Survival Benefit of Myeloablative Therapy with Autologous Stem Cell Transplantation in High-Risk Neuroblastoma: A Systematic Literature Review.

Journal

Targeted oncology
ISSN: 1776-260X
Titre abrégé: Target Oncol
Pays: France
ID NLM: 101270595

Informations de publication

Date de publication:
24 Feb 2024
Historique:
accepted: 12 01 2024
medline: 24 2 2024
pubmed: 24 2 2024
entrez: 24 2 2024
Statut: aheadofprint

Résumé

Multimodal treatment of newly diagnosed high-risk neuroblastoma (HRNB) includes induction chemotherapy, consolidation with myeloablative therapy (MAT) and autologous stem cell transplantation (ASCT), followed by anti-disialoganglioside 2 (GD2) immunotherapy, as recommended by the Children's Oncology Group (COG) and the Society of Paediatric Oncology European Neuroblastoma (SIOPEN). Some centres proposed an alternative approach with induction chemotherapy followed by anti-GD2 immunotherapy, without MAT+ASCT. The aim of this systematic literature review was to compare survival outcomes in patients with HRNB treated with or without MAT+ASCT and with or without subsequent anti-GD2 immunotherapy. The review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. MEDLINE via PubMed and EMBASE databases were systematically searched for randomised controlled trials (RCT) and observational comparative studies in patients with HRNB using search terms for 'neuroblastoma' and ('myeloablative therapy' OR 'stem cell transplantation'). Reporting of at least one survival outcome [event-free survival (EFS), progression-free survival, relapse-free survival and/or overall survival (OS)] was required for inclusion. Outcomes from RCTs were synthesized in meta-analysis, while meta-analysis of non-RCTs was not planned owing to expected heterogeneity. Literature searches produced 2587 results with 41 publications reporting 34 comparative studies included in the review. Of these, 7 publications reported 4 RCTs, and 34 publications reported 30 non-RCT studies. Studies differed with respect to included populations, induction regimen, response to induction, additional treatments and transplantation procedures. Subsequent treatments of relapse were rarely reported and could not be compared. In the meta-analysis, EFS was in favour of MAT+ASCT over conventional chemotherapy or no further treatment [hazard ratio (HR) = 0.78, 95% confidence interval (CI) 0.67-0.91, p = 0.001] with a trend favouring MAT+ASCT for OS (HR = 0.86, 95% CI 0.73-1.00, p = 0.05). Tandem MAT+ASCT was found to improve EFS compared with the single procedure, with improvement in both EFS and OS in patients treated with anti-GD2 therapy. Non-RCT comparative studies were broadly consistent with evidence from the RCTs; however, not all reported survival benefits of MAT+ASCT (single or tandem). Limited comparative evidence on treatment without MAT+ASCT in patients treated with anti-GD2 immunotherapy suggests an increased risk of relapse. In relapsed patients, MAT+ASCT appears to improve OS, but evidence remains scarce. Survival benefits in patients treated with MAT+ASCT confirm that the procedure should remain an integral part of multimodal therapy. In patients treated with anti-GD2 immunotherapy, limited evidence suggests that omitting MAT+ASCT is associated with an increased risk of relapse, and therefore, a change in clinical practice can currently not be recommended. Evidence suggests the use of tandem MAT+ASCT compared with the single procedure, with greater benefits observed in patients treated with anti-GD2 immunotherapy. Limited evidence also suggests improved survival following MAT+ASCT in relapsed patients, which needs to be viewed in light of emerging chemoimmunotherapy in this setting.

