Advertisement

Neuroblastoma pp 213-235 | Cite as

High-Risk Neuroblastoma and Current Protocols

  • Katherine K. MatthayEmail author
  • Dominique Valteau-CouanetEmail author
Chapter

Abstract

High-risk neuroblastoma comprises nearly half of all neuroblastoma and have a long-term survival of <50%. Patients >18 months with International Neuroblastoma Staging System (INSS) stage 4 disease and those with a tumor INSS >1 with MYCN amplification are considered as patients with a high-risk disease in both groups and represent the majority of the patients. The current standard North American and European approach to therapy of high-risk neuroblastoma involves four phases with an intensive induction therapy, a local control using surgery and radiation, a consolidation phase with single or tandem high-dose chemotherapy and autologous transplant, and differentiating and immunotherapy for minimal residual disease (MRD) in the maintenance phase. Future improvements will depend on more extensive tumor molecular profiling at diagnosis and relapse, improvement of the quality of response using immunotherapy or other targeted therapy such as tyrosine kinase inhibitors or 131I-metaiodobenzylguanidine (131I-MIBG), and further improvements of the MRD therapy with more targeted small molecules.

Keywords

High-risk neuroblastoma Very-high-risk neuroblastoma High-dose chemotherapy Autologous stem cell rescue Bu-Mel (Busulfan–Melphalan) 131 MIBG CEM (Carboplatine–Etoposide–Melphalan) Immunotherapy Maintenance treatment 13-Cis-retinoic acid Anti-GD2 

References

  1. 1.
    Evans AE, D’Angio GJ, Randolph J. A proposed staging for children with neuroblastoma. Children’s Cancer Study Group A. Cancer. 1971;27:374–8.CrossRefGoogle Scholar
  2. 2.
    Shimada H, Chatten J, Newton WA Jr, Sachs N, Hamoudi AB, Chiba T, Marsden HB, Misugi K. Histopathologic prognostic factors in neuroblastic tumors: definition of subtypes of ganglioneuroblastoma and an age-linked classification of neuroblastomas. J Natl Cancer Inst. 1984;73:405–16.CrossRefGoogle Scholar
  3. 3.
    Hann HW, Evans AE, Siegel SE, Wong KY, Sather H, Dalton A, Hammond D, Seeger RC. Prognostic importance of serum ferritin in patients with stages III and IV neuroblastoma: the Childrens Cancer Study Group experience. Cancer Res. 1985;45:2843–8.PubMedGoogle Scholar
  4. 4.
    Evans AE, D’Angio GJ, Sather HN, de Lorimier AA, Dalton A, Ungerleider RS, Finklestein JZ, Hammond GD. A comparison of four staging systems for localized and regional neuroblastoma: a report from the Childrens Cancer Study Group. J Clin Oncol. 1990;8:678–88.PubMedCrossRefGoogle Scholar
  5. 5.
    Brodeur GM, Pritchard J, Berthold F, Carlsen NL, Castel V, Castelberry RP, De Bernardi B, Evans AE, Favrot M, Hedborg F, et al. Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment [see comments]. J Clin Oncol. 1993;11:1466–77.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Monclair T, Brodeur GM, Ambros PF, Brisse HJ, Cecchetto G, Holmes K, Kaneko M, London WB, Matthay KK, Nuchtern JG, et al. The International Neuroblastoma Risk Group (INRG) staging system: an INRG Task Force report. J Clin Oncol. 2009;27:298–303.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Shimada H, Ambros IM, Dehner LP, Hata J, Joshi VV, Roald B, Stram DO, Gerbing RB, Lukens JN, Matthay KK, et al. The International Neuroblastoma Pathology Classification (the Shimada system). Cancer. 1999;86:364–72.CrossRefGoogle Scholar
  8. 8.
    Ambros PF, Ambros IM, Brodeur GM, Haber M, Khan J, Nakagawara A, Schleiermacher G, Speleman F, Spitz R, London WB, et al. International consensus for neuroblastoma molecular diagnostics: report from the International Neuroblastoma Risk Group (INRG) Biology Committee. Br J Cancer. 2009;100:1471–82.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Cohn SL, Pearson AD, London WB, Monclair T, Ambros PF, Brodeur GM, Faldum A, Hero B, Iehara T, Machin D, et al. The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol. 2009;27:289–97.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Schleiermacher G, Janoueix-Lerosey I, Ribeiro A, Klijanienko J, Couturier J, Pierron G, Mosseri V, Valent A, Auger N, Plantaz D, et al. Accumulation of segmental alterations determines progression in neuroblastoma. J Clin Oncol. 2010;28:3122–30.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY, Hammond D. Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N Engl J Med. 1985;313:1111–6.CrossRefGoogle Scholar
  12. 12.
    Ladenstein R, Lambert B, Pötschger U, Castellani M-R, Lewington V, Bar-Sever Z, Oudoux A, Śliwińska A, Taborska K, Biassoni L, et al. Validation of the mIBG skeletal SIOPEN scoring method in two independent high-risk neuroblastoma populations: the SIOPEN/HR-NBL1 and COG-A3973 trials. Eur J Nucl Med Mol Imaging. 2018;45:292–305.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Yanik GA, Parisi MT, Naranjo A, Nadel H, Gelfand MJ, Park JR, Ladenstein RL, Poetschger U, Boubaker A, Valteau-Couanet D, et al. Validation of postinduction curie scores in high-risk neuroblastoma: a Children’s Oncology Group and SIOPEN Group Report on SIOPEN/HR-NBL1. J Nucl Med. 2018;59:502–8.PubMedPubMedCentralCrossRefGoogle Scholar
  14. 14.
    Ladenstein R, Pötschger 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.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Depuydt P, Boeva V, Hocking TD, Cannoodt R, Ambros IM, Ambros PF, Asgharzadeh S, Attiyeh EF, Combaret V, Defferrari R, et al. Genomic amplifications and distal 6q loss: novel markers for poor survival in high-risk neuroblastoma patients. J Natl Cancer Inst. 2018;110(10):1084–93.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Cheung N-KV, Zhang J, Lu C, Parker M, Bahrami A, Tickoo SK, Heguy A, Pappo AS, Federico S, Dalton J, et al. Association of age at diagnosis and genetic mutations in patients with neuroblastoma. JAMA. 2012;307:1062–71.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Valentijn LJ, Koster J, Zwijnenburg DA, Hasselt NE, van Sluis P, Volckmann R, van Noesel MM, George RE, Tytgat GAM, Molenaar JJ, et al. TERT rearrangements are frequent in neuroblastoma and identify aggressive tumors. Nat Genet. 2015;47:1411–4.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Green DM, Kun LE, Matthay KK, Meadows AT, Meyer WH, Meyers PA, Spunt SL, Robison LL, Hudson MM. Relevance of historical therapeutic approaches to the contemporary treatment of pediatric solid tumors. Pediatr Blood Cancer. 2013;60:1083–94.PubMedCrossRefGoogle Scholar
  19. 19.
    Matthay KK, Maris JM, Schleiermacher G, Nakagawara A, Mackall CL, Diller L, Weiss WA. Neuroblastoma. Nat Rev Dis Primers. 2016;2:16078.CrossRefGoogle Scholar
  20. 20.
    Pinto NR, Applebaum MA, Volchenboum SL, Matthay KK, London WB, Ambros PF, Nakagawara A, Berthold F, Schleiermacher G, Park JR, et al. Advances in risk classification and treatment strategies for neuroblastoma. J Clin Oncol Off J Am Soc Clin Oncol. 2015;33:3008–17.CrossRefGoogle Scholar
  21. 21.
    Finklestein JZ, Hittle RE, Hammond GD. Evaluation of a high dose cyclophosphamide regimen in childhood tumors. Cancer. 1969;23:1239–42.PubMedCrossRefGoogle Scholar
  22. 22.
    Nitschke R, Starling KA, Vats T, Bryan H. Cis-diamminedichloroplatinum (NSC-119875) in childhood malignancies: a Southwest Oncology Group study. Med Pediatr Oncol. 1978;4:127–32.PubMedCrossRefGoogle Scholar
  23. 23.
    Rivera G, Green A, Hayes A, Avery T, Pratt C. Epipodophyllotoxin VM-26 in the treatment of childhood neuroblastoma. Cancer Treat Rep. 1977;61:1243–8.PubMedGoogle Scholar
  24. 24.
    Cheung NV, Heller G. Chemotherapy dose intensity correlates strongly with response, median survival, and median progression-free survival in metastatic neuroblastoma [see comments]. J Clin Oncol. 1991;9:1050–8.PubMedCrossRefGoogle Scholar
  25. 25.
    George RE, Li S, Medeiros-Nancarrow C, Neuberg D, Marcus K, Shamberger RC, Pulsipher M, Grupp SA, Diller L. High-risk neuroblastoma treated with tandem autologous peripheral-blood stem cell-supported transplantation: long-term survival update. J Clin Oncol Off J Am Soc Clin Oncol. 2006;24:2891–6.CrossRefGoogle Scholar
  26. 26.
    Kretschmar CS, Kletzel M, Murray K, Thorner P, Joshi V, Marcus R, Smith EI, London WB, Castleberry R. Response to paclitaxel, topotecan, and topotecan-cyclophosphamide in children with untreated disseminated neuroblastoma treated in an upfront phase II investigational window: a pediatric oncology group study. J Clin Oncol Off J Am Soc Clin Oncol. 2004;22:4119–26.CrossRefGoogle Scholar
  27. 27.
    Matthay KK, Villablanca JG, Seeger RC, Stram DO, Harris RE, Ramsay NK, Swift P, Shimada H, Black CT, Brodeur GM, 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.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Zage PE, Kletzel M, Murray K, Marcus R, Castleberry R, Zhang Y, London WB, Kretschmar C. Outcomes of the POG 9340/9341/9342 trials for children with high-risk neuroblastoma: a report from the Children’s Oncology Group. Pediatr Blood Cancer. 2008;51:747–53.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Kushner BH, Kramer K, LaQuaglia MP, Modak S, Yataghene K, Cheung N-KV. Reduction from seven to five cycles of intensive induction chemotherapy in children with high-risk neuroblastoma. J Clin Oncol Off J Am Soc Clin Oncol. 2004;22:4888–92.CrossRefGoogle Scholar
  30. 30.
