Aktueller Stand zu perkutanen lokalablativen Verfahren beim hepatozellulären Karzinom

Zusammenfassung

Hintergrund Das hepatozelluläre Karzinom (HCC) ist das fünfthäufigste Tumorleiden weltweit. Da viele HCCs bereits zum Zeitpunkt der Erstdiagnose nicht resektabel sind, haben sich in den letzten Jahrzenten perkutane Tumorablationen als kurativer Therapieansatz für das sehr frühe (BCLC 0) und frühe (BCLC A) HCC etabliert. Ziel dieser Arbeit ist es, einen kompakten Überblick über die aktuell zur Anwendung kommenden perkutanen lokalablativen Verfahren zu geben, basierend auf den technischen Besonderheiten sowie der klinischen Relevanz unter Berücksichtigung der aktuellen Studienlage.

Methode Die Literaturrecherche umfasste alle über MEDLINE und PubMed verfügbaren Originalarbeiten, Reviews und Metaanalysen zu den jeweiligen perkutanen Ablationsverfahren, hierbei wurde vor allem ein Fokus auf randomisiert kontrollierte Studien und Veröffentlichungen aus den letzten 10 Jahren gelegt.

Ergebnisse und Schlussfolgerung Die Radiofrequenzablation (RFA) und Mikrowellenablation (MWA) sind etablierte Verfahren, welche aufgrund ihrer starken Evidenz in internationalen und nationalen Leitlinien bei der Behandlung von HCCs im Stadium BCLC 0 und A mit einem Diameter bis zu 3 cm der chirurgischen Resektion gleichgestellt sind. Für HCCs mit einem Diameter zwischen 3 und 5 cm wird in den aktuellen S3-Leitlinien eine Kombination aus transarterieller Chemoembolisation (TACE) und Thermoablation mittels RFA oder MWA empfohlen, da bei HCCs dieser Größe die Kombinationstherapie der alleinigen Thermoablation überlegen ist und mit der chirurgischen Resektion vergleichbare Ergebnisse bezüglich des Gesamtüberlebens zeigt. Alternative, deutlich seltener eingesetzte thermische Verfahren sind die Kryotherapie (KT) und die Laserablation (LA). Zu den nicht thermischen Verfahren zählen die irreversible Elektroporation (IRE), die interstitielle Brachytherapie (IBT) und als neuestes Verfahren die Elektrochemotherapie (ECT). Aufgrund der noch nicht ausreichenden Evidenz kommen diese bis dato allerdings nur in Einzelfällen und im Rahmen von Studien zum Einsatz. Die nicht thermischen Verfahren stellen jedoch eine sinnvolle Alternative für die Ablation von HCCs in Nachbarschaft zu großen Blutgefäßen und Gallengängen dar, da sie diese Strukturen im Gegensatz zu den thermischen Ablationsverfahren deutlich weniger schädigen. Durch Fortschritte in der Technik der jeweiligen Verfahren, zunehmend gute Evidenz sowie Weiterentwicklungen bei unterstützenden Techniken wie Navigationsgeräten und Fusionsbildgebung könnten die perkutanen Ablationsverfahren in den kommenden Jahren ihre Indikationsstellung zur Behandlung größerer und weiter fortgeschrittener HCCs erweitern.

Kernaussagen:

• RFA und MWA sind für die kurative Therapie von HCC im Stadium BCLC 0 und A bis zu einer Größe von 3 cm der chirurgischen Resektion als Erstlinientherapie gleichgestellt.

• Für HCC mit einer Größe zwischen 3 und 5 cm wird eine Kombination aus TACE und RFA oder MWA empfohlen. Diese Kombinationstherapie zeigt bezüglich Gesamtüberleben der chirurgischen Resektion ähnliche Ergebnisse.

• Alternative Ablationsverfahren kommen bis dato aufgrund der mangelhaften Datenlage nur in Einzelfällen oder im Rahmen von Studien zum Einsatz. Insbesondere nichtthermische Verfahren wie die IRE, die IBT und neuerdings ECT stellen jedoch eine sinnvolle Alternative für die Ablation von HCCs in Nachbarschaft zu großen Blutgefäßen und Gallengängen dar, da sie diese Strukturen im Gegensatz zu thermischen Ablationsverfahren deutlich weniger schädigen.

Zitierweise

• Luerken L, Haimerl M, Doppler M et al. Update on Percutaneous Local Ablative Procedures for the Treatment of Hepatocellular Carcinoma. Fortschr Röntgenstr 2022; 194: 1075 – 1087

Key words

abdomen - ablation procedures - percutaneous

Publication History

Received: 13 August 2021

Accepted: 31 January 2022

Article published online:
11 May 2022

• References

• 1 Galle PR, Forner A, Llovet JM. et al. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma. J Hepatol 2018; 69: 182-236 DOI: 10.1016/j.jhep.2018.03.019.
• 2 Llovet JM, Kelley RK, Villanueva A. et al. Hepatocellular carcinoma. Nature Reviews Disease Primers 2021; 7: 6 DOI: 10.1038/s41572-020-00240-3.
• 3 Llovet JM, Bru C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 1999; 19: 329-338 DOI: 10.1055/s-2007-1007122.
• 4 Leitlinienprogramm Onkologie (Deutsche Krebsgesellschaft DK, AWMF). S3-Leitlinie: Diagnostik und Therapie des hepatozellulären Karzinoms und biliärer Karzinome (Langversion 2.0). 2021 AWMF Registernummer: 032/053OL https://www.leitlinienprogramm-onkologie.de/leitlinien/hcc-und-biliaere-karzinome
• 5 Goldberg SN, Gazelle GS, Compton CC. et al. Treatment of intrahepatic malignancy with radiofrequency ablation: radiologic-pathologic correlation. Cancer 2000; 88: 2452-2463
• 6 Ahmed M, Solbiati L, Brace CL. et al. Image-guided tumor ablation: standardization of terminology and reporting criteria--a 10-year update. Radiology 2014; 273: 241-260 DOI: 10.1148/radiol.14132958.
• 7 Lencioni RA, Allgaier HP, Cioni D. et al. Small hepatocellular carcinoma in cirrhosis: randomized comparison of radio-frequency thermal ablation versus percutaneous ethanol injection. Radiology 2003; 228: 235-240 DOI: 10.1148/radiol.2281020718.
• 8 Lin SM, Lin CJ, Lin CC. et al. Radiofrequency ablation improves prognosis compared with ethanol injection for hepatocellular carcinoma < or =4 cm. Gastroenterology 2004; 127: 1714-1723 DOI: 10.1053/j.gastro.2004.09.003.
• 9 Lencioni R, Cioni D, Crocetti L. et al. Early-stage hepatocellular carcinoma in patients with cirrhosis: long-term results of percutaneous image-guided radiofrequency ablation. Radiology 2005; 234: 961-967 DOI: 10.1148/radiol.2343040350.
• 10 Lin SM, Lin CJ, Lin CC. et al. Randomised controlled trial comparing percutaneous radiofrequency thermal ablation, percutaneous ethanol injection, and percutaneous acetic acid injection to treat hepatocellular carcinoma of 3 cm or less. Gut 2005; 54: 1151-1156 DOI: 10.1136/gut.2004.045203.
• 11 Shiina S, Teratani T, Obi S. et al. A randomized controlled trial of radiofrequency ablation with ethanol injection for small hepatocellular carcinoma. Gastroenterology 2005; 129: 122-130 DOI: 10.1053/j.gastro.2005.04.009.
• 12 Chen MS, Li JQ, Zheng Y. et al. A prospective randomized trial comparing percutaneous local ablative therapy and partial hepatectomy for small hepatocellular carcinoma. Ann Surg 2006; 243: 321-328 DOI: 10.1097/01.sla.0000201480.65519.b8.
• 13 Brunello F, Veltri A, Carucci P. et al. Radiofrequency ablation versus ethanol injection for early hepatocellular carcinoma: A randomized controlled trial. Scand J Gastroenterol 2008; 43: 727-735 DOI: 10.1080/00365520701885481.
• 14 N’Kontchou G, Mahamoudi A, Aout M. et al. Radiofrequency ablation of hepatocellular carcinoma: long-term results and prognostic factors in 235 Western patients with cirrhosis. Hepatology 2009; 50: 1475-1483 DOI: 10.1002/hep.23181.
• 15 Huang J, Yan L, Cheng Z. et al. A randomized trial comparing radiofrequency ablation and surgical resection for HCC conforming to the Milan criteria. Ann Surg 2010; 252: 903-912 DOI: 10.1097/SLA.0b013e3181efc656.
• 16 Rossi S, Ravetta V, Rosa L. et al. Repeated radiofrequency ablation for management of patients with cirrhosis with small hepatocellular carcinomas: a long-term cohort study. Hepatology 2011; 53: 136-147 DOI: 10.1002/hep.23965.
• 17 Feng K, Yan J, Li X. et al. A randomized controlled trial of radiofrequency ablation and surgical resection in the treatment of small hepatocellular carcinoma. J Hepatol 2012; 57: 794-802 DOI: 10.1016/j.jhep.2012.05.007.
• 18 Shiina S, Tateishi R, Arano T. et al Radiofrequency ablation for hepatocellular carcinoma: 10-year outcome and prognostic factors. Am J Gastroenterol 2012; 107: 569-577 ; quiz 578 DOI: 10.1038/ajg.2011.425.
• 19 Brunello F, Cantamessa A, Gaia S. et al. Radiofrequency ablation: technical and clinical long-term outcomes for single hepatocellular carcinoma up to 30 mm. Eur J Gastroenterol Hepatol 2013; 25: 842-849 DOI: 10.1097/MEG.0b013e32835ee5f1.
• 20 Francica G, Saviano A, De Sio I. et al. Long-term effectiveness of radiofrequency ablation for solitary small hepatocellular carcinoma: a retrospective analysis of 363 patients. Dig Liver Dis 2013; 45: 336-341 DOI: 10.1016/j.dld.2012.10.022.
• 21 Kim YS, Lim HK, Rhim H. et al. Ten-year outcomes of percutaneous radiofrequency ablation as first-line therapy of early hepatocellular carcinoma: analysis of prognostic factors. J Hepatol 2013; 58: 89-97 DOI: 10.1016/j.jhep.2012.09.020.
• 22 Lee DH, Lee JM, Lee JY. et al. Radiofrequency ablation of hepatocellular carcinoma as first-line treatment: long-term results and prognostic factors in 162 patients with cirrhosis. Radiology 2014; 270: 900-909 DOI: 10.1148/radiol.13130940.
• 23 Kudo M, Hasegawa K, Kawaguchi Y. et al. A multicenter randomized controlled trial to evaluate the efficacy of surgery versus radiofrequency ablation for small hepatocellular carcinoma (SURF trial): Analysis of overall survival. J Clin Oncol 2021; 39 DOI: 10.1200/JCO.2021.39.15_suppl.4093.
• 24 Ng KKC, Chok KSH, Chan ACY. et al. Randomized clinical trial of hepatic resection versus radiofrequency ablation for early-stage hepatocellular carcinoma. Br J Surg 2017; 104: 1775-1784 DOI: 10.1002/bjs.10677.
• 25 Xia Y, Li J, Liu G. et al. Long-term Effects of Repeat Hepatectomy vs Percutaneous Radiofrequency Ablation Among Patients With Recurrent Hepatocellular Carcinoma: A Randomized Clinical Trial. JAMA Oncol 2020; 6: 255-263 DOI: 10.1001/jamaoncol.2019.4477.
• 26 Miura JT, Johnston FM, Tsai S. et al. Surgical resection versus ablation for hepatocellular carcinoma </= 3 cm: a population-based analysis. HPB (Oxford) 2015; 17: 896-901 DOI: 10.1111/hpb.12446.
• 27 Takayasu K, Arii S, Sakamoto M. et al. Impact of resection and ablation for single hypovascular hepatocellular carcinoma </=2 cm analysed with propensity score weighting. Liver Int 2018; 38: 484-493 DOI: 10.1111/liv.13670.
• 28 Cho YK, Kim JK, Kim MY. et al. Systematic review of randomized trials for hepatocellular carcinoma treated with percutaneous ablation therapies. Hepatology 2009; 49: 453-459 DOI: 10.1002/hep.22648.
• 29 Orlando A, Leandro G, Olivo M. et al. Radiofrequency thermal ablation vs. percutaneous ethanol injection for small hepatocellular carcinoma in cirrhosis: meta-analysis of randomized controlled trials. Am J Gastroenterol 2009; 104: 514-524 DOI: 10.1038/ajg.2008.80.
• 30 Kudo M, Hasegawa K, Kawaguchi Y. et al. A multicenter randomized controlled trial to evaluate the efficacy of surgery versus radiofrequency ablation for small hepatocellular carcinoma (SURF trial): Analysis of overall survival. Journal of Clinical Oncology 2021; 39 DOI: 10.1200/JCO.2021.39.15_suppl.4093.
• 31 Li JK, Liu XH, Cui H. et al. Radiofrequency ablation vs. surgical resection for resectable hepatocellular carcinoma: A systematic review and meta-analysis. Mol Clin Oncol 2020; 12: 15-22 DOI: 10.3892/mco.2019.1941.
• 32 Zhou Y, Zhao Y, Li B. et al. Meta-analysis of radiofrequency ablation versus hepatic resection for small hepatocellular carcinoma. BMC Gastroenterol 2010; 10: 78 DOI: 10.1186/1471-230X-10-78.
• 33 Sala M, Llovet JM, Vilana R. et al. Initial response to percutaneous ablation predicts survival in patients with hepatocellular carcinoma. Hepatology 2004; 40: 1352-1360 DOI: 10.1002/hep.20465.
• 34 Livraghi T, Meloni F, Di Stasi M. et al. Sustained complete response and complications rates after radiofrequency ablation of very early hepatocellular carcinoma in cirrhosis: Is resection still the treatment of choice?. Hepatology 2008; 47: 82-89 DOI: 10.1002/hep.21933.
• 35 Casadei Gardini A, Marisi G, Canale M. et al. Radiofrequency ablation of hepatocellular carcinoma: a meta-analysis of overall survival and recurrence-free survival. Onco Targets Ther 2018; 11: 6555-6567 DOI: 10.2147/OTT.S170836.
• 36 Doyle A, Gorgen A, Muaddi H. et al. Outcomes of radiofrequency ablation as first-line therapy for hepatocellular carcinoma less than 3cm in potentially transplantable patients. J Hepatol 2019; 70: 866-873 DOI: 10.1016/j.jhep.2018.12.027.
• 37 Hermida M, Cassinotto C, Piron L. et al. Multimodal Percutaneous Thermal Ablation of Small Hepatocellular Carcinoma: Predictive Factors of Recurrence and Survival in Western Patients. Cancers (Basel) 2020; 12 DOI: 10.3390/cancers12020313.
• 38 Kang TW, Lim HK, Lee MW. et al. Aggressive Intrasegmental Recurrence of Hepatocellular Carcinoma after Radiofrequency Ablation: Risk Factors and Clinical Significance. Radiology 2015; 276: 274-285 DOI: 10.1148/radiol.15141215.
• 39 Seror O. Percutaneous hepatic ablation: what needs to be known in 2014. Diagn Interv Imaging 2014; 95: 665-675 DOI: 10.1016/j.diii.2014.04.002.
• 40 Doussot A, Lim C, Lahat E. et al. Complications after Hepatectomy for Hepatocellular Carcinoma Independently Shorten Survival: A Western, Single-Center Audit. Ann Surg Oncol 2017; 24: 1569-1578 DOI: 10.1245/s10434-016-5746-6.
• 41 Lu Q, Zhang N-n, Wang F. et al. Surgical and oncological outcomes after laparoscopic vs. open major hepatectomy for hepatocellular carcinoma: a systematic review and meta-analysis. Translational cancer research 2020; 9: 3324-3338
• 42 Lubner MG, Brace CL, Hinshaw JL. et al. Microwave tumor ablation: mechanism of action, clinical results, and devices. J Vasc Interv Radiol 2010; 21: S192-S203 DOI: 10.1016/j.jvir.2010.04.007.
• 43 Harari CM, Magagna M, Bedoya M. et al. Microwave Ablation: Comparison of Simultaneous and Sequential Activation of Multiple Antennas in Liver Model Systems. Radiology 2016; 278: 95-103 DOI: 10.1148/radiol.2015142151.
• 44 Brace CL. Radiofrequency and microwave ablation of the liver, lung, kidney, and bone: what are the differences?. Curr Probl Diagn Radiol 2009; 38: 135-143 DOI: 10.1067/j.cpradiol.2007.10.001.
• 45 Chong CCN, Lee KF, Cheung SYS. et al. Prospective double-blinded randomized controlled trial of Microwave versus RadioFrequency Ablation for hepatocellular carcinoma (McRFA trial). HPB (Oxford) 2020; 22: 1121-1127 DOI: 10.1016/j.hpb.2020.01.008.
• 46 Kamal A, Elmoety AAA, Rostom YAM. et al. Percutaneous radiofrequency versus microwave ablation for management of hepatocellular carcinoma: a randomized controlled trial. J Gastrointest Oncol 2019; 10: 562-571 DOI: 10.21037/jgo.2019.01.34.
• 47 Vietti Violi N, Duran R, Guiu B. et al. 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 2018; 3: 317-325 DOI: 10.1016/S2468-1253(18)30029-3.
• 48 Abdelaziz A, Elbaz T, Shousha HI. et al. Efficacy and survival analysis of percutaneous radiofrequency versus microwave ablation for hepatocellular carcinoma: an Egyptian multidisciplinary clinic experience. Surg Endosc 2014; 28: 3429-3434 DOI: 10.1007/s00464-014-3617-4.
