Role of hepatectomy for recurrent or initially unresectable hepatocellular carcinoma

World Journal of Hepatology

Volumn 6, Issue 12, 2014, Pages 836-843

  Kishi, Yoji ^a   Shimada, Kazuaki ^a   Nara, Satoshi ^a   Esaki, Minoru ^a   Kosuge, Tomoo ^a  

^a NATIONAL CANCER CENTER HOSPITAL   (Japan)

Author keywords

Conversion therapy; Hepatectomy; Hepatocellular carcinoma; Multidisciplinary treatment; Repeat hepatectomy

Indexed keywords

EID: 84920061730     PISSN: None     EISSN: 19485182     Source Type: Journal    
DOI: 10.4254/wjh.v6.i12.836     Document Type: Article

References (67)

1. Poon RT, Fan ST, Lo CM, Liu CL, Wong J. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg 2002; 235: 373-382 [PMID: 11882759 DOI: 101097/00000658-200203000-00009].
2. Poon RT, Fan ST, Lo CM, Liu CL, Wong J. Difference in tumor invasiveness in cirrhotic patients with hepatocellular carcinoma fulfilling the Milan criteria treated by resection and transplantation: impact on long-term survival. Ann Surg 2007; 245: 51-58 [PMID: 17197965 DOI: 10.1097/01.sla.0000225255.01668.65].
3. Arii S, Teramoto K, Kawamura T, Okamoto H, Kaido T, Mori A, Imamura M. Characteristics of recurrent hepatocellular carcinoma in Japan and our surgical experience. J Hepatobiliary Pancreat Surg 2001; 8: 397-403 [PMID: 11702247 DOI: 101007/s005340100000].
4. Poon RT, Fan ST, Lo CM, Liu CL, Wong J. Intrahepatic recurrence after curative resection of hepatocellular carcinoma: long-term results of treatment and prognostic factors. Ann Surg 1999; 229: 216-222 [PMID: 10024103 DOI: 10.1097/00000658-199902000-00009].
5. Chen WT, Chau GY, Lui WY, Tsay SH, King KL, Loong CC, Wu CW. Recurrent hepatocellular carcinoma after hepatic resection: prognostic factors and long-term outcome. Eur J Surg Oncol 2004; 30: 414-420 [PMID: 15063895 DOI: 10.1016/j.ejso.2004.01.013].
6. Tralhão JG, Dagher I, Lino T, Roudié J, Franco D. Treatment of tumour recurrence after resection of hepatocellular carcinoma. Analysis of 97 consecutive patients. Eur J Surg Oncol 2007; 33: 746-751 [PMID: 17188454 DOI: 10.1016/j.ejso.2006.11.015].
7. Nakajima Y, Ko S, Kanamura T, Nagao M, Kanehiro H, Hisanaga M, Aomatsu Y, Ikeda N, Nakano H. Repeat liver resection for hepatocellular carcinoma. J Am Coll Surg 2001; 192: 339-344 [PMID: 11245376].
8. Sugimachi K, Maehara S, Tanaka S, Shimada M, Sugimachi K. Repeat hepatectomy is the most useful treatment for recurrent hepatocellular carcinoma. J Hepatobiliary Pancreat Surg 2001; 8: 410-416 [PMID: 11702249].
9. Minagawa M, Makuuchi M, Takayama T, Kokudo N. Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg 2003; 238: 703-710 [PMID: 14578733 DOI: 10.1097/01.sla.0000094549.11754.e6].
10. Taura K, Ikai I, Hatano E, Fujii H, Uyama N, Shimahara Y. Implication of frequent local ablation therapy for intrahepatic recurrence in prolonged survival of patients with hepatocellular carcinoma undergoing hepatic resection: an analysis of 610 patients over 16 years old. Ann Surg 2006; 244: 265-273 [PMID: 16858190 DOI: 10.1097/01.sla.0000217921.28563.55].
11. Itamoto T, Nakahara H, Amano H, Kohashi T, Ohdan H, Tashiro H, Asahara T. Repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery 2007; 141: 589-597 [PMID: 17462458 DOI: 10.1016/j.surg.2006.12.014].