    Park JR, Scott JR, Stewart CF, London WB, Naranjo A, Santana VM, Shaw PJ, Cohn SL, Matthay KK. Pilot induction regimen incorporating pharmacokinetically guided topotecan for treatment of newly diagnosed high-risk neuroblastoma: a Children’s Oncology Group study. J Clin Oncol Off J Am Soc Clin Oncol. 2011;29:4351–7.CrossRefGoogle Scholar
  31. 31.
    Haas-Kogan DA, Swift PS, Selch M, Haase GM, Seeger RC, Gerbing RB, Stram DO, Matthay KK. Impact of radiotherapy for high-risk neuroblastoma: a Children’s Cancer Group study. Int J Radiat Oncol Biol Phys. 2003;56:28–39.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Wolden SL, Gollamudi SV, Kushner BH, LaQuaglia M, Kramer K, Rosen N, Abramson S, Cheung NV. Local control with multimodality therapy for Stage 4 neuroblastoma. Int J Radiat Oncol Biol Phys. 2000;46:969–74.PubMedCrossRefGoogle Scholar
  33. 33.
    Matthay KK, Seeger RC, Reynolds CP, Stram DO, O’Leary MC, Harris RE, Selch M, Atkinson JB, Haase GM, Ramsay NK. Allogeneic versus autologous purged bone marrow transplantation for neuroblastoma: a report from the Childrens Cancer Group. J Clin Oncol. 1994;12:2382–9.PubMedCrossRefGoogle Scholar
  34. 34.
    Stram DO, Matthay KK, O’Leary M, Reynolds CP, Haase GM, Atkinson JB, Brodeur GM, Seeger RC. Consolidation chemoradiotherapy and autologous bone marrow transplantation versus continued chemotherapy for metastatic neuroblastoma: a report of two concurrent Children’s Cancer Group studies [see comments]. J Clin Oncol. 1996;14:2417–26.PubMedCrossRefGoogle Scholar
  35. 35.
    Berthold F, Boos J, Burdach S, Erttmann R, Henze G, Hermann J, Klingebiel T, Kremens B, Schilling FH, Schrappe M, 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.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    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.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Villablanca JG, Matthay KK, Swift PS, Harris RE, Ramsay NK, Brodeur GM, Sondel PM, Stram D, Reynolds CP, Seeger RC. Phase I trial of carboplatin, etoposide, melphalan and local irradiation (CEM-LI) with purged autologous bone marrow transplantation for children with high risk neuroblastoma. Med Pediatr Oncol. 1999;33:170.Google Scholar
  38. 38.
    Kreissman SG, Seeger RC, Matthay KK, London WB, Sposto R, Grupp SA, Haas-Kogan DA, Laquaglia MP, Yu AL, Diller L, et al. Purged versus non-purged peripheral blood stem-cell transplantation for high-risk neuroblastoma (COG A3973): a randomised phase 3 trial. Lancet Oncol. 2013;14:999–1008.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Bensimhon P, Villablanca JG, Sender LS, Matthay KK, Park JR, Seeger R, London WB, Yap JS, Kreissman SG. Peripheral blood stem cell support for multiple cycles of dose intensive induction therapy is feasible with little risk of tumor contamination in advanced stage neuroblastoma: a report from the Childrens Oncology Group. Pediatr Blood Cancer. 2010;54:596–602.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Grupp SA, Stern JW, Bunin N, Nancarrow C, Ross AA, Mogul M, Adams R, Grier HE, Gorlin JB, Shamberger R, et al. Tandem high-dose therapy in rapid sequence for children with high-risk neuroblastoma. J Clin Oncol Off J Am Soc Clin Oncol. 2000;18:2567–75.CrossRefGoogle Scholar
  41. 41.
    Seif AE, Naranjo A, Baker DL, Bunin NJ, Kletzel M, Kretschmar CS, Maris JM, McGrady PW, von Allmen D, Cohn SL, et al. A pilot study of tandem high-dose chemotherapy with stem cell rescue as consolidation for high-risk neuroblastoma: Children’s Oncology Group study ANBL00P1. Bone Marrow Transplant. 2013;48:947–52.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Park JR, Kreissman SG, London WB, Naranjo A, Cohn SL, Hogarty MD, Tenney SC, Haas-Kogan D, Shaw PJ, Geiger JD, et al. A phase 3 randomized clinical trial (RCT) of tandem myeloablative autologous stem cell transplant (ASCT) using peripheral blood stem cell (PBSC) as consolidation therapy for high-risk neuroblastoma (HR-NB): a Children’s Oncology group (COG) study. J Clin Oncol. 2016;34  https://doi.org/10.1200/JCO.2016.34.15_suppl.LBA3.CrossRefGoogle Scholar
  43. 43.
    Matthay KK, Yanik G, Messina J, Quach A, Huberty J, Cheng SC, Veatch J, Goldsby R, Brophy P, Kersun LS, et al. Phase II study on the effect of disease sites, age, and prior therapy on response to iodine-131-metaiodobenzylguanidine therapy in refractory neuroblastoma. J Clin Oncol. 2007;25:1054–60.PubMedCrossRefGoogle Scholar
  44. 44.
    Wilson JS, Gains JE, Moroz V, Wheatley K, Gaze MN. A systematic review of 131I-meta iodobenzylguanidine molecular radiotherapy for neuroblastoma. Eur J Cancer. 2014;50:801–15.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Federico SM, McCarville MB, Shulkin BL, Sondel PM, Hank JA, Hutson P, Meagher M, Shafer A, Ng CY, Leung W, 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.PubMedCrossRefGoogle Scholar
  46. 46.
    Marachelian A, Villablanca JG, Liu CW, Liu B, Goodarzian F, Lai HA, Shimada H, Tran HC, Parra JA, Gallego R, et al. Expression of five neuroblastoma genes in bone marrow or blood of patients with relapsed/refractory neuroblastoma provides a new biomarker for disease and prognosis. Clin Cancer Res. 2017;23:5374–83.CrossRefGoogle Scholar
  47. 47.
    Yanik GA, Parisi MT, Shulkin BL, Naranjo A, Kreissman SG, London WB, Villablanca JG, Maris JM, Park JR, Cohn SL, et al. Semiquantitative mIBG scoring as a prognostic indicator in patients with stage 4 neuroblastoma: a report from the Children’s oncology group. J Nucl Med. 2013;54:541–8.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Matthay KK. Targeted isotretinoin in neuroblastoma: kinetics, genetics, or absorption. Clin Cancer Res. 2013;19:311–3.PubMedCrossRefGoogle Scholar
  49. 49.
    Veal GJ, Cole M, Errington J, Pearson AD, Foot AB, Whyman G, Boddy AV. Pharmacokinetics and metabolism of 13-cis-retinoic acid (isotretinoin) in children with high-risk neuroblastoma – a study of the United Kingdom Children’s Cancer Study group. Br J Cancer. 2007;96:424–31.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Matthay K, Reynolds C, Seeger R, Shimada H, Adkins E, 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.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Gilman AL, Ozkaynak MF, Matthay KK, Krailo M, Yu AL, Gan J, Sternberg A, Hank JA, Seeger R, Reaman GH, et al. Phase I study of ch14.18 with granulocyte-macrophage colony-stimulating factor and interleukin-2 in children with neuroblastoma after autologous bone marrow transplantation or stem-cell rescue: a report from the Children’s Oncology Group. J Clin Oncol Off J Am Soc Clin Oncol. 2009;27:85–91.CrossRefGoogle Scholar
  52. 52.
    Ozkaynak MF, Sondel PM, Krailo MD, Gan J, Javorsky B, Reisfeld RA, Matthay KK, Reaman GH, Seeger RC. Phase I study of chimeric human/murine anti-ganglioside G(D2) monoclonal antibody (ch14.18) with granulocyte-macrophage colony-stimulating factor in children with neuroblastoma immediately after hematopoietic stem-cell transplantation: a Children’s Cancer Group study. J Clin Oncol. 2000;18:4077–85.CrossRefGoogle Scholar
  53. 53.
    Uttenreuther-Fischer MM, Huang CS, Reisfeld RA, Yu AL. Pharmacokinetics of anti-ganglioside GD2 mAb 14G2a in a phase I trial in pediatric cancer patients. Cancer Immunol Immunother. 1995;41:29–36.PubMedCrossRefGoogle Scholar
  54. 54.
    Yu AL, Uttenreuther MM, Kamps A, Batova A, Reisfeld RA. Combined use of a human-mouse chimeric anti-GD2 (ch14.18) and GM-CSF in the treatment of refractory neuroblastoma. Antib Immunoconjug Radiopharm. 1995;8:12.Google Scholar
  55. 55.
    Hank JA, Robinson RR, Surfus J, Mueller BM, Reisfeld RA, Cheung NK, Sondel PM. Augmentation of antibody dependent cell mediated cytotoxicity following in vivo therapy with recombinant interleukin 2. Cancer Res. 1990;50:5234–9.PubMedGoogle Scholar
  56. 56.
    Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, Smith M, Anderson B, Villablanca JG, Matthay KK, et al. Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med. 2010;363:1324–34.PubMedPubMedCentralCrossRefGoogle Scholar
  57. 57.
    London WB, Frantz CN, Campbell LA, Seeger RC, Brumback BA, Cohn SL, Matthay KK, Castleberry RP, Diller L. Phase II randomized comparison of topotecan plus cyclophosphamide versus topotecan alone in children with recurrent or refractory neuroblastoma: a Children’s Oncology Group study. J Clin Oncol Off J Am Soc Clin Oncol. 2010;28:3808–15.CrossRefGoogle Scholar
  58. 58.