Sections du résumé

BACKGROUND BACKGROUND
Multimodal treatment of newly diagnosed high-risk neuroblastoma (HRNB) includes induction chemotherapy, consolidation with myeloablative therapy (MAT) and autologous stem cell transplantation (ASCT), followed by anti-disialoganglioside 2 (GD2) immunotherapy, as recommended by the Children's Oncology Group (COG) and the Society of Paediatric Oncology European Neuroblastoma (SIOPEN). Some centres proposed an alternative approach with induction chemotherapy followed by anti-GD2 immunotherapy, without MAT+ASCT.
OBJECTIVE OBJECTIVE
The aim of this systematic literature review was to compare survival outcomes in patients with HRNB treated with or without MAT+ASCT and with or without subsequent anti-GD2 immunotherapy.
PATIENTS AND METHODS METHODS
The review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. MEDLINE via PubMed and EMBASE databases were systematically searched for randomised controlled trials (RCT) and observational comparative studies in patients with HRNB using search terms for 'neuroblastoma' and ('myeloablative therapy' OR 'stem cell transplantation'). Reporting of at least one survival outcome [event-free survival (EFS), progression-free survival, relapse-free survival and/or overall survival (OS)] was required for inclusion. Outcomes from RCTs were synthesized in meta-analysis, while meta-analysis of non-RCTs was not planned owing to expected heterogeneity.
RESULTS RESULTS
Literature searches produced 2587 results with 41 publications reporting 34 comparative studies included in the review. Of these, 7 publications reported 4 RCTs, and 34 publications reported 30 non-RCT studies. Studies differed with respect to included populations, induction regimen, response to induction, additional treatments and transplantation procedures. Subsequent treatments of relapse were rarely reported and could not be compared. In the meta-analysis, EFS was in favour of MAT+ASCT over conventional chemotherapy or no further treatment [hazard ratio (HR) = 0.78, 95% confidence interval (CI) 0.67-0.91, p = 0.001] with a trend favouring MAT+ASCT for OS (HR = 0.86, 95% CI 0.73-1.00, p = 0.05). Tandem MAT+ASCT was found to improve EFS compared with the single procedure, with improvement in both EFS and OS in patients treated with anti-GD2 therapy. Non-RCT comparative studies were broadly consistent with evidence from the RCTs; however, not all reported survival benefits of MAT+ASCT (single or tandem). Limited comparative evidence on treatment without MAT+ASCT in patients treated with anti-GD2 immunotherapy suggests an increased risk of relapse. In relapsed patients, MAT+ASCT appears to improve OS, but evidence remains scarce.
CONCLUSIONS CONCLUSIONS
Survival benefits in patients treated with MAT+ASCT confirm that the procedure should remain an integral part of multimodal therapy. In patients treated with anti-GD2 immunotherapy, limited evidence suggests that omitting MAT+ASCT is associated with an increased risk of relapse, and therefore, a change in clinical practice can currently not be recommended. Evidence suggests the use of tandem MAT+ASCT compared with the single procedure, with greater benefits observed in patients treated with anti-GD2 immunotherapy. Limited evidence also suggests improved survival following MAT+ASCT in relapsed patients, which needs to be viewed in light of emerging chemoimmunotherapy in this setting.

Identifiants

DOI: 10.1007/s11523-024-01033-4 PMID: 38401028
pubmed: 38401028
doi: 10.1007/s11523-024-01033-4
pii: 10.1007/s11523-024-01033-4
doi:

