Paediatric low-grade glioma: the role of classical pathology in integrated diagnostic practice.

Glioma MAP kinase Nervous system neoplasms Neuropathology

Journal

Child's nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery
ISSN: 1433-0350
Titre abrégé: Childs Nerv Syst
Pays: Germany
ID NLM: 8503227

Informations de publication

Date de publication:
18 Sep 2024
Historique:
received: 29 05 2024
accepted: 23 08 2024
medline: 19 9 2024
pubmed: 19 9 2024
entrez: 18 9 2024
Statut: aheadofprint

Résumé

Low-grade gliomas are a cause of severe and often life-long disability in children. Pathology plays a key role in their management by establishing the diagnosis, excluding malignant alternatives, predicting outcomes and identifying targetable genetic alterations. Molecular diagnosis has reshaped the terrain of pathology, raising the question of what part traditional histology plays. In this review, we consider the classification and pathological diagnosis of low-grade gliomas and glioneuronal tumours in children by traditional histopathology enhanced by the opportunities afforded by access to comprehensive genetic and epigenetic characterisation.

Identifiants

pubmed: 39294363
doi: 10.1007/s00381-024-06591-6
pii: 10.1007/s00381-024-06591-6
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Brain Tumour Charity
ID : GN-000707
Organisme : Brain Tumour Charity
ID : GN-000707

Informations de copyright

© 2024. The Author(s).

Références

Morin A, Allodji R, Kariyawasam D, et al (2024) Very long-term outcomes of pediatric patients treated for optic pathway gliomas: a longitudinal cohort study. Neuro-Oncol noae045. https://doi.org/10.1093/neuonc/noae045
Fangusaro J, Jones DT, Packer RJ et al (2023) Pediatric low-grade glioma: state-of-the-art and ongoing challenges. Neuro-Oncol 26:25–37. https://doi.org/10.1093/neuonc/noad195
doi: 10.1093/neuonc/noad195
Mueller S, Fangusaro J, Thomas AO, et al (2023) Consensus framework for conducting phase I/II clinical trials for children, adolescents, and young adults with pediatric low-grade glioma: guidelines established by the International Pediatric Low-Grade Glioma Coalition Clinical Trial Working Group. Neuro-Oncol noad227. https://doi.org/10.1093/neuonc/noad227
Ryall S, Zapotocky M, Fukuoka K, et al (2020) Integrated molecular and clinical analysis of 1,000 pediatric low-grade gliomas. 37:569-583.e5. https://doi.org/10.1016/j.ccell.2020.03.011
Sturm D, Capper D, Andreiuolo F, et al (2023) Multiomic neuropathology improves diagnostic accuracy in pediatric neuro-oncology. Nat Med 1–10. https://doi.org/10.1038/s41591-023-02255-1
Pickles JC, Fairchild AR, Stone TJ et al (2020) DNA methylation-based profiling for paediatric CNS tumour diagnosis and treatment: a population-based study. Lancet Child Adolesc Heal 4:121–130. https://doi.org/10.1016/s2352-4642(19)30342-6
doi: 10.1016/s2352-4642(19)30342-6
Capper D, Jones DTW, Sill M et al (2018) DNA methylation-based classification of central nervous system tumours. Nature 555:469–474. https://doi.org/10.1038/nature26000
doi: 10.1038/nature26000 pubmed: 29539639 pmcid: 6093218
Moreira DC, Bouffet E, Qaddoumi I (2024) The greatest challenge for pediatric low-grade glioma. Neuro-Oncol 26:975–976. https://doi.org/10.1093/neuonc/noae004
doi: 10.1093/neuonc/noae004 pubmed: 38339843 pmcid: 11066925
Bailey S, Davidson A, Parkes J et al (2022) How can genomic innovations in pediatric brain tumors transform outcomes in low- and middle-income countries? JCO Glob Oncol 8:e2200156. https://doi.org/10.1200/go.22.00156
doi: 10.1200/go.22.00156 pubmed: 36252166 pmcid: 9812475
Buckland ME, Sarkar C, Santosh V, et al (2023) Announcing the Asian Oceanian Society of Neuropathology guidelines for Adapting Diagnostic Approaches for Practical Taxonomy in Resource‐Restrained Regions (AOSNP‐ADAPTR). Brain Pathol e13201. https://doi.org/10.1111/bpa.13201
Stone TJ, Rowell R, Jayasekera BAP et al (2018) Review: Molecular characteristics of long-term epilepsy-associated tumours (LEATs) and mechanisms for tumour-related epilepsy (TRE). Neuropathol Appl Neurobiol 44:56–69. https://doi.org/10.1111/nan.12459
doi: 10.1111/nan.12459 pubmed: 29315734
Stone TJ, Keeley A, Virasami A et al (2018) Comprehensive molecular characterisation of epilepsy-associated glioneuronal tumours. Acta Neuropathol 135:115–129. https://doi.org/10.1007/s00401-017-1773-z
doi: 10.1007/s00401-017-1773-z pubmed: 29058119
Stone TJ, Mankad K, Tan AP et al (2023) DNA methylation-based classification of glioneuronal tumours synergises with histology and radiology to refine accurate molecular stratification. Neuropathol Appl Neurobiol 49:e12894. https://doi.org/10.1111/nan.12894
doi: 10.1111/nan.12894 pubmed: 36843390 pmcid: 10946721
Blümcke I, Coras R, Wefers AK et al (2019) Review: Challenges in the histopathological classification of ganglioglioma and DNT: microscopic agreement studies and a preliminary genotype-phenotype analysis. Neuropath Appl Neuro 45:95–107. https://doi.org/10.1111/nan.12522
doi: 10.1111/nan.12522
Capper D, Stichel D, Sahm F et al (2018) Practical implementation of DNA methylation and copy-number-based CNS tumor diagnostics: the Heidelberg experience. Acta Neuropathol 136:181–210. https://doi.org/10.1007/s00401-018-1879-y
doi: 10.1007/s00401-018-1879-y pubmed: 29967940 pmcid: 6060790
Jones DTW, Hutter B, Jäger N et al (2013) Recurrent somatic alterations of FGFR1 and NTRK2 in pilocytic astrocytoma. Nat Genet 45:927–932. https://doi.org/10.1038/ng.2682
doi: 10.1038/ng.2682 pubmed: 23817572 pmcid: 3951336
Mirone G, Schiabello L, Chibbaro S et al (2008) Pediatric primary pilocytic astrocytoma of the cerebellopontine angle: a case report. Child’s Nerv Syst 25:247. https://doi.org/10.1007/s00381-008-0690-9
doi: 10.1007/s00381-008-0690-9
Bennett JT, Tan TY, Alcantara D et al (2016) Mosaic activating mutations in FGFR1 cause encephalocraniocutaneous lipomatosis. Am J Hum Genet 98:579–587. https://doi.org/10.1016/j.ajhg.2016.02.006
doi: 10.1016/j.ajhg.2016.02.006 pubmed: 26942290 pmcid: 4800051
Valera ET, McConechy MK, Gayden T et al (2018) Methylome analysis and whole-exome sequencing reveal that brain tumors associated with encephalocraniocutaneous lipomatosis are midline pilocytic astrocytomas. Acta Neuropathol 136:657–660. https://doi.org/10.1007/s00401-018-1898-8
doi: 10.1007/s00401-018-1898-8 pubmed: 30143858 pmcid: 6132939
Schuettpelz LG, McDonald S, Whitesell K et al (2009) Pilocytic astrocytoma in a child with Noonan syndrome. Pediatr Blood Cancer 53:1147–1149. https://doi.org/10.1002/pbc.22193
doi: 10.1002/pbc.22193 pubmed: 19621452
Wippold FJ, Perry A, Lennerz J (2006) Neuropathology for the neuroradiologist: Rosenthal fibers. AJNR Am J Neuroradiol 27:958–961
pubmed: 16687524 pmcid: 7975751
Yamada R, Inoue H, Kuroda J et al (2022) Melanotic pilocytic astrocytoma. Neuropathology. https://doi.org/10.1111/neup.12871
doi: 10.1111/neup.12871 pubmed: 36161674 pmcid: 10084124
Tihan T, Fisher PG, Kepner JL et al (1999) Pediatric astrocytomas with monomorphous pilomyxoid features and a less favorable outcome. J Neuropathol Exp Neurol 58:1061–1068. https://doi.org/10.1097/00005072-199910000-00004
doi: 10.1097/00005072-199910000-00004 pubmed: 10515229
Komotar RJ, Burger PC, Carson BS et al (2004) Pilocytic and pilomyxoid hypothalamic/chiasmatic astrocytomas. Neurosurgery 54:72–80. https://doi.org/10.1227/01.neu.0000097266.89676.25
doi: 10.1227/01.neu.0000097266.89676.25 pubmed: 14683543
Johnson MW, Eberhart CG, Perry A et al (2010) Spectrum of pilomyxoid astrocytomas. Am J Surg Pathol 34:1783–1791. https://doi.org/10.1097/pas.0b013e3181fd66c3
doi: 10.1097/pas.0b013e3181fd66c3 pubmed: 21107083
Fernandez C, Figarella-Branger D, Girard N et al (2003) Pilocytic astrocytomas in children: prognostic factors—a retrospective study of 80 cases. Neurosurgery 53:544–555. https://doi.org/10.1227/01.neu.0000079330.01541.6e
doi: 10.1227/01.neu.0000079330.01541.6e pubmed: 12943571
Rodriguez FJ, Scheithauer BW, Burger PC et al (2010) Anaplasia in pilocytic astrocytoma predicts aggressive behavior. Am J Surg Pathol 34:147–160. https://doi.org/10.1097/pas.0b013e3181c75238
doi: 10.1097/pas.0b013e3181c75238 pubmed: 20061938
Gareton A, Tauziède-Espariat A, Dangouloff-Ros V, et al (2019) The histomolecular criteria established for adult anaplastic pilocytic astrocytoma are not applicable to the pediatric population. Acta neuropathologica 1–17. https://doi.org/10.1007/s00401-019-02088-8
Reinhardt A, Stichel D, Schrimpf D et al (2018) Anaplastic astrocytoma with piloid features, a novel molecular class of IDH wildtype glioma with recurrent MAPK pathway, CDKN2A/B and ATRX alterations. Acta Neuropathol 136:273–291. https://doi.org/10.1007/s00401-018-1837-8
doi: 10.1007/s00401-018-1837-8 pubmed: 29564591
Jacques TS, Buginai M, Rahman S (2024) Metabolic and degenerative disorders of childhood. In: Smith C, Perry A, Jacques TS, Kovacs G (eds) Greenfield’s Neuropathology, 10th edn. CRC Press, pp 421–455
Mateos MK, Birdi N, Basu AP et al (2022) Developmental delay and progressive seizures in 2-month-old child with diffuse MRI abnormalities. Brain Pathol 32:e13049. https://doi.org/10.1111/bpa.13049
doi: 10.1111/bpa.13049 pubmed: 35040226 pmcid: 9234477
Auffret L, Ajlil Y, Tauziède-Espariat A et al (2024) A new subtype of diffuse midline glioma, H3 K27 and BRAF/FGFR1 co-altered: a clinico-radiological and histomolecular characterisation. Acta Neuropathol 147:2. https://doi.org/10.1007/s00401-023-02651-4
doi: 10.1007/s00401-023-02651-4
Rodriguez FJ, Brosnan-Cashman JA, Allen SJ et al (2019) Alternative lengthening of telomeres, ATRX loss and H3–K27M mutations in histologically defined pilocytic astrocytoma with anaplasia. Brain Pathol 29:126–140. https://doi.org/10.1111/bpa.12646
doi: 10.1111/bpa.12646 pubmed: 30192422
Bouffet E, Geoerger B, Moertel C et al (2023) Efficacy and safety of trametinib monotherapy or in combination with dabrafenib in pediatric BRAF V600–mutant low-grade glioma. J Clin Oncol 41:664–674. https://doi.org/10.1200/jco.22.01000
doi: 10.1200/jco.22.01000 pubmed: 36375115
Bouffet E, Hansford JR, Garrè ML et al (2023) Dabrafenib plus trametinib in pediatric glioma with BRAF V600 mutations. N Engl J Med 389:1108–1120. https://doi.org/10.1056/nejmoa2303815
doi: 10.1056/nejmoa2303815 pubmed: 37733309
Petruzzellis G, Valentini D, del Bufalo F et al (2019) Vemurafenib treatment of pleomorphic xanthoastrocytoma in a child with Down syndrome. Front Oncol 9:459–466. https://doi.org/10.3389/fonc.2019.00277
doi: 10.3389/fonc.2019.00277
Murray JC, Donahue DJ, Malik SI et al (2010) Temporal lobe pleomorphic xanthoastrocytoma and acquired BRAF mutation in an adolescent with the constitutional 22q11.2 deletion syndrome. J Neurooncol 102:509–514. https://doi.org/10.1007/s11060-010-0350-2
doi: 10.1007/s11060-010-0350-2 pubmed: 20730472 pmcid: 2998545
Kilickesmez O, Sanal HT, Haholu A, Kocamaz E (2005) Coexistence of pleomorphic xanthoastrocytoma with Sturge-Weber syndrome: MRI features. Pediatr Radiol 35:910–913. https://doi.org/10.1007/s00247-005-1480-0
doi: 10.1007/s00247-005-1480-0 pubmed: 15883827
Chan AK, Han SJ, Choy W et al (2017) Familial melanoma-astrocytoma syndrome: synchronous diffuse astrocytoma and pleomorphic xanthoastrocytoma in a patient with germline CDKN2A/B deletion and a significant family history. Clin Neuropathol 36:213–221. https://doi.org/10.5414/np301022
doi: 10.5414/np301022 pubmed: 28699883 pmcid: 5628627
Vaubel R, Zschernack V, Tran QT, et al (2020) Biology and grading of pleomorphic xanthoastrocytoma—what have we learned about it? Brain pathology (Zurich, Switzerland) bpa.12874–28. https://doi.org/10.1111/bpa.12874
Ebrahimi A, Korshunov A, Reifenberger G et al (2022) Pleomorphic xanthoastrocytoma is a heterogeneous entity with pTERT mutations prognosticating shorter survival. Acta Neuropathol Commun 10:5. https://doi.org/10.1186/s40478-021-01308-1
doi: 10.1186/s40478-021-01308-1 pubmed: 35012690 pmcid: 8751269
Phillips JJ, Gong H, Chen K et al (2019) The genetic landscape of anaplastic pleomorphic xanthoastrocytoma 29:85–96. https://doi.org/10.1111/bpa.12639
doi: 10.1111/bpa.12639
Blümcke I, Wiestler OD (2002) Gangliogliomas: an intriguing tumor entity associated with focal epilepsies. J Neuropathol Exp Neurol 61:575–584. https://doi.org/10.1093/jnen/61.7.575
doi: 10.1093/jnen/61.7.575 pubmed: 12125736
Compton JJ, Laack NNI, Eckel LJ et al (2012) Long-term outcomes for low-grade intracranial ganglioglioma: 30-year experience from the Mayo Clinic: Clinical article. J Neurosurg 117:825–830. https://doi.org/10.3171/2012.7.jns111260
doi: 10.3171/2012.7.jns111260 pubmed: 22957524
Rodriguez FJ, Perry A, Gutmann DH et al (2008) Gliomas in neurofibromatosis type 1: a clinicopathologic study of 100 patients. J Neuropathol Exp Neurol 67:240–249. https://doi.org/10.1097/nen.0b013e318165eb75
doi: 10.1097/nen.0b013e318165eb75 pubmed: 18344915
Pekmezci M, Villanueva-Meyer JE, Goode B et al (2018) The genetic landscape of ganglioglioma. Acta Neuropathol Commun 6:47. https://doi.org/10.1186/s40478-018-0551-z
doi: 10.1186/s40478-018-0551-z pubmed: 29880043 pmcid: 5992851
Platten M, Meyer-Puttlitz B, Blümcke I et al (1997) A novel splice site associated polymorphism in the tuberous sclerosis 2 (TSC2) gene may predispose to the development of sporadic gangliogliomas. J Neuropathol Exp Neurol 56:806–810. https://doi.org/10.1097/00005072-199756070-00007
doi: 10.1097/00005072-199756070-00007 pubmed: 9210877
Becker AJ, Löbach M, Klein H et al (2001) Mutational analysis of TSC1 and TSC2 genes in gangliogliomas. Neuropathol Appl Neurobiol 27:105–114. https://doi.org/10.1046/j.0305-1846.2001.00302.x
doi: 10.1046/j.0305-1846.2001.00302.x pubmed: 11437991
Thom M, Blümcke I, Aronica E (2012) Long-term epilepsy-associated tumors. Brain Pathol 22:350–379. https://doi.org/10.1111/j.1750-3639.2012.00582.x
doi: 10.1111/j.1750-3639.2012.00582.x pubmed: 22497610 pmcid: 8029234
Thom M, Toma A, An S et al (2011) One hundred and one dysembryoplastic neuroepithelial tumors: an adult epilepsy series with immunohistochemical, molecular genetic, and clinical correlations and a review of the literature. J Neuropathology Exp Neurology 70:859–878. https://doi.org/10.1097/nen.0b013e3182302475
doi: 10.1097/nen.0b013e3182302475
Blümcke I, Thom M, Aronica E et al (2011) The clinicopathologic spectrum of focal cortical dysplasias: a consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 52:158–174. https://doi.org/10.1111/j.1528-1167.2010.02777.x
doi: 10.1111/j.1528-1167.2010.02777.x pubmed: 21219302
Palmini A, Paglioli E, Silva VD (2013) Developmental tumors and adjacent cortical dysplasia: single or dual pathology? Epilepsia 54:18–24. https://doi.org/10.1111/epi.12438
doi: 10.1111/epi.12438 pubmed: 24328867
Forsyth PA, Shaw EG, Scheithauer BW et al (1993) Supratentorial pilocytic astrocytomas. A clinicopathologic, prognostic, and flow cytometric study of 51 patients. Cancer 72:1335–1342. https://doi.org/10.1002/1097-0142(19930815)72:4%3c1335::aid-cncr2820720431%3e3.0.co;2-e
doi: 10.1002/1097-0142(19930815)72:4<1335::aid-cncr2820720431>3.0.co;2-e pubmed: 8339223
Collins VP, Jones DTW, Giannini C (2015) Pilocytic astrocytoma: pathology, molecular mechanisms and markers. Acta Neuropathol 129:775–788. https://doi.org/10.1007/s00401-015-1410-7
doi: 10.1007/s00401-015-1410-7 pubmed: 25792358 pmcid: 4436848
Majores M, von Lehe M, Fassunke J et al (2008) Tumor recurrence and malignant progression of gangliogliomas. Cancer 113:3355–3363. https://doi.org/10.1002/cncr.23965
doi: 10.1002/cncr.23965 pubmed: 18988291
Im S-H, Chung CK, Cho B-K et al (2002) Intracranial ganglioglioma: preoperative characteristics and oncologic outcome after surgery. J Neuro-Oncol 59:173–183. https://doi.org/10.1023/a:1019661528350
doi: 10.1023/a:1019661528350
Luyken C, Blümcke I, Fimmers R et al (2004) Supratentorial gangliogliomas: histopathologic grading and tumor recurrence in 184 patients with a median follow-up of 8 years. Cancer 101:146–155. https://doi.org/10.1002/cncr.20332
doi: 10.1002/cncr.20332 pubmed: 15222000
Rumana CS, Valadka AB (1998) Radiation therapy and malignant degeneration of benign supratentorial gangliogliomas. Neurosurgery 42:1038–1043. https://doi.org/10.1097/00006123-199805000-00049
doi: 10.1097/00006123-199805000-00049 pubmed: 9588548
Joyon N, Tauziède-Espariat A, Alentorn A et al (2017) K27M mutation in H3F3A in ganglioglioma grade I with spontaneous malignant transformation extends the histopathological spectrum of the histone H3 oncogenic pathway. Neuropathol Appl Neurobiol 43:271–276. https://doi.org/10.1111/nan.12329
doi: 10.1111/nan.12329 pubmed: 27219822
Kleinschmidt-DeMasters BK, Donson A, Foreman NK, Dorris K (2017) H3 K27M mutation in gangliogliomas can be associated with poor prognosis. Brain Pathol 27:846–850. https://doi.org/10.1111/bpa.12455
doi: 10.1111/bpa.12455 pubmed: 28378357 pmcid: 8029072
Reinhardt A, Pfister K, Schrimpf D et al (2022) Anaplastic ganglioglioma – a diagnosis comprising several distinct tumour types. Neuropath Appl Neuro. https://doi.org/10.1111/nan.12847
doi: 10.1111/nan.12847
Honavar J, Polkey, (1999) Histological heterogeneity of dysembryoplastic neuroepithelial tumour: identification and differential diagnosis in a series of 74 cases. Histopathology 34:342–356. https://doi.org/10.1046/j.1365-2559.1999.00576.x
doi: 10.1046/j.1365-2559.1999.00576.x pubmed: 10231402
Hasselblatt M, Kurlemann G, Rickert CH et al (2004) Familial occurrence of dysembryoplastic neuroepithelial tumor. Neurology 62:1020–1021. https://doi.org/10.1212/01.wnl.0000115266.16119.3a
doi: 10.1212/01.wnl.0000115266.16119.3a pubmed: 15037719
Rivera B, Gayden T, Carrot-Zhang J et al (2016) Germline and somatic FGFR1 abnormalities in dysembryoplastic neuroepithelial tumors. Acta Neuropathol 131:847–863. https://doi.org/10.1007/s00401-016-1549-x
doi: 10.1007/s00401-016-1549-x pubmed: 26920151 pmcid: 5039033
Barba C, Jacques T, Kahane P et al (2013) Epilepsy surgery in neurofibromatosis type 1. Epilepsy Res 105:384–395. https://doi.org/10.1016/j.eplepsyres.2013.02.021
doi: 10.1016/j.eplepsyres.2013.02.021 pubmed: 23597854
McWilliams GD, SantaCruz K, Hart B, Clericuzio C (2016) Occurrence of DNET and other brain tumors in Noonan syndrome warrants caution with growth hormone therapy. Am J Méd Genet Part A 170:195–201. https://doi.org/10.1002/ajmg.a.37379
doi: 10.1002/ajmg.a.37379
Daumas-Duport C, Scheithauer BW, Chodkiewicz J-P et al (1988) Dysembryoplastic neuroepithelial tumor: a surgically curable tumor of young patients with intractable partial seizures. Neurosurgery 23:545–556. https://doi.org/10.1227/00006123-198811000-00002
doi: 10.1227/00006123-198811000-00002 pubmed: 3143922
Komori T, Arai N (2013) DNT is a a pure glial tumor. Neuropathology 33:459–468. https://doi.org/10.1111/neup.12033
doi: 10.1111/neup.12033 pubmed: 23530928
Daumas-Duport C, Varlet P, Bacha S et al (1999) Dysembryoplastic neuroepithelial tumors: nonspecific histological forms – a study of 40 cases J. Neuro-Oncol 41:267–280. https://doi.org/10.1023/a:1006193018140
doi: 10.1023/a:1006193018140
Moazzam AA, Wagle N, Shiroishi MS (2014) Malignant transformation of DNETs. NeuroReport 25:894–899. https://doi.org/10.1097/wnr.0000000000000184
doi: 10.1097/wnr.0000000000000184 pubmed: 25003949
Takita H, Shimono T, Uda T et al (2022) Malignant transformation of a dysembryoplastic neuroepithelial tumor presenting with intraventricular hemorrhage. Radiol Case Rep 17:939–943. https://doi.org/10.1016/j.radcr.2022.01.014
doi: 10.1016/j.radcr.2022.01.014 pubmed: 35140831 pmcid: 8813558
Deng MY, Sill M, Chiang J et al (2018) Molecularly defined diffuse leptomeningeal glioneuronal tumor (DLGNT) comprises two subgroups with distinct clinical and genetic features. Acta Neuropathol 136:239–253. https://doi.org/10.1007/s00401-018-1865-4
doi: 10.1007/s00401-018-1865-4 pubmed: 29766299
Rodriguez FJ, Perry A, Rosenblum MK et al (2012) Disseminated oligodendroglial-like leptomeningeal tumor of childhood: a distinctive clinicopathologic entity. Acta Neuropathol 124:627–641. https://doi.org/10.1007/s00401-012-1037-x
doi: 10.1007/s00401-012-1037-x pubmed: 22941225
Yamasaki T, Sakai N, Shinmura K et al (2018) Anaplastic changes of diffuse leptomeningeal glioneuronal tumor with polar spongioblastoma pattern. Brain Tumor Pathol 35:209–216. https://doi.org/10.1007/s10014-018-0326-z
doi: 10.1007/s10014-018-0326-z pubmed: 30051174
Wiśniewski K, Brandel MG, Gonda DD et al (2022) Prognostic factors in diffuse leptomeningeal glioneuronal tumor (DLGNT): a systematic review. Child’s Nerv Syst 38:1663–1673. https://doi.org/10.1007/s00381-022-05600-w
doi: 10.1007/s00381-022-05600-w
Chiang J, Dalton J, Upadhyaya SA et al (2019) Chromosome arm 1q gain is an adverse prognostic factor in localized and diffuse leptomeningeal glioneuronal tumors with BRAF gene fusion and 1p deletion. Acta Neuropathol 137:179–181. https://doi.org/10.1007/s00401-018-1940-x
doi: 10.1007/s00401-018-1940-x pubmed: 30465258
Jiang H, Qiu L, Song J et al (2022) Clinical progression, pathological characteristics, and radiological findings in children with diffuse leptomeningeal glioneuronal tumors: a systematic review. Front Oncol 12:970076. https://doi.org/10.3389/fonc.2022.970076
doi: 10.3389/fonc.2022.970076 pubmed: 36185310 pmcid: 9525023
Bandopadhayay P, Ramkissoon LA, Jain P et al (2016) MYB-QKI rearrangements in angiocentric glioma drive tumorigenicity through a tripartite mechanism. Nat Genet 48:273–282. https://doi.org/10.1038/ng.3500
doi: 10.1038/ng.3500 pubmed: 26829751 pmcid: 4767685
Lake JA, Donson AM, Prince E et al (2020) Targeted fusion analysis can aid in the classification and treatment of pediatric glioma, ependymoma, and glioneuronal tumors. Pediatr Blood Cancer 67:e28028. https://doi.org/10.1002/pbc.28028
doi: 10.1002/pbc.28028 pubmed: 31595628
Myers KA, Mandelstam SA, Ramantani G et al (2017) The epileptology of Koolen-de Vries syndrome: electro-clinico-radiologic findings in 31 patients. Epilepsia 58:1085–1094. https://doi.org/10.1111/epi.13746
doi: 10.1111/epi.13746 pubmed: 28440867
Li JY, Langford LA, Adesina A et al (2012) The high mitotic count detected by phospho-histone H3 immunostain does not alter the benign behavior of angiocentric glioma. Brain Tumor Pathol 29:68–72. https://doi.org/10.1007/s10014-011-0062-0
doi: 10.1007/s10014-011-0062-0 pubmed: 21892765
Lian F, Wang L-M, Qi X-L et al (2020) MYB-QKI rearrangement in angiocentric glioma. Clin Neuropathol 39:263–270. https://doi.org/10.5414/np301284
doi: 10.5414/np301284 pubmed: 32589128
Han G, Zhang J, Ma Y et al (2020) Clinical characteristics, treatment and prognosis of angiocentric glioma. Oncol Lett 20:1641–1648. https://doi.org/10.3892/ol.2020.11723
doi: 10.3892/ol.2020.11723 pubmed: 32724405 pmcid: 7377082
Wefers AK, Stichel D, Schrimpf D, et al (2019) Isomorphic diffuse glioma is a morphologically and molecularly distinct tumour entity with recurrent gene fusions of MYBL1 or MYB and a benign disease course. Acta neuropathologica 1–17. https://doi.org/10.1007/s00401-019-02078-w
Taratuto AL, Monges J, Lylyk P, Leiguarda R (1984) Superficial cerebral astrocytoma attached to dura: report of six cases in infants. Cancer 54:2505–2512. https://doi.org/10.1002/1097-0142(19841201)54:11%3c2505::aid-cncr2820541132%3e3.0.co;2-g
doi: 10.1002/1097-0142(19841201)54:11<2505::aid-cncr2820541132>3.0.co;2-g pubmed: 6498740
VandenBerg SR, May EE, Rubinstein LJ et al (1987) Desmoplastic supratentorial neuroepithelial tumors of infancy with divergent differentiation potential (“desmoplastic infantile gangliogliomas”): report on 11 cases of a distinctive embryonal tumor with favorable prognosis. J Neurosurg 66:58–71. https://doi.org/10.3171/jns.1987.66.1.0058
doi: 10.3171/jns.1987.66.1.0058 pubmed: 3097276
Jansen AC, Belousova E, Benedik MP et al (2019) Newly diagnosed and growing subependymal giant cell astrocytoma in adults with tuberous sclerosis complex: results from the international TOSCA study. Front Neurol 10:821. https://doi.org/10.3389/fneur.2019.00821
doi: 10.3389/fneur.2019.00821 pubmed: 31428037 pmcid: 6688052
Northrup H, Aronow ME, Bebin EM et al (2021) Updated international tuberous sclerosis complex diagnostic criteria and surveillance and management recommendations. Pediatr Neurol 123:50–66. https://doi.org/10.1016/j.pediatrneurol.2021.07.011
doi: 10.1016/j.pediatrneurol.2021.07.011 pubmed: 34399110
Bongaarts A, Mijnsbergen C, Anink JJ et al (2022) Distinct DNA methylation patterns of subependymal giant cell astrocytomas in tuberous sclerosis complex. Cell Mol Neurobiol 42:2863–2892. https://doi.org/10.1007/s10571-021-01157-5
doi: 10.1007/s10571-021-01157-5 pubmed: 34709498
Sharma MC, Ralte AM, Gaekwad S et al (2004) Subependymal giant cell astrocytoma — a clinicopathological study of 23 cases with special emphasis on histogenesis. Pathol Oncol Res 10:219–224. https://doi.org/10.1007/bf03033764
doi: 10.1007/bf03033764 pubmed: 15619643
Lopes MBS, Altermatt HJ, Scheithauer BW et al (1996) Immunohistochemical characterization of subependymal giant cell astrocytomas. Acta Neuropathol 91:368–375. https://doi.org/10.1007/s004010050438
doi: 10.1007/s004010050438 pubmed: 8928613
Hang J-F, Hsu C-Y, Lin S-C et al (2017) Thyroid transcription factor-1 distinguishes subependymal giant cell astrocytoma from its mimics and supports its cell origin from the progenitor cells in the medial ganglionic eminence. Mod Pathol 30:318–328. https://doi.org/10.1038/modpathol.2016.205
doi: 10.1038/modpathol.2016.205 pubmed: 27910945
Yamada S, Tanikawa M, Matsushita Y, et al (2023) SEGA‐like circumscribed astrocytoma in a non‐NF1 patient, harboring molecular profile of GBM. A case report. Neuropathology. https://doi.org/10.1111/neup.12948
Palsgrove DN, Brosnan-Cashman JA, Giannini C et al (2018) Subependymal giant cell astrocytoma-like astrocytoma: a neoplasm with a distinct phenotype and frequent neurofibromatosis type-1-association. Mod Pathol 31:1787–1800. https://doi.org/10.1038/s41379-018-0103-x
doi: 10.1038/s41379-018-0103-x pubmed: 29973652 pmcid: 6269209
Martin KR, Zhou W, Bowman MJ et al (2017) The genomic landscape of tuberous sclerosis complex. Nat Commun 8:15816. https://doi.org/10.1038/ncomms15816
doi: 10.1038/ncomms15816 pubmed: 28643795 pmcid: 5481739
Reynolds RA, Aum DJ, Gonzalez-Gomez I et al (2023) Subependymal giant-cell astrocytomas in the absence of tuberous sclerosis. J Neurosurg: Pediatr 32:1–7. https://doi.org/10.3171/2023.5.peds23108
doi: 10.3171/2023.5.peds23108
Anan M, Inoue R, Ishii K et al (2009) A rosette-forming glioneuronal tumor of the spinal cord: the first case of a rosette-forming glioneuronal tumor originating from the spinal cord. Hum Pathol 40:898–901. https://doi.org/10.1016/j.humpath.2008.11.010
doi: 10.1016/j.humpath.2008.11.010 pubmed: 19269010
Solis OE, Mehta RI, Lai A et al (2011) Rosette-forming glioneuronal tumor: a pineal region case with IDH1 and IDH2 mutation analyses and literature review of 43 cases J. Neuro-Oncol 102:477–484. https://doi.org/10.1007/s11060-010-0335-1
doi: 10.1007/s11060-010-0335-1
Schlamann A, von Bueren AO, Hagel C et al (2014) An individual patient data meta-analysis on characteristics and outcome of patients with papillary glioneuronal tumor, rosette glioneuronal tumor with neuropil-like islands and rosette forming glioneuronal tumor of the fourth ventricle. PLoS ONE 9:e101211. https://doi.org/10.1371/journal.pone.0101211
doi: 10.1371/journal.pone.0101211 pubmed: 24991807 pmcid: 4084640
Medhi G, Prasad C, Saini J et al (2016) Imaging features of rosette-forming glioneuronal tumours (RGNTs): a series of seven cases. Eur Radiol 26:262–270. https://doi.org/10.1007/s00330-015-3808-y
doi: 10.1007/s00330-015-3808-y pubmed: 26017735
Yang C, Fang J, Li G et al (2017) Histopathological, molecular, clinical and radiological characterization of rosette-forming glioneuronal tumor in the central nervous system. Oncotarget 8:109175–109190. https://doi.org/10.18632/oncotarget.22646
doi: 10.18632/oncotarget.22646 pubmed: 29312599 pmcid: 5752512
Wilson CP, Chakraborty AR, Pelargos PE, et al (2020) Rosette-forming glioneuronal tumor: an illustrative case and a systematic review. Neuro-Oncol Adv 2:vdaa116. https://doi.org/10.1093/noajnl/vdaa116
Appay R, Bielle F, Sievers P et al (2022) Rosette-forming glioneuronal tumours are midline, FGFR1-mutated tumours. Neuropath Appl Neuro 48:e12813. https://doi.org/10.1111/nan.12813
doi: 10.1111/nan.12813
Lerond J, Morisse MC, Letourneur Q et al (2022) Immune microenvironment and lineage tracing help to decipher rosette-forming glioneuronal tumors: a multi-omics analysis. J Neuropathol Exp Neurol 81:873–884. https://doi.org/10.1093/jnen/nlac074
doi: 10.1093/jnen/nlac074 pubmed: 35984315
Cabezas SG, Blanch RS, Sanchez-Sanchez R, Eito AP (2015) Rosette-forming glioneuronal tumour (RGNT) of the fourth ventricle: a highly aggressive case. Brain Tumor Pathol 32:124–130. https://doi.org/10.1007/s10014-014-0195-z
doi: 10.1007/s10014-014-0195-z
Allinson KSJ, O’Donovan DG, Jena R et al (2015) Rosette-forming glioneuronal tumor with dissemination throughout the ventricular system: a case report. Clin Neuropathol 34:64–69. https://doi.org/10.5414/np300682
doi: 10.5414/np300682 pubmed: 25373141
Silveira L, DeWitt J, Thomas A, Tranmer B (2019) Disseminated rosette-forming glioneuronal tumor with spinal drop metastasis, a uniquely aggressive presentation of rare tumor. World Neurosurg 132:7–11. https://doi.org/10.1016/j.wneu.2019.08.055
doi: 10.1016/j.wneu.2019.08.055 pubmed: 31442659
Karafin M, Jallo GI, Ayars M et al (2011) Rosette forming glioneuronal tumor in association with Noonan syndrome: pathobiological implications. Clin Neuropathol 30:297–300. https://doi.org/10.5414/np300374
doi: 10.5414/np300374 pubmed: 22011734 pmcid: 3657471
Lin FY, Bergstrom K, Person R et al (2016) Integrated tumor and germline whole-exome sequencing identifies mutations in MAPK and PI3K pathway genes in an adolescent with rosette-forming glioneuronal tumor of the fourth ventricle. Mol Case Stud 2:a001057. https://doi.org/10.1101/mcs.a001057
doi: 10.1101/mcs.a001057
Fisher MJ, Jones DTW, Li Y, et al (2021) Integrated molecular and clinical analysis of low-grade gliomas in children with neurofibromatosis type 1 (NF1). Acta Neuropathol 1–13. https://doi.org/10.1007/s00401-021-02276-5
Jacques TS, Eldridge C, Patel A et al (2006) Mixed glioneuronal tumour of the fourth ventricle with prominent rosette formation. Neuropathol Appl Neurobiol 32:217–220. https://doi.org/10.1111/j.1365-2990.2005.00692.x
doi: 10.1111/j.1365-2990.2005.00692.x pubmed: 16599951
Matyja E, Grajkowska W, Nauman P et al (2011) Rosette-forming glioneuronal tumor of the fourth ventricle with advanced microvascular proliferation – a case report. Neuropathology 31:427–432. https://doi.org/10.1111/j.1440-1789.2010.01168.x
doi: 10.1111/j.1440-1789.2010.01168.x pubmed: 21092064
Lucas CHG, Gupta R, Doo P, et al (2020) Comprehensive analysis of diverse low-grade neuroepithelial tumors with FGFR1 alterations reveals a distinct molecular signature of rosette-forming glioneuronal tumor. Acta neuropathologica communications 1–17. https://doi.org/10.1186/s40478-020-01027-z
Ellezam B, Theeler BJ, Luthra R et al (2012) Recurrent PIK3CA mutations in rosette-forming glioneuronal tumor. Acta Neuropathol 123:285–287. https://doi.org/10.1007/s00401-011-0886-z
doi: 10.1007/s00401-011-0886-z pubmed: 21997360
Cachia D, Prado MP, Theeler B et al (2014) Synchronous rosette-forming glioneuronal tumor and diffuse astrocytoma with molecular characterization: a case report. Clin Neuropathol 33:407–411. https://doi.org/10.5414/np300767
doi: 10.5414/np300767 pubmed: 24986181
Gessi M, Moneim YA, Hammes J et al (2014) FGFR1 mutations in rosette-forming glioneuronal tumors of the fourth ventricle. J Neuropathol Exp Neurol 73:580–584. https://doi.org/10.1097/nen.0000000000000080
doi: 10.1097/nen.0000000000000080 pubmed: 24806303
Kitamura Y, Komori T, Shibuya M et al (2018) Comprehensive genetic characterization of rosette-forming glioneuronal tumors: independent component analysis by tissue microdissection. Brain Pathol 28:87–93. https://doi.org/10.1111/bpa.12468
doi: 10.1111/bpa.12468 pubmed: 27893178
Sievers P, Appay R, Schrimpf D et al (2019) Rosette-forming glioneuronal tumors share a distinct DNA methylation profile and mutations in FGFR1, with recurrent co-mutation of PIK3CA and NF1. Acta Neuropathol 138:497–504. https://doi.org/10.1007/s00401-019-02038-4
doi: 10.1007/s00401-019-02038-4 pubmed: 31250151
Morassi MDM, Vivaldi MDO, Cobelli MDM, et al (2019) A multifocal glioneuronal tumor with RGNT-like morphology occupying the supratentorial ventricular system and infiltrating the brain parenchyma. World neurosurgery 1–18. https://doi.org/10.1016/j.wneu.2019.10.017
James W, Yousif S, Lau Q, Ng W (2023) Recurrent anaplastic transformation of a Vermian region rosette forming glioneuronal tumour – a rare entity. Case report and review of literature. Int J Surg Case Rep 105:108054. https://doi.org/10.1016/j.ijscr.2023.108054
Halfpenny A, Ferris SP, Grafe M et al (2019) A case of recurrent epilepsy-associated rosette-forming glioneuronal tumor with anaplastic transformation in the absence of therapy. Neuropathology 39:389–393. https://doi.org/10.1111/neup.12586
doi: 10.1111/neup.12586 pubmed: 31435988 pmcid: 6852525
Nair JN, Naidu B, Balasubramanian A, Krishnamurthy G (2024) Polymorphous low-grade neuroepithelial tumour of young (PLNTY): the new kid on the block. Child’s Nerv Syst 40:555–561. https://doi.org/10.1007/s00381-023-06162-1
doi: 10.1007/s00381-023-06162-1
Surrey LF, Jain P, Zhang B et al (2019) Genomic analysis of dysembryoplastic neuroepithelial tumor spectrum reveals a diversity of molecular alterations dysregulating the MAPK and PI3K/mTOR pathways. J Neuropathol Exp Neurol 78:1100–1111. https://doi.org/10.1093/jnen/nlz101
doi: 10.1093/jnen/nlz101 pubmed: 31617914
Huse JT, Snuderl M, Jones DTW et al (2017) Polymorphous low-grade neuroepithelial tumor of the young (PLNTY): an epileptogenic neoplasm with oligodendroglioma-like components, aberrant CD34 expression, and genetic alterations involving the MAP kinase pathway. Acta Neuropathol 133:417–429. https://doi.org/10.1007/s00401-016-1639-9
doi: 10.1007/s00401-016-1639-9 pubmed: 27812792
Ida CM, Johnson DR, Nair AA et al (2021) Polymorphous low-grade neuroepithelial tumor of the young (PLNTY): molecular profiling confirms frequent MAPK pathway activation. J Neuropathology Exp Neurology. https://doi.org/10.1093/jnen/nlab075
doi: 10.1093/jnen/nlab075
Johnson DR, Giannini C, Jenkins RB et al (2019) Plenty of calcification: imaging characterization of polymorphous low-grade neuroepithelial tumor of the young. Neuroradiology 61:1327–1332. https://doi.org/10.1007/s00234-019-02269-y
doi: 10.1007/s00234-019-02269-y pubmed: 31396664
Chaubal A, Paetau A, Zoltick P, Miettinen M (1994) CD34 immunoreactivity in nervous system tumors. Acta Neuropathol 88:454–458. https://doi.org/10.1007/bf00389498
doi: 10.1007/bf00389498 pubmed: 7531384
Netto GC, Bleil CB, Hilbig A, Coutinho LMB (2008) Immunohistochemical evaluation of the microvascular density through the expression of TGF-β (CD 105/endoglin) and CD 34 receptors and expression of the vascular endothelial growth factor (VEGF) in oligodendrogliomas. Neuropathology 28:17–23. https://doi.org/10.1111/j.1440-1789.2007.00825.x
doi: 10.1111/j.1440-1789.2007.00825.x pubmed: 18181830
Perry A, Burton SS, Fuller GN et al (2010) Oligodendroglial neoplasms with ganglioglioma-like maturation: a diagnostic pitfall. Acta Neuropathol 120:237–252. https://doi.org/10.1007/s00401-010-0695-9
doi: 10.1007/s00401-010-0695-9 pubmed: 20464403 pmcid: 2892612
Gupta R, Lucas C-HG, Wu J, et al (2021) Low-grade glioneuronal tumors with FGFR2 fusion resolve into a single epigenetic group corresponding to ‘Polymorphous low-grade neuroepithelial tumor of the young.’ Acta Neuropathol 1–5. https://doi.org/10.1007/s00401-021-02352-w
Bale TA, Sait SF, Benhamida J, et al (2020) Malignant transformation of a polymorphous low grade neuroepithelial tumor of the young (PLNTY). Acta neuropathologica 1–3. https://doi.org/10.1007/s00401-020-02245-4
Ellison DW, Hawkins C, Jones DTW, et al (2019) cIMPACT-NOW update 4: diffuse gliomas characterized by MYB, MYBL1, or FGFR1 alterations or BRAFV600E mutation. Acta neuropathologica 1–5. https://doi.org/10.1007/s00401-019-01987-0
Ryall S, Zapotocky M, Fukuoka K et al (2020) Integrated molecular and clinical analysis of 1,000 pediatric low-grade gliomas. Cancer Cell 37:569-583.e5. https://doi.org/10.1016/j.ccell.2020.03.011
doi: 10.1016/j.ccell.2020.03.011 pubmed: 32289278 pmcid: 7169997
Pickles JC, Stone TJ, Jacques TS (2020) Methylation-based algorithms for diagnosis: experience from neuro-oncology. J Pathology 250:510–517. https://doi.org/10.1002/path.5397
doi: 10.1002/path.5397

Auteurs

Thomas J Stone (TJ)

Developmental Biology and Cancer Research and Teaching Department, UCL GOS Institute of Child Health, London, UK.
Department of Histopathology, Great Ormond Street Hospital, London, UK.

Ashirwad Merve (A)

Developmental Biology and Cancer Research and Teaching Department, UCL GOS Institute of Child Health, London, UK.
Department of Histopathology, Great Ormond Street Hospital, London, UK.
Division of Neuropathology, The National Hospital for Neurology and Neurosurgery, London, UK.

Fernanda Valerio (F)

Department of Histopathology, Great Ormond Street Hospital, London, UK.
Division of Neuropathology, The National Hospital for Neurology and Neurosurgery, London, UK.

Shireena A Yasin (SA)

Developmental Biology and Cancer Research and Teaching Department, UCL GOS Institute of Child Health, London, UK.
Department of Histopathology, Great Ormond Street Hospital, London, UK.

Thomas S Jacques (TS)

Developmental Biology and Cancer Research and Teaching Department, UCL GOS Institute of Child Health, London, UK. t.jacques@ucl.ac.uk.
Department of Histopathology, Great Ormond Street Hospital, London, UK. t.jacques@ucl.ac.uk.

Classifications MeSH