12. Shimada K, Sakamoto Y, Esaki M, Kosuge T, Morizane C, Ikeda M, Ueno H, Okusaka T, Arai Y, Takayasu K. Analysis of prognostic factors affecting survival after initial recurrence and treatment efficacy for recurrence in patients undergoing potentially curative hepatectomy for hepatocellular carcinoma. Ann Surg Oncol 2007; 14: 2337-2347 [PMID: 17503155 DOI: 10.1245/s10434-007-9415-7].
13. Liang HH, Chen MS, Peng ZW, Zhang YJ, Zhang YQ, Li JQ, Lau WY. Percutaneous radiofrequency ablation versus repeat hepatectomy for recurrent hepatocellular carcinoma: a retrospective study. Ann Surg Oncol 2008; 15: 3484-3493 [PMID: 18679754 DOI: 10.1245/s10434-008-0076-y].
14. Choi GH, Kim DH, Kang CM, Kim KS, Choi JS, Lee WJ, Kim BR. Prognostic factors and optimal treatment strategy for intrahepatic nodular recurrence after curative resection of hepatocellular carcinoma. Ann Surg Oncol 2008; 15: 618-629 [PMID: 18004628 DOI: 10.1245/s10434-007-9671-6].
15. Wu CC, Cheng SB, Yeh DC, Wang J, P'eng FK. Second and third hepatectomies for recurrent hepatocellular carcinoma are justified. Br J Surg 2009; 96: 1049-1057 [PMID: 19672929 DOI: 10.1002/bjs.6690].
16. Kishi Y, Saiura A, Yamamoto J, Koga R, Seki M, Morimura R, Yoshioka R, Kokudo N, Yamaguchi T. Repeat treatment for recurrent hepatocellular carcinoma: is it validated? Langenbecks Arch Surg 2011; 396: 1093-1100 [PMID: 21847622 DOI: 101007/s00423-011-0837-0].
17. Huang ZY, Liang BY, Xiong M, Zhan DQ, Wei S, Wang GP, Chen YF, Chen XP. Long-term outcomes of repeat hepatic resection in patients with recurrent hepatocellular carcinoma and analysis of recurrent types and their prognosis: a single-center experience in China. Ann Surg Oncol 2012; 19: 2515-2525 [PMID: 22395985 DOI: 10.1245/s10434-012-2269-7].
18. Tsujita E, Yamashita Y, Takeishi K, Matsuyama A, Tsutsui S, Matsuda H, Toshima T, Taketomi A, Shirabe K, Ishida T, Maehara Y. Poor prognostic factors after repeat hepatectomy for recurrent hepatocellular carcinoma in the modern era. Am Surg 2012; 78: 419-425 [PMID: 22472398].
19. Yamashita Y, Shirabe K, Tsuijita E, Takeishi K, Ikegami T, Yoshizumi T, Soejima Y, Ikeda T, Utsunomiya T, Maehara Y. Third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery 2013; 154: 1038-1045 [PMID: 23973109 DOI: 10.1016/j.surg.2013.04.046].
20. Matsuda M, Fujii H, Kono H, Matsumoto Y. Surgical treatment of recurrent hepatocellular carcinoma based on the mode of recurrence: repeat hepatic resection or ablation are good choices for patients with recurrent multicentric cancer. J Hepatobiliary Pancreat Surg 2001; 8: 353-359 [PMID: 11521181].
21. Japan LCSGo. General rules for the clinical and pathological study of primary liver cancer. 2nd ed. Tokyo: Kenehara, 2003.
22. Poon RT, Ngan H, Lo CM, Liu CL, Fan ST, Wong J. Transarterial chemoembolization for inoperable hepatocellular carcinoma and postresection intrahepatic recurrence. J Surg Oncol 2000; 73: 109-114 [PMID: 10694648].
23. Yang W, Chen MH, Yin SS, Yan K, Gao W, Wang YB, Huo L, Zhang XP, Xing BC. Radiofrequency ablation of recurrent hepatocellular carcinoma after hepatectomy: therapeutic efficacy on early-and late-phase recurrence. AJR Am J Roentgenol 2006; 186: S275-S283 [PMID: 16632688].