    Bagatell R, London WB, Wagner LM, Voss SD, Stewart CF, Maris JM, Kretschmar C, Cohn SL. Phase II study of irinotecan and temozolomide in children with relapsed or refractory neuroblastoma: a Children’s Oncology Group study. J Clin Oncol Off J Am Soc Clin Oncol. 2011;29:208–13.CrossRefGoogle Scholar
  59. 59.
    Rubie H, Chisholm J, Defachelles AS, Morland B, Munzer C, Valteau-Couanet D, Mosseri V, Bergeron C, Weston C, Coze C, et al. Phase II study of temozolomide in relapsed or refractory high-risk neuroblastoma: a joint Societe Francaise des Cancers de l’Enfant and United Kingdom Children Cancer Study Group-New Agents Group Study. J Clin Oncol. 2006;24:5259–64.PubMedCrossRefGoogle Scholar
  60. 60.
    Fox E, Mosse YP, Meany HM, Gurney JG, Khanna G, Jackson HA, Gordon G, Shusterman S, Park JR, Cohn SL, et al. Time to disease progression in children with relapsed or refractory neuroblastoma treated with ABT-751: a report from the Children’s Oncology Group (ANBL0621). Pediatr Blood Cancer. 2014;61:990–6.PubMedCrossRefGoogle Scholar
  61. 61.
    Langevin AM, Bernstein M, Kuhn JG, Blaney SM, Ivy P, Sun J, Chen Z, Adamson PC. A phase II trial of rebeccamycin analogue (NSC #655649) in children with solid tumors: a Children’s Oncology Group study. Pediatr Blood Cancer. 2008;50:577–80.PubMedCrossRefGoogle Scholar
  62. 62.
    Beaty O 3rd, Berg S, Blaney S, Malogolowkin M, Krailo M, Knight R, Schaiquevich P, Stewart C, Chen Z, Nelson M, et al. A phase II trial and pharmacokinetic study of oxaliplatin in children with refractory solid tumors: a Children’s Oncology Group study. Pediatr Blood Cancer. 2010;55:440–5.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Kuttesch JF Jr, Krailo MD, Madden T, Johansen M, Bleyer A, Children’s Oncology Group. Phase II evaluation of intravenous vinorelbine (Navelbine) in recurrent or refractory pediatric malignancies: a Children’s Oncology Group study. Pediatr Blood Cancer. 2009;53:590–3.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Zwerdling T, Krailo M, Monteleone P, Byrd R, Sato J, Dunaway R, Seibel N, Chen Z, Strain J, Reaman G, et al. Phase II investigation of docetaxel in pediatric patients with recurrent solid tumors: a report from the Children’s Oncology Group. Cancer. 2006;106:1821–8.PubMedCrossRefGoogle Scholar
  65. 65.
    Warwick AB, Malempati S, Krailo M, Melemed A, Gorlick R, Ames MM, Safgren SL, Adamson PC, Blaney SM. Phase 2 trial of pemetrexed in children and adolescents with refractory solid tumors: a Children’s Oncology Group study. Pediatr Blood Cancer. 2013;60:237–41.PubMedCrossRefGoogle Scholar
  66. 66.
    Jacobs S, Fox E, Krailo M, Hartley G, Navid F, Wexler L, Blaney SM, Goodwin A, Goodspeed W, Balis FM, et al. Phase II trial of ixabepilone administered daily for five days in children and young adults with refractory solid tumors: a report from the children’s oncology group. Clin Cancer Res. 2010;16:750–4.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    DuBois SG, Chesler L, Groshen S, Hawkins R, Goodarzian F, Shimada H, Yanik G, Tagen M, Stewart C, Mosse YP, et al. Phase I study of vincristine, irinotecan, and 131I-metaiodobenzylguanidine for patients with relapsed or refractory neuroblastoma: a new approaches to neuroblastoma therapy trial. Clin Cancer Res. 2012;18:2679–86.PubMedCrossRefGoogle Scholar
  68. 68.
