Skip to main content

Advertisement

SpringerLink
Log in

Neuro-radiological characteristics of adult diffuse grade II and III insular gliomas classified according to WHO 2016

  • Clinical Study
  • Published:
Journal of Neuro-Oncology Aims and scope Submit manuscript

A Correction to this article was published on 11 March 2019

This article has been updated

Abstract

Introduction

The phenotypic heterogeneity of diffuse gliomas is still inconsistently explained by known molecular abnormalities. Here, we report the molecular and radiological features of diffuse grade WHO II and III gliomas involving the insula and its potential impact on prognosis.

Methods

Clinical, pathological, molecular and neuro-radiological features of 43 consecutive patients who underwent a surgical resection between 2006 and 2013 for a grade II and III gliomas involving the insula was retrospectively analyzed.

Results

Median age was 44.4 years. Eight patients had oligodendrogliomas, IDH mutant (IDHmut) and 1p/19q-codeleted (6 grade II, 2 grade III). Twenty-eight patients had diffuse astrocytomas, IDHmut (22 grade II and 6 grade III) and seven patients had grade II diffuse astrocytomas, IDHwt (A-IDHwt). Vimentin staining was exclusively recorded in tumor cells from A-IDHwt (p = 0.001). Mean cerebral blood volume (CBV) (p = 0.018), maximal value of CBV (p = 0.017) and ratio of the corrected CBV (p = 0.022) were lower for A-IDHwt. Volumetric segmentation of ADC allowed the identification of the tumor cores, which were smaller in A-IDHwt (p < 0.001). The tumor occurrences of A-IDHwt were exclusively located into the temporo-insular region. Median progression-free survival (PFS) and overall survival (OS) were 50.9 months (95% CI: 26.7–75.0) and 80.9 months (60.1–101.6). By multivariate analysis, A-IDHwt (p = 0.009; p = 0.019), 7p gain and 10q loss (p = 0.009; p = 0.016) and vimentin positive staining (p = 0.011; p = 0.029) were associated with poor PFS and OS respectively.

Conclusions

Insular low-grade A-IDHwt presented with poor prognosis despite a smaller tumor core and no evidence of increased perfusion on MR imaging.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Change history

  • 11 March 2019

    In the initial, online publication, the authors' given names were captured as family names and vice versa. The names are correctly shown here. The original article has been corrected.

References

  1. Smith JS, Perry A, Borell TJ et al (2000) Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol 18:636–645

    Article  CAS  PubMed  Google Scholar 

  2. Parsons DW, Jones S, Zhang X et al (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807–1812. https://doi.org/10.1126/science.1164382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Yan H, Parsons DW, Jin G et al (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360:765–773. https://doi.org/10.1056/NEJMoa0808710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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

    Article  PubMed  Google Scholar 

  5. van den Bent MJ, Brandes AA, Taphoorn MJB et al (2013) Adjuvant procarbazine, lomustine, and vincristine chemotherapy in newly diagnosed anaplastic oligodendroglioma: long-term follow-up of EORTC brain tumor group study 26951. J Clin Oncol Off J Am Soc Clin Oncol 31:344–350. https://doi.org/10.1200/JCO.2012.43.2229

    Article  CAS  Google Scholar 

  6. Buckner JC, Shaw EG, Pugh SL et al (2016) Radiation plus procarbazine, CCNU, and Vincristine in low-grade glioma. N Engl J Med 374:1344–1355. https://doi.org/10.1056/NEJMoa1500925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Stupp R, Mason WP, van den Bent MJ et al (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996. https://doi.org/10.1056/NEJMoa043330

    Article  CAS  Google Scholar 

  8. Weller M, van den Bent M, Tonn JC et al (2017) European Association for neuro-oncology (EANO) guideline on the diagnosis and treatment of adult astrocytic and oligodendroglial gliomas. Lancet Oncol 18:e315–e329. https://doi.org/10.1016/S1470-2045(17)30194-8

    Article  PubMed  Google Scholar 

  9. Metellus P, Coulibaly B, Colin C et al (2010) Absence of IDH mutation identifies a novel radiologic and molecular subtype of WHO grade II gliomas with dismal prognosis. Acta Neuropathol 120:719–729. https://doi.org/10.1007/s00401-010-0777-8

    Article  PubMed  Google Scholar 

  10. Tabouret E, Nguyen AT, Dehais C et al (2016) Prognostic impact of the 2016 WHO classification of diffuse gliomas in the French POLA cohort. Acta Neuropathol 132:625–634. https://doi.org/10.1007/s00401-016-1611-8

    Article  PubMed  Google Scholar 

  11. Labussière M, Di Stefano AL, Gleize V et al (2014) TERT promoter mutations in gliomas, genetic associations and clinico-pathological correlations. Br J Cancer 111:2024–2032. https://doi.org/10.1038/bjc.2014.538

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Feber A, Guilhamon P, Lechner M et al (2014) Using high-density DNA methylation arrays to profile copy number alterations. Genome Biol 15:R30. https://doi.org/10.1186/gb-2014-15-2-r30

    Article  PubMed  PubMed Central  Google Scholar 

  13. Iglesias JE, Liu C-Y, Thompson PM, Tu Z (2011) Robust brain extraction across datasets and comparison with publicly available methods. IEEE Trans Med Imaging 30:1617–1634. https://doi.org/10.1109/TMI.2011.2138152

    Article  PubMed  Google Scholar 

  14. Mazziotta J, Toga A, Evans A et al (2001) A four-dimensional probabilistic atlas of the human brain. J Am Med Inform Assoc 8:401–430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Menze BH, Jakab A, Bauer S et al (2015) The multimodal brain tumor image segmentation benchmark (BRATS). IEEE Trans Med Imaging 34:1993–2024. https://doi.org/10.1109/TMI.2014.2377694

    Article  PubMed  Google Scholar 

  16. Duffau H, Capelle L (2004) Preferential brain locations of low-grade gliomas. Cancer 100:2622–2626. https://doi.org/10.1002/cncr.20297

    Article  PubMed  Google Scholar 

  17. Duffau H (2018) Surgery of insular gliomas. Prog Neurol Surg 30:173–185. https://doi.org/10.1159/000464393

    Article  PubMed  Google Scholar 

  18. Michaud K, Duffau H (2016) Surgery of insular and paralimbic diffuse low-grade gliomas: technical considerations. J Neurooncol 130:289–298. https://doi.org/10.1007/s11060-016-2120-2

    Article  PubMed  Google Scholar 

  19. Signorelli F, Guyotat J, Elisevich K, Barbagallo GMV (2010) Review of current microsurgical management of insular gliomas. Acta Neurochir 152:19–26. https://doi.org/10.1007/s00701-009-0450-y

    Article  PubMed  Google Scholar 

  20. Cancer Genome Atlas Research Network, Brat DJ, Verhaak RGW et al (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. N Engl J Med 372:2481–2498. https://doi.org/10.1056/NEJMoa1402121

    Article  CAS  Google Scholar 

  21. Suzuki H, Aoki K, Chiba K et al (2015) Mutational landscape and clonal architecture in grade II and III gliomas. Nat Genet 47:458–468. https://doi.org/10.1038/ng.3273

    Article  CAS  PubMed  Google Scholar 

  22. Jiang H, Cui Y, Wang J, Lin S (2017) Impact of epidemiological characteristics of supratentorial gliomas in adults brought about by the 2016 world health organization classification of tumors of the central nervous system. Oncotarget 8:20354–20361. https://doi.org/10.18632/oncotarget.13555

    Article  PubMed  Google Scholar 

  23. Delfanti RL, Piccioni DE, Handwerker J et al (2017) Imaging correlates for the 2016 update on WHO classification of grade II/III gliomas: implications for IDH, 1p/19q and ATRX status. J Neurooncol 135:601–609. https://doi.org/10.1007/s11060-017-2613-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Tejada Neyra MA, Neuberger U, Reinhardt A et al (2018) Voxel-wise radiogenomic mapping of tumor location with key molecular alterations in patients with glioma. Neuro-Oncol 20:1517–1524. https://doi.org/10.1093/neuonc/noy134

    Article  CAS  PubMed  Google Scholar 

  25. Yamauchi T, Ohno M, Matsushita Y et al (2018) Radiological characteristics based on isocitrate dehydrogenase mutations and 1p/19q codeletion in grade II and III gliomas. Brain Tumor Pathol. https://doi.org/10.1007/s10014-018-0321-4

    Article  PubMed  Google Scholar 

  26. Gaiano N, Fishell G (2002) The role of notch in promoting glial and neural stem cell fates. Annu Rev Neurosci 25:471–490. https://doi.org/10.1146/annurev.neuro.25.030702.130823

    Article  CAS  PubMed  Google Scholar 

  27. Riemenschneider MJ, Koy TH, Reifenberger G (2004) Expression of oligodendrocyte lineage genes in oligodendroglial and astrocytic gliomas. Acta Neuropathol 107:277–282. https://doi.org/10.1007/s00401-003-0809-8

    Article  CAS  PubMed  Google Scholar 

  28. Ehninger D, Kempermann G (2008) Neurogenesis in the adult hippocampus. Cell Tissue Res 331:243–250. https://doi.org/10.1007/s00441-007-0478-3