24. Choi D, Lim HK, Rhim H, Kim YS, Yoo BC, Paik SW, Joh JW, Park CK. Percutaneous radiofrequency ablation for recurrent hepatocellular carcinoma after hepatectomy: longterm results and prognostic factors. Ann Surg Oncol 2007; 14: 2319-2329 [PMID: 17522947 DOI: 10.1245/s10434-006-9220-8].
25. Okuwaki Y, Nakazawa T, Kokubu S, Hidaka H, Tanaka Y, Takada J, Watanabe M, Shibuya A, Minamino T, Saigenji K. Repeat radiofrequency ablation provides survival benefit in patients with intrahepatic distant recurrence of hepatocellular carcinoma. Am J Gastroenterol 2009; 104: 2747-2753 [PMID: 19603009].
26. Belghiti J, Cortes A, Abdalla EK, Régimbeau JM, Prakash K, Durand F, Sommacale D, Dondero F, Lesurtel M, Sauvanet A, Farges O, Kianmanesh R. Resection prior to liver transplantation for hepatocellular carcinoma. Ann Surg 2003; 238: 885-892; discussion 892-893 [PMID: 14631225 DOI: 101097/01.sla.0000098621.74851.65].
27. Hwang S, Lee SG, Moon DB, Ahn CS, Kim KH, Lee YJ, Ha TY, Song GW. Salvage living donor liver transplantation after prior liver resection for hepatocellular carcinoma. Liver Transpl 2007; 13: 741-746 [PMID: 17457860 DOI: 10.1002/lt.21157].
28. Liu F, Wei Y, Wang W, Chen K, Yan L, Wen T, Zhao J, Xu M, Li B. Salvage liver transplantation for recurrent hepatocellular carcinoma within UCSF criteria after liver resection. PLoS One 2012; 7: e48932 [PMID: 23145027 DOI: 10.1371/journal.pone.0048932].
29. Lee S, Hyuck David Kwon C, Man Kim J, Joh JW, Woon Paik S, Kim BW, Wang HJ, Lee KW, Suh KS, Lee SK. Time of hepatocellular carcinoma recurrence after liver resection and alpha-fetoprotein are important prognostic factors for salvage liver transplantation. Liver Transpl 2014; 20: 1057-1063 [PMID: 24862741 DOI: 10.1002/lt.23919].
30. Del Gaudio M, Ercolani G, Ravaioli M, Cescon M, Lauro A, Vivarelli M, Zanello M, Cucchetti A, Vetrone G, Tuci F, Ramacciato G, Grazi GL, Pinna AD. Liver transplantation for recurrent hepatocellular carcinoma on cirrhosis after liver resection: University of Bologna experience. Am J Transplant 2008; 8: 1177-1185 [PMID: 18444925 DOI: 10.1111/j.1600-6143.2008.02229.x].
31. Fuks D, Dokmak S, Paradis V, Diouf M, Durand F, Belghiti J. Benefit of initial resection of hepatocellular carcinoma followed by transplantation in case of recurrence: an intention-to-treat analysis. Hepatology 2012; 55: 132-140 [PMID: 21932387 DOI: 10.1002/hep.24680].
32. Torzilli G, Del Fabbro D, Palmisano A, Marconi M, Makuuchi M, Montorsi M. Salvage hepatic resection after incomplete interstitial therapy for primary and secondary liver tumours. Br J Surg 2007; 94: 208-213 [PMID: 17149716 DOI: 101002/bjs.5603].
33. Masuda T, Beppu T, Ishiko T, Horino K, Baba Y, Mizumoto T, Hayashi H, Okabe H, Horlad H, Doi K, Okabe K, Takamori H, Hirota M, Iyama K, Baba H. Intrahepatic dissemination of hepatocellular carcinoma after local ablation therapy. J Hepatobiliary Pancreat Surg 2008; 15: 589-595 [PMID: 18987928 DOI: 10.1007/s00534-007-1288-4].
