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Multimodal radiofrequency ablation versus laparoscopic hepatic resection for the treatment of primary hepatocellular carcinoma within Milan criteria in severely cirrhotic patients: long-term favorable outcomes over 10 years

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Abstract

Background

Less invasiveness is an important consideration for the treatment of hepatocellular carcinoma (HCC) especially in patients with severe cirrhosis.

Methods

Between April 2000 and September 2016, 100 patients with liver damage B underwent multimodal radiofrequency ablation (RFA; n = 62) or laparoscopic hepatic resection (Lap-HR; n = 38) for primary HCC as defined by the Milan criteria. We compared the operative outcomes and patients’ survival between the two groups.

Results

The RFA group showed worse liver functions as indicated by indocyanine green retention rate (32.9 vs. 22.4%; p < 0.0001) and serum albumin value (3.3 vs. 3.6 g/dl; p = 0.0029). As expected, RFA was less invasive, as indicated by the differences in operation time (166 vs. 288 min.; p < 0.0001) and blood loss (8 vs. 377 g; p < 0.0001). There was no significant difference in the morbidity rate between the two groups; however, the duration of hospital stay of the RFA group was significantly shorter (7 vs. 11 days; p = 0.0002). There were no significant between-group differences regarding overall or disease-free survival.

Conclusion

Multimodal RFA for HCC in patients with severe cirrhosis is associated with less invasiveness and shorter hospital stays, with no compromise in the patients’ survival. In patients with severe cirrhosis, it may be time to consider changing the standard treatment for primary HCC within the Milan criteria to multimodal RFA.

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References

  1. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359-86

    Article  CAS  PubMed  Google Scholar 

  2. Yamashita YI, Tsuijita E, Takeishi K, Ishida T, Ikegami T, Ezaki T, Maeda T, Utsunomiya T, Nagasue N, Shirabe K, Maehara Y (2014) Trends in surgical results of hepatic resection for hepatocellular carcinoma: 1000 consecutive cases over 20 years in a single institution. Am J Surg 207:890–896

    Article  PubMed  Google Scholar 

  3. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, Montalto F, Ammatuna M, Morabito A, Gennari L (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334:693–699

    Article  CAS  PubMed  Google Scholar 

  4. Yamashita Y, Ikeda T, Kurihara T, Yoshida Y, Takeishi K, Itoh S, Harimoto N, Kawanaka H, Shirabe K, Maehara Y (2014) Long-term favorable surgical results of laparoscopic hepatic resection for hepatocellular carcinoma in patients with cirrhosis: a single-center experience over a 10-year period. J Am Coll Surg 219:1117–1123

    Article  PubMed  Google Scholar 

  5. Ishiko T, Beppu T, Sugiyama S, Masuda T, Takahashi M, Komori H, Takamori H, Hirota M, Kanemitu K, Baba H (2008) Radiofrequency ablation with hand-assisted laparoscopic surgery for the treatment of hepatocellular carcinoma in the caudate lobe. Surg Laparosc Endosc Percutan Tech 18:272–276

    Article  PubMed  Google Scholar 

  6. Ishiko T, Beppu T, Chikamoto A, Imai K, Okabe H, Hayashi H, Nitta H, Baba H (2013) Thoracoscopic local ablation with diaphragmatic incision method for liver surface tumor in the hepatic dome. Surg Laparosc Endosc Percutan Tech 23(4):415–418. https://doi.org/10.1097/SLE.0b013e31828e3bba

    Article  PubMed  Google Scholar 

  7. Imai K, Beppu T, Chikamoto A, Mima K, Okabe H, Hayashi H, Nitta H, Ishiko T, Baba H. Salvage treatment for local recurrence of hepatocellular carcinoma after local ablation therapy. Hepatol Res 44: E335-45, 2014

    Article  PubMed  Google Scholar 

  8. European Association For The Study Of The Liver; European Organisation For Research And Treatment Of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56: 908–43, 2012

    Article  Google Scholar 

  9. Makuuchi M, Kokudo N, Arii S, Futagawa S, Kaneko S, Kawasaki S, Matsuyama Y, Okazaki M, Okita K, Omata M, Saida Y, Takayama T, Yamaoka Y (2008) Development of evidence-based clinical guidelines for the diagnosis and treatment of hepatocellular carcinoma in Japan. Hepatol Res 38:37–51