Types de publication

Systematic Review

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Swift CC, Eklund MJ, Kraveka JM, Alazraki AL. Updates in diagnosis, management, and treatment of neuroblastoma. Radiographics. 2018;38:566–80. https://doi.org/10.1148/rg.2018170132 .
doi: 10.1148/rg.2018170132 pubmed: 29528815
Whittle SB, Smith V, Doherty E, Zhao S, McCarty S, Zage PE. Overview and recent advances in the treatment of neuroblastoma. Expert Rev Anticancer Ther. 2017;17:369–86. https://doi.org/10.1080/14737140.2017.1285230 .
doi: 10.1080/14737140.2017.1285230 pubmed: 28142287
Smith MA, Seibel NL, Altekruse SF, Ries LA, Melbert DL, O’Leary M, et al. Outcomes for children and adolescents with cancer: challenges for the twenty-first century. J Clin Oncol. 2010;28:2625–34. https://doi.org/10.1200/jco.2009.27.0421 .
doi: 10.1200/jco.2009.27.0421 pubmed: 20404250 pmcid: 2881732
Park JR, Eggert A, Caron H. Neuroblastoma: biology, prognosis, and treatment. Hematol Oncol Clin North Am. 2010;24:65–86. https://doi.org/10.1016/j.hoc.2009.11.011 .
doi: 10.1016/j.hoc.2009.11.011 pubmed: 20113896
DuBois SG, Macy ME, Henderson TO. High-risk and relapsed neuroblastoma: toward more cures and better outcomes. Am Soc Clin Oncol Educ Book. 2022;42:1–13. https://doi.org/10.1200/EDBK_349783 .
doi: 10.1200/EDBK_349783 pubmed: 35522915
Ladenstein R, Potschger U, Valteau-Couanet D, Luksch R, Castel V, Ash S, 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. https://doi.org/10.3390/cancers12020309 .
doi: 10.3390/cancers12020309 pubmed: 32013055
Bellini A, Pötschger U, Bernard V, Lapouble E, Baulande S, Ambros PF, et al. Frequency and prognostic impact of alk amplifications and mutations in the European Neuroblastoma Study Group (SIOPEN) High-Risk Neuroblastoma Trial (HR-NBL1). J Clin Oncol. 2021;39:3377–90. https://doi.org/10.1200/jco.21.00086 .
doi: 10.1200/jco.21.00086 pubmed: 34115544 pmcid: 8791815
Hogarty MD, Brodeur GM. Chapter 457. Neuroblastoma. In: Rudolph CD, Rudolph AM, Lister GE, First LR, Gershon AA, editors. Rudolph’s Pediatrics. 22nd ed. New York: The McGraw-Hill Companies; 2011.
Smith V, Foster J. High-risk neuroblastoma treatment review. Children (Basel). 2018;5(9):114. https://doi.org/10.3390/children5090114 .
doi: 10.3390/children5090114 pubmed: 30154341
Matthay KK, Reynolds CP, Seeger RC, Shimada H, Adkins ES, Haas-Kogan D, et al. Long-term results for children with high-risk neuroblastoma treated on a randomized trial of myeloablative therapy followed by 13-cis-retinoic acid: a children’s oncology group study. J Clin Oncol. 2009;27:1007–13. https://doi.org/10.1200/JCO.2007.13.8925 .
doi: 10.1200/JCO.2007.13.8925 pubmed: 19171716 pmcid: 2738615
Fish JD, Grupp SA. Stem cell transplantation for neuroblastoma. Bone Marrow Transplant. 2008;41:159–65. https://doi.org/10.1038/sj.bmt.1705929 .
doi: 10.1038/sj.bmt.1705929 pubmed: 18037943
Stram DO, Matthay KK, O’Leary M, Reynolds CP, Haase GM, Atkinson JB, et al. Consolidation chemoradiotherapy and autologous bone marrow transplantation versus continued chemotherapy for metastatic neuroblastoma: a report of two concurrent Children’s Cancer Group studies. J Clin Oncol. 1996;14:2417–26. https://doi.org/10.1200/JCO.1996.14.9.2417 .
doi: 10.1200/JCO.1996.14.9.2417 pubmed: 8823319
Matthay KK, Villablanca JG, Seeger RC, Stram DO, Harris RE, Ramsay NK, et al. Treatment of high-risk neuroblastoma with intensive chemotherapy, radiotherapy, autologous bone marrow transplantation, and 13-cis-retinoic acid. Children’s Cancer Group. N Engl J Med. 1999;341:1165–73. https://doi.org/10.1056/NEJM199910143411601 .
doi: 10.1056/NEJM199910143411601 pubmed: 10519894
Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med. 2010;363:1324–34. https://doi.org/10.1056/NEJMoa0911123 .
doi: 10.1056/NEJMoa0911123 pubmed: 20879881 pmcid: 3086629
Ladenstein R, Potschger U, Valteau-Couanet D, Luksch R, Castel V, Yaniv I, 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;19:1617–29. https://doi.org/10.1016/S1470-2045(18)30578-3 .
doi: 10.1016/S1470-2045(18)30578-3 pubmed: 30442501
