Acute lymphoblastic leukemia in children

New England Journal of Medicine

Volumn 373, Issue 16, 2015, Pages 1541-1552

  Hunger, Stephen P ^a   Mullighan, Charles G ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE LYMPHOBLASTIC LEUKEMIA; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER RISK; CANCER SURVIVAL; CARCINOGENESIS; CHILD; CLINICAL FEATURE; DISEASE ASSOCIATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNE RESPONSE; IMMUNOPHENOTYPING; LONG TERM CARE; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; REVIEW; RISK ASSESSMENT; RISK FACTOR; SHORT COURSE THERAPY; SURVIVAL RATE; SURVIVAL TIME; TREATMENT RESPONSE; ADVERSE EFFECTS; FEMALE; GENE REARRANGEMENT; GENE TRANSLOCATION; GENETICS; IMMUNOTHERAPY; INCIDENCE; INFANT; MALE; MORTALITY; MULTIMODALITY CANCER THERAPY; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PRESCHOOL CHILD; PROGNOSIS; RECURRENT DISEASE;

ANTINEOPLASTIC AGENT;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; CHILD; CHILD, PRESCHOOL; COMBINED MODALITY THERAPY; FEMALE; GENE REARRANGEMENT; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOTHERAPY; INCIDENCE; INFANT; MALE; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; RECURRENCE; RISK FACTORS; SURVIVAL RATE; TRANSLOCATION, GENETIC;

EID: 84944474650     PISSN: 00284793     EISSN: 15334406     Source Type: Journal    
DOI: 10.1056/NEJMra1400972     Document Type: Review

References (92)

1. Smith MA, Seibel NL, Altekruse SF, et al. Outcomes for children and adolescents with cancer: challenges for the twenty-first century. J Clin Oncol 2010; 28: 2625-34.
2. Linabery AM, Ross JA. Trends in childhood cancer incidence in the U.S. (1992- 2004). Cancer 2008; 112: 416-32.
3. Farber S, Diamond LK. Temporary remissions in acute leukemia in children produced by folic acid antagonist, 4-aminopteroyl- glutamic acid. N Engl J Med 1948; 238: 787-93.
4. Ries LAG, Smith MA, Gurney JG, et al. Cancer incidence and survival among children and adolescents: United States SEER Program 1975-1995. Bethesda, MD: National Cancer Institute, SEER Program, 1999.
5. Lim JY, Bhatia S, Robison LL, Yang JJ. Genomics of racial and ethnic disparities in childhood acute lymphoblastic leukemia. Cancer 2014; 120: 955-62.
6. Buitenkamp TD, Izraeli S, Zimmermann M, et al. Acute lymphoblastic leukemia in children with Down syndrome: a retrospective analysis from the Ponte di Legno study group. Blood 2014; 123: 70-7.
7. Perez-Andreu V, Roberts KG, Harvey RC, et al. Inherited GATA3 variants are associated with Ph-like childhood acute lymphoblastic leukemia and risk of relapse. Nat Genet 2013; 45: 1494-8.
8. Treviño LR, Yang W, French D, et al. Germline genomic variants associated with childhood acute lymphoblastic leukemia. Nat Genet 2009; 41: 1001-5.
9. Papaemmanuil E, Hosking FJ, Vijayakrishnan J, et al. Loci on 7p12.2, 10q21.2 and 14q11.2 are associated with risk of childhood acute lymphoblastic leukemia. Nat Genet 2009; 41: 1006-10.
10. Shah S, Schrader KA, Waanders E, et al. A recurrent germline PAX5 mutation confers susceptibility to pre-B cell acute lymphoblastic leukemia. Nat Genet 2013; 45: 1226-31.
11. Zhang MY, Churpek JE, Keel SB, et al. Germline ETV6 mutations in familial thrombocytopenia and hematologic malignancy. Nat Genet 2015; 47: 180-5.
12. Hunger SP, Mullighan CG. Redefining ALL classification: toward detecting highrisk ALL and implementing precision medicine. Blood 2015 May 21 (Epub ahead of print).
13. Harrison CJ. Cytogenetics of paediatric and adolescent acute lymphoblastic leukaemia. Br J Haematol 2009; 144: 147-56.
14. Ma X, Edmonson M, Yergeau D, et al. Rise and fall of subclones from diagnosis to relapse in pediatric B-acute lymphoblastic leukaemia. Nat Commun 2015; 6: 6604.
15. Zhang J, Mullighan CG, Harvey RC, et al. Key pathways are frequently mutated in high-risk childhood acute lymphoblastic leukemia: a report from the Children's Oncology Group. Blood 2011; 118: 3080-7.
16. Nachman JB, Heerema NA, Sather H, et al. Outcome of treatment in children with hypodiploid acute lymphoblastic leukemia. Blood 2007; 110: 1112-5.
17. Holmfeldt L, Wei L, Diaz-Flores E, et al. The genomic landscape of hypodiploid acute lymphoblastic leukemia. Nat Genet 2013; 45: 242-52.
18. Wiemels JL, Cazzaniga G, Daniotti M, et al. Prenatal origin of acute lymphoblastic leukaemia in children. Lancet 1999; 354: 1499-503.
19. Mullighan CG, Phillips LA, Su X, et al. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 2008; 322: 1377-80.
20. Russell LJ, Capasso M, Vater I, et al. Deregulated expression of cytokine receptor gene, CRLF2, is involved in lymphoid transformation in B-cell precursor acute lymphoblastic leukemia. Blood 2009; 114: 2688-98.
21. Russell LJ, De Castro DG, Griffiths M, et al. A novel translocation, t(14;19) (q32;p13), involving IGH@ and the cytokine receptor for erythropoietin. Leukemia 2009; 23: 614-7.
22. Aifantis I, Raetz E, Buonamici S. Molecular pathogenesis of T-cell leukaemia and lymphoma. Nat Rev Immunol 2008; 8: 380-90.
23. Meyer C, Hofmann J, Burmeister T, et al. The MLL recombinome of acute leukemias in 2013. Leukemia 2013; 27: 2165-76.
24. Andersson AK, Ma J, Wang J, et al. The landscape of somatic mutations in infant MLL-rearranged acute lymphoblastic leukemias. Nat Genet 2015; 47: 330-7.
25. Mullighan CG, Goorha S, Radtke I, et al. Genome-wide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 2007; 446: 758-64.
26. Clappier E, Auclerc MF, Rapion J, et al. An intragenic ERG deletion is a marker of an oncogenic subtype of B-cell precursor acute lymphoblastic leukemia with a favorable outcome despite frequent IKZF1 deletions. Leukemia 2014; 28: 70-7.
27. Heerema NA, Carroll AJ, Devidas M, et al. Intrachromosomal amplification of chromosome 21 is associated with inferior outcomes in children with acute lymphoblastic leukemia treated in contemporary standard-risk children's oncology group studies: a report from the Children's Oncology Group. J Clin Oncol 2013; 31: 3397-402.
28. Zhang J, Ding L, Holmfeldt L, et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 2012; 481: 157-63.
29. Coustan-Smith E, Mullighan CG, Onciu M, et al. Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. Lancet Oncol 2009; 10: 147-56.
30. Roberts KG, Li Y, Payne-Turner D, et al. Targetable kinase-activating lesions in Phlike acute lymphoblastic leukemia. N Engl J Med 2014; 371: 1005-15.
31. Kuiper RP, Schoenmakers EF, van Reijmersdal SV, et al. High-resolution genomic profiling of childhood ALL reveals novel recurrent genetic lesions affecting pathways involved in lymphocyte differentiation and cell cycle progression. Leukemia 2007; 21: 1258-66.
32. Smith M, Arthur D, Camitta B, et al. Uniform approach to risk classification and treatment assignment for children with acute lymphoblastic leukemia. J Clin Oncol 1996; 14: 18-24.
33. Pui CH, Sandlund JT, Pei D, et al. Results of therapy for acute lymphoblastic leukemia in black and white children. JAMA 2003; 290: 2001-7.
34. Harvey RC, Mullighan CG, Chen IM, et al. Rearrangement of CRLF2 is associated with mutation of JAK kinases, alteration of IKZF1, Hispanic/Latino ethnicity, and a poor outcome in pediatric B-progenitor acute lymphoblastic leukemia. Blood 2010; 115: 5312-21.
35. Liu GJ, Cimmino L, Jude JG, et al. Pax5 loss imposes a reversible differentiation block in B-progenitor acute lymphoblastic leukemia. Genes Dev 2014; 28: 1337-50.