    DuBois SG, Allen S, Bent M, Hilton JF, Hollinger F, Hawkins R, Courtier J, Mosse YP, Matthay KK. Phase I/II study of (131)I-MIBG with vincristine and 5 days of irinotecan for advanced neuroblastoma. Br J Cancer. 2015a;112:644–9.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    DuBois SG, Groshen S, Park JR, Haas-Kogan DA, Yang X, Geier E, Chen E, Giacomini K, Weiss B, Cohn SL, et al. Phase I study of vorinostat as a radiation sensitizer with 131I-metaiodobenzylguanidine (131I-MIBG) for patients with relapsed or refractory neuroblastoma. Clin Cancer Res. 2015b;21:2715–21.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    DuBois SG, Marachelian A, Fox E, Kudgus RA, Reid JM, Groshen S, Malvar J, Bagatell R, Wagner L, Maris JM, et al. Phase I study of the aurora a kinase inhibitor alisertib in combination with irinotecan and temozolomide for patients with relapsed or refractory neuroblastoma: a NANT (new approaches to neuroblastoma therapy) trial. J Clin Oncol. 2016;34(12):1368–75.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Mosse YP, Lipsitz E, Fox E, Teachey DT, Maris JM, Weigel B, Adamson PC, Ingle MA, Ahern CH, Blaney SM. Pediatric phase I trial and pharmacokinetic study of MLN8237, an investigational oral selective small-molecule inhibitor of Aurora kinase A: a Children’s Oncology Group Phase I Consortium study. Clin Cancer Res. 2012;18:6058–64.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Mosse YP, Voss SD, Lim MS, Rolland D, Minard CG, Fox E, Adamson P, Wilner K, Blaney SM, Weigel BJ. Targeting ALK with crizotinib in pediatric anaplastic large cell lymphoma and inflammatory myofibroblastic tumor: a Children’s Oncology Group study. J Clin Oncol. 2017;35:3215–21.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Infarinato NR, Park JH, Krytska K, Ryles HT, Sano R, Szigety KM, Li Y, Zou HY, Lee NV, Smeal T, et al. The ALK/ROS1 inhibitor PF-06463922 overcomes primary resistance to crizotinib in ALK-driven neuroblastoma. Cancer Discov. 2015;6(1):96–107.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Maurer BJ, Kang MH, Villablanca JG, Janeba J, Groshen S, Matthay KK, Sondel PM, Maris JM, Jackson HA, Goodarzian F, et al. Phase I trial of fenretinide delivered orally in a novel organized lipid complex in patients with relapsed/refractory neuroblastoma: a report from the new approaches to neuroblastoma therapy (NANT) consortium. Pediatr Blood Cancer. 2013;60:1801–8.PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Shusterman S, London WB, Gillies SD, Hank JA, Voss SD, Seeger RC, Reynolds CP, Kimball J, Albertini MR, Wagner B, et al. Antitumor activity of hu14.18-IL2 in patients with relapsed/refractory neuroblastoma: a Children’s Oncology Group (COG) phase II study. J Clin Oncol. 2010;28:4969–75.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Mody R, Naranjo A, Van Ryn C, Yu AL, London WB, Shulkin BL, Parisi MT, Servaes S-E-N, Diccianni MB, Sondel PM, 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;18:946–57.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Kushner BH, Cheung IY, Modak S, Kramer K, Ragupathi G, Cheung NK. Phase I trial of a bivalent gangliosides vaccine in combination with beta-glucan for high-risk neuroblastoma in second or later remission. Clin Cancer Res. 2014;20:1375–82.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Villablanca JG, London WB, Naranjo A, McGrady P, Ames MM, Reid JM, McGovern RM, Buhrow SA, Jackson H, Stranzinger E, et al. Phase II study of oral capsular 4-hydroxyphenylretinamide (4-HPR/fenretinide) in pediatric patients with refractory or recurrent neuroblastoma: a report from the Children’s Oncology Group. Clin Cancer Res. 2011;17:6858–66.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Weigel B, Malempati S, Reid JM, Voss SD, Cho SY, Chen HX, Krailo M, Villaluna D, Adamson PC, Blaney SM. Phase 2 trial of cixutumumab in children, adolescents, and young adults with refractory solid tumors: a report from the Children’s Oncology Group. Pediatr Blood Cancer. 2014;61:452–6.PubMedCrossRefGoogle Scholar
  80. 80.
    Mosse YP, Lim MS, Voss SD, Wilner K, Ruffner K, Laliberte J, Rolland D, Balis FM, Maris JM, Weigel BJ, et al. Safety and activity of crizotinib for paediatric patients with refractory solid tumours or anaplastic large-cell lymphoma: a Children’s Oncology Group phase 1 consortium study. Lancet Oncol. 2013;14:472–80.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Pearson ADJ, Pinkerton CR, Lewis IJ, Imeson J, Ellershaw C, Machin D. High-dose rapid and standard induction chemotherapy for patients aged over 1 year with stage 4 neuroblastoma: a randomised trial. Lancet Oncol. 2008;9:247–56.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Ladenstein R, Valteau-Couanet D, Brock P, Yaniv I, Castel V, Laureys G, Malis J, Papadakis V, Lacerda A, Ruud E, 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 Off J Am Soc Clin Oncol. 2010;28:3516–24.CrossRefGoogle Scholar
  83. 83.
    Amoroso L, Erminio G, Makin G, Pearson ADJ, Brock P, Valteau-Couanet D, Castel V, Pasquet M, Laureys G, Thomas C, et al. Topotecan-vincristine-doxorubicin in stage 4 high-risk neuroblastoma patients failing to achieve a complete metastatic response to rapid COJEC: a SIOPEN study. Cancer Res Treat. 2018;50:148–55.PubMedCrossRefGoogle Scholar
  84. 84.
    Cheung NK, Kushner BH, LaQuaglia M, Kramer K, Gollamudi S, Heller G, Gerald W, Yeh S, Finn R, Larson SM, et al. N7: a novel multi-modality therapy of high risk neuroblastoma (NB) in children diagnosed over 1 year of age. Med Pediatr Oncol. 2001;36:227–30.PubMedCrossRefGoogle Scholar
  85. 85.
