Application of droplet digital PCR in minimal residual disease monitoring of rare fusion transcripts and mutations in haematological malignancies.


Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
16 03 2024
Historique:
received: 13 12 2023
accepted: 13 03 2024
medline: 18 3 2024
pubmed: 17 3 2024
entrez: 17 3 2024
Statut: epublish

Résumé

Leukaemia of various subtypes are driven by distinct chromosomal rearrangement or genetic abnormalities. The leukaemogenic fusion transcripts or genetic mutations serve as molecular markers for minimal residual disease (MRD) monitoring. The current study evaluated the applicability of several droplet digital PCR assays for the detection of these targets at RNA and DNA levels (atypical BCR::ABL1 e19a2, e23a2ins52, e13a2ins74, rare types of CBFB::MYH11 (G and I), PCM1::JAK2, KMT2A::ELL2, PICALM::MLLT10 fusion transcripts and CEBPA frame-shift and insertion/duplication mutations) with high sensitivity. The analytical performances were assessed by the limit of blanks, limit of detection, limit of quantification and linear regression. Our data demonstrated serial MRD monitoring for patients at molecular level could become "digitalized", which was deemed important to guide clinicians in treatment decision for better patient care.

Identifiants

pubmed: 38493200
doi: 10.1038/s41598-024-57016-y
pii: 10.1038/s41598-024-57016-y
doi:

Substances chimiques

ELL2 protein, human 0
Transcriptional Elongation Factors 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

6400

Informations de copyright

© 2024. The Author(s).

