GM-CSF, G-CSF or no cytokine therapy with anti-GD2 immunotherapy for high-risk neuroblastoma.
G-CSF
GM-CSF
anti-GD2 monoclonal antibody
cytokines
dinutuximab
dinutuximab beta
immunotherapy
naxitamab
neuroblastoma
sargramostim
Journal
International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124
Informations de publication
Date de publication:
18 Dec 2023
18 Dec 2023
Historique:
revised:
17
10
2023
received:
14
06
2023
accepted:
14
11
2023
medline:
18
12
2023
pubmed:
18
12
2023
entrez:
18
12
2023
Statut:
aheadofprint
Résumé
Colony-stimulating factors have been shown to improve anti-disialoganglioside 2 (anti-GD2) monoclonal antibody response in high-risk neuroblastoma by enhancing antibody-dependent cell-mediated cytotoxicity (ADCC). A substantial amount of research has focused on recombinant human granulocyte-macrophage colony-stimulating factor (GM-CSF) as an adjuvant to anti-GD2 monoclonal antibodies. There may be a disparity in care among patients as access to GM-CSF therapy and anti-GD2 monoclonal antibodies is not uniform. Only select countries have approved these agents for use, and even with regulatory approvals, access to these agents can be complex and cost prohibitive. This comprehensive review summarizes clinical data regarding efficacy and safety of GM-CSF, recombinant human granulocyte colony-stimulating factor (G-CSF) or no cytokine in combination with anti-GD2 monoclonal antibodies (ie, dinutuximab, dinutuximab beta or naxitamab) for immunotherapy of patients with high-risk neuroblastoma. A substantial body of clinical data support the immunotherapy combination of anti-GD2 monoclonal antibodies and GM-CSF. In contrast, clinical data supporting the use of G-CSF are limited. No formal comparison between GM-CSF, G-CSF and no cytokine has been identified. The treatment of high-risk neuroblastoma with anti-GD2 therapy plus GM-CSF is well established. Suboptimal efficacy outcomes with G-CSF raise concerns about its suitability as an alternative to GM-CSF as an adjuvant in immunotherapy for patients with high-risk neuroblastoma. While programs exist to facilitate obtaining GM-CSF and anti-GD2 monoclonal antibodies in regions where they are not commercially available, continued work is needed to ensure equitable therapeutic options are available globally.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Partner Therapeutics, Inc.
Informations de copyright
© 2023 The Authors. International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.
Références
PDQ Pediatric Treatment Editorial Board. Neuroblastoma treatment (PDQ®): health professional version. In: PDQ Cancer Information Summaries [Internet]. National Cancer Institute (US); 2023. https://www.ncbi.nlm.nih.gov/books/NBK65747/?report=classic
Smith MA, Altekruse SF, Adamson PC, Reaman GH, Seibel NL. Declining childhood and adolescent cancer mortality. Cancer. 2014;120(16):2497-2506. doi:10.1002/cncr.28748
American Cancer Society. Childhood and adolescent cancer. Cancer Statistics Center; 2018. https://cancerstatisticscenter.cancer.org/#!/childhood-cancer
Anderson J, Majzner RG, Sondel PM. Immunotherapy of neuroblastoma: facts and hopes. Clin Cancer Res. 2022;28(15):3196-3206. doi:10.1158/1078-0432.Ccr-21-1356
United Therapeutics, Corp. UNITUXIN®(dinutuximab) Injection, for Intravenous Use. Prescribing Information. United Therapeutics, Corp; 2020.
Y-mabs Therapeutics, Inc. DANYELZA®(naxitamab-gqgk) Injection, for Intravenous Use. Prescribing Information. Y-mabs Therapeutics, Inc; 2020.
EUSA Pharma. QARZIBA®(dinutuximab beta) Concentrate for Solution for Infusion. Summary of Product Characteristics. EUSA Pharma (Netherlands) BV; 2022.
Government of Canada. Drug Product Database online query: Unituxin® (dinutuximab); 2023. https://health-products.canada.ca/dpd-bdpp/
Ohara Pharmaceutical Co Ltd. Recombinant chimeric monoclonal antibody “Unituxin®” marketing authorization approval. News release. https://www.ohara-ch.co.jp/wp/wp-content/uploads/2021/06/202106_23_info_E.pdf
Y-mAbs Therapeutics Inc. Y-mAbs' DANYELZA® (naxitamab-gqgk) for the treatment of high-risk neuroblastoma approved in China. News release. https://ir.ymabs.com/news-releases/news-release-details/y-mabs-danyelzar-naxitamab-gqgk-treatment-high-risk
Y-mAbs Therapeutics Inc. Y-mAbs and Takeda announces marketing authorization in Israel for DANYELZA® (naxitamab-gqgk) for neuroblastoma. News release. https://ir.ymabs.com/news-releases/news-release-details/y-mabs-and-takeda-announces-marketing-authorization-israel
Australian Government. Australian Prescription Medicine Decision Summaries: Qarziba; 2020. https://www.tga.gov.au/resources/auspmd/qarziba
EUSA Pharma Recordati. QARZIBA® (dinutuximab beta) in the treatment of high-risk neuroblastoma [online slide deck]; 2022. https://eusadb.com/docs/EUS2143B_Commercial%20LP_V2_180322.pdf
EUSA Pharma: Recordati Group Company. BeiGene and EUSA Pharma announce China NMPA approval of QARZIBA® (dinutuximab beta) for patients with high-risk neuroblastoma. News release. https://eusapharma.com/news/beigene-and-eusa-pharma-announce-china-nmpa-approval-of-qarziba-dinutuximab-beta-for-patients-with-high-risk-neuroblastoma
Medison Pharma (Israel). QARZIBA®(dinutuximab beta) concentrate for solution for infusion. Summary of product characteristics. 2023.
