Abstract
The management of patients with well-differentiated neuroendocrine tumors (NET) and non-resectable liver metastases is challenging. Liver-directed transarterial embolization (TAE), transarterial chemo-embolization (TACE) and selective internal radiation therapy (SIRT) have a place of choice among other treatment modalities. However, their utilization relies on a low level of proof, due to the lack of prospective data, the absence of comparative studies and considerable heterogeneity between local practices. TAE and TACE generally achieve average symptomatic, biological and radiological responses of 75%, 56% and 50%, with progression-free survival of 12–18 months, with acceptable tolerance. Although not clearly demonstrated, TACE may be more effective than TAE in pancreatic NET, but not in small-intestine NET. SIRT has been developed more recently and may achieve similar results, with improved tolerance, but decreased cost-effectiveness, although no prospective comparison has been published to date. There is currently no strong argument to choose between TAE, TACE and SIRT, and they have not been compared to other treatment modalities. The evaluation of their efficacy has mostly relied on criteria based on size variations, which do not take into account tumor viability and metabolism, and thus may not be relevant. These techniques may be especially effective when performed as first-line therapies, in patients with non-major liver involvement (<75%) and with hypervascular metastases. Finally, studies exploring their combination with systemic therapies are ongoing.
Similar content being viewed by others
Abbreviations
- NELM:
-
Neuroendocrine liver metastasi(e)s
- NET:
-
Neuroendocrine tumor(s)
- OS:
-
Overall survival
- PFS:
-
Progression-free survival
- TACE:
-
Transarterial chemo-embolization
- TAE:
-
Transarterial embolization
- SIRT:
-
Selective internal radiation therapy
References
Frilling A, Modlin IM, Kidd M, Russell C, Breitenstein S, Salem R, et al. Recommendations for management of patients with neuroendocrine liver metastases. Lancet Oncol. 2014;15:e8–21.
Pavel M, O’Toole D, Costa F, Capdevila J, Gross D, Kianmanesh R, et al. ENETS consensus guidelines update for the management of distant metastatic disease of intestinal, pancreatic, bronchial neuroendocrine neoplasms (NEN) and NEN of unknown primary site. Neuroendocrinology. 2016;103:172–85.
Elias D, Lasser P, Ducreux M, Duvillard P, Ouellet J-F, Dromain C, et al. Liver resection (and associated extrahepatic resections) for metastatic well-differentiated endocrine tumors: a 15-year single center prospective study. Surgery. 2003;133:375–82.
Elias D, Lefevre JH, Duvillard P, Goéré D, Dromain C, Dumont F, et al. Hepatic metastases from neuroendocrine tumors with a “thin slice” pathological examination: they are many more than you think. Ann Surg. 2010;251:307–10.
Zappa M, Abdel-Rehim M, Hentic O, Vullierme M-P, Ruszniewski P, Vilgrain V. Liver-directed therapies in liver metastases from neuroendocrine tumors of the gastrointestinal tract. Target Oncol. 2012;7:107–16.
Kennedy A, Bester L, Salem R, Sharma RA, Parks RW, Ruszniewski P. Role of hepatic intra-arterial therapies in metastatic neuroendocrine tumours (NET): guidelines from the NET-Liver-Metastases Consensus Conference. HPB. 2015;17:29–37.
Orgera G, Krokidis M, Cappucci M, Gourtsoyianni S, Tipaldi MA, Hatzidakis A, et al. current status of interventional radiology in the management of gastro-entero-pancreatic neuroendocrine tumours (GEP-NETs). Cardiovasc Intervent Radiol. 2015;38:13–24.
de Mestier L, Dromain C, d’Assignies G, Scoazec J-Y, Lassau N, Lebtahi R, et al. Evaluating digestive neuroendocrine tumor progression and therapeutic responses in the era of targeted therapies: state of the art. Endocr Relat Cancer. 2014;21:R105–20.
de Baere T, Deschamps F, Tselikas L, Ducreux M, Planchard D, Pearson E, et al. GEP-NETS UPDATE: Interventional radiology: role in the treatment of liver metastases from GEP-NETs. Eur J Endocrinol. 2015;172:R151–66.
