Advantages of a genomic DNA-based next-generation sequencing assay for detection of mutant NPM1 measurable residual disease in AML

Abstract: Mutations in the nucleophosmin-1 (NPM1) gene are among the most common molecular aberrations in acute myeloid leukemia (AML). Various studies have established mutant NPM1 (mNPM1) as a faithful molecular measurable residual disease (MRD) marker with prognostic significance. Assessment of pr...

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Main Authors: Christian M. Vonk, Tim Grob, Melissa Rijken, François G. Kavelaars, Jolinda M. L. Konijnenburg, Gert J. Ossenkoppele, Markus G. Manz, Violaine Havelange, Yngvar Fløisand, Bob Löwenberg, Peter J. M. Valk
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:Blood Advances
Online Access:http://www.sciencedirect.com/science/article/pii/S2473952924007043
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author Christian M. Vonk
Tim Grob
Melissa Rijken
François G. Kavelaars
Jolinda M. L. Konijnenburg
Gert J. Ossenkoppele
Markus G. Manz
Violaine Havelange
Yngvar Fløisand
Bob Löwenberg
Peter J. M. Valk
author_facet Christian M. Vonk
Tim Grob
Melissa Rijken
François G. Kavelaars
Jolinda M. L. Konijnenburg
Gert J. Ossenkoppele
Markus G. Manz
Violaine Havelange
Yngvar Fløisand
Bob Löwenberg
Peter J. M. Valk
author_sort Christian M. Vonk
collection DOAJ
description Abstract: Mutations in the nucleophosmin-1 (NPM1) gene are among the most common molecular aberrations in acute myeloid leukemia (AML). Various studies have established mutant NPM1 (mNPM1) as a faithful molecular measurable residual disease (MRD) marker with prognostic significance. Assessment of prognostic mNPM1 is included in the European LeukemiaNet recommendations on MRD detection in AML. Because of recent advancements of promising drugs targeting mNPM1 AML, monitoring of mNPM1 MRD has gained interest, and is generally done by reverse transcriptase quantitative polymerase chain reaction (RT-qPCR). However, these RT-qPCR assays use complementary DNA (cDNA) as input, are based on gene expression levels of mNPM1, and are generally limited to specific mNPM1 gene variants. The main advantages of next-generation sequencing (NGS) using genomic DNA as input are stability, independence of gene expression levels, and the ability to detect any NPM1 variant in a single assay. Here, we comprehensively investigated the applicability of NGS on DNA to detect mNPM1 MRD in a cohort of 119 (cDNA) and 310 (DNA) patients with mNPM1 AML in complete remission after 2 cycles of induction chemotherapy. We demonstrate high correlations in levels and prognostic value between RT-qPCR/cDNA and NGS/DNA approaches, postulating NGS/DNA as an attractive alternative to RT-qPCR. We report that the 2% mNPM1/ABL1 threshold by RT-qPCR/cDNA corresponds to an NGS/DNA variant allele frequency of 0.01%. The NGS/DNA threshold of >0.01% after 2 cycles of induction chemotherapy identifies significantly more patients with AML with an increased relapse risk than current RT-qPCR/cDNA assays. The prognostic significance of mNPM1 MRD appears greatest in patients with AML with FLT3-internal tandem duplications.
