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Cell and Tissue Research

, Volume 372, Issue 2, pp 195–209 | Cite as

Neuroblastoma: clinical and biological approach to risk stratification and treatment

  • Vanessa P. Tolbert
  • Katherine K. Matthay
Review

Abstract

Neuroblastoma is the most common extra-cranial solid tumor of childhood and the most common in the first year of life. It is a unique malignancy in that infants often present with either localized or metastatic disease that can spontaneously regress without intervention while older children can succumb to the disease after months to years of arduous therapy. Given this wide range of outcomes, the International Neuroblastoma Risk Group was created to stratify patients based on presenting characteristics and tumor biology in order to guide intensity of treatment strategies. The goal has been to decrease therapy for low-risk patients to avoid long-term complications while augmenting and targeting therapies for high-risk patients to improve overall survival. The international risk stratification depends on age, stage, histology, MYCN gene amplification status, tumor cell ploidy and segmental chromosomal abnormalities. Treatment for asymptomatic low-risk patients with an estimated survival of > 98% is often observation or surgical resection alone, whereas intermediate-risk patients with an estimated survival of > 90% require moderate doses of response-adjusted chemotherapy along with resection. High-risk patients undergo multiple cycles of combination chemotherapy before surgery, followed by consolidation with myeloablative autologous hematopoietic stem cell transplantation and local radiation and finally immunotherapy with differentiation therapy as maintenance phase. With this approach, outcome for patients with neuroblastoma has improved, as the field continues to expand efforts in more targeted therapies for high-risk patients.

Keywords

Neuroblastoma Pediatric oncology Clinical presentation Treatment Risk classification 

Notes

Funding information

This work was supported by National Cancer Institute P01 CA217959 and the Alex Scott Lemonade Foundation Center of Excellence, Dougherty Foundation, Mildred V. Strouss Chair, and the Conner Fund.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Adkins ES, Sawin R, Gerbing RB, London WB, Matthay KK, Haase GM (2004) Efficacy of complete resection for high-risk neuroblastoma: a Children’s Cancer Group study. J Pediatr Surg 39:931–936PubMedCrossRefGoogle Scholar
  2. Ambros PF, Ambros IM, Brodeur GM, Haber M, Khan J, Nakagawara A, Schleiermacher G, Speleman F, Spitz R, London WB, Cohn SL, Pearson AD, Maris JM (2009) International consensus for neuroblastoma molecular diagnostics: report from the International Neuroblastoma Risk Group (INRG) Biology Committee. Br J Cancer 100:1471–1482PubMedPubMedCentralCrossRefGoogle Scholar
  3. Amoroso L, Erminio G, Makin G, Pearson AD, Brock P, Valteau-Couanet D, Castel V, Pasquet M, Laureys G, Thomas C, Luksch R, Ladenstein R, Haupt R, Garaventa A, Group S (2017) 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 Google Scholar
  4. Antunes NL, Khakoo Y, Matthay KK, Seeger RC, Stram DO, Gerstner E, Abrey LE, Dalmau J (2000) Antineuronal antibodies in patients with neuroblastoma and paraneoplastic opsoclonus-myoclonus. J Pediatr Hematol Oncol 22:315–320PubMedCrossRefGoogle Scholar
  5. Attiyeh EF, London WB, Mosse YP, Wang Q, Winter C, Khazi D, McGrady PW, Seeger RC, Look AT, Shimada H, Brodeur GM, Cohn SL, Matthay KK, Maris JM, Children's Oncology G (2005) Chromosome 1p and 11q deletions and outcome in neuroblastoma. N Engl J Med 353:2243–2253PubMedCrossRefGoogle Scholar
  6. Bagatell R, Beck-Popovic M, London WB, Zhang Y, Pearson AD, Matthay KK, Monclair T, Ambros PF, Cohn SL, International Neuroblastoma Risk G (2009) Significance of MYCN amplification in international neuroblastoma staging system stage 1 and 2 neuroblastoma: a report from the international Neuroblastoma Risk Group database. J Clin Oncol 27:365–370PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bagatell R, London WB, Wagner LM, Voss SD, Stewart CF, Maris JM, Kretschmar C, Cohn SL (2011) Phase II study of irinotecan and temozolomide in children with relapsed or refractory neuroblastoma: a Children’s Oncology Group study. J Clin Oncol 29:208–213PubMedCrossRefGoogle Scholar
  8. Baker DL, Schmidt ML, Cohn SL, Maris JM, London WB, Buxton A, Stram D, Castleberry RP, Shimada H, Sandler A, Shamberger RC, Look AT, Reynolds CP, Seeger RC, Matthay KK, Children's Oncology G (2010) Outcome after reduced chemotherapy for intermediate-risk neuroblastoma. N Engl J Med 363:1313–1323PubMedPubMedCentralCrossRefGoogle Scholar
  9. Beiske K, Burchill SA, Cheung IY, Hiyama E, Seeger RC, Cohn SL, Pearson AD, Matthay KK, International neuroblastoma Risk Group Task F (2009) Consensus criteria for sensitive detection of minimal neuroblastoma cells in bone marrow, blood and stem cell preparations by immunocytology and QRT-PCR: recommendations by the International Neuroblastoma Risk Group Task Force. Br J Cancer 100:1627-1637Google Scholar
  10. Berthold F, Boos J, Burdach S, Erttmann R, Henze G, Hermann J, Klingebiel T, Kremens B, Schilling FH, Schrappe M, Simon T, Hero B (2005) 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 6:649–658PubMedCrossRefGoogle Scholar
  11. Biermann M, Schwarzlmuller T, Fasmer KE, Reitan BC, Johnsen B, Rosendahl K (2013) Is there a role for PET-CT and SPECT-CT in pediatric oncology? Acta Radiol 54:1037–1045PubMedCrossRefGoogle Scholar
  12. Bown N, Cotterill S, Lastowska M, O'Neill S, Pearson AD, Plantaz D, Meddeb M, Danglot G, Brinkschmidt C, Christiansen H, Laureys G, Speleman F, Nicholson J, Bernheim A, Betts DR, Vandesompele J, Van Roy N (1999) Gain of chromosome arm 17q and adverse outcome in patients with neuroblastoma. N Engl J Med 340:1954–1961PubMedCrossRefGoogle Scholar