    Article  PubMed  Google Scholar 

  29. Quiñones-Hinojosa A, Chaichana K (2007) The human subventricular zone: a source of new cells and a potential source of brain tumors. Exp Neurol 205:313–324. https://doi.org/10.1016/j.expneurol.2007.03.016

    Article  PubMed  Google Scholar 

  30. Kurth F, Zilles K, Fox PT et al (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214:519–534. https://doi.org/10.1007/s00429-010-0255-z

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kurth F, Eickhoff SB, Schleicher A et al (2010) Cytoarchitecture and probabilistic maps of the human posterior insular cortex. Cereb Cortex 20:1448–1461. https://doi.org/10.1093/cercor/bhp208

    Article  PubMed  Google Scholar 

  32. Leu K, Ott GA, Lai A et al (2017) Perfusion and diffusion MRI signatures in histologic and genetic subtypes of WHO grade II-III diffuse gliomas. J Neurooncol 134:177–188. https://doi.org/10.1007/s11060-017-2506-9

    Article  CAS  PubMed  Google Scholar 

  33. Suh CH, Kim HS, Jung SC et al (2018) Imaging prediction of isocitrate dehydrogenase (IDH) mutation in patients with glioma: a systemic review and meta-analysis. Eur Radiol. https://doi.org/10.1007/s00330-018-5608-7

    Article  PubMed  Google Scholar 

  34. Villanueva-Meyer JE, Wood MD, Choi BS et al (2018) MRI features and IDH mutational status of grade II diffuse gliomas: impact on diagnosis and prognosis. AJR Am J Roentgenol 210:621–628. https://doi.org/10.2214/AJR.17.18457

    Article  PubMed  Google Scholar 

  35. Brat DJ, Aldape K, Colman H et al (2018) cIMPACT-NOW update 3: recommended diagnostic criteria for “Diffuse astrocytic glioma, IDH-wildtype, with molecular features of glioblastoma, WHO grade IV. Acta Neuropathol 136:805–810. https://doi.org/10.1007/s00401-018-1913-0

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by grants from Institut National du Cancer (Grant No. INCa-DGOS-Inserm 6038), from the Cancéropôle PACA (Grant No. 2015-02 INSUL802) and the GEFLUC Marseille Provence (Groupement Entreprises Françaises Lutte contre le Cancer—PVM-2014-241). We thank the AP-HM Tumor Bank (Authorization Number: AC2018-31053; CRB BB-0033-00097) for providing tissue samples. We also thank the ARTC-Sud patients’s association (Association pour le Recherche sur les Tumeurs Cérébrales).

Author information

Author notes

  1. Paloma Compes and Emeline Tabouret contributed equally to this publication.

Authors and Affiliations

  1. Aix-Marseille Univ, CNRS UMR 7051, INP, Inst Neurophysiopathol, Marseille, France

    Paloma Compes, Emeline Tabouret, Carole Colin, Romain Appay, Olivier Chinot, Philippe Metellus & Dominique Figarella-Branger

  2. AP-HM, Hôpital de la Timone, Service de Neurochirurgie, Marseille, France

    Paloma Compes & Henry Dufour

  3. AP-HM, Hôpital de la Timone, Service de Neurooncologie, Marseille, France

    Emeline Tabouret & Olivier Chinot

  4. Integrated Functional Genomics and Biomarkers Team, UMR6290, CNRS, Université de Rennes 1, Rennes, France

    Amandine Etcheverry & Jean Mosser

  5. AP-HM, Hôpital de la Timone, Service d’Anatomopathologie, Marseille, France

    Romain Appay & Dominique Figarella-Branger

  6. Université Côte d’Azur and Inria Sophia-Antipolis Méditerranée Asclepios Team, Inria Sophia Antipolis, Sophia Antipolis, France

    Nicolas Cordier & Hervé Delingette

  7. Aix Marseille University UMR CNRS 7339, APHM Timone hospital, Marseille, France

    Nadine Girard

  8. Department of Neurosurgery, Clairval Private Hospital, Ramsay Generale de Sante, 13009, Marseille, France

    Philippe Metellus

Authors
  1. Paloma Compes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emeline Tabouret
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Amandine Etcheverry
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carole Colin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Romain Appay
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nicolas Cordier
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jean Mosser
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Olivier Chinot
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Hervé Delingette
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nadine Girard
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Henry Dufour
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Philippe Metellus
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Dominique Figarella-Branger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dominique Figarella-Branger.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The orignal version of this article has been revised: The format of the authors' names has been corrected.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Compes, P., Tabouret, E., Etcheverry, A. et al. Neuro-radiological characteristics of adult diffuse grade II and III insular gliomas classified according to WHO 2016. J Neurooncol 142, 511–520 (2019). https://doi.org/10.1007/s11060-019-03122-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11060-019-03122-1

Keywords

Search

Navigation