• 49 Qian GJ, Wang N, Shen Q. et al. Efficacy of microwave versus radiofrequency ablation for treatment of small hepatocellular carcinoma: experimental and clinical studies. Eur Radiol 2012; 22: 1983-1990 DOI: 10.1007/s00330-012-2442-1.
• 50 Yu J, Yu X, Han Z. et al. Percutaneous cooled-probe microwave versus radiofrequency ablation in early-stage hepatocellular carcinoma: a phase III randomised controlled trial. Gut 2017; 66: 1172-1173
• 51 Gupta P, Maralakunte M, Kumar MP. et al. Overall survival and local recurrence following RFA, MWA, and cryoablation of very early and early HCC: a systematic review and Bayesian network meta-analysis. Eur Radiol 2021; 31: 5400-5408 DOI: 10.1007/s00330-020-07610-1.
• 52 Lu MD, Xu HX, Xie XY. et al. Percutaneous microwave and radiofrequency ablation for hepatocellular carcinoma: a retrospective comparative study. J Gastroenterol 2005; 40: 1054-1060 DOI: 10.1007/s00535-005-1671-3.
• 53 Facciorusso A, Di Maso M, Muscatiello N. Microwave ablation versus radiofrequency ablation for the treatment of hepatocellular carcinoma: A systematic review and meta-analysis. Int J Hyperthermia 2016; 32: 339-344 DOI: 10.3109/02656736.2015.1127434.
• 54 Vogl TJ, Muller PK, Hammerstingl R. et al. Malignant liver tumors treated with MR imaging-guided laser-induced thermotherapy: technique and prospective results. Radiology 1995; 196: 257-265 DOI: 10.1148/radiology.196.1.7540310.
• 55 Amin Z, Donald JJ, Masters A. et al. Hepatic metastases: interstitial laser photocoagulation with real-time US monitoring and dynamic CT evaluation of treatment. Radiology 1993; 187: 339-347 DOI: 10.1148/radiology.187.2.8475270.
• 56 Giorgio A, Tarantino L, de Stefano G. et al. Interstitial laser photocoagulation under ultrasound guidance of liver tumors: results in 104 treated patients. Eur J Ultrasound 2000; 11: 181-188 DOI: 10.1016/s0929-8266(00)00086-0.
• 57 Pacella CM, Bizzarri G, Francica G. et al. Percutaneous laser ablation in the treatment of hepatocellular carcinoma with small tumors: analysis of factors affecting the achievement of tumor necrosis. J Vasc Interv Radiol 2005; 16: 1447-1457 DOI: 10.1097/01.rvi.90000172121.82299.38.
• 58 Francica G, Iodice G, Delle Cave M. et al. Factors predicting complete necrosis rate after ultrasound-guided percutaneous laser thermoablation of small hepatocellular carcinoma tumors in cirrhotic patients: a multivariate analysis. Acta Radiol 2007; 48: 514-519 DOI: 10.1080/02841850701199942.
• 59 Pacella CM, Bizzarri G, Magnolfi F. et al. Laser thermal ablation in the treatment of small hepatocellular carcinoma: results in 74 patients. Radiology 2001; 221: 712-720 DOI: 10.1148/radiol.2213001501.
• 60 Pacella CM, Francica G, Di Lascio FM. et al. Long-term outcome of cirrhotic patients with early hepatocellular carcinoma treated with ultrasound-guided percutaneous laser ablation: a retrospective analysis. J Clin Oncol 2009; 27: 2615-2621 DOI: 10.1200/JCO.2008.19.0082.
• 61 Orlacchio A, Bolacchi F, Chegai F. et al. Comparative evaluation of percutaneous laser and radiofrequency ablation in patients with HCC smaller than 4 cm. Radiol Med 2014; 119: 298-308 DOI: 10.1007/s11547-013-0339-y.
• 62 Di Costanzo GG, Tortora R, D’Adamo G. et al. Radiofrequency ablation versus laser ablation for the treatment of small hepatocellular carcinoma in cirrhosis: a randomized trial. J Gastroenterol Hepatol 2015; 30: 559-565 DOI: 10.1111/jgh.12791.
• 63 Morisco F, Camera S, Guarino M. et al. Laser ablation is superior to TACE in large-sized hepatocellular carcinoma: a pilot case-control study. Oncotarget 2018; 9: 17483-17490 DOI: 10.18632/oncotarget.24756.
