Abdominal Radiology

, Volume 44, Issue 3, pp 923–935 | Cite as

Evaluation of hepatocellular carcinoma ablative margins using fused pre- and post-ablation hepatobiliary phase images

  • Nobuyuki TakeyamaEmail author
  • Naruki Mizobuchi
  • Masashi Sakaki
  • Yu Shimozuma
  • Jiro Munechika
  • Atsushi Kajiwara
  • Manabu Uchikoshi
  • Syojiro Uozumi
  • Yoshimitsu Ohgiya
  • Takehiko Gokan



To retrospectively evaluate the utility of fusion images of pre- and post-ablation hepatobiliary phase (HBP) series to assess the ablation margins after radiofrequency ablation (RFA) of hepatocellular carcinomas (HCCs). Additionally, to identify factors indicative of an adequate ablation margin and predictors of local tumor progression (LTP).


Fifty-nine HCCs in 29 patients were treated by RFA and followed-up for > 1 year (mean 37.9 months). Fusion images of pre- and post-ablation HBP series were created using a non-rigid registration and manual correlation. The ablation margin appearance was classified as ablation margin + (ablation margin completely surrounding the tumor), ablation margin-zero (a partially discontinuous ablation margin without protrusion of HCC), ablation margin—(a partially discontinuous ablation margin with protrusion of HCC), and indeterminate (index tumor was not visible). The minimal ablation margin was measured, and clinical factors were examined to identify other risk factors for LTP.


LTP was observed at follow-up in 12 tumors. The mean minimal ablation margin was 3.6 mm. Multivariate analysis revealed that the ablation margin status was the only significant factor (p = 0.028). The cumulative LTP rates (3.3%, 3.3%, and 3.3% at 1, 2, and 3 years, respectively) in 30 ablation margin + nodules were significantly lower (p = 0.006) than those (20.0%, 28.0%, and 32.2% at 1, 2, and 3 years, respectively) in 25 ablation margin-zero nodules.


Fusion images enable an early assessment of the ablation efficacy in the majority of HCCs. The ablation margin status is a significant factor for LTP.


Fusion RFA EOB-MRI Hepatocellular carcinoma Hepatobiliary phase 


Compliance with ethical standards


No funding was received for this study.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

The Institutional Review Board waived the requirement for informed consent for this retrospective study.