  13. Brodeur GM, Pritchard J, Berthold F, Carlsen NL, Castel V, Castelberry RP, De Bernardi B, Evans AE, Favrot M, Hedborg F et al (1993) Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J Clin Oncol 11:1466–1477PubMedCrossRefGoogle Scholar
  14. Brodeur GM, Seeger RC, Schwab M, Varmus HE, Bishop JM (1984) Amplification of N-myc in untreated human neuroblastomas correlates with advanced disease stage. Science 224:1121–1124PubMedCrossRefGoogle Scholar
  15. Burchill SA, Beiske K, Shimada H, Ambros PF, Seeger R, Tytgat GA, Brock PR, Haber M, Park JR, Berthold F (2017) Recommendations for the standardization of bone marrow disease assessment and reporting in children with neuroblastoma on behalf of the International Neuroblastoma Response Criteria Bone Marrow Working Group. Cancer 123:1095–1105PubMedCrossRefGoogle Scholar
  16. Campbell K, Gastier-Foster JM, Mann M, Naranjo AH, Van Ryn C, Bagatell R, Matthay KK, London WB, Irwin MS, Shimada H, Granger MM, Hogarty MD, Park JR, DuBois SG (2017) Association of MYCN copy number with clinical features, tumor biology, and outcomes in neuroblastoma: a report from the Children’s Oncology Group. Cancer Google Scholar
  17. Chanthery YH, Gustafson WC, Itsara M, Persson A, Hackett CS, Grimmer M, Charron E, Yakovenko S, Kim G, Matthay KK, Weiss WA (2012) Paracrine signaling through MYCN enhances tumor-vascular interactions in neuroblastoma. Sci Transl Med 4:115ra113Google Scholar
  18. Chen Y, Takita J, Choi YL, Kato M, Ohira M, Sanada M, Wang L, Soda M, Kikuchi A, Igarashi T, Nakagawara A, Hayashi Y, Mano H, Ogawa S (2008) Oncogenic mutations of ALK kinase in neuroblastoma. Nature 455:971–974PubMedCrossRefGoogle Scholar
  19. Cheung NK, Zhang J, Lu C, Parker M, Bahrami A, Tickoo SK, Heguy A, Pappo AS, Federico S, Dalton J, Cheung IY, Ding L, Fulton R, Wang J, Chen X, Becksfort J, Wu J, Billups CA, Ellison D, Mardis ER, Wilson RK, Downing JR, Dyer MA, St Jude Children’s Research Hospital-Washington University Pediatric Cancer Genome P (2012) Association of age at diagnosis and genetic mutations in patients with neuroblastoma. JAMA 307:1062–1071PubMedPubMedCentralCrossRefGoogle Scholar
  20. Cohn SL, Pearson AD, London WB, Monclair T, Ambros PF, Brodeur GM, Faldum A, Hero B, Iehara T, Machin D, Mosseri V, Simon T, Garaventa A, Castel V, Matthay KK (2009) The International Neuroblastoma Risk Group (INRG) classification system: an INRG Task Force report. J Clin Oncol Off J Am Soc Clin Oncol 27:289–297CrossRefGoogle Scholar
  21. Cole KA, Huggins J, Laquaglia M, Hulderman CE, Russell MR, Bosse K, Diskin SJ, Attiyeh EF, Sennett R, Norris G, Laudenslager M, Wood AC, Mayes PA, Jagannathan J, Winter C, Mosse YP, Maris JM (2011) RNAi screen of the protein kinome identifies checkpoint kinase 1 (CHK1) as a therapeutic target in neuroblastoma. Proc Natl Acad Sci U S A 108:3336–3341PubMedPubMedCentralCrossRefGoogle Scholar
  22. De Bernardi B, Gerrard M, Boni L, Rubie H, Canete A, Di Cataldo A, Castel V, Forjaz de Lacerda A, Ladenstein R, Ruud E, Brichard B, Couturier J, Ellershaw C, Munzer C, Bruzzi P, Michon J, Pearson AD (2009) Excellent outcome with reduced treatment for infants with disseminated neuroblastoma without MYCN gene amplification. J Clin Oncol 27:1034–1040PubMedCrossRefGoogle Scholar
  23. Decarolis B, Schneider C, Hero B, Simon T, Volland R, Roels F, Dietlein M, Berthold F, Schmidt M (2013) Iodine-123 metaiodobenzylguanidine scintigraphy scoring allows prediction of outcome in patients with stage 4 neuroblastoma: results of the Cologne interscore comparison study. J Clin Oncol 31:944–951PubMedCrossRefGoogle Scholar
  24. Defferrari R, Mazzocco K, Ambros IM, Ambros PF, Bedwell C, Beiske K, Benard J, Berbegall AP, Bown N, Combaret V, Couturier J, Erminio G, Gambini C, Garaventa A, Gross N, Haupt R, Kohler J, Jeison M, Lunec J, Marques B, Martinsson T, Noguera R, Parodi S, Schleiermacher G, Tweddle DA, Valent A, Van Roy N, Vicha A, Villamon E, Tonini GP (2015) Influence of segmental chromosome abnormalities on survival in children over the age of 12 months with unresectable localised peripheral neuroblastic tumours without MYCN amplification. Br J Cancer 112:290–295PubMedCrossRefGoogle Scholar
  25. Di Giannatale A, Dias-Gastellier N, Devos A, Mc Hugh K, Boubaker A, Courbon F, Verschuur A, Ducassoul S, Malekzadeh K, Casanova M, Amoroso L, Chastagner P, Zwaan CM, Munzer C, Aerts I, Landman-Parker J, Riccardi R, Le Deley MC, Geoerger B, Rubie H (2014) 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 50:170–177PubMedCrossRefGoogle Scholar
  26. Dubois SG, Geier E, Batra V, Yee SW, Neuhaus J, Segal M, Martinez D, Pawel B, Yanik G, Naranjo A, London WB, Kreissman S, Baker D, Attiyeh E, Hogarty MD, Maris JM, Giacomini K, Matthay KK (2012) Evaluation of norepinephrine transporter expression and metaiodobenzylguanidine avidity in neuroblastoma: a report from the children’s oncology group. Int J Mol Imaging 2012:250834PubMedPubMedCentralCrossRefGoogle Scholar
  27. DuBois SG, Groshen S, Park JR, Haas-Kogan DA, Yang X, Geier E, Chen E, Giacomini K, Weiss B, Cohn SL, Granger MM, Yanik GA, Hawkins R, Courtier J, Jackson H, Goodarzian F, Shimada H, Czarnecki S, Tsao-Wei D, Villablanca JG, Marachelian A, Matthay KK (2015) Phase I study of vorinostat as a radiation sensitizer with 131I-metaiodobenzylguanidine (131I-MIBG) for patients with relapsed or refractory neuroblastoma. Clin Cancer Res 21:2715–2721PubMedPubMedCentralCrossRefGoogle Scholar
