Clinical and molecular study of radiation-induced gliomas.


Journal

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

Informations de publication

Date de publication:
07 Feb 2024
Historique:
received: 20 10 2023
accepted: 31 01 2024
medline: 8 2 2024
pubmed: 8 2 2024
entrez: 7 2 2024
Statut: epublish

Résumé

In this study, we provide a comprehensive clinical and molecular biological characterization of radiation-induced gliomas (RIG), including a risk assessment for developing gliomas. A cohort of 12 patients who developed RIG 9.5 years (3-31 years) after previous cranial radiotherapy for brain tumors or T-cell acute lymphoblastic leukemia was established. The derived risk of RIG development based on our consecutive cohort of 371 irradiated patients was 1.6% at 10 years and 3.02% at 15 years. Patients with RIG glioma had a dismal prognosis with a median survival of 7.3 months. We described radiology features that might indicate the suspicion of RIG rather than the primary tumor recurrence. Typical molecular features identified by molecular biology examination included the absence of Histon3 mutation, methylation profile of pedHGG-RTK1 and the presence of recurrent PDGFRA amplification and CDKN2A/B deletion. Of the two long-term surviving patients, one had gliomatosis cerebri, and the other had pleomorphic xanthoastrocytoma with BRAF V600E mutation. In summary, our experience highlights the need for tissue diagnostics to allow detailed molecular biological characterization of the tumor, differentiation of the secondary tumor from the recurrence of the primary disease and potentially finding a therapeutic target.

Identifiants

pubmed: 38326438
doi: 10.1038/s41598-024-53434-0
pii: 10.1038/s41598-024-53434-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

3118

Subventions

Organisme : Grantová Agentura, Univerzita Karlova
ID : 204220
Organisme : Grantová Agentura, Univerzita Karlova
ID : PRIMUS/19/MED/06
Organisme : European Union
ID : LX22NPO5102
Organisme : University Hospital Motol
ID : MH CZ-DRO,00064203
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU21-07-00419
Organisme : Ministerstvo Zdravotnictví Ceské Republiky
ID : NU23-08-00460

Informations de copyright

© 2024. The Author(s).

Références

Ohno, M. et al. Assessment of therapeutic outcome and role of reirradiation in patients with radiation-induced glioma. Radiat. Oncol. 17, 85 (2022).
doi: 10.1186/s13014-022-02054-x pubmed: 35505351 pmcid: 9066974
Relling, M. V. et al. High incidence of secondary brain tumours after radiotherapy and antimetabolites. Lancet Lond. Engl. 354, 34–39 (1999).
doi: 10.1016/S0140-6736(98)11079-6
Maluf, F. C., DeAngelis, L. M., Raizer, J. J. & Abrey, L. E. High-grade gliomas in patients with prior systemic malignancies. Cancer. 94, 3219–3224 (2002).
doi: 10.1002/cncr.10595 pubmed: 12115354
Donson, A. M. et al. Unique molecular characteristics of radiation-induced glioblastoma. J. Neuropathol. Exp. Neurol. 66, 740–749 (2007).
doi: 10.1097/nen.0b013e3181257190 pubmed: 17882018
Brat, D. J. et al. Molecular genetic alterations in radiation-induced astrocytomas. Am. J. Pathol. 154, 1431–1438 (1999).
doi: 10.1016/S0002-9440(10)65397-7 pubmed: 10329596 pmcid: 1866591
DeSisto, J. et al. Comprehensive molecular characterization of pediatric radiation-induced high-grade glioma. Nat. Commun. 12, 5531 (2021).
doi: 10.1038/s41467-021-25709-x pubmed: 34545084 pmcid: 8452624
Deng, M. Y. et al. Radiation-induced gliomas represent H3-/IDH-wild type pediatric gliomas with recurrent PDGFRA amplification and loss of CDKN2A/B. Nat. Commun. 12, 5530 (2021).
doi: 10.1038/s41467-021-25708-y pubmed: 34545083 pmcid: 8452680
Paugh, B. S. et al. Integrated molecular genetic profiling of pediatric high-grade gliomas reveals key differences with the adult disease. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 28, 3061–3068 (2010).
doi: 10.1200/JCO.2009.26.7252
Nakao, T. et al. Radiation-induced gliomas: A report of four cases and analysis of molecular biomarkers. Brain. Tumor. Pathol. 34, 149–154 (2017).
doi: 10.1007/s10014-017-0292-x pubmed: 28795231
Onishi, S. et al. Characteristics and therapeutic strategies of radiation-induced glioma: case series and comprehensive literature review. J. Neurooncol. 159, 531–538 (2022).
doi: 10.1007/s11060-022-04090-9 pubmed: 35922583
Cahan, W. G., Woodard, H. Q., Higinbotham, N. L., Stewart, F. W. & Coley, B. L. Sarcoma arising in irradiated bone: Report of eleven cases. Cancer Interdiscip. Int. J. Am. Cancer Soc. 82(1), 8–34 (1998).
Castel, D. et al. Histone H3F3A and HIST1H3B K27M mutations define two subgroups of diffuse intrinsic pontine gliomas with different prognosis and phenotypes. Acta Neuropathol. 130, 815–827 (2015).
doi: 10.1007/s00401-015-1478-0 pubmed: 26399631 pmcid: 4654747
Agaimy, A. et al. V600E BRAF mutations are alternative early molecular events in a subset of KIT/PDGFRA wildtype gastrointestinal stromal tumours. J. Clin. Pathol. 62, 613–616 (2009).
doi: 10.1136/jcp.2009.064550 pubmed: 19561230
Pathak, P. et al. Genetic alterations related to BRAF-FGFR genes and dysregulated MAPK/ERK/mTOR signaling in adult pilocytic astrocytoma. Brain Pathol. 27, 580–589 (2017).
doi: 10.1111/bpa.12444 pubmed: 27608415 pmcid: 8029314
Capper, D. et al. DNA methylation-based classification of central nervous system tumours. Nature. 555, 469–474 (2018).
doi: 10.1038/nature26000 pubmed: 29539639 pmcid: 6093218
Slavc, I. et al. Improved long-term survival of patients with recurrent medulloblastoma treated with a “MEMMAT-like” metronomic antiangiogenic approach. Cancers. 14(20), 5128 (2022).
doi: 10.3390/cancers14205128 pubmed: 36291912 pmcid: 9601092
Stary, J. et al. Intensive chemotherapy for childhood acute lymphoblastic leukemia: Results of the randomized intercontinental trial ALL IC-BFM 2002. J. Clin. Oncol. Off. J. Am. Soc. Clin. Oncol. 32, 174–184 (2014).
doi: 10.1200/JCO.2013.48.6522
Zapletalová, D. et al. Metronomic chemotherapy with the COMBAT regimen in advanced pediatric malignancies: A multicenter experience. Oncology. 82(5), 249–260 (2012).
doi: 10.1159/000336483 pubmed: 22538363
Grogan, P. T. et al. Case report: Radiographic complete response of radiation-induced glioblastoma to front-line radiotherapy: A report and molecular characterization of two unique cases. Front. Neurol. 21(14), 1099424 (2023).
doi: 10.3389/fneur.2023.1099424
Leary, J. B., Anderson-Mellies, A. & Green, A. L. Population-based analysis of radiation-induced gliomas after cranial radiotherapy for childhood cancers. Neuro-Oncol. Adv. 4(1), vdac159 (2022).
doi: 10.1093/noajnl/vdac159
Neglia, J. P. et al. New primary neoplasms of the central nervous system in survivors of childhood cancer: A report from the childhood cancer survivor study. J. Natl. Cancer Inst. 98, 1528–1537 (2006).
doi: 10.1093/jnci/djj411 pubmed: 17077355
Whitehouse, J. P. et al. Defining the molecular features of radiation-induced glioma: A systematic review and meta-analysis. Neuro-Oncol. Adv. 3, vdab109 (2021).
doi: 10.1093/noajnl/vdab109

