Anaplastic ganglioglioma—A diagnosis comprising several distinct tumour types

Annekathrin Reinhardt; Kristin Pfister; Daniel Schrimpf; Damian Stichel; Felix Sahm; David E. Reuss; David Capper; Annika K. Wefers; Azadeh Ebrahimi; Martin Sill; Joerg Felsberg; Guido Reifenberger; Albert Becker; Marco Prinz; Ori Staszewski; Christian Hartmann; Jens Schittenhelm; Dorothee Gramatzki; Michael Weller; Adriana Olar; Elisabeth Jane Rushing; Markus Bergmann; Michael A. Farrell; Ingmar Blümcke; Roland Coras; Jan Beckervordersandforth; Se Hoon Kim; Fabio Rogerio; Petia S. Dimova; Pitt Niehusmann; Andreas Unterberg; Michael Platten; Stefan M. Pfister; Wolfgang Wick; Christel Herold-Mende; Andreas von Deimling

doi:10.1111/nan.12847

Anaplastic ganglioglioma—A diagnosis comprising several distinct tumour types

Annekathrin Reinhardt, Kristin Pfister, Daniel Schrimpf, Damian Stichel, Felix Sahm, David E. Reuss, David Capper, Annika K. Wefers, Azadeh Ebrahimi, Martin Sill, Joerg Felsberg, Guido Reifenberger, Albert Becker, Marco Prinz, Ori Staszewski, Christian Hartmann, Jens Schittenhelm, Dorothee Gramatzki, Michael Weller, Adriana OlarElisabeth Jane Rushing, Markus Bergmann, Michael A. Farrell, Ingmar Blümcke, Roland Coras, Jan Beckervordersandforth, Se Hoon Kim, Fabio Rogerio, Petia S. Dimova, Pitt Niehusmann, Andreas Unterberg, Michael Platten, Stefan M. Pfister, Wolfgang Wick, Christel Herold-Mende, Andreas von Deimling

Department of Pathology

Research output: Contribution to journal › Article › peer-review

1 Citation (Scopus)

Abstract

Aims: Anaplastic ganglioglioma is a rare tumour, and diagnosis has been based on histological criteria. The 5th edition of the World Health Organization Classification of Tumours of the Central Nervous System (CNS WHO) does not list anaplastic ganglioglioma as a distinct diagnosis due to lack of molecular data in previous publications. We retrospectively compiled a cohort of 54 histologically diagnosed anaplastic gangliogliomas to explore whether the molecular profiles of these tumours represent a separate type or resolve into other entities. Methods: Samples were subjected to histological review, desoxyribonucleic acid (DNA) methylation profiling and next-generation sequencing. Morphological and molecular data were summarised to an integrated diagnosis. Results: The majority of tumours designated as anaplastic gangliogliomas resolved into other CNS WHO diagnoses, most commonly pleomorphic xanthoastrocytoma (16/54), glioblastoma, isocitrate dehydrogenase protein (IDH) wild type and diffuse paediatric-type high-grade glioma, H3 wild type and IDH wild type (11 and 2/54), followed by low-grade glial or glioneuronal tumours including pilocytic astrocytoma, dysembryoplastic neuroepithelial tumour and diffuse leptomeningeal glioneuronal tumour (5/54), IDH mutant astrocytoma (4/54) and others (6/54). A subset of tumours (10/54) was not assignable to a CNS WHO diagnosis, and common molecular profiles pointing to a separate entity were not evident. Conclusions: In summary, we show that tumours histologically diagnosed as anaplastic ganglioglioma comprise a wide spectrum of CNS WHO tumour types with different prognostic and therapeutic implications. We therefore suggest assigning this designation with caution and recommend comprehensive molecular workup.

Original language	English
Article number	e12847
Journal	Neuropathology and Applied Neurobiology
Volume	48
Issue number	7
DOIs	https://doi.org/10.1111/nan.12847
Publication status	Published - 2022 Dec

Bibliographical note

Funding Information:
We thank the Genomics and Proteomics Core Facility of the German Cancer Research Center (DKFZ) for conducting the methylation analyses for a part of the aGG series. We thank the DKFZ Heidelberg Center for Personalized Oncology (DKFZ-HIPO) for technical support and funding through HIPO_036. In parts, this work was supported by an Illumina Medical Research Grant and the German Cancer Consortium (DKTK) joint funding project ‘Next Generation Molecular Diagnostics of Malignant Gliomas’. A. R. was funded by the Else Kröner Research College in the framework of her participation in the Research College of Neurooncology, University Hospital Heidelberg. Open Access funding enabled and organized by Projekt DEAL.