Ladenstein R, Potschger U, Pearson ADJ, Brock P, Luksch R, Castel V, et al. Busulfan and melphalan versus carboplatin, etoposide, and melphalan as high-dose chemotherapy for high-risk neuroblastoma (HR-NBL1/SIOPEN): an international, randomised, multi-arm, open-label, phase 3 trial. Lancet Oncol. 2017;18:500–14. https://doi.org/10.1016/S1470-2045(17)30070-0 .
doi: 10.1016/S1470-2045(17)30070-0 pubmed: 28259608
Park JR, Kreissman SG, London WB, Naranjo A, Cohn SL, Hogarty MD, et al. Effect of tandem autologous stem cell transplant vs single transplant on event-free survival in patients with high-risk neuroblastoma: a randomized clinical trial. JAMA. 2019;322:746–55. https://doi.org/10.1001/jama.2019.11642 .
doi: 10.1001/jama.2019.11642 pubmed: 31454045 pmcid: 6714031
Yalcin B, Kremer LC, van Dalen EC. High-dose chemotherapy and autologous haematopoietic stem cell rescue for children with high-risk neuroblastoma. Cochrane Database Syst Rev. 2015;2015: CD006301. https://doi.org/10.1002/14651858.CD006301.pub4 .
doi: 10.1002/14651858.CD006301.pub4 pubmed: 26436598 pmcid: 8783746
Martin A, Schneiderman J, Helenowski IB, Morgan E, Dilley K, Danner-Koptik K, et al. Secondary malignant neoplasms after high-dose chemotherapy and autologous stem cell rescue for high-risk neuroblastoma. Pediatr Blood Cancer. 2014;61:1350–6. https://doi.org/10.1002/pbc.25033 .
doi: 10.1002/pbc.25033 pubmed: 24634399
Applebaum MA, Vaksman Z, Lee SM, Hungate EA, Henderson TO, London WB, et al. Neuroblastoma survivors are at increased risk for second malignancies: a report from the International Neuroblastoma Risk Group Project. Eur J Cancer. 2017;72:177–85. https://doi.org/10.1016/j.ejca.2016.11.022 .
doi: 10.1016/j.ejca.2016.11.022 pubmed: 28033528
Elzembely MM, Dahlberg AE, Pinto N, Leger KJ, Chow EJ, Park JR, et al. Late effects in high-risk neuroblastoma survivors treated with high-dose chemotherapy and stem cell rescue. Pediatr Blood Cancer. 2019;66: e27421. https://doi.org/10.1002/pbc.27421 .
doi: 10.1002/pbc.27421 pubmed: 30151986
Friedman DN, Henderson TO. Late effects and survivorship issues in patients with neuroblastoma. Children (Basel). 2018;5(8):107. https://doi.org/10.3390/children5080107 .
doi: 10.3390/children5080107 pubmed: 30082653
Moke DJ, Luo C, Millstein J, Knight KR, Rassekh SR, Brooks B, et al. Prevalence and risk factors for cisplatin-induced hearing loss in children, adolescents, and young adults: a multi-institutional North American cohort study. Lancet Child Adolesc Health. 2021;5:274–83. https://doi.org/10.1016/s2352-4642(21)00020-1 .
doi: 10.1016/s2352-4642(21)00020-1 pubmed: 33581749 pmcid: 9059427
Spears N, Lopes F, Stefansdottir A, Rossi V, De Felici M, Anderson RA, et al. Ovarian damage from chemotherapy and current approaches to its protection. Hum Reprod Update. 2019;25:673–93. https://doi.org/10.1093/humupd/dmz027 .
doi: 10.1093/humupd/dmz027 pubmed: 31600388 pmcid: 6847836
Laverdière C, Cheung NK, Kushner BH, Kramer K, Modak S, LaQuaglia MP, et al. Long-term complications in survivors of advanced stage neuroblastoma. Pediatr Blood Cancer. 2005;45:324–32. https://doi.org/10.1002/pbc.20331 .
doi: 10.1002/pbc.20331 pubmed: 15714447
Schechter T, Perez-Albuerne E, Lin TF, Irwin MS, Essa M, Desai AV, et al. Veno-occlusive disease after high-dose busulfan-melphalan in neuroblastoma. Bone Marrow Transplant. 2020;55:531–7. https://doi.org/10.1038/s41409-018-0298-y .
doi: 10.1038/s41409-018-0298-y pubmed: 30181580
Niederwieser D, Baldomero H, Bazuaye N, Bupp C, Chaudhri N, Corbacioglu S, et al. One and a half million hematopoietic stem cell transplants: continuous and differential improvement in worldwide access with the use of non-identical family donors. Haematologica. 2022;107:1045–53. https://doi.org/10.3324/haematol.2021.279189 .
doi: 10.3324/haematol.2021.279189 pubmed: 34382386
Kushner BH, Ostrovnaya I, Cheung IY, Kuk D, Modak S, Kramer K, et al. Lack of survival advantage with autologous stem-cell transplantation in high-risk neuroblastoma consolidated by anti-GD2 immunotherapy and isotretinoin. Oncotarget. 2016;7:4155–66. https://doi.org/10.18632/oncotarget.6393 .
doi: 10.18632/oncotarget.6393 pubmed: 26623730
