Log in

Extraventricular site indicates higher grade but better prognosis in adult supratentorial ependymomas: a 14-year single-center retrospective cohort

  • Research
  • Published:
Neurosurgical Review Aims and scope Submit manuscript

Abstract

Supratentorial extraventricular ependymoma (STEE) and supratentorial intraventricular ependymoma (STIE) are two subsets of supratentorial ependymoma (SE). These two subsets have similar gene features and only differ in original sites: STEE occurs in the brain parenchyma, and STIE is located in ventricles and surrounded by cerebral spinal fluid. The present study aims to depict the diversities of these two subsets and elucidate the potential effects of the anatomic site on the tumor with the same type, grade, and molecular features. Sixty-six consecutive adult SE patients from 2008 to 2021 were enrolled in our study. Clinical data, pathological features, and long-term outcomes were analyzed retrospectively. Results demonstrated that adult STEE presented with a higher proportion of WHO grade 3 (P = .028) and higher Ki-67 index (≥10%) (P = .019) compared to adult STIE. Survival analysis demonstrated that patients of grade 3 STEE exhibited a significantly longer overall survival (OS) than patients of grade 3 STIE (median OS, 24.4 months vs. 13.0 months; P = .004). Grade 2 (hazard ratio (HR) = 0.217; P < .001) and gross total resection (GTR) (HR = 0.156; P < .001) were identified as favorable prognostic factors for all adult SE. The STEE was also associated with a lesser hazard of death for patients of grade 3 on multivariate analysis (HR = 0.263; P = .047). These findings suggested that the extraventricular site was an indicator for higher grade and better prognosis in adult supratentorial ependymoma.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

All relevant data are available from the corresponding authors on reasonable request.

References

  1. Rudà R, Reifenberger G, Frappaz D, Pfister SM, Laprie A, Santarius T, Roth P, Tonn JC, Soffietti R, Weller M, Moyal EC (2018) EANO guidelines for the diagnosis and treatment of ependymal tumors. Neuro-Oncology 20(4):445–456. https://doi.org/10.1093/neuonc/nox166

    Article  PubMed  Google Scholar 

  2. Dorfer C, Tonn J, Rutka JT (2016) Ependymoma: a heterogeneous tumor of uncertain origin and limited therapeutic options. Handb Clin Neurol 134:417–431. https://doi.org/10.1016/b978-0-12-802997-8.00025-6

    Article  PubMed  Google Scholar 

  3. Vera-Bolanos E, Aldape K, Yuan Y, Wu J, Wani K, Necesito-Reyes MJ, Colman H, Dhall G, Lieberman FS, Metellus P, Mikkelsen T, Omuro A, Partap S, Prados M, Robins HI, Soffietti R, Wu J, Gilbert MR, Armstrong TS, Foundation C (2015) Clinical course and progression-free survival of adult intracranial and spinal ependymoma patients. Neuro-Oncology 17(3):440–447. https://doi.org/10.1093/neuonc/nou162

    Article  PubMed  Google Scholar 

  4. Acquaye AA, Vera E, Gilbert MR, Armstrong TS (2017) Clinical presentation and outcomes for adult ependymoma patients. Cancer 123(3):494–501. https://doi.org/10.1002/cncr.30355

    Article  PubMed  Google Scholar 

  5. Ostrom QT, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS (2021) CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2014–2018. Neuro-Oncology 23(12 Suppl 2):iii1–iii105. https://doi.org/10.1093/neuonc/noab200

    Article  PubMed  PubMed Central  Google Scholar 

  6. Metellus P, Figarella-Branger D, Guyotat J, Barrie M, Giorgi R, Jouvet A, Chinot O, de Neuro-Oncologie C, de la Societe Francaise de N, the Association des Neuro-Oncologues d’'Expression F (2008) Supratentorial ependymomas: prognostic factors and outcome analysis in a retrospective series of 46 adult patients. Cancer 113(1):175–185. https://doi.org/10.1002/cncr.23530

    Article  PubMed  Google Scholar 

  7. Wang Q, Cheng J, Li J, Zhang S, Liu W, Ju Y, Hui X (2020) The survival and prognostic factors of supratentorial cortical ependymomas: a retrospective cohort study and literature-based analysis. Front Oncol 10:1585. https://doi.org/10.3389/fonc.2020.01585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hollon T, Nguyen V, Smith BW, Lewis S, Junck L, Orringer DA (2016) Supratentorial hemispheric ependymomas: an analysis of 109 adults for survival and prognostic factors. J Neurosurg 125(2):410–418. https://doi.org/10.3171/2015.7.Jns151187

