Login Register Cart 0
Generic placeholder image

Current Chinese Science

Editor-in-Chief

ISSN (Print): 2210-2981
ISSN (Online): 2210-2914

Back
Journal Home About Journal Editorial Board Current Issue Volumes/Issues
Subscribe
Review Article Section: Oncology

Management of Hepatocellular Carcinoma: The East-West Difference

Author(s): Maple Ye Feng and Stephen L. Chan*

Volume 3, Issue 6, 2023

Published on: 21 September, 2023

Page: [467 - 476] Pages: 10

DOI: 10.2174/2210298103666230912143208

Open Access Journals Promotions 2
Abstract

Hepatocellular carcinoma (HCC) is highly prevalent, which contributes to the high disease burden worldwide. It was recognized as the sixth most common cancer and the fourth leading cause of mortality in cancer patients in the Global Cancer Statistics 2018. The management of HCC between eastern and western countries varies from region to region due to the different epidemiology of HCC and the approach of clinicians. Over the past decades, the multidisciplinary team approach has taken a leading role in the therapeutic paradigm of HCC, and the main treatment options include, but are not limited to 1) surgical resection; 2) transarterial chemoembolization (TACE); and 3) systemic therapies. Among these, surgical resection and TACE are applicable in earlyintermediate stage HCC with curative intent, while systemic therapies are mostly applied to advanced unresectable HCC. An individualized approach should be encouraged and tailored for each patient, taking into account the different patient population, staging, and treatment responses to achieve the best efficacy. This review discusses current advances and compares the eastern and western treatment options in the management of HCC.

Keywords: Hepatocellular carcinoma (HCC), surgical resection, transarterial chemoembolization (TACE), systemic therapies, multikinase inhibitors, immune checkpoint inhibitor, east-west difference.

