Abstract
Purpose
To compare the efficiency of three-dimensional (3D) and two-dimensional (2D) contrast-enhanced ultrasound (CEUS)–derived techniques in evaluating the ablative margin (AM) after radiofrequency ablation (RFA) for hepatocellular carcinoma (HCC).
Methods
In total, 98 patients with 98 HCCs were enrolled. The 2D CEUS point-to-point imaging (2D CEUS-PI) was conducted by comparing the pre- and post-RFA 2D CEUS images manually, and the 3D CEUS fusion imaging (3D CEUS-FI) was conducted by fusing the pre- and post-RFA 3D CEUS images automatically. These two techniques were compared in distinguishing an adequate AM ≥ 5 mm. Risk factors for local tumor progression (LTP) after RFA were analyzed by the Kaplan–Meier method with log-rank test.
Results
The mean registration time of 3D CEUS-FI and 2D CEUS-PI was 5.0 and 9.3 min, respectively (p < 0.0001). The kappa coefficient was 0.680 for agreement between 2D CEUS-PI and 3D CEUS-FI in the evaluation of AM (p < 0.0001). Tumors with AM < 5 mm by 2D CEUS-PI were all identified as AM < 5 mm by 3D CEUS-FI. Nonetheless, 16 (26%) tumors identified as AM ≥ 5 mm by 2D CEUS-PI were re-classified as AM < 5 mm by 3D CEUS-FI. During a median follow-up time of 31.2 months (range, 3.2–66.0 months), LTP was identified in 8 tumors. The estimated 1-/2-/3-year cumulative incidence of LTP was 4.4%, 8.1%, and 10.3%, respectively. Higher estimated cumulative incidence of LTP was identified in tumors with AM < 5 mm by 2D CEUS-PI (at 3-year, 27.2% vs 0%; p < 0.001), and by 3D CEUS-FI (at 3-year, 20.7% vs 0%; p = 0.004).
Conclusion
3D CEUS-FI excelled in the evaluation of AM when compared with 2D CEUS-PI. With equivalent efficacy in the prediction of LTP, 3D CEUS-FI was superior to 2D CEUS-PI for its automatic and time-saving procedure.
Clinical relevance statement
3D CEUS fusion imaging may serve as an effective tool in evaluating ablative margin and predicting local tumor progression after RFA in HCC.
Key Points
• Both 2D and 3D CEUS–derived techniques could evaluate ablative margin (AM) after RFA for hepatocellular carcinoma.
• 3D CEUS fusion imaging was more precise in the evaluation of AM compared to 2D CEUS point-to-point imaging, with advantages of its automatic and time-saving procedure.
• An inadequate AM < 5 mm evaluated by CEUS-derived techniques was the only risk factor of LTP after RFA for hepatocellular carcinoma (p < 0.001 for 2D CEUS point-to-point imaging, and p = 0.004 for 3D CEUS fusion imaging).