  28. DuBois SG, Kalika Y, Lukens JN, Brodeur GM, Seeger RC, Atkinson JB, Haase GM, Black CT, Perez C, Shimada H, Gerbing R, Stram DO, Matthay KK (1999) Metastatic sites in stage IV and IVS neuroblastoma correlate with age, tumor biology, and survival. J Pediatr Hematol Oncol 21:181–189PubMedCrossRefGoogle Scholar
  29. DuBois SG, Marachelian A, Fox E, Kudgus RA, Reid JM, Groshen S, Malvar J, Bagatell R, Wagner L, Maris JM, Hawkins R, Courtier J, Lai H, Goodarzian F, Shimada H, Czarnecki S, Tsao-Wei D, Matthay KK, Mosse YP (2016) 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 34:1368–1375PubMedPubMedCentralCrossRefGoogle Scholar
  30. Erdreich-Epstein A, Singh AR, Joshi S, Vega FM, Guo P, Xu J, Groshen S, Ye W, Millard M, Campan M, Morales G, Garlich JR, Laird PW, Seeger RC, Shimada H, Durden DL (2017) Association of high microvessel alphavbeta3 and low PTEN with poor outcome in stage 3 neuroblastoma: rationale for using first in class dual PI3K/BRD4 inhibitor, SF1126. Oncotarget 8:52193–52210PubMedCrossRefGoogle Scholar
  31. Evageliou NF, Haber M, Vu A, Laetsch TW, Murray J, Gamble LD, Cheng NC, Liu K, Reese M, Corrigan KA, Ziegler DS, Webber H, Hayes CS, Pawel B, Marshall GM, Zhao H, Gilmour SK, Norris MD, Hogarty MD (2016) Polyamine antagonist therapies inhibit neuroblastoma initiation and progression. Clin Cancer Res 22:4391–4404PubMedCrossRefGoogle Scholar
  32. Federico SM, McCarville MB, Shulkin BL, Sondel PM, Hank JA, Hutson P, Meagher M, Shafer A, Ng CY, Leung W, Janssen WE, Wu J, Mao S, Brennan RC, Santana VM, Pappo AS, Furman WL (2017) 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 23:6441–6449PubMedCrossRefGoogle Scholar
  33. Fouladi M, Park JR, Stewart CF, Gilbertson RJ, Schaiquevich P, Sun J, Reid JM, Ames MM, Speights R, Ingle AM, Zwiebel J, Blaney SM, Adamson PC (2010) Pediatric phase I trial and pharmacokinetic study of vorinostat: a Children’s Oncology Group phase I consortium report. J Clin Oncol 28:3623–3629PubMedPubMedCentralCrossRefGoogle Scholar
  34. Franscini LC, Vazquez-Montes M, Buclin T, Perera R, Dunand M, Grouzmann E, Beck-Popovic M (2015) Pediatric reference intervals for plasma free and total metanephrines established with a parametric approach: relevance to the diagnosis of neuroblastoma. Pediatr Blood Cancer 62:587–593PubMedCrossRefGoogle Scholar
  35. Gains JE, Bomanji JB, Fersht NL, Sullivan T, D'Souza D, Sullivan KP, Aldridge M, Waddington W, Gaze MN (2011) 177Lu-DOTATATE molecular radiotherapy for childhood neuroblastoma. J Nucl Med 52:1041–1047PubMedCrossRefGoogle Scholar
  36. Gauguet JM, Pace-Emerson T, Grant FD, Shusterman S, DuBois SG, Frazier AL, Voss SD (2017) Evaluation of the utility of 99m Tc-MDP bone scintigraphy versus MIBG scintigraphy and cross-sectional imaging for staging patients with neuroblastoma. Pediatr Blood Cancer 64Google Scholar
  37. Gaze MN, Chang YC, Flux GD, Mairs RJ, Saran FH, Meller ST (2005) Feasibility of dosimetry-based high-dose 131I-meta-iodobenzylguanidine with topotecan as a radiosensitizer in children with metastatic neuroblastoma. Cancer Biother Radiopharm 20:195–199PubMedCrossRefGoogle Scholar
  38. George RE, Li S, Medeiros-Nancarrow C, Neuberg D, Marcus K, Shamberger RC, Pulsipher M, Grupp SA, Diller L (2006) High-risk neuroblastoma treated with tandem autologous peripheral-blood stem cell-supported transplantation: long-term survival update. J Clin Oncol 24:2891–2896PubMedCrossRefGoogle Scholar
  39. George RE, Sanda T, Hanna M, Frohling S, Luther W 2nd, Zhang J, Ahn Y, Zhou W, London WB, McGrady P, Xue L, Zozulya S, Gregor VE, Webb TR, Gray NS, Gilliland DG, Diller L, Greulich H, Morris SW, Meyerson M, Look AT (2008) Activating mutations in ALK provide a therapeutic target in neuroblastoma. Nature 455:975–978PubMedPubMedCentralCrossRefGoogle Scholar
  40. Gustafson WC, Meyerowitz JG, Nekritz EA, Chen J, Benes C, Charron E, Simonds EF, Seeger R, Matthay KK, Hertz NT, Eilers M, Shokat KM, Weiss WA (2014) Drugging MYCN through an allosteric transition in aurora kinase a. Cancer Cell 26:414–427PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hachitanda Y, Tsuneyoshi M, Enjoji M (1989) Expression of pan-neuroendocrine proteins in 53 neuroblastic tumors. An immunohistochemical study with neuron-specific enolase, chromogranin, and synaptophysin. Arch Pathol Lab Med 113:381–384PubMedGoogle Scholar
  42. Hann HW, Evans AE, Siegel SE, Wong KY, Sather H, Dalton A, Hammond D, Seeger RC (1985) Prognostic importance of serum ferritin in patients with Stages III and IV neuroblastoma: the Childrens Cancer Study Group experience. Cancer Res 45:2843–2848PubMedGoogle Scholar
  43. Hann HW, Levy HM, Evans AE (1980) Serum ferritin as a guide to therapy in neuroblastoma. Cancer Res 40:1411–1413PubMedGoogle Scholar
  44. Heczey A, Louis CU, Savoldo B, Dakhova O, Durett A, Grilley B, Liu H, Wu MF, Mei Z, Gee A, Mehta B, Zhang H, Mahmood N, Tashiro H, Heslop HE, Dotti G, Rooney CM, Brenner MK (2017) CAR T cells administered in combination with lymphodepletion and PD-1 inhibition to patients with neuroblastoma. Mol Ther 25:2214–2224PubMedCrossRefPubMedCentralGoogle Scholar
  45. Henssen A, Althoff K, Odersky A, Beckers A, Koche R, Speleman F, Schafers S, Bell E, Nortmeyer M, Westermann F, De Preter K, Florin A, Heukamp L, Spruessel A, Astrahanseff K, Lindner S, Sadowski N, Schramm A, Astorgues-Xerri L, Riveiro ME, Eggert A, Cvitkovic E, Schulte JH (2016) Targeting MYCN-driven transcription by BET-bromodomain inhibition. Clin Cancer Res 22:2470–2481PubMedCrossRefGoogle Scholar
  46. Hero B, Schleiermacher G (2013) Update on pediatric opsoclonus myoclonus syndrome. Neuropediatrics 44:324–329PubMedCrossRefGoogle Scholar
  47. Hero B, Simon T, Spitz R, Ernestus K, Gnekow AK, Scheel-Walter HG, Schwabe D, Schilling FH, Benz-Bohm G, Berthold F (2008) Localized infant neuroblastomas often show spontaneous regression: results of the prospective trials NB95-S and NB97. J Clin Oncol 26:1504–1510PubMedCrossRefGoogle Scholar
  48. Hisashige A, Group NBSE (2014) Effectiveness of nationwide screening program for neuroblastoma in Japan. Glob J Health Sci 6:94–106PubMedPubMedCentralCrossRefGoogle Scholar
  49. Hiyama E, Iehara T, Sugimoto T, Fukuzawa M, Hayashi Y, Sasaki F, Sugiyama M, Kondo S, Yoneda A, Yamaoka H, Tajiri T, Akazawa K, Ohtaki M (2008) Effectiveness of screening for neuroblastoma at 6 months of age: a retrospective population-based cohort study. Lancet 371:1173–1180PubMedCrossRefGoogle Scholar
  50. Iehara T, Hamazaki M, Tajiri T, Kawano Y, Kaneko M, Ikeda H, Hosoi H, Sugimoto T, Sawada T, Japanese Infantile Neuroblastoma Cooperative Study G (2013) Successful treatment of infants with localized neuroblastoma based on their MYCN status. Int J Clin Oncol 18:389–395PubMedCrossRefGoogle Scholar
  51. Infarinato NR, Park JH, Krytska K, Ryles HT, Sano R, Szigety KM, Li Y, Zou HY, Lee NV, Smeal T, Lemmon MA, Mosse YP (2016) The ALK/ROS1 inhibitor PF-06463922 overcomes primary resistance to crizotinib in ALK-driven neuroblastoma. Cancer Discov 6:96–107PubMedCrossRefGoogle Scholar
  52. Irwin MS, Park JR (2015) Neuroblastoma: paradigm for precision medicine. Pediatr Clin N Am 62:225–256CrossRefGoogle Scholar
  53. Janoueix-Lerosey I, Lequin D, Brugieres L, Ribeiro A, de Pontual L, Combaret V, Raynal V, Puisieux A, Schleiermacher G, Pierron G, Valteau-Couanet D, Frebourg T, Michon J, Lyonnet S, Amiel J, Delattre O (2008) Somatic and germline activating mutations of the ALK kinase receptor in neuroblastoma. Nature 455:967–970PubMedCrossRefGoogle Scholar
  54. Kakodkar NC, Peddinti RR, Tian Y, Guerrero LJ, Chlenski A, Yang Q, Salwen HR, Maitland ML, Cohn SL (2012) Sorafenib inhibits neuroblastoma cell proliferation and signaling, blocks angiogenesis, and impairs tumor growth. Pediatr Blood Cancer 59:642–647PubMedCrossRefGoogle Scholar
  55. Kerbl R, Urban CE, Ambros IM, Dornbusch HJ, Schwinger W, Lackner H, Ladenstein R, Strenger V, Gadner H, Ambros PF (2003) Neuroblastoma mass screening in late infancy: insights into the biology of neuroblastic tumors. J Clin Oncol 21:4228–4234PubMedCrossRefGoogle Scholar
  56. Kohler JA, Rubie H, Castel V, Beiske K, Holmes K, Gambini C, Casale F, Munzer C, Erminio G, Parodi S, Navarro S, Marquez C, Peuchmaur M, Cullinane C, Brock P, Valteau-Couanet D, Garaventa A, Haupt R (2013) Treatment of children over the age of one year with unresectable localised neuroblastoma without MYCN amplification: results of the SIOPEN study. Eur J Cancer 49:3671–3679PubMedCrossRefGoogle Scholar
  57. Kreissman SG, Seeger RC, Matthay KK, London WB, Sposto R, Grupp SA, Haas-Kogan DA, Laquaglia MP, Yu AL, Diller L, Buxton A, Park JR, Cohn SL, Maris JM, Reynolds CP, Villablanca JG (2013) Purged versus non-purged peripheral blood stem-cell transplantation for high-risk neuroblastoma (COG A3973): a randomised phase 3 trial. Lancet Oncol 14:999–1008PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kushner BH, Cheung IY, Modak S, Kramer K, Ragupathi G, Cheung NK (2014) 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 20:1375–1382PubMedPubMedCentralCrossRefGoogle Scholar
  59. Kushner BH, Kramer K, Modak S, Cheung NK (2006) Irinotecan plus temozolomide for relapsed or refractory neuroblastoma. J Clin Oncol 24:5271–5276PubMedCrossRefGoogle Scholar
  60. Ladenstein R, Philip T, Lasset C, Hartmann O, Garaventa A, Pinkerton R, Michon J, Pritchard J, Klingebiel T, Kremens B, Pearson A, Coze C, Paolucci P, Frappaz D, Gadner H, Chauvin F (1998) Multivariate analysis of risk factors in stage 4 neuroblastoma patients over the age of one year treated with megatherapy and stem-cell transplantation: a report from the European Bone Marrow Transplantation Solid Tumor Registry. J Clin Oncol 16:953–965PubMedCrossRefGoogle Scholar
  61. Ladenstein R, Potschger U, Pearson ADJ, Brock P, Luksch R, Castel V, Yaniv I, Papadakis V, Laureys G, Malis J, Balwierz W, Ruud E, Kogner P, Schroeder H, de Lacerda AF, Beck-Popovic M, Bician P, Garami M, Trahair T, Canete A, Ambros PF, Holmes K, Gaze M, Schreier G, Garaventa A, Vassal G, Michon J, Valteau-Couanet D, Group SEN (2017) 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 18:500–514PubMedCrossRefGoogle Scholar
  62. Liu YL, Lu MY, Chang HH, Lu CC, Lin DT, Jou ST, Yang YL, Lee YL, Huang SF, Jeng YM, Lee H, Miser JS, Lin KH, Liao YF, Hsu WM, Tzen KY (2016) Diagnostic FDG and FDOPA positron emission tomography scans distinguish the genomic type and treatment outcome of neuroblastoma. Oncotarget 7:18774–18786PubMedPubMedCentralGoogle Scholar
  63. London WB, Castleberry RP, Matthay KK, Look AT, Seeger RC, Shimada H, Thorner P, Brodeur G, Maris JM, Reynolds CP, Cohn SL (2005) Evidence for an age cutoff greater than 365 days for neuroblastoma risk group stratification in the Children’s Oncology Group. J Clin Oncol 23:6459–6465PubMedCrossRefGoogle Scholar
  64. London WB, Frantz CN, Campbell LA, Seeger RC, Brumback BA, Cohn SL, Matthay KK, Castleberry RP, Diller L (2010) 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 28:3808–3815PubMedPubMedCentralCrossRefGoogle Scholar
  65. Louis CU, Savoldo B, Dotti G, Pule M, Yvon E, Myers GD, Rossig C, Russell HV, Diouf O, Liu E, Liu H, Wu MF, Gee AP, Mei Z, Rooney CM, Heslop HE, Brenner MK (2011) Antitumor activity and long-term fate of chimeric antigen receptor-positive T cells in patients with neuroblastoma. Blood 118:6050–6056PubMedPubMedCentralCrossRefGoogle Scholar
  66. Marachelian A, Shimada H, Sano H, Jackson H, Stein J, Sposto R, Matthay KK, Baker D, Villablanca JG (2012) The significance of serial histopathology in a residual mass for outcome of intermediate risk stage 3 neuroblastoma. Pediatr Blood Cancer 58:675–681PubMedCrossRefGoogle Scholar
  67. Maris JM (2010) Recent advances in neuroblastoma. N Engl J Med 362:2202–2211PubMedPubMedCentralCrossRefGoogle Scholar
  68. Matthay KK, Maris JM, Schleiermacher G, Nakagawara A, Mackall CL, Diller L, Weiss WA (2016) Neuroblastoma. Nat Rev Dis Primers 2:16078PubMedCrossRefGoogle Scholar
  69. Matthay KK, Perez C, Seeger RC, Brodeur GM, Shimada H, Atkinson JB, Black CT, Gerbing R, Haase GM, Stram DO, Swift P, Lukens JN (1998) Successful treatment of stage III neuroblastoma based on prospective biologic staging: a Children’s Cancer Group study. J Clin Oncol 16:1256–1264PubMedCrossRefGoogle Scholar
  70. Matthay KK, Shulkin B, Ladenstein R, Michon J, Giammarile F, Lewington V, Pearson AD, Cohn SL (2010) Criteria for evaluation of disease extent by (123)I-metaiodobenzylguanidine scans in neuroblastoma: a report for the International Neuroblastoma Risk Group (INRG) Task Force. Br J Cancer 102:1319–1326PubMedPubMedCentralCrossRefGoogle Scholar
  71. Matthay KK, Villablanca JG, Seeger RC, Stram DO, Harris RE, Ramsay NK, Swift P, Shimada H, Black CT, Brodeur GM, Gerbing RB, Reynolds CP (1999) 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 341:1165–1173PubMedCrossRefGoogle Scholar
  72. Matthay KK, Yanik G, Messina J, Quach A, Huberty J, Cheng SC, Veatch J, Goldsby R, Brophy P, Kersun LS, Hawkins RA, Maris JM (2007) 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 25:1054–1060PubMedCrossRefGoogle Scholar
  73. Maurer BJ, Kang MH, Villablanca JG, Janeba J, Groshen S, Matthay KK, Sondel PM, Maris JM, Jackson HA, Goodarzian F, Shimada H, Czarnecki S, Hasenauer B, Reynolds CP, Marachelian A (2013) 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 60:1801–1808PubMedPubMedCentralCrossRefGoogle Scholar
  74. Meany HJ, London WB, Ambros PF, Matthay KK, Monclair T, Simon T, Garaventa A, Berthold F, Nakagawara A, Cohn SL, Pearson AD, Park JR (2014) Significance of clinical and biologic features in Stage 3 neuroblastoma: a report from the International Neuroblastoma Risk Group project. Pediatr Blood Cancer 61:1932–1939PubMedCrossRefGoogle Scholar
  75. Miettinen M (1987) Synaptophysin and neurofilament proteins as markers for neuroendocrine tumors. Arch Pathol Lab Med 111:813–818PubMedGoogle Scholar
  76. Minturn JE, Evans AE, Villablanca JG, Yanik GA, Park JR, Shusterman S, Groshen S, Hellriegel ET, Bensen-Kennedy D, Matthay KK, Brodeur GM, Maris JM (2011) Phase I trial of lestaurtinib for children with refractory neuroblastoma: a new approaches to neuroblastoma therapy consortium study. Cancer Chemother Pharmacol 68:1057–1065PubMedPubMedCentralCrossRefGoogle Scholar
  77. Modak S, Kushner BH, Basu E, Roberts SS, Cheung NK (2017) Combination of bevacizumab, irinotecan, and temozolomide for refractory or relapsed neuroblastoma: results of a phase II study. Pediatr Blood Cancer 64:Google Scholar
  78. Mody R, Naranjo A, Van Ryn C, Yu AL, London WB, Shulkin BL, Parisi MT, Servaes SE, Diccianni MB, Sondel PM, Bender JG, Maris JM, Park JR, Bagatell R (2017) Irinotecan-temozolomide with temsirolimus or dinutuximab in children with refractory or relapsed neuroblastoma (COG ANBL1221): an open-label, randomised, phase 2 trial. Lancet Oncol 18:946–957PubMedPubMedCentralCrossRefGoogle Scholar
  79. Molenaar JJ, Koster J, Zwijnenburg DA, van Sluis P, Valentijn LJ, van der Ploeg I, Hamdi M, van Nes J, Westerman BA, van Arkel J, Ebus ME, Haneveld F, Lakeman A, Schild L, Molenaar P, Stroeken P, van Noesel MM, Ora I, Santo EE, Caron HN, Westerhout EM, Versteeg R (2012) Sequencing of neuroblastoma identifies chromothripsis and defects in neuritogenesis genes. Nature 483:589–593PubMedCrossRefGoogle Scholar
  80. Monclair T, Brodeur GM, Ambros PF, Brisse HJ, Cecchetto G, Holmes K, Kaneko M, London WB, Matthay KK, Nuchtern JG, von Schweinitz D, Simon T, Cohn SL, Pearson AD (2009) The International Neuroblastoma Risk Group (INRG) staging system: an INRG Task Force report. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 27:298–303CrossRefGoogle Scholar
  81. Morgenstern DA, London WB, Stephens D, Volchenboum SL, Simon T, Nakagawara A, Shimada H, Schleiermacher G, Matthay KK, Cohn SL, Pearson AD, Irwin MS (2016) Prognostic significance of pattern and burden of metastatic disease in patients with stage 4 neuroblastoma: a study from the International Neuroblastoma Risk Group database. Eur J Cancer 65:1–10PubMedCrossRefGoogle Scholar
  82. Mosse YP, Laudenslager M, Longo L, Cole KA, Wood A, Attiyeh EF, Laquaglia MJ, Sennett R, Lynch JE, Perri P, Laureys G, Speleman F, Kim C, Hou C, Hakonarson H, Torkamani A, Schork NJ, Brodeur GM, Tonini GP, Rappaport E, Devoto M, Maris JM (2008) Identification of ALK as a major familial neuroblastoma predisposition gene. Nature 455:930–935PubMedPubMedCentralCrossRefGoogle Scholar
  83. Mosse YP, Lim MS, Voss SD, Wilner K, Ruffner K, Laliberte J, Rolland D, Balis FM, Maris JM, Weigel BJ, Ingle AM, Ahern C, Adamson PC, Blaney SM (2013) 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 14:472–480PubMedPubMedCentralCrossRefGoogle Scholar
  84. Mosse YP, Lipsitz E, Fox E, Teachey DT, Maris JM, Weigel B, Adamson PC, Ingle MA, Ahern CH, Blaney SM (2012) Pediatric phase I trial and pharmacokinetic study of MLN8237, an investigational oral selective small-molecule inhibitor of Aurora kinase : a Children’s Oncology Group Phase I Consortium study. Clin Cancer Res 18:6058–6064PubMedPubMedCentralCrossRefGoogle Scholar
  85. Mullassery D, Farrelly P, Losty PD (2014) Does aggressive surgical resection improve survival in advanced stage 3 and 4 neuroblastoma? A systematic review and meta-analysis. Pediatr Hematol Oncol 31:703–716PubMedCrossRefGoogle Scholar
  86. Nakagawara A, Zaizen Y, Ikeda K, Suita S, Ohgami H, Nagahara N, Sera Y, Akiyama H, Kawakami K, Uchino J (1991) Different genomic and metabolic patterns between mass screening-positive and mass screening-negative later-presenting neuroblastomas. Cancer 68:2037–2044PubMedCrossRefGoogle Scholar
  87. Navid F, Sondel PM, Barfield R, Shulkin BL, Kaufman RA, Allay JA, Gan J, Hutson P, Seo S, Kim K, Goldberg J, Hank JA, Billups CA, Wu J, Furman WL, McGregor LM, Otto M, Gillies SD, Handgretinger R, Santana VM (2014) 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 32:1445–1452PubMedPubMedCentralCrossRefGoogle Scholar
  88. Nickerson HJ, Matthay KK, Seeger RC, Brodeur GM, Shimada H, Perez C, Atkinson JB, Selch M, Gerbing RB, Stram DO, Lukens J (2000) Favorable biology and outcome of stage IV-S neuroblastoma with supportive care or minimal therapy: a Children’s Cancer Group study. J Clin Oncol 18:477–486PubMedCrossRefGoogle Scholar
  89. Nuchtern JG, London WB, Barnewolt CE, Naranjo A, McGrady PW, Geiger JD, Diller L, Schmidt ML, Maris JM, Cohn SL, Shamberger RC (2012) A prospective study of expectant observation as primary therapy for neuroblastoma in young infants: a Children’s Oncology Group study. Ann Surg 256:573–580PubMedPubMedCentralCrossRefGoogle Scholar
  90. Park JR, Bagatell R, Cohn SL, Pearson AD, Villablanca JG, Berthold F, Burchill S, Boubaker A, McHugh K, Nuchtern JG, London WB, Seibel NL, Lindwasser OW, Maris JM, Brock P, Schleiermacher G, Ladenstein R, Matthay KK, Valteau-Couanet D (2017) Revisions to the international neuroblastoma response criteria: a consensus statement from the National Cancer Institute clinical trials planning meeting. J Clin Oncol 35:2580–2587PubMedCrossRefPubMedCentralGoogle Scholar
  91. Park JR, Bagatell R, London WB, Maris JM, Cohn SL, Mattay KK, Hogarty M, Committee COGN (2013) Children’s Oncology Group’s 2013 blueprint for research: neuroblastoma. Pediatr Blood Cancer 60:985–993PubMedCrossRefGoogle Scholar
  92. Park JR, Kreissman SG, London WB, Naranjo A, Cohn SL, Hogarty MD, Tenney SC, Haas-Kogan D, Shaw PJ, Geiger JD, Doski JJ, Gorges SW, Khanna G, Voss SD, Maris JM, Grupp SA, Diller L (2016) A phase III 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 34:LBA3–LBA3CrossRefGoogle Scholar
  93. Park JR, Scott JR, Stewart CF, London WB, Naranjo A, Santana VM, Shaw PJ, Cohn SL, Matthay KK (2011) Pilot induction regimen incorporating pharmacokinetically guided topotecan for treatment of newly diagnosed high-risk neuroblastoma: a Children’s Oncology Group study. J Clin Oncol 29:4351–4357PubMedPubMedCentralCrossRefGoogle Scholar
  94. Park JR, Villablanca JG, London WB, Gerbing RB, Haas-Kogan D, Adkins ES, Attiyeh EF, Maris JM, Seeger RC, Reynolds CP, Matthay KK, Children’s Oncology G (2009) Outcome of high-risk stage 3 neuroblastoma with myeloablative therapy and 13-cis-retinoic acid: a report from the Children’s Oncology Group. Pediatr Blood Cancer 52:44-50Google Scholar
  95. Patterson DM, Gao D, Trahan DN, Johnson BA, Ludwig A, Barbieri E, Chen Z, Diaz-Miron J, Vassilev L, Shohet JM, Kim ES (2011) Effect of MDM2 and vascular endothelial growth factor inhibition on tumor angiogenesis and metastasis in neuroblastoma. Angiogenesis 14:255–266PubMedCrossRefGoogle Scholar
  96. Peifer M, Hertwig F, Roels F, Dreidax D, Gartlgruber M, Menon R, Kramer A, Roncaioli JL, Sand F, Heuckmann JM, Ikram F, Schmidt R, Ackermann S, Engesser A, Kahlert Y, Vogel W, Altmuller J, Nurnberg P, Thierry-Mieg J, Thierry-Mieg D, Mariappan A, Heynck S, Mariotti E, Henrich KO, Gloeckner C, Bosco G, Leuschner I, Schweiger MR, Savelyeva L, Watkins SC, Shao C, Bell E, Hofer T, Achter V, Lang U, Theissen J, Volland R, Saadati M, Eggert A, de Wilde B, Berthold F, Peng Z, Zhao C, Shi L, Ortmann M, Buttner R, Perner S, Hero B, Schramm A, Schulte JH, Herrmann C, O'Sullivan RJ, Westermann F, Thomas RK, Fischer M (2015) Telomerase activation by genomic rearrangements in high-risk neuroblastoma. Nature 526:700–704PubMedPubMedCentralCrossRefGoogle Scholar
  97. Peuchmaur M, d'Amore ES, Joshi VV, Hata J, Roald B, Dehner LP, Gerbing RB, Stram DO, Lukens JN, Matthay KK, Shimada H (2003) Revision of the international Neuroblastoma Pathology Classification: confirmation of favorable and unfavorable prognostic subsets in ganglioneuroblastoma, nodular. Cancer 98:2274–2281PubMedCrossRefGoogle Scholar
  98. Pinto NR, Applebaum MA, Volchenboum SL, Matthay KK, London WB, Ambros PF, Nakagawara A, Berthold F, Schleiermacher G, Park JR, Valteau-Couanet D, Pearson AD, Cohn SL (2015) Advances in risk classification and treatment strategies for neuroblastoma. J Clin Oncol 33:3008–3017PubMedPubMedCentralCrossRefGoogle Scholar
  99. Pritchard J, Cotterill SJ, Germond SM, Imeson J, de Kraker J, Jones DR (2005) 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 44:348–357PubMedCrossRefGoogle Scholar
  100. Pugh TJ, Morozova O, Attiyeh EF, Asgharzadeh S, Wei JS, Auclair D, Carter SL, Cibulskis K, Hanna M, Kiezun A, Kim J, Lawrence MS, Lichenstein L, McKenna A, Pedamallu CS, Ramos AH, Shefler E, Sivachenko A, Sougnez C, Stewart C, Ally A, Birol I, Chiu R, Corbett RD, Hirst M, Jackman SD, Kamoh B, Khodabakshi AH, Krzywinski M, Lo A, Moore RA, Mungall KL, Qian J, Tam A, Thiessen N, Zhao Y, Cole KA, Diamond M, Diskin SJ, Mosse YP, Wood AC, Ji L, Sposto R, Badgett T, London WB, Moyer Y, Gastier-Foster JM, Smith MA, Guidry Auvil JM, Gerhard DS, Hogarty MD, Jones SJ, Lander ES, Gabriel SB, Getz G, Seeger RC, Khan J, Marra MA, Meyerson M, Maris JM (2013) The genetic landscape of high-risk neuroblastoma. Nat Genet 45:279–284PubMedPubMedCentralCrossRefGoogle Scholar
  101. Puissant A, Frumm SM, Alexe G, Bassil CF, Qi J, Chanthery YH, Nekritz EA, Zeid R, Gustafson WC, Greninger P, Garnett MJ, McDermott U, Benes CH, Kung AL, Weiss WA, Bradner JE, Stegmaier K (2013) Targeting MYCN in neuroblastoma by BET bromodomain inhibition. Cancer Discov 3:308–323PubMedPubMedCentralCrossRefGoogle Scholar
  102. Rounbehler RJ, Li W, Hall MA, Yang C, Fallahi M, Cleveland JL (2009) Targeting ornithine decarboxylase impairs development of MYCN-amplified neuroblastoma. Cancer Res 69:547–553PubMedPubMedCentralCrossRefGoogle Scholar
  103. Rubie H, De Bernardi B, Gerrard M, Canete A, Ladenstein R, Couturier J, Ambros P, Munzer C, Pearson AD, Garaventa A, Brock P, Castel V, Valteau-Couanet D, Holmes K, Di Cataldo A, Brichard B, Mosseri V, Marquez C, Plantaz D, Boni L, Michon J (2011) Excellent outcome with reduced treatment in infants with nonmetastatic and unresectable neuroblastoma without MYCN amplification: results of the prospective INES 99.1. J Clin Oncol 29:449–455PubMedCrossRefGoogle Scholar
  104. Rudnick E, Khakoo Y, Antunes NL, Seeger RC, Brodeur GM, Shimada H, Gerbing RB, Stram DO, Matthay KK (2001) Opsoclonus-myoclonus-ataxia syndrome in neuroblastoma: clinical outcome and antineuronal antibodies-a report from the Children’s Cancer Group Study. Med Pediatr Oncol 36:612–622PubMedCrossRefGoogle Scholar
  105. Russell MR, Levin K, Rader J, Belcastro L, Li Y, Martinez D, Pawel B, Shumway SD, Maris JM, Cole KA (2013) Combination therapy targeting the Chk1 and Wee1 kinases shows therapeutic efficacy in neuroblastoma. Cancer Res 73:776–784PubMedCrossRefGoogle Scholar
  106. Saarinen-Pihkala UM, Hovi L, Koivusalo A, Jahnukainen K, Karikoski R, Sariola H, Wikstrom S (2012) Thiotepa and melphalan based single, tandem, and triple high dose therapy and autologous stem cell transplantation for high risk neuroblastoma. Pediatr Blood Cancer 59:1190–1197PubMedCrossRefGoogle Scholar
  107. Saulnier Sholler GL, Gerner EW, Bergendahl G, MacArthur RB, VanderWerff A, Ashikaga T, Bond JP, Ferguson W, Roberts W, Wada RK, Eslin D, Kraveka JM, Kaplan J, Mitchell D, Parikh NS, Neville K, Sender L, Higgins T, Kawakita M, Hiramatsu K, Moriya SS, Bachmann AS (2015) A phase I trial of DFMO targeting polyamine addiction in patients with relapsed/refractory neuroblastoma. PLoS One 10:e0127246PubMedPubMedCentralCrossRefGoogle Scholar
  108. Sawada T, Todo S, Fujita K, Iino S, Imashuku S, Kusunoki T (1982) Mass screening of neuroblastoma in infancy. Am J Dis Child 136:710–712PubMedGoogle Scholar
  109. Schilling FH, Spix C, Berthold F, Erttmann R, Fehse N, Hero B, Klein G, Sander J, Schwarz K, Treuner J, Zorn U, Michaelis J (2002) Neuroblastoma screening at one year of age. N Engl J Med 346:1047–1053PubMedCrossRefGoogle Scholar
  110. Schilling FH, Spix C, Berthold F, Erttmann R, Sander J, Treuner J, Michaelis J (2003) Children may not benefit from neuroblastoma screening at 1 year of age. Updated results of the population based controlled trial in Germany. Cancer Lett 197:19–28PubMedCrossRefGoogle Scholar
  111. Schleiermacher G, Mosseri V, London WB, Maris JM, Brodeur GM, Attiyeh E, Haber M, Khan J, Nakagawara A, Speleman F, Noguera R, Tonini GP, Fischer M, Ambros I, Monclair T, Matthay KK, Ambros P, Cohn SL, Pearson AD (2012) Segmental chromosomal alterations have prognostic impact in neuroblastoma: a report from the INRG project. Br J Cancer 107:1418–1422PubMedPubMedCentralCrossRefGoogle Scholar
  112. Seeger RC, Brodeur GM, Sather H, Dalton A, Siegel SE, Wong KY, Hammond D (1985) Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas. N Engl J Med 313:1111–1116PubMedCrossRefGoogle Scholar
  113. Seif AE, Naranjo A, Baker DL, Bunin NJ, Kletzel M, Kretschmar CS, Maris JM, McGrady PW, von Allmen D, Cohn SL, London WB, Park JR, Diller LR, Grupp SA (2013) 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 48:947–952PubMedPubMedCentralCrossRefGoogle Scholar
  114. Sharp SE, Shulkin BL, Gelfand MJ, Salisbury S, Furman WL (2009) 123I-MIBG scintigraphy and 18F-FDG PET in neuroblastoma. J Nucl Med 50:1237–1243PubMedCrossRefGoogle Scholar
  115. Shimada H, Ambros IM, Dehner LP, Hata J, Joshi VV, Roald B, Stram DO, Gerbing RB, Lukens JN, Matthay KK, Castleberry RP (1999) The International Neuroblastoma Pathology Classification (the Shimada system). Cancer 86:364–372PubMedCrossRefGoogle Scholar
  116. Shimada H, Umehara S, Monobe Y, Hachitanda Y, Nakagawa A, Goto S, Gerbing RB, Stram DO, Lukens JN, Matthay KK (2001) International neuroblastoma pathology classification for prognostic evaluation of patients with peripheral neuroblastic tumors: a report from the Children’s Cancer Group. Cancer 92:2451–2461PubMedCrossRefGoogle Scholar
  117. Shinagawa T, Kitamura T, Katanoda K, Matsuda T, Ito Y, Sobue T (2017) The incidence and mortality rates of neuroblastoma cases before and after the cessation of the mass screening program in Japan: a descriptive study. Int J Cancer 140:618–625PubMedCrossRefGoogle Scholar
  118. Shuster JJ, McWilliams NB, Castleberry R, Nitschke R, Smith EI, Altshuler G, Kun L, Brodeur G, Joshi V, Vietti T et al (1992) Serum lactate dehydrogenase in childhood neuroblastoma. A Pediatric Oncology Group recursive partitioning study. Am J Clin Oncol 15:295–303PubMedCrossRefGoogle Scholar
  119. Shusterman S, London WB, Gillies SD, Hank JA, Voss SD, Seeger RC, Reynolds CP, Kimball J, Albertini MR, Wagner B, Gan J, Eickhoff J, DeSantes KB, Cohn SL, Hecht T, Gadbaw B, Reisfeld RA, Maris JM, Sondel PM (2010) Antitumor activity of hu14.18-IL2 in patients with relapsed/refractory neuroblastoma: a Children’s Oncology Group (COG) phase II study. J Clin Oncol 28:4969–4975PubMedPubMedCentralCrossRefGoogle Scholar
  120. Siebert N, Eger C, Seidel D, Juttner M, Zumpe M, Wegner D, Kietz S, Ehlert K, Veal GJ, Siegmund W, Weiss M, Loibner H, Ladenstein R, Lode HN (2016) Pharmacokinetics and pharmacodynamics of ch14.18/CHO in relapsed/refractory high-risk neuroblastoma patients treated by long-term infusion in combination with IL-2. MAbs 8:604–616PubMedPubMedCentralCrossRefGoogle Scholar
