Skip to main content
Top
Published in: Langenbeck's Archives of Surgery 5/2017

01-08-2017 | ORIGINAL ARTICLE

Treatment and outcomes of recurrent hepatocellular carcinomas

Authors: Gaëtan-Romain Joliat, Pierre Allemann, Ismail Labgaa, Nicolas Demartines, Nermin Halkic

Published in: Langenbeck's Archives of Surgery | Issue 5/2017

Login to get access

Abstract

Purpose

Surgery is one of the best options for curative treatment of hepatocellular carcinomas (HCC). Recurrences are nevertheless common (45–75%). This study aimed to compare overall survival (OS) of patients with recurrent HCC after primary resection to OS of patients without recurrence.

Methods

A retrospective review of all HCC patients operated between 1993 and 2015 was performed. Median and 5-year OS were calculated.

Results

This study included 147 HCC patients. Sixty-seven patients presented a recurrence (46%). Patients with recurrence had a worse prognosis than those without recurrence (median OS 63 vs. 82 months, 5-year OS 47 vs. 54%, p = 0.036). First-line performed treatments were radiofrequency ablation (18, RFA), chemo-embolization (16, TACE), repeat hepatectomy (10), systemic chemotherapy (4), radio-embolization (1), and alcoholization (1). Palliative care was performed in 17 patients. Median OS of patients treated by RFA, TACE, or repeat hepatectomy were similar (77, 71, and 84 months, p = 0.735). Patients treated with chemotherapy/palliative care had lower median OS compared to interventional treatments (20 vs. 77 months, p < 0.0001).