« Previous Next »
[1]
Bray, F.; Ferlay, J.; Soerjomataram, I.; Siegel, R.L.; Torre, L.A.; Jemal, A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin., 2018, 68(6), 394-424.
[http://dx.doi.org/10.3322/caac.21492] [PMID: 30207593]
[2]
Chimed, T.; Sandagdorj, T.; Znaor, A.; Laversanne, M.; Tseveen, B.; Genden, P.; Bray, F. Cancer incidence and cancer control in mongolia: Results from the national cancer registry 2008-12. Int. J. Cancer, 2017, 140(2), 302-309.
[http://dx.doi.org/10.1002/ijc.30463] [PMID: 27716912]
[3]
Marengo, A.; Rosso, C.; Bugianesi, E. Liver cancer: Connections with obesity, fatty liver, and cirrhosis. Annu. Rev. Med., 2016, 67(1), 103-117.
[http://dx.doi.org/10.1146/annurev-med-090514-013832] [PMID: 26473416]
[4]
El-Serag, H.B.; Kanwal, F. Epidemiology of hepatocellular carcinoma in the United States: Where are we? Where do we go? Hepatology, 2014, 60(5), 1767-1775.
[http://dx.doi.org/10.1002/hep.27222] [PMID: 24839253]
[5]
Trinchet, J.C.; Chaffaut, C.; Bourcier, V.; Degos, F.; Henrion, J.; Fontaine, H.; Roulot, D.; Mallat, A.; Hillaire, S.; Cales, P.; Ollivier, I.; Vinel, J-P.; Mathurin, P.; Bronowicki, J-P.; Vilgrain, V.; N’Kontchou, G.; Beaugrand, M.; Chevret, S. Ultrasonographic surveillance of hepatocellular carcinoma in cirrhosis: A randomized trial comparing 3- and 6-month periodicities. Hepatology, 2011, 54(6), 1987-1997.
[http://dx.doi.org/10.1002/hep.24545] [PMID: 22144108]
[6]
Cadier, B.; Bulsei, J.; Nahon, P.; Seror, O.; Laurent, A.; Rosa, I.; Layese, R.; Costentin, C.; Cagnot, C.; Durand-Zaleski, I.; Chevreul, K. Early detection and curative treatment of hepatocellular carcinoma: A cost-effectiveness analysis in France and in the United States. Hepatology, 2017, 65(4), 1237-1248.
[http://dx.doi.org/10.1002/hep.28961] [PMID: 28176349]
[7]
Fong, Z.V.; Tanabe, K.K. The clinical management of hepatocellular carcinoma in the United States, Europe, and Asia: A comprehensive and evidence-based comparison and review. Cancer, 2014, 120(18), 2824-2838.
[http://dx.doi.org/10.1002/cncr.28730] [PMID: 24897995]
[8]
Galle, P.R.; Forner, A.; Llovet, J.M.; Mazzaferro, V.; Piscaglia, F.; Raoul, J-L.; Schirmacher, P.; Vilgrain, V. Management of hepatocellular carcinoma. J. Hepatol., 2018, 69(1), 182-236.
[http://dx.doi.org/10.1016/j.jhep.2018.03.019] [PMID: 29628281]
[9]
Bruix, J.; Sherman, M. Management of hepatocellular carcinoma: An update. Hepatology, 2011, 53(3), 1020-1022.
[http://dx.doi.org/10.1002/hep.24199] [PMID: 21374666]
[10]
Ishizawa, T.; Hasegawa, K.; Aoki, T.; Takahashi, M.; Inoue, Y.; Sano, K.; Imamura, H.; Sugawara, Y.; Kokudo, N.; Makuuchi, M. Neither multiple tumors nor portal hypertension are surgical contraindications for hepatocellular carcinoma. Gastroenterology, 2008, 134(7), 1908-1916.
[http://dx.doi.org/10.1053/j.gastro.2008.02.091] [PMID: 18549877]
[11]
Torzilli, G.; Belghiti, J.; Kokudo, N.; Takayama, T.; Capussotti, L.; Nuzzo, G.; Vauthey, J-N.; Choti, M.A.; De Santibanes, E.; Donadon, M.; Morenghi, E.; Makuuchi, M. A snapshot of the effective indications and results of surgery for hepatocellular carcinoma in tertiary referral centers: Is it adherent to the EASL/AASLD recommendations?: An observational study of the HCC East-West study group. Ann. Surg., 2013, 257(5), 929-937.
[http://dx.doi.org/10.1097/SLA.0b013e31828329b8] [PMID: 23426336]
[12]
Omata, M.; Cheng, A.L.; Kokudo, N.; Kudo, M.; Lee, J.M.; Jia, J.; Tateishi, R.; Han, K-H.; Chawla, Y.K.; Shiina, S.; Jafri, W.; Payawal, D.A.; Ohki, T.; Ogasawara, S.; Chen, P-J.; Lesmana, C.R.A.; Lesmana, L.A.; Gani, R.A.; Obi, S.; Dokmeci, A.K.; Sarin, S.K. Asia-Pacific clinical practice guidelines on the management of hepatocellular carcinoma: A 2017 update. Hepatol. Int., 2017, 11(4), 317-370.
[http://dx.doi.org/10.1007/s12072-017-9799-9] [PMID: 28620797]
[13]
Han, K.H.; Kudo, M.; Ye, S.L.; Choi, J.Y.; Poon, R.T.P.; Seong, J.; Park, J-W.; Ichida, T.; Chung, J.W.; Chow, P.; Cheng, A-L. Asian consensus workshop report: Expert consensus guideline for the management of intermediate and advanced hepatocellular carcinoma in Asia. Oncology, 2011, 81(Suppl. 1), 158-164.
[http://dx.doi.org/10.1159/000333280] [PMID: 22212951]
[14]