    Article  PubMed  Google Scholar 

  9. Amirian ES, Armstrong TS, Aldape KD, Gilbert MR, Scheurer ME (2012) Predictors of survival among pediatric and adult ependymoma cases: a study using Surveillance, Epidemiology, and End Results data from 1973 to 2007. Neuroepidemiology 39(2):116–124. https://doi.org/10.1159/000339320

    Article  PubMed  Google Scholar 

  10. Wu J, Armstrong TS, Gilbert MR (2016) Biology and management of ependymomas. Neuro-Oncology 18(7):902–913. https://doi.org/10.1093/neuonc/now016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Arabzade A, Zhao Y, Varadharajan S, Chen HC, Jessa S, Rivas B, Stuckert AJ, Solis M, Kardian A, Tlais D, Golbourn BJ, Stanton AJ, Chan YS, Olson C, Karlin KL, Kong K, Kupp R, Hu B, Injac SG et al (2021) ZFTA-RELA dictates oncogenic transcriptional programs to drive aggressive supratentorial ependymoma. Cancer Discov 11(9):2200–2215. https://doi.org/10.1158/2159-8290.CD-20-1066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Pajtler KW, Wei Y, Okonechnikov K, Silva PBG, Vouri M, Zhang L, Brabetz S, Sieber L, Gulley M, Mauermann M, Wedig T, Mack N, Imamura Kawasawa Y, Sharma T, Zuckermann M, Andreiuolo F, Holland E, Maass K, Korkel-Qu H et al (2019) YAP1 subgroup supratentorial ependymoma requires TEAD and nuclear factor I-mediated transcriptional programmes for tumorigenesis. Nat Commun 10(1):3914. https://doi.org/10.1038/s41467-019-11884-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Parker M, Mohankumar KM, Punchihewa C, Weinlich R, Dalton JD, Li Y, Lee R, Tatevossian RG, Phoenix TN, Thiruvenkatam R, White E, Tang B, Orisme W, Gupta K, Rusch M, Chen X, Li Y, Nagahawhatte P, Hedlund E et al (2014) C11orf95-RELA fusions drive oncogenic NF-kappaB signalling in ependymoma. Nature 506(7489):451–455. https://doi.org/10.1038/nature13109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Pajtler KW, Witt H, Sill M, Jones DT, Hovestadt V, Kratochwil F, Wani K, Tatevossian R, Punchihewa C, Johann P, Reimand J, Warnatz HJ, Ryzhova M, Mack S, Ramaswamy V, Capper D, Schweizer L, Sieber L, Wittmann A et al (2015) Molecular classification of ependymal tumors across all CNS compartments, histopathological grades, and age groups. Cancer Cell 27(5):728–743. https://doi.org/10.1016/j.ccell.2015.04.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Sun S, Wang J, Zhu M, Beejadhursing R, Gao P, Zhang X, Jiao L, Jiang W, Ke C, Shu K (2018) Clinical, radiological, and histological features and treatment outcomes of supratentorial extraventricular ependymoma: 14 cases from a single center. J Neurosurg 128(5):1396–1402. https://doi.org/10.3171/2017.1.JNS161422

    Article  PubMed  Google Scholar 

  16. Wang M, Zhang R, Liu X, Li D, Qiu C, Zhao P, Zuo Y, Zhang P, Wang J, Sun H (2018) Supratentorial extraventricular ependymomas: a retrospective study focused on long-term outcomes and prognostic factors. Clin Neurol Neurosurg 165:1–6. https://doi.org/10.1016/j.clineuro.2017.12.013

    Article  PubMed  Google Scholar 

  17. Byun J, Kim JH, Kim YH, Cho YH, Hong SH, Kim CJ (2018) Supratentorial extraventricular ependymoma: retrospective analysis of 15 patients at a single institution. World Neurosurg 118:e1–e9. https://doi.org/10.1016/j.wneu.2018.05.192

