Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Transarterial approaches to primary and secondary hepatic malignancies

Nature Reviews Clinical Oncology volume 12, pages 481–489 (2015)Cite this article

Subjects

Key Points

  • Patients with primary and secondary malignancy of the liver are often poor candidates for curative interventions

  • Transarterial locoregional therapies offer a minimally-invasive treatment pathway with promising clinical results and an acceptable adverse-event profile

  • Varying degrees of evidence are available for intra-arterial chemoinfusion, transarterial chemoembolization with and without drug-eluting beads, and radioembolization in the context of cancer within the liver

  • In the appropriate setting, unique survival, safety, and quality-of-life benefits might be provided by transarterial therapies

Abstract

Transarterial therapies in the setting of primary and secondary liver malignancies are becoming an essential part of the oncology landscape. Most patients with hepatic malignancies are not candidates for curative surgical intervention, thereby warranting exploration of alternative means of treatment that preserves quality of life while providing clinical benefit. Herein, the data for intra-arterial chemoinfusion, transarterial chemoembolization, drug-eluting beads, and radioembolization are discussed in the setting of malignancies within the liver; outcome data relating to survival, time-to-progression, time-to-recurrence, and adverse events are presented. Further data regarding different treatment paradigms for hepatocellular carcinoma, metastatic colorectal carcinoma, neuroendocrine tumours, and intrahepatic cholangiocarcinoma are also provided. In light of these and forthcoming data, transarterial therapies seem to offer a viable treatment pathway for select populations of patients.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Key transarterial locoregional therapies that are used for primary and secondary hepatic cancers.

Similar content being viewed by others

References

  1. Jemal, A. et al. Global cancer statistics. CA Cancer J. Clin. 61, 69–90 (2011).

    Article  PubMed  Google Scholar 

  2. Gomaa, A. I., Khan, S. A., Toledano, M. B., Waked, I. & Taylor-Robinson, S. D. Hepatocellular carcinoma: epidemiology, risk factors and pathogenesis. World J. Gastroenterol. 14, 4300–4308 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Siegel, R., Naishadham, D. & Jemal, A. Cancer statistics, 2013. CA Cancer J. Clin. 63, 11–30 (2013).

    Article  PubMed  Google Scholar 

  4. European Association for Study of Liver & European Organisation for Research and Treatment of Cancer. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. Eur. J. Cancer 48, 599–641 (2012).

  5. Bruix, J. & Sherman, M. American Association for the Study of Liver Diseases. Management of hepatocellular carcinoma: an update. Hepatology 53, 1020–1022 (2011).

    Article  PubMed  Google Scholar 

  6. Geschwind, J. F. et al. Yttrium-90 microspheres for the treatment of hepatocellular carcinoma. Gastroenterology 127 (Suppl. 1), S194–S205 (2004).

    Article  CAS  PubMed  Google Scholar 

  7. Llovet, J. M., Fuster, J. & Bruix, J. Intention-to-treat analysis of surgical treatment for early hepatocellular carcinoma: resection versus transplantation. Hepatology 30, 1434–1440 (1999).

    Article  CAS  PubMed  Google Scholar 

  8. Gluer, A. M. et al. Systematic review of actual 10-year survival following resection for hepatocellular carcinoma. HPB (Oxford) 14, 285–290 (2012).

    Article  Google Scholar 

  9. Salem, R. et al. Increased quality of life among hepatocellular carcinoma patients treated with radioembolization, compared with chemoembolization. Clin. Gastroenterol. Hepatol. 11, 1358–1365 (2013).

    Article  PubMed  Google Scholar 

  10. Hickey, R. et al. Cancer concepts and principles: primer for the interventional oncologist-part II. J. Vasc. Interv. Radiol. 24, 1167–1188 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Chapiro, J., Tacher, V. & Geschwind, J. F. Intraarterial therapies for primary liver cancer: state of the art. Expert Rev. Anticancer Ther. 13, 1157–1167 (2013).

    Article  CAS  PubMed  Google Scholar 

  12. Bierman, H. R., Byron, R. L. Jr, Kelley, K. H. & Grady, A. Studies on the blood supply of tumors in man. III. Vascular patterns of the liver by hepatic arteriography in vivo. J. Natl Cancer Inst. 12, 107–131 (1951).