Kushner BH, Modak S, Kramer K, Basu EM, Iglesias-Cardenas F, Roberts SS, et al. Immunotherapy with anti-G(D2) monoclonal antibody in infants with high-risk neuroblastoma. Int J Cancer. 2023;152:259–66. https://doi.org/10.1002/ijc.34233 .
doi: 10.1002/ijc.34233 pubmed: 35913764
Castel V, Canete A, Navarro S, Garcia-Miguel P, Melero C, Acha T, et al. Outcome of high-risk neuroblastoma using a dose intensity approach: improvement in initial but not in long-term results. Med Pediatr Oncol. 2001;37:537–42. https://doi.org/10.1002/mpo.1248 .
doi: 10.1002/mpo.1248 pubmed: 11745893
De Bernardi B, Nicolas B, Boni L, Indolfi P, Carli M, Cordero Di Montezemolo L, et al. Disseminated neuroblastoma in children older than one year at diagnosis: comparable results with three consecutive high-dose protocols adopted by the Italian Co-Operative Group for Neuroblastoma. J Clin Oncol. 2003;21:1592–601. https://doi.org/10.1200/JCO.2003.05.191 .
doi: 10.1200/JCO.2003.05.191 pubmed: 12697885
Mody R, Yu AL, Naranjo A, Zhang FF, London WB, Shulkin BL, 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;38:2160–9. https://doi.org/10.1200/jco.20.00203 .
doi: 10.1200/jco.20.00203 pubmed: 32343642 pmcid: 7325366
Federico SM, McCarville MB, Shulkin BL, Sondel PM, Hank JA, Hutson P, 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;23:6441–9. https://doi.org/10.1158/1078-0432.Ccr-17-0379 .
doi: 10.1158/1078-0432.Ccr-17-0379 pubmed: 28939747 pmcid: 8725652
Mora J. Autologous stem-cell transplantation for high-risk neuroblastoma: historical and critical review. Cancers (Basel). 2022;14(11):2572. https://doi.org/10.3390/cancers14112572 .
doi: 10.3390/cancers14112572 pubmed: 35681553
Kushner BH. Re-thinking transplant for neuroblastoma. Pediatr Blood Cancer. 2021;68: e28961. https://doi.org/10.1002/pbc.28961 .
doi: 10.1002/pbc.28961 pubmed: 33661565
Bird N, Scobie N, Palmer A, Ludwinski D. To transplant, or not to transplant? That is the question. A patient advocate evaluation of autologous stem cell transplant in neuroblastoma. Pediatr Blood Cancer. 2022;69: e29663. https://doi.org/10.1002/pbc.29663 .
doi: 10.1002/pbc.29663 pubmed: 35373890
Flaadt T, Ladenstein RL, Ebinger M, Lode HN, Arnardóttir HB, Poetschger U, et al. Anti-GD2 Antibody dinutuximab beta and low-dose interleukin 2 after haploidentical stem-cell transplantation in patients with relapsed neuroblastoma: a multicenter, phase I/II trial. J Clin Oncol. 2023;41:3135–48. https://doi.org/10.1200/jco.22.01630 .
doi: 10.1200/jco.22.01630 pubmed: 36854071 pmcid: 10256422
Pritchard J, Cotterill SJ, Germond SM, Imeson J, de Kraker J, Jones DR. High dose melphalan in the treatment of advanced neuroblastoma: results of a randomised trial (ENSG-1) by the European Neuroblastoma Study Group. Pediatr Blood Cancer. 2005;44:348–57. https://doi.org/10.1002/pbc.20219 .
doi: 10.1002/pbc.20219 pubmed: 15546135
Berthold F, Boos J, Burdach S, Erttmann R, Henze G, Hermann J, et al. Myeloablative megatherapy with autologous stem-cell rescue versus oral maintenance chemotherapy as consolidation treatment in patients with high-risk neuroblastoma: a randomised controlled trial. Lancet Oncol. 2005;6:649–58. https://doi.org/10.1016/s1470-2045(05)70291-6 .
doi: 10.1016/s1470-2045(05)70291-6 pubmed: 16129365
Berthold F, Ernst A, Hero B, Klingebiel T, Kremens B, Schilling FH, et al. Long-term outcomes of the GPOH NB97 trial for children with high-risk neuroblastoma comparing high-dose chemotherapy with autologous stem cell transplantation and oral chemotherapy as consolidation. Br J Cancer. 2018;119:282–90. https://doi.org/10.1038/s41416-018-0169-8 .
doi: 10.1038/s41416-018-0169-8 pubmed: 29991700 pmcid: 6068129
Hero B, Kremens B, Klingebiel T, Bender-Götze C, Burdach S, Schrappe M, et al. Does megatherapy contribute to survival in metastatic neuroblastoma? A retrospective analysis. German Cooperative Neuroblastoma Study Group. Klin Padiatr. 1997;209:196–200. https://doi.org/10.1055/s-2008-1043950 .
doi: 10.1055/s-2008-1043950 pubmed: 9293450
Simon T, Hero B, Faldum A, Handgretinger R, Schrappe M, Niethammer D, et al. Consolidation treatment with chimeric anti-GD2-antibody ch14.18 in children older than 1 year with metastatic neuroblastoma. J Clin Oncol. 2004;22:3549–57. https://doi.org/10.1200/jco.2004.08.143 .