Del Prete M, Fiore F, Modica R, Marotta V, Marciello F, Ramundo V, et al. Hepatic arterial embolization in patients with neuroendocrine tumors. J Exp Clin Cancer Res. 2014;33:43.
Steward MJ, Warbey VS, Malhotra A, Caplin ME, Buscombe JR, Yu D. Neuroendocrine tumors: role of interventional radiology in therapy. Radiographics. 2008;28:1131–45.
Kim DY, Ryu HJ, Choi JY, Park JY, Lee DY, Kim BK, et al. Radiological response predicts survival following transarterial chemoembolisation in patients with unresectable hepatocellular carcinoma. Aliment Pharmacol Ther. 2012;35:1343–50.
Carrasco CH, Charnsangavej C, Ajani J, Samaan NA, Richli W, Wallace S. The carcinoid syndrome: palliation by hepatic artery embolization. Am J Roentgenol. 1986;147:149–54.
Therasse E, Breittmayer F, Roche A, De Baere T, Indushekar S, Ducreux M, et al. Transcatheter chemoembolization of progressive carcinoid liver metastasis. Radiology. 1993;189:541–7.
Granberg D, Eriksson L-G, Welin S, Kindmark H, Janson ET, Skogseid B, et al. Liver embolization with trisacryl gelatin microspheres (embosphere) in patients with neuroendocrine tumors. Acta Radiol. 2007;48:180–5.
Gupta S. Intra-arterial liver-directed therapies for neuroendocrine hepatic metastases. Semin Interv Radiol. 2013;30:028–38.
Christante D, Pommier S, Givi B, Pommier R. Hepatic artery chemoinfusion with chemoembolization for neuroendocrine cancer with progressive hepatic metastases despite octreotide therapy. Surgery. 2008;144:885–94.
Dong XD, Carr BI. Hepatic artery chemoembolization for the treatment of liver metastases from neuroendocrine tumors: a long-term follow-up in 123 patients. Med Oncol. 2011;28:286–90.
Swärd C, Johanson V, Nieveen van Dijkum E, Jansson S, Nilsson O, Wängberg B, et al. Prolonged survival after hepatic artery embolization in patients with midgut carcinoid syndrome. Br J Surg. 2009;96:517–21.
Dhir M, Shrestha R, Steel JL, Marsh JW, Tsung A, Tublin ME, et al. Initial treatment of unresectable neuroendocrine tumor liver metastases with transarterial chemoembolization using streptozotocin: a 20-year experience. Ann Surg Oncol. 2017;24:450–9.
Hur S, Chung JW, Kim H-C, D-Y O, Lee S-H, Bang Y-J, et al. Survival outcomes and prognostic factors of transcatheter arterial chemoembolization for hepatic neuroendocrine metastases. J Vasc Interv Radiol. 2013;24:947–56.
Eriksson BK, Larsson EG, Skogseid BM, Löfberg AM, Lörelius LE, Oberg KE. Liver embolizations of patients with malignant neuroendocrine gastrointestinal tumors. Cancer. 1998;83:2293–301.
Kim YH, Ajani JA, Carrasco CH, Dumas P, Richli W, Lawrence D, et al. Selective hepatic arterial chemoembolization for liver metastases in patients with carcinoid tumor or islet cell carcinoma. Cancer Investig. 1999;17:474–8.
Varker KA, Martin EW, Klemanski D, Palmer B, Shah MH, Bloomston M. Repeat transarterial chemoembolization (TACE) for progressive hepatic carcinoid metastases provides results similar to first TACE. J Gastrointest Surg. 2007;11:1680–5.
Guiu B, Deschamps F, Aho S, Munck F, Dromain C, Boige V, et al. Liver/biliary injuries following chemoembolisation of endocrine tumours and hepatocellular carcinoma: lipiodol vs. drug-eluting beads. J Hepatol. 2012;56:609–17.
Lewis MA, Jaramillo S, Roberts L, Fleming CJ, Rubin J, Grothey A. Hepatic artery embolization for neuroendocrine tumors: postprocedural management and complications. Oncologist. 2012;17:725–31.
