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Published in: Surgical Endoscopy 1/2019

01-01-2019

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

Authors: 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, Hideo Baba

Published in: Surgical Endoscopy | Issue 1/2019

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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.
Literature
1.
go back to reference 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:E359-86CrossRefPubMed 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:E359-86CrossRefPubMed
2.
go back to reference 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 207:890–896CrossRefPubMed 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 207:890–896CrossRefPubMed
3.
go back to reference 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 334:693–699CrossRefPubMed 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 334:693–699CrossRefPubMed
4.
go back to reference 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 219:1117–1123CrossRefPubMed 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 219:1117–1123CrossRefPubMed
5.
go back to reference 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 18:272–276CrossRefPubMed 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 18:272–276CrossRefPubMed
7.
go back to reference 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, 2014CrossRefPubMed 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, 2014CrossRefPubMed
8.
go back to reference 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, 2012CrossRef 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, 2012CrossRef
9.
go back to reference 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 38:37–51CrossRefPubMed 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 38:37–51CrossRefPubMed
10.
go back to reference 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:e84484CrossRefPubMedPubMedCentral 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:e84484CrossRefPubMedPubMedCentral
11.
go back to reference 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 205:19–26CrossRef 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 205:19–26CrossRef
12.
go back to reference 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 21:961–968CrossRefPubMed 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 21:961–968CrossRefPubMed
13.
go back to reference 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 35:3033–3040PubMed 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 35:3033–3040PubMed
14.
go back to reference 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, 2013CrossRefPubMed 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, 2013CrossRefPubMed
15.
go back to reference 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, 2009CrossRefPubMed 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, 2009CrossRefPubMed
16.
go back to reference 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 154:1038–1045CrossRefPubMed 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 154:1038–1045CrossRefPubMed
17.
go back to reference 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 10:98–102CrossRefPubMed 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 10:98–102CrossRefPubMed
18.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
19.
go back to reference 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, 2012CrossRef 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, 2012CrossRef
20.
go back to reference 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 204:580–587CrossRefPubMed 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 204:580–587CrossRefPubMed
21.
go back to reference 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 199:470–477CrossRefPubMed 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 199:470–477CrossRefPubMed
22.
go back to reference 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, 2015CrossRefPubMed 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, 2015CrossRefPubMed
23.
go back to reference 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, 2010CrossRefPubMed 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, 2010CrossRefPubMed
24.
go back to reference Yamashita T, Honda M, Kaneko S (2011) Molecular mechanisms of hepatocarcinogenesis in chronic hepatitis C virus infection. J Gastroenterol Hepatol 26:960–964CrossRefPubMed Yamashita T, Honda M, Kaneko S (2011) Molecular mechanisms of hepatocarcinogenesis in chronic hepatitis C virus infection. J Gastroenterol Hepatol 26:960–964CrossRefPubMed
25.
go back to reference Liver Cancer Study Group of Japan. General Rules for the Clinical and Pathological Study of Primary Liver Cancer, 3. Tokyo: Kanehara & Co., Ltd., 2010 Liver Cancer Study Group of Japan. General Rules for the Clinical and Pathological Study of Primary Liver Cancer, 3. Tokyo: Kanehara & Co., Ltd., 2010
26.
go back to reference 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 163:515–518CrossRefPubMed 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 163:515–518CrossRefPubMed
27.
go back to reference Chu KF, Dupuy DE (2014) Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer 14:199–208CrossRefPubMed Chu KF, Dupuy DE (2014) Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer 14:199–208CrossRefPubMed
28.
go back to reference 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, 2013CrossRefPubMed 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, 2013CrossRefPubMed
30.
go back to reference 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 19:2027–2034CrossRefPubMed 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 19:2027–2034CrossRefPubMed
Metadata
Title
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
Authors
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
Hideo Baba
Publication date
01-01-2019
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 1/2019
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-018-6264-3

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