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A guide to 90Y radioembolization and its dosimetry

Published:November 28, 2019DOI:https://doi.org/10.1016/j.ejmp.2019.09.236

      Highlights

      • Radioembolization’s clinical steps can be simplified into 6 steps.
      • Most dosimetric factors have been investigated within this review.
      • Current clinical dosimetric methods as well as the emerging methods are discussed in detail.
      • The newly emerging dosimetry is based on SPECT/CT or PET/CT imaging modalities.

      Abstract

      Radioembolization gains continuous traction as a primarily palliative radiation treatment for hepatic tumours. A form of nuclear medicine therapy, Yttrium-90 containing microspheres are catheter guided and injected into the right, left, or a specifically selected hepatic artery. A multitude of comprehensive planning steps exist to ensure a thorough and successful treatment. Clear clinical and physiological guidelines have been established and nuclear imaging is used to plan and verify dose distributions. Radioembolization’s treatment rationale is based on tumour and blood vessel dynamics that allow a targeted treatment approach. However, radioembolization’s dosimetry is grossly oversimplified. In fact, the currently utilized clinical dosimetric standards (e.g. partition method) have persisted since the 1990s. Moreover, the multitude of radioembolization’s intertwining components lies disjointed within the literature. Particularly relevant to new readers, this review provides a methodical guide that presents the treatment rationale behind every clinical step. The emerging dosimetry methods and its factors are further discussed to provide a comprehensive review on an essential research direction.

      Keywords

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      References

        • Roeske J.C.
        • Aydogan B.
        • Bardies M.
        • Humm J.L.
        Small-scale dosimetry: challenges and future directions.
        Semin Nucl Med. 2008; 38: 367-383
        • Kennedy A.S.
        • Nutting C.
        • Coldwell D.
        • Gaiser J.
        • Drachenberg C.
        Pathologic response and microdosimetry of (90)Y microspheres in man: review of four explanted whole livers.
        Int J Radiat Oncol Biol Phys. 2004; 60: 1552-1563
      1. Package insert-therapshere yttrium-90 glass microspheres. Biocompatibles UK Ltd, A BTG International Group Company.

      2. Package insert: sir-spheres microspheres. Sirtex Medical Limited; 2016. pp 9.

        • 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: 1393-1406
        • Cremonesi M.
        • Chiesa C.
        • Strigari L.
        • Ferrari M.
        • Botta F.
        • Guerriero F.
        • et al.
        Radioembolization of hepatic lesions from a radiobiology and dosimetric perspective.
        Front Oncol. 2014; 4: 210
        • Coldwell D.
        • Sangro B.
        • Wasan H.
        • Salem R.
        • Kennedy A.
        General selection criteria of patients for radioembolization of liver tumors: an international working group report.
        Am J Clin Oncol. 2011; 34: 337-341
        • Dezarn W.A.
        • Cessna J.T.
        • DeWerd L.A.
        • Feng W.
        • Gates V.L.
        • Halama J.
        • et al.
        American Association of Physicists in M: Recommendations of the American Association of Physicists in Medicine on dosimetry, imaging, and quality assurance procedures for 90Y microsphere brachytherapy in the treatment of hepatic malignancies.
        Med Phys. 2011; 38: 4824-4845
        • Ahmadzadehfar H.
        • Meyer C.
        • Pieper C.C.
        • Bundschuh R.
        • Muckle M.
        • Gartner F.
        • et al.
        Evaluation of the delivered activity of yttrium-90 resin microspheres using sterile water and 5 % glucose during administration.
        EJNMMI Res. 2015; 5: 54
        • Koran M.E.
        • Stewart S.
        • Baker J.C.
        • Lipnik A.J.
        • Banovac F.
        • Omary R.A.
        • et al.
        Five percent dextrose maximizes dose delivery of Yttrium-90 resin microspheres and reduces rates of premature stasis compared to sterile water.
        Biomed Rep. 2016; 5: 745-748
        • Kis B.
        • Mills M.
        • Hoffe S.E.
        Hepatic radioembolization from transradial access: initial experience and comparison to transfemoral access.
        Diagn Interv Radiol. 2016; 22: 444-449
        • Lau W.Y.
        • Kennedy A.S.
