High-grade gliomas in adolescents and young adults highlight histomolecular differences from their adult and pediatric counterparts.


Journal

Neuro-oncology
ISSN: 1523-5866
Titre abrégé: Neuro Oncol
Pays: England
ID NLM: 100887420

Informations de publication

Date de publication:
17 08 2020
Historique:
pubmed: 7 2 2020
medline: 7 4 2021
entrez: 7 2 2020
Statut: ppublish

Résumé

Considering that pediatric high-grade gliomas (HGGs) are biologically distinct from their adult counterparts, the objective of this study was to define the landscape of HGGs in adolescents and young adults (AYAs). We performed a multicentric retrospective study of 112 AYAs from adult and pediatric Ile-de-France neurosurgical units, treated between 1998 and 2013 to analyze their clinicoradiological and histomolecular profiles. The inclusion criteria were age between 15 and 25 years, histopathological HGG diagnosis, available clinical data, and preoperative and follow-up MRI. MRI and tumoral samples were centrally reviewed. Immunohistochemistry and complementary molecular techniques such as targeted/next-generation sequencing, whole exome sequencing, and DNA-methylation analyses were performed to achieve an integrated diagnosis according to the 2016 World Health Organization (WHO) classification. Based on 80 documented AYA patients, HGGs constitute heterogeneous clinicopathological and molecular groups, with a predominant representation of pediatric subtypes (histone H3-mutants, 40%) but also adult subtypes (isocitrate dehydrogenase [IDH] mutants, 28%) characterized by the rarity of oligodendrogliomas, IDH mutants, and 1p/19q codeletion and the relative high frequency of "rare adult IDH mutations" (20%). H3G34-mutants (14%) represent the most specific subgroup in AYAs. In the H3K27-mutant subgroup, non-brainstem diffuse midline gliomas are more frequent (66.7%) than diffuse intrinsic pontine gliomas (23.8%), contrary to what is observed in children. We found that WHO grade has no prognostic value, but molecular subgrouping has major prognostic importance. HGGs in AYAs could benefit from a specific classification, driven by molecular subtyping rather than age group. Collaborative efforts are needed from pediatric and adult neuro-oncology teams to improve the management of HGGs in AYAs.

Sections du résumé

BACKGROUND
Considering that pediatric high-grade gliomas (HGGs) are biologically distinct from their adult counterparts, the objective of this study was to define the landscape of HGGs in adolescents and young adults (AYAs).
METHODS
We performed a multicentric retrospective study of 112 AYAs from adult and pediatric Ile-de-France neurosurgical units, treated between 1998 and 2013 to analyze their clinicoradiological and histomolecular profiles. The inclusion criteria were age between 15 and 25 years, histopathological HGG diagnosis, available clinical data, and preoperative and follow-up MRI. MRI and tumoral samples were centrally reviewed. Immunohistochemistry and complementary molecular techniques such as targeted/next-generation sequencing, whole exome sequencing, and DNA-methylation analyses were performed to achieve an integrated diagnosis according to the 2016 World Health Organization (WHO) classification.
RESULTS
Based on 80 documented AYA patients, HGGs constitute heterogeneous clinicopathological and molecular groups, with a predominant representation of pediatric subtypes (histone H3-mutants, 40%) but also adult subtypes (isocitrate dehydrogenase [IDH] mutants, 28%) characterized by the rarity of oligodendrogliomas, IDH mutants, and 1p/19q codeletion and the relative high frequency of "rare adult IDH mutations" (20%). H3G34-mutants (14%) represent the most specific subgroup in AYAs. In the H3K27-mutant subgroup, non-brainstem diffuse midline gliomas are more frequent (66.7%) than diffuse intrinsic pontine gliomas (23.8%), contrary to what is observed in children. We found that WHO grade has no prognostic value, but molecular subgrouping has major prognostic importance.
CONCLUSIONS
HGGs in AYAs could benefit from a specific classification, driven by molecular subtyping rather than age group. Collaborative efforts are needed from pediatric and adult neuro-oncology teams to improve the management of HGGs in AYAs.

Identifiants

pubmed: 32025728
pii: 5728472
doi: 10.1093/neuonc/noaa024
pmc: PMC7594566
doi:

Substances chimiques

Isocitrate Dehydrogenase EC 1.1.1.41

Types de publication

Journal Article Multicenter Study Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1190-1202

Commentaires et corrections

Type : CommentIn

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Society for Neuro-Oncology. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

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Auteurs

Alexandre Roux (A)

Department of Neurosurgery, University Hospital Group (GHU) Paris-Sainte-Anne Hospital, Paris, France.
Paris Descartes University, Sorbonne Paris Cité, Paris, France.
Inserm Unit 1266, Imaging Biomarkers of Brain Disorders, Institute of Psychiatry and Neurosciences of Paris, Paris, France.