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spelling doaj-art-baba935dbead4878a791d1290e586fb32025-08-20T03:04:38ZengElsevierBlood Advances2473-95292025-03-01951069107710.1182/bloodadvances.2024014490Advantages of a genomic DNA-based next-generation sequencing assay for detection of mutant NPM1 measurable residual disease in AMLChristian M. Vonk0Tim Grob1Melissa Rijken2François G. Kavelaars3Jolinda M. L. Konijnenburg4Gert J. Ossenkoppele5Markus G. Manz6Violaine Havelange7Yngvar Fløisand8Bob Löwenberg9Peter J. M. Valk10Department of Hematology, Erasmus Medical Center Cancer Institute, University Medical Center Rotterdam, Rotterdam, The NetherlandsDepartment of Hematology, Erasmus Medical Center Cancer Institute, University Medical Center Rotterdam, Rotterdam, The NetherlandsDepartment of Hematology, Erasmus Medical Center Cancer Institute, University Medical Center Rotterdam, Rotterdam, The NetherlandsDepartment of Hematology, Erasmus Medical Center Cancer Institute, University Medical Center Rotterdam, Rotterdam, The NetherlandsDepartment of Hematology, Erasmus Medical Center Cancer Institute, University Medical Center Rotterdam, Rotterdam, The NetherlandsDepartment of Hematology, Cancer Center Amsterdam, Amsterdam University Medical Center, Amsterdam, The NetherlandsDepartment of Medical Oncology and Hematology, Comprehensive Cancer Center Zurich, University and University Hospital Zurich, Zurich, SwitzerlandDepartment of Hematology, Cliniques universitaires Saint-Luc, Brussels, BelgiumCentre for Cancer Cell Reprogramming, Institute of Clinical Medicine, Faculty of Medicine, University of Oslo, Oslo, Norway; Department of Hematology, Oslo University Hospital, Oslo, NorwayDepartment of Hematology, Erasmus Medical Center Cancer Institute, University Medical Center Rotterdam, Rotterdam, The NetherlandsDepartment of Hematology, Erasmus Medical Center Cancer Institute, University Medical Center Rotterdam, Rotterdam, The Netherlands; Correspondence: Peter J. M. Valk, Department of Hematology, Erasmus University Medical Center Rotterdam, Nc806, Wytemaweg 80, 3015 CN Rotterdam Z-H, The Netherlands;Abstract: Mutations in the nucleophosmin-1 (NPM1) gene are among the most common molecular aberrations in acute myeloid leukemia (AML). Various studies have established mutant NPM1 (mNPM1) as a faithful molecular measurable residual disease (MRD) marker with prognostic significance. Assessment of prognostic mNPM1 is included in the European LeukemiaNet recommendations on MRD detection in AML. Because of recent advancements of promising drugs targeting mNPM1 AML, monitoring of mNPM1 MRD has gained interest, and is generally done by reverse transcriptase quantitative polymerase chain reaction (RT-qPCR). However, these RT-qPCR assays use complementary DNA (cDNA) as input, are based on gene expression levels of mNPM1, and are generally limited to specific mNPM1 gene variants. The main advantages of next-generation sequencing (NGS) using genomic DNA as input are stability, independence of gene expression levels, and the ability to detect any NPM1 variant in a single assay. Here, we comprehensively investigated the applicability of NGS on DNA to detect mNPM1 MRD in a cohort of 119 (cDNA) and 310 (DNA) patients with mNPM1 AML in complete remission after 2 cycles of induction chemotherapy. We demonstrate high correlations in levels and prognostic value between RT-qPCR/cDNA and NGS/DNA approaches, postulating NGS/DNA as an attractive alternative to RT-qPCR. We report that the 2% mNPM1/ABL1 threshold by RT-qPCR/cDNA corresponds to an NGS/DNA variant allele frequency of 0.01%. The NGS/DNA threshold of >0.01% after 2 cycles of induction chemotherapy identifies significantly more patients with AML with an increased relapse risk than current RT-qPCR/cDNA assays. The prognostic significance of mNPM1 MRD appears greatest in patients with AML with FLT3-internal tandem duplications.http://www.sciencedirect.com/science/article/pii/S2473952924007043
spellingShingle Christian M. Vonk
Tim Grob
Melissa Rijken
François G. Kavelaars
Jolinda M. L. Konijnenburg
Gert J. Ossenkoppele
Markus G. Manz
Violaine Havelange
Yngvar Fløisand
Bob Löwenberg
Peter J. M. Valk
Advantages of a genomic DNA-based next-generation sequencing assay for detection of mutant NPM1 measurable residual disease in AML
Blood Advances
title Advantages of a genomic DNA-based next-generation sequencing assay for detection of mutant NPM1 measurable residual disease in AML
title_full Advantages of a genomic DNA-based next-generation sequencing assay for detection of mutant NPM1 measurable residual disease in AML
title_fullStr Advantages of a genomic DNA-based next-generation sequencing assay for detection of mutant NPM1 measurable residual disease in AML
title_full_unstemmed Advantages of a genomic DNA-based next-generation sequencing assay for detection of mutant NPM1 measurable residual disease in AML
title_short Advantages of a genomic DNA-based next-generation sequencing assay for detection of mutant NPM1 measurable residual disease in AML
title_sort advantages of a genomic dna based next generation sequencing assay for detection of mutant npm1 measurable residual disease in aml
url http://www.sciencedirect.com/science/article/pii/S2473952924007043
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