        • Kim Y.H.
        • Lai H.K.
        • Lee R.C.
        • Leung T.W.
        • et al.
        Patient selection and activity planning guide for selective internal radiotherapy with yttrium-90 resin microspheres.
        Int J Radiat Oncol Biol Phys. 2012; 82: 401-407
        • Kennedy A.
        • Nag S.
        • Salem R.
        • Murthy R.
        • McEwan A.J.
        • Nutting C.
        • 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: 13-23
        • Riaz A.
        • Awais R.
        • Salem R.
        Side effects of yttrium-90 radioembolization.
        Front Oncol. 2014; 4: 198
        • Salem R.
        • Thurston K.G.
        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: 1251-1278
        • Kennedy A.
        Radioembolization of hepatic tumors.
        J Gastrointest Oncol. 2014; 5: 178-189
        • Vollmar B.
        • Menger M.D.
        The hepatic microcirculation: mechanistic contributions and therapeutic targets in liver injury and repair.
        Physiol Rev. 2009; 89: 1269-1339
        • Bierman H.R.
        • Byron Jr., R.L.
        • 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. 1951; 12: 107-131
        • Van de Wiele C.
        • Maes A.
        • Brugman E.
        • D'Asseler Y.
        • De Spiegeleer B.
        • Mees G.
        • et al.
        SIRT of liver metastases: physiological and pathophysiological considerations.
        Eur J Nucl Med Mol Imaging. 2012; 39: 1646-1655
        • van den Hoven A.F.
        • Smits M.L.
        • de Keizer B.
        • van Leeuwen M.S.
        • van den Bosch M.A.
        • Lam M.G.
        Identifying aberrant hepatic arteries prior to intra-arterial radioembolization.
        Cardiovasc Intervent Radiol. 2014; 37: 1482-1493
        • Michels N.A.
        Newer anatomy of the liver and its variant blood supply and collateral circulation.
        Am J Surg. 1966; 112: 337-347
        • Vesselle G.
        • Petit I.
        • Boucebci S.
        • Rocher T.
        • Velasco S.
        • Tasu J.P.
        Radioembolization with yttrium-90 microspheres work up: Practical approach and literature review.
        Diagn Interv Imaging. 2015; 96: 547-562
        • Uliel L.
        • Royal H.D.
        • Darcy M.D.
        • Zuckerman D.A.
        • Sharma A.
        • Saad N.E.
        From the angio suite to the gamma-camera: vascular mapping and 99mTc-MAA hepatic perfusion imaging before liver radioembolization–a comprehensive pictorial review.
        J Nucl Med. 2012; 53: 1736-1747
        • Braat A.J.
        • Smits M.L.
        • Braat M.N.
        • van den Hoven A.F.
        • Prince J.F.
        • de Jong H.W.
        • et al.
        (9)(0)Y hepatic radioembolization: an update on current practice and recent developments.
        J Nucl Med. 2015; 56: 1079-1087
        • Kao Y.H.
        • Magsombol B.M.
        • Toh Y.
        • Tay K.H.
        • Chow P.
        • Goh A.S.
        • et al.
        Personalized predictive lung dosimetry by technetium-99m macroaggregated albumin SPECT/CT for yttrium-90 radioembolization.
        EJNMMI Res. 2014; 4: 33
        • Hamami M.E.
        • Poeppel T.D.
        • Muller S.
        • Heusner T.
        • Bockisch A.
        • Hilgard P.
        • et al.
        SPECT/CT with 99mTc-MAA in radioembolization with 90Y microspheres in patients with hepatocellular cancer.
        J Nucl Med. 2009; 50: 688-692
        • Allred J.D.
        • Niedbala J.
        • Mikell J.K.
        • Owen D.
        • Frey K.A.
        • Dewaraja Y.K.
        The value of (99m)Tc-MAA SPECT/CT for lung shunt estimation in (90)Y radioembolization: a phantom and patient study.
        EJNMMI Res. 2018; 8: 50
        • Barentsz M.W.
        • Vente M.A.
        • Lam M.G.
        • Smits M.L.
        • Nijsen J.F.
        • Seinstra B.A.
        • et al.
        Technical solutions to ensure safe yttrium-90 radioembolization in patients with initial extrahepatic deposition of (99m)technetium-albumin macroaggregates.