Funding Information:
We thank the Genomics and Proteomics Core Facility of the German Cancer Research Center (DKFZ) for conducting the methylation analyses for a part of the aGG series. We thank the DKFZ Heidelberg Center for Personalized Oncology (DKFZ‐HIPO) for technical support and funding through HIPO_036. In parts, this work was supported by an Illumina Medical Research Grant and the German Cancer Consortium (DKTK) joint funding project ‘Next Generation Molecular Diagnostics of Malignant Gliomas’. A. R. was funded by the Else Kröner Research College in the framework of her participation in the Research College of Neurooncology, University Hospital Heidelberg. Open Access funding enabled and organized by Projekt DEAL.

Publisher Copyright:
© 2022 The Authors. Neuropathology and Applied Neurobiology published by John Wiley & Sons Ltd on behalf of British Neuropathological Society.

All Science Journal Classification (ASJC) codes

Pathology and Forensic Medicine
Histology
Neurology
Clinical Neurology
Physiology (medical)

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10.1111/nan.12847

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Reinhardt, A., Pfister, K., Schrimpf, D., Stichel, D., Sahm, F., Reuss, D. E., Capper, D., Wefers, A. K., Ebrahimi, A., Sill, M., Felsberg, J., Reifenberger, G., Becker, A., Prinz, M., Staszewski, O., Hartmann, C., Schittenhelm, J., Gramatzki, D., Weller, M., ... von Deimling, A. (2022). Anaplastic ganglioglioma—A diagnosis comprising several distinct tumour types. Neuropathology and Applied Neurobiology, 48(7), [e12847]. https://doi.org/10.1111/nan.12847

@article{24673c0287d34d889823c6e6d506da50,

title = "Anaplastic ganglioglioma—A diagnosis comprising several distinct tumour types",

abstract = "Aims: Anaplastic ganglioglioma is a rare tumour, and diagnosis has been based on histological criteria. The 5th edition of the World Health Organization Classification of Tumours of the Central Nervous System (CNS WHO) does not list anaplastic ganglioglioma as a distinct diagnosis due to lack of molecular data in previous publications. We retrospectively compiled a cohort of 54 histologically diagnosed anaplastic gangliogliomas to explore whether the molecular profiles of these tumours represent a separate type or resolve into other entities. Methods: Samples were subjected to histological review, desoxyribonucleic acid (DNA) methylation profiling and next-generation sequencing. Morphological and molecular data were summarised to an integrated diagnosis. Results: The majority of tumours designated as anaplastic gangliogliomas resolved into other CNS WHO diagnoses, most commonly pleomorphic xanthoastrocytoma (16/54), glioblastoma, isocitrate dehydrogenase protein (IDH) wild type and diffuse paediatric-type high-grade glioma, H3 wild type and IDH wild type (11 and 2/54), followed by low-grade glial or glioneuronal tumours including pilocytic astrocytoma, dysembryoplastic neuroepithelial tumour and diffuse leptomeningeal glioneuronal tumour (5/54), IDH mutant astrocytoma (4/54) and others (6/54). A subset of tumours (10/54) was not assignable to a CNS WHO diagnosis, and common molecular profiles pointing to a separate entity were not evident. Conclusions: In summary, we show that tumours histologically diagnosed as anaplastic ganglioglioma comprise a wide spectrum of CNS WHO tumour types with different prognostic and therapeutic implications. We therefore suggest assigning this designation with caution and recommend comprehensive molecular workup.",

author = "Annekathrin Reinhardt and Kristin Pfister and Daniel Schrimpf and Damian Stichel and Felix Sahm and Reuss, {David E.} and David Capper and Wefers, {Annika K.} and Azadeh Ebrahimi and Martin Sill and Joerg Felsberg and Guido Reifenberger and Albert Becker and Marco Prinz and Ori Staszewski and Christian Hartmann and Jens Schittenhelm and Dorothee Gramatzki and Michael Weller and Adriana Olar and Rushing, {Elisabeth Jane} and Markus Bergmann and Farrell, {Michael A.} and Ingmar Bl{\"u}mcke and Roland Coras and Jan Beckervordersandforth and Kim, {Se Hoon} and Fabio Rogerio and Dimova, {Petia S.} and Pitt Niehusmann and Andreas Unterberg and Michael Platten and Pfister, {Stefan M.} and Wolfgang Wick and Christel Herold-Mende and {von Deimling}, Andreas",

