Abstract
Purposes
The indication of endoscopic (laparoscopic and thoracoscopic) hepatic resection (HR) has been expanded in the past decade because of its low invasiveness. However, the indications of endoscopic HR and radiofrequency ablation (RFA) have not yet been determined.
Methods
Among the 906 patients hospitalized for the initial treatment of hepatocellular carcinoma (HCC) between 2000 and 2017, 77 underwent endoscopic partial HR (E-pHR), and 94 underwent endoscopic RFA (E-RFA). We compared the short- and long-term outcomes between the E-pHR and E-RFA groups.
Results
The patients in the E-RFA group were characterized primarily by an impaired liver function. Among the patients with liver damage B or C, the overall survival (OS) in the E-pHR group was significantly worse than in the E-RFA group (3-year OS: 36% vs. 82%, p = 0.003).
Conclusion
E-RFA may be recommended for the initial treatment of HCC in patients with a severely impaired liver function. However, E-pHR should be avoided as the initial treatment of HCC in such patients.
Similar content being viewed by others
References
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136:E359–E386386.
Chen MS, Li JQ, Zheng Y, Guo RP, Liang HH, Zhang YQ, et al. A prospective randomized trial comparing percutaneous local ablative therapy and partial hepatectomy for small hepatocellular carcinoma. Ann Surg. 2006;243:321–8.
Hasegawa K, Makuuchi M, Takayama T, Kokudo N, Arii S, Okazaki M, et al. Surgical resection vs. percutaneous ablation for hepatocellular carcinoma: a preliminary report of the Japanese nationwide survey. J Hepatol. 2008;49:589–94.
Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008;359:378–90.
Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2009;10:25–34.
Meng MB, Cui YL, Lu Y, She B, Chen Y, Guan YS, et al. Transcatheter arterial chemoembolization in combination with radiotherapy for unresectable hepatocellular carcinoma: a systematic review and meta-analysis. Radiother Oncol. 2009;92:184–94.
Imai K, Beppu T, Chikamoto A, Mima K, Okabe H, Hayashi H, et al. Salvage treatment for local recurrence of hepatocellular carcinoma after local ablation therapy. Hepatol Res. 2014;44:E335–E34545.
Wang C, Wang H, Yang W, Hu K, Xie H, Hu KQ, et al. Multicenter randomized controlled trial of percutaneous cryoablation versus radiofrequency ablation in hepatocellular carcinoma. Hepatology (Baltimore, MD). 2015;61:1579–90.
Reich H, McGlynn F, DeCaprio J, Budin R. Laparoscopic excision of benign liver lesions. Obstet Gynecol. 1991;78:956–8.
Buell JF, Cherqui D, Geller DA, O'Rourke N, Iannitti D, Dagher I, et al. The international position on laparoscopic liver surgery: the Louisville Statement, 2008. Ann Surg. 2009;250:825–30.
Wakabayashi G. What has changed after the Morioka consensus conference 2014 on laparoscopic liver resection? Hepatobiliary Surg Nutr. 2016;5:281–9.
Cho JY, Han HS, Wakabayashi G, Soubrane O, Geller D, O'Rourke N, et al. Practical guidelines for performing laparoscopic liver resection based on the second international laparoscopic liver consensus conference. Surg Oncol. 2018;27:A5–9.
Bruix J, Sherman M. Management of hepatocellular carcinoma: an update. Hepatology (Baltimore, MD). 2011;53:1020–2.
Duan C, Liu M, Zhang Z, Ma K, Bie P. Radiofrequency ablation versus hepatic resection for the treatment of early-stage hepatocellular carcinoma meeting Milan criteria: a systematic review and meta-analysis. World J Surg Oncol. 2013;11:190.
Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology (Baltimore, MD). 2005;42:1208–36.
Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, et al. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol. 2001;35:421–30.
Makuuchi M, Kokudo N, Arii S, Futagawa S, Kaneko S, Kawasaki S, et al. Development of evidence-based clinical guidelines for the diagnosis and treatment of hepatocellular carcinoma in Japan. Hepatol Res. 2008;38:37–51.