  1. 1.
    Shiina S, Tateishi R, Arano T, et al. (2012) Radiofrequency ablation for hepatocellular carcinoma: 10-year outcome and prognostic factors. Am J Gastroenterol 107:569–577CrossRefGoogle Scholar
  2. 2.
    Nakazawa T, Kokubu S, Shibuya A, et al. (2007) Radiofrequency ablation of hepatocellular carcinoma: correlation between local tumor progression after ablation and ablative margin. AJR Am J Roentgenol 188:480–488CrossRefGoogle Scholar
  3. 3.
    Kim YS, Lee WJ, Rhim H, et al. (2010) The minimal ablative margin of radiofrequency ablation of hepatocellular carcinoma (> 2 and < 5 cm) needed to prevent local tumor progression: 3D quantitative assessment. AJR Am J Roentgenol 195:758–765CrossRefGoogle Scholar
  4. 4.
    Kei SK, Rim H, Choi D, et al. (2008) Local tumor progression after radiofrequency ablation of liver tumors: analysis of morphologic pattern and site of recurrence. AJR Am J Roentgenol 190:1544–1551CrossRefGoogle Scholar
  5. 5.
    M-h Park, Rhim H, Kim YS, et al. (2008) Spectrum of CT findings after radiofrequency ablation of hepatic tumors. RadioGraphics 28:379–392CrossRefGoogle Scholar
  6. 6.
    Minami Y, Nishida N, Kudo M (2014) Therapeutic response assessment of RFA for HCC: Contrast-enhanced US, CT and MRI. World J Gastroenterol 21:4160–4166CrossRefGoogle Scholar
  7. 7.
    Tomonari A, Tsuji K, Yamazaki H, et al. (2013) Feasibility of fused imaging for the evaluation of radiofrequency ablative margin for hepatocellular carcinoma. Hepatol Res 43:728–734CrossRefGoogle Scholar
  8. 8.
    Makino Y, Imai Y, Igura T, et al. (2013) Utility of computed tomography fusion imaging for the evaluation of the ablative margin of radiofrequency ablation for hepatocellular carcinoma and the correlation to local tumor progression. Hepatol Res 43:950–958CrossRefGoogle Scholar
  9. 9.
    Kim KW, Lee JM, Klotz E, et al. (2011) Safety margin assessment after radiofrequency ablation of the liver using registration of preprocedure and postprocedure CT images. AJR Am J Roentgenol 196:W565–W572CrossRefGoogle Scholar
  10. 10.
    Shin S, Lee JM, Kim KY, et al. (2014) Postablation assessment using follow-up registration of CT images before and after Radiofrequency Ablation (RFA): prospective evaluation of midterm therapeutic results of RFA for Hepatocellular Carcinoma. AJR Am J Roentgenol 203:70–77CrossRefGoogle Scholar
  11. 11.
    Vandenbroucke F, Vandemeulebroucke J, Buls N, Thoeni RF, de Mey J (2018) Can tumor coverage evaluated 24 h post-radiofrequency ablation predict local tumor progression of liver metastases? Int J Comput Assist Radiol Surg. Google Scholar
  12. 12.
    Mori K, Fukuda K, Asaoka H, et al. (2009) Radiofrequency ablation of the liver: determination of ablative margin at MR imaging with impaired clearance of ferucarbotran-feasibility study. Radiology 251:557–565CrossRefGoogle Scholar
  13. 13.
    Onishi H, Matsushita M, Murakami T, et al. (2004) MR appearances of radiofrequency thermal ablation region: histopathologic correlation with dog liver models and an autopsy case. Acad Radiol 11:1180–1189CrossRefGoogle Scholar
  14. 14.
    Khankan A, Murakami T, Onishi H, et al. (2008) Hepatocellular carcinoma treated with radiofrequency ablation: an early evaluation with magnetic resonance imaging. J Magn Reson Imaging 27:546–551CrossRefGoogle Scholar
  15. 15.
    Koda M, Tokunaga S, Miyoshi K, et al. (2012) Assessment of ablative margin by unenhanced magnetic resonance imaging after radiofrequency ablation for hepatocellular carcinoma. Eur J Radiol 81:2730–2736CrossRefGoogle Scholar
  16. 16.
    Kim SM, Shin SS, Lee BC, et al. (2017) Imaging evaluation of ablative margin and index tumor immediately after radiofrequency ablation for hepatocellular carcinoma: comparison between multidetector-row CT and MR imaging. Abdom Radiol 42:2527–2537CrossRefGoogle Scholar
  17. 17.
    Yoon JH, Lee EJ, Cha SS, et al. (2010) Comparison of gadoxetic acid-enhanced MR imaging versus four-phase multi-detector row computed tomography in assessing tumor regression after radiofrequency ablation in subjects with hepatocellular carcinomas. J Vasc Interv Radiol 21:348–356CrossRefGoogle Scholar
  18. 18.