    Mora J, Cruz O, Lavarino C, Rios J, Vancells M, Parareda A, Salvador H, Suñol M, Carrasco R, Guillen A, et al. Results of induction chemotherapy in children older than 18 months with stage-4 neuroblastoma treated with an adaptive-to-response modified N7 protocol (mN7). Clin Transl Oncol. 2015;17:521–9.PubMedCrossRefGoogle Scholar
  86. 86.
    Kohler JA, Ellershaw C, Machin D, Neuroblastoma Working Group of the Children’s Cancer and Leukaemia Group. Response to N7 induction chemotherapy in children more than one year of age diagnosed with metastatic neuroblastoma treated in UKCCSG centers. Pediatr Blood Cancer. 2007;49:234–9.PubMedCrossRefGoogle Scholar
  87. 87.
    Valteau-Couanet D, Michon J, Boneu A, Rodary C, Perel Y, Bergeron C, Rubie H, Coze C, Plantaz D, Bernard F, et al. Results of induction chemotherapy in children older than 1 year with a stage 4 neuroblastoma treated with the NB 97 French Society of Pediatric Oncology (SFOP) protocol. J Clin Oncol Off J Am Soc Clin Oncol. 2005;23:532–40.CrossRefGoogle Scholar
  88. 88.
    Valteau-Couanet D, Le Deley M-C, Bergeron C, Ducassou S, Michon J, Rubie H, Le Teuff G, Coze C, Plantaz D, Sirvent N, et al. Long-term results of the combination of the N7 induction chemotherapy and the busulfan-melphalan high dose chemotherapy. Pediatr Blood Cancer. 2014;61:977–81.PubMedCrossRefGoogle Scholar
  89. 89.
    Hartmann O, Valteau-Couanet D, Vassal G, Lapierre V, Brugières L, Delgado R, Couanet D, Lumbroso J, Benhamou E. Prognostic factors in metastatic neuroblastoma in patients over 1 year of age treated with high-dose chemotherapy and stem cell transplantation: a multivariate analysis in 218 patients treated in a single institution. Bone Marrow Transplant. 1999;23:789–95.PubMedCrossRefGoogle Scholar
  90. 90.
    Proust-Houdemont S, Pasqualini C, Blanchard P, Dufour C, Benhamou E, Goma G, Semeraro M, Raquin M-A, Hartmann O, Valteau-Couanet D. Busulfan-melphalan in high-risk neuroblastoma: the 30-year experience of a single institution. Bone Marrow Transplant. 2016;51:1076–81.PubMedCrossRefGoogle Scholar
  91. 91.
    Ladenstein R, Poetschger U, Gray J, Valteau-Couanet D, Luksch R, Castel V, et al. Toxicity and outcome of anti-GD2 antibody ch14.18/CHO in front-line, high-risk patients with neuroblastoma: Final results of the phase III immunotherapy randomisation (HR-NBL1/SIOPEN trial). J Clin Oncol. 2016;34:10500.CrossRefGoogle Scholar
  92. 92.
    Lode HN, Valteau-Couanet D, Garaventa A, Gray J, Castel V, Yaniv I, et al. Long-term infusion of anti-GD2 antibody ch14.18/CHO in combination with interleukin-2 (IL2) activity and efficacy in high-risk relapsed/refractory neuroblastoma patients. J Clin Oncol. 2015;33:10080.CrossRefGoogle Scholar
  93. 93.
    Pasqualini C, Dufour C, Goma G, Raquin M-A, Lapierre V, Valteau-Couanet D. Tandem high-dose chemotherapy with thiotepa and busulfan-melphalan and autologous stem cell transplantation in very high-risk neuroblastoma patients. Bone Marrow Transplant. 2016;51:227–31.PubMedCrossRefGoogle Scholar
  94. 94.
    Gaze MN, Chang Y-C ‘i, Flux GD, Mairs RJ, Saran FH, Meller ST. Feasibility of dosimetry-based high-dose 131I-meta-iodobenzylguanidine with topotecan as a radiosensitizer in children with metastatic neuroblastoma. Cancer Biother Radiopharm. 2005;20:195–9.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Gaze MN, Bomanji JB, Lacerda A, Saran FH, Brock PR, Uyttebroeck A, et al. Long-term outcome of MATIN, a schedule of high-administered activity iodine 131 metaiodobenzylguanidine and topotecan in neuroblastoma: a SIOPEN study. Toronto: ANR; 2012.Google Scholar
  96. 96.
    Ferry I, Kolesnikov-Gauthier H, Oudoux A, Cougnenc O, Schleiermacher G, Michon J, Bogart E, Chastagner P, Proust S, Valteau-Couanet D, et al. Feasibility of busulfan melphalan and stem cell rescue after 131I-MIBG and topotecan therapy for refractory or relapsed metastatic neuroblastoma: the French experience. J Pediatr Hematol Oncol. 2018;40(6):426–32.PubMedCrossRefGoogle Scholar
  97. 97.
    Berthold F, Burdach S, Kremens B, Lampert F, Niethammer D, Riehm H, Ritter J, Treuner J, Utsch S, Zieschang J. 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.PubMedCrossRefGoogle Scholar
  98. 98.
