Gliomatosis cerebri in children: A poor prognostic phenotype of diffuse gliomas with a distinct molecular profile


Por: Nussbaumer G, Benesch M, Grabovska Y, Mackay A, Castel D, Grill J, Alonso MM, Antonelli M, Bailey S, Baugh JN, Biassoni V, Blattner Johnson M, Broniscer A, Carai A, Colafati GS, Colditz N, Corbacioglu S, Crampsie S, Entz-Werle N, Eyrich M, Friker LL, Frühwald MC, Garrè ML, Gerber NU, Giangaspero F, Gil-da-Costa MJ, Graf N, Hargrave D, Hauser P, Herrlinger U, Hoffmann M, Hulleman E, Izquierdo E, Jacobs S, Karremann M, Kattamis A, Kebudi R, Kortmann RD, Kwiecien R, Massimino M, Mastronuzzi A, Miele E, Morana G, Noack CM, Pentikainen V, Perwein T, Pfister SM, Pietsch T, Roka K, Rossi S, Rutkowski S, Schiavello E, Seidel C, Šterba J, Sturm D, Sumerauer D, Tacke A, Temelso S, Valentini C, van Vuurden D, Varlet P, Veldhuijzen van Zanten SEM, Vinci M, von Bueren AO, Warmuth-Metz M, Wesseling P, Wiese M, Wolff JEA, Zamecnik J, Morales-La Madrid A, Bison B, Gielen GH, Jones DTW, Jones C and Kramm CM

Publicada: 1 sep 2024 Ahead of Print: 8 may 2024
Resumen:
Background. The term gliomatosis cerebri (GC), a radiology-defined highly infiltrating diffuse glioma, has been abandoned since molecular GC-associated features could not be established. Methods. We conducted a multinational retrospective study of 104 children and adolescents with GC providing comprehensive clinical and (epi-)genetic characterization. Results. Median overall survival (OS) was 15.5 months (interquartile range, 10.9-27.7) with a 2-year survival rate of 28%. Histopathological grading correlated significantly with median OS: CNS WHO grade II: 47.8 months (25.2-55.7); grade III: 15.9 months (11.4-26.3); grade IV: 10.4 months (8.8-14.4). By DNA methylation profiling (n = 49), most tumors were classified as pediatric-type diffuse high-grade glioma (pedHGG), H3-/IDH-wild-type (n = 31/49, 63.3%) with enriched subclasses pedHGG_RTK2 (n = 19), pedHGG_A/B (n = 6), and pedHGG_MYCN (n = 5), but only one pedHGG_RTK1 case. Within the pedHGG, H3-/IDH-wild-type subgroup, recurrent alterations in EGFR (n = 10) and BCOR (n = 9) were identified. Additionally, we observed structural aberrations in chromosome 6 in 16/49 tumors (32.7%) across tumor types. In the pedHGG, H3-/IDH-wild-type subgroup TP53 alterations had a significant negative effect on OS. Conclusions. Contrary to previous studies, our representative pediatric GC study provides evidence that GC has a strong predilection to arise on the background of specific molecular features (especially pedHGG_RTK2, pedHGG_A/B, EGFR and BCOR mutations, chromosome 6 rearrangements). Key Points The presence of gliomatosis cerebri (GC) phenotype may be considered as an independent dismal prognostic factor in hemispheric pediatric-type diffuse gliomas. The methylome-based subtypes pediatric-type diffuse high-grade glioma (pedHGG)_RTK2A/B and (provisional) pedHGG_A/B were significantly associated with GC. EGFR and BCOR alterations and rearrangements of chromosome 6 were the most common genetic features in pediatric GC.

Filiaciones:
Nussbaumer G:
 Division of Pediatric Hematology and Oncology, Department of Pediatrics and Adolescent Medicine, Medical University of Graz, Graz, Austria

Benesch M:
 Division of Pediatric Hematology and Oncology, Department of Pediatrics and Adolescent Medicine, Medical University of Graz, Graz, Austria

Grabovska Y:
 Division of Molecular Pathology, Institute of Cancer Research, London, UK

Mackay A:
 Division of Molecular Pathology, Institute of Cancer Research, London, UK

Castel D:
 Department of Pediatric and Adolescent Oncology, Gustave Roussy, Université Paris-Saclay, Villejuif, France

 U981, Molecular Predictors and New Targets in Oncology, Team Genomics and Oncogenesis of Pediatric Brain Tumors, INSERM, Gustave Roussy, Université Paris-Saclay, Villejuif, France

Grill J:
 Department of Pediatric and Adolescent Oncology, Gustave Roussy, Université Paris-Saclay, Villejuif, France

 U981, Molecular Predictors and New Targets in Oncology, Team Genomics and Oncogenesis of Pediatric Brain Tumors, INSERM, Gustave Roussy, Université Paris-Saclay, Villejuif, France

Alonso MM:
 Health Research Institute of Navarra (IdiSNA), Pamplona, Navarra, Spain

