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Radionuclide Therapy for Tumors of the Liver and Biliary Tract

  • Federica Guidoccio
  • Giuseppe Boni
  • Duccio Volterrani
  • Giuliano Mariani
Chapter

Abstract

The liver can be the site of both primary and metastatic malignancies. Besides hepatocellular carcinoma (HCC, ranking fifth among the most common malignancies worldwide) [1], different solid tumors primarily arising in other tissues/organs, most importantly colorectal cancer (CRC), frequently give rise to metastases in the liver [2].

Keywords

Liver tumors Radioembolization therapy 131I-Lipiodol 188Re-Lipiodol 90Y-Microspheres 166Ho-Microspheres Pretreatment imaging with 99mTc-MAA Hepatocellular carcinoma Intrahepatic cholangiocarcinoma Metastatic liver tumors 

References

  1. 1.
    El-Serag HB. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology. 2012;142:1264–73.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    van der Pool AE, Damhuis RA, Ijzermans JN, de Wilt JH, Eggermont AM, Kranse R, et al. Trends in incidence, treatment and survival of patients with stage IV colorectal cancer: a population-based series. Color Dis. 2012;14:56–61.CrossRefGoogle Scholar
  3. 3.
    Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F, et al. Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med. 1996;334:693–9.PubMedCrossRefGoogle Scholar
  4. 4.
    Ingold JA, Reed GB, Kaplan HS, Bagshaw MA. Radiation hepatitis. Am J Roentgenol Radium Ther Nucl Med. 1965;93:200–8.PubMedGoogle Scholar
  5. 5.
    Lawrence TS, Robertson JM, Anscher MS, Jirtle RL, Ensminger WD, Fajardo LF. Hepatic toxicity resulting from cancer treatment. Int J Radiat Oncol Biol Phys. 1995;31:1237–48.PubMedCrossRefGoogle Scholar
  6. 6.
    Yu H, Burke CT. Comparison of percutaneous ablation technologies in the treatment of malignant liver tumors. Semin Intervent Radiol. 2014;31:129–37.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Stuart K. Chemoembolization in the management of liver tumors. Oncologist. 2003;8:425–37.PubMedCrossRefGoogle Scholar
  8. 8.
    Geschwind JFH. Chemoembolization for hepatocellular carcinoma: where does the truth lie? J Vasc Interv Radiol. 2002;13:991–4.PubMedCrossRefGoogle Scholar
  9. 9.
    Varela M, Real MI, Burrel M, Forner A, Sala M, Brunet M, et al. Chemoembolization of hepatocellular carcinoma with drug eluting beads: efficacy and doxorubicin pharmacokinetics. J Hepatol. 2007;46:474–81.PubMedCrossRefGoogle Scholar
  10. 10.
    Llovet JM, Real MI, Montaña X, Planas R, Coll S, Aponte J, et al. Arterial embolisation or chemoembolisation versus symptomatic treatment in patients with unresectable hepatocellular carcinoma: a randomised controlled trial. Lancet. 2002;359(9319):1734–9.PubMedCrossRefGoogle Scholar
  11. 11.
    Kettenbach J, Stadler A, Katzler IV, Schernthaner R, Blum M, Lammer J, et al. Drug-loaded microspheres for the treatment of liver cancer: review of current results. Cardiovasc Intervent Radiol. 2008;31:468–76.PubMedCrossRefGoogle Scholar
  12. 12.
    European Association For The Study Of The Liver; European Organisation For Research And Treatment Of Cancer. EASLEORT Clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2012;56:908–43.CrossRefGoogle Scholar
  13. 13.
    Salem R, Lewandowski RJ, Atassi B, Gordon SC, Gates VL, Barakat O, et al. Treatment of unresectable hepatocellular carcinoma with use of 90Y microspheres (TheraSphere): safety, tumor response, and survival. J Vasc Interv Radiol. 2005;16:1627–39.PubMedCrossRefGoogle Scholar
  14. 14.
    Raoul JL, Bourguet P, Bretagne JF, Duvauferrier R, Coornaert S, Darnault P, et al. Hepatic artery injection of I-131-labelled lipiodol. Part I. Biodistribution study results in patients with hepatocellular carcinoma. Radiology. 1988;168:541–5.PubMedCrossRefGoogle Scholar
  15. 15.
    Nakajo M, Kobayashi H, Shimabukuro K, Shirono K, Sakata H, Taguchi M, et al. Biodistribution and in vivo kinetics of iodine-131 lipiodol infused via the hepatic artery of patients with hepatic cancers. J Nucl Med. 1988;29:1066–77.PubMedGoogle Scholar
  16. 16.