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Abbreviations
- 2D CEUS-PI:
-
Two-dimensional contrast-enhanced ultrasound point-to-point imaging
- 3D CEUS-FI:
-
Three-dimensional contrast-enhanced ultrasound fusion imaging
- AM:
-
Ablative margin
- HCC:
-
Hepatocellular carcinoma
- LTP:
-
Local tumor progression
- RFA:
-
Radiofrequency ablation
References
Sung H, Ferlay J, Siegel RL et al (2021) Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 71:209–249
Reig M, Forner A, Rimola J et al (2022) BCLC strategy for prognosis prediction and treatment recommendation: The 2022 update. J Hepatol 76:681–693
Takayama T, Hasegawa K, Izumi N et al (2022) Surgery versus radiofrequency ablation for small hepatocellular carcinoma: a randomized controlled trial (SURF Trial). Liver Cancer 11:209–218
Lee MW, Kang D, Lim HK et al (2020) Updated 10-year outcomes of percutaneous radiofrequency ablation as first-line therapy for single hepatocellular carcinoma < 3 cm: emphasis on association of local tumor progression and overall survival. Eur Radiol 30:2391–2400
Sakakibara M, Ohkawa K, Katayama K et al (2014) Three-dimensional registration of images obtained before and after radiofrequency ablation of hepatocellular carcinoma to assess treatment adequacy. AJR Am J Roentgenol 202:W487-495
Hai Y, Savsani E, Chong W, Eisenbrey J, Lyshchik A (2021) Meta-analysis and systematic review of contrast-enhanced ultrasound in evaluating the treatment response after locoregional therapy of hepatocellular carcinoma. Abdom Radiol (NY) 46:5162–5179
Kisaka Y, Hirooka M, Kumagi T et al (2006) Usefulness of contrast-enhanced ultrasonography with abdominal virtual ultrasonography in assessing therapeutic response in hepatocellular carcinoma treated with radiofrequency ablation. Liver Int 26:1241–1247
Xu EJ, Lv SM, Li K et al (2018) Immediate evaluation and guidance of liver cancer thermal ablation by three-dimensional ultrasound/contrast-enhanced ultrasound fusion imaging. Int J Hyperthermia 34:870–876
Ye J, Huang G, Zhang X et al (2019) Three-dimensional contrast-enhanced ultrasound fusion imaging predicts local tumor progression by evaluating ablative margin of radiofrequency ablation for hepatocellular carcinoma: a preliminary report. Int J Hyperthermia 36:55–64
Zhang X, Huang G, Ye J et al (2019) 3-D contrast-enhanced ultrasound fusion imaging: a new technique to evaluate the ablative margin of radiofrequency ablation for hepatocellular carcinoma. Ultrasound Med Biol 45:1933–1943
Bruix J, Sherman M (2011) Management of hepatocellular carcinoma: an update. Hepatology 53:1020–1022
Seror O, N’Kontchou G, Nault JC et al (2016) Hepatocellular carcinoma within milan criteria: no-touch multibipolar radiofrequency ablation for treatment-long-term results. Radiology 280:611–621
Yang Y, Chen Y, Ye F et al (2021) Late recurrence of hepatocellular carcinoma after radiofrequency ablation: a multicenter study of risk factors, patterns, and survival. Eur Radiol 31:3053–3064
Liu M, Huang GL, Xu M et al (2017) Percutaneous thermal ablation for the treatment of colorectal liver metastases and hepatocellular carcinoma: a comparison of local therapeutic efficacy. Int J Hyperthermia 33:446–453
Ahmed M, Solbiati L, Brace CL et al (2014) Image-guided tumor ablation: standardization of terminology and reporting criteria–a 10-year update. Radiology 273:241–260
Zheng H, Liu K, Yang Y et al (2022) Microwave ablation versus radiofrequency ablation for subcapsular hepatocellular carcinoma: a propensity score-matched study. Eur Radiol 32:4657–4666
Choi D, Lim HK, Kim SH et al (2000) Hepatocellular carcinoma treated with percutaneous radio-frequency ablation: usefulness of power Doppler US with a microbubble contrast agent in evaluating therapeutic response-preliminary results. Radiology 217:558–563
Ahn SJ, Lee JM, Lee DH et al (2017) Real-time US-CT/MR fusion imaging for percutaneous radiofrequency ablation of hepatocellular carcinoma. J Hepatol 66:347–354
Song KD, Lee MW, Rhim H, Cha DI, Chong Y, Lim HK (2013) Fusion imaging-guided radiofrequency ablation for hepatocellular carcinomas not visible on conventional ultrasound. AJR Am J Roentgenol 201:1141–1147
Kisaka Y, Hirooka M, Koizumi Y et al (2010) Contrast-enhanced sonography with abdominal virtual sonography in monitoring radiofrequency ablation of hepatocellular carcinoma. J Clin Ultrasound 38:138–144
Bo XW, Xu HX, Guo LH et al (2017) Ablative safety margin depicted by fusion imaging with post-treatment contrast-enhanced ultrasound and pre-treatment CECT/CEMRI after radiofrequency ablation for liver cancers. Br J Radiol 90:20170063
Wang Y, Jing X, Ding J (2016) Clinical value of dynamic 3-dimensional contrast-enhanced ultrasound imaging for the assessment of hepatocellular carcinoma ablation. Clin Imaging 40:402–406
Cao J, Dong Y, Mao F, Wang W (2018) Dynamic three-dimensional contrast-enhanced ultrasound to predict therapeutic response of radiofrequency ablation in hepatocellular carcinoma: preliminary findings. Biomed Res Int 2018:6469703
Xu HX, Lu MD, Xie XH et al (2010) Treatment response evaluation with three-dimensional contrast-enhanced ultrasound for liver cancer after local therapies. Eur J Radiol 76:81–88
Chen J, Lin Z, Lin Q, Lin R, Yan Y, Chen J (2020) Percutaneous radiofrequency ablation for small hepatocellular carcinoma in hepatic dome under MR-guidance: clinical safety and efficacy. Int J Hyperthermia 37:192–201
Song KD, Lee MW, Rhim H et al (2018) Percutaneous US/MRI fusion-guided radiofrequency ablation for recurrent subcentimeter hepatocellular carcinoma: technical feasibility and therapeutic outcomes. Radiology 288:878–886
Vietti Violi N, Duran R, Guiu B et al (2018) Efficacy of microwave ablation versus radiofrequency ablation for the treatment of hepatocellular carcinoma in patients with chronic liver disease: a randomised controlled phase 2 trial. Lancet Gastroenterol Hepatol 3:317–325
Kim TH, Koh YH, Kim BH et al (2021) Proton beam radiotherapy vs. radiofrequency ablation for recurrent hepatocellular carcinoma: a randomized phase III trial. J Hepatol 74:603–612
Yang Y, Chen Y, Zhang X et al (2021) Predictors and patterns of recurrence after radiofrequency ablation for hepatocellular carcinoma within up-to-seven criteria: a multicenter retrospective study. Eur J Radiol 138:109623
Ikeda K, Seki T, Umehara H et al (2007) Clinicopathologic study of small hepatocellular carcinoma with microscopic satellite nodules to determine the extent of tumor ablation by local therapy. Int J Oncol 31:485–491
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 188:480–488
Jiang C, Liu B, Chen S, Peng Z, Xie X, Kuang M (2018) Safety margin after radiofrequency ablation of hepatocellular carcinoma: precise assessment with a three-dimensional reconstruction technique using CT imaging. Int J Hyperthermia 34:1135–1141
Kaye EA, Cornelis FH, Petre EN et al (2019) Volumetric 3D assessment of ablation zones after thermal ablation of colorectal liver metastases to improve prediction of local tumor progression. Eur Radiol 29:2698–2705
Okusaka T, Okada S, Ueno H et al (2002) Satellite lesions in patients with small hepatocellular carcinoma with reference to clinicopathologic features. Cancer 95:1931–1937
Hu HT, Wang Z, Huang XW et al (2019) Ultrasound-based radiomics score: a potential biomarker for the prediction of microvascular invasion in hepatocellular carcinoma. Eur Radiol 29:2890–2901
Funding
This research was supported by the National Natural Science Foundation of China [Grants No. 92059201, No. 81530055, and No. 81501493].
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Haiyi Long and Xiaoyu Zhou share the first authorship.
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Long, H., Zhou, X., Zhang, X. et al. 3D fusion is superior to 2D point-to-point contrast-enhanced US to evaluate the ablative margin after RFA for hepatocellular carcinoma. Eur Radiol 34, 1247–1257 (2024). https://doi.org/10.1007/s00330-023-10023-5
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DOI: https://doi.org/10.1007/s00330-023-10023-5