    CAS  PubMed  Google Scholar 

  13. Gyves, J. W. et al. Definition of hepatic tumor microcirculation by single photon emission computerized tomography (SPECT). J. Nucl. Med. 25, 972–977 (1984).

    CAS  PubMed  Google Scholar 

  14. Lewandowski, R. J., Geschwind, J. F., Liapi, E. & Salem, R. Transcatheter intraarterial therapies: rationale and overview. Radiology 259, 641–657 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Hildebrandt, B. et al. Interventionally implanted port catheter systems for hepatic arterial infusion of chemotherapy in patients with colorectal liver metastases: a phase II-study and historical comparison with the surgical approach. BMC Cancer 7, 69 (2007).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Arai, Y. et al. Management of patients with unresectable liver metastases from colorectal and gastric cancer employing an implantable port system. Cancer Chemother. Pharm. 31 (Suppl.), S99–S102 (1992).

    Article  Google Scholar 

  17. Sakamoto, N. et al. Ultrasound-guided radiological placement of central venous port via the subclavian vein: a retrospective analysis of 500 cases at a single institute. Cardiovasc. Intervent. Radiol. 33, 989–994 (2010).

    Article  PubMed  Google Scholar 

  18. Collins, J. M. Pharmacologic rationale for regional drug delivery. J. Clin. Oncol. 2, 498–504 (1984).

    Article  CAS  PubMed  Google Scholar 

  19. Ensminger, W. D. Intrahepatic arterial infusion of chemotherapy: pharmacologic principles. Semin. Oncol. 29, 119–125 (2002).

    Article  CAS  PubMed  Google Scholar 

  20. Hickey, R. et al. Cancer concepts and principles: primer for the interventional oncologist—part I. J. Vasc. Interv. Radiol. 24, 1157–1164 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Ensminger, W. D. et al. A clinical–pharmacological evaluation of hepatic arterial infusions of 5-fluoro-2′-deoxyuridine and 5-fluorouracil. Cancer Res. 38, 3784–3792 (1978).

    CAS  PubMed  Google Scholar 

  22. Park, J. G. et al. Enhancement of fluorinated pyrimidine-induced cytotoxicity by leucovorin in human colorectal carcinoma cell lines. J. Natl Cancer Inst. 80, 1560–1564 (1988).

    Article  CAS  PubMed  Google Scholar 

  23. Hohn, D. C. et al. A randomized trial of continuous intravenous versus hepatic intraarterial floxuridine in patients with colorectal cancer metastatic to the liver: the Northern California Oncology Group trial. J. Clin. Oncol. 7, 1646–1654 (1989).

    Article  CAS  PubMed  Google Scholar 

  24. Chang, A. E. et al. A prospective randomized trial of regional versus systemic continuous 5-fluorodeoxyuridine chemotherapy in the treatment of colorectal liver metastases. Ann. Surg. 206, 685–693 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Kerr, D. J. et al. Intrahepatic arterial versus intravenous fluorouracil and folinic acid for colorectal cancer liver metastases: a multicentre randomised trial. Lancet 361, 368–373 (2003).

    Article  CAS  PubMed  Google Scholar 

  26. Lorenz, M. & Muller, H. H. Randomized, multicenter trial of fluorouracil plus leucovorin administered either via hepatic arterial or intravenous infusion versus fluorodeoxyuridine administered via hepatic arterial infusion in patients with nonresectable liver metastases from colorectal carcinoma. J. Clin. Oncol. 18, 243–254 (2000).

    Article  CAS  PubMed  Google Scholar 

  27. Gupta, S. et al. Hepatic artery embolization and chemoembolization for treatment of patients with metastatic carcinoid tumors: the MD Anderson experience. Cancer J. 9, 261–267 (2003).