• 64 Rong G, Bai W, Dong Z. et al. Long-term outcomes of percutaneous cryoablation for patients with hepatocellular carcinoma within Milan criteria. PLoS One 2015; 10: e0123065 DOI: 10.1371/journal.pone.0123065.
• 65 Xu J, Noda C, Erickson A. et al. Radiofrequency Ablation vs. Cryoablation for Localized Hepatocellular Carcinoma: A Propensity-matched Population Study. Anticancer Res 2018; 38: 6381-6386 DOI: 10.21873/anticanres.12997.
• 66 Wang C, Wang H, Yang W. et al. Multicenter randomized controlled trial of percutaneous cryoablation versus radiofrequency ablation in hepatocellular carcinoma. Hepatology 2015; 61: 1579-1590 DOI: 10.1002/hep.27548.
• 67 Ei S, Hibi T, Tanabe M. et al. Cryoablation provides superior local control of primary hepatocellular carcinomas of >2 cm compared with radiofrequency ablation and microwave coagulation therapy: an underestimated tool in the toolbox. Ann Surg Oncol 2015; 22: 1294-1300 DOI: 10.1245/s10434-014-4114-7.
• 68 Kim R, Kang TW, Cha DI. et al. Percutaneous cryoablation for perivascular hepatocellular carcinoma: Therapeutic efficacy and vascular complications. Eur Radiol 2019; 29: 654-662 DOI: 10.1007/s00330-018-5617-6.
• 69 Glazer DI, Tatli S, Shyn PB. et al. Percutaneous Image-Guided Cryoablation of Hepatic Tumors: Single-Center Experience With Intermediate to Long-Term Outcomes. Am J Roentgenol American journal of roentgenology 2017; 209: 1381-1389 DOI: 10.2214/Am J Roentgenol.16.17582.
• 70 Mahnken AH, Konig AM, Figiel JH. Current Technique and Application of Percutaneous Cryotherapy. Rofo 2018; 190: 836-846 DOI: 10.1055/a-0598-5134.
• 71 Tang C, Shen J, Feng W. et al. Combination Therapy of Radiofrequency Ablation and Transarterial Chemoembolization for Unresectable Hepatocellular Carcinoma: A Retrospective Study. Medicine (Baltimore) 2016; 95: e3754 DOI: 10.1097/MD.0000000000003754.
• 72 Peng ZW, Zhang YJ, Chen MS. et al. Radiofrequency ablation with or without transcatheter arterial chemoembolization in the treatment of hepatocellular carcinoma: a prospective randomized trial. J Clin Oncol 2013; 31: 426-432 DOI: 10.1200/JCO.2012.42.9936.
• 73 Zhang R, Shen L, Zhao L. et al. Combined transarterial chemoembolization and microwave ablation versus transarterial chemoembolization in BCLC stage B hepatocellular carcinoma. Diagn Interv Radiol 2018; 24: 219-224 DOI: 10.5152/dir.2018.17528.
• 74 Endo K, Kuroda H, Oikawa T. et al. Efficacy of combination therapy with transcatheter arterial chemoembolization and radiofrequency ablation for intermediate-stage hepatocellular carcinoma. Scand J Gastroenterol 2018; 53: 1575-1583 DOI: 10.1080/00365521.2018.1548645.
• 75 Gui CH, Baey S, D’Cruz RT. et al. Trans-arterial chemoembolization + radiofrequency ablation versus surgical resection in hepatocellular carcinoma – A meta-analysis. Eur J Surg Oncol 2020; 46: 763-771 DOI: 10.1016/j.ejso.2020.01.004.
• 76 Zhang TQ, Huang ZM, Shen JX. et al. Safety and effectiveness of multi-antenna microwave ablation-oriented combined therapy for large hepatocellular carcinoma. Therap Adv Gastroenterol 2019; 12: 1756284819862966 DOI: 10.1177/1756284819862966.
• 77 Weaver JC, Chizmadzhev YA. Theory of Electroporation: A Review. Bioelectrochemistry and Bioenergetics 1996; 41: 135-160
• 78 Lee EW, Chen C, Prieto VE. et al. Advanced hepatic ablation technique for creating complete cell death: irreversible electroporation. Radiology 2010; 255: 426-433 DOI: 10.1148/radiol.10090337.
• 79 Kalra N, Gupta P, Chawla Y. et al. Locoregional treatment for hepatocellular carcinoma: The best is yet to come. World J Radiol 2015; 7: 306-318 DOI: 10.4329/wjr.v7.i10.306.
• 80 Scheffer HJ, Nielsen K, de Jong MC. et al Irreversible electroporation for nonthermal tumor ablation in the clinical setting: a systematic review of safety and efficacy. J Vasc Interv Radiol 2014; 25: 997-1011 ; quiz 1011 DOI: 10.1016/j.jvir.2014.01.028.
