Whole tumor ablation of locally recurred hepatocellular carcinoma including retained iodized oil after transarterial chemoembolization improves progression-free survival

  • Dong Ho Lee
  • Jeong Min LeeEmail author
  • Pyo Nyun Kim
  • Yun-Jin Jang
  • Tae Wook Kang
  • Hyunchul Rhim
  • Jung Wook Seo
  • Young Joon Lee



To evaluate and compare clinical outcomes of two different radiofrequency ablation (RFA) methods for locally recurred hepatocellular carcinoma (LrHCC) after locoregional treatment.


Our institutional review board approved this study with a waiver of informed consent. A total of 313 patients previously treated with transarterial chemoembolization (TACE) (n = 167) and RFA (n = 146) with a single LrHCC ≤ 3 cm was included from five tertiary referral hospitals. RFA was done for LrHCCs using either viable tumor alone ablation (VTA) method (VTA: n = 61 in the TACE group and n = 127 in the RFA group) or whole tumor ablation (WTA) method which includes both viable tumor and retained iodized oil or previously ablated zone (WTA: n = 106 in the TACE group and n = 19 in the RFA group). Local tumor progression (LTP)-free survival as well as progression-free survival (PFS) were estimated using the Kaplan-Meier method, and prognostic factors were evaluated using the Cox proportional hazards regression model.


In 167 patients with LrHCC who underwent TACE, the 5-year LTP-free survival after RFA was significantly higher with the VTA method than with the WTA method (26.9% vs. 87.8%; p < 0.001; hazard ratio (HR) = 8.53 [4.16–17.5]). The estimated 5-year PFS after RFA for LrHCC after TACE using the VTA method was 5.7%, which was significantly lower than that with the WTA method (26.4%) (p = 0.014; HR = 1.62 [1.10–2.38]). However, in 146 patients with LrHCC after initial RFA, there were no significant differences in cumulative incidence of LTP (p = 0.514) or PFS (p = 0.905) after RFA between the two ablation methods.


For RFA of LrHCC after TACE, the WTA method including both viable tumor and retained iodized oil could significantly lower LTP and improve PFS than VTA.

Key Points

Whole tumor ablation (WTA) could provide significantly better local tumor control for locally recurred HCC (LrHCC) after TACE than viable tumor alone ablation (VTA).

WTA for LrHCC after TACE could also provide significantly better progression-free survival than VTA.

Regarding LrHCC after RFA, VTA would provide a comparable clinical outcome to WTA.


Hepatocellular carcinoma Ablation techniques Progression-free survival Chemoembolization Therapeutic 





Confidence interval


Computed tomography


Extrahepatic metastasis


Hepatocellular carcinoma


Hazard ratio


Intrahepatic distant recurrence


Locally recurred hepatocellular carcinoma


Local tumor progression


Magnetic resonance


Progression-free survival


Radiofrequency ablation


Transarterial chemoembolization





The authors state that this study was supported by a grant from the Korean Society of Imaging-guided Tumor Ablation (KSITA) (grant number KSITA-201701).

Compliance with ethical standards


The scientific guarantor of this publication is Jeong Min Lee.

Conflict of interest

The authors declare that they have no competing interests.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional review board.

Ethical approval

Institutional review board approval was obtained.


• Retrospective

• Observational

• Performed at five institutes

Supplementary material

330_2018_5993_MOESM1_ESM.docx (28 kb)
ESM 1 (DOCX 27 kb)


  1. 1.
    Parkin DM, Bray F, Ferlay J, Pisani P (2001) Estimating the world cancer burden: Globocan 2000. Int J Cancer 94:153–156CrossRefGoogle Scholar
  2. 2.
    N’Kontchou G, Mahamoudi A, Aout M et al (2009) Radiofrequency ablation of hepatocellular carcinoma: long-term results and prognostic factors in 235 Western patients with cirrhosis. Hepatology 50:1475–1483CrossRefGoogle Scholar
  3. 3.
    Shiina S, Tateishi R, Arano T et al (2012) Radiofrequency ablation for hepatocellular carcinoma: 10-year outcome and prognostic factors. Am J Gastroenterol 107:569–577 quiz 578CrossRefGoogle Scholar
  4. 4.
    Kim YS, Lim HK, Rhim H et al (2013) Ten-year outcomes of percutaneous radiofrequency ablation as first-line therapy of early hepatocellular carcinoma: analysis of prognostic factors. J Hepatol 58:89–97CrossRefGoogle Scholar
  5. 5.
    Lee DH, Lee JM, Lee JY et al (2014) Radiofrequency ablation of hepatocellular carcinoma as first-line treatment: long-term results and prognostic factors in 162 patients with cirrhosis. Radiology 270:900–909CrossRefGoogle Scholar
  6. 6.
    European Association for the Study of the Liver (2018) EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 69:182–236Google Scholar
  7. 7.
    Heimbach JK, Kulik LM, Finn RS et al (2018) AASLD guidelines for the treatment of hepatocellular carcinoma. Hepatology 67:358–380CrossRefGoogle Scholar
  8. 8.
    Park JW, Chen M, Colombo M et al (2015) Global patterns of hepatocellular carcinoma management from diagnosis to death: the BRIDGE study. Liver Int 35:2155–2166CrossRefGoogle Scholar
  9. 9.
    Chung YH (2005) A strategy for early detection of recurrent hepatocellular carcinoma following initial remission by transcatheter arterial chemoembolization. Intervirology 48:46–51CrossRefGoogle Scholar
  10. 10.
    Min JH, Lee MW, Rhim H et al (2012) Radiofrequency ablation for viable hepatocellular carcinoma around retained iodized oil after transcatheter arterial chemoembolization: usefulness of biplane fluoroscopy plus ultrasound guidance. Korean J Radiol 13:784–794CrossRefGoogle Scholar
  11. 11.
    Kim JH, Kim PN, Won HJ, Shin YM (2014) Viable hepatocellular carcinoma around retained iodized oil after transarterial chemoembolization: radiofrequency ablation of viable tumor plus retained iodized oil versus viable tumor alone. AJR Am J Roentgenol 203:1127–1131CrossRefGoogle Scholar
  12. 12.
    European Association for the Study of the Liver, European Organisation for Research and Treatment of Cancer (2012) EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 56:908–943CrossRefGoogle Scholar
  13. 13.
    Ahmed M, Solbiati L, Brace CL et al (2014) Image-guided tumor ablation: standardization of terminology and reporting criteria—a 10-year update. Radiology 273:241–260CrossRefGoogle Scholar
  14. 14.
    Lee DH, Lee JM, Kang TW et al (2017) Clinical outcomes of radiofrequency ablation for early hypovascular HCC: a multicenter retrospective study. Radiology.
  15. 15.
    Lee DH, Lee JM, Lee JY et al (2015) Non-hypervascular hepatobiliary phase hypointense nodules on gadoxetic acid-enhanced MRI: risk of HCC recurrence after radiofrequency ablation. J Hepatol 62:1122–1130CrossRefGoogle Scholar
  16. 16.
    Goldberg SN, Grassi CJ, Cardella JF et al (2005) Image-guided tumor ablation: standardization of terminology and reporting criteria. Radiology 235:728–739CrossRefGoogle Scholar
  17. 17.
    Golfieri R, Cappelli A, Cucchetti A et al (2011) Efficacy of selective transarterial chemoembolization in inducing tumor necrosis in small (<5 cm) hepatocellular carcinomas. Hepatology 53:1580–1589CrossRefGoogle Scholar
  18. 18.
    Kwan SW, Fidelman N, Ma E, Kerlan RK Jr, Yao FY (2012) Imaging predictors of the response to transarterial chemoembolization in patients with hepatocellular carcinoma: a radiological-pathological correlation. Liver Transpl 18:727–736CrossRefGoogle Scholar
  19. 19.
    Kim SJ, Choi MS, Kang JY et al (2009) Prediction of complete necrosis of hepatocellular carcinoma treated with transarterial chemoembolization prior to liver transplantation. Gut Liver 3:285–291CrossRefGoogle Scholar
  20. 20.
    Willatt JM, Hussain HK, Adusumilli S, Marrero JA (2008) MR imaging of hepatocellular carcinoma in the cirrhotic liver: challenges and controversies. Radiology 247:311–330CrossRefGoogle Scholar
  21. 21.
    Lee DH, Lee JM, Klotz E et al (2013) Detection of recurrent hepatocellular carcinoma in cirrhotic liver after transcatheter arterial chemoembolization: value of quantitative color mapping of the arterial enhancement fraction of the liver. Korean J Radiol 14:51–60CrossRefGoogle Scholar
  22. 22.
    Goldberg SN, Gazelle GS, Compton CC, Mueller PR, Tanabe KK (2000) Treatment of intrahepatic malignancy with radiofrequency ablation: radiologic-pathologic correlation. Cancer 88:2452–2463CrossRefGoogle Scholar
  23. 23.
    Morimoto M, Sugimori K, Shirato K et al (2002) Treatment of hepatocellular carcinoma with radiofrequency ablation: radiologic-histologic correlation during follow-up periods. Hepatology 35:1467–1475CrossRefGoogle Scholar
  24. 24.
    Brillet PY, Paradis V, Brancatelli G et al (2006) Percutaneous radiofrequency ablation for hepatocellular carcinoma before liver transplantation: a prospective study with histopathologic comparison. AJR Am J Roentgenol 186:S296–S305CrossRefGoogle Scholar
  25. 25.
    Hocquelet A, Aubé C, Rode A et al (2017) Comparison of no-touch multi-bipolar vs. monopolar radiofrequency ablation for small HCC. J Hepatol 66:67–74CrossRefGoogle Scholar
  26. 26.
    Ding J, Jing X, Liu J, et al (2013) Comparison of two different thermal techniques for the treatment of hepatocellular carcinoma. Eur J Radiol 82:1379–1384Google Scholar

Copyright information

© European Society of Radiology 2019

Authors and Affiliations

  • Dong Ho Lee
  • Jeong Min Lee
    • 1
    • 2
    Email author
  • Pyo Nyun Kim
    • 3
  • Yun-Jin Jang
    • 3
  • Tae Wook Kang
    • 4
  • Hyunchul Rhim
    • 4
  • Jung Wook Seo
    • 5
  • Young Joon Lee
    • 6
  1. 1.Department of RadiologySeoul National University HospitalSeoulSouth Korea
  2. 2.Institute of Radiation Medicine, College of MedicineSeoul National UniversitySeoulSouth Korea
  3. 3.Department of Radiology and Research Institute of RadiologyUniversity of Ulsan, Asan Medical CenterSeoulSouth Korea
  4. 4.Department of Radiology, Samsung Medical Center, School of MedicineSungkyunkwan UniversitySeoulSouth Korea
  5. 5.Department of RadiologyInje University Ilsan Paik HospitalGoyangSouth Korea
  6. 6.Department of Radiology, Seoul St. Mary’s Hospital, College of MedicineThe Catholic University of KoreaSeoulSouth Korea

Personalised recommendations