McKeague K, Lyseng-Williamson KA. Dinutuximab beta in high-risk neuroblastoma: a profile of its use. Drugs Ther Perspect. 2018;34:281-287. doi:10.1007/s40267-018-0522-2
Lazarus HM, Ragsdale CE, Gale RP, Lyman GH. Sargramostim (rhu GM-CSF) as cancer therapy (systematic review) and an immunomodulator. A drug before its time? Front Immunol. 2021;12:706186. doi:10.3389/fimmu.2021.706186
Mora J. Dinutuximab for the treatment of pediatric patients with high-risk neuroblastoma. Expert Rev Clin Pharmacol. 2016;9(5):647-653. doi:10.1586/17512433.2016.1160775
Yu AL, Gilman AL, Ozkaynak MF, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med. 2010;363(14):1324-1334. doi:10.1056/NEJMoa0911123
Barker E, Mueller BM, Handgretinger R, Herter M, Yu AL, Reisfeld RA. Effect of a chimeric anti-ganglioside GD2 antibody on cell-mediated lysis of human neuroblastoma cells. Cancer Res. 1991;51(1):144-149.
Kushner BH, Cheung NK. GM-CSF enhances 3F8 monoclonal antibody-dependent cellular cytotoxicity against human melanoma and neuroblastoma. Blood. 1989;73(7):1936-1941.
Kushner BH, Cheung NK. Clinically effective monoclonal antibody 3F8 mediates nonoxidative lysis of human neuroectodermal tumor cells by polymorphonuclear leukocytes. Cancer Res. 1991;51(18):4865-4870.
Bruchelt G, Handgretinger R, Kimmig A, et al. Effects of granulocytes on human neuroblastoma cells measured by chemiluminescence and chromium-51 release assay. J Biolumin Chemilumin. 1989;3(2):93-96. doi:10.1002/bio.1170030212
Kushner BH, Cheung NK. Absolute requirement of CD11/CD18 adhesion molecules, FcRII and the phosphatidylinositol-linked FcRIII for monoclonal antibody-mediated neutrophil antihuman tumor cytotoxicity. Blood. 1992;79(6):1484-1490.
Hank JA, Robinson RR, Surfus J, et al. Augmentation of antibody dependent cell mediated cytotoxicity following in vivo therapy with recombinant interleukin 2. Cancer Res. 1990;50(17):5234-5239.
Munn DH, Cheung NK. Interleukin-2 enhancement of monoclonal antibody-mediated cellular cytotoxicity against human melanoma. Cancer Res. 1987;47(24 Pt 1):6600-6605.
Desai AV, Gilman AL, Ozkaynak MF, et al. Outcomes following GD2-directed postconsolidation therapy for neuroblastoma after cessation of random assignment on ANBL0032: a report from the Children's Oncology Group. J Clin Oncol. 2022;40(35):4107-4118. doi:10.1200/jco.21.02478
Lode HN, Valteau-Couanet D, Gray J, et al. Randomized use of anti-GD2 antibody dinutuximab beta (DB) long-term infusion with and without subcutaneous interleukin-2 (scIL-2) in high-risk neuroblastoma patients with relapsed and refractory disease: results from the SIOPEN LTI-trial [abstract]. J Clin Oncol. 2019;37:10014. doi:10.1200/JCO.2019.37.15_suppl.10014
Ladenstein R, Pötschger U, Valteau-Couanet D, et al. Interleukin 2 with anti-GD2 antibody ch14.18/CHO (dinutuximab beta) in patients with high-risk neuroblastoma (HR-NBL1/SIOPEN): a multicentre, randomised, phase 3 trial. Lancet Oncol. 2018;19(12):1617-1629. doi:10.1016/s1470-2045(18)30578-3
Ladenstein RL, Poetschger U, Valteau-Couanet D, et al. Randomization of dose-reduced subcutaneous interleukin-2 (scIL2) in maintenance immunotherapy (IT) with anti-GD2 antibody dinutuximab beta (DB) long-term infusion (LTI) in front-line high-risk neuroblastoma patients: early results from the HR-NBL1/SIOPEN trial [abstract]. J Clin Oncol. 2019;37(15 suppl):10013.
Martinez Sanz P, van Rees DJ, van Zogchel LMJ, et al. G-CSF as a suitable alternative to GM-CSF to boost dinutuximab-mediated neutrophil cytotoxicity in neuroblastoma treatment. J Immunother Cancer. 2021;9(5):e002259. doi:10.1136/jitc-2020-002259
Trapnell BC, Abe S. Colony stimulating factors. In: Janes SM, ed. Encyclopedia of Respiratory Medicine. Academic Press; 2006:540-546.