Omata, M.; Lesmana, L.A.; Tateishi, R.; Chen, P.J.; Lin, S.M.; Yoshida, H.; Kudo, M.; Lee, J.M.; Choi, B.I.; Poon, R.T.P.; Shiina, S.; Cheng, A.L.; Jia, J-D.; Obi, S.; Han, K.H.; Jafri, W.; Chow, P.; Lim, S.G.; Chawla, Y.K.; Budihusodo, U.; Gani, R.A.; Lesmana, C.R.; Putranto, T.A.; Liaw, Y.F.; Sarin, S.K. Asian pacific association for the study of the liver consensus recommendations on hepatocellular carcinoma. Hepatol. Int., 2010, 4(2), 439-474.
[http://dx.doi.org/10.1007/s12072-010-9165-7] [PMID: 20827404]
[15]
Shi, J.; Lai, E.C.H.; Li, N.; Guo, W.X.; Xue, J.; Lau, W.Y.; Wu, M-C.; Cheng, S-Q. Surgical treatment of hepatocellular carcinoma with portal vein tumor thrombus. Ann. Surg. Oncol., 2010, 17(8), 2073-2080.
[http://dx.doi.org/10.1245/s10434-010-0940-4] [PMID: 20131013]
[16]
Zhou, J.; Sun, H.; Wang, Z.; Cong, W.; Wang, J.; Zeng, M.; Zhou, W.; Bie, P.; Liu, L.; Wen, T.; Han, G.; Wang, M.; Liu, R.; Lu, L.; Ren, Z.; Chen, M.; Zeng, Z.; Liang, P.; Liang, C.; Chen, M.; Yan, F.; Wang, W.; Ji, Y.; Yun, J.; Cai, D.; Chen, Y.; Cheng, W.; Cheng, S.; Dai, C.; Guo, W.; Hua, B.; Huang, X.; Jia, W.; Li, Y.; Li, Y.; Liang, J.; Liu, T.; Lv, G.; Mao, Y.; Peng, T.; Ren, W.; Shi, H.; Shi, G.; Tao, K.; Wang, W.; Wang, X.; Wang, Z.; Xiang, B.; Xing, B.; Xu, J.; Yang, J.; Yang, J.; Yang, Y.; Yang, Y.; Ye, S.; Yin, Z.; Zhang, B.; Zhang, B.; Zhang, L.; Zhang, S.; Zhang, T.; Zhao, Y.; Zheng, H.; Zhu, J.; Zhu, K.; Liu, R.; Shi, Y.; Xiao, Y.; Dai, Z.; Teng, G.; Cai, J.; Wang, W.; Cai, X.; Li, Q.; Shen, F.; Qin, S.; Dong, J.; Fan, J. Guidelines for the diagnosis and treatment of hepatocellular carcinoma (2019 Edition). Liver Cancer, 2020, 9(6), 682-720.
[http://dx.doi.org/10.1159/000509424] [PMID: 33442540]
[17]
Cheung, T.T.T.; Kwok, P.C.H.; Chan, S.; Cheung, C.C.; Lee, A.S.; Lee, V.; Cheng, H-C.; Chia, N-H.; Chong, C.C.N.; Lai, T-W.; Law, A.L.Y.; Luk, M-Y.; Tong, C.C.; Yau, T.C.C. Hong kong consensus statements for the management of unresectable hepatocellular carcinoma. Liver Cancer, 2018, 7(1), 40-54.
[http://dx.doi.org/10.1159/000485984] [PMID: 29662832]
[18]
Yau, T.; Tang, V.Y.F.; Yao, T.J.; Fan, S.T.; Lo, C.M.; Poon, R.T.P. Development of hong kong liver cancer staging system with treatment stratification for patients with hepatocellular carcinoma. Gastroenterology, 2014, 146(7), 1691-700.e3.
[http://dx.doi.org/10.1053/j.gastro.2014.02.032] [PMID: 24583061]
[19]
Chui, A.M.N.; Yau, T.C.C.; Cheung, T.T. An overview in management of hepatocellular carcinoma in Hong Kong using the Hong Kong Liver Cancer (HKLC) staging system. Global Health Med., 2020, 2(5), 312-318.
[http://dx.doi.org/10.35772/ghm.2020.01062] [PMID: 33330826]
[20]
Korean Liver Cancer Study Group (KLCSG);; National Cancer Center, Korea (NCC).. 2014 KLCSG-NCC Korea practice guideline for the management of hepatocellular carcinoma. Gut. Liver, 2015, 9(3), 267-317.
[PMID: 25918260]
[21]
Kudo, M.; Matsui, O.; Izumi, N.; Iijima, H.; Kadoya, M.; Imai, Y.; Okusaka, T.; Miyayama, S.; Tsuchiya, K.; Ueshima, K.; Hiraoka, A.; Ikeda, M.; Ogasawara, S.; Yamashita, T.; Minami, T.; Yamakado, K. JSH consensus-based clinical practice guidelines for the management of hepatocellular carcinoma: 2014 update by the liver cancer study group of Japan. Liver Cancer, 2014, 3(3-4), 458-468.
[http://dx.doi.org/10.1159/000343875] [PMID: 26280007]
[22]
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, 45(2)
[http://dx.doi.org/10.1111/hepr.12464] [PMID: 25625806]
[23]
Kudo, M.; Kitano, M.; Sakurai, T.; Nishida, N. General rules for the clinical and pathological study of primary liver cancer, nationwide follow-up survey and clinical practice guidelines: The outstanding achievements of the liver cancer study group of Japan. Dig. Dis., 2015, 33(6), 765-770.
[http://dx.doi.org/10.1159/000439101] [PMID: 26488173]
[24]
Kudo, M.; Han, K.H.; Ye, S.L.; Zhou, J.; Huang, Y.H.; Lin, S.M.; Wang, C-K.; Ikeda, M.; Chan, S.L.; Choo, S.P.; Miyayama, S.; Cheng, A.L. A changing paradigm for the treatment of intermediate-stage hepatocellular carcinoma: Asia-pacific primary liver cancer expert consensus statements. Liver Cancer, 2020, 9(3), 245-260.
[http://dx.doi.org/10.1159/000507370] [PMID: 32647629]
[25]
Choo, S.P.; Tan, W.L.; Goh, B.K.P.; Tai, W.M.; Zhu, A.X. Comparison of hepatocellular carcinoma in Eastern versus Western populations. Cancer, 2016, 122(22), 3430-3446.