  121. Simon T, Haberle B, Hero B, von Schweinitz D, Berthold F (2013) Role of surgery in the treatment of patients with stage 4 neuroblastoma age 18 months or older at diagnosis. J Clin Oncol 31:752–758PubMedCrossRefGoogle Scholar
  122. Stiller CA, Parkin DM (1992) International variations in the incidence of neuroblastoma. Int J Cancer 52:538–543PubMedCrossRefGoogle Scholar
  123. Strother DR, London WB, Schmidt ML, Brodeur GM, Shimada H, Thorner P, Collins MH, Tagge E, Adkins S, Reynolds CP, Murray K, Lavey RS, Matthay KK, Castleberry R, Maris JM, Cohn SL (2012) Outcome after surgery alone or with restricted use of chemotherapy for patients with low-risk neuroblastoma: results of Children’s Oncology Group study P9641. J Clin Oncol 30:1842–1848PubMedPubMedCentralCrossRefGoogle Scholar
  124. Taggart DR, London WB, Schmidt ML, DuBois SG, Monclair TF, Nakagawara A, De Bernardi B, Ambros PF, Pearson AD, Cohn SL, Matthay KK (2011) Prognostic value of the stage 4S metastatic pattern and tumor biology in patients with metastatic neuroblastoma diagnosed between birth and 18 months of age. J Clin Oncol 29:4358–4364PubMedPubMedCentralCrossRefGoogle Scholar
  125. Talleur AC, Triplett BM, Federico S, Mamcarz E, Janssen W, Wu J, Shook D, Leung W, Furman WL (2017) Consolidation therapy for newly diagnosed pediatric patients with high-risk neuroblastoma using busulfan/melphalan, autologous hematopoietic cell transplantation, anti-GD2 antibody, granulocyte-macrophage colony-stimulating factor, interleukin-2, and haploidentical natural killer cells. Biol Blood Marrow Transplant 23:1910–1917PubMedCrossRefGoogle Scholar
  126. Trochet D, Bourdeaut F, Janoueix-Lerosey I, Deville A, de Pontual L, Schleiermacher G, Coze C, Philip N, Frebourg T, Munnich A, Lyonnet S, Delattre O, Amiel J (2004) Germline mutations of the paired-like homeobox 2B (PHOX2B) gene in neuroblastoma. Am J Hum Genet 74:761–764PubMedPubMedCentralCrossRefGoogle Scholar
  127. Vaishnavi A, Le AT, Doebele RC (2015) TRKing down an old oncogene in a new era of targeted therapy. Cancer Discov 5:25–34PubMedCrossRefGoogle Scholar
  128. Vo KT, Matthay KK, Neuhaus J, London WB, Hero B, Ambros PF, Nakagawara A, Miniati D, Wheeler K, Pearson AD, Cohn SL, DuBois SG (2014) Clinical, biologic, and prognostic differences on the basis of primary tumor site in neuroblastoma: a report from the international neuroblastoma risk group project. J Clin Oncol 32:3169–3176PubMedPubMedCentralCrossRefGoogle Scholar
  129. von Allmen D, Davidoff AM, London WB, Van Ryn C, Haas-Kogan DA, Kreissman SG, Khanna G, Rosen N, Park JR, La Quaglia MP (2017) Impact of extent of resection on local control and survival in patients from the COG A3973 study with high-risk neuroblastoma. J Clin Oncol 35:208–216CrossRefGoogle Scholar
  130. Wagner LM, Adams VR (2017) Targeting the PD-1 pathway in pediatric solid tumors and brain tumors. Onco Targets Ther 10:2097–2106PubMedPubMedCentralCrossRefGoogle Scholar
  131. Wilson JS, Gains JE, Moroz V, Wheatley K, Gaze MN (2014) A systematic review of 131I-meta iodobenzylguanidine molecular radiotherapy for neuroblastoma. Eur J Cancer 50:801–815PubMedCrossRefGoogle Scholar
  132. Woods WG, Gao RN, Shuster JJ, Robison LL, Bernstein M, Weitzman S, Bunin G, Levy I, Brossard J, Dougherty G, Tuchman M, Lemieux B (2002) Screening of infants and mortality due to neuroblastoma. N Engl J Med 346:1041–1046PubMedCrossRefGoogle Scholar
  133. Yamamoto K, Hayashi Y, Hanada R, Kikuchi A, Ichikawa M, Tanimura M, Yoshioka S (1995) Mass screening and age-specific incidence of neuroblastoma in Saitama Prefecture, Japan. J Clin Oncol 13:2033–2038PubMedCrossRefGoogle Scholar
  134. Yanik G, Naranjo A, Parisi MT, Shulkin BL, Nadel H, Gelfand MJ, Ladenstein R, Boubaker A, Poetschger U, Valteau-Couanet D, Kreissman SG, Park JR, Matthay KK (2015) Impact of post-induction curie scores in high-risk neuroblastoma. Biology of Blood and Marrow Transplantation 21:S107–S107CrossRefGoogle Scholar
  135. Yanik GA, Parisi MT, Naranjo A, Nadel H, Gelfand MJ, Park JR, Ladenstein RL, Poetschger U, Boubaker A, Valteau-Couanet D, Lambert B, Castellani MR, Bar-Sever Z, Oudoux A, Kaminska A, Kreissman SG, Shulkin BL, Matthay KK (2017) Validation of post-induction Curie scores in high risk neuroblastoma. A Children’s Oncology Group (COG) and SIOPEN group report on SIOPEN/HR-NBL1. J Nucl MedGoogle Scholar
  136. Yanik GA, Parisi MT, Shulkin BL, Naranjo A, Kreissman SG, London WB, Villablanca JG, Maris JM, Park JR, Cohn SL, McGrady P, Matthay KK (2013) Semiquantitative mIBG scoring as a prognostic indicator in patients with stage 4 neuroblastoma: a report from the Children’s oncology group. J Nucl Med 54:541–548PubMedPubMedCentralCrossRefGoogle Scholar
  137. Yu AL, Gilman AL, Ozkaynak MF, London WB, Kreissman SG, Chen HX, Smith M, Anderson B, Villablanca JG, Matthay KK, Shimada H, Grupp SA, Seeger R, Reynolds CP, Buxton A, Reisfeld RA, Gillies SD, Cohn SL, Maris JM, Sondel PM, Children's Oncology G (2010) Anti-GD2 antibody with GM-CSF, interleukin-2, and isotretinoin for neuroblastoma. N Engl J Med 363:1324–1334PubMedPubMedCentralCrossRefGoogle Scholar
  138. Zhou MJ, Doral MY, DuBois SG, Villablanca JG, Yanik GA, Matthay KK (2015) Different outcomes for relapsed versus refractory neuroblastoma after therapy with (131)I-metaiodobenzylguanidine ((131)I-MIBG). Eur J Cancer 51:2465–2472PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Pediatrics, UCSF Helen Diller Family Comprehensive Cancer Center, and UCSF Benioff Children’s HospitalUniversity of CaliforniaSan FranciscoUSA

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