Hoffmann RT, Paprottka P, Jakobs TF, Trumm CG, Reiser MF. Arterial therapies of non-colorectal cancer metastases to the liver (from chemoembolization to radioembolization). Abdom Imaging. 2011;36:671–6.
Chen JX, Rose S, White SB, El-Haddad G, Fidelman N, Yarmohammadi H, et al. Embolotherapy for neuroendocrine tumor liver metastases: prognostic factors for hepatic progression-free survival and overall survival. Cardiovasc Intervent Radiol. 2017;40:69–80.
Joskin J, de Baere T, Auperin A, Tselikas L, Guiu B, Farouil G, et al. Predisposing factors of liver necrosis after transcatheter arterial chemoembolization in liver metastases from neuroendocrine tumor. Cardiovasc Intervent Radiol. 2015;38:372–80.
Kitano M, Davidson GW, Shirley LA, Schmidt CR, Guy GE, Khabiri H, et al. Transarterial chemoembolization for metastatic neuroendocrine tumors with massive hepatic tumor burden: is the benefit worth the risk? Ann Surg Oncol. 2016;23:4008–15.
Bloomston M, Al-Saif O, Klemanski D, Pinzone JJ, Martin EW, Palmer B, et al. Hepatic artery chemoembolization in 122 patients with metastatic carcinoid tumor: lessons learned. J Gastrointest Surg. 2007;11:264–71.
Roche A, Girish BV, de Baere T, Ducreux M, Elias D, Laplanche A, et al. Prognostic factors for chemoembolization in liver metastasis from endocrine tumors. Hepato-Gastroenterology. 2004;51:1751–6.
Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45:228–47.
Bhagat N, Reyes DK, Lin M, Kamel I, Pawlik TM, Frangakis C, et al. Phase II study of chemoembolization with drug-eluting beads in patients with hepatic neuroendocrine metastases: high incidence of biliary injury. Cardiovasc Intervent Radiol. 2013;36:449–59.
Guo Y, Yaghmai V, Salem R, Lewandowski RJ, Nikolaidis P, Larson AC, et al. Imaging tumor response following liver-directed intra-arterial therapy. Abdom Imaging. 2013;38:1286–99.
Lencioni R, Llovet JM. Modified RECIST (mRECIST) assessment for hepatocellular carcinoma. Semin Liver Dis. 2010;30:52–60.
Choi H, Charnsangavej C, Faria SC, Macapinlac HA, Burgess MA, Patel SR, et al. Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single institution with imatinib mesylate: proposal of new computed tomography response criteria. J Clin Oncol. 2007;25:1753–9.
Chun YS, Vauthey J-N, Boonsirikamchai P, Maru DM, Kopetz S, Palavecino M, et al. Association of computed tomography morphologic criteria with pathologic response and survival in patients treated with bevacizumab for colorectal liver metastases. J Am Med Assoc. 2009;302:2338–44.
Sahu S, Schernthaner R, Ardon R, Chapiro J, Zhao Y, Sohn JH, et al. Imaging biomarkers of tumor response in neuroendocrine liver metastases treated with transarterial chemoembolization: can enhancing tumor burden of the whole liver help predict patient survival? Radiology. 2017;283:883–94.
Tacher V, Lin M, Duran R, Yarmohammadi H, Lee H, Chapiro J, et al. Comparison of existing response criteria in patients with hepatocellular carcinoma treated with transarterial chemoembolization using a 3D quantitative approach. Radiology. 2016;278:275–84.
Liapi E, Geschwind J-F, Vossen JA, Buijs M, Georgiades CS, Bluemke DA, et al. Functional MRI evaluation of tumor response in patients with neuroendocrine hepatic metastasis treated with transcatheter arterial chemoembolization. Am J Roentgenol. 2008;190:67–73.
Gowdra Halappa V, Corona-Villalobos CP, Bonekamp S, Li Z, Reyes D, Cosgrove D, et al. Neuroendocrine liver metastasis treated by using intraarterial therapy: volumetric functional imaging biomarkers of early tumor response and survival. Radiology. 2013;266:502–13.
Li Z, Bonekamp S, Halappa VG, Corona-Villalobos CP, Pawlik T, Bhagat N, et al. Islet cell liver metastases: assessment of volumetric early response with functional MR imaging after transarterial chemoembolization. Radiology. 2012;264:97–109.