36. Schwickert TA, Tagoh H, Gültekin S, et al. Stage-specific control of early B cell development by the transcription factor Ikaros. Nat Immunol 2014; 15: 283-93.
37. Hunger SP, Lu X, Devidas M, et al. Improved survival for children and adolescents from 1990-2005: a report from the Children's Oncology Group. J Clin Oncol 2012; 30: 1663-9.
38. Van Vlierberghe P, Palomero T, Khiabanian H, et al. PHF6 mutations in T-cell acute lymphoblastic leukemia. Nat Genet 2010; 42: 338-42.
39. Van der Meulen J, Sanghvi V, Mavrakis K, et al. The H3K27me3 demethylase UTX is a gender-specific tumor suppressor in Tcell acute lymphoblastic leukemia. Blood 2015; 125: 13-21.
40. Moorman AV, Ensor HM, Richards SM, et al. Prognostic effect of chromosomal abnormalities in childhood B-cell precursor acute lymphoblastic leukaemia: results from the UK Medical Research Council ALL97/99 randomised trial. Lancet Oncol 2010; 11: 429-38.
41. Aricò M, Schrappe M, Hunger SP, et al. Clinical outcome of children with newly diagnosed Philadelphia chromosomepositive acute lymphoblastic leukemia treated between 1995 and 2005. J Clin Oncol 2010; 28: 4755-61.
42. Harrison CJ, Moorman AV, Schwab C, et al. An international study of intrachromosomal amplification of chromosome 21 (iAMP21): cytogenetic characterization and outcome. Leukemia 2014; 28: 1015-21.
43. Mullighan CG, Su X, Zhang J, et al. Deletion of IKZF1 and prognosis in acute lymphoblastic leukemia. N Engl J Med 2009; 360: 470-80.
44. Kuiper RP, Waanders E, van der Velden VH, et al. IKZF1 deletions predict relapse in uniformly treated pediatric precursor B-ALL. Leukemia 2010; 24: 1258-64.
45. Coustan-Smith E, Sancho J, Hancock ML, et al. Clinical importance of minimal residual disease in childhood acute lymphoblastic leukemia. Blood 2000; 96: 2691-6.
46. Borowitz MJ, Devidas M, Hunger SP, et al. Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia and its relationship to other prognostic factors: a Children's Oncology Group study. Blood 2008; 111: 5477-85.
47. Campana D. Minimal residual disease monitoring in childhood acute lymphoblastic leukemia. Curr Opin Hematol 2012; 19: 313-8.
48. Pui CH, Pei D, Coustan-Smith E, et al. Clinical utility of sequential minimal residual disease measurements in the context of risk-based therapy in childhood acute lymphoblastic leukaemia: a prospective study. Lancet Oncol 2015; 16: 465-74.
49. Conter V, Bartram CR, Valsecchi MG, et al. Molecular response to treatment redefines all prognostic factors in children and adolescents with B-cell precursor acute lymphoblastic leukemia: results in 3184 patients of the AIEOP-BFM ALL 2000 study. Blood 2010; 115: 3206-14.
50. Schrappe M, Valsecchi MG, Bartram CR, et al. Late MRD response determines relapse risk overall and in subsets of childhood T-cell ALL: results of the AIEOP-BFMALL 2000 study. Blood 2011; 118: 2077-84.
51. Vora A, Goulden N, Mitchell C, et al. Augmented post-remission therapy for a minimal residual disease-defined high-risk subgroup of children and young people with clinical standard-risk and intermediate- risk acute lymphoblastic leukaemia (UKALL 2003): a randomised controlled trial. Lancet Oncol 2014; 15: 809-18.
52. Faham M, Zheng J, Moorhead M, et al. Deep-sequencing approach for minimal residual disease detection in acute lymphoblastic leukemia. Blood 2012; 120: 5173-80.
53. George P, Hernandez K, Hustu O, Borella L, Holton C, Pinkel D. A study of "total therapy" of acute lymphocytic leukemia in children. J Pediatr 1968; 72: 399-408.
54. Aur RJ, Simone J, Hustu HO, et al. Central nervous system therapy and combination chemotherapy of childhood lymphocytic leukemia. Blood 1971; 37: 272-81.
55. Riehm H, Gadner H, Henze G, Langermann H-J, Odenwald E. The Berlin childhood acute lymphoblastic leukemia therapy study, 1970-1976. Am J Pediatr Hematol Oncol 1980; 2: 299-306.