 Solid Tumor Program, Center for the Applied Medical Research, Pamplona, Navarra, Spain

 Department of Pediatrics, Clínica Universidad de Navarra, Pamplona, Spain

Antonelli M:
 Department of Radiological, Oncological and Anatomo-Pathological Sciences, Sapienza University, Rome, Italy

Bailey S:
 Department of Paediatric Oncology, Sir James Spence Institute of Child Health, Royal Victoria Infirmary Queen Victoria Road, Newcastle upon Tyne, UK

Baugh JN:
 Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands

Biassoni V:
 Pediatric Oncology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy

Blattner Johnson M:
 Hopp Children's Cancer Center (KiTZ), Heidelberg, Germany

 Division of Pediatric Glioma Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany

Broniscer A:
 Division of Hematology-Oncology, Children's Hospital of Pittsburgh, Pittsburgh, PA, USA

Carai A:
 Neurosurgery Unit, Bambino Gesù Children's Hospital (IRCCS), Rome, Italy

Colafati GS:
 Oncological Neuroradiology and Advanced Diagnostics Unit, Bambino Gesù Children's Hospital (IRCCS), Rome, Italy

Colditz N:
 Division of Pediatric Hematology and Oncology, University Medical Center Göttingen, Göttingen, Germany

Corbacioglu S:
 Department of Pediatric Hematology, Oncology and Stem Cell Transplantation, University of Regensburg, Regensburg, Germany

Crampsie S:
 Division of Molecular Pathology, Institute of Cancer Research, London, UK

Entz-Werle N:
 Pediatric Onco-Hematology Department - Pediatrics III, University Hospital of Strasbourg, Strasbourg, France

 UMR CNRS 7021 - Laboratory of Bioimagery and Pathologies Team tumor signaling and therapeutic targets, University of Strasbourg, Illkirch, France

Eyrich M:
 Pediatric Hematology and Oncology, Department of Pediatrics, University Hospital Würzburg, Würzburg, Germany

Friker LL:
 Institute of Neuropathology, DGNN Brain Tumor Reference Center, University of Bonn Medical Center, Bonn, Germany

Frühwald MC:
 Pediatric and Adolescent Medicine, Swabian Children's Cancer Center, University Medical Center Augsburg, Augsburg, Germany

Garrè ML:
 Neuro-Oncology Unit, IRCSS Istituto Giannina Gaslini, Genoa, Italy

Gerber NU:
 Department of Oncology and Children's Research Centre, University Children's Hospital, Zurich, Switzerland

Giangaspero F:
 Department of Radiological, Oncological and Anatomo-Pathological Sciences, Sapienza University, Rome, Italy

Gil-da-Costa MJ:
 Pediatric Oncology Department, University Hospital São João, Porto, Portugal

Graf N:
 Department of Pediatric Oncology and Hematology, Saarland University, Homburg, Germany

Hargrave D:
 Pediatric Oncology, Great Ormond Street Hospital for Children, London, UK

Hauser P:
 Second Department of Pediatrics, Semmelweis University, Budapest, Hungary

Herrlinger U:
 Division of Clinical Neuro-Oncology, Department of Neurology, University Hospital Bonn, Bonn, Germany

Hoffmann M:
 Division of Pediatric Hematology and Oncology, University Medical Center Göttingen, Göttingen, Germany

Hulleman E:
 Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands

Izquierdo E:
 Division of Molecular Pathology, Institute of Cancer Research, London, UK

Jacobs S:
 Department of Pediatric Hematology and Oncology, University Hospitals Leuven, Belgium and Pediatric Oncology, Department of Oncology, KU Leuven, Belgium

Karremann M:
 Department of Pediatric and Adolescent Medicine, University Medical Center Mannheim, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany

Kattamis A:
 Division of Pediatric Hematology-Oncology, First Department of Pediatrics, National and Kapodistrian University of Athens, "Aghia Sophia" Children's Hospital, Athens, Greece

Kebudi R:
 Division of Pediatric Hematology-Oncology, Institute of Oncology, Istanbul University, Istanbul, Turkey

Kortmann RD:
 Department of Radiation Oncology, University of Leipzig, Leipzig, Germany

Kwiecien R:
 Institute of Biostatistics and Clinical Research, University of Münster, Münster, Germany

Massimino M:
 Pediatric Oncology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy

Mastronuzzi A:
 Department of Onco-Hematology, Gene and Cell Therapy, Bambino Gesù Children's Hospital (IRCCS), Rome, Italy

Miele E:
 Department of Onco-Hematology, Gene and Cell Therapy, Bambino Gesù Children's Hospital (IRCCS), Rome, Italy

Morana G:
 Department of Neurosciences, University of Turin, Turin, Italy

Noack CM:
 Center of Radiology, Department of Diagnostic and Interventional Radiology and Neuroradiology, Hospital of Fulda, Fulda, Germany

Pentikainen V:
 Division of Hematology-Oncology and Stem Cell Transplantation, Children's Hospital, Helsinki University Hospital, Helsinki, Finland

