinoma in patients with cirrhosis: Meta-analysis. Br. J. Surg. 2021, 109, 21–29. [Google Scholar] [CrossRef] [PubMed]
- Kamarajah, S.K.; Gujjuri, R.R.; Hilal, M.A.; Manas, D.M.; White, S.A. Does minimally invasive liver resection improve long-term survival compared to open resection for hepatocellular carcinoma? A systematic review and meta-analysis. Scand. J. Surg. 2022, 111, 14574969211042455. [Google Scholar] [CrossRef] [PubMed]
- Pan, Y.; Xia, S.; Cai, J.; Chen, K.; Cai, X. Efficacy of Laparoscopic Hepatectomy versus Open Surgery for Hepatocellular Carcinoma with Cirrhosis: A Meta-analysis of Case-Matched Studies. Front. Oncol. 2021, 11, 652272. [Google Scholar] [CrossRef]
- Liao, K.; Yang, K.; Cao, L.; Lu, Y.; Zheng, B.; Li, X.; Wang, X.; Li, J.; Chen, J.; Zheng, S. Laparoscopic Anatomical Versus Non-anatomical hepatectomy in the Treatment of Hepatocellular Carcinoma: A randomised controlled trial. Int. J. Surg. 2022, 102, 106652. [Google Scholar] [CrossRef]
- Liu, F.; Wang, H.; Ma, W.; Li, J.; Liu, Y.; Tang, S.; Li, K.; Jiang, P.; Yang, Z.; He, Y.; et al. Short- and Long-Term Outcomes of Indocyanine Green Fluorescence Navigation- Versus Conventional-Laparoscopic Hepatectomy for Hepatocellular Carcinoma: A Propensity Score-Matched, Retrospective, Cohort Study. Ann. Surg. Oncol. 2023, 30, 1991–2002. [Google Scholar] [CrossRef]
- D’Hondt, M.; Tamby, E.; Boscart, I.; Turcotte, S.; Parmentier, I.; Pottel, H.; Lapointe, R.; Ovaere, S.; Vansteenkiste, F.; Vandenbroucke-Menu, F. Laparoscopic versus open parenchymal preserving liver resections in the posterosuperior segments: A case-matched study. Surg. Endosc. 2018, 32, 1478–1485. [Google Scholar] [CrossRef]
- Allaire, M.; Goumard, C.; Lim, C.; Le Cleach, A.; Wagner, M.; Scatton, O. New frontiers in liver resection for hepatocellular carcinoma. JHEP Rep. 2020, 2, 100134. [Google Scholar] [CrossRef]
- Hobeika, C.; Nault, J.C.; Barbier, L.; Schwarz, L.; Lim, C.; Laurent, A.; Gay, S.; Salamé, E.; Scatton, O.; Soubrane, O.; et al. Influence of surgical approach and quality of resection on the probability of cure for early-stage HCC occurring in cirrhosis. JHEP Rep. 2020, 2, 100153. [Google Scholar] [CrossRef]
- Prodeau, M.; Drumez, E.; Duhamel, A.; Vibert, E.; Farges, O.; Lassailly, G.; Mabrut, J.Y.; Hardwigsen, J.; Régimbeau, J.M.; Soubrane, O.; et al. An ordinal model to predict the risk of symptomatic liver failure in patients with cirrhosis undergoing hepatectomy. J. Hepatol. 2019, 71, 920–929. [Google Scholar] [CrossRef] [PubMed]
- Berardi, G.; Ivanics, T.; Sapisochin, G.; Ratti, F.; Sposito, C.; Nebbia, M.; D’Souza, D.M.; Pascual, F.; Dogeas, E.; Tohme, S.; et al. Minimally Invasive Versus Open Liver Resections for Hepatocellular Carcinoma in Patients with Metabolic Syndrome. Ann. Surg. 2023, 278, e1041–e1047. [Google Scholar] [CrossRef]
- Berardi, G.; Morise, Z.; Sposito, C.; Igarashi, K.; Panetta, V.; Simonelli, I.; Kim, S.; Goh, B.K.P.; Kubo, S.; Tanaka, S.; et al. Development of a nomogram to predict outcome after liver resection for hepatocellular carcinoma in Child-Pugh B cirrhosis. J. Hepatol. 2020, 72, 75–84. [Google Scholar] [CrossRef] [PubMed]
- Berardi, G.; Ratti, F.; Sposito, C.; Nebbia, M.; D’Souza, D.M.; Pascual, F.; Dogeas, E.; Tohme, S.; D’Amico, F.E.; Alessandris, R.; et al. Model to predict major complications following liver resection for HCC in patients with metabolic syndrome. Hepatology 2023, 77, 1527–1539. [Google Scholar] [CrossRef] [PubMed]