    Smits ML, Nijsen JF, van den Bosch MA, Lam MG, Vente MA, Huijbregts JE, et al. Holmium-166 radioembolization for the treatment of patients with liver metastases: design of the phase I HEPAR trial. J Exp Clin Cancer Res. 2010;29:70.  https://doi.org/10.1186/1756-9966-29-70.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Nowicki ML, Cwikla JB, Sankowski AJ, Shcherbinin S, Grimmes J, Celler A, et al. Initial study of radiological and clinical efficacy radioembolization using 188Re-human serum albumin (HSA) microspheres in patients with progressive, unresectable primary or secondary liver cancers. Med Sci Monit. 2014;20:1353–62.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Bhattacharya S, Dhillon AP, Winslet MC, Davidson BR, Shukla N, Gupta SD, et al. Human liver cancer cells and endothelial cells incorporate iodised oil. Br J Cancer. 1996;73:877–81.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Madsen MT, Park CH, Thakur ML. Dosimetry of iodine-131 ethiodol in the treatment of hepatoma. J Nucl Med. 1988;29:1038–44.PubMedGoogle Scholar
  20. 20.
    Monsieurs MA, Bacher K, Brans B, Vral A, De Ridder L, Dierckx RA, et al. Patient dosimetry for 131I-lipiodol therapy. Eur J Nucl Med Mol Imaging. 2003;30:554–61.PubMedCrossRefGoogle Scholar
  21. 21.
    Bhattacharya S, Novell JR, Dusheiko GM, Hilson AJ, Dick R, Hobbs KE. Epirubicin-Lipiodol chemotherapy versus 131iodine-lipiodol radiotherapy in the treatment of unresectable hepatocellular carcinoma. Cancer. 1995;76:2202–10.PubMedCrossRefGoogle Scholar
  22. 22.
    Yoo HS, Park CH, Lee JT, Kim KW, Yoon CS, Suh JH, et al. Small hepatocellular carcinoma: high dose internal radiation therapy with superselective intra-arterial injection of I-131-labeled Lipiodol. Cancer Chemother Pharmacol. 1994;33:S128–S33.PubMedCrossRefGoogle Scholar
  23. 23.
    Leung WT, Lau WY, Ho S, Chan M, Leung N, Lin J, et al. Selective internal radiation therapy with intra-arterial iodine-131-Lipiodol in inoperable hepatocellular carcinoma. J Nucl Med. 1994;35:1313–8.PubMedGoogle Scholar
  24. 24.
    Raoul JL, Guyader D, Bretagne JF, Duvauferrier R, Bourguet P, Bekhechi D, et al. Randomized controlled trial for hepatocellular carcinoma with portal vein thrombosis: intra-arterial iodine-131-iodized oil versus medical support. J Nucl Med. 1994;35:1782–7.PubMedGoogle Scholar
  25. 25.
    Boucher E, Garin E, Guillygomac’h A, Olivie D, Boudjema K, Raoul JL. Intra-arterial injection of iodine-131-labeled lipiodol for treatment of hepatocellular carcinoma. Radiother Oncol. 2007;82:76–82.PubMedCrossRefGoogle Scholar
  26. 26.
    Partensky C, Sassolas G, Henry L, Paliard P, Maddern GJ. Intra-arterial iodine 131-labeled lipiodol as adjuvant therapy after curative liver resection for hepatocellular carcinoma: a phase 2 clinical study. Arch Surg. 2000;135:1298–300.PubMedCrossRefGoogle Scholar
  27. 27.
    Lau WY, Lai EC, Leung TW, Yu SC. Adjuvant intra-arterial iodine-131-labeled lipiodol for resectable hepatocellular carcinoma: a prospective randomized trial-update on 5-year and 10-year survival. Ann Surg. 2008;247:43–8.PubMedCrossRefGoogle Scholar
  28. 28.
    Lee YS, Jeong JM, Kim YJ, Chung JW, Park JH, Suh YG, et al. Synthesis of 188Re-labelled long chain alkyl diaminedithiol for therapy of liver cancer. Nucl Med Commun. 2002;23:237–42.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    De Ruyck K, Lambert B, Bacher K, Gemmel F, De Vos F, Vral A, et al. Biologic dosimetry of 188Re-HDD/lipiodol versus 131I-lipiodol therapy in patients with hepatocellular carcinoma. J Nucl Med. 2004;45:612–8.PubMedGoogle Scholar
  30. 30.
    Kumar A, Srivastava DN, Chau TT, Long HD, Bal C, Chandra P, et al. Inoperable hepatocellular carcinoma: transarterial 188Re HDD-labeled iodized oil for treatment. Prospective multicenter clinical trial. Radiology. 2007;243:509–19.PubMedCrossRefGoogle Scholar
  31. 31.
    Sato K, Lewandowski RJ, Bui JT, Omary R, Hunter RD, Kulik L, et al. Treatment of unresectable primary and metastatic liver cancer with yttrium-90 microspheres (TheraSphere): assessment of hepatic arterial embolization. Cardiovasc Intervent Radiol. 2006;29:522–9.PubMedCrossRefGoogle Scholar
  32. 32.
