European Radiology

, Volume 28, Issue 8, pp 3522–3531 | Cite as

Combined transcatheter arterial chemoembolization and radiofrequency ablation versus hepatectomy for recurrent hepatocellular carcinoma after initial surgery: a propensity score matching study

  • Zhenwei Peng
  • Mengchao Wei
  • Shuling Chen
  • Manxia Lin
  • Chunlin Jiang
  • Jie Mei
  • Bin Li
  • Yu Wang
  • Jiaping Li
  • Xiaoyan Xie
  • Ming Kuang



To compare retrospectively the efficacy of transcatheter arterial chemoembolization (TACE) plus radiofrequency ablation (RFA) (TACE-RFA) with that of repeat hepatectomy in the treatment of initial recurrent hepatocellular carcinoma (HCC) after hepatectomy by propensity score matching (PSM).


From September 2006 to June 2015, 186 patients who underwent TACE-RFA (n=107) or repeat hepatectomy (n=79) for recurrent HCC ≤ 5.0 cm were included. The overall survival (OS) and disease-free survival (DFS) were compared. PSM was used to correct potential confounding factors between these two groups.


1-, 3-, and 5-year OS rates after TACE-RFA and repeat hepatectomy were 84.6%, 66.9%, 49.1%, and 84.8%, 60.2%, 51.9%, respectively (p=.871). The corresponding DFS rates were 58.2%, 35.2%, 29.6% and 64.8%, 41.6%, 38.3% (p=.258). TACE-RFA has lower major complication rates (p=.009) and shorter hospital stay (p<.001). After PSM, 1-, 3-, 5- year OS rates after TACE-RFA (n=51) and repeat hepatectomy (n=51) were 84.3%, 60.4%, 46.4% and 84.3%, 64.5%, 49.8% (p=.951), the corresponding DFS rates were 54.9%, 35.0%, 30.6% and 58.7%, 35.8%, and 33.6% (p=.733). AFP and micro-vessel invasion of initial tumour were significant prognostic factors for OS and DFS, respectively.


TACE-RFA provides comparable OS and DFS to repeat hepatectomy, fewer major complications and shorter hospital stay.

Key Points

• TACE-RFA achieved similar OS and DFS with repeat hepatectomy for recurrent HCC

• Major complication rate was lower in the TACE-RFA group

• The hospital stay was shorter in the TACE-RFA group

• AFP was a predictor for OS, MVI was a predictor for DFS

• The treatment strategies were not significant prognostic factor for OS or DFS


Carcinoma, Hepatocellular Hepatectomy Propensity Score Chemoembolization, Therapeutic Radio waves 



Alpha fetoprotein




Contrast-enhanced computed tomography


Contrast enhanced ultrasound


Disease-free survival


Hepatocellular carcinoma


Local tumour progression


Micro-vessel invasion


Overall survival


Propensity score matching


Radiofrequency ablation


Transarterial chemoembolization



Nothing to declare.


This study has received funding from the National Natural Science Foundation of China (No.81770608) and the Kelin Outstanding Young Scientist of the First Affiliated Hospital of Sun Yat-sen University for Zhen-Wei Peng.

Compliance with ethical standards


The scientific guarantor of this publication is Ming Kuang.

Conflict of interest

The authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper

Informed consent

Written informed consent was waived in this study.

Ethical approval

Institutional Review Board approval was obtained.


• retrospective

• observational

• performed at one institution

Supplementary material

330_2017_5166_MOESM1_ESM.docx (17 kb)
ESM 1 (DOCX 16 kb)


  1. 1.
    Llovet JM, Burroughs A, Bruix J (2003) Hepatocellular carcinoma. Lancet 362:1907–1917CrossRefPubMedGoogle Scholar
  2. 2.
    Itamoto T, Nakahara H, Amano H et al (2007) Repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery 141:589–597CrossRefPubMedGoogle Scholar
  3. 3.
    Camma C, Di Marco V, Orlando A et al (2005) Treatment of hepatocellular carcinoma in compensated cirrhosis with radio-frequency thermal ablation (RFTA): a prospective study. J Hepatol 42:535–540CrossRefPubMedGoogle Scholar
  4. 4.
    Poon RT, Fan ST, Tsang FH, Wong J (2002) Locoregional therapies for hepatocellular carcinoma: a critical review from the surgeon's perspective. Ann Surg 235:466–486CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Song KD, Lim HK, Rhim H et al (2015) Repeated Hepatic Resection versus Radiofrequency Ablation for Recurrent Hepatocellular Carcinoma after Hepatic Resection: A Propensity Score Matching Study. Radiology 275:599–608CrossRefPubMedGoogle Scholar
  6. 6.
    Tateishi R, Shiina S, Teratani T et al (2005) Percutaneous radiofrequency ablation for hepatocellular carcinoma. An analysis of 1000 cases. Cancer 103:1201–1209CrossRefPubMedGoogle Scholar
  7. 7.
    Peng ZW, Zhang YJ, Chen MS et al (2013) Radiofrequency ablation with or without transcatheter arterial chemoembolization in the treatment of hepatocellular carcinoma: a prospective randomized trial. J Clin Oncol 31:426–432CrossRefPubMedGoogle Scholar
  8. 8.
    Kim JH, Won HJ, Shin YM et al (2011) Medium-sized (3.1-5.0 cm) hepatocellular carcinoma: transarterial chemoembolization plus radiofrequency ablation versus radiofrequency ablation alone. Ann Surg Oncol 18:1624–1629CrossRefPubMedGoogle Scholar
  9. 9.
    Morimoto M, Numata K, Kondou M, Nozaki A, Morita S, Tanaka K (2010) Midterm outcomes in patients with intermediate-sized hepatocellular carcinoma: a randomized controlled trial for determining the efficacy of radiofrequency ablation combined with transcatheter arterial chemoembolization. Cancer 116:5452–5460CrossRefPubMedGoogle Scholar
  10. 10.
    Peng ZW, Zhang YJ, Liang HH, Lin XJ, Guo RP, Chen MS (2012) Recurrent hepatocellular carcinoma treated with sequential transcatheter arterial chemoembolization and RF ablation versus RF ablation alone: a prospective randomized trial. Radiology 262:689–700CrossRefPubMedGoogle Scholar
  11. 11.
    Shibata T, Isoda H, Hirokawa Y, Arizono S, Shimada K, Togashi K (2009) Small hepatocellular carcinoma: is radiofrequency ablation combined with transcatheter arterial chemoembolization more effective than radiofrequency ablation alone for treatment? Radiology 252:905–913CrossRefPubMedGoogle Scholar
  12. 12.
    Kagawa T, Koizumi J, Kojima S et al (2010) Transcatheter arterial chemoembolization plus radiofrequency ablation therapy for early stage hepatocellular carcinoma: comparison with surgical resection. Cancer 116:3638–3644CrossRefPubMedGoogle Scholar
  13. 13.
    Yamakado K, Nakatsuka A, Takaki H et al (2008) Early-stage hepatocellular carcinoma: radiofrequency ablation combined with chemoembolization versus hepatectomy. Radiology 247:260–266CrossRefPubMedGoogle Scholar
  14. 14.
    D'Agostino RB Jr (1998) Propensity score methods for bias reduction in the comparison of a treatment to a non-randomized control group. Stat Med 17:2265–2281CrossRefPubMedGoogle Scholar
  15. 15.
    Bruix J, Sherman M (2005) Management of hepatocellular carcinoma. Hepatology 42:1208–1236CrossRefPubMedGoogle Scholar
  16. 16.
    Fan W, Zhang Y, Wang Y, Yao X, Yang J, Li J (2015) Neutrophil-to-lymphocyte and platelet-to-lymphocyte ratios as predictors of survival and metastasis for recurrent hepatocellular carcinoma after transarterial chemoembolization. PLoS One 10:e0119312CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Strasberg SM (2005) Nomenclature of hepatic anatomy and resections: a review of the Brisbane 2000 system. J Hepatobiliary Pancreat Surg 12:351–355CrossRefPubMedGoogle Scholar
  18. 18.