- Troisi, R.I.; Berardi, G.; Morise, Z.; Cipriani, F.; Ariizumi, S.; Sposito, C.; Panetta, V.; Simonelli, I.; Kim, S.; Goh, B.K.P.; et al. Laparoscopic and open liver resection for hepatocellular carcinoma with Child-Pugh B cirrhosis: Multicentre propensity score-matched study. Br. J. Surg. 2021, 108, 196–204. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, Y.; Aikawa, M.; Kato, T.; Takase, K.; Watanabe, Y.; Okada, K.; Okamoto, K.; Koyama, I. Influence of Child-Pugh B7 and B8/9 cirrhosis on laparoscopic liver resection for hepatocellular carcinoma: A retrospective cohort study. Surg. Endosc. 2023, 37, 1316–1333. [Google Scholar] [CrossRef] [PubMed]
- Vitale, A.; Peck-Radosavljevic, M.; Giannini, E.G.; Vibert, E.; Sieghart, W.; Van Poucke, S.; Pawlik, T.M. Personalized treatment of patients with very early hepatocellular carcinoma. J. Hepatol. 2017, 66, 412–423. [Google Scholar] [CrossRef] [PubMed]
- Cillo, U.; Noaro, G.; Vitale, A.; Neri, D.; D’Amico, F.; Gringeri, E.; Farinati, F.; Vincenzi, V.; Vigo, M.; Zanus, G. Laparoscopic microwave ablation in patients with hepatocellular carcinoma: A prospective cohort study. HPB 2014, 16, 979–986. [Google Scholar] [CrossRef] [PubMed]
- Lanari, J.; Caregari, S.; Billato, I.; Gringeri, E.; D’Amico, F.; Gemo, G.; Bassi, D.; D’Amico, F.E.; Boetto, R.; Bertacco, A.; et al. Textbook Outcome of Laparoscopic Microwave Ablation for Hepatocellular Carcinoma. Cancers 2023, 15, 436. [Google Scholar] [CrossRef] [PubMed]
- Vitale, A.; Lai, Q. Selection of patients with hepatocellular cancer: A difficult balancing between equity, utility, and benefit. Transl. Gastroenterol. Hepatol. 2017, 2, 75. [Google Scholar] [CrossRef]
- Vitale, A.; Scolari, F.; Bertacco, A.; Gringeri, E.; D’Amico, F.; Bassi, D.; D’Amico, F.E.; Angeli, P.; Burra, P.; Lai, Q.; et al. Sustained Complete Response after Biological Downstaging in Patients with Hepatocellular Carcinoma: XXL-Like Prioritization for Liver Transplantation or “Wait and See” Strategy? Cancers 2021, 13, 2406. [Google Scholar] [CrossRef]
- Manzia, T.M.; Trapani, S.; Nardi, A.; Ricci, A.; Lenci, I.; Milana, M.; Angelico, R.; De Feo, T.M.; Agnes, S.; Andorno, E.; et al. Temporal trends of waitlistings for liver transplantation in Italy: The ECALITA (Evolution of IndiCAtion in LIver transplantation in ITAly) registry study. Dig. Liver Dis. 2022, 54, 1664–1671. [Google Scholar] [CrossRef] [PubMed]
- Manzia, T.M.; Angelico, R.; Toti, L.; Bellini, M.I.; Sforza, D.; Palmieri, G.; Orlando, G.; Tariciotti, L.; Angelico, M.; Tisone, G. Long-term, maintenance MMF monotherapy improves the fibrosis progression in liver transplant recipients with recurrent hepatitis C. Transpl. Int. 2011, 24, 461–468. [Google Scholar] [CrossRef]
- Mazzaferro, V.; Citterio, D.; Bhoori, S.; Bongini, M.; Miceli, R.; De Carlis, L.; Colledan, M.; Salizzoni, M.; Romagnoli, R.; Antonelli, B.; et al. Liver transplantation in hepatocellular carcinoma after tumour downstaging (XXL): A randomised, controlled, phase 2b/3 trial. Lancet Oncol. 2020, 21, 947–956. [Google Scholar] [CrossRef] [PubMed]
- Lai, Q.; Vitale, A.; Iesari, S.; Finkenstedt, A.; Mennini, G.; Spoletini, G.; Hoppe-Lotichius, M.; Vennarecci, G.; Manzia, T.M.; Nicolini, D.; et al. Intention-to-treat survival benefit of liver transplantation in patients with hepatocellular cancer. Hepatology 2017, 66, 1910–1919. [Google Scholar] [CrossRef] [PubMed]
- Levi Sandri, G.B.; Lai, Q.; Ravaioli, M.; Di Sandro, S.; Balzano, E.; Pagano, D.; Magistri, P.; Di Benedetto, F.; Rossi, M.; Gruttadauria, S.; et al. The Role of Salvage Transplantation in Patients Initially Treated with Open Versus Minimally Invasive Liver Surgery: An Intention-to-Treat Analysis. Liver Transpl. 2020, 26, 878–887. [Google Scholar] [CrossRef] [PubMed]