doi: 10.1200/jco.2004.08.143 pubmed: 15337804
Simon T, Hero B, Faldum A, Handgretinger R, Schrappe M, Niethammer D, et al. Infants with stage 4 neuroblastoma: the impact of the chimeric anti-GD2-antibody ch14.18 consolidation therapy. Klin Padiatr. 2005;217:147–52. https://doi.org/10.1055/s-2005-836518 .
doi: 10.1055/s-2005-836518 pubmed: 15858706
Imaizumi M, Watanabe A, Kikuta A, Takano T, Ito E, Shimizu T, et al. Improved survival of children with advanced neuroblastoma treated by intensified therapy including myeloablative chemotherapy with stem cell transplantation: a retrospective analysis from the Tohoku Neuroblastoma Study Group. Tohoku J Exp Med. 2001;195:73–83. https://doi.org/10.1620/tjem.195.73 .
doi: 10.1620/tjem.195.73 pubmed: 11846211
Yan J, Jie L, Jiaxing Y, Yanna C, Zhanglin L, Zhongyuan L, et al. Analysis of the efficacy of autologous peripheral blood stem cell transplantation in high-risk neuroblastoma. Int J Med Sci. 2022;19:1715–23. https://doi.org/10.7150/ijms.76305 .
doi: 10.7150/ijms.76305 pubmed: 36237985 pmcid: 9553861
Luksch R, Podda M, Gandola L, Polastri D, Piva L, Castellani R, et al. Stage 4 neuroblastoma: sequential hemi-body irradiation or high-dose chemotherapy plus autologous haemopoietic stem cell transplantation to consolidate primary treatment. Br J Cancer. 2005;92:1984–8. https://doi.org/10.1038/sj.bjc.6602615 .
doi: 10.1038/sj.bjc.6602615 pubmed: 15900298 pmcid: 2361794
Mossé YP, Deyell RJ, Berthold F, Nagakawara A, Ambros PF, Monclair T, et al. Neuroblastoma in older children, adolescents and young adults: a report from the International Neuroblastoma Risk Group project. Pediatr Blood Cancer. 2014;61:627–35. https://doi.org/10.1002/pbc.24777 .
doi: 10.1002/pbc.24777 pubmed: 24038992
Moon SB, Park KW, Jung SE, Youn WJ. Neuroblastoma: treatment outcome after incomplete resection of primary tumors. Pediatr Surg Int. 2009;25:789–93. https://doi.org/10.1007/s00383-009-2417-8 .
doi: 10.1007/s00383-009-2417-8 pubmed: 19629500
Chamberlain RS, Quinones R, Dinndorf P, Movassaghi N, Goodstein M, Newman K. Complete surgical resection combined with aggressive adjuvant chemotherapy and bone marrow transplantation prolongs survival in children with advanced neuroblastoma. Ann Surg Oncol. 1995;2:93–100. https://doi.org/10.1007/bf02303622 .
doi: 10.1007/bf02303622 pubmed: 7728576
Castel V, García-Miguel P, Melero C, Navajas A, Navarro S, Molina J, et al. The treatment of advanced neuroblastoma. Results of the Spanish Neuroblastoma Study Group (SNSG) studies. Eur J Cancer. 1995;31a:642–5. https://doi.org/10.1016/0959-8049(95)00072-q .
doi: 10.1016/0959-8049(95)00072-q pubmed: 7576986
Ohnuma N, Takahashi H, Kaneko M, Uchino J, Takeda T, Iwafuchi, et al. Treatment combined with bone marrow transplantation for advanced neuroblastoma: an analysis of patients who were pretreated intensively with the protocol of the Study Group of Japan. Med Pediatr Oncol. 1995;24:181–7. https://doi.org/10.1002/mpo.2950240308 .
doi: 10.1002/mpo.2950240308 pubmed: 7838040
Berthold F, Burdach S, Kremens B, Lampert F, Niethammer D, Riehm H, et al. The role of chemotherapy in the treatment of children with neuroblastoma stage IV: the GPO (German Pediatric Oncology Society) experience. Klin Padiatr. 1990;202:262–9. https://doi.org/10.1055/s-2007-1025531 .
doi: 10.1055/s-2007-1025531 pubmed: 2203940
Kaneko M, Tsuchida Y, Uchino J, Takeda T, Iwafuchi M, Ohnuma N, et al. Treatment results of advanced neuroblastoma with the first Japanese study group protocol. Study Group of Japan for Treatment of Advanced Neuroblastoma. J Pediatr Hematol Oncol. 1999;21:190–7. https://doi.org/10.1097/00043426-199905000-00006 .
doi: 10.1097/00043426-199905000-00006 pubmed: 10363851
Kaneko M, Tsuchida Y, Mugishima H, Ohnuma N, Yamamoto K, Kawa K, et al. Intensified chemotherapy increases the survival rates in patients with stage 4 neuroblastoma with MYCN amplification. J Pediatr Hematol Oncol. 2002;24:613–21. https://doi.org/10.1097/00043426-200211000-00004 .
doi: 10.1097/00043426-200211000-00004 pubmed: 12439032