        Cardiovasc Intervent Radiol. 2011; 34: 1074-1079
        • Lopez B.
        • Mahvash A.
        • Lam M.
        • Kappadath S.C.
        Calculation of lung mean dose and quantification of error for (90) Y-microsphere radioembolization using (99m) Tc-MAA SPECT/CT and diagnostic chest CT.
        Med Phys. 2019; 46: 3929-3940
        • Strasberg S.M.
        • Belghiti J.
        • Clavien P.-A.
        • Gadzijev E.
        • Garden J.O.
        • Lau W.-Y.
        • et al.
        The Brisbane 2000 terminology of liver anatomy and resections.
        HPB. 2000; 2: 333-339
        • Germain T.
        • Favelier S.
        • Cercueil J.P.
        • Denys A.
        • Krause D.
        • Guiu B.
        Liver segmentation: practical tips.
        Diagn Interv Imaging. 2014; 95: 1003-1016
        • Vouche M.
        • Lewandowski R.J.
        • Atassi R.
        • Memon K.
        • Gates V.L.
        • Ryu R.K.
        • et al.
        Radiation lobectomy: time-dependent analysis of future liver remnant volume in unresectable liver cancer as a bridge to resection.
        J Hepatol. 2013; 59: 1029-1036
        • Seidensticker R.
        • Seidensticker M.
        • Damm R.
        • Mohnike K.
        • Schutte K.
        • Malfertheiner P.
        • et al.
        Hepatic toxicity after radioembolization of the liver using (90)Y-microspheres: sequential lobar versus whole liver approach.
        Cardiovasc Intervent Radiol. 2012; 35: 1109-1118
        • Lewandowski R.J.
        • Donahue L.
        • Chokechanachaisakul A.
        • Kulik L.
        • Mouli S.
        • Caicedo J.
        • et al.
        (90) Y radiation lobectomy: Outcomes following surgical resection in patients with hepatic tumors and small future liver remnant volumes.
        J Surg Oncol. 2016; 114: 99-105
        • Riaz A.
        • Gates V.L.
        • Atassi B.
        • Lewandowski R.J.
        • Mulcahy M.F.
        • Ryu R.K.
        • et al.
        Radiation segmentectomy: a novel approach to increase safety and efficacy of radioembolization.
        Int J Radiat Oncol Biol Phys. 2011; 79: 163-171
        • Wondergem M.
        • Smits M.L.
        • Elschot M.
        • de Jong H.W.
        • Verkooijen H.M.
        • van den Bosch M.A.
        • et al.
        99mTc-macroaggregated albumin poorly predicts the intrahepatic distribution of 90Y resin microspheres in hepatic radioembolization.
        J Nucl Med. 2013; 54: 1294-1301
        • Gulec S.A.
        • Mesoloras G.
        • Stabin M.
        Dosimetric techniques in 90Y-microsphere therapy of liver cancer: The MIRD equations for dose calculations.
        J Nucl Med. 2006; 47: 1209-1211
        • Ho S.
        • Lau W.Y.
        • Leung T.W.
        • Chan M.
        • Johnson P.J.
        • Li A.K.
        Clinical evaluation of the partition model for estimating radiation doses from yttrium-90 microspheres in the treatment of hepatic cancer.
        Eur J Nucl Med. 1997; 24: 293-298
        • Leung T.W.
        • Lau W.Y.
        • Ho S.K.
        • Ward S.C.
        • Chow J.H.
        • Chan M.S.
        • et al.
        Radiation pneumonitis after selective internal radiation treatment with intraarterial 90yttrium-microspheres for inoperable hepatic tumors.
        Int J Radiat Oncol Biol Phys. 1995; 33: 919-924
        • Leung W.T.
        • Lau W.Y.
        • Ho S.K.
        • Chan M.
        • Leung N.W.
        • Lin J.
        • et al.
        Measuring lung shunting in hepatocellular carcinoma with intrahepatic-arterial technetium-99m macroaggregated albumin.
        J Nucl Med. 1994; 35: 70-73
        • Smits M.L.
        • Elschot M.
        • Sze D.Y.
        • Kao Y.H.
        • Nijsen J.F.