Bhattacharya P, Thiruppathi M, Elshabrawy HA, Alharshawi K, Kumar P, Prabhakar BS. GM-CSF: an immune modulatory cytokine that can suppress autoimmunity. Cytokine. 2015;75(2):261-271. doi:10.1016/j.cyto.2015.05.030
Demetri GD, Griffin JD. Granulocyte colony-stimulating factor and its receptor. Blood. 1991;78(11):2791-2808.
Peters WP, Stuart A, Affronti ML, Kim CS, Coleman RE. Neutrophil migration is defective during recombinant human granulocyte-macrophage colony-stimulating factor infusion after autologous bone marrow transplantation in humans. Blood. 1988;72(4):1310-1315.
Wolach B, van der Laan LJ, Maianski NA, et al. Growth factors G-CSF and GM-CSF differentially preserve chemotaxis of neutrophils aging in vitro. Exp Hematol. 2007;35(4):541-550. doi:10.1016/j.exphem.2006.12.008
Kownatzki E, Liehl E, Aschauer H, Uhrich S. Inhibition of chemotactic migration of human neutrophilic granulocytes by recombinant human granulocyte-macrophage colony-stimulating factor. Immunopharmacology. 1990;19(2):139-143. doi:10.1016/0162-3109(90)90049-k
Yong KL. Granulocyte colony-stimulating factor (G-CSF) increases neutrophil migration across vascular endothelium independent of an effect on adhesion: comparison with granulocyte-macrophage colony-stimulating factor (GM-CSF). Br J Haematol. 1996;94(1):40-47. doi:10.1046/j.1365-2141.1996.d01-1752.x
Griffin JD, Spertini O, Ernst TJ, et al. Granulocyte-macrophage colony-stimulating factor and other cytokines regulate surface expression of the leukocyte adhesion molecule-1 on human neutrophils, monocytes, and their precursors. J Immunol. 1990;145(2):576-584.
Rahman I, Collado Sánchez A, Davies J, et al. L-selectin regulates human neutrophil transendothelial migration. J Cell Sci. 2021;134(3):jcs250340. doi:10.1242/jcs.250340
Coleman DL, Chodakewitz JA, Bartiss AH, Mellors JW. Granulocyte-macrophage colony-stimulating factor enhances selective effector functions of tissue-derived macrophages. Blood. 1988;72(2):573-578.
Chung S, Ranjan R, Lee YG, et al. Distinct role of FoxO1 in M-CSF- and GM-CSF-differentiated macrophages contributes LPS-mediated IL-10: implication in hyperglycemia. J Leukoc Biol. 2015;97(2):327-339. doi:10.1189/jlb.3A0514-251R
Rosler B, Herold S. Lung epithelial GM-CSF improves host defense function and epithelial repair in influenza virus pneumonia - a new therapeutic strategy? Mol Cell Pediatr. 2016;3(1):29. doi:10.1186/s40348-016-0055-5
Castro-Dopico T, Fleming A, Dennison TW, et al. GM-CSF calibrates macrophage defense and wound healing programs during intestinal infection and inflammation. Cell Rep. 2020;32(1):107857. doi:10.1016/j.celrep.2020.107857
Schneider E, Petit-Bertron AF, Bricard R, et al. IL-33 activates unprimed murine basophils directly in vitro and induces their in vivo expansion indirectly by promoting hematopoietic growth factor production. J Immunol. 2009;183(6):3591-3597. doi:10.4049/jimmunol.0900328
Hornell TM, Beresford GW, Bushey A, Boss JM, Mellins ED. Regulation of the class II MHC pathway in primary human monocytes by granulocyte-macrophage colony-stimulating factor. J Immunol. 2003;171(5):2374-2383. doi:10.4049/jimmunol.171.5.2374
Chitta S, Santambrogio L, Stern LJ. GMCSF in the absence of other cytokines sustains human dendritic cell precursors with T cell regulatory activity and capacity to differentiate into functional dendritic cells. Immunol Lett. 2008;116(1):41-54. doi:10.1016/j.imlet.2007.11.013
Eksioglu EA, Mahmood SS, Chang M, Reddy V. GM-CSF promotes differentiation of human dendritic cells and T lymphocytes toward a predominantly type 1 proinflammatory response. Exp Hematol. 2007;35(8):1163-1171. doi:10.1016/j.exphem.2007.05.001
Arellano M, Lonial S. Clinical uses of GM-CSF, a critical appraisal and update. Biologics. 2008;2(1):13-27. doi:10.2147/btt.s1355
Dranoff G, Jaffee E, Lazenby A, et al. Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc Natl Acad Sci U S A. 1993;90(8):3539-3543. doi:10.1073/pnas.90.8.3539
Chaplin DD. Overview of the immune response. J Allergy Clin Immunol. 2010;125(2 Suppl 2):S3-S23. doi:10.1016/j.jaci.2009.12.980
Demers M, Wong SL, Martinod K, et al. Priming of neutrophils toward NETosis promotes tumor growth. Oncoimmunology. 2016;5(5):e1134073. doi:10.1080/2162402x.2015.1134073
Lu J, Sun K, Yang H, et al. Sepsis inflammation impairs the generation of functional dendritic cells by targeting their progenitors. Front Immunol. 2021;12:732612. doi:10.3389/fimmu.2021.732612
Arpinati M, Green CL, Heimfeld S, Heuser JE, Anasetti C. Granulocyte-colony stimulating factor mobilizes T helper 2-inducing dendritic cells. Blood. 2000;95(8):2484-2490.
