Skip to main content
Top
Published in: Annals of Hematology 10/2020

Open Access 01-10-2020 | Acute Myeloid Leukemia | Original Article

Allogeneic stem cell transplantation mitigates the adverse prognostic impact of high diagnostic BAALC and MN1 expression in AML

Authors: Madlen Jentzsch, Marius Bill, Juliane Grimm, Dominic Brauer, Donata Backhaus, Karoline Goldmann, Julia Schulz, Dietger Niederwieser, Uwe Platzbecker, Sebastian Schwind

Published in: Annals of Hematology | Issue 10/2020

Login to get access

Abstract

For most acute myeloid leukemia (AML) patients, an allogeneic hematopoietic stem cell transplantation (HSCT) offers the highest chance of sustained remissions and long-term survival. At diagnosis, high expression of the AML-associated genes BAALC (brain and acute leukemia, cytoplasmic) and MN1 (meningioma-1) were repeatedly linked to inferior outcomes in patients consolidated with chemotherapy while data for patients receiving HSCT remain limited. Using clinically applicable digital droplet PCR assays, we analyzed the diagnostic BAALC/ABL1 and MN1/ABL1 copy numbers in 302 AML patients. High BAALC/ABL1 and MN1/ABL1 copy numbers associated with common adverse prognostic factors at diagnosis. However, while high diagnostic copy numbers of both genes associated with shorter event free survival (EFS) and overall survival (OS) in patients receiving chemotherapy, there was no prognostic impact in patients undergoing HSCT. Our data suggests that the adverse prognostic impact of high BAALC and MN1 expression are mitigated by allogeneic HSCT. But preHSCT BAALC/ABL1 and MN1/ABL1 assessed in remission prior to HSCT remained prognosticators for EFS and OS independent of the diagnostic expression status. Whether allogeneic HSCT may improve survival for AML patients with high diagnostic BAALC or MN1 expression should be investigated prospectively and may improve informed decisions towards individualized consolidation options in AML.
Appendix
Available only for authorised users
Literature
1.
go back to reference Döhner H, Estey E, Grimwade D, Amadori S, Appelbaum FR, Büchner T et al (2017) Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood 129:424–447CrossRef Döhner H, Estey E, Grimwade D, Amadori S, Appelbaum FR, Büchner T et al (2017) Diagnosis and management of AML in adults: 2017 ELN recommendations from an international expert panel. Blood 129:424–447CrossRef
2.
go back to reference McSweeney PA, Niederwieser D, Shizuru JA, Sandmaier BM, Molina AJ, Maloney DG et al (2001) Hematopoietic cell transplantation in older patients with hematologic malignancies: replacing high-dose cytotoxic therapy with graft-versus- tumor effects. Blood 97:3390–3400CrossRef McSweeney PA, Niederwieser D, Shizuru JA, Sandmaier BM, Molina AJ, Maloney DG et al (2001) Hematopoietic cell transplantation in older patients with hematologic malignancies: replacing high-dose cytotoxic therapy with graft-versus- tumor effects. Blood 97:3390–3400CrossRef
3.
go back to reference Horowitz MM, Gale RP, Sondel PM, Goldman JM, Kersey J, Kolb HJ et al (1990) Graft-versus-leukemia reactions after bone marrow transplantation. Blood 75:555–562CrossRef Horowitz MM, Gale RP, Sondel PM, Goldman JM, Kersey J, Kolb HJ et al (1990) Graft-versus-leukemia reactions after bone marrow transplantation. Blood 75:555–562CrossRef
4.
go back to reference Heuser M, Beutel G, Krauter J, Döhner K, von Neuhoff N, Schlegelberger B et al (2006) High meningioma 1 (MN1) expression as a predictor for poor outcome in acute myeloid leukemia with normal cytogenetics. Blood 108:3898–3905CrossRef Heuser M, Beutel G, Krauter J, Döhner K, von Neuhoff N, Schlegelberger B et al (2006) High meningioma 1 (MN1) expression as a predictor for poor outcome in acute myeloid leukemia with normal cytogenetics. Blood 108:3898–3905CrossRef
5.
go back to reference Heuser M, Berg T, Kuchenbauer F, Lai CK, Park G, Fung S et al (2012) Functional role of BAALC in leukemogenesis. Leukemia 26:532–536CrossRef Heuser M, Berg T, Kuchenbauer F, Lai CK, Park G, Fung S et al (2012) Functional role of BAALC in leukemogenesis. Leukemia 26:532–536CrossRef
6.