Imai K, Beppu T, Chikamoto A, Doni K, Okabe H, Hayashi H, et al. Comparison between hepatic resection and radiofrequency ablation as first-line treatment for solitary small-sized hepatocellular carcinoma of 3 cm or less. Hepatol Res. 2013;43:853–64.
Liu JG, Wang YJ, Du Z. Radiofrequency ablation in the treatment of small hepatocellular carcinoma: a meta analysis. World J Gastroenterol. 2010;16:3450–6.
Nitta H, Nakagawa S, Kaida T, Arima K, Higashi T, Taki K, et al. Pre-treatment double- or triple-positive tumor markers are predictive of a poor outcome for patients undergoing radiofrequency ablation for hepatocellular carcinoma. Surg Today. 2017;47:375–84.
Zhou Y, Zhao Y, Li B, Xu D, Yin Z, Xie F, et al. Meta-analysis of radiofrequency ablation versus hepatic resection for small hepatocellular carcinoma. BMC Gastroenterol. 2010;10:78.
Ito T, Tanaka S, Iwai S, Takemura S, Hagihara A, Uchida-Kobayashi S, et al. Outcomes of laparoscopic hepatic resection versus percutaneous radiofrequency ablation for hepatocellular carcinoma located at the liver surface: a case-control study with propensity score matching. Hepatol Res. 2016;46:565–74.
Lai EC, Tang CN. Radiofrequency ablation versus hepatic resection for hepatocellular carcinoma within the Milan criteria—a comparative study. Int J Surg. 2013;11:77–80.
Feng K, Yan J, Li X, Xia F, Ma K, Wang S, et al. A randomized controlled trial of radiofrequency ablation and surgical resection in the treatment of small hepatocellular carcinoma. J Hepatol. 2012;57:794–802.
Ueno S, Sakoda M, Kubo F, Hiwatashi K, Tateno T, Baba Y, et al. Surgical resection versus radiofrequency ablation for small hepatocellular carcinomas within the Milan criteria. J Hepatobiliary Pancreat Surg. 2009;16:359–66.
Hasegawa K, Kokudo N, Makuuchi M, Izumi N, Ichida T, Kudo M, et al. Comparison of resection and ablation for hepatocellular carcinoma: a cohort study based on a Japanese nationwide survey. J Hepatol. 2013;58:724–9.
Martin RC 2nd, Mbah NA, St Hill R, Kooby D, Weber S, Scoggins CR, et al. Laparoscopic versus open hepatic resection for hepatocellular carcinoma: improvement in outcomes and similar cost. World J Surg. 2015;39:1519–26.
Takahara T, Wakabayashi G, Beppu T, Aihara A, Hasegawa K, Gotohda N, et al. Long-term and perioperative outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci. 2015;22:721–7.
Franken C, Lau B, Putchakayala K, DiFronzo LA. Comparison of short-term outcomes in laparoscopic vs open hepatectomy. JAMA Surg. 2014;149:941–6.
Jiang B, Yan X, Zhang JH. Meta-analysis of laparoscopic versus open liver resection for hepatocellular carcinoma. Hepatol Res. 2018;48:635–63.
Santambrogio R, Barabino M, Bruno S, Mariani N, Maroni N, Bertolini E, et al. Surgical resection vs. ablative therapies through a laparoscopic approach for hepatocellular carcinoma: a comparative study. J Gastrointest Surg. 2017;22:650–60.
Yazici P, Akyuz M, Yigitbas H, Dural C, Okoh A, Aydin N, et al. A comparison of perioperative outcomes in elderly patients with malignant liver tumors undergoing laparoscopic liver resection versus radiofrequency ablation. Surg Endosc. 2017;31:1269–74.
Ikai I, Takayasu K, Omata M, Okita K, Nakanuma Y, Matsuyama Y, et al. A modified Japan Integrated Stage score for prognostic assessment in patients with hepatocellular carcinoma. J Gastroenterol. 2006;41:884–92.