Guibal A, Lefort T, Chardon L, Benslama N, Mulé S, Pilleul F, et al. Contrast-enhanced ultrasound after devascularisation of neuroendocrine liver metastases: functional and morphological evaluation. Eur Radiol. 2013;23:805–15.
Pitt SC, Knuth J, Keily JM, McDermott JC, Weber SM, Chen H, et al. Hepatic neuroendocrine metastases: chemo- or bland embolization? J Gastrointest Surg. 2008;12:1951–60.
Maire F, Lombard-Bohas C, O’Toole D, Vullierme M-P, Rebours V, Couvelard A, et al. Hepatic arterial embolization versus chemoembolization in the treatment of liver metastases from well-differentiated midgut endocrine tumors: a prospective randomized study. Neuroendocrinology. 2012;96:294–300.
Fiore F, Del Prete M, Franco R, Marotta V, Ramundo V, Marciello F, et al. Transarterial embolization (TAE) is equally effective and slightly safer than transarterial chemoembolization (TACE) to manage liver metastases in neuroendocrine tumors. Endocrine. 2014;47:177–82.
Ruutiainen AT, Soulen MC, Tuite CM, Clark TWI, Mondschein JI, Stavropoulos SW, et al. Chemoembolization and bland embolization of neuroendocrine tumor metastases to the liver. J Vasc Interv Radiol. 2007;18:847–55.
Pericleous M, Caplin ME, Tsochatzis E, Yu D, Morgan-Rowe L, Toumpanakis C. Hepatic artery embolization in advanced neuroendocrine tumors: efficacy and long-term outcomes: embolization of neuroendocrine tumors. Asia Pac J Clin Oncol. 2016;12:61–9.
Gupta S, Johnson MM, Murthy R, Ahrar K, Wallace MJ, Madoff DC, et al. Hepatic arterial embolization and chemoembolization for the treatment of patients with metastatic neuroendocrine tumors: variables affecting response rates and survival. Cancer. 2005;104:1590–602.
Marrache F, Vullierme MP, Roy C, El Assoued Y, Couvelard A, O’Toole D, et al. Arterial phase enhancement and body mass index are predictors of response to chemoembolisation for liver metastases of endocrine tumours. Br J Cancer. 2007;96:49–55.
Strosberg JR, Choi J, Cantor AB, Kvols LK. Selective hepatic artery embolization for treatment of patients with metastatic carcinoid and pancreatic endocrine tumors. Cancer Control. 2006;13:72–8.
Ho AS, Picus J, Darcy MD, Tan B, Gould JE, Pilgram TK, et al. Long-term outcome after chemoembolization and embolization of hepatic metastatic lesions from neuroendocrine tumors. Am J Roentgenol. 2007;188:1201–7.
Pelage J-P, Fohlen A, Mitry E, Lagrange C, Beauchet A, Rougier P. Chemoembolization of neuroendocrine liver metastases using streptozocin and tris-acryl microspheres: embozar (EMBOsphere + ZAnosaR) study. Cardiovasc Intervent Radiol. 2017;40:394–400.
de Baere T, Deschamps F, Teriitheau C, Rao P, Conengrapht K, Schlumberger M, et al. Transarterial chemoembolization of liver metastases from well differentiated gastroenteropancreatic endocrine tumors with doxorubicin-eluting beads: preliminary results. J Vasc Interv Radiol. 2008;19:855–61.
Gaur SK, Friese JL, Sadow CA, Ayyagari R, Binkert CA, Schenker MP, et al. Hepatic arterial chemoembolization using drug-eluting beads in gastrointestinal neuroendocrine tumor metastatic to the liver. Cardiovasc Intervent Radiol. 2011;34:566–72.
Makary MS, Kapke J, Yildiz V, Pan X, Dowell JD. Conventional versus drug-eluting bead transarterial chemoembolization for neuroendocrine tumor liver metastases. J Vasc Interv Radiol. 2016;27:1298–304.