56. Pui CH, Campana D, Pei D, et al. Treating childhood acute lymphoblastic leukemia without cranial irradiation. N Engl J Med 2009; 360: 2730-41.
57. Vrooman LM, Stevenson KE, Supko JG, et al. Postinduction dexamethasone and individualized dosing of Escherichia Coli L-asparaginase each improve outcome of children and adolescents with newly diagnosed acute lymphoblastic leukemia: results from a randomized study - Dana-Farber Cancer Institute ALL Consortium Protocol 00-01. J Clin Oncol 2013; 31: 1202-10.
58. Vora A, Goulden N, Wade R, et al. Treatment reduction for children and young adults with low-risk acute lymphoblastic leukaemia defined by minimal residual disease (UKALL 2003): a randomised controlled trial. Lancet Oncol 2013; 14: 199-209.
59. Veerman AJ, Kamps WA, van den Berg H, et al. Dexamethasone-based therapy for childhood acute lymphoblastic leukaemia: results of the prospective Dutch Childhood Oncology Group (DCOG) protocol ALL-9 (1997-2004). Lancet Oncol 2009; 10: 957-66.
60. Domenech C, Suciu S, De Moerloose B, et al. Dexamethasone (6 mg/m2/day) and prednisolone (60 mg/m2/day) were equally effective as induction therapy for childhood acute lymphoblastic leukemia in the EORTC CLG 58951 randomized trial. Haematologica 2014; 99: 1220-7.
61. Schmiegelow K, Forestier E, Hellebostad M, et al. Long-term results of NOPHO ALL-92 and ALL-2000 studies of childhood acute lymphoblastic leukemia. Leukemia 2010; 24: 345-54.
62. Bhatia S, Landier W, Hageman L, et al. 6MP adherence in a multiracial cohort of children with acute lymphoblastic leukemia: a Children's Oncology Group study. Blood 2014; 124: 2345-53.
63. Moriyama T, Relling MV, Yang JJ. Inherited genetic variation in childhood acute lymphoblastic leukemia. Blood 2015 May 21 (Epub ahead of print).
64. Krull KR, Brinkman TM, Li C, et al. Neurocognitive outcomes decades after treatment for childhood acute lymphoblastic leukemia: a report from the St Jude lifetime cohort study. J Clin Oncol 2013; 31: 4407-15.
65. Nguyen K, Devidas M, Cheng SC, et al. Factors influencing survival after relapse from acute lymphoblastic leukemia: a Children's Oncology Group study. Leukemia 2008; 22: 2142-50.
66. Raetz EA, Bhatla T. Where do we stand in the treatment of relapsed acute lymphoblastic leukemia? Hematology Am Soc Hematol Educ Program 2012; 2012: 129-36.
67. Mullighan CG, Zhang J, Kasper LH, et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature 2011; 471: 235-9.
68. Meyer JA, Wang J, Hogan LE, et al. Relapse-specific mutations in NT5C2 in childhood acute lymphoblastic leukemia. Nat Genet 2013; 45: 290-4.
69. Peters C, Schrappe M, von Stackelberg A, et al. Stem-cell transplantation in children with acute lymphoblastic leukemia: a prospective international multicenter trial comparing sibling donors with matched unrelated donors - the ALL-SCTBFM- 2003 trial. J Clin Oncol 2015; 33: 1265-74.
70. Tzoneva G, Perez-Garcia A, Carpenter Z, et al. Activating mutations in the NT5C2 nucleotidase gene drive chemotherapy resistance in relapsed ALL. Nat Med 2013; 19: 368-71.
71. Li B, Li H, Bai Y, et al. Negative feedback- defective PRPS1 mutants drive thiopurine resistance in relapsed childhood ALL. Nat Med 2015; 21: 563-71.
72. Collins FS, Varmus H. A new initiative on precision medicine. N Engl J Med 2015; 372: 793-5.
73. Kantarjian H, Sawyers C, Hochhaus A, et al. Hematologic and cytogenetic responses to imatinib mesylate in chronic myelogenous leukemia. N Engl J Med 2002; 346: 645-52.
74. Ross DM, Branford S, Seymour JF, et al. Safety and efficacy of imatinib cessation for CML patients with stable undetectable minimal residual disease: results from the TWISTER study. Blood 2013; 122: 515-22.
75. Mullighan CG, Miller CB, Radtke I, et al. BCR-ABL1 lymphoblastic leukaemia is characterized by the deletion of Ikaros. Nature 2008; 453: 110-4.
76. Schultz KR, Carroll A, Heerema NA, et al. Long-term follow-up of imatinib in pediatric Philadelphia chromosome-positive acute lymphoblastic leukemia: Children's Oncology Group study AALL0031. Leukemia 2014; 28: 1467-71.
77. Schultz KR, Bowman WP, Aledo A, et al. Improved early event-free survival with imatinib in Philadelphia chromosomepositive acute lymphoblastic leukemia: a Children's Oncology Group study. J Clin Oncol 2009; 27: 5175-81.
78. Biondi A, Schrappe M, De Lorenzo P, et al. Imatinib after induction for treatment of children and adolescents with Philadelphia- chromosome-positive acute lymphoblastic leukaemia (EsPhALL): a randomised, open-label, intergroup study. Lancet Oncol 2012; 13: 936-45.
79. Den Boer ML, van Slegtenhorst M, De Menezes RX, et al. A subtype of childhood acute lymphoblastic leukaemia with poor treatment outcome: a genome-wide classification study. Lancet Oncol 2009; 10: 125-34.
80. Weston BW, Hayden MA, Roberts KG, et al. Tyrosine kinase inhibitor therapy induces remission in a patient with refractory EBF1-PDGFRB-positive acute lymphoblastic leukemia. J Clin Oncol 2013; 31(25): e413-e416.
81. Maude SL, Frey N, Shaw PA, et al. Chimeric antigen receptor T cells for sustained remissions in leukemia. N Engl J Med 2014; 371: 1507-17.
82. Topp MS, Gökbuget N, Stein AS, et al. Safety and activity of blinatumomab for adult patients with relapsed or refractory B-precursor acute lymphoblastic leukaemia: a multicentre, single-arm, phase 2 study. Lancet Oncol 2015; 16: 57-66.
83. Blanco E, Beyene J, Maloney AM, et al. Non-relapse mortality in pediatric acute lymphoblastic leukemia: a systematic review and meta-analysis. Leuk Lymphoma 2012; 53: 878-85.
84. Te Winkel ML, Pieters R, Wind EJ, Bessems JH, van den Heuvel-Eibrink MM. Management and treatment of osteonecrosis in children and adolescents with acute lymphoblastic leukemia. Haematologica 2014; 99: 430-6.
85. Mattano LA Jr, Devidas M, Nachman JB, et al. Effect of alternate-week versus continuous dexamethasone scheduling on the risk of osteonecrosis in paediatric patients with acute lymphoblastic leukaemia: results from the CCG-1961 randomised cohort trial. Lancet Oncol 2012; 13: 906-15.
86. Oeffinger KC, Mertens AC, Sklar CA, et al. Chronic health conditions in adult survivors of childhood cancer. N Engl J Med 2006; 355: 1572-82.
87. Stock W. Adolescents and young adults with acute lymphoblastic leukemia. Hematology Am Soc Hematol Educ Program 2010; 2010: 21-9.
88. Pulte D, Gondos A, Brenner H. Improvement in survival in younger patients with acute lymphoblastic leukemia from the 1980s to the early 21st century. Blood 2009; 113: 1408-11.
89. DeAngelo DJ, Stevenson KE, Dahlberg SE, et al. Long-term outcome of a pediatric- inspired regimen used for adults aged 18-50 years with newly diagnosed acute lymphoblastic leukemia. Leukemia 2015; 29: 526-34.
90. Yeoh AE, Tan D, Li CK, Hori H, Tse E, Pui CH. Management of adult and paediatric acute lymphoblastic leukaemia in Asia: resource-stratified guidelines from the Asian Oncology Summit 2013. Lancet Oncol 2013; 14(12): e508-e523.
91. Stary J, Zimmermann M, Campbell M, et al. Intensive chemotherapy for childhood acute lymphoblastic leukemia: results of the randomized intercontinental trial ALL IC-BFM 2002. J Clin Oncol 2014; 32: 174-84.
92. Navarrete M, Rossi E, Brivio E, et al. Treatment of childhood acute lymphoblastic leukemia in central America: a lowermiddle income countries experience. Pediatr Blood Cancer 2014; 61: 803-9.