Klaassen RJ, Trebo MM, Koplewitz BZ, Weitzman SS, Calderwood S. High-risk neuroblastoma in Ontario: a report of experience from 1989 to 1995. J Pediatr Hematol Oncol. 2003;25:8–13. https://doi.org/10.1097/00043426-200301000-00004 .
doi: 10.1097/00043426-200301000-00004 pubmed: 12544767
Aksoylar S, Varan A, Vergin C, Hazar V, Akici F, Dagdemir A, et al. Treatment of high-risk neuroblastoma: national protocol results of the Turkish Pediatric Oncology Group. J Cancer Res Ther. 2017;13:284–90. https://doi.org/10.4103/0973-1482.183205 .
doi: 10.4103/0973-1482.183205 pubmed: 28643749
Cheung NK, Cheung IY, Kushner BH, Ostrovnaya I, Chamberlain E, Kramer K, 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;30:3264–70. https://doi.org/10.1200/jco.2011.41.3807 .
doi: 10.1200/jco.2011.41.3807 pubmed: 22869886 pmcid: 3434986
Mora J, Castañeda A, Flores MA, Santa-María V, Garraus M, Gorostegui M, 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. https://doi.org/10.3389/fphar.2020.575009 .
doi: 10.3389/fphar.2020.575009 pubmed: 33324208 pmcid: 7723438
Mora J, Castañeda A, Gorostegui M, Santa-María V, Garraus M, Muñoz JP, 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: e29121. https://doi.org/10.1002/pbc.29121 .
doi: 10.1002/pbc.29121 pubmed: 34022112
Simon T, Hero B, Faldum A, Handgretinger R, Schrappe M, Klingebiel T, et al. Long term outcome of high-risk neuroblastoma patients after immunotherapy with antibody ch14.18 or oral metronomic chemotherapy. BMC Cancer. 2011;11:21. https://doi.org/10.1186/1471-2407-11-21 .
doi: 10.1186/1471-2407-11-21 pubmed: 21244693 pmcid: 3031264
Sung KW, Ahn HS, Cho B, Choi YM, Chung NG, Hwang TJ, et al. Efficacy of tandem high-dose chemotherapy and autologous stem cell rescue in patients over 1 year of age with stage 4 neuroblastoma: the Korean Society of Pediatric Hematology-Oncology experience over 6 years (2000–2005). J Korean Med Sci. 2010;25:691–7. https://doi.org/10.3346/jkms.2010.25.5.691 .
doi: 10.3346/jkms.2010.25.5.691 pubmed: 20436703 pmcid: 2858826
Qayed M, Chiang KY, Ricketts R, Alazraki A, Tahvildari A, Haight A, et al. Tandem stem cell rescue as consolidation therapy for high-risk neuroblastoma. Pediatr Blood Cancer. 2012;58:448–52. https://doi.org/10.1002/pbc.23155 .
doi: 10.1002/pbc.23155 pubmed: 21538822
Suh JM, Yoo KH, Sung KW, Kim JY, Cho EJ, Koo HH, et al. High-dose chemotherapy and autologous stem cell rescue in patients with high-risk stage 3 neuroblastoma: 10-year experience at a single center. J Korean Med Sci. 2009;24:660–7. https://doi.org/10.3346/jkms.2009.24.4.660 .
doi: 10.3346/jkms.2009.24.4.660 pubmed: 19654949 pmcid: 2719186
Kim EK, Kang HJ, Park JA, Choi HS, Shin HY, Ahn HS. Retrospective analysis of peripheral blood stem cell transplantation for the treatment of high-risk neuroblastoma. J Korean Med Sci. 2007;22(Suppl):S66-72. https://doi.org/10.3346/jkms.2007.22.S.S66 .
doi: 10.3346/jkms.2007.22.S.S66 pubmed: 17923758 pmcid: 2694391
Frappaz D, Michon J, Coze C, Berger C, Plouvier E, Lasset C, et al. LMCE3 treatment strategy: results in 99 consecutively diagnosed stage 4 neuroblastomas in children older than 1 year at diagnosis. J Clin Oncol. 2000;18:468–76. https://doi.org/10.1200/jco.2000.18.3.468 .
doi: 10.1200/jco.2000.18.3.468 pubmed: 10653862
Simon T, Berthold F, Borkhardt A, Kremens B, De Carolis B, Hero B. Treatment and outcomes of patients with relapsed, high-risk neuroblastoma: results of German trials. Pediatr Blood Cancer. 2011;56:578–83. https://doi.org/10.1002/pbc.22693 .
doi: 10.1002/pbc.22693 pubmed: 21298742
Lerman B, Li Y, Carlowicz C, Granger M, Cash T, Sadanand A, et al. Progression-free survival and patterns of response in patients with relapsed high-risk neuroblastoma treated with irinotecan/temozolomide/dinutuximab/GM-CSF. J Clin Oncol. 2023;41:508–16. https://doi.org/10.1200/JCO.22.01273 .
doi: 10.1200/JCO.22.01273 pubmed: 36206505
Kushner BH, Kramer K, LaQuaglia MP, Modak S, Yataghene K, Cheung NK. Reduction from seven to five cycles of intensive induction chemotherapy in children with high-risk neuroblastoma. J Clin Oncol. 2004;22:4888–92. https://doi.org/10.1200/jco.2004.02.101 .
doi: 10.1200/jco.2004.02.101 pubmed: 15611504