- Laurent, A.; Tayar, C.; Andréoletti, M.; Lauzet, J.Y.; Merle, J.C.; Cherqui, D. Laparoscopic liver resection facilitates salvage liver transplantation for hepatocellular carcinoma. J. Hepatobiliary Pancreat. Surg. 2009, 16, 310–314. [Google Scholar] [CrossRef] [PubMed]
- Rhu, J.; Kim, J.M.; Choi, G.S.; Kwon, C.H.D.; Joh, J.W.; Soubrane, O. Laparoscopy of hepatocellular carcinoma is helpful in minimizing intra-abdominal adhesion during salvage transplantation. Ann. Surg. Treat. Res. 2018, 95, 258–266. [Google Scholar] [CrossRef] [PubMed]
- Serenari, M.; Lenzi, J.; Cucchetti, A.; Cipriani, F.; Donadon, M.; Ardito, F.; Fazio, F.; Nicolini, D.; Iaria, M.; Famularo, S.; et al. The Effect of a Liver Transplant Program on the Outcomes of Resectable Hepatocellular Carcinoma: A Nationwide Multicenter Analysis. Ann. Surg. 2023, 277, 664–671. [Google Scholar] [CrossRef]
- Vitale, A.; Cabibbo, G.; Iavarone, M.; Viganò, L.; Pinato, D.J.; Ponziani, F.R.; Lai, Q.; Casadei-Gardini, A.; Celsa, C.; Galati, G.; et al. Personalised management of patients with hepatocellular carcinoma: A multiparametric therapeutic hierarchy concept. Lancet Oncol. 2023, 24, e312–e322. [Google Scholar] [CrossRef]
- Vitale, A.; Trevisani, F.; Farinati, F.; Cillo, U. Treatment of Hepatocellular Carcinoma in the Precision Medicine Era: From Treatment Stage Migration to Therapeutic Hierarchy. Hepatology 2020, 72, 2206–2218. [Google Scholar] [CrossRef]
- Trevisani, F.; Vitale, A.; Kudo, M.; Kulik, L.; Park, J.W.; Pinato, D.J.; Cillo, U. Merits and boundaries of the BCLC staging and treatment algorithm: Learning from the past to improve the future with a novel proposal. J. Hepatol. 2024; in press. [Google Scholar] [CrossRef] [PubMed]
Year | Author | Journal | Study Type | N° of Patients | Outcomes |
---|---|---|---|---|---|
2016 | Tan To Cheung et al. [49] | Annals of Surgery | Retrospective Propensity score matching | 110 MILS 330 OPEN | -Increased 1-, 3-, and 5-year overall survival (98.9%, 89.8%, and 83.7% in the laparoscopic group, and 94%, 79.3%, and 67.4% vin the open group) |
2018 | Goh et al. [51] | International Journal of Surgery | Meta-analysis (five non-randomized case-matched studies) | 276 MILS 612 OPEN | -Lower tumor recurrence -Increased 1-, 3-, and 5-year overall survival -Increased disease-free survival at 1 year |
2019 | Jiang et al. [52] | Journal of Lap and Advanced Surgical Techniques | Meta-analysis (17 non-randomized case-matched studies) | 798 MILS 1206 OPEN | -Increased 1-, 3-, and 5-year overall survival -Increased disease-free survival at 1 year -Decreased blood loss and transfusion rates -Decreased postoperative complications -Wider surgical margin -Decreased postoperative hospital stay -Decreased mortality |
2021 | Pan et al. [55] | Frontiers in Oncology | Meta-analysis (12 non-randomized case-matched studies) | 784 MILS 1191 OPEN | -Increased 1-, 3-, and 5-year overall survival -Decreased overall and major complications -Decreased porstoperative mortality -Decreased postoperative liver failure and ascites |
2021 | Kabir et al. [53] | British Journal of Surgery | Meta-analysis (11 non-randomized case-matched studies) | 690 MILS 928 OPEN | -A 16% reduction in the hazard ratio of death -Decreased length of stay -Decreased blood loss -Decreased overall and major complications |
2022 | Kaibori et al. [50] | Liver Cancer | Retrospective Propensity score analysis | 146 MILS 807 OPEN | -Increased overall disease-free survival -Increased disease-free and overall survival for sub-group of patients with single HCC or >4 cm. -Decreased postoperative complictions -Decreased postoperative hepatic decompensation |
2022 | Kamarajah et al. [54] | Scandinavian Journal of Surgery | Meta-analysis (50 non-randomized studies) | 4071 MILS 9660 OPEN | -Increased 3-year disease-specific mortality -Increased 5-year all-cause mortality |
