Intraprocedurally EOB-MRI/US fusion imaging focusing on hepatobiliary phase findings can help to reduce the recurrence of hepatocellular carcinoma after radiofrequency ablation

References

• Omata M, Cheng A, Kokudo N, et al. Asia-Pacific clinical practice guidelines on the management of hepatocellular carcinoma: a 2017 update. Hepatol Int. 2017;11(4):317–370.
   PubMed Web of Science ®Google Scholar
• Liver EAFT. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2018;69(1):182–236.
   PubMed Web of Science ®Google Scholar
• Kang TW, Lim HK, Cha DI. Aggressive tumor recurrence after radiofrequency ablation for hepatocellular carcinoma. Clin Mol Hepatol. 2017;23(1):95–101.
   PubMed Web of Science ®Google Scholar
• Hirooka M, Ochi H, Koizumi Y, et al. Local recurrence of hepatocellular carcinoma in the tumor blood drainage area following radiofrequency ablation. Mol Clin Oncol. 2014;2(2):182–186.
   PubMedGoogle Scholar
• Gong Y, Tang Y, Geng Y, et al. Comparative safety and effectiveness of ultrasound-guided radiofrequency ablation combined with preoperative three-dimensional reconstruction versus surgical resection for solitary hepatocellular carcinoma of 3–5 cm. J Cancer. 2019;10(22):5568–5574.
   PubMed Web of Science ®Google Scholar
• Ganne-Carrie N, Nault JC, Ziol M, et al. Predicting recurrence following radiofrequency percutaneous ablation for hepatocellular carcinoma. Hepat Oncol. 2014;1(4):395–408.
   PubMedGoogle Scholar
• Harrison LE, Koneru B, Baramipour P, et al. Locoregional recurrences are frequent after radiofrequency ablation for hepatocellular carcinoma. J Am Coll Surg. 2003;197(5):759–764.
   PubMed Web of Science ®Google Scholar
• Reginelli A, Vacca G, Segreto T, et al. Can microvascular invasion in hepatocellular carcinoma be predicted by diagnostic imaging? A critical review. Future Oncol. 2018;14(28):2985–2994.
   PubMed Web of Science ®Google Scholar
• Kawaguchi T, Shimose S, Torimura T. Challenges and prospects in prediction and treatment for hepatocellular carcinoma with microvascular invasion. Hepatobiliary Surg Nutr. 2019;8(6):651–654.
   PubMed Web of Science ®Google Scholar
• Joo I, Lee JM. Recent advances in the imaging diagnosis of hepatocellular carcinoma: value of gadoxetic acid-enhanced MRI. Liver Cancer. 2016;5(1):67–87.
   PubMed Web of Science ®Google Scholar
• Kudo M, Matsui O, Izumi N. et al. JSH consensus-based clinical practice guidelines for the management of hepatocellular carcinoma: 2014 update by the liver cancer study group of Japan. Liver Cancer. 2014;3(3–4):458–468.
   PubMed Web of Science ®Google Scholar
• Lee S, Kang TW, Song KD, et al. Effect of microvascular invasion risk on early recurrence of hepatocellular carcinoma after surgery and radiofrequency ablation. Annals Surgery. 2019. Doi: 10.1097/SLA.0000000000003268
   Web of Science ®Google Scholar
• Lee S, Kim SH, Lee JE, et al. Preoperative gadoxetic acid-enhanced MRI for predicting microvascular invasion in patients with single hepatocellular carcinoma. J Hepatol. 2017;67(3):526–534.
   PubMed Web of Science ®Google Scholar
• Ariizumi S, Kitagawa K, Kotera Y, et al. A non-smooth tumor margin in the hepatobiliary phase of gadoxetic acid disodium (Gd-EOB-DTPA)-enhanced magnetic resonance imaging predicts microscopic portal vein invasion, intrahepatic metastasis, and early recurrence after hepatectomy in patients with hepatocellular carcinoma. J Hepatobiliary Pancreat Sci. 2011;18(4):575–585.
   PubMed Web of Science ®Google Scholar
• Ahn SY, Lee JM, Joo I, et al. Prediction of microvascular invasion of hepatocellular carcinoma using gadoxetic acid-enhanced MR and (18)F-FDG PET/CT. Abdom Imaging. 2015;40(4):843–851.
   PubMedGoogle Scholar
• Lee LH, Hwang JI, Cheng YC, et al. Comparable outcomes of ultrasound versus computed tomography in the guidance of radiofrequency ablation for hepatocellular carcinoma. PLoS One. 2017;12(1):e169655.
   PubMed Web of Science ®Google Scholar
• Song KD, Lee MW, Rhim H, et al. Percutaneous US/MRI fusion-guided radiofrequency ablation for recurrent subcentimeter hepatocellular carcinoma: technical feasibility and therapeutic outcomes. Radiology. 2018;288(3):878–886.
   PubMed Web of Science ®Google Scholar
• Sanga K, Numata K, Nihonmatsu H, et al. Use of intra-procedural fusion imaging combining contrast-enhanced ultrasound using a perflubutane-based contrast agent and auto sweep three-dimensional ultrasound for guiding radiofrequency ablation and evaluating its efficacy in patients with hepatocellular carcinoma. Int J Hyperthermia. 2020;37(1):202–211.
   PubMed Web of Science ®Google Scholar
• Toshikuni N, Takuma Y, Tomokuni J, et al. Planning sonography using real-time virtual sonography and contrast-enhanced sonography for radiofrequency ablation of inconspicuous hepatocellular carcinoma nodules. Hepatogastroenterol. 2015;62(139):661–666.
