Association of minimal residual disease with clinical outcome in pediatric and adult acute lymphoblastic leukemia: A meta-analysis

JAMA Oncology

Volumn 3, Issue 7, 2017, Pages

  Berry, Donald A ^a   Zhou, Shouhao ^a   Higley, Howard ^b   Mukundan, Lata ^b   Fu, Shuangshuang ^c   Reaman, Gregory H ^d   Wood, Brent L ^e   Kelloff, Gary J ^f   Jessup, J Milburn ^g   Radich, Jerald P ^h  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b CCS Associates   (United States)

^c UNIVERSITY OF TEXAS   (United States)

^d CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL CANCER INSTITUTE   (United States)

^g INOVA FAIRFAX HOSPITAL   (United States)

^h USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACUTE LYMPHOBLASTIC LEUKEMIA; ADULT; AGE DISTRIBUTION; ARTICLE; B LYMPHOCYTE; CHILD; DISEASE ASSOCIATION; DRUG APPROVAL; DRUG CONTROL; DRUG EFFICACY; DRUG RESEARCH; EVENT FREE SURVIVAL; FOLLOW UP; GENOTYPE PHENOTYPE CORRELATION; HUMAN; META ANALYSIS; MINIMAL RESIDUAL DISEASE; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PHILADELPHIA 1 CHROMOSOME; PUBLICATION; REFERENCE VALUE; SAMPLE SIZE; T LYMPHOCYTE; PATHOLOGY; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

ADULT; CHILD; HUMANS; NEOPLASM, RESIDUAL; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROGNOSIS; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 85023204470     PISSN: 23742437     EISSN: 23742445     Source Type: Journal    
DOI: 10.1001/jamaoncol.2017.0580     Document Type: Article

References (64)