• 81 Gupta P, Maralakunte M, Sagar S. et al. Efficacy and safety of irreversible electroporation for malignant liver tumors: a systematic review and meta-analysis. Eur Radiol 2021; DOI: 10.1007/s00330-021-07742-y.
• 82 Vogel A, Cervantes A, Chau I. et al. Hepatocellular carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 2018; 29: iv238-iv255 DOI: 10.1093/annonc/mdy308.
• 83 Ricke J, Wust P, Stohlmann A. et al. CT-Guided brachytherapy. A novel percutaneous technique for interstitial ablation of liver metastases. Strahlenther Onkol 2004; 180: 274-280 DOI: 10.1007/s00066-004-1179-4.
• 84 Walter F, Nierer L, Rottler M. et al. Comparison of liver exposure in CT-guided high-dose rate (HDR) interstitial brachytherapy versus SBRT in hepatocellular carcinoma. Radiat Oncol 2021; 16: 86 DOI: 10.1186/s13014-021-01812-7.
• 85 Denecke T, Stelter L, Schnapauff D. et al. CT-guided Interstitial Brachytherapy of Hepatocellular Carcinoma before Liver Transplantation: an Equivalent Alternative to Transarterial Chemoembolization?. Eur Radiol 2015; 25: 2608-2616 DOI: 10.1007/s00330-015-3660-0.
• 86 Mohnike K, Wieners G, Schwartz F. et al. Computed tomography-guided high-dose-rate brachytherapy in hepatocellular carcinoma: safety, efficacy, and effect on survival. Int J Radiat Oncol Biol Phys 2010; 78: 172-179 DOI: 10.1016/j.ijrobp.2009.07.1700.
• 87 Collettini F, Schreiber N, Schnapauff D. et al. CT-guided high-dose-rate brachytherapy of unresectable hepatocellular carcinoma. Strahlenther Onkol 2015; 191: 405-412 DOI: 10.1007/s00066-014-0781-3.
• 88 Collettini F, Schnapauff D, Poellinger A. et al. Hepatocellular carcinoma: computed-tomography-guided high-dose-rate brachytherapy (CT-HDRBT) ablation of large (5-7 cm) and very large (>7 cm) tumours. Eur Radiol 2012; 22: 1101-1109 DOI: 10.1007/s00330-011-2352-7.
• 89 Mohnike K, Steffen IG, Seidensticker M. et al. Radioablation by Image-Guided (HDR) Brachytherapy and Transarterial Chemoembolization in Hepatocellular Carcinoma: A Randomized Phase II Trial. Cardiovasc Intervent Radiol 2019; 42: 239-249 DOI: 10.1007/s00270-018-2127-5.
• 90 Geboers B, Scheffer HJ, Graybill PM. et al. High-Voltage Electrical Pulses in Oncology: Irreversible Electroporation, Electrochemotherapy, Gene Electrotransfer, Electrofusion, and Electroimmunotherapy. Radiology 2020; 295: 254-272 DOI: 10.1148/radiol.2020192190.
• 91 Miklavcic D, Mali B, Kos B. et al. Electrochemotherapy: from the drawing board into medical practice. Biomed Eng Online 2014; 13: 29 DOI: 10.1186/1475-925X-13-29.
• 92 Gehl J, Sersa G, Matthiessen LW. et al. Updated standard operating procedures for electrochemotherapy of cutaneous tumours and skin metastases. Acta Oncol 2018; 57: 874-882 DOI: 10.1080/0284186X.2018.1454602.
• 93 Mir LM, Belehradek M, Domenge C. et al. [Electrochemotherapy, a new antitumor treatment: first clinical trial]. C R Acad Sci III 1991; 313: 613-618
• 94 Leitlinienprogramm Onkologie (Deutsche Krebsgesellschaft DK, AWMF). S3-Leitlinie zur Diagnostik, Therapie und Nachsorge des Melanoms, Version 3.3 – Juli 2020. AWMF-Register-Nummer: 032/024OL.
• 95 O’Sullivan JM, Huddart RA, Norman AR. et al. Predicting the risk of bleomycin lung toxicity in patients with germ-cell tumours. Ann Oncol 2003; 14: 91-96 DOI: 10.1093/annonc/mdg020.
• 96 Edhemovic I, Brecelj E, Gasljevic G. et al. Intraoperative electrochemotherapy of colorectal liver metastases. J Surg Oncol 2014; 110: 320-327 DOI: 10.1002/jso.23625.
• 97 Coletti L, Battaglia V, De Simone P. et al. Safety and feasibility of electrochemotherapy in patients with unresectable colorectal liver metastases: A pilot study. Int J Surg 2017; 44: 26-32 DOI: 10.1016/j.ijsu.2017.06.033.