        • Iagaru A.H.
        • et al.
        Radioembolization dosimetry: the road ahead.
        Cardiovasc Intervent Radiol. 2015; 38: 261-269
        • Vauthey J.N.
        • Abdalla E.K.
        • Doherty D.A.
        • Gertsch P.
        • Fenstermacher M.J.
        • Loyer E.M.
        • et al.
        Body surface area and body weight predict total liver volume in Western adults.
        Liver Transpl. 2002; 8: 233-240
        • Lam M.G.
        • Louie J.D.
        • Abdelmaksoud M.H.
        • Fisher G.A.
        • Cho-Phan C.D.
        • Sze D.Y.
        Limitations of body surface area-based activity calculation for radioembolization of hepatic metastases in colorectal cancer.
        J Vasc Interv Radiol. 2014; 25: 1085-1093
        • Grosser O.S.
        • Ulrich G.
        • Furth C.
        • Pech M.
        • Ricke J.
        • Amthauer H.
        • et al.
        Intrahepatic activity distribution in radioembolization with yttrium-90-labeled resin microspheres using the body surface area method–a less than perfect model.
        J Vasc Interv Radiol. 2015; 26: 1615-1621
        • Kao Y.H.
        • Tan E.H.
        • Ng C.E.
        • Goh S.W.
        Clinical implications of the body surface area method versus partition model dosimetry for yttrium-90 radioembolization using resin microspheres: a technical review.
        Ann Nucl Med. 2011; 25: 455-461
        • Ho S.
        • Lau W.Y.
        • Leung T.W.
        • Chan M.
        • Ngar Y.K.
        • Johnson P.J.
        • et al.
        Partition model for estimating radiation doses from yttrium-90 microspheres in treating hepatic tumours.
        Eur J Nucl Med. 1996; 23: 947-952
        • Kao Y.H.
        • Hock Tan A.E.
        • Burgmans M.C.
        • Irani F.G.
        • Khoo L.S.
        • Gong Lo R.H.
        • et al.
        Image-guided personalized predictive dosimetry by artery-specific SPECT/CT partition modeling for safe and effective 90Y radioembolization.
        J Nucl Med. 2012; 53: 559-566
        • Mikell J.K.
        • Mahvash A.
        • Siman W.
        • Baladandayuthapani V.
        • Mourtada F.
        • Kappadath S.C.
        Selective internal radiation therapy with yttrium-90 glass microspheres: biases and uncertainties in absorbed dose calculations between clinical dosimetry models.
        Int J Radiat Oncol Biol Phys. 2016; 96: 888-896
        • Hashikin N.A.A.
        • Yeong C.H.
        • Guatelli S.
        • Abdullah B.J.J.
        • Ng K.H.
        • Malaroda A.
        • et al.
        Systematic investigation on the validity of partition model dosimetry for (90)Y radioembolization using Monte Carlo simulation.
        Phys Med Biol. 2017; 62: 7342-7356
        • Oda M.
        • Yokomori H.
        • Han J.Y.
        Regulatory mechanisms of hepatic microcirculation.
        Clin Hemorheol Microcirc. 2003; 29: 167-182
        • Fox R.A.
        • Klemp P.F.
        • Egan G.
        • Mina L.L.
        • Burton M.A.
        • Gray B.N.
        Dose distribution following selective internal radiation therapy.
        Int J Radiat Oncol Biol Phys. 1991; 21: 463-467
        • Campbell A.M.
        • Bailey I.H.
        • Burton M.A.
        Analysis of the distribution of intra-arterial microspheres in human liver following hepatic yttrium-90 microsphere therapy.
        Phys Med Biol. 2000; 45: 1023-1033
        • Campbell A.M.
        • Bailey I.H.
        • Burton M.A.
        Tumour dosimetry in human liver following hepatic yttrium-90 microsphere therapy.
        Phys Med Biol. 2001; 46: 487-498
        • Hogberg J.
        • Rizell M.
        • Hultborn R.
        • Svensson J.
        • Henrikson O.
        • Molne J.
        • et al.
        Heterogeneity of microsphere distribution in resected liver and tumour tissue following selective intrahepatic radiotherapy.
        EJNMMI Res. 2014; 4: 48
        • Hogberg J.