Conclusions

Recurrence after surgical HCC resection is frequent and negatively impacts OS. Interventional treatments of recurrences offered improved outcomes compared to medical care. In selected patients, RFA, TACE, and repeat hepatectomy allowed similar OS as non-recurrent cases.
Literature
2.
go back to reference Lafaro K, Grandhi MS, Herman JM, Pawlik TM (2016) The importance of surgical margins in primary malignancies of the liver. J Surg Oncol 113:296–303CrossRefPubMed Lafaro K, Grandhi MS, Herman JM, Pawlik TM (2016) The importance of surgical margins in primary malignancies of the liver. J Surg Oncol 113:296–303CrossRefPubMed
3.
go back to reference Sangiovanni A, Colombo M (2016) Treatment of hepatocellular carcinoma: beyond international guidelines. Liver Int 36(Suppl 1):124–129CrossRefPubMed Sangiovanni A, Colombo M (2016) Treatment of hepatocellular carcinoma: beyond international guidelines. Liver Int 36(Suppl 1):124–129CrossRefPubMed
4.
go back to reference Liu H, Wang Z-G, Fu S-Y, Li A-J, Pan Z-Y, Zhou W-P et al (2016) Randomized clinical trial of chemoembolization plus radiofrequency ablation versus partial hepatectomy for hepatocellular carcinoma within the Milan criteria. Br J Surg 103:348–356CrossRefPubMed Liu H, Wang Z-G, Fu S-Y, Li A-J, Pan Z-Y, Zhou W-P et al (2016) Randomized clinical trial of chemoembolization plus radiofrequency ablation versus partial hepatectomy for hepatocellular carcinoma within the Milan criteria. Br J Surg 103:348–356CrossRefPubMed
5.
go back to reference Meniconi RL, Komatsu S, Perdigao F, Boëlle P-Y, Soubrane O, Scatton O (2015) Recurrent hepatocellular carcinoma: a Western strategy that emphasizes the impact of pathologic profile of the first resection. Surgery 157:454–462CrossRefPubMed Meniconi RL, Komatsu S, Perdigao F, Boëlle P-Y, Soubrane O, Scatton O (2015) Recurrent hepatocellular carcinoma: a Western strategy that emphasizes the impact of pathologic profile of the first resection. Surgery 157:454–462CrossRefPubMed
6.
go back to reference An HJ, Shin WY, Lee K-Y, Ahn S-I (2015) A comparison of the risk factors of intrahepatic recurrence, early recurrence, and multiple recurrences after resection for single nodular hepatocellular carcinoma. Korean J Hepato-Biliary-Pancreat Surg 19:89–97CrossRef An HJ, Shin WY, Lee K-Y, Ahn S-I (2015) A comparison of the risk factors of intrahepatic recurrence, early recurrence, and multiple recurrences after resection for single nodular hepatocellular carcinoma. Korean J Hepato-Biliary-Pancreat Surg 19:89–97CrossRef
7.
go back to reference Hwang S, Lee Y-J, Kim K-H, Ahn C-S, Moon D-B, Ha T-Y et al (2015) The impact of tumor size on long-term survival outcomes after resection of solitary hepatocellular carcinoma: single-institution experience with 2558 patients. J Gastrointest Surg 19:1281–1290CrossRefPubMed Hwang S, Lee Y-J, Kim K-H, Ahn C-S, Moon D-B, Ha T-Y et al (2015) The impact of tumor size on long-term survival outcomes after resection of solitary hepatocellular carcinoma: single-institution experience with 2558 patients. J Gastrointest Surg 19:1281–1290CrossRefPubMed
8.
go back to reference Tabrizian P, Jibara G, Shrager B, Schwartz M, Roayaie S (2015) Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg 261:947–955CrossRefPubMed Tabrizian P, Jibara G, Shrager B, Schwartz M, Roayaie S (2015) Recurrence of hepatocellular cancer after resection: patterns, treatments, and prognosis. Ann Surg 261:947–955CrossRefPubMed
9.
go back to reference Wang D-Y, Liu L, Qi X-S, Su C-P, Chen X, Liu X et al (2015) Hepatic re-resection versus transarterial chemoembolization for the treatment of recurrent hepatocellular carcinoma after initial resection: a systematic review and meta-analysis. Asian Pac J Cancer Prev 16:5573–5578CrossRefPubMed Wang D-Y, Liu L, Qi X-S, Su C-P, Chen X, Liu X et al (2015) Hepatic re-resection versus transarterial chemoembolization for the treatment of recurrent hepatocellular carcinoma after initial resection: a systematic review and meta-analysis. Asian Pac J Cancer Prev 16:5573–5578CrossRefPubMed
10.
go back to reference Yamashita Y-I, Yoshida Y, Kurihara T, Itoh S, Harimoto N, Ikegami T et al (2015) Surgical results for recurrent hepatocellular carcinoma after curative hepatectomy: repeat hepatectomy versus salvage living donor liver transplantation. Liver Transplant 21:961–968CrossRef Yamashita Y-I, Yoshida Y, Kurihara T, Itoh S, Harimoto N, Ikegami T et al (2015) Surgical results for recurrent hepatocellular carcinoma after curative hepatectomy: repeat hepatectomy versus salvage living donor liver transplantation. Liver Transplant 21:961–968CrossRef