Nanashima A, Sumida Y, Abo T, Shindou H, Fukuoka H, Takeshita H, et al. Modified Japan Integrated Staging is currently the best available staging system for hepatocellular carcinoma patients who have undergone hepatectomy. J Gastroenterol. 2006;41:250–6.
Ban D, Tanabe M, Ito H, Otsuka Y, Nitta H, Abe Y, et al. A novel difficulty scoring system for laparoscopic liver resection. J Hepatobiliary Pancreat Sci. 2014;21:745–53.
Yamao T, Imai K, Yamashita YI, Umezaki N, Tsukamoto M, Kitano Y, et al. Thoracoscopic surgery for hepatocellular carcinoma located in the hepatic dome: technical aspect and oncological results. Asian J Endosc Surg. 2019. https://doi.org/10.1111/ases.12755.
Doni K, Beppu T, Ishiko T, Chikamoto A, Hayashi H, Imai K, et al. Endoscopic radiofrequency ablation in elderly patients with hepatocellular carcinoma. Anticancer Res. 2015;35:3033–40.
Imai K, Beppu T, Nakayama Y, Ishiko T, Horino K, Komori H, et al. Preoperative prediction of poorly differentiated components in small-sized hepatocellular carcinoma for safe local ablation therapy. J Surg Oncol. 2009;100:121–6.
Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240:205–13.
Utsunomiya T, Shimada M, Kudo M, Ichida T, Matsui O, Izumi N, et al. Nationwide study of 4741 patients with non-B non-C hepatocellular carcinoma with special reference to the therapeutic impact. Ann Surg. 2014;259:336–45.
Kudo M, Chung H, Haji S, Osaki Y, Oka H, Seki T, et al. Validation of a new prognostic staging system for hepatocellular carcinoma: the JIS score compared with the CLIP score. Hepatology (Baltimore, MD). 2004;40:1396–405.
Yamao T, Imai K, Yamashita YI, Kaida T, Nakagawa S, Mima K, et al. Surgical treatment strategy for hepatocellular carcinoma in patients with impaired liver function: hepatic resection or radiofrequency ablation? HPB Off J Int Hepatol Pancreat Biliary Assoc. 2018;20:244–50.
Hori T, Nagata K, Hasuike S, Onaga M, Motoda M, Moriuchi A, et al. Risk factors for the local recurrence of hepatocellular carcinoma after a single session of percutaneous radiofrequency ablation. J Gastroenterol. 2003;38:977–81.
Park W, Chung YH, Kim JA, Jin YJ, Lee D, Shim JH, et al. Recurrences of hepatocellular carcinoma following complete remission by transarterial chemoembolization or radiofrequency therapy: focused on the recurrence patterns. Hepatol Res. 2013;43:1304–12.
Li L, Zhang J, Liu X, Li X, Jiao B, Kang T. Clinical outcomes of radiofrequency ablation and surgical resection for small hepatocellular carcinoma: a meta-analysis. J Gastroenterol Hepatol. 2012;27:51–8.
Liu L, Wang Z, Jiang S, Shao B, Liu J, Zhang S, et al. Perioperative allogenenic blood transfusion is associated with worse clinical outcomes for hepatocellular carcinoma: a meta-analysis. PLoS ONE ONE. 2013;8:e64261.
Xun Y, Tian H, Hu L, Yan P, Yang K, Guo T. The impact of perioperative allogeneic blood transfusion on prognosis of hepatocellular carcinoma after radical hepatectomy: a systematic review and meta-analysis of cohort studies. Medicine. 2018;97:e12911.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
Masayo Tsukamoto and co-authors declare that we have no conflicts of interest.
Ethical approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Declaration of Helsinki and its later amendments or comparable ethical standards.
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Tsukamoto, M., Imai, K., Yamashita, Yi. et al. Endoscopic hepatic resection and endoscopic radiofrequency ablation as initial treatments for hepatocellular carcinoma within the Milan criteria. Surg Today 50, 402–412 (2020). https://doi.org/10.1007/s00595-019-01903-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00595-019-01903-9