    Article  PubMed  Google Scholar 

  10. Wang Y, Luo Q, Li Y, Deng S, Wei S, Li X (2014) Radiofrequency ablation versus hepatic resection for small hepatocellular carcinomas: a meta-analysis of randomized and nonrandomized controlled trials. PLoS ONE 9:e84484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yamashita Y, Taketomi A, Itoh S, Kitagawa D, Kayashima H, Harimoto N, Tsujita E, Kuroda Y, Maehara Y (2017) Longterm favorable results of limited hepatic resections for patients with hepatocellular carcinoma: 20 years of experience. J Am Coll Surg 205:19–26

    Article  Google Scholar 

  12. Yamashita Y, Yoshida Y, Kurihara T, Itoh S, Harimoto N, Ikegami T, Yoshizumi T, Uchiyama H, Shirabe K (2015) Maehara Y. Surgical results for recurrent hepatocellular carcinoma after curative hepatectomy: Repeat hepatectomy versus salvage living donor liver transplantation. Liver Transpl 21:961–968

    Article  PubMed  Google Scholar 

  13. Doi K, Beppu T, Ishiko T, Chikamoto A, Hayashi H, Imai K, Nitta H, Baba Y, Masuda T, Okabe K, Kuramoto M, Kudo K, Ogata K, Ohchi T, Takamori H, Kikuchi K, Baba H (2015) Endoscopic radiofrequency ablation in elderly patients with hepatocellular carcinoma. Anticancer Res 35:3033–3040

    PubMed  Google Scholar 

  14. Imai K, Beppu T, Chikamoto A, Doi K, Okabe H, Hayashi H, Nitta H, Ishiko T, Takamori H, Baba H. Comparison between hepatic resection and radiofrequency ablation as first-line treatment for solitary small-sized hepatocellular carcinoma of 3 cm or less. Hepatol Res 43: 853–64, 2013

    Article  PubMed  Google Scholar 

  15. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, de Santibañes E, Pekolj J, Slankamenac K, Bassi C, Graf R, Vonlanthen R, Padbury R, Cameron JL, Makuuchi M. The Clavien-Dindo classification of surgical complications: 5-year experience. Ann Surg 250: 187–96, 2009

    Article  PubMed  Google Scholar 

  16. Yamashita Y, Shirabe K, Tsuijita E, Takeishi K, Ikegami T, Yoshizumi T, Soejima Y, Ikeda T, Utsunomiya T, Maehara Y (2013) Third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery 154:1038–1045

    Article  PubMed  Google Scholar 

  17. Kanematsu T, Furuta T, Takenaka K et al (1989) A 5-year experience of lipiodolization: selective regional chemotherapy for 200 patients with hepatocellular carcinoma. Hepatology 10:98–102

    Article  CAS  PubMed  Google Scholar 

  18. Kokudo N, Hasegawa K, Akahane M, Igaki H, Izumi N, Ichida T, Uemoto S, Kaneko S, Kawasaki S, Ku Y, Kudo M, Kubo S, Takayama T, Tateishi R, Fukuda T, Matsui O, Matsuyama Y, Murakami T, Arii S, Okazaki M, Makuuchi M. Evidence-based Clinical Practice Guidelines for Hepatocellular Carcinoma: The Japan Society of Hepatology 2013 update (3rd JSH-HCC Guidelines). Hepatol Res. 2015 https://doi.org/10.1111/hepr.12464

    Article  PubMed  Google Scholar 

  19. European Association For The Study Of The Liver1; European Organisation For Research And Treatment Of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56: 908–43, 2012

    Article  Google Scholar 

  20. Taketomi A, Kitagawa D, Itoh S, Harimoto N, Yamashita Y, Gion T, Shirabe K, Shimada M, Maehara Y (2007) Trends in morbidity and mortality after hepatic resection for hepatocellular carcinoma: an institute’s experience with 625 patients. J Am Coll Surg 204:580–587