2023 | Di Benedetto et al. [46] | JAMA Surg | Retrospective Propensity score matching | 106 MILS (robotic) 106 OPEN | -Decreased post-hepatectomy liver failure -Decreased hospital stay -Decreased admissions to intensive care |
2023 | Kato et al. [48] | Cancers | Retrospective Propensity score matching | 91 MILS 91 OPEN | -Longer overall survival and recurrence-free survival -Decreased blood loss and transfusion rates -Decreased 90-day morbidity and mortality -Decreased bile leak -Decreased postoperative hospital stay |
Year | Author | Journal | Study Type | N° of Patients | Results |
---|---|---|---|---|---|
2019 | Prodeau et al. [61] | Journal of Hepatology | Prospective observational study | 112 MILS 231 OPEN | MILS was independently inversely correlated to the likelihood of postoperative liver failure. |
2020 | Hobeika et al. [60] | JHEP Reports | Prospective observational study | 267 MILS 158 OPEN | MILS was independently correlated to textbook outcomes. |
2020 | Berardi et al. [63] | Journal of Hepatology | Retrospective study | 122 MILS 131 OPEN | MILS was independently inversely correlated to major morbidity in Child-B cirrhosis. |
2023 | Berardi et al. [64] | Hepatology | Retrospective study | 445 MILS 642 OPEN | MILS was independently inversely correlated to major morbidity in patients with metabolic syndrome. |
Year | Author | Journal | Study Type | N° of Patients | Outcomes |
---|---|---|---|---|---|
2009 | Laurent et al. [77] | Journal of Hepatobiliary and Pancreatic Surgery | Retrospective monocentric study | 12 MILS 12 OPEN | LT after MILS was correlated to reduced operative time, blood loss, and transfusion requirements. |
2018 | Rhu et al. [78] | Annals of Surgical Treatment and Research | Retrospective monocentric study | 10 MILS 52 OPEN | MILS reduced intra-abdominal adhesions during salvage LT. |
2020 | Levi Sandri et al. [76] | Liver Transplantation | Retrospective multicentric study | 44 MILS 167 OPEN | MILS was independently correlated to a reduced risk of delisting, post-transplant death, and HCC recurrence. |
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Vitale, A.; Angelico, R.; Sensi, B.; Lai, Q.; Kauffmann, E.; Scalera, I.; Serenari, M.; Ginesini, M.; Romano, P.; Furlanetto, A.; et al. What Is the Role of Minimally Invasive Liver Surgery in Treating Patients with Hepatocellular Carcinoma on Cirrhosis? Cancers 2024, 16, 966. https://doi.org/10.3390/cancers16050966
Vitale A, Angelico R, Sensi B, Lai Q, Kauffmann E, Scalera I, Serenari M, Ginesini M, Romano P, Furlanetto A, et al. What Is the Role of Minimally Invasive Liver Surgery in Treating Patients with Hepatocellular Carcinoma on Cirrhosis? Cancers. 2024; 16(5):966. https://doi.org/10.3390/cancers16050966
Chicago/Turabian StyleVitale, Alessandro, Roberta Angelico, Bruno Sensi, Quirino Lai, Emanuele Kauffmann, Irene Scalera, Matteo Serenari, Michael Ginesini, Pierluigi Romano, Alessandro Furlanetto, and et al. 2024. "What Is the Role of Minimally Invasive Liver Surgery in Treating Patients with Hepatocellular Carcinoma on Cirrhosis?" Cancers 16, no. 5: 966. https://doi.org/10.3390/cancers16050966
APA StyleVitale, A., Angelico, R., Sensi, B., Lai, Q., Kauffmann, E., Scalera, I., Serenari, M., Ginesini, M., Romano, P., Furlanetto, A., & D’Amico, F., on behalf of the Italian Chapter of IHPBA (AICEP, Associazione Italiana di Chirurgia Epatobilio-Pancreatica). (2024). What Is the Role of Minimally Invasive Liver Surgery in Treating Patients with Hepatocellular Carcinoma on Cirrhosis? Cancers, 16(5), 966. https://doi.org/10.3390/cancers16050966