Auteurs

Katerina Trkova (K)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.
Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

David Sumerauer (D)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.
Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Adela Bubenikova (A)

Department of Neurosurgery, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Lenka Krskova (L)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.
Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Pathology and Molecular Medicine, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Ales Vicha (A)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.
Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Miroslav Koblizek (M)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.
Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Pathology and Molecular Medicine, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Josef Zamecnik (J)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.
Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Pathology and Molecular Medicine, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Bruno Jurasek (B)

Department of Radiology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Martin Kyncl (M)

Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Radiology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Bela Malinova (B)

Department of Oncology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Barbora Ondrova (B)

Proton Therapy Center Czech, Budínova 1a, 180 00, Prague, Czech Republic.

David T W Jones (DTW)

Division of Pediatric Glioma Research, Hopp Children's Cancer Center (KiTZ), Heidelberg, Germany.
National Center for Tumor Diseases (NCT), NCT Heidelberg, a partnership between DKFZ and Heidelberg University Hospital, Heidelberg, Germany.
German Cancer Research Center (DKFZ), Heidelberg, Germany.

Martin Sill (M)

Division of Pediatric Glioma Research, Hopp Children's Cancer Center (KiTZ), Heidelberg, Germany.
National Center for Tumor Diseases (NCT), NCT Heidelberg, a partnership between DKFZ and Heidelberg University Hospital, Heidelberg, Germany.
German Cancer Research Center (DKFZ), Heidelberg, Germany.

Martina Strnadova (M)

Department of Pathology and Molecular Medicine, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Lucie Stolova (L)

Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Adela Misove (A)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.
Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Vladimir Benes (V)

Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic.
Department of Neurosurgery, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic.

Michal Zapotocky (M)

Prague Brain Tumor Research Group, Second Faculty of Medicine, Charles University and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic. michal.zapotocky@fnmotol.cz.
Center for Pediatric Neuro-Oncology, University Hospital Motol, V Uvalu 84 , 15006, Prague 5, Czech Republic. michal.zapotocky@fnmotol.cz.
Department of Pediatric Hematology and Oncology, Second Faculty of Medicine, Charles University Prague and University Hospital Motol, V Uvalu 84, 15006, Prague 5, Czech Republic. michal.zapotocky@fnmotol.cz.

Classifications MeSH