12.
go back to reference Song KD, Lim HK, Rhim H, Lee MW, Kim Y-S, Lee WJ et al (2015) Repeated hepatic resection versus radiofrequency ablation for recurrent hepatocellular carcinoma after hepatic resection: a propensity score matching study. Radiology 275:599–608CrossRefPubMed Song KD, Lim HK, Rhim H, Lee MW, Kim Y-S, Lee WJ et al (2015) Repeated hepatic resection versus radiofrequency ablation for recurrent hepatocellular carcinoma after hepatic resection: a propensity score matching study. Radiology 275:599–608CrossRefPubMed
13.
go back to reference Fukuhara T, Aikata H, Hyogo H, Honda Y, Morio K, Morio R et al (2015) Efficacy of radiofrequency ablation for initial recurrent hepatocellular carcinoma after curative treatment: comparison with primary cases. Eur J Radiol 84:1540–1545CrossRefPubMed Fukuhara T, Aikata H, Hyogo H, Honda Y, Morio K, Morio R et al (2015) Efficacy of radiofrequency ablation for initial recurrent hepatocellular carcinoma after curative treatment: comparison with primary cases. Eur J Radiol 84:1540–1545CrossRefPubMed
14.
go back to reference Chen X, Chen Y, Li Q, Ma D, Shen B, Peng C (2015) Radiofrequency ablation versus surgical resection for intrahepatic hepatocellular carcinoma recurrence: a meta-analysis. J Surg Res 195:166–174CrossRefPubMed Chen X, Chen Y, Li Q, Ma D, Shen B, Peng C (2015) Radiofrequency ablation versus surgical resection for intrahepatic hepatocellular carcinoma recurrence: a meta-analysis. J Surg Res 195:166–174CrossRefPubMed
15.
go back to reference Mazzaferro V, Bhoori S, Sposito C, Bongini M, Langer M, Miceli R et al (2011) Milan criteria in liver transplantation for hepatocellular carcinoma: an evidence-based analysis of 15 years of experience. Liver Transplant 17(Suppl 2):S44–S57CrossRef Mazzaferro V, Bhoori S, Sposito C, Bongini M, Langer M, Miceli R et al (2011) Milan criteria in liver transplantation for hepatocellular carcinoma: an evidence-based analysis of 15 years of experience. Liver Transplant 17(Suppl 2):S44–S57CrossRef
16.
go back to reference Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefPubMedPubMedCentral Dindo D, Demartines N, Clavien P-A (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213CrossRefPubMedPubMedCentral
17.
go back to reference Slankamenac K, Nederlof N, Pessaux P, de Jonge J, Wijnhoven BPL, Breitenstein S, et al (2014) The comprehensive complication index: a novel and more sensitive endpoint for assessing outcome and reducing sample size in randomized controlled trials. Ann Surg 260:757-762-763 Slankamenac K, Nederlof N, Pessaux P, de Jonge J, Wijnhoven BPL, Breitenstein S, et al (2014) The comprehensive complication index: a novel and more sensitive endpoint for assessing outcome and reducing sample size in randomized controlled trials. Ann Surg 260:757-762-763
18.
go back to reference Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET et al (1982) Toxicity and response criteria of the eastern cooperative oncology group. Am J Clin Oncol 5:649–655CrossRefPubMed Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET et al (1982) Toxicity and response criteria of the eastern cooperative oncology group. Am J Clin Oncol 5:649–655CrossRefPubMed
19.
go back to reference Zhang X, Li C, Wen T, Yan L, Li B, Yang J et al (2015) Appropriate treatment strategies for intrahepatic recurrence after curative resection of hepatocellular carcinoma initially within the Milan criteria: according to the recurrence pattern. Eur J Gastroenterol Hepatol 27:933–940CrossRefPubMed Zhang X, Li C, Wen T, Yan L, Li B, Yang J et al (2015) Appropriate treatment strategies for intrahepatic recurrence after curative resection of hepatocellular carcinoma initially within the Milan criteria: according to the recurrence pattern. Eur J Gastroenterol Hepatol 27:933–940CrossRefPubMed
20.
go back to reference Shah SA, Cleary SP, Wei AC, Yang I, Taylor BR, Hemming AW et al (2007) Recurrence after liver resection for hepatocellular carcinoma: risk factors, treatment, and outcomes. Surgery 141:330–339CrossRefPubMed Shah SA, Cleary SP, Wei AC, Yang I, Taylor BR, Hemming AW et al (2007) Recurrence after liver resection for hepatocellular carcinoma: risk factors, treatment, and outcomes. Surgery 141:330–339CrossRefPubMed
21.