   PubMedGoogle Scholar
• Kunishi Y, Numata K, Morimoto M, et al. Efficacy of fusion imaging combining sonography and hepatobiliary phase MRI with Gd-EOB-DTPA to detect small hepatocellular carcinoma. Am J Roentgenol. 2012;198(1):106–114.
   PubMed Web of Science ®Google Scholar
• Nishigori S, Numata K, Irie K, et al. Fusion imaging with contrast-enhanced ultrasonography for evaluating the early therapeutic efficacy of radiofrequency ablation for small hypervascular hepatocellular carcinomas with iso-echoic or unclear margins on conventional ultrasonography. J Med Ultrason. 2018;45(3):405–415.
   PubMed Web of Science ®Google Scholar
• International Working Party. Terminology of nodular hepatocellular lesions. Hepatology. 1995;22(3):983–993.
   PubMed Web of Science ®Google Scholar
• International-Consensus-Group-for-Hepatocellular-Neoplasia. Pathologic diagnosis of early hepatocellular carcinoma: a report of the international consensus group for hepatocellular neoplasia. Hepatology. 2009;49(2):658–664.
   PubMed Web of Science ®Google Scholar
• Wang F, Numata K, Nakano M, et al. Diagnostic value of imaging methods in the histological four grading of hepatocellular carcinoma. Diagnostics. 2020;10(5):321.
   Web of Science ®Google Scholar
• Lee JY, Minami Y, Choi BI, et al. The AFSUMB consensus statements and recommendations for the clinical practice of contrast-enhanced ultrasound using Sonazoid. Ultrasonography. 2020;39(3):191–220.
   PubMed Web of Science ®Google Scholar
• Facciorusso A, Del PV, Antonino M, et al. Post-recurrence survival in hepatocellular carcinoma after percutaneous radiofrequency ablation. Dig Liver Dis. 2014;46(11):1014–1019.
   PubMedGoogle Scholar
• Kim SH, Lim HK, Choi D, et al. Percutaneous radiofrequency ablation of hepatocellular carcinoma: effect of histologic grade on therapeutic results. AJR Am J Roentgenol. 2006;186(5_supplement):S327–S333.
   PubMed Web of Science ®Google Scholar
• Kondo F. Histological features of early hepatocellular carcinomas and their developmental process: for daily practical clinical application: hepatocellular carcinoma. Hepatol Int. 2009;3(1):283–293.
   PubMed Web of Science ®Google Scholar
• Cho ES, Choi JY. MRI features of hepatocellular carcinoma related to biologic behavior. Korean J Radiol. 2015;16(3):449–464.
   PubMed Web of Science ®Google Scholar
• Fukuda S, Itamoto T, Nakahara H, et al. Clinicopathologic features and prognostic factors of resected solitary small-sized hepatocellular carcinoma. Hepatogastroenterology. 2005;52(64):1163–1167.
   PubMedGoogle Scholar
• Lam VW, Ng KK, Chok KS, et al. Risk factors and prognostic factors of local recurrence after radiofrequency ablation of hepatocellular carcinoma. J Am Coll Surg. 2008;207(1):20–29.
   PubMed Web of Science ®Google Scholar
• Ng KK, Poon RT, Lo CM, et al. Analysis of recurrence pattern and its influence on survival outcome after radiofrequency ablation of hepatocellular carcinoma. J Gastrointest Surg. 2008;12(1):183–191.
   PubMed Web of Science ®Google Scholar
• Sakuraoka Y, Kubota K, Imura J, et al. Microsatellite analysis of recurrent lesions confirms merit of anatomical liver resection for hepatocellular carcinoma. Anticancer Res. 2019;39(8):4315–4324.
   PubMed Web of Science ®Google Scholar
• Minami Y, Kudo M. Ultrasound fusion imaging technologies for guidance in ablation therapy for liver cancer. J Med Ultrasonics. 2020;47(2):257–263.
   PubMed Web of Science ®Google Scholar
• Huang HW. Influence of blood vessel on the thermal lesion formation during radiofrequency ablation for liver tumors. Med Phys. 2013;40(7):73303.
   PubMed Web of Science ®Google Scholar
• Nuta J, Shingaki N, Ida Y, et al. Irregular defects in hepatocellular carcinomas during the kupffer phase of contrast-enhanced ultrasonography with perfluorobutane microbubbles: pathological features and metastatic recurrence after surgical resection. Ultrasound Med Biol. 2017;43(9):1829–1836.
   PubMed Web of Science ®Google Scholar
• Nuta J, Tamai H, Mori Y, et al. Kupffer imaging by contrast-enhanced sonography with perfluorobutane microbubbles is associated with outcomes after radiofrequency ablation of hepatocellular carcinoma. J Ultrasound Med. 2016;35(2):359–371.
   PubMed Web of Science ®Google Scholar
• Xu E, Long Y, Li K, et al. Comparison of CT/MRI-CEUS and US-CEUS fusion imaging techniques in the assessment of the thermal ablation of liver tumors. Int J Hyperthermia. 2018;35(1):159–167.
   PubMed Web of Science ®Google Scholar
• Roccarina D, Garcovich M, Ainora ME, et al. Usefulness of contrast enhanced ultrasound in monitoring therapeutic response after hepatocellular carcinoma treatment. World J Hepatol. 2015;7(14):1866–1874.
   PubMed Web of Science ®Google Scholar