[http://dx.doi.org/10.1002/cncr.30237] [PMID: 27622302]
[26]
Liver Cancer Study Group of Japan. The general rules for the clinical and pathological study of primary liver cancer. Jpn. J. Surg., 1989, 19(1), 98-129.
[http://dx.doi.org/10.1007/BF02471576] [PMID: 2659865]
[27]
Khan, A.R.; Wei, X.; Xu, X. Portal vein tumor thrombosis and hepatocellular carcinoma - The changing tides. J. Hepatocell. Carcinoma, 2021, 8, 1089-1115.
[http://dx.doi.org/10.2147/JHC.S318070] [PMID: 34522691]
[28]
Lv, W.F.; Liu, K.C.; Lu, D.; Zhou, C.Z.; Cheng, D.L.; Xiao, J.K.; Zhang, X-M.; Zhang, Z-F. Transarterial chemoembolization for hepatocellular carcinoma combined with portal vein tumor thrombosis. Cancer Manag. Res., 2018, 10, 4719-4726.
[http://dx.doi.org/10.2147/CMAR.S166527] [PMID: 30410405]
[29]
Chow, P.K.H.; Choo, S.P.; Ng, D.C.E.; Lo, R.H.G.; Wang, M.L.C.; Toh, H.C.; Tai, D.W.M.; Goh, B.K.P.; Wong, J.S.; Tay, K.H.; Goh, A.S.W.; Yan, S.X.; Loke, K.S.H.; Thang, S.P.; Gogna, A.; Too, C.W.; Irani, F.G.; Leong, S.; Lim, K.H.; Thng, C.H. National cancer centre singapore consensus guidelines for hepatocellular carcinoma. Liver Cancer, 2016, 5(2), 97-106.
[http://dx.doi.org/10.1159/000367759] [PMID: 27386428]
[30]
Poon, R.T.P.; Cheung, T.T.T.; Kwok, P.C.H.; Lee, A.S.; Li, T.W.; Loke, K.L.; Chan, S.L.; Cheung, M-T.; Lai, T-W.; Cheung, C-C.; Cheung, F-Y.; Loo, C-K.; But, Y-K.; Hsu, S-J.; Yu, S.C-H.; Yau, T. Hong Kong consensus recommendations on the management of hepatocellular carcinoma. Liver Cancer, 2015, 4(1), 51-69.
[http://dx.doi.org/10.1159/000367728] [PMID: 26020029]
[31]
Arii, S.; Sata, M.; Sakamoto, M.; Shimada, M.; Kumada, T.; Shiina, S.; Yamashita, T.; Kokudo, N.; Tanaka, M.; Takayama, T.; Kudo, M. Management of hepatocellular carcinoma: Report of consensus meeting in the 45th annual meeting of the japan society of hepatology (2009). Hepatol. Res., 2010, 40(7), 667-685.
[http://dx.doi.org/10.1111/j.1872-034X.2010.00673.x] [PMID: 20633193]
[32]
Finn, R.S.; Zhu, A.X.; Farah, W.; Almasri, J.; Zaiem, F.; Prokop, L.J.; Murad, M.H.; Mohammed, K. Therapies for advanced stage hepatocellular carcinoma with macrovascular invasion or metastatic disease: A systematic review and meta-analysis. Hepatology, 2018, 67(1), 422-435.
[http://dx.doi.org/10.1002/hep.29486] [PMID: 28881497]
[33]
Vogel, A.; Cervantes, A.; Chau, I.; Daniele, B.; Llovet, J.M.; Meyer, T.; Nault, J-C.; Neumann, U.; Ricke, J.; Sangro, B.; Schirmacher, P.; Verslype, C.; Zech, C.J.; Arnold, D.; Martinelli, E. Correction to: “Hepatocellular carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up”. Ann. Oncol., 2019, 30(5), 871-873.
[http://dx.doi.org/10.1093/annonc/mdy510] [PMID: 31987361]
[34]
Lyu, N.; Wang, X.; Li, J.B.; Lai, J.F.; Chen, Q.F.; Li, S.L.; Deng, H-J.; He, M.; Mu, L-W.; Zhao, M. Arterial chemotherapy of oxaliplatin plus fluorouracil versus sorafenib in advanced hepatocellular carcinoma: A biomolecular exploratory, randomized, phase III trial (FOHAIC-1). J. Clin. Oncol., 2022, 40(5), 468-480.
[http://dx.doi.org/10.1200/JCO.21.01963] [PMID: 34905388]
[35]
Mazzaferro, V.; Llovet, J.M.; Miceli, R.; Bhoori, S.; Schiavo, M.; Mariani, L.; Camerini, T.; Roayaie, S.; Schwartz, M.E.; Grazi, G.L.; Adam, R.; Neuhaus, P.; Salizzoni, M.; Bruix, J.; Forner, A.; De Carlis, L.; Cillo, U.; Burroughs, A.K.; Troisi, R.; Rossi, M.; Gerunda, G.E.; Lerut, J.; Belghiti, J.; Boin, I.; Gugenheim, J.; Rochling, F.; Van Hoek, B.; Majno, P. Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: A retrospective, exploratory analysis. Lancet Oncol., 2009, 10(1), 35-43.
[http://dx.doi.org/10.1016/S1470-2045(08)70284-5] [PMID: 19058754]
[36]
Llovet, J.M.; Real, M.I.; Montaña, X.; Planas, R.; Coll, S.; Aponte, J.; Ayuso, C.; Sala, M.; Muchart, J.; Solà, R.; Rodés, J.; Bruix, J. Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: A randomised controlled trial. Lancet, 2002, 359(9319), 1734-1739.
[http://dx.doi.org/10.1016/S0140-6736(02)08649-X] [PMID: 12049862]
[37]
Johnson, P.J.; Berhane, S.; Kagebayashi, C.; Satomura, S.; Teng, M.; Reeves, H.L.; O’Beirne, J.; Fox, R.; Skowronska, A.; Palmer, D.; Yeo, W.; Mo, F.; Lai, P.; Iñarrairaegui, M.; Chan, S.L.; Sangro, B.; Miksad, R.; Tada, T.; Kumada, T.; Toyoda, H. Assessment of liver function in patients with hepatocellular carcinoma: A new evidence-based approach-the ALBI grade. J. Clin. Oncol., 2015, 33(6), 550-558.