    Salem R, Thurston KG. Radioembolization with 90Yttrium microspheres: a state-of-the-art brachytherapy treatment for primary and secondary liver malignancies. Part 1: Technical and methodologic considerations. J Vasc Interv Radiol. 2006;17:1251–78.CrossRefGoogle Scholar
  33. 33.
    Hamami ME, Poeppel TD, Müller S, Heusner T, Bockisch A, Hilgard P, Antoch G. SPECT/CT with 99mTc-MAA in radioembolization with 90Y microspheres in patients with hepatocellular cancer. J Nucl Med. 2009;50:688–92.PubMedCrossRefGoogle Scholar
  34. 34.
    Grosser OS, Rufi J, Kupitz D, Pethe A, Ulrich G, Genseke P, et al. Pharmacokinetics of 99mTc-MAA- and 99mTc-HSA microspheres used in preradioembolization dosimetry: influence on the liver–lung shunt. J Nucl Med. 2016;57:925–7.PubMedCrossRefGoogle Scholar
  35. 35.
    Sabet A, Ahmadzadehfar H, Muckle M, Haslerud T, Wilhelm K, Biersack HJ, et al. Significance of oral administration of sodium perchlorate in planning liver-directed radioembolisation. J Nucl Med. 2011;52:1063–7.PubMedCrossRefGoogle Scholar
  36. 36.
    Dale RG. Dose-rate effects in targeted radiotherapy. Phys Med Biol. 1996;41:1871–84.PubMedCrossRefGoogle Scholar
  37. 37.
    Ho S, Lau WY, Leung TW, Chan M, Chan KW, Lee WY, et al. Partition model for estimating radioation doses from yttrium-90 microspheres in treating hepatic tumors. Eur J Nucl Med. 1996;23:947–52.CrossRefGoogle Scholar
  38. 38.
    Kennedy AS, Dezarn WA, McNeillie P, Overton C, England M, Sailer SL. Fractionation, dose selection, and response of hepatic metastases of neuroendocrine tumors after 90Y-microsphere brachytherapy. Brachytheraphy. 2006;5:103–4.Google Scholar
  39. 39.
    Kennedy AS, Dezarn WA, McNeillie P, Overton C, England M, Sailer SL. Dose selection of resin 90Y-microspheres for liver brachytherapy: a single center review. Brachytheraphy. 2006;5:104.Google Scholar
  40. 40.
    Flamen P, Vanderlinden B, Delatte P, Ghanem G, Ameye L, Van Den Eyden M, et al. Multimodality imaging can predict the metabolic response of unresectable colorectal liver metastases to radioembolisation therapy with yttrium-90 labeled resin microspheres. Phys Med Biol. 2008;53:6591–3.PubMedCrossRefGoogle Scholar
  41. 41.
    Jiang M, Fischman A, Nowakowski FS, Sherif Heiba S, Zhuangyu Zhang Z, Kneusaurek K, et al. Segmental perfusion differences on paired Tc-99m macroaggregated albumin (MAA) hepatic perfusion imaging and yttrium-90 (Y-90) bremsstrahlung imaging studies in SIR-sphere radioembolization: associations with angiography. J Nucl Med Radiat Ther. 2012;3:122.CrossRefGoogle Scholar
  42. 42.
    Wondergem M, Smits MLJ, Elschot M, de Jong HWAM, Verkooijen HM, van den Bosch MAAJ, et al. 99mTc-Macroaggregated albumin poorly predicts the intrahepatic distribution of 90Y resin microspheres in hepatic radioembolization. J Nucl Med. 2013;54:1294–301.PubMedCrossRefGoogle Scholar
  43. 43.
    Lau WY, Sangro B, Chen PJ, Cheng SQ, Chow P, Lee RC, et al. Treatment for hepatocellular carcinoma with portal vein tumor thrombosis: the emerging role for radioembolization using yttrium-90. Oncology. 2013;84:311–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Garin E, Lenoir L, Rolland Y, Edeline J, Mesbah H, Laffont S, et al. Dosimetry based on 99mTc-macroaggregated albumin SPECT/CT accurately predicts tumor response and survival in hepatocellular carcinoma patients treated with 90Y-loaded glass microspheres: preliminary results. J Nucl Med. 2012;53:255–63.CrossRefGoogle Scholar
  45. 45.
    Mazzaferro V, Sposito C, Bhoori S, Romito R, Chiesa C, Morosi C, et al. Yttrium-90 radioembolization for intermediate-advanced hepatocellular carcinoma: a phase 2 study. Hepatology. 2013;57:1826–37.PubMedCrossRefGoogle Scholar
  46. 46.