Berthold F, Faldum A, Ernst A, Boos J, Dilloo D, Eggert A, et al. Extended induction chemotherapy does not improve the outcome for high-risk neuroblastoma patients: results of the randomized open-label GPOH trial NB2004-HR. Ann Oncol. 2020;31:422–9. https://doi.org/10.1016/j.annonc.2019.11.011 .
doi: 10.1016/j.annonc.2019.11.011 pubmed: 32067684
Garaventa A, Poetschger U, Valteau-Couanet D, Luksch R, Castel V, Elliott M, et al. Randomized trial of two induction therapy regimens for high-risk neuroblastoma: HR-NBL1.5 International Society of Pediatric Oncology European Neuroblastoma Group Study. J Clin Oncol. 2021;39:2552–63. https://doi.org/10.1200/jco.20.03144 .
doi: 10.1200/jco.20.03144 pubmed: 34152804
Kushner BH, Kramer K, Cheung NK. Phase II trial of the anti-G(D2) monoclonal antibody 3F8 and granulocyte-macrophage colony-stimulating factor for neuroblastoma. J Clin Oncol. 2001;19:4189–94. https://doi.org/10.1200/jco.2001.19.22.4189 .
doi: 10.1200/jco.2001.19.22.4189 pubmed: 11709561
Mora J, Castañeda A, Gorostegui M, Varo A, Perez-Jaume S, Simao 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. https://doi.org/10.3390/cancers15092535 .
doi: 10.3390/cancers15092535 pubmed: 37174002
Eleveld TF, Vernooij L, Schild L, Koopmans B, Alles LK, Ebus ME, et al. MEK inhibition causes BIM stabilization and increased sensitivity to BCL-2 family member inhibitors in RAS-MAPK-mutated neuroblastoma. Front Oncol. 2023;13:1130034. https://doi.org/10.3389/fonc.2023.1130034 .
doi: 10.3389/fonc.2023.1130034 pubmed: 36895472 pmcid: 9990464
Koneru B, Farooqi A, Nguyen TH, Chen WH, Hindle A, Eslinger C, et al. ALT neuroblastoma chemoresistance due to telomere dysfunction-induced ATM activation is reversible with ATM inhibitor AZD0156. Sci Transl Med. 2021;13(607). https://doi.org/10.1126/scitranslmed.abd5750 .
doi: 10.1126/scitranslmed.abd5750 pubmed: 34408079 pmcid: 9208664
Valentijn LJ, Koster J, Zwijnenburg DA, Hasselt NE, van Sluis P, Volckmann R, et al. TERT rearrangements are frequent in neuroblastoma and identify aggressive tumors. Nat Genet. 2015;47:1411–4. https://doi.org/10.1038/ng.3438 .
doi: 10.1038/ng.3438 pubmed: 26523776
Hartmann O, Le Corroller AG, Blaise D, Michon J, Philip I, Norol F, et al. Peripheral blood stem cell and bone marrow transplantation for solid tumors and lymphomas: hematologic recovery and costs. A randomized, controlled trial. Ann Intern Med. 1997;126:600–7. https://doi.org/10.7326/0003-4819-126-8-199704150-00002 .
doi: 10.7326/0003-4819-126-8-199704150-00002 pubmed: 9103126
Eguchi H, Takaue Y, Kawano Y, Watanabe A, Watanabe T, Kikuta A, et al. Peripheral blood stem cell autografts for the treatment of children over 1 year old with stage IV neuroblastoma: a long-term follow-up. Bone Marrow Transplant. 1998;21:1011–4. https://doi.org/10.1038/sj.bmt.1701207 .
doi: 10.1038/sj.bmt.1701207 pubmed: 9632274
Schmidt ML, Lal A, Seeger RC, Maris JM, Shimada H, O’Leary M, et al. Favorable prognosis for patients 12 to 18 months of age with stage 4 nonamplified MYCN neuroblastoma: a Children’s Cancer Group Study. J Clin Oncol. 2005;23:6474–80. https://doi.org/10.1200/jco.2005.05.183 .
doi: 10.1200/jco.2005.05.183 pubmed: 16116154

Auteurs

Urszula Żebrowska (U)

Department of Paediatric Oncology and Haematology, University Children's Hospital of Krakow, 265 Wielicka str, 30-663, Krakow, Poland.

Walentyna Balwierz (W)

Department of Paediatric Oncology and Haematology, University Children's Hospital of Krakow, 265 Wielicka str, 30-663, Krakow, Poland.
Department of Paediatric Oncology and Haematology, Jagiellonian University Medical College, 265 Wielicka str, 30-663, Krakow, Poland.

Jarosław Wechowski (J)

EUSA Pharma, Breakspear Park, Breakspear Way, Hemel Hempstead, HP2 4TZ, UK.

Aleksandra Wieczorek (A)

Department of Paediatric Oncology and Haematology, University Children's Hospital of Krakow, 265 Wielicka str, 30-663, Krakow, Poland. a.wieczorek@uj.edu.pl.
Department of Paediatric Oncology and Haematology, Jagiellonian University Medical College, 265 Wielicka str, 30-663, Krakow, Poland. a.wieczorek@uj.edu.pl.
ORCID: 0000-0001-6750-2628

Classifications MeSH