[http://dx.doi.org/10.1200/JCO.2014.57.9151] [PMID: 25512453]
[38]
Hiraoka, A.; Michitaka, K.; Kumada, T.; Izumi, N.; Kadoya, M.; Kokudo, N.; Kubo, S.; Matsuyama, Y.; Nakashima, O.; Sakamoto, M.; Takayama, T.; Kokudo, T.; Kashiwabara, K.; Kudo, M. Validation and potential of albumin-bilirubin grade and prognostication in a nationwide survey of 46,681 hepatocellular carcinoma patients in Japan: The need for a more detailed evaluation of hepatic function. Liver Cancer, 2017, 6(4), 325-336.
[http://dx.doi.org/10.1159/000479984] [PMID: 29234636]
[39]
Kimura, H.; Ohkawa, K.; Miyazaki, M.; Sakakibara, M.; Imanaka, K.; Tamura, T.; Sueyoshi, H.; Takada, R.; Fukutake, N.; Uehara, H.; Ashida, R.; Ioka, T.; Nakazawa, T.; Nakanishi, K.; Katayama, K. Subclassification of patients with intermediate-stage (Barcelona Clinic Liver Cancer stage-B) hepatocellular carcinoma using the up-to-seven criteria and serum tumor markers. Hepatol. Int., 2017, 11(1), 105-114.
[http://dx.doi.org/10.1007/s12072-016-9771-0] [PMID: 27766479]
[40]
Izumoto, H.; Hiraoka, A.; Ishimaru, Y.; Murakami, T.; Kitahata, S.; Ueki, H.; Aibiki, T.; Okudaira, T.; Miyamoto, Y.; Yamago, H.; Iwasaki, R.; Tomida, H.; Mori, K.; Kishida, M.; Tsubouchi, E.; Miyata, H.; Ninomiya, T.; Kawasaki, H.; Hirooka, M.; Matsuura, B.; Abe, M.; Hiasa, Y.; Michitaka, K.; Kudo, M. Validation of newly proposed time to transarterial chemoembolization progression in intermediate-stage hepatocellular carcinoma cases. Oncology, 2017, 93(Suppl. 1), 120-126.
[http://dx.doi.org/10.1159/000481242] [PMID: 29258105]
[41]
Wang, Q.; Xia, D.; Bai, W.; Wang, E.; Sun, J.; Huang, M.; Mu, W.; Yin, G.; Li, H.; Zhao, H.; Li, J.; Zhang, C.; Zhu, X.; Wu, J.; Li, J.; Gong, W.; Li, Z.; Lin, Z.; Pan, X.; Shi, H.; Shao, G.; Liu, J.; Yang, S.; Zheng, Y.; Xu, J.; Song, J.; Wang, W.; Wang, Z.; Zhang, Y.; Ding, R.; Zhang, H.; Yu, H.; Zheng, L.; Gu, W.; You, N.; Wang, G.; Zhang, S.; Feng, L.; Liu, L.; Zhang, P.; Li, X.; Chen, J.; Xu, T.; Zhou, W.; Zeng, H.; Zhang, Y.; Huang, W.; Jiang, W.; Zhang, W.; Shao, W.; Li, L.; Niu, J.; Yuan, J.; Li, X.; Lv, Y.; Li, K.; Yin, Z.; Xia, J.; Fan, D.; Han, G. Development of a prognostic score for recommended TACE candidates with hepatocellular carcinoma: A multicentre observational study. J. Hepatol., 2019, 70(5), 893-903.
[http://dx.doi.org/10.1016/j.jhep.2019.01.013] [PMID: 30660709]
[42]
Kim, J.H.; Shim, J.H.; Lee, H.C.; Sung, K.B.; Ko, H.K.; Ko, G.Y.; Gwon, D.I.; Kim, J.W.; Lim, Y-S.; Park, S.H. New intermediate-stage subclassification for patients with hepatocellular carcinoma treated with transarterial chemoembolization. Liver Int., 2017, 37(12), 1861-1868.
[http://dx.doi.org/10.1111/liv.13487] [PMID: 28581250]
[43]
Hucke, F.; Pinter, M.; Graziadei, I.; Bota, S.; Vogel, W.; Müller, C.; Heinzl, H.; Waneck, F.; Trauner, M.; Peck-Radosavljevic, M.; Sieghart, W. How to STATE suitability and START transarterial chemoembolization in patients with intermediate stage hepatocellular carcinoma. J. Hepatol., 2014, 61(6), 1287-1296.
[http://dx.doi.org/10.1016/j.jhep.2014.07.002] [PMID: 25016222]
[44]
Prince, D.; Liu, K.; Xu, W.; Chen, M.; Sun, J.Y.; Lu, X.J.; Ji, J. Management of patients with intermediate stage hepatocellular carcinoma. Ther. Adv. Med. Oncol., 2020, 12, 1758835920970840.
[http://dx.doi.org/10.1177/1758835920970840] [PMID: 33224278]
[45]
Wilhelm, S.M.; Carter, C.; Tang, L.; Wilkie, D.; McNabola, A.; Rong, H.; Chen, C.; Zhang, X.; Vincent, P.; McHugh, M.; Cao, Y.; Shujath, J.; Gawlak, S.; Eveleigh, D.; Rowley, B.; Liu, L.; Adnane, L.; Lynch, M.; Auclair, D.; Taylor, I.; Gedrich, R.; Voznesensky, A.; Riedl, B.; Post, L.E.; Bollag, G.; Trail, P.A. BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Res., 2004, 64(19), 7099-7109.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-1443] [PMID: 15466206]
[46]
Llovet, J.M.; Ricci, S.; Mazzaferro, V.; Hilgard, P.; Gane, E.; Blanc, J.F.; de Oliveira, A.C.; Santoro, A.; Raoul, J-L.; Forner, A.; Schwartz, M.; Porta, C.; Zeuzem, S.; Bolondi, L.; Greten, T.F.; Galle, P.R.; Seitz, J-F.; Borbath, I.; Häussinger, D.; Giannaris, T.; Shan, M.; Moscovici, M.; Voliotis, D.; Bruix, J. Sorafenib in advanced hepatocellular carcinoma. N. Engl. J. Med., 2008, 359(4), 378-390.