    Berthold F, Hero B, Kremens B, Handgretinger R, Henze G, Schilling FH, Schrappe M, Simon T, Spix C. Long-term results and risk profiles of patients in five consecutive trials (1979–1997) with stage 4 neuroblastoma over 1 year of age. Cancer Lett. 2003;197:11–7.PubMedCrossRefGoogle Scholar
  99. 99.
    Park JR, Slattery J, Gooley T, Hawkins D, Lindsley K, Villablanca JG, et al. Phase I topotecan preparative regimen for high-risk neuroblastoma, high-grade glioma, and refractory/recurrent pediatric solid tumors. Med Pediatr Oncol. 2000;35:719–23.PubMedCrossRefGoogle Scholar
  100. 100.
    Längler A, Christaras A, Abshagen K, Krauth K, Hero B, Berthold F. Topotecan in the treatment of refractory neuroblastoma and other malignant tumors in childhood – a phase-II-study. Klin Padiatr. 2002;214:153–6.PubMedCrossRefGoogle Scholar
  101. 101.
    Furman WL, Shulkin BL, SA F, MB M, AM D, MJ K, et al. Early response rates and Curie scores at end of induction: an update from a phase II study of an anti-GD2 monoclonal antibody (mAb) with chemotherapy (CT) in newly diagnosed patients (pts) with high-risk (HR) neuroblastoma (NB). J Clin Oncol. 2017;35(Suppl):10534.CrossRefGoogle Scholar
  102. 102.
    Rubie H, Geoerger B, Frappaz D, Schmitt A, Leblond P, Ndiaye A, Aerts I, Le Deley M-C, Gentet J-C, Paci A, et al. Phase I study of topotecan in combination with temozolomide (TOTEM) in relapsed or refractory paediatric solid tumours. Eur J Cancer. 2010;1990(46):2763–70.CrossRefGoogle Scholar
  103. 103.
    Di Giannatale A, Dias-Gastellier N, Devos A, Mc Hugh K, Boubaker A, Courbon F, Verschuur A, Ducassoul S, Malekzadeh K, Casanova M, et al. Phase II study of temozolomide in combination with topotecan (TOTEM) in relapsed or refractory neuroblastoma: a European Innovative Therapies for Children with Cancer-SIOP-European Neuroblastoma study. Eur J Cancer. 2014;50:170–7.PubMedCrossRefGoogle Scholar
  104. 104.
    Segerström L, Fuchs D, Bäckman U, Holmquist K, Christofferson R, Azarbayjani F. The anti-VEGF antibody bevacizumab potently reduces the growth rate of high-risk neuroblastoma xenografts. Pediatr Res. 2006;60:576–81.PubMedCrossRefGoogle Scholar
  105. 105.
    Dickson PV, Hamner JB, Sims TL, Fraga CH, Ng CYC, Rajasekeran S, Hagedorn NL, McCarville MB, Stewart CF, Davidoff AM. Bevacizumab-induced transient remodeling of the vasculature in neuroblastoma xenografts results in improved delivery and efficacy of systemically administered chemotherapy. Clin Cancer Res. 2007;13:3942–50.PubMedCrossRefGoogle Scholar
  106. 106.
    Corbacioglu S, Steinbach D, Lode HN, Gruhn B, Fruehwald M, Broeckelmann M, Suttorp M, Escherich G, Cario G, Ehlert K, et al. The RIST design: a molecularly targeted multimodal approach for the treatment of patients with relapsed and refractory neuroblastoma. J Clin Oncol. 2013;31:–10017.Google Scholar
  107. 107.
    Moreno L, Caron H, Geoerger B, Eggert A, Schleiermacher G, Brock P, Valteau-Couanet D, Chesler L, Schulte JH, De Preter K, et al. Accelerating drug development for neuroblastoma – new drug development strategy: an innovative therapies for children with cancer, European Network for Cancer Research in Children and Adolescents and International Society of Paediatric Oncology Europe Neuroblastoma project. Expert Opin Drug Discov. 2017;12:801–11.PubMedGoogle Scholar
  108. 108.
    Illhardt T, Toporski J, Feuchtinger T, Turkiewicz D, Teltschik H-M, Ebinger M, Schwarze C-P, Holzer U, Lode HN, Albert MH, et al. Haploidentical stem cell transplantation for refractory/relapsed neuroblastoma. Biol Blood Marrow Transplant. 2018;24:1005–12.PubMedCrossRefGoogle Scholar
  109. 109.
    Thomas S, Straathof K, Himoudi N, Anderson J, Pule M. An optimized GD2-targeting retroviral cassette for more potent and safer cellular therapy of neuroblastoma and other cancers. PLoS One. 2016;11:e0152196.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Pediatric Hematology-OncologyUniversity of California San Francisco School of Medicine and UCSF Benioff Children’s HospitalSan FranciscoUSA
  2. 2.Children and Adolescent Oncology DepartmentGustave RoussyVillejuif CedexFrance

Personalised recommendations