go back to reference Hou Y-F, Li B, Wei Y-G, Yang J-Y, Wen T-F, Xu M-Q et al (2015) Second hepatectomy improves survival in patients with microvascular invasive hepatocellular carcinoma meeting the Milan criteria. Medicine (Baltimore) 94:e2070CrossRef Hou Y-F, Li B, Wei Y-G, Yang J-Y, Wen T-F, Xu M-Q et al (2015) Second hepatectomy improves survival in patients with microvascular invasive hepatocellular carcinoma meeting the Milan criteria. Medicine (Baltimore) 94:e2070CrossRef
22.
go back to reference Thomasset SC, Dennison AR, Garcea G (2015) Ablation for recurrent hepatocellular carcinoma: a systematic review of clinical efficacy and prognostic factors. World J Surg 39:1150–1160CrossRefPubMed Thomasset SC, Dennison AR, Garcea G (2015) Ablation for recurrent hepatocellular carcinoma: a systematic review of clinical efficacy and prognostic factors. World J Surg 39:1150–1160CrossRefPubMed
23.
go back to reference Zhang C, Zhang J, Li X, Li L, Li X, Zhou X (2015) Is radiofrequency ablation equal to surgical re-resection for recurrent hepatocellular carcinoma meeting the Milan criteria? A meta-analysis. J BUON 20:223–230PubMed Zhang C, Zhang J, Li X, Li L, Li X, Zhou X (2015) Is radiofrequency ablation equal to surgical re-resection for recurrent hepatocellular carcinoma meeting the Milan criteria? A meta-analysis. J BUON 20:223–230PubMed
24.
go back to reference Jin Y-J, Lee J-W, Lee OH, Chung HJ, Kim YS, Lee JI et al (2014) Transarterial chemoembolization versus surgery/radiofrequency ablation for recurrent hepatocellular carcinoma with or without microvascular invasion. J Gastroenterol Hepatol 29:1056–1064CrossRefPubMed Jin Y-J, Lee J-W, Lee OH, Chung HJ, Kim YS, Lee JI et al (2014) Transarterial chemoembolization versus surgery/radiofrequency ablation for recurrent hepatocellular carcinoma with or without microvascular invasion. J Gastroenterol Hepatol 29:1056–1064CrossRefPubMed
25.
go back to reference Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S et al (2003) Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 38:200–207CrossRefPubMed Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S et al (2003) Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol 38:200–207CrossRefPubMed
26.
go back to reference Shah SA, Greig PD, Gallinger S, Cattral MS, Dixon E, Kim RD et al (2006) Factors associated with early recurrence after resection for hepatocellular carcinoma and outcomes. J Am Coll Surg 202:275–283CrossRefPubMed Shah SA, Greig PD, Gallinger S, Cattral MS, Dixon E, Kim RD et al (2006) Factors associated with early recurrence after resection for hepatocellular carcinoma and outcomes. J Am Coll Surg 202:275–283CrossRefPubMed
27.
28.
go back to reference Ali MA, Li W-F, Wang J-H, Lin C-C, Chen Y-J, Lin T-L et al (2016) Impact of pathological features of primary hepatocellular carcinoma on the outcomes of intrahepatic recurrence management: single center experience from southern Taiwan. HPB 18:851–860CrossRefPubMedPubMedCentral Ali MA, Li W-F, Wang J-H, Lin C-C, Chen Y-J, Lin T-L et al (2016) Impact of pathological features of primary hepatocellular carcinoma on the outcomes of intrahepatic recurrence management: single center experience from southern Taiwan. HPB 18:851–860CrossRefPubMedPubMedCentral
29.
go back to reference Wan X, Zhai X, Yan Z, Yang P, Li J, Wu D et al (2016) Retrospective analysis of transarterial chemoembolization and sorafenib in Chinese patients with unresectable and recurrent hepatocellular carcinoma. Oncotarget 7:83806–83816PubMedPubMedCentral Wan X, Zhai X, Yan Z, Yang P, Li J, Wu D et al (2016) Retrospective analysis of transarterial chemoembolization and sorafenib in Chinese patients with unresectable and recurrent hepatocellular carcinoma. Oncotarget 7:83806–83816PubMedPubMedCentral
30.
go back to reference Chen R, Gan Y, Ge N, Chen Y, Wang Y, Zhang B et al (2016) Transarterial chemoembolization versus radiofrequency ablation for recurrent hepatocellular carcinoma after resection within Barcelona clinic liver cancer stage 0/a: a retrospective comparative study. J Vasc Interv Radiol 27:1829–1836CrossRefPubMed Chen R, Gan Y, Ge N, Chen Y, Wang Y, Zhang B et al (2016) Transarterial chemoembolization versus radiofrequency ablation for recurrent hepatocellular carcinoma after resection within Barcelona clinic liver cancer stage 0/a: a retrospective comparative study. J Vasc Interv Radiol 27:1829–1836CrossRefPubMed
31.
go back to reference Zhang J, Zhou Z-G, Huang Z-X, Yang K-L, Chen J-C, Chen J-B et al (2016) Prospective, single-center cohort study analyzing the efficacy of complete laparoscopic resection on recurrent hepatocellular carcinoma. Chin J Cancer 35:25CrossRefPubMedPubMedCentral Zhang J, Zhou Z-G, Huang Z-X, Yang K-L, Chen J-C, Chen J-B et al (2016) Prospective, single-center cohort study analyzing the efficacy of complete laparoscopic resection on recurrent hepatocellular carcinoma. Chin J Cancer 35:25CrossRefPubMedPubMedCentral