note = "Funding Information: We thank the Genomics and Proteomics Core Facility of the German Cancer Research Center (DKFZ) for conducting the methylation analyses for a part of the aGG series. We thank the DKFZ Heidelberg Center for Personalized Oncology (DKFZ-HIPO) for technical support and funding through HIPO_036. In parts, this work was supported by an Illumina Medical Research Grant and the German Cancer Consortium (DKTK) joint funding project {\textquoteleft}Next Generation Molecular Diagnostics of Malignant Gliomas{\textquoteright}. A. R. was funded by the Else Kr{\"o}ner Research College in the framework of her participation in the Research College of Neurooncology, University Hospital Heidelberg. Open Access funding enabled and organized by Projekt DEAL. Funding Information: We thank the Genomics and Proteomics Core Facility of the German Cancer Research Center (DKFZ) for conducting the methylation analyses for a part of the aGG series. We thank the DKFZ Heidelberg Center for Personalized Oncology (DKFZ‐HIPO) for technical support and funding through HIPO_036. In parts, this work was supported by an Illumina Medical Research Grant and the German Cancer Consortium (DKTK) joint funding project {\textquoteleft}Next Generation Molecular Diagnostics of Malignant Gliomas{\textquoteright}. A. R. was funded by the Else Kr{\"o}ner Research College in the framework of her participation in the Research College of Neurooncology, University Hospital Heidelberg. Open Access funding enabled and organized by Projekt DEAL. Publisher Copyright: {\textcopyright} 2022 The Authors. Neuropathology and Applied Neurobiology published by John Wiley & Sons Ltd on behalf of British Neuropathological Society.",

year = "2022",

month = dec,

doi = "10.1111/nan.12847",

language = "English",

volume = "48",

journal = "Neuropathology and Applied Neurobiology",

issn = "0305-1846",

publisher = "Wiley-Blackwell",

number = "7",

}

Reinhardt, A, Pfister, K, Schrimpf, D, Stichel, D, Sahm, F, Reuss, DE, Capper, D, Wefers, AK, Ebrahimi, A, Sill, M, Felsberg, J, Reifenberger, G, Becker, A, Prinz, M, Staszewski, O, Hartmann, C, Schittenhelm, J, Gramatzki, D, Weller, M, Olar, A, Rushing, EJ, Bergmann, M, Farrell, MA, Blümcke, I, Coras, R, Beckervordersandforth, J, Kim, SH, Rogerio, F, Dimova, PS, Niehusmann, P, Unterberg, A, Platten, M, Pfister, SM, Wick, W, Herold-Mende, C & von Deimling, A 2022, 'Anaplastic ganglioglioma—A diagnosis comprising several distinct tumour types', Neuropathology and Applied Neurobiology, vol. 48, no. 7, e12847. https://doi.org/10.1111/nan.12847

TY - JOUR

T1 - Anaplastic ganglioglioma—A diagnosis comprising several distinct tumour types

AU - Reinhardt, Annekathrin

AU - Pfister, Kristin

AU - Schrimpf, Daniel

AU - Stichel, Damian

AU - Sahm, Felix

AU - Reuss, David E.

AU - Capper, David

AU - Wefers, Annika K.

AU - Ebrahimi, Azadeh

AU - Sill, Martin

AU - Felsberg, Joerg

AU - Reifenberger, Guido

AU - Becker, Albert

AU - Prinz, Marco

AU - Staszewski, Ori

AU - Hartmann, Christian

AU - Schittenhelm, Jens

AU - Gramatzki, Dorothee

AU - Weller, Michael

AU - Olar, Adriana

AU - Rushing, Elisabeth Jane

AU - Bergmann, Markus

AU - Farrell, Michael A.

AU - Blümcke, Ingmar

AU - Coras, Roland

AU - Beckervordersandforth, Jan

AU - Kim, Se Hoon

AU - Rogerio, Fabio

AU - Dimova, Petia S.

AU - Niehusmann, Pitt

AU - Unterberg, Andreas

AU - Platten, Michael

AU - Pfister, Stefan M.

AU - Wick, Wolfgang

AU - Herold-Mende, Christel

AU - von Deimling, Andreas

N1 - Funding Information: We thank the Genomics and Proteomics Core Facility of the German Cancer Research Center (DKFZ) for conducting the methylation analyses for a part of the aGG series. We thank the DKFZ Heidelberg Center for Personalized Oncology (DKFZ-HIPO) for technical support and funding through HIPO_036. In parts, this work was supported by an Illumina Medical Research Grant and the German Cancer Consortium (DKTK) joint funding project ‘Next Generation Molecular Diagnostics of Malignant Gliomas’. A. R. was funded by the Else Kröner Research College in the framework of her participation in the Research College of Neurooncology, University Hospital Heidelberg. Open Access funding enabled and organized by Projekt DEAL. Funding Information: We thank the Genomics and Proteomics Core Facility of the German Cancer Research Center (DKFZ) for conducting the methylation analyses for a part of the aGG series. We thank the DKFZ Heidelberg Center for Personalized Oncology (DKFZ‐HIPO) for technical support and funding through HIPO_036. In parts, this work was supported by an Illumina Medical Research Grant and the German Cancer Consortium (DKTK) joint funding project ‘Next Generation Molecular Diagnostics of Malignant Gliomas’. A. R. was funded by the Else Kröner Research College in the framework of her participation in the Research College of Neurooncology, University Hospital Heidelberg. Open Access funding enabled and organized by Projekt DEAL. Publisher Copyright: © 2022 The Authors. Neuropathology and Applied Neurobiology published by John Wiley & Sons Ltd on behalf of British Neuropathological Society.

PY - 2022/12

Y1 - 2022/12

N2 - Aims: Anaplastic ganglioglioma is a rare tumour, and diagnosis has been based on histological criteria. The 5th edition of the World Health Organization Classification of Tumours of the Central Nervous System (CNS WHO) does not list anaplastic ganglioglioma as a distinct diagnosis due to lack of molecular data in previous publications. We retrospectively compiled a cohort of 54 histologically diagnosed anaplastic gangliogliomas to explore whether the molecular profiles of these tumours represent a separate type or resolve into other entities. Methods: Samples were subjected to histological review, desoxyribonucleic acid (DNA) methylation profiling and next-generation sequencing. Morphological and molecular data were summarised to an integrated diagnosis. Results: The majority of tumours designated as anaplastic gangliogliomas resolved into other CNS WHO diagnoses, most commonly pleomorphic xanthoastrocytoma (16/54), glioblastoma, isocitrate dehydrogenase protein (IDH) wild type and diffuse paediatric-type high-grade glioma, H3 wild type and IDH wild type (11 and 2/54), followed by low-grade glial or glioneuronal tumours including pilocytic astrocytoma, dysembryoplastic neuroepithelial tumour and diffuse leptomeningeal glioneuronal tumour (5/54), IDH mutant astrocytoma (4/54) and others (6/54). A subset of tumours (10/54) was not assignable to a CNS WHO diagnosis, and common molecular profiles pointing to a separate entity were not evident. Conclusions: In summary, we show that tumours histologically diagnosed as anaplastic ganglioglioma comprise a wide spectrum of CNS WHO tumour types with different prognostic and therapeutic implications. We therefore suggest assigning this designation with caution and recommend comprehensive molecular workup.

AB - Aims: Anaplastic ganglioglioma is a rare tumour, and diagnosis has been based on histological criteria. The 5th edition of the World Health Organization Classification of Tumours of the Central Nervous System (CNS WHO) does not list anaplastic ganglioglioma as a distinct diagnosis due to lack of molecular data in previous publications. We retrospectively compiled a cohort of 54 histologically diagnosed anaplastic gangliogliomas to explore whether the molecular profiles of these tumours represent a separate type or resolve into other entities. Methods: Samples were subjected to histological review, desoxyribonucleic acid (DNA) methylation profiling and next-generation sequencing. Morphological and molecular data were summarised to an integrated diagnosis. Results: The majority of tumours designated as anaplastic gangliogliomas resolved into other CNS WHO diagnoses, most commonly pleomorphic xanthoastrocytoma (16/54), glioblastoma, isocitrate dehydrogenase protein (IDH) wild type and diffuse paediatric-type high-grade glioma, H3 wild type and IDH wild type (11 and 2/54), followed by low-grade glial or glioneuronal tumours including pilocytic astrocytoma, dysembryoplastic neuroepithelial tumour and diffuse leptomeningeal glioneuronal tumour (5/54), IDH mutant astrocytoma (4/54) and others (6/54). A subset of tumours (10/54) was not assignable to a CNS WHO diagnosis, and common molecular profiles pointing to a separate entity were not evident. Conclusions: In summary, we show that tumours histologically diagnosed as anaplastic ganglioglioma comprise a wide spectrum of CNS WHO tumour types with different prognostic and therapeutic implications. We therefore suggest assigning this designation with caution and recommend comprehensive molecular workup.

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U2 - 10.1111/nan.12847

DO - 10.1111/nan.12847

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JO - Neuropathology and Applied Neurobiology

JF - Neuropathology and Applied Neurobiology

IS - 7

M1 - e12847

ER -

Anaplastic ganglioglioma—A diagnosis comprising several distinct tumour types

Abstract

Bibliographical note

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