    Article  PubMed  Google Scholar 

  18. Khatri D, Bhaisora K, Das KK, Pandey S, Sardhara J, Mehrotra A, Srivastava AK, Jaiswal A, Behari S, Kumar R, Jaiswal S (2019) Surgical outcome in cortical ependymoma: a single centre experience of 18 cases. J Clin Neurosci 60:49–57. https://doi.org/10.1016/j.jocn.2018.10.036

    Article  PubMed  Google Scholar 

  19. Shuangshoti S, Rushing EJ, Mena H, Olsen C, Sandberg GD (2005) Supratentorial extraventricular ependymal neoplasms: a clinicopathologic study of 32 patients. Cancer 103(12):2598–2605. https://doi.org/10.1002/cncr.21111

    Article  PubMed  Google Scholar 

  20. Louis DN, Perry A, Wesseling P, Brat DJ, Cree IA, Figarella-Branger D, Hawkins C, Ng HK, Pfister SM, Reifenberger G, Soffietti R, von Deimling A, Ellison DW (2021) The 2021 WHO Classification of Tumors of the Central Nervous System: a summary. Neuro-Oncology 23(8):1231–1251. https://doi.org/10.1093/neuonc/noab106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, Ellison DW (2016) The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta Neuropathol 131(6):803–820. https://doi.org/10.1007/s00401-016-1545-1

    Article  PubMed  Google Scholar 

  22. Metellus P, Guyotat J, Chinot O, Durand A, Barrie M, Giorgi R, Jouvet A, Figarella-Branger D (2010) Adult intracranial WHO grade II ependymomas: long-term outcome and prognostic factor analysis in a series of 114 patients. Neuro-Oncology 12(9):976–984. https://doi.org/10.1093/neuonc/noq047

    Article  PubMed  PubMed Central  Google Scholar 

  23. Thorp N, Gandola L (2019) Management of ependymoma in children, adolescents and young adults. Clin Oncol (Royal College of Radiologists (Great Britain)) 31(3):162–170. https://doi.org/10.1016/j.clon.2018.12.001

    Article  CAS  Google Scholar 

  24. Yaşargil MG, Abdulrauf SI (2008) Surgery of intraventricular tumors. Neurosurgery 62(6 Suppl 3):1029–1040; discussion 1040-1021. https://doi.org/10.1227/01.neu.0000333768.12951.9a

    Article  PubMed  Google Scholar 

  25. John JK, Robin AM, Pabaney AH, Rammo RA, Schultz LR, Sadry NS, Lee IY (2017) Complications of ventricular entry during craniotomy for brain tumor resection. J Neurosurg 127(2):426–432. https://doi.org/10.3171/2016.7.Jns16340

    Article  PubMed  Google Scholar 

  26. Grabb PA, Albright AL, Pang D (1992) Dissemination of supratentorial malignant gliomas via the cerebrospinal fluid in children. Neurosurgery 30(1):64–71. https://doi.org/10.1227/00006123-199201000-00012

    Article  CAS  PubMed  Google Scholar 

  27. Metellus P, Barrie M, Figarella-Branger D, Chinot O, Giorgi R, Gouvernet J, Jouvet A, Guyotat J (2007) Multicentric French study on adult intracranial ependymomas: prognostic factors analysis and therapeutic considerations from a cohort of 152 patients. Brain J Neurol 130(Pt 5):1338–1349. https://doi.org/10.1093/brain/awm046

    Article  Google Scholar 

  28. Reni M, Brandes AA, Vavassori V, Cavallo G, Casagrande F, Vastola F, Magli A, Franzin A, Basso U, Villa E (2004) A multicenter study of the prognosis and treatment of adult brain ependymal tumors. Cancer 100(6):1221–1229. https://doi.org/10.1002/cncr.20074

    Article  PubMed  Google Scholar 

  29. Orringer D, Lau D, Khatri S, Zamora-Berridi GJ, Zhang K, Wu C, Chaudhary N, Sagher O (2012) Extent of resection in patients with glioblastoma: limiting factors, perception of resectability, and effect on survival. J Neurosurg 117(5):851–859. https://doi.org/10.3171/2012.8.Jns12234

    Article  PubMed  Google Scholar 

  30. Niazi TN, Jensen EM, Jensen RL (2009) WHO Grade II and III supratentorial hemispheric ependymomas in adults: case series and review of treatment options. J Neuro-Oncol 91(3):323–328. https://doi.org/10.1007/s11060-008-9717-z

    Article  Google Scholar 

  31. Armstrong TS, Vera-Bolanos E, Bekele BN, Aldape K, Gilbert MR (2010) Adult ependymal tumors: prognosis and the M. D. Anderson Cancer Center experience. Neuro-Oncology 12(8):862–870. https://doi.org/10.1093/neuonc/noq009

    Article  PubMed  PubMed Central  Google Scholar 

  32. Zhao F, Wu T, Wang LM, Zhang J, Zhang H, Li SW, Zhang S, Li P, Wang B, Luo L, Liu PN (2021) Survival and prognostic factors of adult intracranial ependymoma: a single-institutional analysis of 236 patients. Am J Surg Pathol 45(7):979–987. https://doi.org/10.1097/pas.0000000000001669

    Article  PubMed  Google Scholar 

  33. Merchant TE, Bendel AE, Sabin ND, Burger PC, Shaw DW, Chang E, Wu S, Zhou T, Eisenstat DD, Foreman NK, Fuller CE, Anderson ET, Hukin J, Lau CC, Pollack IF, Laningham FH, Lustig RH, Armstrong FD, Handler MH et al (2019) Conformal radiation therapy for pediatric ependymoma, chemotherapy for incompletely resected ependymoma, and observation for completely resected, supratentorial ependymoma. J Clin Oncol Off J Am Soc Clin Oncol 37(12):974–983. https://doi.org/10.1200/jco.18.01765

    Article  CAS  Google Scholar 

  34. Wang X, Han F, Lv Y, Gao J, Du Z, Zhang J (2021) Supratentorial extraventricular ependymomas: imaging features and the added value of apparent diffusion coefficient. J Comput Assist Tomogr 45(3):463–471. https://doi.org/10.1097/rct.0000000000001164

    Article  PubMed  Google Scholar 

  35. Guyotat J, Signorelli F, Desme S, Frappaz D, Madarassy G, Montange MF, Jouvet A, Bret P (2002) Intracranial ependymomas in adult patients: analyses of prognostic factors. J Neuro-Oncol 60(3):255–268. https://doi.org/10.1023/a:1021136029072

    Article  CAS  Google Scholar 

  36. **ong Z, Zhang J, Li Z, Jiang J, Han Q, Sun S, Wu X, Wang Y, Lei T, Chen J (2015) A comparative study of intraventricular central neurocytomas and extraventricular neurocytomas. J Neuro-Oncol 121(3):521–529. https://doi.org/10.1007/s11060-014-1659-z

    Article  CAS  Google Scholar 

  37. Anderson NR, Minutolo NG, Gill S, Klichinsky M (2021) Macrophage-based approaches for cancer immunotherapy. Cancer Res 81(5):1201–1208. https://doi.org/10.1158/0008-5472.Can-20-2990

    Article  CAS  PubMed  Google Scholar 

  38. Noy R, Pollard JW (2014) Tumor-associated macrophages: from mechanisms to therapy. Immunity 41(1):49–61. https://doi.org/10.1016/j.immuni.2014.06.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank the staff from the Department of Neurosurgery, West China Hospital, Sichuan University for their support and for clinical data collection.

Funding

This work was supported by a grant from Sichuan Province Science and Technology Support Program (2017SZ0006 to YL), Post-Doctor Research Project, West China Hospital, Sichuan University (Grant No. 2021HXBH010 to TL and Grant No. 2020HXBH159 to MZ).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. YL, MC, SC, MZ, and TL designed the study. SC, MZ, and TL wrote the manuscript. SC, MZ, SZ, and TL collected and analyzed clinical and follow-up data. NC reviewed the pathological diagnosis of all cases. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Mina Chen or Yanhui Liu.

Ethics declarations

Ethical approval and consent to participate

Clinical data collection and use were performed strictly with ethics regulations and approved by the institutional review board of West China Hospital based on local ethics regulations and the 1964 Helsinki declaration and its later amendments. All patients signed written consent for clinical data collection and use.

Consent for publication

The authors affirm that human research participants provided informed consent for the publication of the images in Fig. 1.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

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

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, S., Zuo, M., Li, T. et al. Extraventricular site indicates higher grade but better prognosis in adult supratentorial ependymomas: a 14-year single-center retrospective cohort. Neurosurg Rev 45, 3771–3778 (2022). https://doi.org/10.1007/s10143-022-01885-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10143-022-01885-2

Keywords

Navigation