[http://dx.doi.org/10.1056/NEJMoa0708857] [PMID: 18650514]
[47]
Cheng, A.L.; Kang, Y.K.; Chen, Z.; Tsao, C.J.; Qin, S.; Kim, J.S.; Luo, R.; Feng, J.; Ye, S.; Yang, T-S.; Xu, J.; Sun, Y.; Liang, H.; Liu, J.; Wang, J.; Tak, W.Y.; Pan, H.; Burock, K.; Zou, J.; Voliotis, D.; Guan, Z. 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(1), 25-34.
[http://dx.doi.org/10.1016/S1470-2045(08)70285-7] [PMID: 19095497]
[48]
Bruix, J.; Raoul, J.L.; Sherman, M.; Mazzaferro, V.; Bolondi, L.; Craxi, A.; Galle, P.R.; Santoro, A.; Beaugrand, M.; Sangiovanni, A.; Porta, C.; Gerken, G.; Marrero, J.A.; Nadel, A.; Shan, M.; Moscovici, M.; Voliotis, D.; Llovet, J.M. Efficacy and safety of sorafenib in patients with advanced hepatocellular carcinoma: Subanalyses of a phase III trial. J. Hepatol., 2012, 57(4), 821-829.
[http://dx.doi.org/10.1016/j.jhep.2012.06.014] [PMID: 22727733]
[49]
Chen, B.B.; Shih, I.L.; Wu, C.H.; Hsu, C.; Chen, C.H.; Shih, T.T.F.; Liu, K-L.; Liang, P-C. Comparison of characteristics and transarterial chemoembolization outcomes in patients with unresectable hepatocellular carcinoma and different viral etiologies. J. Vasc. Interv. Radiol., 2014, 25(3), 371-378.
[http://dx.doi.org/10.1016/j.jvir.2013.10.027] [PMID: 24468045]
[50]
Kudo, M.; Finn, R.S.; Qin, S.; Han, K.H.; Ikeda, K.; Piscaglia, F.; Baron, A.; Park, J-W.; Han, G.; Jassem, J.; Blanc, J.F.; Vogel, A.; Komov, D.; Evans, T.R.J.; Lopez, C.; Dutcus, C.; Guo, M.; Saito, K.; Kraljevic, S.; Tamai, T.; Ren, M.; Cheng, A-L. Lenvatinib versus sorafenib in first-line treatment of patients with unresectable hepatocellular carcinoma: A randomised phase 3 non-inferiority trial. Lancet, 2018, 391(10126), 1163-1173.
[http://dx.doi.org/10.1016/S0140-6736(18)30207-1] [PMID: 29433850]
[51]
Bruix, J.; Qin, S.; Merle, P.; Granito, A.; Huang, Y.H.; Bodoky, G.; Pracht, M.; Yokosuka, O.; Rosmorduc, O.; Breder, V.; Gerolami, R.; Masi, G.; Ross, P.J.; Song, T.; Bronowicki, J-P.; Ollivier-Hourmand, I.; Kudo, M.; Cheng, A-L.; Llovet, J.M.; Finn, R.S.; LeBerre, M-A.; Baumhauer, A.; Meinhardt, G.; Han, G. Regorafenib for patients with hepatocellular carcinoma who progressed on sorafenib treatment (RESORCE): A randomised, double-blind, placebo-controlled, phase 3 trial. Lancet, 2017, 389(10064), 56-66.
[http://dx.doi.org/10.1016/S0140-6736(16)32453-9] [PMID: 27932229]
[52]
Abou-Alfa, G.K.; Meyer, T.; Cheng, A.L.; El-Khoueiry, A.B.; Rimassa, L.; Ryoo, B.Y.; Cicin, I.; Merle, P.; Chen, Y.; Park, J-W.; Blanc, J-F.; Bolondi, L.; Klümpen, H-J.; Chan, S.L.; Zagonel, V.; Pressiani, T.; Ryu, M-H.; Venook, A.P.; Hessel, C.; Borgman-Hagey, A.E.; Schwab, G.; Kelley, R.K. Cabozantinib in patients with advanced and progressing hepatocellular carcinoma. N. Engl. J. Med., 2018, 379(1), 54-63.
[http://dx.doi.org/10.1056/NEJMoa1717002] [PMID: 29972759]
[53]
Zhu, A.X.; Kang, Y.K.; Yen, C.J.; Finn, R.S.; Galle, P.R.; Llovet, J.M.; Assenat, E.; Brandi, G.; Pracht, M.; Lim, H.Y.; Rau, K-M.; Motomura, K.; Ohno, I.; Merle, P.; Daniele, B.; Shin, D.B.; Gerken, G.; Borg, C.; Hiriart, J-B.; Okusaka, T.; Morimoto, M.; Hsu, Y.; Abada, P.B.; Kudo, M. Ramucirumab after sorafenib in patients with advanced hepatocellular carcinoma and increased α-fetoprotein concentrations (REACH-2): A randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol., 2019, 20(2), 282-296.
[http://dx.doi.org/10.1016/S1470-2045(18)30937-9] [PMID: 30665869]
[54]
Qin, S.; Li, Q.; Gu, S.; Chen, X.; Lin, L.; Wang, Z.; Xu, A.; Chen, X.; Zhou, C.; Ren, Z.; Yang, L.; Xu, L.; Bai, Y.; Chen, L.; Li, J.; Pan, H.; Cao, B.; Fang, W.; Wu, W.; Wang, G.; Cheng, Y.; Yu, Z.; Zhu, X.; Jiang, D.; Lu, Y.; Wang, H.; Xu, J.; Bai, L.; Liu, Y.; Lin, H.; Wu, C.; Zhang, Y.; Yan, P.; Jin, C.; Zou, J. Apatinib as second-line or later therapy in patients with advanced hepatocellular carcinoma (AHELP): A multicentre, double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Gastroenterol. Hepatol., 2021, 6(7), 559-568.
[http://dx.doi.org/10.1016/S2468-1253(21)00109-6] [PMID: 33971141]
[55]
Zhu, A.X.; Finn, R.S.; Edeline, J.; Cattan, S.; Ogasawara, S.; Palmer, D.; Verslype, C.; Zagonel, V.; Fartoux, L.; Vogel, A.; Sarker, D.; Verset, G.; Chan, S.L.; Knox, J.; Daniele, B.; Webber, A.L.; Ebbinghaus, S.W.; Ma, J.; Siegel, A.B.; Cheng, A-L.; Kudo, M.; Alistar, A.; Asselah, J.; Blanc, J-F.; Borbath, I.; Cannon, T.; Chung, K.; Cohn, A.; Cosgrove, D.P.; Damjanov, N.; Gupta, M.; Karino, Y.; Karwal, M.; Kaubisch, A.; Kelley, R.; Van Laethem, J-L.; Larson, T.; Lee, J.; Li, D.; Manhas, A.; Manji, G.A.; Numata, K.; Parsons, B.; Paulson, A.S.; Pinto, C.; Ramirez, R.; Ratnam, S.; Rizell, M.; Rosmorduc, O.; Sada, Y.; Sasaki, Y.; Stal, P.I.; Strasser, S.; Trojan, J.; Vaccaro, G.; Van Vlierberghe, H.; Weiss, A.; Weiss, K-H.; Yamashita, T. Pembrolizumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib (KEYNOTE-224): A non-randomised, open-label phase 2 trial. Lancet Oncol., 2018, 19(7), 940-952.
[http://dx.doi.org/10.1016/S1470-2045(18)30351-6] [PMID: 29875066]
[56]
Finn, R.S.; Ryoo, B.Y.; Merle, P.; Kudo, M.; Bouattour, M.; Lim, H.Y.; Breder, V.; Edeline, J.; Chao, Y.; Ogasawara, S.; Yau, T.; Garrido, M.; Chan, S.L.; Knox, J.; Daniele, B.; Ebbinghaus, S.W.; Chen, E.; Siegel, A.B.; Zhu, A.X.; Cheng, A-L. Pembrolizumab as second-line therapy in patients with advanced hepatocellular carcinoma in KEYNOTE-240: A randomized, double-blind, phase III trial. J. Clin. Oncol., 2020, 38(3), 193-202.
[http://dx.doi.org/10.1200/JCO.19.01307] [PMID: 31790344]
[57]
Qin, S.; Chen, Z.; Fang, W.; Ren, Z.; Xu, R.; Ryoo, B.Y.; Meng, Z.; Bai, Y.; Chen, X.; Liu, X.; Xiao, J.; Ho, G.F.; Mao, Y.; Ye, X.; Ying, J.; Li, J.; Zhong, W.Y.; Zhou, Y.; Siegel, A.B.; Hao, C. Pembrolizumab plus best supportive care versus placebo plus best supportive care as second-line therapy in patients in Asia with advanced hepatocellular carcinoma (HCC): Phase 3 KEYNOTE-394 study. J. Clin. Oncol., 2022, 40(4_s)(Suppl.), 383.
[http://dx.doi.org/10.1200/JCO.2022.40.4_suppl.383]
[58]
El-Khoueiry, A.B.; Sangro, B.; Yau, T.; Crocenzi, T.S.; Kudo, M.; Hsu, C.; Kim, T-Y.; Choo, S-P.; Trojan, J.; Welling, T.H., III; Meyer, T.; Kang, Y-K.; Yeo, W.; Chopra, A.; Anderson, J.; Dela Cruz, C.; Lang, L.; Neely, J.; Tang, H.; Dastani, H.B.; Melero, I. Nivolumab in patients with advanced hepatocellular carcinoma (CheckMate 040): An open-label, non-comparative, phase 1/2 dose escalation and expansion trial. Lancet, 2017, 389(10088), 2492-2502.
[http://dx.doi.org/10.1016/S0140-6736(17)31046-2] [PMID: 28434648]
[59]
Yau, T.; Park, J.W.; Finn, R.S.; Cheng, A.L.; Mathurin, P.; Edeline, J.; Kudo, M.; Han, K-H.; Harding, J.J.; Merle, P.; Rosmorduc, O.; Wyrwicz, L.; Schott, E.; Choo, S.P.; Kelley, R.K.; Begic, D.; Chen, G.; Neely, J.; Anderson, J.; Sangro, B. CheckMate 459: A randomized, multi-center phase III study of nivolumab (NIVO) vs sorafenib (SOR) as first-line (1L) treatment in patients (pts) with advanced hepatocellular carcinoma (aHCC). Ann. Oncol., 2019, 30, v874-v875.
[http://dx.doi.org/10.1093/annonc/mdz394.029]
[60]
Yau, T.; Park, J.W.; Finn, R.S.; Cheng, A.L.; Mathurin, P.; Edeline, J.; Kudo, M.; Harding, J.J.; Merle, P.; Rosmorduc, O.; Wyrwicz, L.; Schott, E.; Choo, S.P.; Kelley, R.K.; Sieghart, W.; Assenat, E.; Zaucha, R.; Furuse, J.; Abou-Alfa, G.K.; El-Khoueiry, A.B.; Melero, I.; Begic, D.; Chen, G.; Neely, J.; Wisniewski, T.; Tschaika, M.; Sangro, B. Nivolumab versus sorafenib in advanced hepatocellular carcinoma (CheckMate 459): A randomised, multicentre, open-label, phase 3 trial. Lancet Oncol., 2022, 23(1), 77-90.
[http://dx.doi.org/10.1016/S1470-2045(21)00604-5] [PMID: 34914889]
[61]
Finn, R.S.; Qin, S.; Ikeda, M.; Galle, P.R.; Ducreux, M.; Kim, T.Y.; Lim, H.Y.; Kudo, M.; Breder, V.V.; Merle, P.; Kaseb, A.O.; Li, D.; Verret, W.; Shao, H.; Liu, J.; Li, L.; Zhu, A.X.; Cheng, A-L. IMbrave150: Updated overall survival (OS) data from a global, randomized, open-label phase III study of atezolizumab (atezo) + bevacizumab (bev) versus sorafenib (sor) in patients (pts) with unresectable hepatocellular carcinoma (HCC). J. Clin. Oncol., 2021, 39(3_s)(Suppl.), 267.
[http://dx.doi.org/10.1200/JCO.2021.39.3_suppl.267]
[62]
Finn, R.S.; Qin, S.; Ikeda, M.; Galle, P.R.; Ducreux, M.; Kim, T.Y.; Kudo, M.; Breder, V.; Merle, P.; Kaseb, A.O.; Li, D.; Verret, W.; Xu, D-Z.; Hernandez, S.; Liu, J.; Huang, C.; Mulla, S.; Wang, Y.; Lim, H.Y.; Zhu, A.X.; Cheng, A-L. Atezolizumab plus bevacizumab in unresectable hepatocellular carcinoma. N. Engl. J. Med., 2020, 382(20), 1894-1905.
[http://dx.doi.org/10.1056/NEJMoa1915745] [PMID: 32402160]
[63]
Cheng, A.L.; Qin, S.; Ikeda, M.; Galle, P.R.; Ducreux, M.; Kim, T.Y.; Lim, H.Y.; Kudo, M.; Breder, V.; Merle, P.; Kaseb, A.O.; Li, D.; Verret, W.; Ma, N.; Nicholas, A.; Wang, Y.; Li, L.; Zhu, A.X.; Finn, R.S. Updated efficacy and safety data from IMbrave150: Atezolizumab plus bevacizumab vs. sorafenib for unresectable hepatocellular carcinoma. J. Hepatol., 2022, 76(4), 862-873.
[http://dx.doi.org/10.1016/j.jhep.2021.11.030] [PMID: 34902530]
[64]
Yau, T.; Kang, Y.K.; Kim, T.Y.; El-Khoueiry, A.B.; Santoro, A.; Sangro, B.; Melero, I.; Kudo, M.; Hou, M-M.; Matilla, A.; Tovoli, F.; Knox, J.J.; Ruth He, A.; El-Rayes, B.F.; Acosta-Rivera, M.; Lim, H-Y.; Neely, J.; Shen, Y.; Wisniewski, T.; Anderson, J.; Hsu, C. Efficacy and safety of nivolumab plus ipilimumab in patients with advanced hepatocellular carcinoma previously treated with sorafenib: The checkmate 040 randomized clinical trial. JAMA Oncol., 2020, 6(11), e204564.
[http://dx.doi.org/10.1001/jamaoncol.2020.4564] [PMID: 33001135]
[65]
Abou-Alfa, G.K.; Chan, S.L.; Kudo, M.; Lau, G.; Kelley, R.K.; Furuse, J.; Sukeepaisarnjaroen, W.; Kang, Y-K.; Dao, T.V.; De Toni, E.N.; Rimassa, L.; Breder, V.V.; Vasilyev, A.; Heurgue, A.; Tam, V.; Mody, K.; Thungappa, S.C.; He, P.; Negro, A.; Sangro, B. Phase 3 randomized, open-label, multicenter study of tremelimumab (T) and durvalumab (D) as first-line therapy in patients (pts) with unresectable hepatocellular carcinoma (uHCC): HIMALAYA. J. Clin. Oncol., 2022, 40(S4), 379.
[http://dx.doi.org/10.1200/JCO.2022.40.4_suppl.379]
[66]
Abou-Alfa Ghassan, K; Lau, G; Kudo, M; Chan Stephen, L; Kelley Robin, K; Furuse, J Tremelimumab plus durvalumab in unresectable hepatocellular carcinoma., NEJM Evid., 2022, 1(8), EVIDoa2100070.,
[http://dx.doi.org/10.1056/EVIDoa2100070]
[67]
Chang, T.T.; Sawhney, R.; Monto, A.; Davoren, J.B.; Kirkland, J.G.; Stewart, L.; Corvera, C.U. Implementation of a multidisciplinary treatment team for hepatocellular cancer at a Veterans Affairs Medical Center improves survival. HPB, 2008, 10(6), 405-411.
[http://dx.doi.org/10.1080/13651820802356572] [PMID: 19088925]
[68]
Yopp, A.C.; Mansour, J.C.; Beg, M.S.; Arenas, J.; Trimmer, C.; Reddick, M.; Pedrosa, I.; Khatri, G.; Yakoo, T.; Meyer, J.J.; Shaw, J.; Marrero, J.A.; Singal, A.G. Establishment of a multidisciplinary hepatocellular carcinoma clinic is associated with improved clinical outcome. Ann. Surg. Oncol., 2014, 21(4), 1287-1295.
[http://dx.doi.org/10.1245/s10434-013-3413-8] [PMID: 24318095]
[69]
Singh, A.; Settleman, J. EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene, 2010, 29(34), 4741-4751.
[http://dx.doi.org/10.1038/onc.2010.215] [PMID: 20531305]
[70]
van Malenstein, H.; Dekervel, J.; Verslype, C.; Van Cutsem, E.; Windmolders, P.; Nevens, F.; van Pelt, J. Long-term exposure to sorafenib of liver cancer cells induces resistance with epithelial-to-mesenchymal transition, increased invasion and risk of rebound growth. Cancer Lett., 2013, 329(1), 74-83.
[http://dx.doi.org/10.1016/j.canlet.2012.10.021] [PMID: 23111106]
[71]
Chen, X.; Lingala, S.; Khoobyari, S.; Nolta, J.; Zern, M.A.; Wu, J. Epithelial mesenchymal transition and hedgehog signaling activation are associated with chemoresistance and invasion of hepatoma subpopulations. J. Hepatol., 2011, 55(4), 838-845.
[http://dx.doi.org/10.1016/j.jhep.2010.12.043] [PMID: 21334406]
[72]
Ruiz de Galarreta, M.; Bresnahan, E.; Molina-Sánchez, P.; Lindblad, K.E.; Maier, B.; Sia, D.; Puigvehi, M.; Miguela, V.; Casanova-Acebes, M.; Dhainaut, M.; Villacorta-Martin, C.; Singhi, A.D.; Moghe, A.; von Felden, J.; Tal Grinspan, L.; Wang, S.; Kamphorst, A.O.; Monga, S.P.; Brown, B.D.; Villanueva, A.; Llovet, J.M.; Merad, M.; Lujambio, A. β-Catenin activation promotes immune escape and resistance to Anti-PD-1 therapy in hepatocellular carcinoma. Cancer Discov., 2019, 9(8), 1124-1141.
[http://dx.doi.org/10.1158/2159-8290.CD-19-0074] [PMID: 31186238]

Rights & Permissions Print Cite
Article Metrics
7
1
Wayfinder Image
Open Access Journals Promotions
© 2024 Bentham Science Publishers | Privacy Policy