    Ahmadzadehfar H, Muckle M, Sabet A, Wilhelm K, Kuhl C, Biermann K, et al. The significance of bremsstrahlung SPECT/CT after yttrium-90 radioembolisation treatment in the prediction of extrahepatic side effects. Eur J Nucl Med Mol Imaging. 2011;39:309–15.CrossRefGoogle Scholar
  47. 47.
    Lhommel R, Goffette P, Van del Eynde M, Jamar F, Pauwels S, Bilbao JI, et al. Yttrium-90 TOF PET scan demonstrates high-resolution biodistribution after liver SIRT. Eur J Nucl Med Mol Imaging. 2009;36:1696.PubMedCrossRefGoogle Scholar
  48. 48.
    Lhommel R, van Elmbt L, Goffette P, Van den Eynde M, Jamar F, Pauwels S, et al. Feasibility of 90Y TOF PET-based dosimetry in liver metastasis therapy using SIR-Spheres. Eur J Nucl Med Mol Imaging. 2010;37:1654–62.PubMedCrossRefGoogle Scholar
  49. 49.
    Kao YH, Tan EH, Lim KY, Eng CE, Goh SW. Yttrium-90 internal pair production imaging using first generation PET/CT provides high resolution images for qualitative diagnostic purposes. Br J Radiol. 2012;85:1018–9.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Wright CL, Zhang J, Tweedle MF, Knopp MV, Hall NC. Theranostic imaging of yttrium-90. Biomed Res Int. 2015;2015:481279.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Gnesin S, Canetti L, Adib S, Cherbuin N, Silva-Monteiro M, Bize P, et al. Partition model based 99mTc-MAA SPECT/CT predictive dosimetry compared to 90Y TOF PET/CT post treatment dosimetry in radioembolisation of hepatocellular carcinoma: a quantitative agreement comparison. J Nucl Med. 2016;57:1672–8.PubMedCrossRefGoogle Scholar
  52. 52.
    Riaz A, Memon K, Miller FH, Nikolaidis P, Kulik LM, Lewandowski RJ, et al. Role of the EASL, RECIST, and WHO response guidelines alone or in combination for hepatocellular carcinoma: radiologic-pathologic correlation. J Hepatol. 2011;54:695–704.PubMedCrossRefGoogle Scholar
  53. 53.
    Wong CY, Qing F, Savin M, Campbell J, Gates VL, Sherpa KM, et al. Reduction of metastatic load to liver after intraarterial hepatic yttrium-90 radioembolization as evaluated by [18F]fluorodeoxyglucose positron emission tomographic imaging. J Vasc Interv Radiol. 2005;16:1101–6.PubMedCrossRefGoogle Scholar
  54. 54.
    Miller FH, Keppke AL, Reddy D, Huang J, Jin J, Mulcahy MF, Salem R. Response of liver metastases after treatment with yttrium-90 microspheres: role of size, necrosis, and PET. AJR Am J Roentgenol. 2007;188:776–83.PubMedCrossRefGoogle Scholar
  55. 55.
    Flamen P, Vanderlinden B, Delatte P, Ghanem G, Ameye L, Van Den Eynde M, et al. Multimodality imaging can predict the metabolic response of unresectable colorectal liver metastases to radioembolization therapy with Yttrium-90 labeled resin microspheres. Phys Med Biol. 2008;53:6591–603.PubMedCrossRefGoogle Scholar
  56. 56.
    Haug AR, Heinemann V, Bruns CJ, Hoffmann R, Jakobs T, Bartenstein P, Hacker M. 18F-FDG PET independently predicts survival in patients with cholangiocellular carcinoma treated with 90Y microspheres. Eur J Nucl Med Mol Imaging. 2011;38:1037–45.PubMedCrossRefGoogle Scholar
  57. 57.
    Sabet A, Ahmadzadehfar H, Bruhman J, Sabet A, Meyer C, Wasmuth JC, et al. Survival in patients with hepatocellular carcinoma treated with 90Y-microsphere radioembolization. Prediction by 18F-FDG PET. Nuklearmedizin. 2014;53:39–45.PubMedCrossRefGoogle Scholar
  58. 58.
    Hartenbach M, Weber S, Albert NL, Hartenbach S, Hirtl A, Zacherl MJ, et al. Evaluating treatment response of radioembolization in intermediate-stage hepatocellular carcinoma patients using 18F-fluoroethylcholine PET/CT. J Nucl Med. 2015;56:1661–6.PubMedCrossRefGoogle Scholar
  59. 59.
    Zerizer I, Al-Nahhas A, Towey D, Tait P, Ariff B, Wasan H, et al. The role of early 18F-FDG PET/CT in prediction of progression-free survival after 90Y radioembolization: comparison with RECIST and tumour density criteria. Eur J Nucl Med Mol Imaging. 2012;39:1391–9.PubMedCrossRefGoogle Scholar
  60. 60.
