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Digestive Disease Interventions 2017; 01(02): 105-114
DOI: 10.1055/s-0037-1603891
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Choice of Intra-arterial Therapy for Hepatocellular Carcinoma: Evidence and Future Horizons

Mansur A. Ghani
1   Department of Radiology and Biomedical Imaging, Yale University School of Medicine, New Haven, Connecticut
,
Vinayak Thakur
1   Department of Radiology and Biomedical Imaging, Yale University School of Medicine, New Haven, Connecticut
,
Jean-François Geschwind
1   Department of Radiology and Biomedical Imaging, Yale University School of Medicine, New Haven, Connecticut
› Author Affiliations
Further Information

Publication History

17 December 2016

11 May 2017

Publication Date:
12 June 2017 (online)

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Abstract

Hepatocellular carcinoma is the second most common cause of cancer-related deaths worldwide. Along with viral and alcoholic hepatitis, obesity is the leading cause for increasing incidence in the western world, specifically in the United States. As most patients initially present with intermediate to advanced stage disease, curative therapies such as ablation, surgical resection, or liver transplantation cannot usually be applied. Thus, intra-arterial therapies (IATs), such as transarterial chemoembolization (TACE), have become a mainstay of treatment. Several variations of transarterial embolotherapy, such as bland transarterial embolization or drug-eluting bead TACE, are currently available and used in clinical practice. Yttrium-90 radioembolization is a distinct IAT that relies on delivery of radiation to surrounding tissue for tumor death. However, no clear guidelines or evidence exist that would favor one of these options over the other, leaving the decision-making process open to influence by local expertise and experience. In addition, combining TACE with systemic antiangiogenic agents, such as the multityrosine kinase inhibitor sorafenib, has been investigated in several prospective clinical trials without clearly demonstrating substantial survival benefits of the combination over TACE alone. This review will summarize and discuss the available clinical evidence and indications for each treatment modality with the goal of facilitating clinical decision-making processes, and provide an overview of the ongoing efforts to compare different IAT modalities.

Keywords

intra-arterial therapy - HCC - cTACE - TAE - DEB-TACE
 

  • References

  • 1 El-Serag HB. Hepatocellular carcinoma. N Engl J Med 2011; 365 (12) 1118-1127
    CrossrefPubMedGoogle Scholar
  • 2 Ferlay J, Soerjomataram I, Dikshit R. , et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2015; 136 (05) E359-E386
    CrossrefPubMedGoogle Scholar
  • 3 El-Serag HB, Kanwal F. . Epidemiology of hepatocellular carcinoma in the United States: where are we? Where do we go? Hepatology 2014; 60 (05) 1767-1775
    CrossrefPubMed
  • 4 Arciero CA, Sigurdson ER. Liver-directed therapies for hepatocellular carcinoma. J Natl Compr Canc Netw 2006; 4 (08) 768-774
    CrossrefPubMedGoogle Scholar
  • 5 Lewandowski RJ, Geschwind JF, Liapi E, Salem R. Transcatheter intraarterial therapies: rationale and overview. Radiology 2011; 259 (03) 641-657
    CrossrefPubMedGoogle Scholar
  • 6 Benson III AB, Abrams TA, Ben-Josef E. , et al. NCCN clinical practice guidelines in oncology: hepatobiliary cancers. J Natl Compr Canc Netw 2009; 7 (04) 350-391