Perwein T:
 Division of Pediatric Hematology and Oncology, Department of Pediatrics and Adolescent Medicine, Medical University of Graz, Graz, Austria

Pfister SM:
 Hopp Children's Cancer Center (KiTZ), Heidelberg, Germany

 Division of Pediatric Neurooncology, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany

 Department of Pediatric Oncology, Hematology & Immunology, Heidelberg University Hospital, Heidelberg, Germany

 National Center for Tumor Diseases (NCT) Heidelberg, Heidelberg, Germany

Pietsch T:
 Institute of Neuropathology, DGNN Brain Tumor Reference Center, University of Bonn Medical Center, Bonn, Germany

Roka K:
 Division of Pediatric Hematology-Oncology, First Department of Pediatrics, National and Kapodistrian University of Athens, "Aghia Sophia" Children's Hospital, Athens, Greece

Rossi S:
 Pathology Unit, Bambino Gesù Children's Hospital (IRCCS), Rome, Italy

Rutkowski S:
 Department of Pediatric Hematology and Oncology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

Schiavello E:
 Pediatric Oncology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy

Seidel C:
 Department of Radiation Oncology, University of Leipzig, Leipzig, Germany

Šterba J:
 Department of Pediatric Oncology, University Hospital Brno and Faculty of Medicine, Masaryk University, Brno, Czech Republic

Sturm D:
 Hopp Children's Cancer Center (KiTZ), Heidelberg, Germany

 Division of Pediatric Glioma Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany

 Department of Pediatric Oncology, Hematology & Immunology, Heidelberg University Hospital, Heidelberg, Germany

Sumerauer D:
 Department of Pediatric Hematology and Oncology, 2nd Faculty of Medicine, Charles University in Prague and University Hospital Motol, Prague, Czech Republic

Tacke A:
 Division of Pediatric Hematology and Oncology, University Medical Center Göttingen, Göttingen, Germany

Temelso S:
 Division of Molecular Pathology, Institute of Cancer Research, London, UK

Valentini C:
 Department of Radiotherapy and Radiation Oncology, Faculty of Medicine and University Hospital Carl Gustav Carus, Technical University Dresden, Dresden, Germany

van Vuurden D:
 Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands

Varlet P:
 GHU-Paris Psychiatry and Neuroscience, Sainte-Anne Hospital, Department of Neuropathology, Paris, France

Veldhuijzen van Zanten SEM:
 Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands

 Department of Radiology and Nuclear Medicine, Erasmus MC, Rotterdam, The Netherlands

Vinci M:
 Department of Onco-Hematology, Gene and Cell Therapy, Bambino Gesù Children's Hospital (IRCCS), Rome, Italy

von Bueren AO:
 Department of Pediatrics, Obstetrics and Gynecology, Division of Pediatric Hematology and Oncology, University Hospital Geneva, Geneva, Switzerland

Warmuth-Metz M:
 Institute of Diagnostic and Interventional Neuroradiology, University of Würzburg, Würzburg, Germany

Wesseling P:
 Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands

 Department of Pathology, Amsterdam UMC, Amsterdam, The Netherlands

Wiese M:
 Neurosurgery Unit, Bambino Gesù Children's Hospital (IRCCS), Rome, Italy

Wolff JEA:
 AbbVie Inc, Oncology Development, North Chicago, IL, USA

Zamecnik J:
 Department of Pathology and Molecular Medicine, 2nd Faculty of Medicine, Charles University in Prague and University Hospital Motol, Prague, Czech Republic

Morales-La Madrid A:
 Pediatric Neuro-Oncology, Pediatric Cancer Center Barcelona, Hospital Sant Joan de Deu, Barcelona, Spain

Bison B:
 Diagnostic and Interventional Neuroradiology, Faculty of Medicine, University of Augsburg, Augsburg, Germany

 Neuroradiological Reference Center for the pediatric brain tumor (HIT) studies of the German Society of Pediatric Oncology and Hematology, University Augsburg, Faculty of Medicine, Germany

Gielen GH:
 Institute of Neuropathology, DGNN Brain Tumor Reference Center, University of Bonn Medical Center, Bonn, Germany

Jones DTW:
 Hopp Children's Cancer Center (KiTZ), Heidelberg, Germany

 Division of Pediatric Glioma Research, German Cancer Research Center (DKFZ) and German Cancer Consortium (DKTK), Heidelberg, Germany

Jones C:
 Division of Molecular Pathology, Institute of Cancer Research, London, UK

Kramm CM:
 Division of Pediatric Hematology and Oncology, University Medical Center Göttingen, Göttingen, Germany
ISSN: 15228517





NEURO-ONCOLOGY
Editorial
OXFORD UNIV PRESS INC, JOURNALS DEPT, 2001 EVANS RD, CARY, NC 27513, Estados Unidos America
Tipo de documento: Article
Volumen: 26 Número: 9
Páginas: 1723-1737
WOS Id: 001458375800001
ID de PubMed: 38717379
imagen Green Submitted, Green Published, hybrid

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