1. Kantarjian H, Shah NP, Hochhaus A, et al. Dasatinib versus imatinib in newly diagnosed chronic-phase chronic myeloid leukemia. N Engl J Med. 2010;362(24):2260-2270.
2. Saglio G, Kim DW, Issaragrisil S, et al; ENESTnd Investigators. Nilotinib versus imatinib for newly diagnosed chronic myeloid leukemia. N Engl J Med. 2010;362(24):2251-2259.
3. Buccisano F, Maurillo L, Gattei V, et al. The kinetics of reduction of minimal residual disease impacts on duration of response and survival of patients with acute myeloid leukemia. Leukemia. 2006;20(10):1783-1789.
4. Walter RB, Buckley SA, Pagel JM, et al. Significance of minimal residual disease before myeloablative allogeneic hematopoietic cell transplantation for AML in first and second complete remission. Blood. 2013;122(10):1813-1821.
5. Borowitz MJ, Wood BL, Devidas M, et al. Prognostic significance of minimal residual disease in high risk B-ALL: a report from Children’s Oncology Group study AALL0232. Blood. 2015;126 (8):964-971.
6. Gökbuget N, Kneba M, Raff T, et al; German Multicenter Study Group for Adult Acute Lymphoblastic Leukemia. Adult patients with acute lymphoblastic leukemia and molecular failure display a poor prognosis and are candidates for stem cell transplantation and targeted therapies. Blood. 2012;120(9):1868-1876.
7. Böttcher S, Ritgen M, Fischer K, et al. Minimal residual disease quantification is an independent predictor of progression-free and overall survival in chronic lymphocytic leukemia: a multivariate analysis from the randomized GCLLSG CLL8 trial. J Clin Oncol. 2012;30(9):980-988.
8. Korthals M, Sehnke N, Kronenwett R, et al. The level of minimal residual disease in the bone marrow of patients with multiple myeloma before high-dose therapy and autologous blood stem cell transplantation is an independent predictive parameter. Biol Blood Marrow Transplant. 2012;18 (3):423-431.e3.
9. Borowitz MJ, Devidas M, Hunger SP, et al; Children’s Oncology Group. 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(12):5477-5485.
10. 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 (3):199-209.
11. Brüggemann M, Raff T, Flohr T, et al; German Multicenter Study Group for Adult Acute Lymphoblastic Leukemia. Clinical significance of minimal residual disease quantification in adult patients with standard-risk acute lymphoblastic leukemia. Blood. 2006;107(3):1116-1123.
12. Bassan R, Spinelli O, Oldani E, et al. Improved risk classification for risk-specific therapy based on the molecular study of minimal residual disease (MRD) in adult acute lymphoblastic leukemia (ALL). Blood. 2009;113(18):4153-4162.
13. Patel B, Rai L, Buck G, et al. Minimal residual disease is a significant predictor of treatment failure in non T-lineage adult acute lymphoblastic leukaemia: final results of the international trial UKALL XII/ECOG2993. Br J Haematol. 2010;148(1): 80-89.
14. Gaipa G, Cazzaniga G, Valsecchi MG, et al. Time point-dependent concordance of flow cytometry and real-time quantitative polymerase chain reaction for minimal residual disease detection in childhood acute lymphoblastic leukemia. Haematologica. 2012;97(10):1582-1593.
15. Irving J, Jesson J, Virgo P, et al; UKALL Flow MRD Group; UK MRD steering Group. Establishment and validation of a standard protocol for the detection of minimal residual disease in B lineage childhood acute lymphoblastic leukemia by flow cytometry in a multi-center setting. Haematologica. 2009;94(6):870-874.
16. Malec M, van der Velden VH, Björklund E, et al. Analysis of minimal residual disease in childhood acute lymphoblastic leukemia: comparison between RQ-PCR analysis of Ig/TcR gene rearrangements and multicolor flow cytometric immunophenotyping. Leukemia. 2004;18(10): 1630-1636.
17. Ryan J, Quinn F, Meunier A, et al. Minimal residual disease detection in childhood acute lymphoblastic leukaemia patients at multiple time-points reveals high levels of concordance between molecular and immunophenotypic approaches. Br J Haematol. 2009;144(1):107-115.
18. Guyot P, Ades AE, Ouwens MJ, Welton NJ. Enhanced secondary analysis of survival data: reconstructing the data from published Kaplan-Meier survival curves. BMC Med Res Methodol. 2012;12:9.
19. Broglio KR, Quintana M, Foster M, et al. Association of pathologic complete response to neoadjuvant therapy in HER2-positive breast cancer with long-term outcomes: A meta-analysis. JAMA Oncol. 2016;2(6):751-760.
20. Bachanova V, Burke MJ, Yohe S, et al. Unrelated cord blood transplantation in adult and pediatric acute lymphoblastic leukemia: effect of minimal residual disease on relapse and survival. Biol Blood Marrow Transplant. 2012;18(6):963-968.
21. Beldjord K, Chevret S, Asnafi V, et al; Group for Research on Adult Acute Lymphoblastic Leukemia (GRAALL). Oncogenetics and minimal residual disease are independent outcome predictors in adult patients with acute lymphoblastic leukemia. Blood. 2014;123(24):3739-3749.
22. Bowman WP, Larsen EL, Devidas M, et al. Augmented therapy improves outcome for pediatric high risk acute lymphocytic leukemia: results of Children’s Oncology Group trial P9906. Pediatr Blood Cancer. 2011;57(4):569-577.
23. Chen IM, Harvey RC, Mullighan CG, et al. Outcome modeling with CRLF2, IKZF1, JAK, and minimal residual disease in pediatric acute lymphoblastic leukemia: a Children’s Oncology Group study. Blood. 2012;119(15):3512-3522.
24. 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(16):3206-3214.
25. Eckert C, Henze G, Seeger K, et al. Use of allogeneic hematopoietic stem-cell transplantation based on minimal residual disease response improves outcomes for children with relapsed acute lymphoblastic leukemia in the intermediate-risk group. J Clin Oncol. 2013;31(21): 2736-2742.
26. Eckert C, von Stackelberg A, Seeger K, et al. Minimal residual disease after induction is the strongest predictor of prognosis in intermediate risk relapsed acute lymphoblastic leukaemia - long-term results of trial ALL-REZ BFM P95/96. Eur J Cancer. 2013;49(6):1346-1355.
27. Flohr T, Schrauder A, Cazzaniga G, et al; International BFM Study Group (I-BFM-SG). Minimal residual disease-directed risk stratification using real-time quantitative PCR analysis of immunoglobulin and T-cell receptor gene rearrangements in the international multicenter trial AIEOP-BFM ALL 2000 for childhood acute lymphoblastic leukemia. Leukemia. 2008;22(4): 771-782.
28. Foster JH, Hawkins DS, Loken MR, Wells DA, Thomson B. Minimal residual disease detected prior to hematopoietic cell transplantation. Pediatr Blood Cancer. 2011;57(1):163-165.
29. Holowiecki J, Krawczyk-Kulis M, Giebel S, et al. Status of minimal residual disease after induction predicts outcome in both standard and high-risk Ph-negative adult acute lymphoblastic leukaemia. The Polish Adult Leukemia Group ALL 4-2002 MRD Study. Br J Haematol. 2008;142(2):227-237.
30. Imashuku S, Terui K, Matsuyama T, et al; multi-institutional collaborative study in Japan. Lack of clinical utility of minimal residual disease detection in allogeneic stem cell recipients with childhood acute lymphoblastic leukemia: multi-institutional collaborative study in Japan. Bone Marrow Transplant. 2003;31(12):1127-1135.
31. Kang H, Chen IM, Wilson CS, et al. Gene expression classifiers for relapse-free survival and minimal residual disease improve risk classification and outcome prediction in pediatric B-precursor acute lymphoblastic leukemia. Blood. 2010;115(7): 1394-1405.
32. Krampera M, Vitale A, Vincenzi C, et al. Outcome prediction by immunophenotypic minimal residual disease detection in adult T-cell acute lymphoblastic leukaemia. Br J Haematol. 2003;120(1):74-79.
33. Lee S, Kim DW, Cho BS, et al. Impact of minimal residual disease kinetics during imatinib-based treatment on transplantation outcome in Philadelphia chromosome-positive acute lymphoblastic leukemia. Leukemia. 2012;26(11): 2367-2374.
34. Meleshko AN, Savva NN, Fedasenka UU, et al. Prognostic value of MRD-dynamics in childhood acute lymphoblastic leukemia treated according to the MB-2002/2008 protocols. Leuk Res. 2011;35 (10):1312-1320.
35. Mortuza FY, Papaioannou M, Moreira IM, et al. Minimal residual disease tests provide an independent predictor of clinical outcome in adult acute lymphoblastic leukemia. J Clin Oncol. 2002; 20(4):1094-1104.
36. Pane F, Cimino G, Izzo B, et al; GIMEMA group. Significant reduction of the hybrid BCR/ABL transcripts after induction and consolidation therapy is a powerful predictor of treatment response in adult Philadelphia-positive acute lymphoblastic leukemia. Leukemia. 2005;19(4): 628-635.
37. Pulsipher MA, Langholz B, Wall DA, et al. The addition of sirolimus to tacrolimus/methotrexate GVHD prophylaxis in children with ALL: a phase 3 Children’s Oncology Group/Pediatric Blood and Marrow Transplant Consortium trial. Blood. 2014; 123(13):2017-2025.
38. Raff T, Gökbuget N, Lüschen S, et al; GMALL Study Group. Molecular relapse in adult standard-risk ALL patients detected by prospective MRD monitoring during and after maintenance treatment: data from the GMALL 06/99 and 07/03 trials. Blood. 2007;109(3):910-915.
39. Ravandi F, Jorgensen JL, Thomas DA, et al. Detection of MRD may predict the outcome of patients with Philadelphia chromosome-positive ALL treated with tyrosine kinase inhibitors plus chemotherapy. Blood. 2013;122(7):1214-1221.
40. Ribera JM, Oriol A, Morgades M, et al. Treatment of high-risk Philadelphia chromosome-negative acute lymphoblastic leukemia in adolescents and adults according to early cytologic response and minimal residual disease after consolidation assessed by flow cytometry: final results of the PETHEMA ALL-AR-03 trial. J Clin Oncol. 2014;32(15):1595-1604.
41. Salah-Eldin M, Abousamra NK, Azzam H. Clinical significance of minimal residual disease in young adults with standard-risk/Ph-negative precursor B-acute lymphoblastic leukemia: results of prospective study. Med Oncol. 2014;31(5):938.
42. Spinelli O, Peruta B, Tosi M, et al. Clearance of minimal residual disease after allogeneic stem cell transplantation and the prediction of the clinical outcome of adult patients with high-risk acute lymphoblastic leukemia. Haematologica. 2007;92 (5):612-618.
43. Stirewalt DL, Guthrie KA, Beppu L, et al. Predictors of relapse and overall survival in Philadelphia chromosome-positive acute lymphoblastic leukemia after transplantation. Biol Blood Marrow Transplant. 2003;9(3):206-212.
44. Stow P, Key L, Chen X, et al. Clinical significance of low levels of minimal residual disease at the end of remission induction therapy in childhood acute lymphoblastic leukemia. Blood. 2010;115(23):4657-4663.
45. Sutton R, Shaw PJ, Venn NC, et al. Persistent MRD before and after allogeneic BMT predicts relapse in children with acute lymphoblastic leukaemia. Br J Haematol. 2015;168(3):395-404.
46. Tucunduva L, Ruggeri A, Sanz G, et al. Impact of minimal residual disease on outcomes after umbilical cord blood transplantation for adults with Philadelphia-positive acute lymphoblastic leukaemia: an analysis on behalf of Eurocord, Cord Blood Committee and the Acute Leukaemia working party of the European group for Blood and Marrow Transplantation. Br J Haematol. 2014;166 (5):749-757.
47. Van der Velden VH, Corral L, Valsecchi MG, et al; Interfant-99 Study Group. Prognostic significance of minimal residual disease in infants with acute lymphoblastic leukemia treated within the Interfant-99 protocol. Leukemia. 2009;23(6): 1073-1079.
48. Vidriales MB, Pérez JJ, López-Berges MC, et al. Minimal residual disease in adolescent (older than 14 years) and adult acute lymphoblastic leukemias: early immunophenotypic evaluation has high clinical value. Blood. 2003;101(12):4695-4700.
49. Vilmer E, Suciu S, Ferster A, et al; Children Leukemia Cooperative Group. Long-term results of three randomized trials (58831, 58832, 58881) in childhood acute lymphoblastic leukemia: a CLCG-EORTC report. Leukemia. 2000;14(12): 2257-2266.
50. Zhao XS, Liu YR, Zhu HH, et al. Monitoring MRD with flow cytometry: an effective method to predict relapse for ALL patients after allogeneic hematopoietic stem cell transplantation. Ann Hematol. 2012;91(2):183-192.
51. Zhou J, Goldwasser MA, Li A, et al; Dana-Farber Cancer Institute ALL Consortium. Quantitative analysis of minimal residual disease predicts relapse in children with B-lineage acute lymphoblastic leukemia in DFCI ALL Consortium Protocol 95-01. Blood. 2007;110(5):1607-1611.
52. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009;6(7):e1000100.
53. Berry DA. Bayesian clinical trials. Nat Rev Drug Discov. 2006;5(1):27-36.
54. Gelman A, Carlin JB, Stern HS, Dunson DB, Vehtari A, Rubin DB. Bayesian Data Analysis. 3rd ed. Boca Raton, Florida: Chapman and Hall–CRC Press; 2013.
55. Higgins JPT, Green S, eds. Cochrane Handbook for Systematic Reviews of Interventions, Version 5.1.0. The Cochrane Collaboration, 2011. http://handbook.cochrane.org. Accessed July 24, 2016.
56. Borenstein M, Hedges LV, Higgins JPT, Rothstein HR. Introduction to Meta-Analysis. Chichester, West Sussex, United Kingdom: John Wiley and Sons, Ltd; 2009.
57. US Food and Drug Administration. Guidance for industry: pathological complete response in neoadjuvant treatment of high-risk early-stage breast cancer: use as an end point to support accelerated approval. October 2014. http://www.fda.gov/downloads/drugs/guidancecomplianceregulatoryinformation/guidances/ucm305501.pdf. Accessed July 24, 2016.
58. Cortazar P, Zhang L, Untch M, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet. 2014;384(9938):164-172.
59. Berry DA, Hudis CA. Neoadjuvant therapy in breast cancer as a basis for drug approval. JAMA Oncol. 2015;1(7):875-876.
60. Berry DA. Right-sizing adjuvant and neoadjuvant clinical trials in breast cancer. Clin Cancer Res. 2016;22(1):3-5.
61. Berry DA. Emerging innovations in clinical trial design. Clin Pharmacol Ther. 2016;99(1):82-91.
62. Topp MS, Kufer P, Gökbuget N, et al. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy-refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. J Clin Oncol. 2011; 29(18):2493-2498.
63. Wu D, Sherwood A, Fromm JR, et al. High-throughput sequencing detects minimal residual disease in acute T lymphoblastic leukemia. Sci Transl Med. 2012;4(134):134ra63.
64. Larimore K, McCormick MW, Robins HS, Greenberg PD. Shaping of human germline IgH repertoires revealed by deep sequencing. J Immunol. 2012;189(6):3221-3230.