    CrossrefPubMedGoogle Scholar
  • 7 Mannelli L, Kim S, Hajdu CH, Babb JS, Clark TW, Taouli B. Assessment of tumor necrosis of hepatocellular carcinoma after chemoembolization: diffusion-weighted and contrast-enhanced MRI with histopathologic correlation of the explanted liver. AJR Am J Roentgenol 2009; 193 (04) 1044-1052
    CrossrefPubMedGoogle Scholar
  • 8 Sergio A, Cristofori C, Cardin R. , et al. Transcatheter arterial chemoembolization (TACE) in hepatocellular carcinoma (HCC): the role of angiogenesis and invasiveness. Am J Gastroenterol 2008; 103 (04) 914-921
    CrossrefPubMedGoogle Scholar
  • 9 Scartozzi M, Faloppi L, Bianconi M. , et al. The role of LDH serum levels in predicting global outcome in HCC patients undergoing TACE: implications for clinical management. PLoS One 2012; 7 (03) e32653
    CrossrefPubMedGoogle Scholar
  • 10 Llovet JM, Ricci S, Mazzaferro V. , et al; SHARP Investigators Study Group. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008; 359 (04) 378-390
    CrossrefPubMedGoogle Scholar
  • 11 Cheng A-L, Kang Y-K, Chen Z. , et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol 2009; 10 (01) 25-34
    CrossrefPubMedGoogle Scholar
  • 12 Yamada R, Nakatsuka H, Nakamura K. , et al. Hepatic artery embolization in 32 patients with unresectable hepatoma. Osaka City Med J 1980; 26 (02) 81-96
    PubMedGoogle Scholar
  • 13 Idée JM, Guiu B. Use of Lipiodol as a drug-delivery system for transcatheter arterial chemoembolization of hepatocellular carcinoma: a review. Crit Rev Oncol Hematol 2013; 88 (03) 530-549
    CrossrefPubMedGoogle Scholar
  • 14 Yumoto Y, Jinno K, Tokuyama K. , et al. Hepatocellular carcinoma detected by iodized oil. Radiology 1985; 154 (01) 19-24
    CrossrefPubMedGoogle Scholar
  • 15 Bruix J, Sherman M. ; American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma: an update. Hepatology 2011; 53 (03) 1020-1022
    CrossrefPubMedGoogle Scholar
  • 16 Petruzzi NJ, Frangos AJ, Fenkel JM. , et al. Single-center comparison of three chemoembolization regimens for hepatocellular carcinoma. J Vasc Interv Radiol 2013; 24 (02) 266-273
    CrossrefPubMedGoogle Scholar
  • 17 Mouli SK, Hickey R, Thornburg B. , et al. Single- versus triple-drug chemoembolization for hepatocellular carcinoma: comparing outcomes by toxicity, imaging response, and survival. J Vasc Interv Radiol 2016; 27 (09) 1279-1287
    CrossrefPubMedGoogle Scholar
  • 18 Brown DB, Gould JE, Gervais DA. , et al; Society of Interventional Radiology Technology Assessment Committee and the International Working Group on Image-Guided Tumor Ablation. Transcatheter therapy for hepatic malignancy: standardization of terminology and reporting criteria. J Vasc Interv Radiol 2009; 20 (7, Suppl): S425-S434
    CrossrefPubMedGoogle Scholar
  • 19 Kim YJ, Lee HG, Park JM. , et al. Polyvinyl alcohol embolization adjuvant to oily chemoembolization in advanced hepatocellular carcinoma with arterioportal shunts. Korean J Radiol 2007; 8 (04) 311-319
    CrossrefPubMedGoogle Scholar
  • 20 Laurent A, Beaujeux R, Wassef M, Rüfenacht D, Boschetti E, Merland JJ. Trisacryl gelatin microspheres for therapeutic embolization, I: development and in vitro evaluation. AJNR Am J Neuroradiol 1996; 17 (03) 533-540
    PubMedGoogle Scholar
  • 21 Pelletier G, Roche A, Ink O. , et al. A randomized trial of hepatic arterial chemoembolization in patients with unresectable hepatocellular carcinoma. J Hepatol 1990; 11 (02) 181-184