    Article  PubMed  Google Scholar 

  28. Clark, O. H. et al. Neuroendocrine tumors. J. Natl Compr. Canc. Netw. 4, 102–138 (2006).

    Article  CAS  PubMed  Google Scholar 

  29. Rhee, T. K. et al. 90Y Radioembolization for metastatic neuroendocrine liver tumors: preliminary results from a multi-institutional experience. Ann. Surg. 247, 1029–1035 (2008).

    Article  PubMed  Google Scholar 

  30. King, J. et al. Radioembolization with selective internal radiation microspheres for neuroendocrine liver metastases. Cancer 113, 921–929 (2008).

    Article  PubMed  Google Scholar 

  31. Covey, A. M. et al. Particle embolization of recurrent hepatocellular carcinoma after hepatectomy. Cancer 106, 2181–2189 (2006).

    Article  PubMed  Google Scholar 

  32. Nagino, M. et al. Right or left trisegment portal vein embolization before hepatic trisegmentectomy for hilar bile duct carcinoma. Surgery 117, 677–681 (1995).

    Article  CAS  PubMed  Google Scholar 

  33. Hwang, S. et al. Sequential preoperative ipsilateral hepatic vein embolization after portal vein embolization to induce further liver regeneration in patients with hepatobiliary malignancy. Ann. Surg. 249, 608–616 (2009).

    Article  PubMed  Google Scholar 

  34. Tanaka, H. et al. Preoperative portal vein embolization improves prognosis after right hepatectomy for hepatocellular carcinoma in patients with impaired hepatic function. Br. J. Surg. 87, 879–882 (2000).

    Article  CAS  PubMed  Google Scholar 

  35. Kruskal, J. B. et al. In vivo and in vitro analysis of the effectiveness of doxorubicin combined with temporary arterial occlusion in liver tumors. J. Vasc. Interv. Radiol. 4, 741–747 (1993).

    Article  CAS  PubMed  Google Scholar 

  36. Terayama, N. et al. Accumulation of iodized oil within the nonneoplastic liver adjacent to hepatocellular carcinoma via the drainage routes of the tumor after transcatheter arterial embolization. Cardiovasc. Intervent. Radiol. 24, 383–387 (2001).

    Article  CAS  PubMed  Google Scholar 

  37. Raoul, J. L. et al. Chemoembolization of hepatocellular carcinomas. A study of the biodistribution and pharmacokinetics of doxorubicin. Cancer 70, 585–590 (1992).

    Article  CAS  PubMed  Google Scholar 

  38. Nakamura, H., Hashimoto, T., Oi, H. & Sawada, S. Transcatheter oily chemoembolization of hepatocellular carcinoma. Radiology 170, 783–786 (1989).

    Article  CAS  PubMed  Google Scholar 

  39. Konno, T. et al. Effect of arterial administration of high-molecular-weight anticancer agent SMANCS with lipid lymphographic agent on hepatoma: a preliminary report. Eur. J. Cancer Clin. Oncol. 19, 1053–1065 (1983).

    Article  CAS  PubMed  Google Scholar 

  40. Nakamura, H. et al. Transcatheter embolization of hepatocellular carcinoma: assessment of efficacy in cases of resection following embolization. Radiology 147, 401–405 (1983).

    Article  CAS  PubMed  Google Scholar 

  41. Bhattacharya, S. et al. Human liver cancer cells and endothelial cells incorporate iodised oil. Br. J. Cancer 73, 877–881 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Bhattacharya, S., Novell, J. R., Winslet, M. C. & Hobbs, K. E. Iodized oil in the treatment of hepatocellular carcinoma. Br. J. Surg. 81, 1563–1571 (1994).

    Article  CAS  PubMed  Google Scholar 

  43. Marelli, L. et al. Transarterial therapy for hepatocellular carcinoma: which technique is more effective? A systematic review of cohort and randomized studies. Cardiovasc. Intervent. Radiol. 30, 6–25 (2007).

    Article  PubMed  Google Scholar 

  44. Coldwell, D. M., Stokes, K. R. & Yakes, W. F. Embolotherapy: agents, clinical applications, and techniques. Radiographics 14, 623–643 (1994).

    Article  CAS  PubMed  Google Scholar 

  45. Yamada, R. et al. Hepatic artery embolization in 120 patients with unresectable hepatoma. Radiology 148, 397–401 (1983).

    Article  CAS  PubMed  Google Scholar 

  46. Yamada, R. et al. Hepatic artery embolization in 32 patients with unresectable hepatoma. Osaka City Med. J. 26, 81–96 (1980).

    CAS  PubMed  Google Scholar 

  47. 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. 56, 908–943 (2012).

  48. Llovet, J. M. et al. Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial. Lancet 359, 1734–1739 (2002).

    Article  PubMed  Google Scholar 

  49. Lo, C. M. et al. Randomized controlled trial of transarterial lipiodol chemoembolization for unresectable hepatocellular carcinoma. Hepatology 35, 1164–1171 (2002).

    Article  CAS  PubMed  Google Scholar 

  50. Lammer, J. et al. Prospective randomized study of doxorubicin-eluting-bead embolization in the treatment of hepatocellular carcinoma: results of the PRECISION V study. Cardiovasc. Intervent. Radiol. 33, 41–52 (2010).

    Article  PubMed  Google Scholar 

  51. Hong, K. et al. New intra-arterial drug delivery system for the treatment of liver cancer: preclinical assessment in a rabbit model of liver cancer. Clin. Cancer Res. 12, 2563–2567 (2006).

    Article  CAS  PubMed  Google Scholar 

  52. Lewis, A. L. et al. DC bead: in vitro characterization of a drug-delivery device for transarterial chemoembolization. J. Vasc. Interv. Radiol. 17, 335–342 (2006).

    Article  PubMed  Google Scholar 

  53. Aliberti, C., Tilli, M., Benea, G. & Fiorentini, G. Trans-arterial chemoembolization (TACE) of liver metastases from colorectal cancer using irinotecan-eluting beads: preliminary results. Anticancer Res. 26, 3793–3795 (2006).

    CAS  PubMed  Google Scholar 

  54. Lee, K. H. et al. Doxorubicin-loaded QuadraSphere microspheres: plasma pharmacokinetics and intratumoral drug concentration in an animal model of liver cancer. Cardiovasc. Intervent. Radiol. 33, 576–582 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Varela, M. et al. Chemoembolization of hepatocellular carcinoma with drug eluting beads: efficacy and doxorubicin pharmacokinetics. J. Hepatol. 46, 474–481 (2007).

    Article  CAS  PubMed  Google Scholar 

  56. Poon, R. T. et al. A phase I/II trial of chemoembolization for hepatocellular carcinoma using a novel intra-arterial drug-eluting bead. Clin. Gastroenterol. Hepatol. 5, 1100–1108 (2007).

    Article  CAS  PubMed  Google Scholar 

  57. Song, M. J. et al. Comparative study between doxorubicin-eluting beads and conventional transarterial chemoembolization for treatment of hepatocellular carcinoma. J. Hepatol. 57, 1244–1250 (2012).

    Article  CAS  PubMed  Google Scholar 

  58. Sarfaraz, M. et al. Physical aspects of yttrium-90 microsphere therapy for nonresectable hepatic tumors. Med. Phys. 30, 199–203 (2003).

    Article  CAS  PubMed  Google Scholar 

  59. Salem, R., Thurston, K. G., Carr, B. I., Goin, J. E. & Geschwind, J. F. Yttrium-90 microspheres: radiation therapy for unresectable liver cancer. J. Vasc. Interv. Radiol. 13, S223–S229 (2002).

    Article  PubMed  Google Scholar 

  60. Dancey, J. E. et al. Treatment of nonresectable hepatocellular carcinoma with intrahepatic 90Y-microspheres. J. Nucl. Med. 41, 1673–1681 (2000).

    CAS  PubMed  Google Scholar 

  61. Andrews, J. C. et al. Hepatic radioembolization with yttrium-90 containing glass microspheres: preliminary results and clinical follow-up. J. Nucl. Med. 35, 1637–1644 (1994).

    CAS  PubMed  Google Scholar 

  62. Riaz, A. et al. Radiation segmentectomy: a novel approach to increase safety and efficacy of radioembolization. Int. J. Radiat. Oncol. Biol. Phys. 79, 163–171 (2011).

    Article  PubMed  Google Scholar 

  63. Kennedy, A. S., Nutting, C., Coldwell, D., Gaiser, J. & Drachenberg, C. Pathologic response and microdosimetry of 90Y microspheres in man: review of four explanted whole livers. Int. J. Radiat. Oncol. Biol. Phys. 60, 1552–1563 (2004).

    Article  CAS  PubMed  Google Scholar 

  64. Emami, B. et al. Tolerance of normal tissue to therapeutic irradiation. Int. J. Radiat. Oncol. Biol. Phys. 21, 109–122 (1991).

    Article  CAS  PubMed  Google Scholar 

  65. TheraSphere® Yttrium-90 microspheres package insert [online], (MDS Nordion, 2004).

  66. Van de Wiele, C. Radioembolization of hepatocellular carcinoma. Curr. Drug Discov. Technol. 7, 247–252 (2010).

    Article  CAS  PubMed  Google Scholar 

  67. Salem, R. & Thurston, K. G. Radioembolization with 90yttrium microspheres: a state-of-the-art brachytherapy treatment for primary and secondary liver malignancies. Part 2: special topics. J. Vasc. Interv. Radiol. 17, 1425–1439 (2006).

    Article  PubMed  Google Scholar 

  68. Hilgard, P. et al. Radioembolization with yttrium-90 glass microspheres in hepatocellular carcinoma: European experience on safety and long-term survival. Hepatology 52, 1741–1749 (2010).

    Article  CAS  PubMed  Google Scholar 

  69. Kulik, L. M. et al. Safety and efficacy of 90Y radiotherapy for hepatocellular carcinoma with and without portal vein thrombosis. Hepatology 47, 71–81 (2008).

    Article  PubMed  Google Scholar 

  70. Salem, R. et al. Radioembolization results in longer time-to-progression and reduced toxicity compared with chemoembolization in patients with hepatocellular carcinoma. Gastroenterology 140, 497–507 (2011).

    Article  PubMed  Google Scholar 

  71. Seidensticker, R. et al. Matched-pair comparison of radioembolization plus best supportive care versus best supportive care alone for chemotherapy refractory liver-dominant colorectal metastases. Cardiovasc. Intervent. Radiol. 35, 1066–1073 (2012).

    Article  PubMed  Google Scholar 

  72. Ibrahim, S. M. et al. Treatment of unresectable cholangiocarcinoma using yttrium-90 microspheres: results from a pilot study. Cancer 113, 2119–2128 (2008).

    Article  CAS  PubMed  Google Scholar 

  73. Saxena, A., Bester, L., Chua, T. C., Chu, F. C. & Morris, D. L. Yttrium-90 radiotherapy for unresectable intrahepatic cholangiocarcinoma: a preliminary assessment of this novel treatment option. Ann. Surg. Oncol. 17, 484–491 (2010).

    Article  PubMed  Google Scholar 

  74. Jiang, G., Xu, X., Ren, S. & Wang, L. Combining transarterial chemoembolization with radiofrequency ablation for hepatocellular carcinoma. Tumour Biol. 35, 3405–3408 (2014).

    Article  CAS  PubMed  Google Scholar 

  75. Hickey, R. et al. Chemoradiation of hepatic malignancies: prospective, phase 1 study of full-dose capecitabine with escalating doses of yttrium-90 radioembolization. Int. J. Radiat. Oncol. Biol. Phys. 88, 1025–1031 (2014).

    Article  PubMed  Google Scholar 

  76. Llovet, J. M. et al. Cost effectiveness of adjuvant therapy for hepatocellular carcinoma during the waiting list for liver transplantation. Gut 50, 123–128 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Kulik, L. et al. Prospective randomized pilot study of Y90 ± sorafenib as bridge to transplantation in hepatocellular carcinoma. J. Hepatol. 61, 309–317 (2014).

    Article  CAS  PubMed  Google Scholar 

  78. Okusaka, T. et al. Transarterial chemotherapy alone versus transarterial chemoembolization for hepatocellular carcinoma: a randomized phase III trial. J. Hepatol. 51, 1030–1036 (2009).

    Article  CAS  PubMed  Google Scholar 

  79. Llovet, J. M. et al. Design and endpoints of clinical trials in hepatocellular carcinoma. J. Natl Cancer Inst. 100, 698–711 (2008).

    Article  PubMed  Google Scholar 

  80. Lo C. M. et al. Randomized controlled trial of transarterial lipiodol chemoembolization for unresectable hepatocellular carcinoma. Hepatology 35, 1164–1171 (2002).

    Article  CAS  PubMed  Google Scholar 

  81. Takayasu, K. et al. Prospective cohort study of transarterial chemoembolization for unresectable hepatocellular carcinoma in 8510 patients. Gastroenterology 131, 461–469 (2006).

    Article  CAS  PubMed  Google Scholar 

  82. Bargellini, I. et al. Transarterial chemoembolization in very early and early-stage hepatocellular carcinoma patients excluded from curative treatment: a prospective cohort study. Eur. J. Radiol. 81, 1173–1178 (2012).

    Article  PubMed  Google Scholar 

  83. Miyayama, S. et al. Ultraselective transcatheter arterial chemoembolization with a 2-F tip microcatheter for small hepatocellular carcinomas: relationship between local tumor recurrence and visualization of the portal vein with iodized oil. J. Vasc. Interv. Radiol. 18, 365–376 (2007).

    Article  PubMed  Google Scholar 

  84. Yang, H. J. et al. Small single-nodule hepatocellular carcinoma: comparison of transarterial chemoembolization, radiofrequency ablation, and hepatic resection by using inverse probability weighting. Radiology 271, 909–918 (2014).

    Article  PubMed  Google Scholar 

  85. Salem, R. et al. Treatment of unresectable hepatocellular carcinoma with use of 90Y microspheres (TheraSphere): safety, tumor response, and survival. J. Vasc. Interv. Radiol. 16, 1627–1639 (2005).

    Article  PubMed  Google Scholar 

  86. Kulik, L. M. et al. Yttrium-90 microspheres (TheraSphere) treatment of unresectable hepatocellular carcinoma: downstaging to resection, RFA and bridge to transplantation. J. Surg. Oncol. 94, 572–586 (2006).

    Article  CAS  PubMed  Google Scholar 

  87. Vouche, M. et al. Unresectable solitary HCC not amenable to RFA: multicenter radiology–pathology correlation and survival of radiation segmentectomy. Hepatology 60, 192–201 (2014).

    Article  PubMed  Google Scholar 

  88. Georgiades, C. S., Hong, K., D'Angelo, M. & Geschwind, J. F. Safety and efficacy of transarterial chemoembolization in patients with unresectable hepatocellular carcinoma and portal vein thrombosis. J. Vasc. Interv. Radiol. 16, 1653–1659 (2005).

    Article  PubMed  Google Scholar 

  89. Tazawa, J. et al. Radiation therapy in combination with transcatheter arterial chemoembolization for hepatocellular carcinoma with extensive portal vein involvement. J. Gastroenterol. Hepatol. 16, 660–665 (2001).

    Article  CAS  PubMed  Google Scholar 

  90. Fan, J. et al. Multimodality treatment in hepatocellular carcinoma patients with tumor thrombi in portal vein. World J. Gastroenterol. 7, 28–32 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Sato, K. et al. Treatment of unresectable primary and metastatic liver cancer with yttrium-90 microspheres (TheraSphere): assessment of hepatic arterial embolization. Cardiovasc. Intervent. Radiol. 29, 522–529 (2006).

    Article  PubMed  Google Scholar 

  92. Salem, R. et al. Radioembolization for hepatocellular carcinoma using Yttrium-90 microspheres: a comprehensive report of long-term outcomes. Gastroenterology 138, 52–64 (2010).

    Article  CAS  PubMed  Google Scholar 

  93. US National Library of Medicine. ClinicalTrials.gov [online], (2014).

  94. Siegel, R., Desantis, C. & Jemal, A. Colorectal cancer statistics, 2014. CA Cancer. J. Clin. 64, 104–117 (2014).

    Article  PubMed  Google Scholar 

  95. Nelson, H. et al. Guidelines 2000 for colon and rectal cancer surgery. J. Natl Cancer Inst. 93, 583–596 (2001).

    Article  CAS  PubMed  Google Scholar 

  96. Kemeny, N. et al. Intrahepatic or systemic infusion of fluorodeoxyuridine in patients with liver metastases from colorectal carcinoma. A randomized trial. Ann. Intern. Med. 107, 459–465 (1987).

    Article  CAS  PubMed  Google Scholar 

  97. Martin, J. K. Jr et al. Intra-arterial floxuridine vs systemic fluorouracil for hepatic metastases from colorectal cancer. A randomized trial. Arch. Surg. 125, 1022–1027 (1990).

    Article  PubMed  Google Scholar 

  98. Wagman, L. D. et al. A prospective, randomized evaluation of the treatment of colorectal cancer metastatic to the liver. J. Clin. Oncol. 8, 1885–1893 (1990).

    Article  CAS  PubMed  Google Scholar 

  99. Rougier, P. et al. Hepatic arterial infusion of floxuridine in patients with liver metastases from colorectal carcinoma: long-term results of a prospective randomized trial. J. Clin. Oncol. 10, 1112–1118 (1992).

    Article  CAS  PubMed  Google Scholar 

  100. Allen-Mersh, T. G., Earlam, S., Fordy, C., Abrams, K. & Houghton, J. Quality of life and survival with continuous hepatic-artery floxuridine infusion for colorectal liver metastases. Lancet 344, 1255–1260 (1994).

    Article  CAS  PubMed  Google Scholar 

  101. Kemeny, N. E. et al. Hepatic arterial infusion versus systemic therapy for hepatic metastases from colorectal cancer: a randomized trial of efficacy, quality of life, and molecular markers (CALGB 9481). J. Clin. Oncol. 24, 1395–1403 (2006).

    Article  CAS  PubMed  Google Scholar 

  102. Tellez, C. et al. Phase II trial of chemoembolization for the treatment of metastatic colorectal carcinoma to the liver and review of the literature. Cancer 82, 1250–1259 (1998).

    Article  CAS  PubMed  Google Scholar 

  103. Patel, A. et al. Single-center experience with elective transcatheter coil embolization of splenic artery aneurysms: technique and midterm follow-up. J. Vasc. Interv. Radiol. 23, 893–899 (2012).

    Article  PubMed  Google Scholar 

  104. Vogl, T. J. et al. Repeated transarterial chemoembolization in the treatment of liver metastases of colorectal cancer: prospective study. Radiology 250, 281–289 (2009).

    Article  PubMed  Google Scholar 

  105. Lewandowski, R. J. et al. Twelve-year experience of radioembolization for colorectal hepatic metastases in 214 patients: survival by era and chemotherapy. Eur. J. Nucl. Med. Mol. Imaging 41, 1861–1869 (2014).

    Article  CAS  PubMed  Google Scholar 

  106. Fiorentini, G. Trans-arterial chemoembolization of liver metastases from colorectal carcinoma adopting drug eluting-beads loaded with irinotecan compared to FOLFIRI: results at two years of a phase III clinical trial. Presented at The World Conference on Interventional Oncology 2011 (WCIO 2011).

  107. Martin, R. C. et al. Hepatic intra-arterial injection of drug-eluting bead, irinotecan (DEBIRI) in unresectable colorectal liver metastases refractory to systemic chemotherapy: results of multi-institutional study. Ann. Surg. Oncol. 18, 192–198 (2011).

    Article  PubMed  Google Scholar 

  108. Van Hazel, G. et al. Randomised phase 2 trial of SIR-Spheres plus fluorouracil/leucovorin chemotherapy versus fluorouracil/leucovorin chemotherapy alone in advanced colorectal cancer. J. Surg. Oncol. 88, 78–85 (2004).

    Article  CAS  PubMed  Google Scholar 

  109. Gray, B. et al. Randomised trial of SIR-Spheres plus chemotherapy vs. chemotherapy alone for treating patients with liver metastases from primary large bowel cancer. Ann. Oncol. 12, 1711–1720 (2001).