34. Portolani N, Baiocchi GL, Coniglio A, Grazioli L, Frassi E, Gheza F, Giulini SM. Sequential multidisciplinary treatment of hepatocellular carcinoma: the role of surgery as rescue therapy for failure of percutaneous ablation therapies. J Surg Oncol 2009; 100: 580-584 [PMID: 19697354 DOI: 10.1002/jso.21375].
35. Sugo H, Ishizaki Y, Yoshimoto J, Imamura H, Kawasaki S. Salvage hepatectomy for local recurrent hepatocellular carcinoma after ablation therapy. Ann Surg Oncol 2012; 19: 2238-2245 [PMID: 22302262 DOI: 10.1245/s10434-012-2220-y].
36. 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 2014; Epub ahead of print [PMID: 24552247 DOI: 10.1111/hepr.12313].
37. Tanaka T, Yamanaka N, Oriyama T, Furukawa K, Okamoto E. Factors regulating tumor pressure in hepatocellular carcinoma and implications for tumor spread. Hepatology 1997; 26 283-287 [PMID: 9252135 DOI: 10.1002/hep.510260205].
38. Ruzzenente A, Manzoni GD, Molfetta M, Pachera S, Genco B, Donataccio M, Guglielmi A. Rapid progression of hepatocellular carcinoma after Radiofrequency Ablation. World J Gastroenterol 2004; 10: 1137-1140 [PMID: 15069713].
39. Takayama T, Makuuchi M, Hasegawa K. Single HCC smaller than 2 cm: surgery or ablation?: surgeon's perspective. J Hepatobiliary Pancreat Sci 2010; 17: 422-424 [PMID: 19936598 DOI: 10.1007/s00534-009-0239-7].
40. Kudo M, Chung H. Single HCC between 2 and 5 cm: the grey zone: hepatologist's perspective. J Hepatobiliary Pancreat Sci 2010; 17: 434-437 [PMID: 19902137 DOI: 10.1007/s00534-009-0242-z].
41. Huang J, Yan L, Cheng Z, Wu H, Du L, Wang J, Xu Y, Zeng Y. A randomized trial comparing radiofrequency ablation and surgical resection for HCC conforming to the Milan criteria. Ann Surg 2010; 252: 903-912 [PMID: 21107100 DOI: 10.1097/SLA.0b013e3181efc656].
42. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, Montalto F, Ammatuna M, Morabito A, Gennari L. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 1996; 334: 693-699 [PMID: 8594428].
43. Hasegawa K, Kokudo N, Makuuchi M, Izumi N, Ichida T, Kudo M, Ku Y, Sakamoto M, Nakashima O, Matsui O, Matsuyama Y. Comparison of resection and ablation for hepatocellular carcinoma: a cohort study based on a Japanese nationwide survey. J Hepatol 2013; 58: 724-729 [PMID: 23178708 DOI: 10.1016/j.jhep.2012.11.009].
44. Bruix J, Sherman M. Management of hepatocellular carcinoma. Hepatology 2005; 42: 1208-1236 [PMID: 16250051 DOI: 101002/hep.20933].
45. Bruix J, Sherman M, Llovet JM, Beaugrand M, Lencioni R, Burroughs AK, Christensen E, Pagliaro L, Colombo M, Rodés J. Clinical management of hepatocellular carcinoma. Conclusions of the Barcelona-2000 EASL conference. European Association for the Study of the Liver. J Hepatol 2001; 35 421-430 [PMID: 11592607].
46. Llovet JM, Brú C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 1999; 19 329-338 [PMID: 10518312 DOI: 10.1055/s-2007-1007122].
47. 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. Development of evidencebased clinical guidelines for the diagnosis and treatment of hepatocellular carcinoma in Japan. Hepatol Res 2008; 38: 37-51 [PMID: 18039202 DOI: 10.1111/j.1872-034X.2007.00216.x].
48. Itoh S, Morita K, Ueda S, Sugimachi K, Yamashita Y, Gion T, Fukuzawa K, Wakasugi K, Taketomi A, Maehara Y. Longterm results of hepatic resection combined with intraoperative local ablation therapy for patients with multinodular hepatocellular carcinomas. Ann Surg Oncol 2009; 16: 3299-3307 [PMID: 19826875 DOI: 10.1245/s10434-009-0721-0].
49. Wakabayashi H, Ushiyama T, Ishimura K, Izuishi K, Karasawa Y, Masaki T, Watanabe S, Kuriyama S, Maeta H. Significance of reduction surgery in multidisciplinary treatment of advanced hepatocellular carcinoma with multiple intrahepatic lesions. J Surg Oncol 2003; 82: 98-103 [PMID: 12561065 DOI: 10.1002/jso.10203].
50. Folprecht G, Gruenberger T, Bechstein WO, Raab HR, Lordick F, Hartmann JT, Lang H, Frilling A, Stoehlmacher J, Weitz J, Konopke R, Stroszczynski C, Liersch T, Ockert D, Herrmann T, Goekkurt E, Parisi F, Köhne CH. Tumour response and secondary resectability of colorectal liver metastases following neoadjuvant chemotherapy with cetuximab: the CELIM randomised phase 2 trial. Lancet Oncol 2010; 11:38-47 [PMID: 19942479 DOI: 10.1016/S1470-2045(09)70330-4].
51. Beppu T, Miyamoto Y, Sakamoto Y, Imai K, Nitta H, Hayashi H, Chikamoto A, Watanabe M, Ishiko T, Baba H. Chemotherapy and targeted therapy for patients with initially unresectable colorectal liver metastases, focusing on conversion hepatectomy and long-term survival. Ann Surg Oncol 2014; 21 Suppl 3: S405-S413 [PMID: 24570379 DOI: 10.1245/s10434-014-3577-x].
52. D'angelica MI, Correa-Gallego C, Paty PB, Cercek A, Gewirtz AN, Chou JF, Capanu M, Kingham TP, Fong Y, Dematteo RP, Allen PJ, Jarnagin WR, Kemeny N. Phase II Trial of Hepatic Artery Infusional and Systemic Chemotherapy for Patients With Unresectable Hepatic Metastases From Colorectal Cancer: Conversion to Resection and Longterm Outcomes. Ann Surg 2014; Epub ahead of print [PMID: 24646562 DOI: 10.1097/SLA.0000000000000614].
53. Yao FY, Kerlan RK, Hirose R, Davern TJ, Bass NM, Feng S, Peters M, Terrault N, Freise CE, Ascher NL, Roberts JP. Excellent outcome following down-staging of hepatocellular carcinoma prior to liver transplantation: an intention-to-treat analysis. Hepatology 2008; 48: 819-827 [PMID: 18688876 DOI: 101002/hep.22412].
54. Lei JY, Yan LN, Wang WT. Transplantation vs resection for hepatocellular carcinoma with compensated liver function after downstaging therapy. World J Gastroenterol 2013; 19: 4400-4408 [PMID: 23885153 DOI: 10.3748/wjg.v19.i27.4400].
55. Fan J, Tang ZY, Yu YQ, Wu ZQ, Ma ZC, Zhou XD, Zhou J, Qiu SJ, Lu JZ. Improved survival with resection after transcatheter arterial chemoembolization (TACE) for unresectable hepatocellular carcinoma. Dig Surg 1998; 15: 674-678 [PMID: 9845635 DOI: 10.1159/000018676].
56. Tang ZY, Zhou XD, Ma ZC, Wu ZQ, Fan J, Qin LX, Yu Y. Downstaging followed by resection plays a role in improving prognosis of unresectable hepatocellular carcinoma. Hepatobiliary Pancreat Dis Int 2004; 3: 495-498 [PMID: 15567731].
57. Blazer DG, Kishi Y, Maru DM, Kopetz S, Chun YS, Overman MJ, Fogelman D, Eng C, Chang DZ, Wang H, Zorzi D, Ribero D, Ellis LM, Glover KY, Wolff RA, Curley SA, Abdalla EK, Vauthey JN. Pathologic response to preoperative chemotherapy: a new outcome end point after resection of hepatic colorectal metastases. J Clin Oncol 2008; 26: 5344-5351 [PMID: 18936472 DOI: 10.1200/JCO.2008.17.5299].