Johan Pallud (J)

Department of Neurosurgery, University Hospital Group (GHU) Paris-Sainte-Anne Hospital, Paris, France.
Paris Descartes University, Sorbonne Paris Cité, Paris, France.
Inserm Unit 1266, Imaging Biomarkers of Brain Disorders, Institute of Psychiatry and Neurosciences of Paris, Paris, France.

Raphaël Saffroy (R)

Department of Biochemistry, Paul-Brousse Hospital, Villejuif, France.

Myriam Edjlali-Goujon (M)

Department of Neuroradiology, Sainte-Anne Hospital, Paris, France.

Marie-Anne Debily (MA)

Inserm Unit 981, Biomarkers and New Therapeutic Targets in Oncology Team, Genomics and Oncogenesis of Brain Tumors, Paris-Sud University, Paris-Saclay University, Villejuif, France.
Evry University, Paris-Saclay University, Evry cedex, France.

Nathalie Boddaert (N)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.
Department of Neuroradiology, Necker Enfants-Malades Hospital, Paris, France.

Marc Sanson (M)

Brain and Spine Institute (ICM), Experimental Neuro-Oncology Department, Inserm U1127, Sorbonne University, Paris, France.
Department of Neurology 2, Mazarin Unit, Pitié-Salpêtrière Hospital, Paris, France.

Stéphanie Puget (S)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.
Department of Neurosurgery, Necker Enfants-Malades Hospital, Paris, France.

Steven Knafo (S)

Department of Neurosurgery, Bicêtre Hospital, Paris-Sud University, Kremlin-Bicêtre, France.

Clovis Adam (C)

Department of Pathology, Bicêtre Hospital, Paris-Sud University, Kremlin-Bicêtre, France.

Thierry Faillot (T)

Department of Neurosurgery, Beaujon Hospital, Clichy, France.

Dominique Cazals-Hatem (D)

Department of Pathology, Beaujon Hospital, Clichy, France.

Emmanuel Mandonnet (E)

Department of Neurosurgery, Lariboisière Hospital, Paris, France.
Paris 7 University, Paris, France.

Marc Polivka (M)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.
Inserm Unit 1266, Imaging Biomarkers of Brain Disorders, Institute of Psychiatry and Neurosciences of Paris, Paris, France.
Department of Pathology, Lariboisière Hospital, Paris, France.

Georges Dorfmüller (G)

Department of Pediatric Neurosurgery, Rothschild Foundation Hospital, Paris, France.

Aurélie Dauta (A)

Department of Neurosurgery, Henri-Mordor Hospital, Créteil, France.

Mathilde Desplanques (M)

Department of Neuropathology, GHU Paris-Sainte-Anne Hospital, Paris, France.

Albane Gareton (A)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.

Mélanie Pages (M)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.
Inserm Unit 1266, Imaging Biomarkers of Brain Disorders, Institute of Psychiatry and Neurosciences of Paris, Paris, France.
Department of Pathology, Lariboisière Hospital, Paris, France.

Arnault Tauziede-Espariat (A)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.
Inserm Unit 1266, Imaging Biomarkers of Brain Disorders, Institute of Psychiatry and Neurosciences of Paris, Paris, France.

Jacques Grill (J)

Inserm Unit 981, Biomarkers and New Therapeutic Targets in Oncology Team, Genomics and Oncogenesis of Brain Tumors, Paris-Sud University, Paris-Saclay University, Villejuif, France.
Department of Pediatric Oncology, Gustave-Roussy University Hospital, Paris-Sud University, Paris-Saclay University, Villejuif, France.

Franck Bourdeaut (F)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.
SIREDO Oncology Center (Care, Innovation and Research for Children and AYA with Cancer), Institut Curie, Paris, France.

François Doz (F)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.
SIREDO Oncology Center (Care, Innovation and Research for Children and AYA with Cancer), Institut Curie, Paris, France.

Frédéric Dhermain (F)

Department of Radiotherapy, Gustave Roussy University Hospital, Villejuif, France.

Karima Mokhtari (K)

Department of Neuroradiology, Necker Enfants-Malades Hospital, Paris, France.
Department of Neuropathology, Pitié-Salpêtrière Hospital, Paris, France.

Fabrice Chretien (F)

Department of Neurosurgery, University Hospital Group (GHU) Paris-Sainte-Anne Hospital, Paris, France.

Dominique Figarella-Branger (D)

Department of Pathology and Neuropathology, Timone Hospital, Marseille, France.

Pascale Varlet (P)

Paris Descartes University, Sorbonne Paris Cité, Paris, France.
Inserm Unit 1266, Imaging Biomarkers of Brain Disorders, Institute of Psychiatry and Neurosciences of Paris, Paris, France.

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