        • Rizell M.
        • Hultborn R.
        • Svensson J.
        • Henrikson O.
        • Molne J.
        • et al.
        Increased absorbed liver dose in Selective Internal Radiation Therapy (SIRT) correlates with increased sphere-cluster frequency and absorbed dose inhomogeneity.
        EJNMMI Phys. 2015; 2: 10
        • Lam M.G.
        • Louie J.D.
        • Iagaru A.H.
        • Goris M.L.
        • Sze D.Y.
        Safety of repeated yttrium-90 radioembolization.
        Cardiovasc Intervent Radiol. 2013; 36: 1320-1328
        • Lewandowski R.J.
        • Minocha J.
        • Memon K.
        • Riaz A.
        • Gates V.L.
        • Ryu R.K.
        • et al.
        Sustained safety and efficacy of extended-shelf-life (90)Y glass microspheres: long-term follow-up in a 134-patient cohort.
        Eur J Nucl Med Mol Imaging. 2014; 41: 486-493
        • Walrand S.
        • Hesse M.
        • Chiesa C.
        • Lhommel R.
        • Jamar F.
        The low hepatic toxicity per Gray of 90Y glass microspheres is linked to their transport in the arterial tree favoring a nonuniform trapping as observed in posttherapy PET imaging.
        J Nucl Med. 2014; 55: 135-140
        • Walrand S.
        • Hesse M.
        • Jamar F.
        • Lhommel R.
        A hepatic dose-toxicity model opening the way toward individualized radioembolization planning.
        J Nucl Med. 2014; 55: 1317-1322
        • Gulec S.A.
        • Sztejnberg M.L.
        • Siegel J.A.
        • Jevremovic T.
        • Stabin M.
        Hepatic structural dosimetry in (90)Y microsphere treatment: a Monte Carlo modeling approach based on lobular microanatomy.
        J Nucl Med. 2010; 51: 301-310
        • Pasciak A.S.
        • Bourgeois A.C.
        • Bradley Y.C.
        A microdosimetric analysis of absorbed dose to tumor as a function of number of microspheres per unit volume in 90Y radioembolization.
        J Nucl Med. 2016; 57: 1020-1026
        • Van Audenhaege K.
        • Van Holen R.
        • Vandenberghe S.
        • Vanhove C.
        • Metzler S.D.
        • Moore S.C.
        Review of SPECT collimator selection, optimization, and fabrication for clinical and preclinical imaging.
        Med Phys. 2015; 42: 4796-4813
        • Bailey D.L.
        • Willowson K.P.
        Quantitative SPECT/CT: SPECT joins PET as a quantitative imaging modality.
        Eur J Nucl Med Mol Imaging. 2014; 41: S17-S25
        • Siman W.
        • Mikell J.K.
        • Kappadath S.C.
        Practical reconstruction protocol for quantitative (90)Y bremsstrahlung SPECT/CT.
        Med Phys. 2016; 43: 5093
        • Rong X.
        • Du Y.
        • Frey E.C.
        A method for energy window optimization for quantitative tasks that includes the effects of model-mismatch on bias: application to Y-90 bremsstrahlung SPECT imaging.
        Phys Med Biol. 2012; 57: 3711-3725
        • Li T.
        • Ao E.C.I.
        • Lambert B.
        • Brans B.
        • Vandenberghe S.
        • Mok G.S.P.
        Quantitative imaging for targeted radionuclide therapy dosimetry – technical review.
        Theranostics. 2017; 7: 4551-4565
        • Elschot M.
        • Lam M.G.
        • van den Bosch M.A.
        • Viergever M.A.
        • de Jong H.W.
        Quantitative Monte Carlo-based 90Y SPECT reconstruction.
        J Nucl Med. 2013; 54: 1557-1563
        • Rong X.
        • Du Y.
        • Ljungberg M.
        • Rault E.
        • Vandenberghe S.
        • Frey E.C.
        Development and evaluation of an improved quantitative (90)Y bremsstrahlung SPECT method.
        Med Phys. 2012; 39: 2346-2358
        • Dewaraja Y.K.
        • Chun S.Y.
        • Srinivasa R.N.
        • Kaza R.K.
        • Cuneo K.C.
        • Majdalany B.S.
        • et al.
        Improved quantitative (90) Y bremsstrahlung SPECT/CT reconstruction with Monte Carlo scatter modeling.
        Med Phys. 2017; 44: 6364-6376
        • Lhommel R.
        • Goffette P.
        • Van den Eynde M.
        • Jamar F.
        • Pauwels S.
        • Bilbao J.I.
        • et al.
        Yttrium-90 TOF PET scan demonstrates high-resolution biodistribution after liver SIRT.
        Eur J Nucl Med Mol Imaging. 2009; 36: 1696
        • Gates V.L.
        • Esmail A.A.
        • Marshall K.
        • Spies S.
        • Salem R.
        Internal pair production of 90Y permits hepatic localization of microspheres using routine PET: proof of concept.
        J Nucl Med. 2011; 52: 72-76
        • Willowson K.P.
        • Tapner M.
        • Team Q.I.
        • Bailey D.L.
        A multicentre comparison of quantitative (90)Y PET/CT for dosimetric purposes after radioembolization with resin microspheres: the QUEST Phantom Study.
        Eur J Nucl Med Mol Imaging. 2015; 42: 1202-1222
        • Yue J.
        • Mauxion T.
        • Reyes D.K.
        • Lodge M.A.
        • Hobbs R.F.
        • Rong X.
        • et al.
        Comparison of quantitative Y-90 SPECT and non-time-of-flight PET imaging in post-therapy radioembolization of liver cancer.
        Med Phys. 2016; 43: 5779
        • Elschot M.
        • Vermolen B.J.
        • Lam M.G.
        • de Keizer B.
        • van den Bosch M.A.
        • de Jong H.W.
        Quantitative comparison of PET and Bremsstrahlung SPECT for imaging the in vivo yttrium-90 microsphere distribution after liver radioembolization.
        PLoS One. 2013; 8e55742
        • Kao Y.H.
        • Steinberg J.D.
        • Tay Y.S.
        • Lim G.K.
        • Yan J.
        • Townsend D.W.
        • et al.
        Post-radioembolization yttrium-90 PET/CT - part 1: diagnostic reporting.
        EJNMMI Res. 2013; 3: 56
        • Od J.
        A review of 3D image-based dosimetry, technical considerations and emerging perspectives in (90)Y microsphere therapy.
        J Diagn Imaging Ther. 2015; 2: 1-34
        • Mikell J.K.
        • Mahvash A.
        • Siman W.
        • Mourtada F.
        • Kappadath S.C.
        Comparing voxel-based absorbed dosimetry methods in tumors, liver, lung, and at the liver-lung interface for (90)Y microsphere selective internal radiation therapy.
        EJNMMI Phys. 2015; 2: 16
        • Gallio E.
        • Richetta E.
        • Finessi M.
        • Stasi M.
        • Pellerito R.E.
        • Bisi G.
        • et al.
        Calculation of tumour and normal tissue biological effective dose in (90)Y liver radioembolization with different dosimetric methods.
        Phys Med. 2016; 32: 1738-1744
        • Lanconelli N.
        • Pacilio M.
        • Lo Meo S.
        • Botta F.
        • Di Dia A.
        • Aroche A.T.
        • et al.
        A free database of radionuclide voxel S values for the dosimetry of nonuniform activity distributions.
        Phys Med Biol. 2012; 57: 517-533
        • Campbell J.M.
        • Wong C.O.
        • Muzik O.
        • Marples B.
        • Joiner M.
        • Burmeister J.
        Early dose response to yttrium-90 microsphere treatment of metastatic liver cancer by a patient-specific method using single photon emission computed tomography and positron emission tomography.
        Int J Radiat Oncol Biol Phys. 2009; 74: 313-320
        • Kao Y.H.
        A clinical dosimetric perspective uncovers new evidence and offers new insight in favor of 99mTc-macroaggregated albumin for predictive dosimetry in 90Y resin microsphere radioembolization.
        J Nucl Med. 2013; 54: 2191-2192
        • Lam M.G.
        • Wondergem M.
        • Elschot M.
        • Smits M.L.
        Reply: A clinical dosimetric perspective uncovers new evidence and offers new insight in favor of 99mTc-macroaggregated albumin for predictive dosimetry in 90Y resin microsphere radioembolization.
        J Nucl Med. 2013; 54: 2192-2193
        • Ulrich G.
        • Dudeck O.
        • Furth C.
        • Ruf J.
        • Grosser O.S.
        • Adolf D.
        • et al.
        Predictive value of intratumoral 99mTc-macroaggregated albumin uptake in patients with colorectal liver metastases scheduled for radioembolization with 90Y-microspheres.
        J Nucl Med. 2013; 54: 516-522
        • Fournier L.
        • Ammari S.
        • Thiam R.
        • Cuenod C.A.
        Imaging criteria for assessing tumour response: RECIST, mRECIST, Cheson.
        Diagn Interv Imaging. 2014; 95: 689-703
        • Kao Y.H.
        Results confounded by a disregard for basic dose-response radiobiology.
        J Nucl Med. 2013; 54: 1682-1683
        • Lam M.G.
        • Smits M.L.
        Value of 99mTc-macroaggregated albumin SPECT for radioembolization treatment planning.
        J Nucl Med. 2013; 54: 1681-1682
        • 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: 255-263
        • 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 with 90Y TOF PET/CT posttreatment dosimetry in radioembolization of hepatocellular carcinoma: a quantitative agreement comparison.
        J Nucl Med. 2016; 57: 1672-1678
        • Song Y.S.
        • Paeng J.C.
        • Kim H.C.
        • Chung J.W.
        • Cheon G.J.
        • Chung J.K.
        • et al.
        PET/CT-based dosimetry in 90Y-microsphere selective internal radiation therapy: single cohort comparison with pretreatment planning on (99m)Tc-MAA imaging and correlation with treatment efficacy.
        Medicine (Baltimore). 2015; 94e945
        • D'Arienzo M.
        • Chiaramida P.
        • Chiacchiararelli L.
        • Coniglio A.
        • Cianni R.
        • Salvatori R.
        • et al.
        90Y PET-based dosimetry after selective internal radiotherapy treatments.
        Nucl Med Commun. 2012; 33: 633-640
        • D'Arienzo M.
        • Filippi L.
        • Chiaramida P.
        • Chiacchiararelli L.
        • Cianni R.
        • Salvatori R.
        • et al.
        Absorbed dose to lesion and clinical outcome after liver radioembolization with 90Y microspheres: a case report of PET-based dosimetry.
        Ann Nucl Med. 2013; 27: 676-680
        • Kao Y.H.
        • Steinberg J.D.
        • Tay Y.S.
        • Lim G.K.
        • Yan J.
        • Townsend D.W.
        • et al.
        Post-radioembolization yttrium-90 PET/CT - part 2: dose-response and tumor predictive dosimetry for resin microspheres.
        EJNMMI Res. 2013; 3: 57
        • Srinivas S.M.
        • Natarajan N.
        • Kuroiwa J.
        • Gallagher S.
        • Nasr E.
        • Shah S.N.
        • et al.
        Determination of radiation absorbed dose to primary liver tumors and normal liver tissue using post-radioembolization (90)Y PET.
        Front Oncol. 2014; 4: 255
        • Strigari L.
        • Sciuto R.
        • Rea S.
        • Carpanese L.
        • Pizzi G.
        • Soriani A.
        • et al.
        Efficacy and toxicity related to treatment of hepatocellular carcinoma with 90Y-SIR spheres: radiobiologic considerations.
        J Nucl Med. 2010; 51: 1377-1385
        • Chan K.T.
        • Alessio A.M.
        • Johnson G.E.
        • Vaidya S.
        • Kwan S.W.
        • Monsky W.
        • et al.
        Prospective trial using internal pair-production positron emission tomography to establish the yttrium-90 radioembolization dose required for response of hepatocellular carcinoma.
        Int J Radiat Oncol Biol Phys. 2018; 101: 358-365
        • Kappadath S.C.
        • Mikell J.
        • Balagopal A.
        • Baladandayuthapani V.
        • Kaseb A.
        • Mahvash A.
        Hepatocellular carcinoma tumor dose response after (90)Y-radioembolization with glass microspheres using (90)Y-SPECT/CT-based voxel dosimetry.
        Int J Radiat Oncol Biol Phys. 2018; 102: 451-461