go back to reference Baldus CD, Tanner SM, Kusewittb DF, Liyanarachchi S, Choi C, Caligiuri MA et al (2003) BAALC, a novel marker of human hematopoietic progenitor cells. Exp Hematol 31:1051–1056PubMed Baldus CD, Tanner SM, Kusewittb DF, Liyanarachchi S, Choi C, Caligiuri MA et al (2003) BAALC, a novel marker of human hematopoietic progenitor cells. Exp Hematol 31:1051–1056PubMed
7.
go back to reference Tanner SM, Austin JL, Leone G, Rush LJ, Plass C, Heinonen K et al (2001) BAALC, the human member of a novel mammalian neuroectoderm gene lineage, is implicated in hematopoiesis and acute leukemia. Proc Natl Acad Sci U S A 98:13901–13906CrossRef Tanner SM, Austin JL, Leone G, Rush LJ, Plass C, Heinonen K et al (2001) BAALC, the human member of a novel mammalian neuroectoderm gene lineage, is implicated in hematopoiesis and acute leukemia. Proc Natl Acad Sci U S A 98:13901–13906CrossRef
8.
go back to reference Lekanne Deprez RH, Groen NA, van Biezen NA, Hagemeijer A, van Drunen E, Koper JW et al (1991) A t(4;22) in a meningioma points to the localization of a putative tumor-suppressor gene. Am J Hum Genet 48:783–790PubMedPubMedCentral Lekanne Deprez RH, Groen NA, van Biezen NA, Hagemeijer A, van Drunen E, Koper JW et al (1991) A t(4;22) in a meningioma points to the localization of a putative tumor-suppressor gene. Am J Hum Genet 48:783–790PubMedPubMedCentral
9.
go back to reference Langer C, Radmacher MD, Ruppert AS, Whitman SP, Paschka P, Mrózek K et al (2008) High BAALC expression associates with other molecular prognostic markers, poor outcome, and a distinct gene expression signature in cytogenetically normal patients younger than 60 years with acute myeloid leukemia: a Cancer and Leukemia Group B (CALGB) study. Blood 111:5371–5379CrossRef Langer C, Radmacher MD, Ruppert AS, Whitman SP, Paschka P, Mrózek K et al (2008) High BAALC expression associates with other molecular prognostic markers, poor outcome, and a distinct gene expression signature in cytogenetically normal patients younger than 60 years with acute myeloid leukemia: a Cancer and Leukemia Group B (CALGB) study. Blood 111:5371–5379CrossRef
10.
go back to reference Schwind S, Marcucci G, Maharry K, Radmacher MD, Mrózek K, Holland KB et al (2010) BAALC and ERG expression levels are associated with outcome and distinct gene and microRNA expression profiles in older patients with de novo cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study. Blood 116:5660–5669CrossRef Schwind S, Marcucci G, Maharry K, Radmacher MD, Mrózek K, Holland KB et al (2010) BAALC and ERG expression levels are associated with outcome and distinct gene and microRNA expression profiles in older patients with de novo cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B study. Blood 116:5660–5669CrossRef
11.
go back to reference Schwind S, Marcucci G, Kohlschmidt J, Radmacher MD, Mrózek K, Maharry K et al (2011) Low expression of MN1 associates with better treatment response in older patients with de novo cytogenetically normal acute myeloid leukemia. Blood 118:4188–4198CrossRef Schwind S, Marcucci G, Kohlschmidt J, Radmacher MD, Mrózek K, Maharry K et al (2011) Low expression of MN1 associates with better treatment response in older patients with de novo cytogenetically normal acute myeloid leukemia. Blood 118:4188–4198CrossRef
12.
go back to reference Metzeler KH, Dufour A, Benthaus T, Hummel M, Sauerland MC, Heinecke A et al (2009) ERG expression is an independent prognostic factor and allows refined risk stratification in cytogenetically normal acute myeloid leukemia: a comprehensive analysis of ERG, MN1, and BAALC transcript levels using oligonucleotide microarrays. J Clin Oncol 27:5031–5038CrossRef Metzeler KH, Dufour A, Benthaus T, Hummel M, Sauerland MC, Heinecke A et al (2009) ERG expression is an independent prognostic factor and allows refined risk stratification in cytogenetically normal acute myeloid leukemia: a comprehensive analysis of ERG, MN1, and BAALC transcript levels using oligonucleotide microarrays. J Clin Oncol 27:5031–5038CrossRef
13.