• 98 Djokic M, Cemazar M, Popovic P. et al. Electrochemotherapy as treatment option for hepatocellular carcinoma, a prospective pilot study. Eur J Surg Oncol 2018; 44: 651-657 DOI: 10.1016/j.ejso.2018.01.090.
• 99 Gasljevic G, Edhemovic I, Cemazar M. et al. Histopathological findings in colorectal liver metastases after electrochemotherapy. PLoS One 2017; 12: e0180709 DOI: 10.1371/journal.pone.0180709.
• 100 Djokic M, Dezman R, Cemazar M. et al. Percutaneous image guided electrochemotherapy of hepatocellular carcinoma: technological advancement. Radiol Oncol 2020; 54: 347-352
• 101 Luerken L, Doppler M, Brunner SM. et al. Stereotactic Percutaneous Electrochemotherapy as Primary Approach for Unresectable Large HCC at the Hepatic Hilum. CardioVascular and Interventional Radiology 2021; DOI: 10.1007/s00270-021-02841-1.
• 102 Beyer LP, Pregler B, Michalik K. et al. Evaluation of a robotic system for irreversible electroporation (IRE) of malignant liver tumors: initial results. Int J Comput Assist Radiol Surg 2017; 12: 803-809 DOI: 10.1007/s11548-016-1485-1.
• 103 Engstrand J, Toporek G, Harbut P. et al. Stereotactic CT-Guided Percutaneous Microwave Ablation of Liver Tumors With the Use of High-Frequency Jet Ventilation: An Accuracy and Procedural Safety Study. Am J Roentgenol American journal of roentgenology 2017; 208: 193-200 DOI: 10.2214/Am J Roentgenol.15.15803.
• 104 Beyer LP, Lurken L, Verloh N. et al. Stereotactically navigated percutaneous microwave ablation (MWA) compared to conventional MWA: a matched pair analysis. Int J Comput Assist Radiol Surg 2018; 13: 1991-1997 DOI: 10.1007/s11548-018-1778-7.
• 105 Mbalisike EC, Vogl TJ, Zangos S. et al. Image-guided microwave thermoablation of hepatic tumours using novel robotic guidance: an early experience. Eur Radiol 2015; 25: 454-462 DOI: 10.1007/s00330-014-3398-0.
• 106 Abdullah BJ, Yeong CH, Goh KL. et al. Robotic-assisted thermal ablation of liver tumours. Eur Radiol 2015; 25: 246-257 DOI: 10.1007/s00330-014-3391-7.
• 107 Durand P, Moreau-Gaudry A, Silvent AS. et al. Computer assisted electromagnetic navigation improves accuracy in computed tomography guided interventions: A prospective randomized clinical trial. PLoS One 2017; 12: e0173751 DOI: 10.1371/journal.pone.0173751.
• 108 Beyer LP, Pregler B, Niessen C. et al. Robot-assisted microwave thermoablation of liver tumors: a single-center experience. Int J Comput Assist Radiol Surg 2016; 11: 253-259 DOI: 10.1007/s11548-015-1286-y.
• 109 Solbiati M, Passera KM, Rotilio A. et al. Augmented reality for interventional oncology: proof-of-concept study of a novel high-end guidance system platform. Eur Radiol Exp 2018; 2: 18 DOI: 10.1186/s41747-018-0054-5.
• 110 Mauri G, Cova L, De Beni S. et al. Real-time US-CT/MRI image fusion for guidance of thermal ablation of liver tumors undetectable with US: results in 295 cases. Cardiovasc Intervent Radiol 2015; 38: 143-151 DOI: 10.1007/s00270-014-0897-y.
• 111 Marty M, Sersa G, Garbay JR. et al. Electrochemotherapy – An easy, highly effective and safe treatment of cutaneous and subcutaneous metastases: Results of ESOPE (European Standard Operating Procedures of Electrochemotherapy) study. European Journal of Cancer Supplements 2006; 4: 3-13 DOI: 10.1016/j.ejcsup.2006.08.002.
• 112 Probst U, Fuhrmann I, Beyer L. et al. Electrochemotherapy as a New Modality in Interventional Oncology: A Review. Technology in Cancer Research & Treatment 2018; 17: 1-12 DOI: 10.1177/1533033818785329.
• 113 Djokic M, Cemazar M, Popovic P. et al. Electrochemotherapy as treatment option for hepatocellular carcinoma, a prospective pilot study. Eur J Surg Oncol 2018; 44: 651-657