Bunse CE, Tischer S, Lahrberg J, et al. Granulocyte colony-stimulating factor impairs CD8(+) T cell functionality by interfering with central activation elements. Clin Exp Immunol. 2016;185(1):107-118. doi:10.1111/cei.12794
Fukuda M, Horibe K, Furukawa K. Enhancement of in vitro and in vivo anti-tumor activity of anti-GD2 monoclonal antibody 220-51 against human neuroblastoma by granulocyte-macrophage colony-stimulating factor and granulocyte colony-stimulating factor. Int J Mol Med. 1998;2(4):471-475. doi:10.3892/ijmm.2.4.471
Ahmad A, Laborada G, Bussel J, Nesin M. Comparison of recombinant granulocyte colony-stimulating factor, recombinant human granulocyte-macrophage colony-stimulating factor and placebo for treatment of septic preterm infants. Pediatr Infect Dis J. 2002;21(11):1061-1065. doi:10.1097/00006454-200211000-00017
Beveridge RA, Miller JA, Kales AN, et al. A comparison of efficacy of sargramostim (yeast-derived RhuGM-CSF) and filgrastim (bacteria-derived RhuG-CSF) in the therapeutic setting of chemotherapy-induced myelosuppression. Cancer Invest. 1998;16(6):366-373. doi:10.3109/07357909809115775
Beveridge RA, Miller JA, Kales AN, et al. Randomized trial comparing the tolerability of sargramostim (yeast-derived RhuGM-CSF) and filgrastim (bacteria-derived RhuG-CSF) in cancer patients receiving myelosuppressive chemotherapy. Support Care Cancer. 1997;5(4):289-298.
Cheung NK, Guo H, Hu J, Tassev DV, Cheung IY. Humanizing murine IgG3 anti-GD2 antibody m3F8 substantially improves antibody-dependent cell-mediated cytotoxicity while retaining targeting in vivo. Oncoimmunology. 2012;1(4):477-486. doi:10.4161/onci.19864
Theruvath J, Menard M, Smith BAH, et al. Anti-GD2 synergizes with CD47 blockade to mediate tumor eradication. Nat Med. 2022;28(2):333-344. doi:10.1038/s41591-021-01625-x
Park JA, Cheung NV. Targets and antibody formats for immunotherapy of neuroblastoma. J Clin Oncol. 2020;38(16):1836-1848. doi:10.1200/jco.19.01410
Munn DH, Cheung NK. Phagocytosis of tumor cells by human monocytes cultured in recombinant macrophage colony-stimulating factor. J Exp Med. 1990;172(1):231-237. doi:10.1084/jem.172.1.231
Sakakura K, Takahashi H, Kaira K, et al. Relationship between tumor-associated macrophage subsets and CD47 expression in squamous cell carcinoma of the head and neck in the tumor microenvironment. Lab Invest. 2016;96(9):994-1003. doi:10.1038/labinvest.2016.70
Yu AL, Gilman AL, Ozkaynak MF, et al. Long-term follow-up of a phase III study of ch14.18 (dinutuximab) + cytokine immunotherapy in children with high-risk neuroblastoma: COG study ANBL0032. Clin Cancer Res. 2021;27(8):2179-2189. doi:10.1158/1078-0432.Ccr-20-3909
Arnold IC, Artola-Boran M, Gurtner A, et al. The GM-CSF-IRF5 signaling axis in eosinophils promotes antitumor immunity through activation of type 1 T cell responses. J Exp Med. 2020;217(12):e20190706. doi:10.1084/jem.20190706
Carretero R, Sektioglu IM, Garbi N, Salgado OC, Beckhove P, Hämmerling GJ. Eosinophils orchestrate cancer rejection by normalizing tumor vessels and enhancing infiltration of CD8(+) T cells. Nat Immunol. 2015;16(6):609-617. doi:10.1038/ni.3159
Mattei F, Andreone S, Marone G, et al. Eosinophils in the tumor microenvironment. Adv Exp Med Biol. 2020;1273:1-28. doi:10.1007/978-3-030-49270-0_1
Cheung IY, Hsu K, Cheung NK. Activation of peripheral-blood granulocytes is strongly correlated with patient outcome after immunotherapy with anti-GD2 monoclonal antibody and granulocyte-macrophage colony-stimulating factor. J Clin Oncol. 2012;30(4):426-432. doi:10.1200/jco.2011.37.6236
Igietseme JU, Zhu X, Black CM. Chapter 15 - fc receptor-dependent immunity. In: Ackerman ME, Nimmerjahn F, eds. Antibody Fc. Academic Press; 2014:269-281.
Nazha B, Inal C, Owonikoko TK. Disialoganglioside GD2 expression in solid tumors and role as a target for cancer therapy. Front Oncol. 2020;10:1000. doi:10.3389/fonc.2020.01000
Russ A, Hua AB, Montfort WR, et al. Blocking “on't eat me” signal of CD47-SIRPα in hematological malignancies, an in-depth review. Blood Rev. 2018;32(6):480-489. doi:10.1016/j.blre.2018.04.005
Kohrt HE, Houot R, Marabelle A, et al. Combination strategies to enhance antitumor ADCC. Immunotherapy. 2012;4(5):511-527. doi:10.2217/imt.12.38
Nguyen R, Moustaki A, Norrie JL, et al. Interleukin-15 enhances anti-GD2 antibody-mediated cytotoxicity in an orthotopic PDX model of neuroblastoma. Clin Cancer Res. 2019;25(24):7554-7564. doi:10.1158/1078-0432.Ccr-19-1045
Metelitsa LS, Gillies SD, Super M, Shimada H, Reynolds CP, Seeger RC. Antidisialoganglioside/granulocyte macrophage-colony-stimulating factor fusion protein facilitates neutrophil antibody-dependent cellular cytotoxicity and depends on FcgammaRII (CD32) and Mac-1 (CD11b/CD18) for enhanced effector cell adhesion and azurophil granule exocytosis. Blood. 2002;99(11):4166-4173. doi:10.1182/blood.v99.11.4166
Redlinger RE, Mailliard RB, Barksdale EM. Neuroblastoma and dendritic cell function. Semin Pediatr Surg. 2004;13(1):61-71. doi:10.1053/j.sempedsurg.2003.09.009
Shurin GV, Shurin MR, Bykovskaia S, Shogan J, Lotze MT, Barksdale EM Jr. Neuroblastoma-derived gangliosides inhibit dendritic cell generation and function. Cancer Res. 2001;61(1):363-369.
Walker SR, Ogagan PD, DeAlmeida D, Aboka AM, Barksdale EM. Neuroblastoma impairs chemokine-mediated dendritic cell migration in vitro. J Pediatr Surg. 2006;41(1):260-265. doi:10.1016/j.jpedsurg.2005.10.073
Zeng L, Li SH, Xu SY, et al. Clinical significance of a CD3/CD8-based immunoscore in neuroblastoma patients using digital pathology. Front Immunol. 2022;13:878457. doi:10.3389/fimmu.2022.878457
Cheung NK, Cheung IY, Kramer K, et al. Key role for myeloid cells: phase II results of anti-G(D2) antibody 3F8 plus granulocyte-macrophage colony-stimulating factor for chemoresistant osteomedullary neuroblastoma. Int J Cancer. 2014;135(9):2199-2205. doi:10.1002/ijc.28851
Ozkaynak MF, Gilman AL, London WB, et al. A comprehensive safety trial of chimeric antibody 14.18 with GM-CSF, IL-2, and isotretinoin in high-risk neuroblastoma patients following myeloablative therapy: Children's Oncology Group Study ANBL0931. Front Immunol. 2018;9:1355. doi:10.3389/fimmu.2018.01355
Mody R, Naranjo A, van Ryn C, et al. Irinotecan-temozolomide with temsirolimus or dinutuximab in children with refractory or relapsed neuroblastoma (COG ANBL1221): an open-label, randomised, phase 2 trial. Lancet Oncol. 2017;18(7):946-957. doi:10.1016/s1470-2045(17)30355-8
Brodeur GM, Pritchard J, Berthold F, et al. Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J Clin Oncol. 1993;11(8):1466-1477. doi:10.1200/jco.1993.11.8.1466
Mody R, Yu AL, Naranjo A, et al. Irinotecan, temozolomide, and dinutuximab with GM-CSF in children with refractory or relapsed neuroblastoma: a report from the Children's Oncology Group. J Clin Oncol. 2020;38(19):2160-2169. doi:10.1200/jco.20.00203
Lerman BJ, Li Y, Carlowicz C, et al. Progression-free survival and patterns of response in patients with relapsed high-risk neuroblastoma treated with irinotecan/temozolomide/dinutuximab/granulocyte-macrophage colony-stimulating factor. J Clin Oncol. 2023;41(3):508-516. doi:10.1200/jco.22.01273
Park JR, Bagatell R, Cohn SL, et al. Revisions to the international neuroblastoma response criteria: a consensus statement from the National Cancer Institute clinical trials planning meeting. J Clin Oncol. 2017;35(22):2580-2587. doi:10.1200/jco.2016.72.0177
Federico SM, Naranjo A, Zhang F, et al. A pilot induction regimen incorporating dinutuximab and sargramostim for the treatment of newly diagnosed high-risk neuroblastoma: a report from the Children's Oncology Group [abstract]. J Clin Oncol. 2022;40:10003.
Mora J, Chan G, Morgenstern DA, et al. Naxitamab treatment for relapsed or refractory high-risk neuroblastoma: outcomes from the first prespecified analyses of the pivotal 201 trial [poster]. Presented at: ESMO congress (European Society for Medical Oncology); September 9-13, 2022; Paris, France. Ann Oncol. 2022;33(S7):S956. doi:10.1016/j.annonc.2022.07.1017
Kushner BH, Modak S, Basu E, et al. High-dose naxitamab (humanized-3F8) plus stepped-up dosing of granulocyte-macrophage colony-stimulating factor (GM-CSF) for resistant osteomedullary neuroblastoma: major responses and outpatient treatment in a phase II trial [abstract]. Pediatr Blood Cancer. 2020;67(Suppl 4):S32.
Kushner BH, Cheung IY, Modak S, Basu EM, Roberts SS, Cheung NK. Humanized 3F8 anti-GD2 monoclonal antibody dosing with granulocyte-macrophage colony-stimulating factor in patients with resistant neuroblastoma: a phase 1 clinical trial. JAMA Oncol. 2018;4(12):1729-1735. doi:10.1001/jamaoncol.2018.4005
Modak S, Kushner BH, Mauguen A, et al. Naxitamab-based chemoimmunotherapy for resistant high-risk neuroblastoma: results of “HITS” phase II study [poster]. Presented at: ASCO annual meeting (American Society of Clinical Oncology); June 2-6, 2022; Chicago, IL. J Clin Oncol. 2022;40:10028.
Muñoz JP, Larrosa C, Chamorro S, et al. Early salvage chemo-immunotherapy with irinotecan, temozolomide and naxitamab plus GM-CSF (HITS) for patients with primary refractory high-risk neuroblastoma provide the best chance for long-term outcomes. Cancers (Basel). 2023;15(19):4837. doi:10.3390/cancers15194837
Mora J, Castañeda A, Gorostegui M, et al. Naxitamab combined with granulocyte-macrophage colony-stimulating factor as consolidation for high-risk neuroblastoma patients in first complete remission under compassionate use-updated outcome report. Cancers (Basel). 2023;15(9):2535. doi:10.3390/cancers15092535
Mora J, Castañeda A, Gorostegui M, et al. Naxitamab combined with granulocyte-macrophage colony-stimulating factor as consolidation for high-risk neuroblastoma patients in complete remission. Pediatr Blood Cancer. 2021;68(10):e29121. doi:10.1002/pbc.29121
Partner Therapeutics, Inc. LEUKINE®(Sargramostim) for Injection, for Subcutaneous or Intravenous Use. Prescribing Information. Partner Therapeutics, Inc; 2023.
Tannerpharma Group. Ptx Partnership: Leaping Beyond Boundaries. Tannerpharma Group; 2023.
Gay AN, Chang S, Rutland L, et al. Granulocyte colony stimulating factor alters the phenotype of neuroblastoma cells: implications for disease-free survival of high-risk patients. J Pediatr Surg. 2008;43(5):837-842. doi:10.1016/j.jpedsurg.2007.12.024
Hsu DM, Agarwal S, Benham A, et al. G-CSF receptor positive neuroblastoma subpopulations are enriched in chemotherapy-resistant or relapsed tumors and are highly tumorigenic. Cancer Res. 2013;73(13):4134-4146. doi:10.1158/0008-5472.Can-12-4056
Agarwal S, Lakoma A, Chen Z, et al. G-CSF promotes neuroblastoma tumorigenicity and metastasis via STAT3-dependent cancer stem cell activation. Cancer Res. 2015;75(12):2566-2579. doi:10.1158/0008-5472.Can-14-2946
Amgen Inc. NEUPOGEN®(Filgrastim) Injection, for Subcutaneous or Intravenous Use. Prescribing Information. Amgen Inc; 2023.
Qi C, Wang L, Duan G. Preoperative neutrophil-to-lymphocyte ratio (NLR) as a prognostic biomarker for patients with high-risk neuroblastoma. Asian J Surg. 2022;46:2474-2475. doi:10.1016/j.asjsur.2022.12.069
Lazic D, Kromp F, Rifatbegovic F, et al. Landscape of bone marrow metastasis in human neuroblastoma unraveled by transcriptomics and deep multiplex imaging. Cancers (Basel). 2021;13(17):4311. doi:10.3390/cancers13174311
Whittle SB, Smith V, Silverstein A, et al. Is high-risk neuroblastoma induction chemotherapy possible without G-CSF? A pilot study of safety and treatment delays in the absence of primary prophylactic hematopoietic growth factors. Pediatr Blood Cancer. 2020;67(10):e28417. doi:10.1002/pbc.28417
Ladenstein R, Valteau-Couanet D, Brock P, et al. Randomized trial of prophylactic granulocyte colony-stimulating factor during rapid COJEC induction in pediatric patients with high-risk neuroblastoma: the European HR-NBL1/SIOPEN study. J Clin Oncol. 2010;28(21):3516-3524. doi:10.1200/jco.2009.27.3524
Miśkiewicz-Migoń I, Miśkiewicz-Bujna J, Rosa M, et al. Severe, reversible acute lung injury during autologous hematopoietic stem cell mobilization after filgrastim in a child with neuroblastoma: a case report. Transplant Proc. 2020;52(9):2849-2853. doi:10.1016/j.transproceed.2020.06.027
van Woensel JB, Knoester H, Leeuw JA, van Aalderen WM. Acute respiratory insufficiency during doxorubicin, cyclophosphamide, and G-CSF therapy. Lancet. 1994;344(8924):759-760. doi:10.1016/s0140-6736(94)92253-5
Matsumura T, Maruyama-Tabata H, Kuwahara Y, Sawada T, Ikeda T. Subretinal haemorrhage after granulocyte colony-stimulating factor. Lancet. 1997;350(9074):336. doi:10.1016/s0140-6736(05)63386-7
Hara J, Nitani C, Kawamoto H, et al. A phase I/IIa study of antidisialoganglioside antibody dinutuximab in Japanese patients with neuroblastoma. J Pediatr Hematol Oncol. 2021;43(3):e358-e364. doi:10.1097/mph.0000000000001684
Mueller I, Ehlert K, Endres S, et al. Tolerability, response and outcome of high-risk neuroblastoma patients treated with long-term infusion of anti-GD(2) antibody ch14.18/CHO. MAbs. 2018;10(1):55-61. doi:10.1080/19420862.2017.1402997
European Medicines Agency. Assessment report: Dinutuximab beta. 2017 https://www.ema.europa.eu/en/documents/assessment-report/dinutuximab-beta-apeiron-epar-public-assessment-report_en.pdf
Lode H, Ehlert K, Huber S, et al. Single agent activity of the anti-GD2 antibody dinutuximab beta long-term infusion in high-risk neuroblastoma patients with relapsed and refractory disease. A multicenter phase II trial [abstract]. Pediatr Blood Cancer. 2022;69:S70.
Gray J, Moreno L, Weston R, et al. BEACON-Immuno: Results of the dinutuximab beta (dB) randomization of the BEACON-Neuroblastoma phase 2 trial-A European Innovative Therapies for Children with Cancer (ITCC)-International Society of Paediatric Oncology Europe Neuroblastoma Group (SIOPEN) trial [abstract]. J Clin Oncol. 2022;40:10002. doi:10.1200/JCO.2022.40.16_suppl.10002
Flaadt T, Lang P, Ebinger M, et al. Haploidentical stem cell transplantation and subsequent immunotherapy with antiGD2 antibody for patients with relapsed metastatic neuroblastoma [abstract]. Pediatr Blood Cancer. 2020;67(Suppl 4):S33.
Federico SM, McCarville MB, Shulkin BL, et al. A pilot trial of humanized anti-GD2 monoclonal antibody (hu14.18K322A) with chemotherapy and natural killer cells in children with recurrent/refractory neuroblastoma. Clin Cancer Res. 2017;23(21):6441-6449. doi:10.1158/1078-0432.Ccr-17-0379
Chen P, Chen F, Zhou B. Comparisons of therapeutic efficacy and safety of ipilimumab plus GM-CSF versus ipilimumab alone in patients with cancer: a meta-analysis of outcomes. Drug des Devel Ther. 2018;12:2025-2038. doi:10.2147/dddt.S154258
Correale P, Botta C, Rotundo MS, et al. Gemcitabine, oxaliplatin, levofolinate, 5-fluorouracil, granulocyte-macrophage colony-stimulating factor, and interleukin-2 (GOLFIG) versus FOLFOX chemotherapy in metastatic colorectal cancer patients: the GOLFIG-2 multicentric open-label randomized phase III trial. J Immunother. 2014;37(1):26-35. doi:10.1097/CJI.0000000000000004
Hodi FS, Lee S, McDermott DF, et al. Ipilimumab plus sargramostim vs ipilimumab alone for treatment of metastatic melanoma: a randomized clinical trial. JAMA. 2014;312(17):1744-1753. doi:10.1001/jama.2014.13943
Rini BI, Fong L, Weinberg V, Kavanaugh B, Small EJ. Clinical and immunological characteristics of patients with serologic progression of prostate cancer achieving long-term disease control with granulocyte-macrophage colony-stimulating factor. J Urol. 2006;175(6):2087-2091. doi:10.1016/s0022-5347(06)00261-8
Schmeler KM, Vadhan-Raj S, Ramirez PT, et al. A phase II study of GM-CSF and rIFN-gamma1b plus carboplatin for the treatment of recurrent, platinum-sensitive ovarian, fallopian tube and primary peritoneal cancer. Gynecol Oncol. 2009;113(2):210-215. doi:10.1016/j.ygyno.2009.02.007
Dorr RT. Clinical properties of yeast-derived versus Escherichia coli-derived granulocyte-macrophage colony-stimulating factor. Clin Ther. 1993;15(1):19-29.
Ladenstein R, Pötschger U, Valteau-Couanet D, et al. Investigation of the role of dinutuximab beta-based immunotherapy in the SIOPEN high-risk neuroblastoma 1 trial (HR-NBL1). Cancers (Basel). 2020;12(2):309. doi:10.3390/cancers12020309
ClinicalTrials.Gov. Naxitamab added to induction for newly diagnosed high-risk neuroblastoma; 2022. https://clinicaltrials.gov/ct2/show/NCT05489887
Blom T, Lurvink R, Aleven L, et al. Treatment-related toxicities during anti-GD2 immunotherapy in high-risk neuroblastoma patients. Front Oncol. 2020;10:601076. doi:10.3389/fonc.2020.601076
Mora J, Chan GC, Morgenstern DA, et al. Outpatient administration of naxitamab in combination with granulocyte-macrophage colony-stimulating factor in patients with refractory and/or relapsed high-risk neuroblastoma: Management of adverse events. Cancer Rep (Hoboken). 2023;6(1):e1627. doi:10.1002/cnr2.1627
Varo A, Castañeda Heredia A, Chamorro S, et al. Novel infusion strategy reduces severe adverse events caused by anti-GD2 monoclonal antibody naxitamab. Front Oncol. 2023;13:1164949. doi:10.3389/fonc.2023.1164949
Furman WL, McCarville B, Shulkin BL, et al. Improved outcome in children with newly diagnosed high-risk neuroblastoma treated with chemoimmunotherapy: updated results of a phase II study using hu14.18K322A. J Clin Oncol. 2022;40(4):335-344. doi:10.1200/jco.21.01375
Navid F, Sondel PM, Barfield R, et al. Phase I trial of a novel anti-GD2 monoclonal antibody, Hu14.18K322A, designed to decrease toxicity in children with refractory or recurrent neuroblastoma. J Clin Oncol. 2014;32(14):1445-1452. doi:10.1200/jco.2013.50.4423
Kushner BH, Ostrovnaya I, Cheung IY, et al. Lack of survival advantage with autologous stem-cell transplantation in high-risk neuroblastoma consolidated by anti-GD2 immunotherapy and isotretinoin. Oncotarget. 2016;7(4):4155-4166. doi:10.18632/oncotarget.6393
Mora J, Castañeda A, Flores MA, et al. The role of autologous stem-cell transplantation in high-risk neuroblastoma consolidated by anti-GD2 immunotherapy. Results of two consecutive studies. Front Pharmacol. 2020;11:575009. doi:10.3389/fphar.2020.575009
Cheung NK, Cheung IY, Kushner BH, et al. Murine anti-GD2 monoclonal antibody 3F8 combined with granulocyte-macrophage colony-stimulating factor and 13-cis-retinoic acid in high-risk patients with stage 4 neuroblastoma in first remission. J Clin Oncol. 2012;30(26):3264-3270. doi:10.1200/jco.2011.41.3807
Kushner BH, LaQuaglia MP, Modak S, et al. MYCN-amplified stage 2/3 neuroblastoma: excellent survival in the era of anti-G(D2) immunotherapy. Oncotarget. 2017;8(56):95293-95302. doi:10.18632/oncotarget.20513
Cheung IY, Cheung NV, Modak S, et al. Survival impact of anti-GD2 antibody response in a phase II ganglioside vaccine trial among patients with high-risk neuroblastoma with prior disease progression. J Clin Oncol. 2021;39(3):215-226. doi:10.1200/jco.20.01892
Cheung IY, Mauguen A, Modak S, et al. Effect of oral β-glucan on antibody response to ganglioside vaccine in patients with high-risk neuroblastoma: a phase 2 randomized clinical trial. JAMA Oncol. 2023;9(2):242-250. doi:10.1001/jamaoncol.2022.5999
ClinicalTrials.Gov. A study of a vaccine in combination with β-glucan and GM-CSF in people with neuroblastoma; 2023. https://clinicaltrials.gov/ct2/show/NCT04936529
Eger C, Siebert N, Seidel D, et al. Generation and characterization of a human/mouse chimeric GD2-mimicking anti-idiotype antibody ganglidiximab for active immunotherapy against neuroblastoma. PloS One. 2016;11(3):e0150479. doi:10.1371/journal.pone.0150479
Klingel L, Siebert N, Troschke-Meurer S, et al. Immune response and outcome of high-risk neuroblastoma patients immunized with anti-Idiotypic antibody ganglidiomab: results from compassionate-use treatments. Cancers (Basel). 2022;14(23):5802. doi:10.3390/cancers14235802
Lode HN, Schmidt M, Seidel D, et al. Vaccination with anti-idiotype antibody ganglidiomab mediates a GD(2)-specific anti-neuroblastoma immune response. Cancer Immunol Immunother. 2013;62(6):999-1010. doi:10.1007/s00262-013-1413-y
Modak S, Cheung NK. Disialoganglioside directed immunotherapy of neuroblastoma. Cancer Invest. 2007;25(1):67-77. doi:10.1080/07357900601130763
ClinicalTrials.Gov. Humanized monoclonal antibody 3F8 (Hu3F8) with granulocyte-macrophage colony stimulating factor (GM-CSF) in the treatment of recurrent osteosarcoma; 2023. https://clinicaltrials.gov/ct2/show/NCT02502786
ClinicalTrials.Gov. Dinutuximab in combination with sargramostim in treating patients with recurrent osteosarcoma. 2023 https://clinicaltrials.gov/ct2/show/NCT02484443
ClinicalTrials.Gov. Activated T cells armed with GD2 bispecific antibody in children and young adults with neuroblastoma and osteosarcoma; 2019. https://clinicaltrials.gov/ct2/show/NCT02173093
Y-mAbs Therapeutics Inc. Y-mAbs announces presentation of naxitamab data at AACR. News release. 2023 https://ir.ymabs.com/news-releases/news-release-details/y-mabs-announces-presentation-naxitamab-data-aacr
Organisation for Economic Co-operation and Development (OECD). Addressing challenges in access to oncology medicines: Analytical report 2020. 2020 https://www.oecd.org/health/health-systems/Addressing-Challenges-in-Access-to-Oncology-Medicines-Analytical-Report.pdf
FarmaMondo. FarmaMondo to exclusively manage access of Qarziba® (Dinutuximab Beta) by EUSA Pharma for patients with high risk neuroblastoma in LATAM and APAC regions. 2019. https://farmamondo.com/farmamondo-to-exclusively-manage-access-of-qarziba-dinutuximab-beta-by-eusa-pharma-for-patients-with-high-risk-neuroblastoma-in-latam-and-apac-regions/
Clinigen. Clinigen Group and United Therapeutics initiate managed access program for Unituxin™ (dinutuximab) injection for high risk neuroblastoma. 2015. https://www.clinigengroup.com/news/news-container/2015/clinigen-group-and-united-therapeutics-initiate-managed-access-program-for-unituxin-dinutuximab-injection-for-high-risk-neuroblastoma/
Y-mAbs Therapeutics Inc. Expanded access programs & policies; 2023. https://ymabs.com/expanded-access-programs-policies/