58. Ravaioli M, Grazi GL, Ercolani G, Fiorentino M, Cescon M, Golfieri R, Trevisani F, Grigioni WF, Bolondi L, Pinna AD. Partial necrosis on hepatocellular carcinoma nodules facilitates tumor recurrence after liver transplantation. Transplantation 2004; 78: 1780-1786 [PMID: 15614151].
59. Wu CC, Ho YZ, Ho WL, Wu TC, Liu TJ, P'eng FK. Preoperative transcatheter arterial chemoembolization for resectable large hepatocellular carcinoma: a reappraisal. Br J Surg 1995; 82 122-126 [PMID: 7881929].
60. Chen XP, Hu DY, Zhang ZW, Zhang BX, Chen YF, Zhang WG, Qiu FZ. Role of mesohepatectomy with or without transcatheter arterial chemoembolization for large centrally located hepatocellular carcinoma. Dig Surg 2007; 24: 208-213 [PMID: 17522469 DOI: 10.1159/000102901].
61. Kishi Y, Saiura A, Yamamoto J, Koga R, Seki M, Morimura R, Yoshioka R, Kokudo N, Yamaguchi T. Preoperative transarterial chemoembolization for hepatocellular carcinoma. Hepatogastroenterology 2012; 59: 2295-2299 [PMID: 23435144].
62. Adachi E, Matsumata T, Nishizaki T, Hashimoto H, Tsuneyoshi M, Sugimachi K. Effects of preoperative transcatheter hepatic arterial chemoembolization for hepatocellular carcinoma. The relationship between postoperative course and tumor necrosis. Cancer 1993; 72: 3593-3598 [PMID: 8252473].
63. Kulik LM, Carr BI, Mulcahy MF, Lewandowski RJ, Atassi B, Ryu RK, Sato KT, Benson A, Nemcek AA, Gates VL, Abe-cassis M, Omary RA, Salem R. Safety and efficacy of 90Y radiotherapy for hepatocellular carcinoma with and without portal vein thrombosis. Hepatology 2008; 47: 71-81 [PMID: 18027884 DOI: 10.1002/hep.21980].
64. Leung TW, Patt YZ, Lau WY, Ho SK, Yu SC, Chan AT, Mok TS, Yeo W, Liew CT, Leung NW, Tang AM, Johnson PJ. Complete pathological remission is possible with systemic combination chemotherapy for inoperable hepatocellular carcinoma. Clin Cancer Res 1999; 5: 1676-1681 [PMID: 10430068].
65. Lau WY, Ho SK, Yu SC, Lai EC, Liew CT, Leung TW. Salvage surgery following downstaging of unresectable hepatocellular carcinoma. Ann Surg 2004; 240: 299-305 [PMID: 15273555 DOI: 10.1097/01.sla.0000133123.11932.19].
66. Yeo W, Mok TS, Zee B, Leung TW, Lai PB, Lau WY, Koh J, Mo FK, Yu SC, Chan AT, Hui P, Ma B, Lam KC, Ho WM, Wong HT, Tang A, Johnson PJ. A randomized phase III study of doxorubicin versus cisplatin/interferon alpha-2b/doxorubicin/fluorouracil (PIAF) combination chemotherapy for unresectable hepatocellular carcinoma. J Natl Cancer Inst 2005; 97: 1532-1538 [PMID: 16234567 DOI: 10.1093/jnci/dji315].
67. Kaseb AO, Shindoh J, Patt YZ, Roses RE, Zimmitti G, Lozano RD, Hassan MM, Hassabo HM, Curley SA, Aloia TA, Abbruzzese JL, Vauthey JN. Modified cisplatin/interferon a-2b/doxorubicin/5-fluorouracil (PIAF) chemotherapy in patients with no hepatitis or cirrhosis is associated with improved response rate, resectability, and survival of initially unresectable hepatocellular carcinoma. Cancer 2013; 119: 3334-3342 [PMID: 23821538 DOI: 10.1002/cncr.28209].