    Koda M, Tokunaga S, Okamoto T, et al. (2015) Clinical usefulness of the ablative margin assessed bymagnetic resonance imaging with Gd-EOB-DTPA for radiofrequency ablation of hepatocellular carcinoma. J Hepatol 63:1360–1367CrossRefGoogle Scholar
  19. 19.
    Takeyama N, Vidhyarkorn S, Chung DJ, et al. (2016) Does hepatobiliary phase sequence qualitatively outperform unenhanced T1-weighted imaging in assessment of the ablation margin 24 hours after thermal ablation of hepatocellular carcinomas? Abdom Radiol 41:1942–1955CrossRefGoogle Scholar
  20. 20.
    Makino Y, Imai Y, Igura T, et al. (2015) Comparative evaluation of three-dimensional Gd-EOB-DTPA-enhanced MR fusion imaging with CT fusion imaging in the assessment of treatment effect of radiofrequency ablation of hepatocellular carcinoma. Abdom Imaging 40:102–111CrossRefGoogle Scholar
  21. 21.
    Sakakibara M, Ohkawa K, Katayama K, et al. (2015) Three-dimensional registration of images obtained before and after radiofrequency ablation of hepatocellular carcinoma to assess treatment adequacy. AJR Am J Roentgenol 202:W487–W495CrossRefGoogle Scholar
  22. 22.
    Wang XL, Li K, Su ZZ, et al. (2015) Assessment of radiofrequency ablation margin by MRI-MRI image fusion in hepatocellular carcinoma. World J Gastroenterol 21:5345–5351CrossRefGoogle Scholar
  23. 23.
    Boas FE, Do B, Louie JD (2015) Optimal imaging surveillance schedules after liver-directed therapy for hepatocellular carcinoma. J Vasc Interv Radiol 26:69–73CrossRefGoogle Scholar
  24. 24.
    The Japan Society of Hepatology. Clinical practice guidelines for hepatocellular carcinoma, 2013.>.r Study Group of Japan
  25. 25.
    Kubo M, Matsui O, Sakamoto M, et al. (2013) Role of gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid-enhanced magnetic resonance imaging in the management of hepatocellular carcinoma: consensus at the Symposium of the 48th Annual Meeting of the Liver Cancer. Oncology 84(suppl 1):21–27Google Scholar
  26. 26.
    Lee SR, Kilcoyne A, Kambadakone A, Arellano R (2016) Interventional Oncology: pictorial review of post-ablation imaging of liver and renal tumor. Abdom Radiol 41:677–705CrossRefGoogle Scholar
  27. 27.
    Dromain C, De Baere T, Elias D, et al. (2002) Hepatic tumors treated with percutaneous radio-frequency ablation: CT and MR imaging follow-up. Radiology 223:255–262CrossRefGoogle Scholar
  28. 28.
    Liu CH, Arellano RS, Uppot RN, et al. (2010) Radiofrequency ablation of hepatic tumours: effect of post-ablation margin on local tumour progression. Eur Radiol 20:877–885CrossRefGoogle Scholar
  29. 29.
    Kudo M (2004) Local ablation therapy for hepatocellular carcinoma: current status and future perspectives. J Gastroenterol 39:205–214CrossRefGoogle Scholar
  30. 30.
    Koda M, Tokunaga S, Miyoshi K, et al. (2013) Ablative margin states by magnetic resonance imaging with ferucarbotran in radiofrequency ablation for hepatocellular carcinoma can predict local tumor progression. J Gastroenterol 48:1283–1292CrossRefGoogle Scholar
  31. 31.
    Kim YS, Rim H, Lim HK, et al. (2011) Coagulation necrosis induced by radiofrequency ablation in the liver: histopathologic and radiologic review of usual to extremely rare changes. Radiographics 31:377–390CrossRefGoogle Scholar
  32. 32.
    Higaki A, Ito K, Tamada T, et al. (2014) Prognosis of small hepatocellular nodules detected only at the hepatobiliary phase of Gd-EOB-DTPA-enhanced MR imaging as hypointensity in cirrhosis or chronic hepatitis. Eur Radiol 24:2476–2481CrossRefGoogle Scholar
  33. 33.
    Chang WC, Chen RC, Chou CT, et al. (2014) Histological grade of hepatocellular carcinoma correlates with arterial enhancement on gadoxetic acid-enhanced and diffusion-weighted MR images. Abdom Imaging 39:1202–1212CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Nobuyuki Takeyama
    • 1
    Email author
  • Naruki Mizobuchi
    • 2
  • Masashi Sakaki
    • 3
  • Yu Shimozuma
    • 3
  • Jiro Munechika
    • 2
  • Atsushi Kajiwara
    • 3
  • Manabu Uchikoshi
    • 3
  • Syojiro Uozumi
    • 3
  • Yoshimitsu Ohgiya
    • 2
  • Takehiko Gokan
    • 2
  1. 1.Department of RadiologyShowa University Fujigaoka HospitalYokohama-CityJapan
  2. 2.Department of RadiologyShowa University School of MedicineTokyoJapan
  3. 3.Department of GastroenterologyShowa University School of MedicineTokyoJapan

Personalised recommendations