    CrossrefPubMedGoogle Scholar
  • 22 Cheng AL, Amarapurkar D, Chao Y. , et al. Re-evaluating transarterial chemoembolization for the treatment of hepatocellular carcinoma: consensus recommendations and review by an International Expert Panel. Liver Int 2014; 34 (02) 174-183
    CrossrefPubMedGoogle Scholar
  • 23 Yamashita Y, Torashima M, Oguni T. , et al. Liver parenchymal changes after transcatheter arterial embolization therapy for hepatoma: CT evaluation. Abdom Imaging 1993; 18 (04) 352-356
    CrossrefPubMedGoogle Scholar
  • 24 Ernst O, Sergent G, Mizrahi D, Delemazure O, Paris JC, L'Herminé C. Treatment of hepatocellular carcinoma by transcatheter arterial chemoembolization: comparison of planned periodic chemoembolization and chemoembolization based on tumor response. AJR Am J Roentgenol 1999; 172 (01) 59-64
    CrossrefPubMedGoogle Scholar
  • 25 Wang S-Y, Zhu W-H, Vargulick S, Lin SB, Meng Z-Q. Nausea and vomiting after transcatheter arterial chemoembolization for hepatocellular carcinoma: incidence and risk factor analysis. Asian Pac J Cancer Prev 2013; 14 (10) 5995-6000
    CrossrefPubMedGoogle Scholar
  • 26 Marelli L, Stigliano R, Triantos C. , et al. Transarterial therapy for hepatocellular carcinoma: which technique is more effective? A systematic review of cohort and randomized studies. Cardiovasc Intervent Radiol 2007; 30 (01) 6-25
    CrossrefPubMedGoogle Scholar
  • 27 Llovet JM, Brú C, Bruix J. Prognosis of hepatocellular carcinoma: the BCLC staging classification. Semin Liver Dis 1999; 19 (03) 329-338
    Article in Thieme ConnectPubMedGoogle Scholar
  • 28 Brown DB, Fundakowski CE, Lisker-Melman M. , et al. Comparison of MELD and Child-Pugh scores to predict survival after chemoembolization for hepatocellular carcinoma. J Vasc Interv Radiol 2004; 15 (11) 1209-1218
    CrossrefPubMedGoogle Scholar
  • 29 Madden MV, Krige JE, Bailey S. , et al. Randomised trial of targeted chemotherapy with lipiodol and 5-epidoxorubicin compared with symptomatic treatment for hepatoma. Gut 1993; 34 (11) 1598-1600
    CrossrefPubMedGoogle Scholar
  • 30 Groupe d'Etude et de Traitement du Carcinome Hépatocellulaire. A comparison of lipiodol chemoembolization and conservative treatment for unresectable hepatocellular carcinoma. N Engl J Med 1995; 332 (19) 1256-1261
    CrossrefPubMedGoogle Scholar
  • 31 Llovet JM, Real MI, Montaña X. , et al; Barcelona Liver Cancer Group. Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial. Lancet 2002; 359 (9319): 1734-1739
    CrossrefPubMedGoogle Scholar
  • 32 Lo C-M, Ngan H, Tso W-K. , et al. Randomized controlled trial of transarterial lipiodol chemoembolization for unresectable hepatocellular carcinoma. Hepatology 2002; 35 (05) 1164-1171
    CrossrefPubMedGoogle Scholar
  • 33 Llovet JM, Bruix J. Systematic review of randomized trials for unresectable hepatocellular carcinoma: chemoembolization improves survival. Hepatology 2003; 37 (02) 429-442
    CrossrefPubMedGoogle Scholar
  • 34 European Association for the Study of the Liver; European Organisation for Research and Treatment of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol 2012; 56 (04) 908-943
    CrossrefPubMedGoogle Scholar
  • 35 Kudo M, Han G, Finn RS. , et al. Brivanib as adjuvant therapy to transarterial chemoembolization in patients with hepatocellular carcinoma: a randomized phase III trial. Hepatology 2014; 60 (05) 1697-1707
    CrossrefPubMedGoogle Scholar
  • 36 Kim KM, Kim JH, Park IS. , et al. Reappraisal of repeated transarterial chemoembolization in the treatment of hepatocellular carcinoma with portal vein invasion. J Gastroenterol Hepatol 2009; 24 (05) 806-814
    CrossrefPubMedGoogle Scholar
  • 37 Luo J, Guo R-P, Lai ECH. , et al. Transarterial chemoembolization for unresectable hepatocellular carcinoma with portal vein tumor thrombosis: a prospective comparative study. Ann Surg Oncol 2011; 18 (02) 413-420
    CrossrefPubMedGoogle Scholar
  • 38 Chung GE, Lee J-H, Kim HY. , et al. Transarterial chemoembolization can be safely performed in patients with hepatocellular carcinoma invading the main portal vein and may improve the overall survival. Radiology 2011; 258 (02) 627-634
    CrossrefPubMedGoogle Scholar
  • 39 Gorodetski B, Chapiro J, Schernthaner R. , et al. Advanced-stage hepatocellular carcinoma with portal vein thrombosis: conventional versus drug-eluting beads transcatheter arterial chemoembolization. Eur Radiol 2017; 27 (02) 526-535
    CrossrefPubMedGoogle Scholar
  • 40 Zhao Y, Duran R, Chapiro J. , et al. Transarterial chemoembolization for the treatment of advanced-stage hepatocellular carcinoma. J Gastrointest Surg 2016; 20 (12) 2002-2009
    CrossrefPubMedGoogle Scholar
  • 41 Zhao Y, Wang WJ, Guan S. , et al. Sorafenib combined with transarterial chemoembolization for the treatment of advanced hepatocellular carcinoma: a large-scale multicenter study of 222 patients. Ann Oncol 2013; 24 (07) 1786-1792
    CrossrefPubMedGoogle Scholar
  • 42 Hong K, Khwaja A, Liapi E, Torbenson MS, Georgiades CS, Geschwind JF. New intra-arterial drug delivery system for the treatment of liver cancer: preclinical assessment in a rabbit model of liver cancer. Clin Cancer Res 2006; 12 (08) 2563-2567
    CrossrefPubMedGoogle Scholar
  • 43 Lammer J, Malagari K, Vogl T. , et al; PRECISION V Investigators. Prospective randomized study of doxorubicin-eluting-bead embolization in the treatment of hepatocellular carcinoma: results of the PRECISION V study. Cardiovasc Intervent Radiol 2010; 33 (01) 41-52
    CrossrefPubMedGoogle Scholar
  • 44 Reyes DK, Vossen JA, Kamel IR. , et al. Single-center phase II trial of transarterial chemoembolization with drug-eluting beads for patients with unresectable hepatocellular carcinoma: initial experience in the United States. Cancer J 2009; 15 (06) 526-532
    CrossrefPubMedGoogle Scholar
  • 45 Constantin M, Fundueanu G, Bortolotti F, Cortesi R, Ascenzi P, Menegatti E. Preparation and characterisation of poly(vinyl alcohol)/cyclodextrin microspheres as matrix for inclusion and separation of drugs. Int J Pharm 2004; 285 (1-2): 87-96
    CrossrefPubMedGoogle Scholar
  • 46 Qian J, Truebenbach J, Graepler F. , et al. Application of poly-lactide-co-glycolide-microspheres in the transarterial chemoembolization in an animal model of hepatocellular carcinoma. World J Gastroenterol 2003; 9 (01) 94-98
    CrossrefPubMedGoogle Scholar
  • 47 Gonzalez MV, Tang Y, Phillips GJ. , et al. Doxorubicin eluting beads-2: methods for evaluating drug elution and in-vitro:in-vivo correlation. J Mater Sci Mater Med 2008; 19 (02) 767-775
    CrossrefPubMedGoogle Scholar
  • 48 Malagari K, Pomoni M, Spyridopoulos TN. , et al. Safety profile of sequential transcatheter chemoembolization with DC Bead™: results of 237 hepatocellular carcinoma (HCC) patients. Cardiovasc Intervent Radiol 2011; 34 (04) 774-785
    CrossrefPubMedGoogle Scholar
  • 49 Gholamrezanezhad A, Mirpour S, Geschwind JF. , et al. Evaluation of 70-150-μm doxorubicin-eluting beads for transcatheter arterial chemoembolization in the rabbit liver VX2 tumour model. Eur Radiol 2016; 26 (10) 3474-3482
    CrossrefPubMedGoogle Scholar
  • 50 Spreafico C, Cascella T, Facciorusso A. , et al. Transarterial chemoembolization for hepatocellular carcinoma with a new generation of beads: clinical-radiological outcomes and safety profile. Cardiovasc Intervent Radiol 2015; 38 (01) 129-134
    CrossrefPubMedGoogle Scholar
  • 51 Lewis AL, Gonzalez MV, Lloyd AW. , et al. DC bead: in vitro characterization of a drug-delivery device for transarterial chemoembolization. J Vasc Interv Radiol 2006; 17 (2, Pt 1): 335-342
    CrossrefPubMedGoogle Scholar
  • 52 Namur J, Citron SJ, Sellers MT. , et al. Embolization of hepatocellular carcinoma with drug-eluting beads: doxorubicin tissue concentration and distribution in patient liver explants. J Hepatol 2011; 55 (06) 1332-1338
    CrossrefPubMedGoogle Scholar
  • 53 Varela M, Real MI, Burrel M. , et al. Chemoembolization of hepatocellular carcinoma with drug eluting beads: efficacy and doxorubicin pharmacokinetics. J Hepatol 2007; 46 (03) 474-481
    CrossrefPubMedGoogle Scholar
  • 54 Poon RTP, Tso WK, Pang RWC. , et al. A phase I/II trial of chemoembolization for hepatocellular carcinoma using a novel intra-arterial drug-eluting bead. Clin Gastroenterol Hepatol 2007; 5 (09) 1100-1108
    CrossrefPubMedGoogle Scholar
  • 55 Malagari K, Chatzimichael K, Alexopoulou E. , et al. Transarterial chemoembolization of unresectable hepatocellular carcinoma with drug eluting beads: results of an open-label study of 62 patients. Cardiovasc Intervent Radiol 2008; 31 (02) 269-280
    CrossrefPubMedGoogle Scholar
  • 56 Malagari K, Pomoni M, Moschouris H. , et al. Chemoembolization with doxorubicin-eluting beads for unresectable hepatocellular carcinoma: five-year survival analysis. Cardiovasc Intervent Radiol 2012; 35 (05) 1119-1128
    CrossrefPubMedGoogle Scholar
  • 57 Burrel M, Reig M, Forner A. , et al. Survival of patients with hepatocellular carcinoma treated by transarterial chemoembolisation (TACE) using Drug Eluting Beads. Implications for clinical practice and trial design. J Hepatol 2012; 56 (06) 1330-1335
    CrossrefPubMedGoogle Scholar
  • 58 Kalva SP, Pectasides M, Liu R. , et al. Safety and effectiveness of chemoembolization with drug-eluting beads for advanced-stage hepatocellular carcinoma. Cardiovasc Intervent Radiol 2014; 37 (02) 381-387
    CrossrefPubMedGoogle Scholar
  • 59 Prajapati HJ, Dhanasekaran R, El-Rayes BF. , et al. Safety and efficacy of doxorubicin drug-eluting bead transarterial chemoembolization in patients with advanced hepatocellular carcinoma. J Vasc Interv Radiol 2013; 24 (03) 307-315
    CrossrefPubMedGoogle Scholar
  • 60 Grosso M, Vignali C, Quaretti P. , et al. Transarterial chemoembolization for hepatocellular carcinoma with drug-eluting microspheres: preliminary results from an Italian multicentre study. Cardiovasc Intervent Radiol 2008; 31 (06) 1141-1149
    CrossrefPubMedGoogle Scholar
  • 61 Malagari K, Pomoni M, Moschouris H. , et al. Chemoembolization of hepatocellular carcinoma with HepaSphere 30-60 μm. Safety and efficacy study. Cardiovasc Intervent Radiol 2014; 37 (01) 165-175
    CrossrefPubMedGoogle Scholar
  • 62 Golfieri R, Giampalma E, Renzulli M. , et al; Precision Italia Study Group. Randomised controlled trial of doxorubicin-eluting beads vs conventional chemoembolisation for hepatocellular carcinoma. Br J Cancer 2014; 111 (02) 255-264
    CrossrefPubMedGoogle Scholar
  • 63 Song MJ, Chun HJ, Song DS. , et al. Comparative study between doxorubicin-eluting beads and conventional transarterial chemoembolization for treatment of hepatocellular carcinoma. J Hepatol 2012; 57 (06) 1244-1250
    CrossrefPubMedGoogle Scholar
  • 64 Zou JH, Zhang L, Ren ZG, Ye S-L. Efficacy and safety of cTACE versus DEB-TACE in patients with hepatocellular carcinoma: a meta-analysis. J Dig Dis 2016; 17 (08) 510-517
    CrossrefPubMedGoogle Scholar
  • 65 Duran R, Sharma K, Dreher MR. , et al. A novel inherently radiopaque bead for transarterial embolization to treat liver cancer - a pre-clinical study. Theranostics 2016; 6 (01) 28-39
    CrossrefPubMedGoogle Scholar
  • 66 Levy EB, Krishnasamy VP, Lewis AL. , et al. First human experience with directly image-able iodinated embolization microbeads. Cardiovasc Intervent Radiol 2016; 39 (08) 1177-1186
    CrossrefPubMedGoogle Scholar
  • 67 Brown KT, Do RK, Gonen M. , et al. Randomized trial of hepatic artery embolization for hepatocellular carcinoma using doxorubicin-eluting microspheres compared with embolization with microspheres alone. J Clin Oncol 2016; 34 (17) 2046-2053
    CrossrefPubMedGoogle Scholar
  • 68 Maluccio MA, Covey AM, Porat LB. , et al. Transcatheter arterial embolization with only particles for the treatment of unresectable hepatocellular carcinoma. J Vasc Interv Radiol 2008; 19 (06) 862-869
    CrossrefPubMedGoogle Scholar
  • 69 Bruix J, Llovet JM, Castells A. , et al. Transarterial embolization versus symptomatic treatment in patients with advanced hepatocellular carcinoma: results of a randomized, controlled trial in a single institution. Hepatology 1998; 27 (06) 1578-1583
    CrossrefPubMedGoogle Scholar
  • 70 Xie Z-B, Ma L, Wang X-B. , et al. Transarterial embolization with or without chemotherapy for advanced hepatocellular carcinoma: a systematic review. Tumour Biol 2014; 35 (09) 8451-8459
    CrossrefPubMedGoogle Scholar
  • 71 Malagari K, Pomoni M, Kelekis A. , et al. Prospective randomized comparison of chemoembolization with doxorubicin-eluting beads and bland embolization with BeadBlock for hepatocellular carcinoma. Cardiovasc Intervent Radiol 2010; 33 (03) 541-551
    CrossrefPubMedGoogle Scholar
  • 72 Atassi B, Bangash AK, Bahrani A. , et al. Multimodality imaging following 90Y radioembolization: a comprehensive review and pictorial essay. Radiographics 28 (01) 81-99 . doi:10.1148/rg.281065721
    PubMedGoogle Scholar
  • 73 Kennedy A, Nag S, Salem R. , et al. Recommendations for radioembolization of hepatic malignancies using yttrium-90 microsphere brachytherapy: a consensus panel report from the radioembolization brachytherapy oncology consortium. Int J Radiat Oncol Biol Phys 2007; 68 (01) 13-23 . doi:10.1016/j.ijrobp.2006.11.060
    CrossrefPubMedGoogle Scholar
  • 74 Riaz A, Lewandowski RJ, Kulik LM. , et al. Complications following radioembolization with yttrium-90 microspheres: a comprehensive literature review. J Vasc Interv Radiol 2009; 20 (09) 1121-30 ; quiz 1131. doi:10.1016/j.jvir.2009.05.030
    Google Scholar
  • 75 Lewandowski RJ, Kulik LM, Riaz A. , et al. A comparative analysis of transarterial downstaging for hepatocellular carcinoma: chemoembolization versus radioembolization. Am J Transplant 2009; 9 (08) 1920-1928 . doi:10.1111/j.1600-6143.2009.02695.x
    CrossrefPubMedGoogle Scholar
  • 76 Salem R, Gordon AC, Mouli S. , et al. Y90 Radioembolization significantly prolongs time to progression compared with chemoembolization in patients with hepatocellular carcinoma. Gastroenterology 2016; 151 (06) 1155-1163.e2 . doi:10.1053/j.gastro.2016.08.029
    CrossrefPubMedGoogle Scholar
  • 77 Pan L-H, Zhao C, Ma Y-L. Is Y90 radioembolization superior or comparable to transarterial chemoembolization for treating hepatocellular carcinoma?. Gastroenterology 2017; 152 (06) 1627-1628 . doi:10.1053/j.gastro.2016.10.048
    CrossrefPubMedGoogle Scholar
  • 78 Duran R, Deltenre P, Denys A. RE: Y90 radioembolization significantly prolongs time to progression compared with chemoembolization in patients with hepatocellular carcinoma. Gastroenterology 2017; 152 (06) 1625-1626 . doi:10.1053/j.gastro.2016.09.069
    CrossrefPubMedGoogle Scholar
  • 79 Ludwig JM, Zhang D, Xing M, Kim HS. Meta-analysis: adjusted indirect comparison of drug-eluting bead transarterial chemoembolization versus 90Y-radioembolization for hepatocellular carcinoma. Eur Radiol 2017; 27 (05) 2031-2041 . doi:10.1007/s00330-016-4548-3
    CrossrefPubMedGoogle Scholar
  • 80 Kudo M, Imanaka K, Chida N. , et al. Phase III study of sorafenib after transarterial chemoembolisation in Japanese and Korean patients with unresectable hepatocellular carcinoma. Eur J Cancer 2011; 47 (14) 2117-2127
    CrossrefPubMedGoogle Scholar
  • 81 Pawlik TM, Reyes DK, Cosgrove D, Kamel IR, Bhagat N, Geschwind J-FH. Phase II trial of sorafenib combined with concurrent transarterial chemoembolization with drug-eluting beads for hepatocellular carcinoma. J Clin Oncol 2011; 29 (30) 3960-3967
    CrossrefPubMedGoogle Scholar
  • 82 Lencioni R, Llovet JM, Han G. , et al. Sorafenib or placebo plus TACE with doxorubicin-eluting beads for intermediate stage HCC: the SPACE trial. J Hepatol 2016; 64 (05) 1090-1098
    CrossrefPubMedGoogle Scholar
  • 83 Geschwind J-F, Kudo M, Marrero JA. , et al. TACE treatment in patients with sorafenib-treated unresectable hepatocellular carcinoma in clinical practice: final analysis of GIDEON. Radiology 2016; 279 (02) 630-640
    CrossrefPubMedGoogle Scholar
  • 84 Lewandowski RJ, Andreoli JM, Hickey R. , et al. Angiogenic response following radioembolization: results from a randomized pilot study of Yttrium-90 with or without sorafenib. J Vasc Interv Radiol 2016; 27 (09) 1329-1336 . doi:10.1016/j.jvir.2016.03.043
    CrossrefPubMedGoogle Scholar
  • 85 Ricke J, Bulla K, Kolligs F. , et al. Safety and toxicity of radioembolization plus sorafenib in advanced hepatocellular carcinoma: analysis of the European multicentre trial SORAMIC. Liver Int 2015; 35 (02) 620-626 . doi:10.1111/liv.12622
    CrossrefPubMedGoogle Scholar
  • 86 Chow PKH, Poon DYH, Khin M-W. , et al. Multicenter phase II study of sequential radioembolization-sorafenib therapy for inoperable hepatocellular carcinoma. PLoS One 2014; 9 (03) e90909 . doi:10.1371/journal.pone.0090909
    CrossrefPubMedGoogle Scholar
  • 87 Vouche M, Kulik L, Atassi R. , et al. Radiological-pathological analysis of WHO, RECIST, EASL, mRECIST and DWI: imaging analysis from a prospective randomized trial of Y90 ± sorafenib. Hepatology 2013; 58 (05) 1655-1666 . doi:10.1002/hep.26487
    CrossrefPubMedGoogle Scholar
  • 88 Liu Z, Gao F, Yang G. , et al. Combination of radiofrequency ablation with transarterial chemoembolization for hepatocellular carcinoma: an up-to-date meta-analysis. Tumour Biol 2014; 35 (08) 7407-7413
    CrossrefPubMedGoogle Scholar
  • 89 Lencioni R. Management of hepatocellular carcinoma with transarterial chemoembolization in the era of systemic targeted therapy. Crit Rev Oncol Hematol 2012; 83 (02) 216-224
    CrossrefPubMedGoogle Scholar
  • 90 Nishiofuku H, Tanaka T, Matsuoka M. , et al. Transcatheter arterial chemoembolization using cisplatin powder mixed with degradable starch microspheres for colorectal liver metastases after FOLFOX failure: results of a phase I/II study. J Vasc Interv Radiol 2013; 24 (01) 56-65
    CrossrefPubMedGoogle Scholar
  • 91 Pieper CC, Meyer C, Vollmar B, Hauenstein K, Schild HH, Wilhelm KE. Temporary arterial embolization of liver parenchyma with degradable starch microspheres (EmboCept®S) in a swine model. Cardiovasc Intervent Radiol 2015; 38 (02) 435-441
    CrossrefPubMedGoogle Scholar
  • 92 Orlacchio A, Chegai F, Merolla S. , et al. Downstaging disease in patients with hepatocellular carcinoma outside up-to-seven criteria: strategies using degradable starch microspheres transcatheter arterial chemo-embolization. World J Hepatol 2015; 7 (12) 1694-1700
    CrossrefPubMedGoogle Scholar
  • 93 Dreher MR, Sharma KV, Woods DL. , et al. Radiopaque drug-eluting beads for transcatheter embolotherapy: experimental study of drug penetration and coverage in swine. J Vasc Interv Radiol 2012; 23 (02) 257-64.e4
    CrossrefPubMedGoogle Scholar
  • 94 Bonomo G, Pedicini V, Monfardini L. , et al. Bland embolization in patients with unresectable hepatocellular carcinoma using precise, tightly size-calibrated, anti-inflammatory microparticles: first clinical experience and one-year follow-up. Cardiovasc Intervent Radiol 2010; 33 (03) 552-559
    CrossrefPubMedGoogle Scholar
  • 95 Gonzalez-Guindalini FD, Botelho MP, Harmath CB. , et al. Assessment of liver tumor response to therapy: role of quantitative imaging. Radiographics 2013; 33 (06) 1781-1800
    CrossrefPubMedGoogle Scholar
  • 96 Lencioni R, Llovet JM. Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis 2010; 30 (01) 52-60
    Article in Thieme ConnectPubMedGoogle Scholar
  • 97 Forner A, Ayuso C, Varela M. , et al. Evaluation of tumor response after locoregional therapies in hepatocellular carcinoma: are response evaluation criteria in solid tumors reliable?. Cancer 2009; 115 (03) 616-623
    CrossrefPubMedGoogle Scholar
  • 98 Lin M, Pellerin O, Bhagat N. , et al. Quantitative and volumetric European Association for the Study of the Liver and Response Evaluation Criteria in Solid Tumors measurements: feasibility of a semiautomated software method to assess tumor response after transcatheter arterial chemoembolization. J Vasc Interv Radiol 2012; 23 (12) 1629-1637
    CrossrefPubMedGoogle Scholar
  • 99 Chapiro J, Wood LD, Lin M. , et al. Radiologic-pathologic analysis of contrast-enhanced and diffusion-weighted MR imaging in patients with HCC after TACE: diagnostic accuracy of 3D quantitative image analysis. Radiology 2014; 273 (03) 746-758
    CrossrefPubMedGoogle Scholar
  • 100 Ganapathy-Kanniappan S, Vali M, Kunjithapatham R. , et al. 3-bromopyruvate: a new targeted antiglycolytic agent and a promise for cancer therapy. Curr Pharm Biotechnol 2010; 11 (05) 510-517
    CrossrefPubMedGoogle Scholar
  • 101 Miyayama S, Yamashiro M, Hashimoto M. , et al. Identification of small hepatocellular carcinoma and tumor-feeding branches with cone-beam CT guidance technology during transcatheter arterial chemoembolization. J Vasc Interv Radiol 2013; 24 (04) 501-508
    CrossrefPubMedGoogle Scholar