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Ytrrium-90 transarterial radioembolization in patients with gastrointestinal malignancies

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Abstract

Transarterial radioembolization (TARE) with yttrium-90 (Y90) is a promising alternative strategy to treat liver tumors and liver metastasis from colorectal cancer (CRC), as it selectively delivers radioactive isotopes to the tumor via the hepatic artery, sparring surrounding liver tissue. The landscape of TARE indications is constantly evolving. This strategy is considered for patients with hepatocellular carcinoma (HCC) with liver-confined disease and preserved liver function in whom neither TACE nor systemic therapy is possible. In patients with liver metastases from CRC, TARE is advised when other chemotherapeutic options have failed. Recent phase III trials have not succeeded to prove benefit in overall survival; however, it has helped to better understand the patients that may benefit from TARE based on subgroup analysis. New strategies and treatment combinations are being investigated in ongoing clinical trials. The aim of this review is to summarize the clinical applications of TARE in patients with gastrointestinal malignancies.

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References

  1. Li H, Wu F, Duan M, Zhang G. Drug-eluting bead transarterial chemoembolization (TACE) vs conventional TACE in treating hepatocellular carcinoma patients with multiple conventional TACE treatments history: a comparison of efficacy and safety. Med. 2019;98(21): e15314. https://doi.org/10.1097/MD.0000000000015314.

    Article  CAS  Google Scholar 

  2. Tr M, Or G. Hepatic artery catheterization for liver perfusion. Arch Surg. 1961;82(3):423–5. https://doi.org/10.1001/archsurg.1961.01300090093018.

    Article  Google Scholar 

  3. Ariel IM. Treatment of inoperable primary pancreatic and liver cancer by the intra-arterial administration of radioactive isotopes (y90 radiating microspheres). Ann Surg. 1965;162(2):267–78. https://doi.org/10.1097/00000658-196508000-00018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Simon N, Warner R, Baron M, Rudavsky A. Intra-arterial irradiation of carcinoid tumors of the liver. Am J Roentgenol. 1968;102:552–61.

    Article  CAS  Google Scholar 

  5. Anderson JH, Angerson WJ, Willmott N, Kerr DJ, McArdle CS, Cooke TG. Regional delivery of microspheres to liver metastases: the effects of particle size and concentration on intrahepatic distribution. Br J Cancer. 1991;64:1031. https://doi.org/10.1038/bjc.1991.459.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Meade VM, Burton MA, Gray BN, Self GW. Distribution of different sized microspheres in experimental hepatic tumours. Eur J Cancer Clin Oncol. 1987;23:37–41. https://doi.org/10.1016/0277-5379(87)90416-0.

    Article  CAS  PubMed  Google Scholar 

  7. Saini A, Wallace A, Alzubaidi S, et al. History and evolution of yttrium-90 radioembolization for hepatocellular carcinoma. J Clin Med. 2019. https://doi.org/10.3390/jcm8010055.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Gholam PM, Iyer R, Johnson MS. Multidisciplinary management of patients with unresectable hepatocellular carcinoma: a critical appraisal of current evidence. Cancers (Basel). 2019;11(6):873. https://doi.org/10.3390/cancers11060873.

    Article  CAS  Google Scholar 

  9. Giammarile F, Bodei L, Chiesa C, 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(7):1393–406. https://doi.org/10.1007/s00259-011-1812-2.

    Article  CAS  PubMed  Google Scholar 

  10. 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.

    Article  PubMed  Google Scholar 

  11. Smits ML, Nijsen JF, van den Bosch MA, et al. Holmium-166 radioembolisation in patients with unresectable, chemorefrac-tory liver metastases (HEPAR trial): a phase 1, dose-escalation study [published correction appears in Lancet Oncol. 2012 Nov;13(11):e464]. Lancet Oncol. 2012;13(10):1025–34. https://doi.org/10.1016/S1470-2045(12)70334-0.

    Article  CAS  PubMed  Google Scholar 

  12. Kavali PK, Gandhi RT. Suvranu Ganguli. Yttrium-90 radioembolization mapping and therapy. Endovasc Today. 2016;15(4):66–71.

    Google Scholar 

  13. Klimkowski S, Baker JC, Brown DB. Red flags, pitfalls, and cautions in Y90 radiotherapy. Tech Vasc Interv Radiol. 2019;22(2):63–9. https://doi.org/10.1053/j.tvir.2019.02.005 (Epub 27 Feb 2019, PMID: 31079712).

    Article  PubMed  Google Scholar 

  14. Riaz A, Awais R, Salem R. Side effects of yttrium-90 radioembolization. Front Oncol. 2014;4:198. https://doi.org/10.3389/fonc.2014.00198.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Vogel A, Cervantes I, Chau B, Daniele J, Llovet T, Meyer J-C, Nault U, Neumann J, Ricke B, et al. Hepatocellular carcinoma: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018;29(Suppl 4):iv238–55.

    Article  CAS  PubMed  Google Scholar 

  16. The Cancer of the Liver Italian Program (CLIP) investigators. A new prognostic system for hepatocellular carcinoma: a retrospective study of 435 patients: the Cancer of the Liver Italian Program (CLIP) investigators. Hepatology. 1998;28(3):751.

  17. Salem R, Gilbertsen M, Butt Z, et al. Increased quality of life among hepatocellular carcinoma patients treated with radio-embolization, compared with chemoembolization. Clin Gastroenterol Hepatol. 2013;11(10):1358-1365.e1. https://doi.org/10.1016/j.cgh.2013.04.028.

    Article  PubMed  Google Scholar 

  18. Jakobs TF, Saleem S, Atassi B, Reda E, Lewandowski RJ, Yaghmai V, et al. Fibrosis, portal hypertension, and hepatic volume changes induced by intra-arterial radiotherapy with 90yttrium microspheres. Dig Dis Sci. 2008;53(9):2556–63. https://doi.org/10.1007/s10620-007-0148-z (Epub 2 008 Jan 31).

    Article  CAS  PubMed  Google Scholar 

  19. Titano J, Voutsinas N, Kim E. The role of radioembolization in bridging and downstaging hepatocellular carcinoma to curative therapy. Semin Nucl Med. 2019;49(3):189–96. https://doi.org/10.1053/j.semnuclmed.2019.01.003 (Epub 2019 Feb 23).

    Article  PubMed  Google Scholar 

  20. Teo JY, Goh BK, Cheah FK, Allen JC, Lo RH, Bg DC, et al. Underlying liver disease influences volumetric changes in the spared hemiliver after selective internal radia- tion therapy with 90Y in patients with hepatocellular carcinoma. J Digest Dis. 2014;15(8):444–50. https://doi.org/10.1111/1751-2980.12162.

    Article  CAS  Google Scholar 

  21. Vouche M, Lewandowski RJ, Atassi R, Memon K, Gates VL, Ryu RK, et al. Radiation lobectomy: time-dependent analysis of future liver remained in unresecable liver cancer as a bridge to resection. J Hepatol. 2013;59(5):1029–36. https://doi.org/10.1016/j.jhep.2013.06.015 (Epub 25 Jun 2013).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Riaz A, Gates VL, Atassi B, et al. Radiation segmentectomy: a novel approach to increase safety and efficacy of radioembo-lization. Int J Radiat Oncol Biol Phys. 2011;79(1):163–71. https://doi.org/10.1016/j.ijrobp.2009.10.062.

    Article  PubMed  Google Scholar 

  23. Vouche M, Habib A, Ward TJ, et al. Unresectable solitary hepatocellular carcinoma not amenable to radiofrequency ablation: multicenter radiology–pathology correlation and survival of radiation segmentectomy. Hepatology. 2014;60(1):192.

    Article  PubMed  Google Scholar 

  24. Parikh ND, Waljee AK, Singal AG. Downstaging hepatocellular carcinoma: a systematic review and pooled analysis. Liver Transpl. 2015;21(9):1142–52. https://doi.org/10.1002/lt.24169.

    Article  PubMed  Google Scholar 

  25. Soin AS, Bhangui P, Kataria T, Baijal SS, Piplani T, Gautam D, et al. Experience with LDLT in patients with hepatocellular carcinoma and portal vein tumor thrombosis postdownstaging. Transplantation. 2020. https://doi.org/10.1097/TP.0000000000003162.

    Article  PubMed  Google Scholar 

  26. Salem R, Gordon AC, Mouli S, et al. Y90 radioembolization significantly prolongs time to progression compared with chemoembolization in patients with hepatocellular carcinoma. Gastroenterology. 2016;151(6):1155-1163.e2. https://doi.org/10.1053/j.gastro.2016.08.029.

    Article  PubMed  Google Scholar 

  27. 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(11):1632–8. https://doi.org/10.1016/j.jvir.2013.07.026.

    Article  PubMed  Google Scholar 

  28. Ettorre GM, Levi Sandri GB, Laurenzi A, Colasanti M, Meniconi RL, Lionetti R, et al. Yttrium-90 radioemboli-zation for hepatocellular carcinoma prior to liver transplantation. World J Surg. 2017;41(1):241–9. https://doi.org/10.1007/s00268-016-3682.

    Article  PubMed  Google Scholar 

  29. Agopian VG, Harlander-Locke MP, Ruiz RM, Klintmalm GB, Senguttuvan S, Florián SS, et al. Impact of pretransplant bridging locoregional therapy for patients with hepatocellular carcinoma within milan criteria undergoing liver trans-plantation: analysis of 3601 patients from the US Multicenter HCC Transplant Consortium. Ann Surg. 2017;266(3):525–35. https://doi.org/10.1097/SLA.0000000000002381.

    Article  PubMed  Google Scholar 

  30. Lobo L, Yakoub D, Picado O, Ripat C, Péndola F, Sharma R, et al. Unresectable hepatocellular carcinoma: radioembolization versus chemoembolization: a systematic review and meta-analysis. Cardiovasc Intervent Radiol. 2016;39:1580–8. https://doi.org/10.1007/s00270-016-1426-y.

    Article  PubMed  Google Scholar 

  31. Ludwig JM, Zhang D, Xiong M, Kim HS. Meta-analysis: adjusted indirect comparison of drug-eluting bead transarterial chemoembolization versus 90Y-radioembolization for hepatocellular carcinoma. Eur Radiol. 2017;27(5):2031–41. https://doi.org/10.1007/s00330-016-4548-3.

    Article  PubMed  Google Scholar 

  32. Salem R, Lewandowski RJ, Kulik L, et al. Radioembolization results in longer time-to-progression and reduced toxicity compared with chemoembolization in patients with hepatocellular carcinoma. Gastroenterology. 2011;140:497–507.

    Article  PubMed  Google Scholar 

  33. Kumasi A, Acharya SK, Singh SP, Arora A, Dhiman RK, Aggarwal R, et al. 2019 Update of indian national association for study of the liver consensus on prevention, diagnosis, and management of hepatocellular carcinoma in india: the Puri II Recommendations. J Clin Exp Hepatol. 2020;10(1):43–80. https://doi.org/10.1016/j.jceh.2019.09.007 (Epub 23 Sep 2019).

    Article  Google Scholar 

  34. Riaz A, Gabr A, Abouchaleh N, et al. Radioembolization for hepatocellular carcinoma: statistical confirmation of improved survival in responders by landmark analyses. Hepatology. 2018;67:873–83.

    Article  PubMed  Google Scholar 

  35. European Association for the Study of the Liver. Electronic address: easloffice@easloffice.eu; European Association for the Study of the Liver. EASL Clinical Practice Guidelines: Management of hepatocellular carcinoma [published correction ap-pears in J Hepatol. 2019 Apr;70(4):817]. J Hepatol. 2018;69(1):182–236. https://doi.org/10.1016/j.jhep.2018.03.019

  36. 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(R)): assessment of hepatic arterial embolization. Cardiovasc Intervent Radiol. 2006;29:522–9.

    Article  PubMed  Google Scholar 

  37. Salem R, Lewandowski R, Roberts C, Goin J, Thurston K, Abouljoud M, Courtney A. Use of Yttrium-90 glass micro-spheres (therasphere) for the treatment of unresectable hepatocellular carcinoma in patients with portal vein thrombosis. J Vasc Interv Radiol. 2004;15:335–45. https://doi.org/10.1097/01.RVI.0000123319.20705.92.

    Article  PubMed  Google Scholar 

  38. Kulik LM, Carr BI, Mulcahy MF, Lewandowski RJ, Atassi B, Ryu RK, Sato KT, Benson A, Nemcek AA, Gates VL, et al. Safety and efficacy of 90Y radiotherapy for hepatocellular carcinoma with and without portal vein thrombosis. Hepatology. 2008;47:71–81. https://doi.org/10.1002/hep.21980.

    Article  PubMed  Google Scholar 

  39. Salem R, Lewandowski RJ, Mulcahy MF, Riaz A, Ryu RK, Ibrahim S, Atassi B, Baker T, Gates V, Miller FH, et al. Radioembolization for hepatocellular carcinoma using Yttrium-90 microspheres: a comprehensive report of long-term outcomes. Gastroenterology. 2010;138:52–64. https://doi.org/10.1053/j.gastro.2009.09.006.

    Article  CAS  PubMed  Google Scholar 

  40. Mazzaferro V, Sposito C, Bhoori S, Romito R, Chiesa C, Morosi C, Maccauro M, Marchianò A, Bongini M, Lanocita R, et al. Yttrium-90 radioembolization for intermediate-advanced hepatocellular carcinoma: a phase 2 study. Hepatology. 2013;57:1826–37. https://doi.org/10.1002/hep.26014.

    Article  CAS  PubMed  Google Scholar 

  41. Pracht M, Edeline J, Lenoir L, Latournerie M, Mesbash AO, et al. Ipsilateral portal vein tumor thrombosis treated with Yttrium-90 glass microbes-here radioembolization: preliminary results. Int J Hepatol. 2013. https://doi.org/10.1155/2013/827649.

    Article  PubMed  PubMed Central  Google Scholar 

  42. She WH, Cheung TT, Yau TC, Chan AC, Chok KS, Chu FS, et al. Survival analysis of transarterial radioembolization with Yttrium-90 for hepatocellular carcinoma patients with HBV infection. Hepatobiliary Surg Nutr. 2014;3:185–93.

    PubMed  PubMed Central  Google Scholar 

  43. Somma F, Stoia V, Serra N, D’Angelo R, Gatta G, Fiore F. Yttrium-90 trans-arterial radioembolization in advanced-stage HCC: The impact of portal vein thrombosis on survival. PLoS ONE. 2019;14(5):e0216935.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Cardarelli-Leite L, Chung J, Klass D, et al. Ablative transarterial radioembolization improves survival in patients with HCC and portal vein tumor thrombus. Cardiovasc Intervent Radiol. 2020;43(3):411–22. https://doi.org/10.1007/s00270-019-02404-5.

    Article  PubMed  Google Scholar 

  45. Spreafico C, Sposito C, Vaiani M, Cascella T, Bhoori S, Morosidad C, et al. J Hepatol. 2018;68(4):724–32. https://doi.org/10.1016/j.jhep.2017.12.026.

    Article  PubMed  Google Scholar 

  46. Kim PH, Choi SH, Kim JH, Park SH. Comparison of radioembolization and sorafenib for the treatment of hepatocellular carcinoma with portal vein tumor thrombosis: a systematic review and meta-analysis of safety and efficacy. Korean J Radiol. 2019;20(3):385–98. https://doi.org/10.3348/kjr.2018.0496.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Viagrain V, Pereira H, Assenat E, Guiu B, Llonca AD, Pageaux GP, et al. Efficacy and safety of selective internal radiotherapy with yttrium-90 resin microspheres compared with sorafenib in locally advanced and inoperable hepatocellular carcinoma (SARAH): an open-label randomised controlled phase 3 trial. Lancet oncol. 2017;18(12):1624–36. https://doi.org/10.1016/S1470-2045(17)30683-6.

    Article  Google Scholar 

  48. Chow PKH, Gandhi M, Tan SB, Khin MW, Khasbazar A, Ong J, et al. SIRveNIB: selective internal radiation therapy versus sorafenib in Asia-Pacific patients with hepatocellular carcinoma. J Clin Oncol. 2018;36(19):1913–21. https://doi.org/10.1200/JCO.2017.76.0892.

    Article  CAS  PubMed  Google Scholar 

  49. Ricke J, Klümpen HJ, Amthauer H, et al. Impact of combined selective internal radiation therapy and sorafenib on survival in advanced hepatocellular carcinoma. J Hepatol. 2019;71(6):1164–74. https://doi.org/10.1016/j.jhep.2019.08.006.

    Article  CAS  PubMed  Google Scholar 

  50. Venerito M, Pech M, Canbay A, et al. NEMESIS: noninferiority, individual-patient metaanalysis of selective internal radi-ation therapy with 90Y resin microspheres versus sorafenib in advanced hepatocellular carcinoma. J Nucl Med. 2020;61(12):1736–42. https://doi.org/10.2967/jnumed.120.242933.

    Article  CAS  PubMed  Google Scholar 

  51. Chauhan N, Bukovcan J, Boucher E, et al. Intra-Arterial theraSphere Yttrium-90 glass microspheres in the treatment of patients with unresectable hepatocellular carcinoma: protocol for the STOP-HCC Phase 3 randomized controlled trial. JMIR Res Protoc. 2018;7(8):e11234. https://doi.org/10.2196/11234.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Fernandez FG, Drebin JA, Linehan DC, Dehdashti F, Siegel BA, Strasberg SM. Five-year survival after resection of hepatic metastases from colorectal cancer in patients screened by positron emission tomography with F-18 fluorodeoxyglucose (FDG-PET). Ann Surg. 2004;240(3):438–50. https://doi.org/10.1097/01.sla.0000138076.72547.b1.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Van Hazel G, Blackwell A, Anderson J, et al. Randomised phase 2 trial of SIR-spheres plus fluorouracil/leucovorin chemo-therapy versus fluorouracil/leucovorin chemotherapy alone in advanced colorectal cancer. J Surg Oncol. 2004;88(2):78–85.

    Article  PubMed  Google Scholar 

  54. van Hazel GA, Heinemann V, Sharma NK, et al. SIRFLOX: randomized phase III trial comparing first-line mFOLFOX6 (plus or minus bevacizumab) versus mFOLFOX6 (plus or minus bevacizumab) plus selective internal radiation therapy in patients with metastatic colorectal cáncer [published correction appears in J Clin Oncol. 2016 Nov 20;34(33):4059]. J Clin Oncol. 2016;34(15):1723–31. https://doi.org/10.1200/JCO.2015.66.1181.

    Article  CAS  PubMed  Google Scholar 

  55. Wasan HS, Gibbs P, Sharma NK, et al. First-line selective internal radiotherapy plus chemotherapy versus chemotherapy alone in patients with liver metastases from colorectal cancer (FOXFIRE, SIRFLOX, and FOXFIRE-Global): a combined analysis of three multicentre, randomised, phase 3 trials. Lancet Oncol. 2017;18(9):1159–71. https://doi.org/10.1016/S1470-2045(17)30457-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Wolsenholme J, Fusco F, Gray AM, Moschandreas J, Virdee PS, Love S, et al. Quality of life in the FOXFIRE, SIRFLOX and FOXFIRE-globa; Randomised trials of selective internal radiotherapy for metastatic colorectal cancer. Int J Cancer. 2019. https://doi.org/10.1002/ijc.32828.

    Article  Google Scholar 

  57. Gibbs P, Heinemann V, Sharma NK, et al. Effect of primary tumor side on survival outcomes in untreated patients with metastatic colorectal cancer when selective internal radiation therapy is added to chemotherapy: combined analysis of two randomized controlled studies. Clin Colorectal Cancer. 2018;17(4):e617–29. https://doi.org/10.1016/j.clcc.2018.06.001.

    Article  PubMed  Google Scholar 

  58. Stintzing S, Tejpar S, Gibbs P, Thiebach L, Lenz HJ. Understanding the role of primary tumor localisation in colorectal cancer treatment and outcomes. Eur J Cancer. 2017;84:69–80. https://doi.org/10.1016/j.ejca.2017.07.016.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Wasan H, Sharma R, Heinemann V, et al. FOXFIRE-SIRFLOX-FOXFIRE global prospective randomised studies of first-line selective internal radiotherapy (SIRT) in patients with liver metastases from colorectal cancer: KRAS mutation and tumour site analysis. Ann Oncol. 2017;28:v615.

    Article  Google Scholar 

  60. Mulcahy MF, Mahvash A, Pracht M, et al. Radioembolization with chemotherapy for colorectal liver metastases: a randomized, open-label, international, multicenter Phase III Trial [published online ahead of print, 2021 Sep 20]. J Clin Oncol. 2021. https://doi.org/10.1200/JCO.21.01839.

    Article  PubMed  Google Scholar 

  61. Rostambeigi N, Dekarske AS, Austin EE, et al. Cost effectiveness of radioembolization compared with conventional transarterial chemoembolization for treatment of hepatocellular carcinoma. J Vasc Interv Radiol. 2014;25:1075–84.

    Article  PubMed  Google Scholar 

  62. Lentz RW, Messersmith WA. Transarterial radioembolization in patients with unresectable colorectal cancer liver me-tastases [published online ahead of print, 2021 Sep 20]. J Clin Oncol. 2021. https://doi.org/10.1200/JCO.21.01993.

    Article  PubMed  Google Scholar 

  63. Van Cutsem E, Cervantes A, Adam R, et al. ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol. 2016;27(8):1386–422. https://doi.org/10.1093/annonc/mdw235.

    Article  PubMed  Google Scholar 

  64. Hendlisz A, Van den Eynde M, Peeters M, Maleux G, Lam-bert B, Vannoote J, et al. Phase III trial comparing protracted intravenous fluorouracil infusion alone or with yttrium-90 resin microspheres radioembolization for liver-limited metastatic colo-rectal cancer refractory to standard chemotherapy. J Clin Oncol. 2010;28:3687–94.

    Article  CAS  PubMed  Google Scholar 

  65. Gray BN, Anderson JE, Burton MA, et al. Regression of liver metastases following treatment with yttrium-90 microspheres. Aust N Z J Surg. 1992;62(2):105–10. https://doi.org/10.1111/j.1445-2197.1992.tb00006.x.

    Article  CAS  PubMed  Google Scholar 

  66. Cosimelli M, Golfieri R, Cagol PP, et al. Multi-centre phase II clinical trial of yttrium-90 resin microspheres alone in unre-sectable, chemotherapy refractory colorectal liver metastases. Br J Cancer. 2010;103(3):324–31. https://doi.org/10.1038/sj.bjc.6605770.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Cianni R, Urigo C, Notarianni E, et al. Radioembolisation using yttrium 90 (Y-90) in patients affected by unresectable hepatic metastases. Radiol Med. 2010;115(4):619–33. https://doi.org/10.1007/s11547-010-0496-1.

    Article  CAS  PubMed  Google Scholar 

  68. Sofocleous CT, Violari EG, Sotirchos VS, et al. Radioembolization as a salvage therapy for heavily pretreated patients with colorectal cancer liver metastases: factors that affect outcomes. Clin Colorectal Cancer. 2015;14(4):296–305. https://doi.org/10.1016/j.clcc.2015.06.003.

    Article  PubMed  PubMed Central  Google Scholar 

  69. Lewandowski RJ, Memon K, Mulcahy MF, et al. Twelve-year experience of radioembolization for colorectal hepatic metas-tases in 214 patients: survival by era and chemotherapy. Eur J Nucl Med Mol Imaging. 2014;41(10):1861–9. https://doi.org/10.1007/s00259-014-2799-2.

    Article  CAS  PubMed  Google Scholar 

  70. Kennedy A, Cohn M, Coldwell DM, et al. Updated survival outcomes and analysis of long-term survivors from the MORE study on safety and efficacy of radioembolization in patients with unresectable colorectal cancer liver metastases [published correction appears in J Gastrointest Oncol. 2018 Apr;9(2):E13-E14]. J Gastrointest Oncol. 2017;8(4):614–24. https://doi.org/10.2103/jgo.2017.03.10.

    Article  PubMed  PubMed Central  Google Scholar 

  71. Case MD, Ghodadra A, Novelli PM, et al. KRAS status and survival in multicenter study of RAS mutations (MURAS) in patients with colorectal liver metastases receiving Y90 radioembolization treatment. J Clin Oncol. 2020. https://doi.org/10.1097/SLA.0b013e3182a5025a.

    Article  Google Scholar 

  72. Lahti SJ, Xing M, Zhang D, et al. kras status as an independent prognostic factor for survival after yttrium-90 radioemboli-zation therapy for unresectable colorectal cancer liver metastases. J Vasc Interv Radiol. 2015;26:1102–11.

    Article  PubMed  Google Scholar 

  73. Magnetta MJ, Ghodadra A, Lahti SJ, et al. Connecting cancer biology and clinical outcomes to imaging in KRAS mutant and wild-type colorectal cancer liver tumors following selective internal radiation therapy with yttrium-90. Abdom Radiol (NY). 2017;42:451–9.

    Article  Google Scholar 

  74. Bester L, Meteling B, Pocock N, et al. Radioembolization versus standard care of hepatic metastases: comparative retro-spective cohort study of survival outcomes and adverse events in salvage patients. J Vasc Interv Radiol. 2012;23:96–105.

    Article  PubMed  Google Scholar 

  75. Seidensticker R, Denecke T, Kraus P, 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. 2012;35:1066–73.

    Article  PubMed  Google Scholar 

  76. Fahmueller YN, Nagel D, Hoffmann RT, et al. Predictive and prognostic value of circulating nucleosomes and serum bi-omarkers in patients with metastasized colorectal cancer undergoing Selective Internal Radiation Therapy. BMC Cancer. 2012;12:5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Fahmueller YN, Nagel D, Hoffmann RT, et al. Immunogenic cell death biomarkers HMGB1, RAGE, and DNAse indicate response to radioembolization therapy and prognosis in colorectal cancer patients. Int J Cancer. 2013;132:2349–58.

    Article  CAS  PubMed  Google Scholar 

  78. Carpizo DR, Gensure RH, Yu X, et al. Pilot study of angiogenic response to yttrium-90 radioembolization with resin mi-crospheres. J Vasc Interv Radiol. 2014;25:297-306.e1.

    Article  PubMed  Google Scholar 

  79. Tohme S, Sukato D, Chalhoub D, et al. Neutrophil-lymphocyte ratio is a simple and novel biomarker for prediction of sur-vival after radioembolization for metastatic colorectal cancer. Ann Surg Oncol. 2015;22:1701–2170.

    Article  PubMed  Google Scholar 

  80. de Baere T, Tselikas L, Yevich S, et al. The role of image-guided therapy in the management of colorectal cancer metastatic disease. Eur J Cancer. 2017;75:231–42. https://doi.org/10.1016/j.ejca.2017.01.010.

    Article  PubMed  Google Scholar 

  81. Campbell SR, Balagamwala EH, Woody NM, Stephans KL. Multimodality management of colorectal liver oligometastases. Appl Rad Oncol. 2019;8(3):9–16.

    Google Scholar 

  82. Ray CE, Edwards A, Smith MT. Metaanalysis of survival, complications, and imaging response following chemotherapy-based transarterial therapy in patients with unresectable intrahepatic cholangiocarcinoma. J Vasc Interv Radiol. 2013;24(8):1218–26.

    Article  PubMed  Google Scholar 

  83. 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(1):120–7. https://doi.org/10.1016/j.ejso.2014.09.007.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Roayaie S, Guarrera JV, Ye MQ, et al. Aggressive surgical treatment of intrahepatic cholangiocarcinoma: predictors of out-comes. J Am Coll Surg. 1998;187(4):365–72. https://doi.org/10.1016/s1072-7515(98)00203-8.

    Article  CAS  PubMed  Google Scholar 

  85. Valle J, Wasan H, Palmer DH, et al. Cisplatin plus gemcitabine versus gemcitabine for biliary tract cancer. N Engl J Med. 2010;362(14):1273–81. https://doi.org/10.1056/NEJMoa0908721.

    Article  CAS  PubMed  Google Scholar 

  86. Mouli S, Memon K, Baker T. Yttrium-90 radioembolization for intrahepatic cholangiocarcinoma: safety, response, and survival analysis. J Vasc Interv Radiol. 2013;24(8):1227–34.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Martinez BK, Flanders V, Gupta NK, Natarajan K, Underhill MP, Cooke J. Development of a Y90 radioembolization program in a community hospital setting for treatment of metastatic and primary liver tumors. J Vasc Interv Radiol. 2013;24(5):759.e32-759.e33.

    Google Scholar 

  88. Zhen Y, Liu B, Chang Z, Ren H, Liu Z, Zheng J. A pooled analysis of transarterial radioembolization with yttrium-90 mi-crospheres for the treatment of unresectable intrahepatic cholangiocarcinoma. Onco Targets Ther. 2019;12:4489–98. https://doi.org/10.2147/OTT.S202875.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. White J, Carolan-Rees G, Dale M, et al. Yttrium-90 transarterial radioembolization for chemotherapy-refractory intrahe-patic cholangiocarcinoma: a prospective, Observational Study. J Vasc Interv Radiol. 2019;30(8):1185–92. https://doi.org/10.1016/j.jvir.2019.03.018.

    Article  PubMed  Google Scholar 

  90. Akinwande O, Shah V, Mills A, et al. Chemoembolization versus radioembolization for the treatment of unresectable in-trahepatic cholangiocarcinoma in a single institution image-based efficacy and comparative toxicity. Hepat Oncol. 2017;4(3):75–81. https://doi.org/10.2217/hep-2017-0005.

    Article  PubMed  PubMed Central  Google Scholar 

  91. Mosconi C, Solaini L, Vara G, et al. Transarterial chemoembolization and radioembolization for unresectable intrahepatic cholangiocarcinoma-a systemic review and meta-analysis. Cardiovasc Intervent Radiol. 2021;44(5):728–38. https://doi.org/10.1007/s00270-021-02800-w.

    Article  PubMed  Google Scholar 

  92. Köhler M, Harders F, Lohöfer F, et al. Prognostic factors for overall survival in advanced intrahepatic cholangiocarcinoma treated with Yttrium-90 radioembolization. J Clin Med. 2019;9(1):56. https://doi.org/10.3390/jcm9010056.

    Article  CAS  PubMed Central  Google Scholar 

  93. Nezami N, Camacho JC, Kokabi N, El-Rayes BF, Kim HS. Phase Ib trial of gemcitabine with yttrium-90 in patients with hepatic metastasis of pancreatobiliary origin. J Gastrointest Oncol. 2019;10(5):944–56. https://doi.org/10.21037/jgo.2019.05.10.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Edeline J, Touchefeu Y, Guiu B, et al. Radioembolization plus chemotherapy for first-line treatment of locally advanced intrahepatic cholangiocarcinoma: a phase 2 clinical trial. JAMA Oncol. 2020;6(1):51–9. https://doi.org/10.1001/jamaoncol.2019.3702.

    Article  PubMed  Google Scholar 

  95. Helmberger T, Golfieri R, Pech M, et al. Clinical application of trans-arterial radioembolization in hepatic malignancies in Europe: first results from the prospective Multicentre Observational Study CIRSE Registry for SIR-Spheres Therapy (CIRT). Cardiovasc Intervent Radiol. 2021;44(1):21–35. https://doi.org/10.1007/s00270-020-02642-y.

    Article  PubMed  Google Scholar 

  96. Kim AY, Frantz S, Brower J, Akhter N. Radioembolization with Yttrium-90 microspheres for the treatment of liver metastases of pancreatic adenocarcinoma: a multicenter analysis. J Vasc Interv Radiol. 2019;30(3):298-304.e2. https://doi.org/10.1016/j.jvir.2018.09.020.

    Article  PubMed  Google Scholar 

  97. Kayaleh R, Krzyston H, Rishi A, et al. Transarterial radioembolization treatment of pancreatic cancer patients with liver-dominant metastatic disease using Yttrium-90 glass microspheres: a single-institution retrospective study. J Vasc Interv Radiol. 2020;31(7):1060–8. https://doi.org/10.1016/j.jvir.2019.11.037.

    Article  PubMed  Google Scholar 

  98. Cao C, Yan TD, Morris DL, Bester L. Radioembolization with yttrium-90 microspheres for pancreatic cancer liver metastases: results from a pilot study. Tumori. 2010;96(6):955–8.

    Article  CAS  PubMed  Google Scholar 

  99. Michl M, Haug AR, Jakobs TF, et al. Radioembolization with Yttrium-90 microspheres (SIRT) in pancreatic cancer patients with liver metastases: efficacy, safety and prognostic factors. Oncology. 2014;86(1):24–32. https://doi.org/10.1159/000355821.

    Article  CAS  PubMed  Google Scholar 

  100. Kim AY, Unger K, Wang H, Pishvaian MJ. Incorporating Yttrium-90 trans-arterial radioembolization (TARE) in the treatment of metastatic pancreatic adenocarcioma: a single center experience. BMC Cancer. 2016;16:492. https://doi.org/10.1186/s12885-016-2552-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Kennedy A, Bester L, Salem R, et al. Role of hepatic intra-arterial therapies in metastatic neuroendocrine tumors (NET): guidelines from the NET-Liver-Metastases Consensus Conference. HPB (Oxford). 2015;17(1):29–37. https://doi.org/10.1111/hpb.12326.

    Article  Google Scholar 

  102. Nigri G, Petrucciani N, Debs T, et al. Treatment options for PNET liver metastases: a systematic review. World J Surg Oncol. 2018;16:142. https://doi.org/10.1186/s12957-018-1446-y.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Delle Fave G, O’Toole D, Sundin A, et al. ENETS consensus guidelines update for gastroduodenal neuroendocrine neo-plasms. Neuroendocrinology. 2016;103(2):119–24. https://doi.org/10.1159/000443168.

    Article  CAS  PubMed  Google Scholar 

  104. Egger ME, Armstrong E, Martin RC 2nd, et al. Transarterial chemoembolization vs radioembolization for neuroendocrine liver metastases: a multi-institutional analysis. J Am Coll Surg. 2020;230(4):363–70. https://doi.org/10.1016/j.jamcollsurg.2019.12.026.

    Article  PubMed  Google Scholar 

  105. Jia Z, Wang W. Yttrium-90 radioembolization for unresectable metastatic neuroendocrine liver tumor: a systematic review. Eur J Radiol. 2018;100:23–9. https://doi.org/10.1016/j.ejrad.2018.01.012.

    Article  PubMed  Google Scholar 

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Acknowledgements

Figure 1 was created with BioRender, with the unvaluable help of Isabel Solares (Internal Medicine service, 12 de Octubre University Hospital, Madrid, Spain).

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Authors and Affiliations

  1. Department of Medical Oncology, Hospital Universitario La Paz, 28046, Madrid, Spain

    D. Viñal

  2. Department of General and Digestive Surgery, Hospital Universitario del Henares, Coslada, 28822, Madrid, Spain

    A. Minaya-Bravo

  3. Universidad Francisco de Vitoria, Madrid, Spain

    A. Minaya-Bravo

  4. Department of General and Digestive Surgery, Hospital Universitario La Paz, 28046, Madrid, Spain

    I. Prieto

  5. Department of Medical Oncology, Hospital Universitario La Paz, IdiPAZ, Catedra UAM-AMGEN, CIBERONC, 28046, Madrid, Spain

    J. Feliu & N. Rodriguez-Salas

  6. Paseo de la Castellana 261, 28045, Madrid, Spain

    D. Viñal

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Conceptualization, NRS; writing—original draft preparation, DV, AM, NRS; writing—review and editing, MIP, JF; supervision, JF, NRS; All authors have read and agreed to the published version of the manuscript.

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Viñal, D., Minaya-Bravo, A., Prieto, I. et al. Ytrrium-90 transarterial radioembolization in patients with gastrointestinal malignancies. Clin Transl Oncol 24, 796–808 (2022). https://doi.org/10.1007/s12094-021-02745-z

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