    Sabet A, Meyer C, Aouf A, Sabet A, Ghamari S, Pieper CC, et al. Early post-treatment FDG PET predicts survival after 90Y microsphere radioembolization in liver-dominant metastatic colorectal cancer. Eur J Nucl Med Mol Imaging. 2015;42:370–6.PubMedCrossRefGoogle Scholar
  61. 61.
    Haug AR, Tiega Donfack BP, Trumm C, Zech CJ, Michl M, Laubender RP, et al. 18F-FDG PET/CT predicts survival after radioembolization of hepatic metastases from breast cancer. J Nucl Med. 2012;53:371–7.PubMedCrossRefGoogle Scholar
  62. 62.
    Filippi L, Scopinaro F, Pelle G, Cianni R, Salvatori R, Schillaci O, et al. Molecular response assessed by 68Ga-DOTANOC and survival after 90Y microsphere therapy in patients with liver metastases from neuroendocrine tumours. Eur J Nucl Med Mol Imaging. 2016;43:432–40.PubMedCrossRefGoogle Scholar
  63. 63.
    Fidelman N, Kerlan RK Jr. Transarterial chemoembolization and 90Y radioembolization for hepatocellular carcinoma: review of current applications beyond intermediate-stage disease. AJR Am J Roentgenol. 2015;205:742–52.PubMedCrossRefGoogle Scholar
  64. 64.
    Braat AJ, Huijbregts JE, Molenaar IQ, Borel Rinkes IH, van den Bosch MA, Lam MG. Hepatic radioembolization as a bridge to liver surgery. Front Oncol. 2014;4:199.  https://doi.org/10.3389/fonc.2014.00199.. eCollection 2014CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Lewandowski RJ, Donahue L, Chokechanachaisakul A, Kulik L, Mouli S, Caicedo J, et al. 90Y radiation lobectomy: outcomes following surgical resection in patients with hepatic tumors and small future liver remnant volumes. J Surg Oncol. 2016;114:99–105.PubMedCrossRefGoogle Scholar
  66. 66.
    Teo JY, Allen JC Jr, Ng DC, Choo SP, Tai DW, Chang JP, et al. A systematic review of contralateral liver lobe hypertrophy after unilobar selective internal radiation therapy with Y90. HPB (Oxford). 2016;18:7–12.CrossRefGoogle Scholar
  67. 67.
    Johnson GE, Monsky WL, Valji K, Hippe DS, Padia SA. Yttrium-90 radioembolization as a salvage treatment following chemoembolization for hepatocellular carcinoma. J Vasc Interv Radiol. 2016;27:1123–9.PubMedCrossRefGoogle Scholar
  68. 68.
    Chow PK, Poon DY, Khin MW, Singh H, Han HS, Goh AS, et al, Asia-Pacific Hepatocellular Carcinoma Trials Group. Multicenter phase II study of sequential radioembolization-sorafenib therapy for inoperable hepatocellular carcinoma. PLoS One. 2014;9(3):e90909.  https://doi.org/10.1371/journal.pone.0090909. eCollection 2014.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Kulik L, Vouche M, Koppe S, Lewandowski RJ, Mulcahy MF, Ganger D, et al. Prospective randomized pilot study of Y90 +/− sorafenib as bridge to transplantation in hepatocellular carcinoma. J Hepatol. 2014;61:309–17.PubMedCrossRefGoogle Scholar
  70. 70.
    Ricke J, Bulla K, Kolligs F, Peck-Radosavljevic M, Reimer P, Sangro B, et al. Safety and toxicity of radioembolization plus Sorafenib in advanced hepatocellular carcinoma: analysis of the European multicentre trial SORAMIC. Liver Int. 2015;35:620–6.PubMedCrossRefGoogle Scholar
  71. 71.
    Lorenzin D, Pravisani R, Leo CA, Bugiantella W, Soardo G, Carnelutti A, et al. Complete remission of unresectable hepatocellular carcinoma after combined sorafenib and adjuvant yttrium-90 radioembolization. Cancer Biother Radiopharm. 2016;31:65–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Sangha BS, Nimeiri H, Hickey R, Salem R, Lewandowski RJ. Radioembolization as a treatment strategy for metastatic colorectal cancer to the liver: what can we learn from the SIRFLOX trial? Curr Treat Options Oncol. 2016;17:26.PubMedCrossRefGoogle Scholar
  73. 73.
    Dutton SJ, Kenealy N, Love SB, Wasan HS, Sharma RA, FOXFIRE Protocol Development Group and the NCRI Colorectal Clinical Study Group. FOXFIRE protocol: an open-label, randomised, phase III trial of 5-fluorouracil, oxaliplatin and folinic acid (OxMdG) with or without interventional Selective Internal Radiation Therapy (SIRT) as first-line treatment for patients with unresectable liver-only or liver-dominant metastatic colorectal cancer. BMC Cancer. 2014;14:497.  https://doi.org/10.1186/1471-2407-14-497.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Geschwind JF, Salem R, Carr BI, Soulen MC, Thurston KG, Goin KA, et al. Yttrium-90 microspheres for the treatment of hepatocellular carcinoma. Gastroenterology. 2004;127:S194–205.PubMedCrossRefGoogle Scholar
  75. 75.
    Salem R, Lewandowsky RJ, Mulcahy MF, Riaz A, Ryu RK, Ibrahim S, et al. Radioembolisation for hepatocellular carcinoma using Yttrium-90 microspheres. a comprehensive report of long term outcomes. Gastroenterology. 2010;138:52–64.PubMedCrossRefGoogle Scholar
  76. 76.
    Kulik LM, Atassi B, van Holsbeeck L, Souman T, Lewandowski RJ, Mulcahy MF, et al. Yttrium-90 microspheres (TheraSphere®) treatment of unresectable hepatocellular carcinoma: downstaging to resection, RFA and bridge to transplantation. J Surg Oncol. 2006;94:572–86.PubMedCrossRefGoogle Scholar
  77. 77.
    Tohme S, Sukato D, Chen HW, Amesur N, Zajko AB, Humar A, et al. Yttrium-90 radioembolization as a bridge to liver transplantation: a single-institution experience. J Vasc Interv Radiol. 2013;24:1632–8.PubMedCrossRefGoogle Scholar
  78. 78.
    Abdelfattah MR, Al-Sebayel M, Broering D, Alsuhaibani H. Radioembolization using yttrium-90 microspheres as bridging and downstaging treatment for unresectable hepatocellular carcinoma before liver transplantation: initial single-center experience. Transplant Proc. 2015;47:408–11.PubMedCrossRefGoogle Scholar
  79. 79.
    Kulik LM, Carr BI, Mulcahy MF, Lewandowski RJ, Atassi B, Ryu RK, et al. Safety and efficacy of 90Y radiotherapy for hepatocellular carcinoma with and without portal vein thrombosis. Hepatology. 2008;47:71–81.PubMedCrossRefGoogle Scholar
  80. 80.
    Ibrahim SM, Mulcahy MF, Lewandowski RJ, Sato KT, Ryu RK, Masterson EJ, et al. Treatment of unresectable cholangiocarcinoma using yttrium-90 microspheres: results from a pilot study. Cancer. 2008;113:2119–28.PubMedCrossRefGoogle Scholar
  81. 81.
    Al-Adra DP, Gill RS, Axford SJ, Shi X, Kneteman N, Liau SS. Treatment of unresectable intrahepatic cholangiocarcinoma with yttrium-90 radioembolization: a systematic review and pooled analysis. Eur J Surg Oncol. 2015;41:120–7.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Rayar M, Sulpice L, Edeline J, Garin E, Levi Sandri GB, Meunier B, et al. Intra-arterial yttrium-90 radioembolization combined with systemic chemotherapy is a promising method for downstaging unresectable huge intrahepatic cholangiocarcinoma to surgical treatment. Ann Surg Oncol. 2015;22:3102–8.PubMedCrossRefGoogle Scholar
  83. 83.
    Boehm LM, Jayakrishnan TT, Miura JT, Zacharias AJ, Johnston FM, Turaga KK, et al. Comparative effectiveness of hepatic artery based therapies for unresectable intrahepatic cholangiocarcinoma. J Surg Oncol. 2015;111:213–20.PubMedCrossRefGoogle Scholar
  84. 84.
    Valle J, Wasan H, Palmer DH, Cunningham D, Anthoney A, Maraveyas A, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362:1273–81.PubMedCrossRefGoogle Scholar
  85. 85.
    Welsh JS, Kennedy AS, Thomadsen B. Selective Internal Radiation Therapy (SIRT) for liver metastases secondary to colorectal adenocarcinoma. Int J Radiat Oncol Biol Phys. 2006;66:S62–73.PubMedCrossRefGoogle Scholar
  86. 86.
    Wong CY, Salem R, Raman S, Gates VL, Dworkin HJ. Evaluating 90Y-glass microsphere treatment response of unresectable colorectal liver metastases by [18F]FDG PET: a comparison with CT or MRI. Eur J Nucl Med Mol Imaging. 2002;29:815–20.PubMedCrossRefGoogle Scholar
  87. 87.
    Van den Eynde M, Flamen P, El Nakadi I, Liberale G, Delatte P, Larsimont D, et al. Inducing resectability of chemotherapy-refractory colorectal liver metastasis by radioembolization with yttrium-90 microspheres. Clin Nucl Med. 2008;33:697–9.PubMedCrossRefGoogle Scholar
  88. 88.
    Gray B, Van Hazel G, Hope M, Burton M, Moroz P, Anderson J, 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. 2001;12:1711–20.PubMedCrossRefGoogle Scholar
  89. 89.
    Goin JE, Dancey JE, Hermann GA, Sickles CJ, Roberts CA, MacDonald JS. Treatment of unresectable metastatic colorectal carcinoma to the liver with intrahepatic Y-90 microspheres: a dose-ranging study. World J Nucl Med. 2003;2:216–25.Google Scholar
  90. 90.
    Van Hazel G, Blackwell A, Anderson J, Price D, Moroz P, Bower G, et al. Randomised phase 2 trial of SIR-Spheres plus fluorouracil/leucovorin chemotherapy versus fluorouracil/leucovorinchemotherapy alone in advanced colorectal cancer. J Surg Oncol. 2004;88:78–85.PubMedCrossRefGoogle Scholar
  91. 91.
    Sharma RA, Van Hazel GA, Morgan B, Berry DP, Blanshard K, Price D, Bower G, et al. Radioembolization of liver metastases from colorectal cancer using yttrium-90 microspheres with concomitant systemic oxaliplatin, fluorouracil, and leucovorin chemotherapy. J Clin Oncol. 2007;25:1099–106.PubMedCrossRefGoogle Scholar
  92. 92.
    van Hazel GA, Pavlakis N, Goldstein D, Olver IN, Tapner MJ, Price D, et al. Treatment of fluorouracil-refractory patients with liver metastases from colorectal cancer by using yttrium-90 resin microspheres plus concomitant systemic irinotecan chemotherapy. J Clin Oncol. 2009;27:4089–95.PubMedCrossRefGoogle Scholar
  93. 93.
    Gibbs P, Heinemann V, Sharma NK, Findlay MPN, Ricke J, Gebski V, et al. SIRFLOX Study Group. SIRFLOX: randomized phase III trial comparing first-line mFOLFOX6 ± bevacizumab (bev) versus mFOLFOX6 + selective internal radiation therapy (SIRT) ± bev in patients (pts) with metastatic colorectal cancer (mCRC). J Clin Oncol. 2015;33(Suppl):3502.CrossRefGoogle Scholar
  94. 94.
    Hong K, McBride JD, Georgiades CS, Reyes DK, Herman JM, Kamel IR, et al. Salvage therapy for liver-dominant colorectal metastatic adenocarcinoma: comparison between transcatheter arterial chemoembolization versus yttrium-90 radioembolization. J Vasc Interv Radiol. 2009;20:360–7.PubMedCrossRefGoogle Scholar
  95. 95.
    Saxena A, Bester L, Shan L, Perera M, Gibbs P, Meteling B, et al. A systematic review on the safety and efficacy of yttrium-90 radioembolization for unresectable, chemorefractory colorectal cancer liver metastases. J Cancer Res Clin Oncol. 2014;140:537–47.PubMedCrossRefGoogle Scholar
  96. 96.
    Kennedy AS, Ball D, Cohen SJ, Cohn M, Coldwell DM, Drooz A, et al. Multicenter evaluation of the safety and efficacy of radioembolization in patients with unresectable colorectal liver metastases selected as candidates for 90Y resin microspheres. J Gastrointest Oncol. 2015;6:134–42.PubMedPubMedCentralGoogle Scholar
  97. 97.
    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.PubMedCrossRefGoogle Scholar
  98. 98.
    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 patients. Am J Clin Oncol. 2008;31:271–9.PubMedCrossRefGoogle Scholar
  99. 99.
    Giammarile F, Bodei L, Chiesa C, Flux G, Forrer F, Kraeber-Bodere F, et al. EANM procedure guideline for the treatment of liver cancer and liver metastases with intra-arterial radioactive compounds. Eur J Nucl Med Mol Imaging. 2011;38:1393–406.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Shepherd FA, Rotstein LE, Houle S, Yip TC, Paul K, Sniderman KW. A phase I dose escalation trial of yttrium-90 microspheres in the treatment of primary hepatocellular carcinoma. Cancer. 1992;70:2250–4.PubMedCrossRefGoogle Scholar
  101. 101.
    Yan ZP, Lin G, Zhao HY, Dong YH. An experimental study and clinical pilot trials on yttrium-90 glass microspheres through the hepatic artery for treatment of primary liver cancer. Cancer. 1993;72:3210–5.PubMedCrossRefGoogle Scholar
  102. 102.
    Lau WY, Leung WT, Ho S, Cotton LA, Ensminger WD, Shapiro B. Treatment of inoperable hepatocellular carcinoma with intrahepatic arterial yttrium-90 microspheres: a phase I and II study. Br J Cancer. 1994;70:994–9.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Andrews JC, Walker SC, Ackermann RJ, Cotton LA, Ensminger WD, Shapiro B. Hepatic radioembolization with yttrium-90 containing glass microspheres: preliminary results and clinical follow-up. J Nucl Med. 1994;35:1637–44.PubMedGoogle Scholar
  104. 104.
    Mahnken AH. Current status of transarterial radioembolization. World J Radiol. 2016;8:449–59.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Nijsen JFW, Seppenwoolde JH, Havenith T, Bos C, Bakker CJG, Van het Schip AD. Liver tumors: MR imaging of radioactive holmium microspheres – Phantom and rabbit study. Radiology. 2004;231:491–9.PubMedCrossRefGoogle Scholar
  106. 106.
    Seppenwoolde JH, Nijsen JFW, Bartels LW, Zielhuis SW, Van het Schip AD, Bakker CJ. Internal radiation therapy of liver tumors: qualitative and quantitative magnetic resonance imaging of the biodistribution of holmium-loaded microspheres in animal models. Magn Reson Med. 2004;53:76–84.CrossRefGoogle Scholar
  107. 107.
    De Wit TC, Xiao J, Nijsen JF, Van het Schip FD, Staelens SG, Van Rijk PP, Beekman FJ. Hybrid scatter correction applied to quantitative holmium-166 SPECT. Phys Med Biol. 2006;51:4773–87.PubMedCrossRefGoogle Scholar
  108. 108.
    Zielhuis SW, Nijsen JFW, De Roos R, Krijger GC, Van Rijk PP, Hennink WE, et al. Production of GMP-grade radioactive holmium loaded poly(l-lactic acid) microspheres for clinical application. Int J Pharm. 2006;311:69–74.PubMedCrossRefGoogle Scholar
  109. 109.
    Zielhuis SW, Nijsen JFW, Krijger GC, Van het Schip AD, Hennink WE. Holmium-loaded poly(L-lactic acid) microspheres: in vitro degradation study. Biomacromolecules. 2006;7:2217–23.PubMedCrossRefGoogle Scholar
  110. 110.
    Bult W, Vente MA, Zonnenberg BA, Van het Schip AD, Nijsen JF. Microsphere radioembolization of liver malignancies: current developments. Q J Nucl Med Mol Imaging. 2009;53:325–35.PubMedGoogle Scholar
  111. 111.
    Elschot M, Nijsen JF, Dam AJ, de Jong HW. Quantitative evaluation of scintillation camera imaging characteristics of isotopes used in liver radioembolization. PLoS One. 2011;6:e26174.  https://doi.org/10.1371/journal.pone.0026174.. Epub 2011 Nov 3CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Nijsen JFW, Rook D, Brandt CJWM, Meijer R, Dullens H, Zonnenberg BA, et al. Targeting of liver tumour in rats by selective delivery of holmium-166 loaded microspheres: a biodistribution study. Eur J Nucl Med. 2001;28:743–9.PubMedCrossRefGoogle Scholar
  113. 113.
    Zielhuis SW, Nijsen JFW, Seppenwoolde JH, Bakker CJG, Krijger GC, Dullens HF, et al. Long-term toxicity of holmium-loaded poly(L-lactic acid) microspheres in rats. Biomaterials. 2007;28:4591–9.PubMedCrossRefGoogle Scholar
  114. 114.
    Vente MAD, Nijsen JFW, De Wit TC, Seppenwoolde JH, Krijger GC, Seevinck PR, et al. Clinical effects of transcatheter hepatic arterial embolization with holmium-166 poly(L-lactic acid) microspheres in healthy pigs. Eur J Nucl Med Mol Imaging. 2008;35:1259–71.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Smits ML, Nijsen JF, van den Bosch MA, Lam MG, Vente MA, Mali WP, et al. Holmium-166 radioembolisation in patients with unresectable, chemorefractory liver metastases (HEPAR trial): a phase 1, dose-escalation study. Lancet Oncol. 2012;13:1025–34.PubMedCrossRefGoogle Scholar
  116. 116.
    Braat AJAT, Prince JF, van Rooij R, Bruijnen RCG, van den Bosch MAAJ, Lam MGEH. Safety analysis of holmium-166 microsphere scout dose imaging during radioembolisation work-up: a cohort study. Eur Radiol. 2018;28:920–8.PubMedCrossRefGoogle Scholar
  117. 117.
    Prince JF, van den Bosch MAAJ, Nijsen JFW, Smits MLJ, van den Hoven AF et al. Efficacy of radioembolization with holmium-166 microspheres in salvage patients with liver metastases: a phase 2 study. J Nucl Med. 2017. pii: jnumed.117.197194.  https://doi.org/10.2967/jnumed.117.197194. Epub ahead of printPubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Federica Guidoccio
    • 1
  • Giuseppe Boni
    • 2
  • Duccio Volterrani
    • 1
  • Giuliano Mariani
    • 1
  1. 1.Regional Center of Nuclear Medicine, Department of Translational Research and Advanced Technologies in Medicine and SurgeryUniversity of PisaPisaItaly
  2. 2.Regional Center of Nuclear MedicineUniversity Hospital of PisaPisaItaly

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