go back to reference Langer C, Marcucci G, Holland KB, Radmacher MD, Maharry K, Paschka P et al (2009) Prognostic importance of MN1 transcript levels, and biologic insights from MN1-associated gene and microRNA expression signatures in cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B Study. J Clin Oncol 27:3198–3204CrossRef Langer C, Marcucci G, Holland KB, Radmacher MD, Maharry K, Paschka P et al (2009) Prognostic importance of MN1 transcript levels, and biologic insights from MN1-associated gene and microRNA expression signatures in cytogenetically normal acute myeloid leukemia: a Cancer and Leukemia Group B Study. J Clin Oncol 27:3198–3204CrossRef
14.
go back to reference Baldus CD, Tanner SM, Ruppert AS, Whitman SP, Archer KJ, Marcucci G et al (2003) BAALC expression predicts clinical outcome of de novo acute myeloid leukemia patients with normal cytogenetics: a Cancer and Leukemia Group B study. Blood 102:1613–1618CrossRef Baldus CD, Tanner SM, Ruppert AS, Whitman SP, Archer KJ, Marcucci G et al (2003) BAALC expression predicts clinical outcome of de novo acute myeloid leukemia patients with normal cytogenetics: a Cancer and Leukemia Group B study. Blood 102:1613–1618CrossRef
15.
go back to reference Jentzsch M, Bill M, Grimm J, Schulz J, Goldmann K, Beinicke S et al (2017) High BAALC copy numbers in peripheral blood prior to allogeneic transplantation predict early relapse in acute myeloid leukemia patients. Oncotarget. 8:87944–87954CrossRef Jentzsch M, Bill M, Grimm J, Schulz J, Goldmann K, Beinicke S et al (2017) High BAALC copy numbers in peripheral blood prior to allogeneic transplantation predict early relapse in acute myeloid leukemia patients. Oncotarget. 8:87944–87954CrossRef
16.
go back to reference Jentzsch M, Bill M, Grimm J, Schulz J, Beinicke S, Häntschel J et al (2019) Prognostic impact of blood MN1 copy numbers before allogeneic stem cell transplantation in patients with acute myeloid leukemia. HemaSphere 3:e167CrossRef Jentzsch M, Bill M, Grimm J, Schulz J, Beinicke S, Häntschel J et al (2019) Prognostic impact of blood MN1 copy numbers before allogeneic stem cell transplantation in patients with acute myeloid leukemia. HemaSphere 3:e167CrossRef
17.
go back to reference Weber S, Alpermann T, Dicker F, Jeromin S, Nadarajah N, Eder C et al (2014) BAALC expression: a suitable marker for prognostic risk stratification and detection of residual disease in cytogenetically normal acute myeloid leukemia. Blood Cancer J 4:e173CrossRef Weber S, Alpermann T, Dicker F, Jeromin S, Nadarajah N, Eder C et al (2014) BAALC expression: a suitable marker for prognostic risk stratification and detection of residual disease in cytogenetically normal acute myeloid leukemia. Blood Cancer J 4:e173CrossRef
18.
go back to reference Najima Y, Ohashi K, Kawamura M, Onozuka Y, Yamaguchi T, Akiyama H et al (2010) Molecular monitoring of BAALC expression in patients with CD34-positive acute leukemia. J Hematol 91:636–645 Najima Y, Ohashi K, Kawamura M, Onozuka Y, Yamaguchi T, Akiyama H et al (2010) Molecular monitoring of BAALC expression in patients with CD34-positive acute leukemia. J Hematol 91:636–645
19.
go back to reference Carturan S, Petiti J, Rosso V, Calabrese C, Signorino E, Bot-Sartor G et al (2016) Variable but consistent pattern of meningioma 1 gene (MN1) expression in different genetic subsets of acute myelogenous leukaemia and its potential use as a marker for minimal residual disease detection. Oncotarget 7:74082–74096CrossRef Carturan S, Petiti J, Rosso V, Calabrese C, Signorino E, Bot-Sartor G et al (2016) Variable but consistent pattern of meningioma 1 gene (MN1) expression in different genetic subsets of acute myelogenous leukaemia and its potential use as a marker for minimal residual disease detection. Oncotarget 7:74082–74096CrossRef
20.
go back to reference Zhang J, Shi J, Zhang G, Zhang X, Yang X, Yang S et al (2018) BAALC and ERG expression levels at diagnosis have no prognosis impact on acute myeloid leukemia patients undergoing allogeneic hematopoietic stem cell transplantation. Ann Hematol 97(8):1391–1397CrossRef Zhang J, Shi J, Zhang G, Zhang X, Yang X, Yang S et al (2018) BAALC and ERG expression levels at diagnosis have no prognosis impact on acute myeloid leukemia patients undergoing allogeneic hematopoietic stem cell transplantation. Ann Hematol 97(8):1391–1397CrossRef
21.
go back to reference Hindson CM, Chevillet JR, Briggs HA, Gallichotte EN, Ruf IK, Hindson BJ et al (2013) Absolute quantification by droplet digital PCR versus analog real- time PCR. Nat Methods 10:1003–1005CrossRef Hindson CM, Chevillet JR, Briggs HA, Gallichotte EN, Ruf IK, Hindson BJ et al (2013) Absolute quantification by droplet digital PCR versus analog real- time PCR. Nat Methods 10:1003–1005CrossRef
22.
go back to reference Jentzsch M, Bill M, Grimm J, Schulz J, Schuhmann L, Brauer D et al (2020) High expression of the stem cell marker GPR56 at diagnosis identifies acute myeloid leukemia patients at higher relapse risk after allogeneic stem cell transplantation in context with the CD34+/CD38- population. Haematologica. https://doi.org/10.3324/haematol.2019.229260 Jentzsch M, Bill M, Grimm J, Schulz J, Schuhmann L, Brauer D et al (2020) High expression of the stem cell marker GPR56 at diagnosis identifies acute myeloid leukemia patients at higher relapse risk after allogeneic stem cell transplantation in context with the CD34+/CD38- population. Haematologica. https://​doi.​org/​10.​3324/​haematol.​2019.​229260
23.
go back to reference Bill M, Jentzsch M, Grimm J, Schubert K, Lange T, Cross M et al (2017) Prognostic impact of the European LeukemiaNet standardized reporting system in older AML patients receiving stem cell transplantation after non-myeloablative conditioning. Bone Marrow Transplant 52:932–935CrossRef Bill M, Jentzsch M, Grimm J, Schubert K, Lange T, Cross M et al (2017) Prognostic impact of the European LeukemiaNet standardized reporting system in older AML patients receiving stem cell transplantation after non-myeloablative conditioning. Bone Marrow Transplant 52:932–935CrossRef
24.
go back to reference Grimm J, Bill M, Jentzsch M, Beinicke S, Häntschel J, Goldmann K et al (2019) Clinical impact of clonal hematopoiesis in acute myeloid leukemia patients receiving allogeneic transplantation. Bone Marrow Transplant 54:1189–1197CrossRef Grimm J, Bill M, Jentzsch M, Beinicke S, Häntschel J, Goldmann K et al (2019) Clinical impact of clonal hematopoiesis in acute myeloid leukemia patients receiving allogeneic transplantation. Bone Marrow Transplant 54:1189–1197CrossRef
26.
go back to reference Breems DA, van Putten WLJ, De Greef GE, Van Zelderen-Bhola SL, Gerssen-Schoorl KB, Mellink CH et al (2008) Monosomal karyotype in acute myeloid leukemia: a better indicator of poor prognosis than a complex karyotype. J Clin Oncol 26:4791–4797CrossRef Breems DA, van Putten WLJ, De Greef GE, Van Zelderen-Bhola SL, Gerssen-Schoorl KB, Mellink CH et al (2008) Monosomal karyotype in acute myeloid leukemia: a better indicator of poor prognosis than a complex karyotype. J Clin Oncol 26:4791–4797CrossRef
27.
go back to reference Bienz M, Ludwig M, Leibundgut EO, Mueller BU, Ratschiller D, Solenthaler M et al (2005) Risk assessment in patients with acute myeloid leukemia and a normal karyotype. Clin Cancer Res 11:1416–1424CrossRef Bienz M, Ludwig M, Leibundgut EO, Mueller BU, Ratschiller D, Solenthaler M et al (2005) Risk assessment in patients with acute myeloid leukemia and a normal karyotype. Clin Cancer Res 11:1416–1424CrossRef
28.
go back to reference Baldus CD, Thiede C, Soucek S, Bloomfield CD, Thiel E, Ehninger G (2006) BAALC expression and FLT3 internal tandem duplication mutations in acute myeloid leukemia patients with normal cytogenetics: prognostic implications. J Clin Oncol 24:790–797CrossRef Baldus CD, Thiede C, Soucek S, Bloomfield CD, Thiel E, Ehninger G (2006) BAALC expression and FLT3 internal tandem duplication mutations in acute myeloid leukemia patients with normal cytogenetics: prognostic implications. J Clin Oncol 24:790–797CrossRef
29.
go back to reference Brand J, van Vliet MH, de Best L, Valk PJ, Viëtor HE, Löwenberg B et al (2013) A standardized microarray assay for the independent gene expression markers in AML: EVI1 and BAALC. Exp Hematol Oncol 2:7CrossRef Brand J, van Vliet MH, de Best L, Valk PJ, Viëtor HE, Löwenberg B et al (2013) A standardized microarray assay for the independent gene expression markers in AML: EVI1 and BAALC. Exp Hematol Oncol 2:7CrossRef
30.
go back to reference Santamaría C, Chillón MC, García-Sanz R, Pérez C, Caballero MD, Mateos MV et al (2010) BAALC is an important predictor of refractoriness to chemotherapy and poor survival in intermediate-risk acute myeloid leukemia (AML). Ann Hematol 89:453–458CrossRef Santamaría C, Chillón MC, García-Sanz R, Pérez C, Caballero MD, Mateos MV et al (2010) BAALC is an important predictor of refractoriness to chemotherapy and poor survival in intermediate-risk acute myeloid leukemia (AML). Ann Hematol 89:453–458CrossRef
31.
go back to reference Damiani D, Tiribelli M, Franzoni A, Michelutti A, Fabbro D, Cavallin M et al (2013) BAALC overexpression retains its negative prognostic role across all cytogenetic risk groups in acute myeloid leukemia patients. Am J Hematol 88:848–852CrossRef Damiani D, Tiribelli M, Franzoni A, Michelutti A, Fabbro D, Cavallin M et al (2013) BAALC overexpression retains its negative prognostic role across all cytogenetic risk groups in acute myeloid leukemia patients. Am J Hematol 88:848–852CrossRef
32.
go back to reference Haferlach C, Kern W, Schindela S, Kohlmann A, Alpermann T, Schnittger S et al (2012) Gene expression of BAALC, CDKNIB, ERG and MN1 adds independent prognostic information to cytogenetics and molecular mutations in adult acute myeloid leukemia. Genes Chromosom Cancer 51:257–265CrossRef Haferlach C, Kern W, Schindela S, Kohlmann A, Alpermann T, Schnittger S et al (2012) Gene expression of BAALC, CDKNIB, ERG and MN1 adds independent prognostic information to cytogenetics and molecular mutations in adult acute myeloid leukemia. Genes Chromosom Cancer 51:257–265CrossRef
33.
go back to reference Yoon JH, Kim HJ, Shin SH, Yahng SA, Lee SE, Cho BS et al (2014) Implication of higher BAALC expression in combination with other gene mutations in adult cytogenetically normal acute myeloid leukemia. Leuk Lymphoma 55:110–120CrossRef Yoon JH, Kim HJ, Shin SH, Yahng SA, Lee SE, Cho BS et al (2014) Implication of higher BAALC expression in combination with other gene mutations in adult cytogenetically normal acute myeloid leukemia. Leuk Lymphoma 55:110–120CrossRef
34.
go back to reference Liu T, Jankovic D, Brault L, Ehret S, Baty F, Stavropoulou V et al (2010) Functional characterization of high levels of meningioma 1 as collaborating oncogene in acute leukemia. Leukemia 24:601–512CrossRef Liu T, Jankovic D, Brault L, Ehret S, Baty F, Stavropoulou V et al (2010) Functional characterization of high levels of meningioma 1 as collaborating oncogene in acute leukemia. Leukemia 24:601–512CrossRef
35.
go back to reference Hills RK, Castaigne S, Appelbaum FR et al (2014) Addition of gemtuzumab ozogamicin to induction chemotherapy in adult patients with acute myeloid leukaemia: a meta-analysis of individual patient data from randomised controlled trials. Lancet Oncol 15(9):986–996CrossRef Hills RK, Castaigne S, Appelbaum FR et al (2014) Addition of gemtuzumab ozogamicin to induction chemotherapy in adult patients with acute myeloid leukaemia: a meta-analysis of individual patient data from randomised controlled trials. Lancet Oncol 15(9):986–996CrossRef
36.
go back to reference Ho AD, Schetelig J, Bochtler T, Schaich M, Schäfer-Eckart K, Hänel M et al (2016) Allogeneic stem cell transplantation improves survival in patients with acute myeloid leukemia characterized by a high allelic ratio of mutant FLT3-ITD. Biol Blood Marrow Transplant 22:462–469CrossRef Ho AD, Schetelig J, Bochtler T, Schaich M, Schäfer-Eckart K, Hänel M et al (2016) Allogeneic stem cell transplantation improves survival in patients with acute myeloid leukemia characterized by a high allelic ratio of mutant FLT3-ITD. Biol Blood Marrow Transplant 22:462–469CrossRef
37.
go back to reference Grimm J, Jentzsch M, Bill M et al (2020) Prognostic Impact of the European LeukemiaNet 2017 risk classification in acute myeloid leukemia patients receiving allogeneic transplantation. Blood Adv In Press Grimm J, Jentzsch M, Bill M et al (2020) Prognostic Impact of the European LeukemiaNet 2017 risk classification in acute myeloid leukemia patients receiving allogeneic transplantation. Blood Adv In Press
38.
go back to reference Araki D, Wood BL, Othus M, Radich JP, Halpern AB, Zhou Y et al (2016) Allogeneic hematopoietic cell transplantation for acute myeloid leukemia: time to move toward a minimal residual disease–based definition of complete remission? J Clin Oncol 34:329–336CrossRef Araki D, Wood BL, Othus M, Radich JP, Halpern AB, Zhou Y et al (2016) Allogeneic hematopoietic cell transplantation for acute myeloid leukemia: time to move toward a minimal residual disease–based definition of complete remission? J Clin Oncol 34:329–336CrossRef
39.
go back to reference Zhou Y, Othus M, Araki D, Wood BL, Radich JP, Halpern AB et al (2016) Pre- and post-transplant quantification of measurable (‘minimal’) residual disease via multiparameter flow cytometry in adult acute myeloid leukemia. Leukemia 30:1456–1464CrossRef Zhou Y, Othus M, Araki D, Wood BL, Radich JP, Halpern AB et al (2016) Pre- and post-transplant quantification of measurable (‘minimal’) residual disease via multiparameter flow cytometry in adult acute myeloid leukemia. Leukemia 30:1456–1464CrossRef
40.
go back to reference Thol F, Gabdoulline R, Liebich A, Klement P, Schiller J, Kandziora C et al (2018) Measurable residual disease monitoring by NGS before allogeneic hematopoietic cell transplantation in AML. Blood 132:1703–1713CrossRef Thol F, Gabdoulline R, Liebich A, Klement P, Schiller J, Kandziora C et al (2018) Measurable residual disease monitoring by NGS before allogeneic hematopoietic cell transplantation in AML. Blood 132:1703–1713CrossRef
41.
go back to reference Bill M, Grimm J, Jentzsch M, Kloss L, Goldmann K, Schulz J et al (2018) Digital droplet PCR-based absolute quantification of pre-transplant NPM1 mutation burden predicts relapse in acute myeloid leukemia patients. Ann Hematol 97:1757–1765CrossRef Bill M, Grimm J, Jentzsch M, Kloss L, Goldmann K, Schulz J et al (2018) Digital droplet PCR-based absolute quantification of pre-transplant NPM1 mutation burden predicts relapse in acute myeloid leukemia patients. Ann Hematol 97:1757–1765CrossRef
Metadata
Title
Allogeneic stem cell transplantation mitigates the adverse prognostic impact of high diagnostic BAALC and MN1 expression in AML
Authors
Madlen Jentzsch
Marius Bill
Juliane Grimm
Dominic Brauer
Donata Backhaus
Karoline Goldmann
Julia Schulz
Dietger Niederwieser
Uwe Platzbecker
Sebastian Schwind
Publication date
01-10-2020
Publisher
Springer Berlin Heidelberg
Published in
Annals of Hematology / Issue 10/2020
Print ISSN: 0939-5555
Electronic ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-020-04235-8

Other articles of this Issue 10/2020

Annals of Hematology 10/2020 Go to the issue