    Ahmed M, Solbiati L, Brace CL et al (2014) Image-guided tumour ablation: standardization of terminology and reporting criteria--a 10-year update. Radiology 273:241–260CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Sobin LHWC (2002) TNM Classification of Malignant Tumours. John Wiley, Hoboken, NJGoogle Scholar
  20. 20.
    Cancer NIO (2010) Common Terminology Criteria for Adverse Events ( CTCAE ).Google Scholar
  21. 21.
    Omary RA, Bettmann MA, Cardella JF et al (2003) Quality improvement guidelines for the reporting and archiving of interventional radiology procedures. J Vasc Interv Radiol 14:S293–S295CrossRefPubMedGoogle Scholar
  22. 22.
    Kang TW, Kim JM, Rhim H et al (2015) Small Hepatocellular Carcinoma: Radiofrequency Ablation versus Nonanatomic Resection--Propensity Score Analyses of Long-term Outcomes. Radiology 275:908–919CrossRefPubMedGoogle Scholar
  23. 23.
    Kang TW, Lim HK, Lee MW et al (2016) Long-term Therapeutic Outcomes of Radiofrequency Ablation for Subcapsular versus Nonsubcapsular Hepatocellular Carcinoma: A Propensity Score Matched Study. Radiology 280:300–312CrossRefPubMedGoogle Scholar
  24. 24.
    Takuma Y, Takabatake H, Morimoto Y et al (2013) Comparison of combined transcatheter arterial chemoembolization and radiofrequency ablation with surgical resection by using propensity score matching in patients with hepatocellular carcinoma within Milan criteria. Radiology 269:927–937CrossRefPubMedGoogle Scholar
  25. 25.
    Chang WT, Kao WY, Chau GY et al (2012) Hepatic resection can provide long-term survival of patients with non-early-stage hepatocellular carcinoma: extending the indication for resection? Surgery 152:809–820CrossRefPubMedGoogle Scholar
  26. 26.
    Park YN (2011) Update on precursor and early lesions of hepatocellular carcinomas. Arch Pathol Lab Med 135:704–715CrossRefPubMedGoogle Scholar
  27. 27.
    Goldberg SN, Hahn PF, Tanabe KK et al (1998) Percutaneous radiofrequency tissue ablation: does perfusion-mediated tissue cooling limit coagulation necrosis? J Vasc Interv Radiol 9:101–111CrossRefPubMedGoogle Scholar
  28. 28.
    Higuchi T, Kikuchi M, Okazaki M (1994) Hepatocellular carcinoma after transcatheter hepatic arterial embolization. A histopathologic study of 84 resected cases. Cancer 73:2259–2267CrossRefPubMedGoogle Scholar
  29. 29.
    Yamashiki N, Yoshida H, Tateishi R et al (2007) Recurrent hepatocellular carcinoma has an increased risk of subsequent recurrence after curative treatment. J Gastroenterol Hepatol 22:2155–2160CrossRefPubMedGoogle Scholar
  30. 30.
    Huang ZY, Liang BY, Xiong M et al (2012) Long-term outcomes of repeat hepatic resection in patients with recurrent hepatocellular carcinoma and analysis of recurrent types and their prognosis: a single-centre experience in China. Ann Surg Oncol 19:2515–2525CrossRefPubMedGoogle Scholar
  31. 31.
    Lim KC, Chow PK, Allen JC et al (2011) Microvascular invasion is a better predictor of tumour recurrence and overall survival following surgical resection for hepatocellular carcinoma compared to the Milan criteria. Ann Surg 254:108–113CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2018

Authors and Affiliations

  • Zhenwei Peng
    • 1
    • 2
  • Mengchao Wei
    • 3
  • Shuling Chen
    • 4
  • Manxia Lin
    • 4
  • Chunlin Jiang
    • 4
  • Jie Mei
    • 2
  • Bin Li
    • 2
  • Yu Wang
    • 5
  • Jiaping Li
    • 5
  • Xiaoyan Xie
    • 4
  • Ming Kuang
    • 3
    • 4
  1. 1.Department of OncologyThe First Affiliated Hospital of Sun Yat-sen UniversityGuangzhouChina
  2. 2.Clinical Trials UnitThe First Affiliated Hospital of Sun Yat-sen UniversityGuangzhouChina
  3. 3.Department of Liver SurgeryThe First Affiliated Hospital of Sun Yat-sen UniversityGuangzhouChina
  4. 4.Division of Interventional UltrasoundThe First Affiliated Hospital of Sun Yat-sen UniversityGuangzhouChina
  5. 5.Department of Interventional OncologyThe First Affiliated Hospital of Sun Yat-sen UniversityGuangzhouChina

Personalised recommendations