32.
go back to reference Zou Q, Li J, Wu D, Yan Z, Wan X, Wang K et al (2016) Nomograms for pre-operative and post-operative prediction of long-term survival of patients who underwent repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg Oncol 23:2618–2626CrossRefPubMed Zou Q, Li J, Wu D, Yan Z, Wan X, Wang K et al (2016) Nomograms for pre-operative and post-operative prediction of long-term survival of patients who underwent repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg Oncol 23:2618–2626CrossRefPubMed
33.
go back to reference Koh PS, Chan ACY, Cheung TT, Chok KSH, Dai WC, Poon RTP et al (2016) Efficacy of radiofrequency ablation compared with transarterial chemoembolization for the treatment of recurrent hepatocellular carcinoma: a comparative survival analysis. HPB 18:72–78CrossRefPubMedPubMedCentral Koh PS, Chan ACY, Cheung TT, Chok KSH, Dai WC, Poon RTP et al (2016) Efficacy of radiofrequency ablation compared with transarterial chemoembolization for the treatment of recurrent hepatocellular carcinoma: a comparative survival analysis. HPB 18:72–78CrossRefPubMedPubMedCentral
34.
go back to reference Yong C-C, Tsai M-C, Lin C-C, Wang C-C, Lu S-N, Hung C-H et al (2016) Comparison of salvage living donor liver transplantation and local regional therapy for recurrent hepatocellular carcinoma. World J Surg 40:2472–2480CrossRefPubMed Yong C-C, Tsai M-C, Lin C-C, Wang C-C, Lu S-N, Hung C-H et al (2016) Comparison of salvage living donor liver transplantation and local regional therapy for recurrent hepatocellular carcinoma. World J Surg 40:2472–2480CrossRefPubMed
35.
go back to reference Zu Q-Q, Liu S, Zhou C-G, Yang Z-Q, Xia J-G, Zhao L-B et al (2015) Chemoembolization of recurrent hepatoma after curative resection: prognostic factors. AJR Am J Roentgenol 204:1322–1328CrossRefPubMed Zu Q-Q, Liu S, Zhou C-G, Yang Z-Q, Xia J-G, Zhao L-B et al (2015) Chemoembolization of recurrent hepatoma after curative resection: prognostic factors. AJR Am J Roentgenol 204:1322–1328CrossRefPubMed
36.
go back to reference Wang K, Liu G, Li J, Yan Z, Xia Y, Wan X et al (2015) Early intrahepatic recurrence of hepatocellular carcinoma after hepatectomy treated with re-hepatectomy, ablation or chemoembolization: a prospective cohort study. Eur J Surg Oncol 41:236–242CrossRefPubMed Wang K, Liu G, Li J, Yan Z, Xia Y, Wan X et al (2015) Early intrahepatic recurrence of hepatocellular carcinoma after hepatectomy treated with re-hepatectomy, ablation or chemoembolization: a prospective cohort study. Eur J Surg Oncol 41:236–242CrossRefPubMed
37.
go back to reference Mise Y, Hasegawa K, Shindoh J, Ishizawa T, Aoki T, Sakamoto Y et al (2015) The feasibility of third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 262:347–357CrossRefPubMed Mise Y, Hasegawa K, Shindoh J, Ishizawa T, Aoki T, Sakamoto Y et al (2015) The feasibility of third or more repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 262:347–357CrossRefPubMed
38.
go back to reference Yamashita Y-I, Imai D, Bekki Y, Takeishi K, Tsujita E, Ikegami T et al (2014) Surgical outcomes of anatomical resection for solitary recurrent hepatocellular carcinoma. Anticancer Res 34:4421–4426PubMed Yamashita Y-I, Imai D, Bekki Y, Takeishi K, Tsujita E, Ikegami T et al (2014) Surgical outcomes of anatomical resection for solitary recurrent hepatocellular carcinoma. Anticancer Res 34:4421–4426PubMed
39.
go back to reference Cheng Y-C, Chen T-W, Fan H-L, Yu C-Y, Chang H-C, Hsieh C-B (2014) Transarterial chemoembolization for intrahepatic multiple recurrent HCC after liver resection or transplantation. Ann Transplant 19:309–301CrossRefPubMed Cheng Y-C, Chen T-W, Fan H-L, Yu C-Y, Chang H-C, Hsieh C-B (2014) Transarterial chemoembolization for intrahepatic multiple recurrent HCC after liver resection or transplantation. Ann Transplant 19:309–301CrossRefPubMed
Metadata
Title
Treatment and outcomes of recurrent hepatocellular carcinomas
Authors
Gaëtan-Romain Joliat
Pierre Allemann
Ismail Labgaa
Nicolas Demartines
Nermin Halkic
Publication date
01-08-2017
Publisher
Springer Berlin Heidelberg
Published in
Langenbeck's Archives of Surgery / Issue 5/2017
Print ISSN: 1435-2443
Electronic ISSN: 1435-2451
DOI
https://doi.org/10.1007/s00423-017-1582-9

Other articles of this Issue 5/2017

Langenbeck's Archives of Surgery 5/2017 Go to the issue