Minh DD, Chapiro J, Gorodetski B, Huang Q, Liu C, Smolka S, et al. Intra-arterial therapy of neuroendocrine tumour liver metastases: comparing conventional TACE, drug-eluting beads TACE and yttrium-90 radioembolisation as treatment options using a propensity score analysis model. Eur Radiol. 2017:1–11. https;//doi.org/10.1007/s00330-017-4856-2.
Onesti JK, Shirley LA, Saunders ND, Davidson GW, Dillhoff ME, Khabiri H, et al. Elevated alkaline phosphatase prior to transarterial chemoembolization for neuroendocrine tumors predicts worse outcomes. J Gastrointest Surg. 2016;20:580–6.
Ruszniewski P, Rougier P, Roche A, Legmann P, Sibert A, Hochlaf S, et al. Hepatic arterial chemoembolization in patients with liver metastases of endocrine tumors. A prospective phase II study in 24 patients. Cancer. 1993;71:2624–30.
Arrese D, McNally ME, Chokshi R, Feria-Arias E, Schmidt C, Klemanski D, et al. Extrahepatic disease should not preclude transarterial chemoembolization for metastatic neuroendocrine carcinoma. Ann Surg Oncol. 2013;20:1114–20.
Zappa M, Hentic O, Vullierme M-P, Lagadec M, Ronot M, Ruszniewski P, et al. Is visual radiological evaluation of liver tumour burden in patients with neuroendocrine tumours reproducible? Endocr Connect. 2017;6:33–8.
Brown KT, Koh BY, Brody LA, Getrajdman GI, Susman J, Fong Y, et al. Particle embolization of hepatic neuroendocrine metastases for control of pain and hormonal symptoms. J Vasc Interv Radiol. 1999;10:397–403.
Kress O, Wagner H-J, Wied M, Klose KJ, Arnold R, Alfke H. Transarterial chemoembolization of advanced liver metastases of neuroendocrine tumors--a retrospective single-center analysis. Digestion. 2003;68:94–101.
Kim W, Clark TW, Baum RA, Soulen MC. Risk factors for liver abscess formation after hepatic chemoembolization. J Vasc Interv Radiol. 2001;12:965–8.
de Baere T, Roche A, Amenabar JM, Lagrange C, Ducreux M, Rougier P, et al. Liver abscess formation after local treatment of liver tumors. Hepatology. 1996;23:1436–40.
Woo S, Chung JW, Hur S, Joo S-M, Kim H-C, Jae HJ, et al. Liver abscess after transarterial chemoembolization in patients with bilioenteric anastomosis: frequency and risk factors. Am J Roentgenol. 2013;200:1370–7.
Cao CQ, Yan TD, Bester L, Liauw W, Morris DL. Radioembolization with yttrium microspheres for neuroendocrine tumour liver metastases. Br J Surg. 2010;97:537–43.
Kalinowski M, Dressler M, König A, El-Sheik M, Rinke A, Höffken H, et al. Selective internal radiotherapy with Yttrium-90 microspheres for hepatic metastatic neuroendocrine tumors: a prospective single center study. Digestion. 2009;79:137–42.
King J, Quinn R, Glenn DM, Janssen J, Tong D, Liaw W, et al. Radioembolization with selective internal radiation microspheres for neuroendocrine liver metastases. Cancer. 2008;113:921–9.
Saxena A, Chua TC, Bester L, Kokandi A, Morris DL. Factors predicting response and survival after yttrium-90 radioembolization of unresectable neuroendocrine tumor liver metastases: a critical appraisal of 48 cases. Ann Surg. 2010;251:910–6.
Rhee TK, Lewandowski RJ, Liu DM, Mulcahy MF, Takahashi G, Hansen PD, et al. 90Y Radioembolization for metastatic neuroendocrine liver tumors: preliminary results from a multi-institutional experience. Ann Surg. 2008;247:1029–35.
Kennedy AS, Dezarn WA, McNeillie P, Coldwell D, Nutting C, Carter D, et al. Radioembolization for unresectable neuroendocrine hepatic metastases using resin 90Y-microspheres: early results in 148 patients. Am J Clin Oncol. 2008;31:271–9.
Memon K, Lewandowski RJ, Mulcahy MF, Riaz A, Ryu RK, Sato KT, et al. Radioembolization for neuroendocrine liver metastases: safety, imaging, and long-term outcomes. Int J Radiat Oncol Biol Phys. 2012;83:887–94.
Devcic Z, Rosenberg J, Braat AJA, Techasith T, Banerjee A, Sze DY, et al. The efficacy of hepatic 90Y resin radioembolization for metastatic neuroendocrine tumors: a meta-analysis. J Nucl Med. 2014;55:1404–10.
Ozao-Choy J, Friedman ML, Kim AS, Wachsman A, Wolin EM, Yu R, et al. Radioembolization for treatment of liver metastases from neuroendocrine tumors: correlation with imaging and biomarkers. Pancreas. 2013;42:358–60.
Peker A, Cicek O, Soydal C, Kucuk NO, Bilgic S. Radioembolization with yttrium-90 resin microspheres for neuroendocrine tumor liver metastases. Diagn Interv Radiol. 2015;21:54–9.
Paprottka PM, Hoffmann R-T, Haug A, Sommer WH, Raessler F, Trumm CG, et al. Radioembolization of symptomatic, unresectable neuroendocrine hepatic metastases using yttrium-90 microspheres. Cardiovasc Intervent Radiol. 2012;35:334–42.
Fidelman N, Kerlan RK Jr, Hawkins RA, Pampaloni M, Taylor AG, Kohi MP, et al. Radioembolization with 90Y glass microspheres for the treatment of unresectable metastatic liver disease from chemotherapy-refractory gastrointestinal cancers: final report of a prospective pilot study. J Gastrointest Oncol. 2016;7:860–74.
Benson AB, Geschwind J-F, Mulcahy MF, Rilling W, Siskin G, Wiseman G, et al. Radioembolisation for liver metastases: results from a prospective 151 patient multi-institutional phase II study. Eur J Cancer. 2013;49:3122–30.
Cramer B, Xing M, Kim HS. Prospective longitudinal quality of life assessment in patients with neuroendocrine tumor liver metastases treated with 90Y radioembolization. Clin Nucl Med. 2016;41:e493–7.
Ludwig JM, Ambinder EM, Ghodadra A, Xing M, Prajapati HJ, Kim HS. Lung shunt fraction prior to Yttrium-90 radioembolization predicts survival in patients with neuroendocrine liver metastases: single-center prospective analysis. Cardiovasc Intervent Radiol. 2016;39:1007–14.
Sommer WH, Ceelen F, García-Albéniz X, Paprottka PM, Auernhammer CJ, Armbruster M, et al. Defining predictors for long progression-free survival after radioembolisation of hepatic metastases of neuroendocrine origin. Eur Radiol. 2013;23:3094–103.
Neperud J. Can imaging patterns of neuroendocrine hepatic metastases predict response yttruim-90 radioembolotherapy? World J Radiol. 2013;5:241.
Shaheen M, Hassanain M, Aljiffry M, Cabrera T, Chaudhury P, Simoneau E, et al. Predictors of response to radio-embolization (TheraSphere®) treatment of neuroendocrine liver metastasis. HPB. 2012;14:60–6.
Fan KY, Wild AT, Halappa VG, Kumar R, Ellsworth S, Ziegler M, et al. Neuroendocrine tumor liver metastases treated with yttrium-90 radioembolization. Contemp Clin Trials. 2016;50:143–9.
Miller FH, Keppke AL, Reddy D, Huang J, Jin J, Mulcahy MF, et al. Response of liver metastases after treatment with Yttrium-90 microspheres: role of size, necrosis, and PET. Am J Roentgenol. 2007;188:776–83.
Filippi L, Scopinaro F, Pelle G, Cianni R, Salvatori R, Schillaci O, et al. Molecular response assessed by (68)Ga-DOTANOC and survival after (90)Y microsphere therapy in patients with liver metastases from neuroendocrine tumours. Eur J Nucl Med Mol Imaging. 2016;43:432–40.
Ceelen F, Theisen D, de Albéniz XG, Auernhammer CJ, Haug AR, D’Anastasi M, et al. Towards new response criteria in neuroendocrine tumors: Which changes in MRI parameters are associated with longer progression-free survival after radioembolization of liver metastases?: Imaging changes after radioembolization. J Magn Reson Imaging. 2015;41:361–8.
Kukuk GM, Mürtz P, Träber F, Meyer C, Ullrich J, Gieseke J, et al. Diffusion-weighted imaging with acquisition of three b-values for response evaluation of neuroendocrine liver metastases undergoing selective internal radiotherapy. Eur Radiol. 2014;24:267–76.
Cholapranee A, van Houten D, Deitrick G, Dagli M, Sudheendra D, Mondschein JI, et al. Risk of liver abscess formation in patients with prior biliary intervention following yttrium-90 radioembolization. Cardiovasc Intervent Radiol. 2015;38:397–400.
Kennedy AS, McNeillie P, Dezarn WA, Nutting C, Sangro B, Wertman D, et al. Treatment parameters and outcome in 680 treatments of internal radiation with resin 90Y-microspheres for unresectable hepatic tumors. Int J Radiat Oncol Biol Phys. 2009;74:1494–500.
Goin JE, Salem R, Carr BI, Dancey JE, Soulen MC, Geschwind JFH, et al. Treatment of unresectable hepatocellular carcinoma with intrahepatic yttrium 90 microspheres: factors associated with liver toxicities. J Vasc Interv Radiol. 2005;16:205–13.
Braat MNGJA, van Erpecum KJ, Zonnenberg BA, van den Bosch MAJ, Lam MGEH. Radioembolization-induced liver disease: a systematic review. Eur J Gastroenterol Hepatol. 2017;29:144–52.
Yang TX, Chua TC, Morris DL. Radioembolization and chemoembolization for unresectable neuroendocrine liver metastases - a systematic review. Surg Oncol. 2012;21:299–308.
Engelman ES, Leon-Ferre R, Naraev BG, Sharma N, Sun S, O’Dorisio TM, et al. Comparison of transarterial liver-directed therapies for low-grade metastatic neuroendocrine tumors in a single institution. Pancreas. 2014;43:219–25.
Whitney R, Vàlek V, Fages JF, Garcia A, Narayanan G, Tatum C, et al. Transarterial chemoembolization and selective internal radiation for the treatment of patients with metastatic neuroendocrine tumors: a comparison of efficacy and cost. Oncologist. 2011;16:594–601.
Singla S, LeVea CM, Pokuri VK, Attwood KM, Wach MM, Tomaszewski GM, et al. Ki67 score as a potential predictor in the selection of liver-directed therapies for metastatic neuroendocrine tumors: a single institutional experience. J Gastrointest Oncol. 2016;7:441–8.
Du S, Ni J, Weng L, Ma F, Li S, Wang W, et al. Aggressive Locoregional Treatment Improves the Outcome of Liver Metastases from Grade 3 Gastroenteropancreatic Neuroendocrine Tumors. Medicine (Baltimore). 2015;94:e1429.
Osborne DA, Zervos EE, Strosberg J, Boe BA, Malafa M, Rosemurgy AS, et al. Improved outcome with cytoreduction versus embolization for symptomatic hepatic metastases of carcinoid and neuroendocrine tumors. Ann Surg Oncol. 2006;13:572–81.
Touzios JG, Kiely JM, Pitt SC, Rilling WS, Quebbeman EJ, Wilson SD, et al. Neuroendocrine hepatic metastases: does aggressive management improve survival? Ann Surg. 2005;241:776–85.
Strosberg JR, Weber JM, Choi J, Campos TL, Valone TL, Han G, et al. A phase II clinical trial of sunitinib following hepatic transarterial embolization for metastatic neuroendocrine tumors. Ann Oncol. 2012;23:2335–41.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of interest
LM: Pfizer, Novartis, Ipsen.
MZ: Pfizer.
OH: Pfizer, Novartis, Ipsen, Keocyt.
VV: none.
PR: Pfizer, Novartis, Ipsen.
Rights and permissions
About this article
Cite this article
de Mestier, L., Zappa, M., Hentic, O. et al. Liver transarterial embolizations in metastatic neuroendocrine tumors. Rev Endocr Metab Disord 18, 459–471 (2017). https://doi.org/10.1007/s11154-017-9431-2
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11154-017-9431-2