    Article  CAS  PubMed  Google Scholar 

  110. Hendlisz, A. et al. Phase III trial comparing protracted intravenous fluorouracil infusion alone or with yttrium-90 resin microspheres radioembolization for liver-limited metastatic colorectal cancer refractory to standard chemotherapy. J. Clin. Oncol. 28, 3687–3694 (2010).

    Article  CAS  PubMed  Google Scholar 

  111. Mayo, S. C. et al. Surgical management of hepatic neuroendocrine tumor metastasis: results from an international multi-institutional analysis. Ann. Surg. Oncol. 17, 3129–3136 (2010).

    Article  PubMed  Google Scholar 

  112. Gupta, S. et al. Hepatic arterial embolization and chemoembolization for the treatment of patients with metastatic neuroendocrine tumors: variables affecting response rates and survival. Cancer 104, 1590–1602 (2005).

    Article  PubMed  Google Scholar 

  113. Roche, A. et al. Trans-catheter arterial chemoembolization as first-line treatment for hepatic metastases from endocrine tumors. Eur. Radiol. 13, 136–140 (2003).

    PubMed  Google Scholar 

  114. Memon, K. et al. Radioembolization for neuroendocrine liver metastases: safety, imaging, and long-term outcomes. Int. J. Radiat. Oncol. Biol. Phys. 83, 887–894 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Edge, S. B. & Compton, C. C. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann. Surg. Oncol. 17, 1471–1474 (2010).

    Article  PubMed  Google Scholar 

  116. El-Serag, H. B. et al. Risk of hepatobiliary and pancreatic cancers after hepatitis C virus infection: a population-based study of U.S. veterans. Hepatology 49, 116–123 (2009).

    Article  PubMed  Google Scholar 

  117. Solorzano, C. C. et al. Nonfunctioning islet cell carcinoma of the pancreas: survival results in a contemporary series of 163 patients. Surgery 130, 1078–1085 (2001).

    Article  CAS  PubMed  Google Scholar 

  118. Kiefer, M. V. et al. Chemoembolization of intrahepatic cholangiocarcinoma with cisplatinum, doxorubicin, mitomycin C, ethiodol, and polyvinyl alcohol: a 2-center study. Cancer 117, 1498–1505 (2010).

    Article  PubMed  CAS  Google Scholar 

  119. Kim, J. H. et al. Transcatheter arterial chemoembolization or chemoinfusion for unresectable intrahepatic cholangiocarcinoma: clinical efficacy and factors influencing outcomes. Cancer 113, 1614–1622 (2008).

    Article  PubMed  Google Scholar 

  120. Hyder, O. et al. Intra-arterial therapy for advanced intrahepatic cholangiocarcinoma: a multi-institutional analysis. Ann. Surg. Oncol. 20, 3779–3786 (2013).

    Article  PubMed  Google Scholar 

  121. Mouli, S. et al. Yttrium-90 radioembolization for intrahepatic cholangiocarcinoma: safety, response, and survival analysis. J. Vasc. Interv. Radiol. 24, 1227–1234 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Radiology, Section of Interventional Radiology and Division of Interventional Oncology, Northwestern University, 676 North St Clair, Suite 800, Chicago, 60611, IL, USA

    Ali Habib, Kush Desai, Ryan Hickey, Bartley Thornburg, Robert Lewandowski & Riad Salem

Authors
  1. Ali Habib
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kush Desai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ryan Hickey
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bartley Thornburg
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robert Lewandowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Riad Salem
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A.H., K.D., R.H., B.T., and R.L. made substantial contributions to researching data for the article. All authors contributed substantially to writing and review/editing of the manuscript before submission. A.H., R.L., and R.S. contributed to discussion of content and approval of the final manuscript.

Corresponding author

Correspondence to Riad Salem.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Habib, A., Desai, K., Hickey, R. et al. Transarterial approaches to primary and secondary hepatic malignancies. Nat Rev Clin Oncol 12, 481–489 (2015). https://doi.org/10.1038/nrclinonc.2015.78

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrclinonc.2015.78

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing