The utility of DNA methylation analysis in elderly patients with pilocytic astrocytoma morphology.

Humans Aged Child, Preschool Child Adolescent Young Adult Adult Middle Aged Aged, 80 and over DNA Methylation Retrospective Studies Brain Neoplasms / pathology Mutation Astrocytoma / pathology Isocitrate Dehydrogenase / genetics

DNA methylation Elderly High-grade astrocytoma with piloid features Pilocytic astrocytoma

Journal

Journal of neuro-oncology

ISSN: 1573-7373

Titre abrégé: J Neurooncol

Pays: United States

ID NLM: 8309335

Informations de publication

Date de publication:
Oct 2022

Historique:

received: 13 08 2022

accepted: 07 09 2022

pubmed: 16 9 2022

medline: 3 11 2022

entrez: 15 9 2022

Statut: ppublish

Résumé

Pilocytic astrocytoma (PA) is a circumscribed low-grade astrocytic glioma, generally considered to be associated with a good prognosis. However, a subset of PA patients shows unfavorable outcomes. In this study, we retrospectively reviewed PA patients and performed further molecular analysis, such as DNA methylation profiling, to identify prognostic factors. We analyzed 29 histologically-confirmed PA patients from a single center from 2002 to 2021 and conducted integrated molecular analyses among elderly PA patients since age was an independent prognostic factor for poor outcomes. The median age at diagnosis was 14 years (range 3-82 years) and 4 patients (14%) were elderly (patients ≥ 60 years old). Age over 60 was associated with poor progression-free survival and overall survival. We performed DNA methylation analysis on 2 of the 4 elderly patients. Both cases were histologically diagnosed as PA, but DNA methylation profiling revealed one as high-grade astrocytoma with piloid features (all methylation class scores were below 0.3 in both v11b4 and v12.5) and the other as glioblastoma, IDH-wildtype (score was over 0.5 in both v11b4 and v12.5), using the German Cancer Research Center methylation profiling classifiers and t-SNE analysis. Elderly patients with PA morphology showed unfavorable outcomes in this cohort. In those patients, further molecular analysis and DNA methylation profiling revealed the possibility of high-grade astrocytic tumors, including newly defined entities.

Identifiants

DOI: 10.1007/s11060-022-04131-3 PMID: 36107362

pubmed: 36107362

doi: 10.1007/s11060-022-04131-3

pii: 10.1007/s11060-022-04131-3

doi:

Substances chimiques

Isocitrate Dehydrogenase EC 1.1.1.41

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

Pagination

179-189

Subventions

Organisme : Japanese Ministry of Education, Culture, Sports, Science and Technology

ID : 22K06951

Organisme : Japanese Ministry of Education, Culture, Sports, Science and Technology

ID : 21K20803

Organisme : National Cancer Center Rare Cancer Grant

ID : G007

Informations de copyright

Références

Ostrom QT, Cioffi G, Waite K, et al. (2021) CBTRUS Statistical Report: primary brain and other central nervous system tumors diagnosed in the United States in 2014–2018. Neuro Oncol 23: iii1-iii105. https://doi.org/10.1093/neuonc/noab200

Board WCoTE (2021) Central nervous system tumours. International Agency for Research on Cancer, Lyon

Tomita Y, Hibler EA, Suruga Y et al (2022) Age is a major determinant for poor prognosis in patients with pilocytic astrocytoma: a SEER population study. Clin Exp Med. https://doi.org/10.1007/s10238-022-00882-5

doi: 10.1007/s10238-022-00882-5 pubmed: 36063258

Dodgshun AJ, Maixner WJ, Hansford JR et al (2016) Low rates of recurrence and slow progression of pediatric pilocytic astrocytoma after gross-total resection: justification for reducing surveillance imaging. J Neurosurg Pediatr 17:569–572. https://doi.org/10.3171/2015.9.Peds15449

doi: 10.3171/2015.9.Peds15449 pubmed: 26722760

Jungk C, Reinhardt A, Warta R et al (2019) Extent of resection, MGMT promoter methylation status and tumor location independently predict progression-free survival in adult sporadic pilocytic astrocytoma. Cancers (Basel). https://doi.org/10.3390/cancers11081072

doi: 10.3390/cancers11081072

Nelson AJ, Zakaria R, Jenkinson MD et al (2019) Extent of resection predicts risk of progression in adult pilocytic astrocytoma. Br J Neurosurg 33:343–347. https://doi.org/10.1080/02688697.2018.1549315

doi: 10.1080/02688697.2018.1549315 pubmed: 30653383

Mair MJ, Wöhrer A, Furtner J et al (2020) Clinical characteristics and prognostic factors of adult patients with pilocytic astrocytoma. J Neurooncol 148:187–198. https://doi.org/10.1007/s11060-020-03513-9

doi: 10.1007/s11060-020-03513-9 pubmed: 32342331 pmcid: 7280326

Bond KM, Hughes JD, Porter AL et al (2018) Adult pilocytic astrocytoma: an institutional series and systematic literature review for extent of resection and recurrence. World Neurosurg 110:276–283. https://doi.org/10.1016/j.wneu.2017.11.102

doi: 10.1016/j.wneu.2017.11.102 pubmed: 29180079

Theeler BJ, Ellezam B, Sadighi ZS et al (2014) Adult pilocytic astrocytomas: clinical features and molecular analysis. Neuro Oncol 16:841–847. https://doi.org/10.1093/neuonc/not246

doi: 10.1093/neuonc/not246 pubmed: 24470550 pmcid: 4022218

Jones DT, Gronych J, Lichter P et al (2012) MAPK pathway activation in pilocytic astrocytoma. Cell Mol Life Sci 69:1799–1811. https://doi.org/10.1007/s00018-011-0898-9

doi: 10.1007/s00018-011-0898-9 pubmed: 22159586

Kurani H, Gurav M, Shetty O et al (2019) Pilocytic astrocytomas: BRAFV600E and BRAF fusion expression patterns in pediatric and adult age groups. Childs Nerv Syst 35:1525–1536. https://doi.org/10.1007/s00381-019-04282-1

doi: 10.1007/s00381-019-04282-1 pubmed: 31321520

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

Kameda M, Otani Y, Ichikawa T et al (2017) Congenital glioblastoma with distinct clinical and molecular characteristics: case reports and a literature review. World Neurosurg. https://doi.org/10.1016/j.wneu.2017.02.026

doi: 10.1016/j.wneu.2017.02.026 pubmed: 28214639

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

Johnson DR, Brown PD, Galanis E et al (2012) Pilocytic astrocytoma survival in adults: analysis of the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute. J Neurooncol 108:187–193. https://doi.org/10.1007/s11060-012-0829-0

doi: 10.1007/s11060-012-0829-0 pubmed: 22367412

Stuer C, Vilz B, Majores M et al (2007) Frequent recurrence and progression in pilocytic astrocytoma in adults. Cancer 110:2799–2808. https://doi.org/10.1002/cncr.23148

doi: 10.1002/cncr.23148 pubmed: 17973253

Voronina N, Aichmuller C, Kolb T et al (2021) The age of adult pilocytic astrocytoma cells. Oncogene 40:2830–2841. https://doi.org/10.1038/s41388-021-01738-0

doi: 10.1038/s41388-021-01738-0 pubmed: 33731860 pmcid: 8062266

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

Louis DN, Perry A, Reifenberger G et al (2016) The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 131:803–820. https://doi.org/10.1007/s00401-016-1545-1

doi: 10.1007/s00401-016-1545-1 pubmed: 27157931

Bender K, Perez E, Chirica M et al (2021) High-grade astrocytoma with piloid features (HGAP): the Charite experience with a new central nervous system tumor entity. J Neurooncol 153:109–120. https://doi.org/10.1007/s11060-021-03749-z

doi: 10.1007/s11060-021-03749-z pubmed: 33905054 pmcid: 8131327

Giannini C, Scheithauer BW, Burger PC et al (1999) Cellular proliferation in pilocytic and diffuse astrocytomas. J Neuropathol Exp Neurol 58:46–53. https://doi.org/10.1097/00005072-199901000-00006

doi: 10.1097/00005072-199901000-00006 pubmed: 10068313

Collins VP, Jones DT, 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

Ono T, Takahashi M, Hatakeyama J et al (2019) Clinical significance of molecular diagnosis of pilocytic astrocytoma: a case report. NMC Case Rep J 6:95–99. https://doi.org/10.2176/nmccrj.cr.2018-0282

doi: 10.2176/nmccrj.cr.2018-0282 pubmed: 31417840 pmcid: 6692597

Shibui S, Narita Y, Mizusawa J et al (2013) Randomized trial of chemoradiotherapy and adjuvant chemotherapy with nimustine (ACNU) versus nimustine plus procarbazine for newly diagnosed anaplastic astrocytoma and glioblastoma (JCOG0305). Cancer Chemother Pharmacol 71:511–521. https://doi.org/10.1007/s00280-012-2041-5

doi: 10.1007/s00280-012-2041-5 pubmed: 23228988