    Article  PubMed  Google Scholar 

  21. Harimoto N, Shirabe K, Ikegami T, Yoshizumi T, Maeda T, Kajiyama K, Yamanaka T, Maehara Y (2015) Postoperative complications are predictive of poor prognosis in hepatocellular carcinoma. J Surg Res 199:470–477

    Article  PubMed  Google Scholar 

  22. Morise Z, Ciria R, Cherqui D, Chen KH, Belli G, Wakabayashi G. 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: 342–52, 2015

    Article  PubMed  Google Scholar 

  23. Liu Z, Zhou Y, Zhang P, Qin H. Meta-analysis of the therapeutic effect of hepatectomy versus radiofrequency ablation for the treatment of hepatocellular carcinoma. Surg Laparosc Endosc Percutan Tech 20: 130–40, 2010

    Article  PubMed  Google Scholar 

  24. Yamashita T, Honda M, Kaneko S (2011) Molecular mechanisms of hepatocarcinogenesis in chronic hepatitis C virus infection. J Gastroenterol Hepatol 26:960–964

    Article  CAS  PubMed  Google Scholar 

  25. Liver Cancer Study Group of Japan. General Rules for the Clinical and Pathological Study of Primary Liver Cancer, 3. Tokyo: Kanehara & Co., Ltd., 2010

    Google Scholar 

  26. Hemming AW, Scudamore CH, Shackleton CR, Pudek M, Erb SR (1992) Indocyanine green clearance as a predictor of successful hepatic resection in cirrhotic patients. Am J Surg 163:515–518

    Article  CAS  PubMed  Google Scholar 

  27. Chu KF, Dupuy DE (2014) Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer 14:199–208

    Article  CAS  PubMed  Google Scholar 

  28. Mima K, Hayashi H, Imai K, Kuroki H, Nakagawa S, Okabe H, Chikamoto A, Watanabe M, Beppu T, Baba H. High CD44s expression is associated with the EMT expression profile and intrahepatic dissemination of hepatocellular carcinoma after local ablation therapy. J Hepatobiliary Pancreat Sci 20: 429–434, 2013

    Article  PubMed  Google Scholar 

  29. Yamashita Y, Shirabe K, Aishima S, Maehara Y Predictors of microvascular invasion in hepatocellular carcinoma. Dig Dis. 33: 655–660, 2015. https://doi.org/10.1159/000438475.

    Article  PubMed  Google Scholar 

  30. Yamashita Y, Tsuijita E, Takeishi K, Fujiwara M, Kira S, Mori M, Aishima S, Taketomi A, Shirabe K, Ishida T, Maehara Y (2012) Predictors for microinvasion of small hepatocellular carcinoma ≤ 2 cm. Ann Surg Oncol 19:2027–2034

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Gastroenterological Surgery, Graduate School of Life Sciences, Kumamoto University, 1-1-1 Honjyo, Chuo-ku, Kumamoto, 860-8556, Japan

    Yo-ichi Yamashita, Katsunori Imai, Takayoshi Kaida, Takanobu Yamao, Masayo Tsukamoto, Shigeki Nakagawa, Hirohisa Okabe, Akira Chikamoto, Takatoshi Ishiko & Hideo Baba

  2. Department of Surgery and Science, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan

    Tomoharu Yoshizumi, Tetsuo Ikeda & Yoshihiko Maehara

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  1. Yo-ichi Yamashita
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  2. Katsunori Imai
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  3. Takayoshi Kaida
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  4. Takanobu Yamao
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Correspondence to Yo-ichi Yamashita.

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Yo-ichi Yamashita, Katsunori Imai, Takayoshi Kaida, Takanobu Yamao, Masayo Tsukamoto, Shigeki Nakagawa, Hirohisa Okabe, Akira Chikamoto, Takatoshi Ishiko, Tomoharu Yoshizumi, Tetsuo Ikeda, Yoshihiko Maehara, and Hideo Baba have no conflict of interest or financial ties to disclose.

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Yamashita, Yi., Imai, K., Kaida, T. et al. Multimodal radiofrequency ablation versus laparoscopic hepatic resection for the treatment of primary hepatocellular carcinoma within Milan criteria in severely cirrhotic patients: long-term favorable outcomes over 10 years. Surg Endosc 33, 46–51 (2019). https://doi.org/10.1007/s00464-018-6264-3

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