Références

Bruggemann, M. & Kotrova, M. Minimal residual disease in adult ALL: Technical aspects and implications for correct clinical interpretation. Blood Adv. 1, 2456–2466 (2017).
doi: 10.1182/bloodadvances.2017009845 pubmed: 29296895 pmcid: 5729622
Buckley, S. A. et al. Minimal residual disease prior to allogeneic hematopoietic cell transplantation in acute myeloid leukemia: A meta-analysis. Haematologica 102, 865–873 (2017).
doi: 10.3324/haematol.2016.159343 pubmed: 28126965 pmcid: 5477605
Short, N. J. et al. Association of measurable residual disease with survival outcomes in patients with acute myeloid leukemia: A systematic review and meta-analysis. JAMA Oncol. 6, 1890–1899 (2020).
doi: 10.1001/jamaoncol.2020.4600 pubmed: 33030517 pmcid: 7545346
Shah, N. P. NCCN guidelines updates: Discontinuing TKI therapy in the treatment of chronic myeloid leukemia. J. Natl. Compr. Cancer Netw. 17, 611–613 (2019).
Jabbour, E. & Kantarjian, H. Chronic myeloid leukemia: 2020 Update on diagnosis, therapy and monitoring. Am. J. Hematol. 95, 691–709 (2020).
doi: 10.1002/ajh.25792 pubmed: 32239758
Jennings, L. J., George, D., Czech, J., Yu, M. & Joseph, L. Detection and quantification of BCR-ABL1 fusion transcripts by droplet digital PCR. J. Mol. Diagn. 16, 174–179 (2014).
doi: 10.1016/j.jmoldx.2013.10.007 pubmed: 24389534
Brunetti, C. et al. Droplet digital PCR is a reliable tool for monitoring minimal residual disease in acute promyelocytic leukemia. J. Mol. Diagn. 19, 437–444 (2017).
doi: 10.1016/j.jmoldx.2017.01.004 pubmed: 28268092
Coccaro, N. et al. Droplet digital PCR is a robust tool for monitoring minimal residual disease in adult Philadelphia-positive acute lymphoblastic leukemia. J. Mol. Diagn. 20, 474–482 (2018).
doi: 10.1016/j.jmoldx.2018.03.002 pubmed: 29625246
Scott, S. et al. Assessment of droplet digital polymerase chain reaction for measuring BCR-ABL1 in chronic myeloid leukaemia in an international interlaboratory study. Br. J. Haematol. 194, 53–60 (2021).
doi: 10.1111/bjh.17521 pubmed: 34114218
Kadkol, S. S., Bruno, A., Dodge, C., Lindgren, V. & Ravandi, F. Comprehensive analysis of CBFbeta-MYH11 fusion transcripts in acute myeloid leukemia by RT-PCR analysis. J. Mol. Diagn. 6, 22–27 (2004).
doi: 10.1016/S1525-1578(10)60487-4 pubmed: 14736823 pmcid: 1867465
Armbruster, D. A. & Pry, T. Limit of blank, limit of detection and limit of quantitation. Clin. Biochem. Rev. 29(Suppl 1), S49-52 (2008).
pubmed: 18852857 pmcid: 2556583
Baccarani, M. et al. European LeukemiaNet recommendations for the management of chronic myeloid leukemia: 2013. Blood 122, 872–884 (2013).
doi: 10.1182/blood-2013-05-501569 pubmed: 23803709 pmcid: 4915804
van Dongen, J. J. et al. Standardized RT-PCR analysis of fusion gene transcripts from chromosome aberrations in acute leukemia for detection of minimal residual disease. Report of the BIOMED-1 Concerted Action: Investigation of minimal residual disease in acute leukemia. Leukemia 13, 1901–1928 (1999).
doi: 10.1038/sj.leu.2401592 pubmed: 10602411
Burmeister, T. & Reinhardt, R. A multiplex PCR for improved detection of typical and atypical BCR-ABL fusion transcripts. Leuk. Res. 32, 579–585 (2008).
doi: 10.1016/j.leukres.2007.08.017 pubmed: 17928051
Bernardi, S. et al. Digital PCR improves the quantitation of DMR and the selection of CML candidates to TKIs discontinuation. Cancer Med. 8, 2041–2055 (2019).
doi: 10.1002/cam4.2087 pubmed: 30950237 pmcid: 6536984
Nicolini, F. E. et al. Evaluation of residual disease and TKI duration are critical predictive factors for molecular recurrence after stopping imatinib first-line in chronic phase CML patients. Clin. Cancer Res. 25, 6606–6613 (2019).
doi: 10.1158/1078-0432.CCR-18-3373 pubmed: 31292142
Dohner, H. et al. Diagnosis and management of AML in adults: 2022 Recommendations from an international expert panel on behalf of the ELN. Blood 140, 1345–1377 (2022).
doi: 10.1182/blood.2022016867 pubmed: 35797463
Ommen, H. B. Monitoring minimal residual disease in acute myeloid leukaemia: A review of the current evolving strategies. Ther. Adv. Hematol. 7, 3–16 (2016).
doi: 10.1177/2040620715614529 pubmed: 26834951 pmcid: 4713887
Schuurhuis, G. J. et al. Minimal/measurable residual disease in AML: A consensus document from the European LeukemiaNet MRD Working Party. Blood 131, 1275–1291 (2018).
doi: 10.1182/blood-2017-09-801498 pubmed: 29330221 pmcid: 5865231
Heuser, M. et al. 2021 Update on MRD in acute myeloid leukemia: A consensus document from the European LeukemiaNet MRD Working Party. Blood 138, 2753–2767 (2021).
doi: 10.1182/blood.2021013626 pubmed: 34724563 pmcid: 8718623
Au, C. H., Wa, A., Ho, D. N., Chan, T. L. & Ma, E. S. Clinical evaluation of panel testing by next-generation sequencing (NGS) for gene mutations in myeloid neoplasms. Diagn. Pathol. 11, 11 (2016).
doi: 10.1186/s13000-016-0456-8 pubmed: 26796102 pmcid: 4722624
Perl, A. E. et al. Gilteritinib or chemotherapy for relapsed or refractory FLT3-mutated AML. N. Engl. J. Med. 381, 1728–1740 (2019).
doi: 10.1056/NEJMoa1902688 pubmed: 31665578
DiNardo, C. D. et al. Durable remissions with Ivosidenib in IDH1-mutated relapsed or refractory AML. N. Engl. J. Med. 378, 2386–2398 (2018).
doi: 10.1056/NEJMoa1716984 pubmed: 29860938
Stein, E. M. et al. Enasidenib in mutant IDH2 relapsed or refractory acute myeloid leukemia. Blood 130, 722–731 (2017).
doi: 10.1182/blood-2017-04-779405 pubmed: 28588020 pmcid: 5572791
Fiskus, W. et al. Effective Menin inhibitor-based combinations against AML with MLL rearrangement or NPM1 mutation (NPM1c). Blood Cancer J. 12, 5 (2022).
doi: 10.1038/s41408-021-00603-3 pubmed: 35017466 pmcid: 8752621
Issa, G. C. et al. The menin inhibitor revumenib in KMT2A-rearranged or NPM1-mutant leukaemia. Nature 615, 920–924 (2023).
doi: 10.1038/s41586-023-05812-3 pubmed: 36922593 pmcid: 10060155
Cilloni, D. et al. Digital PCR in myeloid malignancies: Ready to replace quantitative PCR? Int. J. Mol. Sci. 20 (2019).
Grassi, S. et al. Digital droplet PCR is a specific and sensitive tool for detecting IDH2 mutations in acute myeloid leukemia patients. Cancers (Basel) 12 (2020).
Mencia-Trinchant, N. et al. Minimal residual disease monitoring of acute myeloid leukemia by massively multiplex digital PCR in patients with NPM1 mutations. J. Mol. Diagn. 19, 537–548 (2017).
doi: 10.1016/j.jmoldx.2017.03.005 pubmed: 28525762 pmcid: 5500824
Hoffmeister, L. M. et al. Panel-based RNA fusion sequencing improves diagnostics of pediatric acute myeloid leukemia. Leukemia (2023).
Au, C. H. et al. Rapid detection of chromosomal translocation and precise breakpoint characterization in acute myeloid leukemia by nanopore long-read sequencing. Cancer Genet. 239, 22–25 (2019).
doi: 10.1016/j.cancergen.2019.08.005 pubmed: 31473470
DiNardo, K. W., LeBlanc, T. W. & Chen, H. Novel agents and regimens in acute myeloid leukemia: Latest updates from 2022 ASH Annual Meeting. J. Hematol. Oncol. 16, 17 (2023).
doi: 10.1186/s13045-023-01411-x pubmed: 36869366 pmcid: 9983204
Young, A. L., Davis, H. C. & Challen, G. A. Droplet digital PCR for oncogenic KMT2A fusion detection. J. Mol. Diagn. 25, 898–906 (2023).
doi: 10.1016/j.jmoldx.2023.09.006 pubmed: 37813299
Gronlund, J. K. et al. Droplet digital PCR for sensitive relapse detection in acute myeloid leukaemia patients transplanted by reduced intensity conditioning. Eur. J. Haematol. (2024).

Auteurs

Beca B K Ip (BBK)

Division of Molecular Pathology, Department of Pathology, Hong Kong Sanatorium & Hospital, Happy Valley, Hong Kong.

Anthony T C Wong (ATC)

Division of Molecular Pathology, Department of Pathology, Hong Kong Sanatorium & Hospital, Happy Valley, Hong Kong.

Janet Hei Yin Law (JHY)

Division of Molecular Pathology, Department of Pathology, Hong Kong Sanatorium & Hospital, Happy Valley, Hong Kong.

Chun Hang Au (CH)

Division of Molecular Pathology, Department of Pathology, Hong Kong Sanatorium & Hospital, Happy Valley, Hong Kong.

Shing Yan Ma (SY)

Specialist in Haematology & Haematological Oncology, Causeway Bay, Hong Kong.

James C S Chim (JCS)

Department of Medicine and Comprehensive Oncology Centre, Hong Kong Sanatorium & Hospital, Happy Valley, Hong Kong.

Raymond H S Liang (RHS)

Department of Medicine and Comprehensive Oncology Centre, Hong Kong Sanatorium & Hospital, Happy Valley, Hong Kong.

Anskar Y H Leung (AYH)

Department of Medicine, The University of Hong Kong, Pok Fu Lam, Hong Kong.

Thomas S K Wan (TSK)

Division of Molecular Pathology, Department of Pathology, Hong Kong Sanatorium & Hospital, Happy Valley, Hong Kong.

Edmond S K Ma (ESK)

Division of Molecular Pathology, Department of Pathology, Hong Kong Sanatorium & Hospital, Happy Valley, Hong Kong. eskma@hksh.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH