Prospective use of molecular minimal residual disease for risk stratification in children and adolescents with acute lymphoblastic leukemia : Long-term results of the AIEOP-BFM ALL 2000 trial in Austria.
Acute lymphoblastic leukemia
Minimal residual disease
Outcome
Prognosis
Stratification
Journal
Wiener klinische Wochenschrift
ISSN: 1613-7671
Titre abrégé: Wien Klin Wochenschr
Pays: Austria
ID NLM: 21620870R
Informations de publication
Date de publication:
03 Aug 2023
03 Aug 2023
Historique:
received:
29
05
2023
accepted:
28
06
2023
medline:
3
8
2023
pubmed:
3
8
2023
entrez:
3
8
2023
Statut:
aheadofprint
Résumé
Since 1979 Austrian children and adolescents with acute lymphoblastic leukemia (ALL) have been treated according to protocols of the Berlin-Frankfurt-Münster (BFM) study group. The Associazione Italiana di Ematologia e Oncologia Pediatrica and BFM (AIEOP-BFM) ALL 2000 study was designed to prospectively study patient stratification into three risk groups using minimal residual disease (MRD) on two time points during the patient's early disease course. The MRD levels were monitored by detection of clone-specific rearrangements of the immunoglobulin and T‑cell receptor genes applying a quantitative polymerase chain reaction-based technique. The 7‑year event-free survival (EFS) and overall survival rates for all 608 Austrian patients treated between June 1999 and December 2009 within the AIEOP-BFM 2000 study were 84 ± 2% and 91 ± 1%, respectively, with a median observation time of 6.58 years. Event-free survival for patients with precursor B‑cell and T‑cell ALL were 84 ± 2% (n = 521) and 84 ± 4% (n = 87; p = 0.460), respectively. The MRD assessment was feasible in 94% of the patients and allowed the definition of precursor B‑cell ALL patients with a low, intermediate or high risk of relapse even on top of clinically relevant subgroups. A similar finding with respect to MRD relevance in T‑ALL patients was not possible due to the small number of patients and events. Since this pivotal international AIEOP-BFM ALL 2000 trial, molecular response to treatment has been continuously used with additional refinements to stratify patients into different risk groups in all successive trials of the AIEOP-BFM ALL study group.
Identifiants
pubmed: 37535134
doi: 10.1007/s00508-023-02249-6
pii: 10.1007/s00508-023-02249-6
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : St. Anna CCRI
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
Hunger SP, Mullighan CG. Acute lymphoblastic leukemia in children. N Engl J Med. 2015;373(16):1541–52.
doi: 10.1056/NEJMra1400972
pubmed: 26465987
Pui CH. Recent advances in childhood acute lymphoblastic leukemia. J Formos Med Assoc. 2004;103(2):85–95.
pubmed: 15083238
Pui CH. Precision medicine in acute lymphoblastic leukemia. Front Med. 2020;14(6):689–700.
doi: 10.1007/s11684-020-0759-8
pubmed: 33074527
pmcid: 9671279
Moricke A, Zimmermann M, Reiter A, Gadner H, Odenwald E, Harbott J, et al. Prognostic impact of age in children and adolescents with acute lymphoblastic leukemia: data from the trials ALL-BFM 86, 90, and 95. Klin Padiatr. 2005;217(6):310–20.
doi: 10.1055/s-2005-872515
pubmed: 16307416
Moricke A, Zimmermann M, Reiter A, Henze G, Schrauder A, Gadner H, et al. Long-term results of five consecutive trials in childhood acute lymphoblastic leukemia performed by the ALL-BFM study group from 1981 to 2000. Leukemia. 2010;24(2):265–84.
doi: 10.1038/leu.2009.257
pubmed: 20010625
Pieters R, de Groot-Kruseman H, Van der Velden V, Fiocco M, van den Berg H, de Bont E, et al. Successful therapy reduction and intensification for childhood acute lymphoblastic leukemia based on minimal residual disease monitoring: study ALL10 from the Dutch childhood oncology group. J Clin Oncol. 2016;34(22):2591–601.
doi: 10.1200/JCO.2015.64.6364
pubmed: 27269950
Schmiegelow K, Forestier E, Hellebostad M, Heyman M, Kristinsson J, Soderhall S, et al. Long-term results of NOPHO ALL-92 and ALL-2000 studies of childhood acute lymphoblastic leukemia. Leukemia. 2010;24(2):345–54.
doi: 10.1038/leu.2009.251
pubmed: 20010622
Biondi A, Valsecchi MG, Seriu T, D’Aniello E, Willemse MJ, Fasching K, et al. Molecular detection of minimal residual disease is a strong predictive factor of relapse in childhood B‑lineage acute lymphoblastic leukemia with medium risk features. A case control study of the International BFM study group. Leukemia. 2000;14(11):1939–43.
doi: 10.1038/sj.leu.2401922
pubmed: 11069029
Conter V, Bartram CR, Valsecchi MG, Schrauder A, Panzer-Grumayer R, Moricke A, 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):3206–14.
doi: 10.1182/blood-2009-10-248146
pubmed: 20154213
Coustan-Smith E, Sancho J, Hancock ML, Boyett JM, Behm FG, Raimondi SC, et al. Clinical importance of minimal residual disease in childhood acute lymphoblastic leukemia. Blood. 2000;96(8):2691–6.
doi: 10.1182/blood.V96.8.2691
pubmed: 11023499
Schrappe M, Valsecchi MG, Bartram CR, Schrauder A, Panzer-Grumayer R, Moricke A, et al. Late MRD response determines relapse risk overall and in subsets of childhood T‑cell ALL: results of the AIEOP-BFM-ALL 2000 study. Blood. 2011;118(8):2077–84.
doi: 10.1182/blood-2011-03-338707
pubmed: 21719599
van Dongen JJ, Seriu T, Panzer-Grumayer ER, Biondi A, Pongers-Willemse MJ, Corral L, et al. Prognostic value of minimal residual disease in acute lymphoblastic leukaemia in childhood. Lancet. 1998;352(9142):1731–8.
doi: 10.1016/S0140-6736(98)04058-6
pubmed: 9848348
Willemse MJ, Seriu T, Hettinger K, d’Aniello E, Hop WC, Panzer-Grumayer ER, et al. Detection of minimal residual disease identifies differences in treatment response between T‑ALL and precursor B‑ALL. Blood. 2002;99(12):4386–93.
doi: 10.1182/blood.V99.12.4386
pubmed: 12036866
Zhou J, Goldwasser MA, Li A, Dahlberg SE, Neuberg D, Wang H, et al. 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):1607–11.
doi: 10.1182/blood-2006-09-045369
pubmed: 17485550
pmcid: 1975844
Dworzak MN, Froschl G, Printz D, Mann G, Potschger U, Muhlegger N, et al. Prognostic significance and modalities of flow cytometric minimal residual disease detection in childhood acute lymphoblastic leukemia. Blood. 2002;99(6):1952–8.
doi: 10.1182/blood.V99.6.1952
pubmed: 11877265
Pieters R, Schrappe M, De Lorenzo P, Hann I, De Rossi G, Felice M, et al. A treatment protocol for infants younger than 1 year with acute lymphoblastic leukaemia (Interfant-99): an observational study and a multicentre randomised trial. Lancet. 2007;370(9583):240–50.
doi: 10.1016/S0140-6736(07)61126-X
pubmed: 17658395
Biondi A, Schrappe M, De Lorenzo P, Castor A, Lucchini G, Gandemer V, 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(9):936–45.
doi: 10.1016/S1470-2045(12)70377-7
pubmed: 22898679
pmcid: 3431502
van der Does-van den Berg A, Bartram CR, Basso G, Benoit YC, Biondi A, Debatin KM, et al. Minimal requirements for the diagnosis, classification, and evaluation of the treatment of childhood acute lymphoblastic leukemia (ALL) in the “BFM family” cooperative group. Med Pediatr Oncol. 1992;20(6):497–505.
doi: 10.1002/mpo.2950200603
pubmed: 1435520
Bene MC, Castoldi G, Knapp W, Ludwig WD, Matutes E, Orfao A, et al. Proposals for the immunological classification of acute leukemias. European group for the immunological characterization of leukemias (EGIL). Leukemia. 1995;9(10):1783–6.
pubmed: 7564526
Attarbaschi A, Mann G, Konig M, Dworzak MN, Trebo MM, Muhlegger N, et al. Incidence and relevance of secondary chromosome abnormalities in childhood TEL/AML1+ acute lymphoblastic leukemia: an interphase FISH analysis. Leukemia. 2004;18(10):1611–6.
doi: 10.1038/sj.leu.2403471
pubmed: 15356655
Reismuller B, Steiner M, Pichler H, Dworzak M, Urban C, Meister B, et al. High hyperdiploid acute lymphoblastic leukemia (ALL)-A 25-year population-based survey of the Austrian ALL-BFM (Berlin-Frankfurt-Munster) study group. Pediatr Blood Cancer. 2017; https://doi.org/10.1002/pbc.26327 .
doi: 10.1002/pbc.26327
pubmed: 27804199
Flohr T, Schrauder A, Cazzaniga G, Panzer-Grumayer R, van der Velden V, Fischer S, et al. 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):771–82.
doi: 10.1038/leu.2008.5
pubmed: 18239620
Attarbaschi A, Mann G, Zimmermann M, Bader P, Barisone E, Basso G, et al. Randomized post-induction and delayed intensification therapy in high-risk pediatric acute lymphoblastic leukemia: long-term results of the international AIEOP-BFM ALL 2000 trial. Leukemia. 2020;34(6):1694–700.
doi: 10.1038/s41375-019-0670-y
pubmed: 31806872
Locatelli F, Valsecchi MG, Moricke A, Zimmermann M, Gruhn B, Biondi A, et al. Protocol II vs protocol III given twice during reinduction therapy in children with medium-risk ALL. Blood. 2017;130(19):2146–9.
doi: 10.1182/blood-2017-05-782086
pubmed: 28939722
Schrappe M, Bleckmann K, Zimmermann M, Biondi A, Moricke A, Locatelli F, et al. Reduced-intensity delayed intensification in standard-risk pediatric acute lymphoblastic leukemia defined by undetectable minimal residual disease: results of an international randomized trial (AIEOP-BFM ALL 2000). J Clin Oncol. 2018;36(3):244–53.
doi: 10.1200/JCO.2017.74.4946
pubmed: 29148893
Moricke A, Zimmermann M, Valsecchi MG, Stanulla M, Biondi A, Mann G, et al. Dexamethasone vs prednisone in induction treatment of pediatric ALL: results of the randomized trial AIEOP-BFM ALL 2000. Blood. 2016;127(17):2101–12.
doi: 10.1182/blood-2015-09-670729
pubmed: 26888258
Kalbfleisch JD, Prentice RL. The statisticalanalysis of failure time data. New York: JohnWiley and Sons; 1980, 163–188.
Hunger SP, Winick NJ, Sather HN, Carroll WL. Therapy of low-risk subsets of childhood acute lymphoblastic leukemia: when do we say enough? Pediatr Blood Cancer. 2005;45(7):876–80.
doi: 10.1002/pbc.20501
pubmed: 16007585
Bertaina A, Vinti L, Strocchio L, Gaspari S, Caruso R, Algeri M, et al. The combination of bortezomib with chemotherapy to treat relapsed/refractory acute lymphoblastic leukaemia of childhood. Br J Haematol. 2017;176(4):629–36.
doi: 10.1111/bjh.14505
pubmed: 28116786
von Stackelberg A, Locatelli F, Zugmaier G, Handgretinger R, Trippett TM, Rizzari C, et al. Phase I/phase II study of blinatumomab in pediatric patients with relapsed/refractory acute lymphoblastic leukemia. J Clin Oncol. 2016;34(36):4381–9.
doi: 10.1200/JCO.2016.67.3301
Gaynon PS, Desai AA, Bostrom BC, Hutchinson RJ, Lange BJ, Nachman JB, et al. Early response to therapy and outcome in childhood acute lymphoblastic leukemia: a review. Cancer. 1997;80(9):1717–26.
doi: 10.1002/(SICI)1097-0142(19971101)80:9<1717::AID-CNCR4>3.0.CO;2-B
pubmed: 9351539
Larsen EC, Devidas M, Chen S, Salzer WL, Raetz EA, Loh ML, et al. Dexamethasone and high-dose methotrexate improve outcome for children and young adults with high-risk B‑acute lymphoblastic leukemia: a report from children’s oncology group study AALL0232. J Clin Oncol. 2016;34(20):2380–8.
doi: 10.1200/JCO.2015.62.4544
pubmed: 27114587
pmcid: 4981974
Seibel NL, Steinherz PG, Sather HN, Nachman JB, Delaat C, Ettinger LJ, et al. Early postinduction intensification therapy improves survival for children and adolescents with high-risk acute lymphoblastic leukemia: a report from the children’s oncology group. Blood. 2008;111(5):2548–55.
doi: 10.1182/blood-2007-02-070342
pubmed: 18039957
pmcid: 2254538
Toft N, Birgens H, Abrahamsson J, Griskevicius L, Hallbook H, Heyman M, et al. Results of NOPHO ALL2008 treatment for patients aged 1–45 years with acute lymphoblastic leukemia. Leukemia. 2018;32(3):606–15.
doi: 10.1038/leu.2017.265
pubmed: 28819280
Vora A, Goulden N, Mitchell C, Hancock J, Hough R, Rowntree 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(8):809–18.
doi: 10.1016/S1470-2045(14)70243-8
pubmed: 24924991
Arico M, Conter V, Valsecchi MG, Rizzari C, Boccalatte MF, Barisone E, et al. Treatment reduction in highly selected standard-risk childhood acute lymphoblastic leukemia. The AIEOP ALL-9501 study. Haematologica. 2005;90(9):1186–91.
pubmed: 16154841
Moricke A, Reiter A, Zimmermann M, Gadner H, Stanulla M, Dordelmann M, et al. Risk-adjusted therapy of acute lymphoblastic leukemia can decrease treatment burden and improve survival: treatment results of 2169 unselected pediatric and adolescent patients enrolled in the trial ALL-BFM 95. Blood. 2008;111(9):4477–89.
doi: 10.1182/blood-2007-09-112920
pubmed: 18285545
Schrappe M, Reiter A, Ludwig WD, Harbott J, Zimmermann M, Hiddemann W, et al. Improved outcome in childhood acute lymphoblastic leukemia despite reduced use of anthracyclines and cranial radiotherapy: results of trial ALL-BFM 90. German-Austrian-Swiss ALL-BFM study group. Blood. 2000;95(11):3310–22.
pubmed: 10828010
Borowitz MJ, Devidas M, Hunger SP, Bowman WP, Carroll AJ, Carroll WL, 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(12):5477–85.
doi: 10.1182/blood-2008-01-132837
pubmed: 18388178
pmcid: 2424148
Cave H, van der Werff ten Bosch J, Suciu S, Guidal C, Waterkeyn C, Otten J, et al. Clinical significance of minimal residual disease in childhood acute lymphoblastic leukemia. European organization for research and treatment of cancer—childhood leukemia cooperative group. N Engl J Med. 1998;339(9):591–8.
doi: 10.1056/NEJM199808273390904
pubmed: 9718378
Basso G, Veltroni M, Valsecchi MG, Dworzak MN, Ratei R, Silvestri D, et al. Risk of relapse of childhood acute lymphoblastic leukemia is predicted by flow cytometric measurement of residual disease on day 15 bone marrow. J Clin Oncol. 2009;27(31):5168–74.
doi: 10.1200/JCO.2008.20.8934
pubmed: 19805690
Maurer-Granofszky M, Schumich A, Buldini B, Gaipa G, Kappelmayer J, Mejstrikova E, et al. An extensive quality control and quality assurance (QC/QA) program significantly improves inter-laboratory concordance rates of flow-cytometric minimal residual disease assessment in acute lymphoblastic leukemia: an I‑BFM-FLOW-network report. Cancers (Basel). 2021;13(23):6148. https://doi.org/10.3390/cancers13236148 .
doi: 10.3390/cancers13236148
pubmed: 34885257
Testi AM, Attarbaschi A, Valsecchi MG, Moricke A, Cario G, Niggli F, et al. Outcome of adolescent patients with acute lymphoblastic leukaemia aged 10–14 years as compared with those aged 15–17 years: long-term results of 1094 patients of the AIEOP-BFM ALL 2000 study. Eur J Cancer. 2019;122:61–71.
doi: 10.1016/j.ejca.2019.09.004
pubmed: 31629941