Skip to main content

Advertisement

Log in

The diagnostic value of contrast enhancement on MRI in diffuse and anaplastic gliomas

  • Original Article - Tumor - Glioma
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Purpose

We evaluated differentiations in gadolinium contrast enhancement (CE) between low-grade WHO °II and high-grade WHO °III gliomas in conventional MRI, which have been repeatedly questioned.

Methods

Ninety-nine patients, who underwent first resection of WHO°II and °III gliomas, were retrospectively retrieved from a prospective database. The quantitative metric volume of Gd-CE in T1-weighted pre-operative MRI was measured using volumetric segmentation.

Results

The OR to detect CE in anaplastic gliomas was seven times higher than that in diffuse gliomas (CI95% 2.8–17.2, p<0.0001). No CE was seen in 50% (8/16) of focal anaplastic and in 28% (10/36) of entirely anaplastic gliomas. CE was present in 21% (10/47) of diffuse gliomas. Anaplasia correlated with a larger CE volume (r=0.49, p<0.0001) and provided additional 4 cmof CE volume compared to entirely diffuse tumors. The OR to have CE was 3.6 times for IDH1 wild-type tumors (CI95% 1.3–10.2, p=0.05) and 4.8 for tumors with ATRX expression (CI95% 1.3–17.2, p=0.05). In all sub-groups, at least a quarter of cases showed no CE at all and there were cases with present CE.

Conclusion

CE is associated with higher odds of unfavorable prognostic features like anaplasia, wild-type IDH1 and retained ATRX. There was no CE in one-fourth of anaplastic gliomas and half of gliomas with focal anaplasia.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Availability of data and material

The raw data was generated in the authors’ institution. The data that support the findings of this study are available on reasonable request from the corresponding author. The data are not publicly available due their containing information that could compromise the privacy of research participants.

References

  1. Barker FG, 2nd, Chang SM, Huhn SL, Davis RL, Gutin PH, McDermott MW, Wilson CB, Prados MD199 Age and the risk of anaplasia in magnetic resonance-nonenhancing supratentorial cerebral tumors. Cancer 80:936–941

  2. Bender Multiple test procedures other than Bonferroni’s deserve wider use.

  3. Claus EB, Walsh KM, Wiencke JK, Molinaro AM, Wiemels JL, Schildkraut JM, Bondy ML, Berger M, Jenkins R, Wrensch M (2015) Survival and low-grade glioma: the emergence of genetic information. Neurosurg Focus 38:E6. https://doi.org/10.3171/2014.10.FOCUS12367

    Article  PubMed  PubMed Central  Google Scholar 

  4. Daumas-Duport C, Scheithauer B, O’Fallon J, Kelly P (1988) Grading of astrocytomas. A simple and reproducible method Cancer 62:2152–2165. https://doi.org/10.1002/1097-0142(19881115)62:10%3c2152::aid-cncr2820621015%3e3.0.co;2-t

    Article  CAS  PubMed  Google Scholar 

  5. Editors PO 2019 Retraction: EGFR inhibition in glioma cells modulates rho signaling to inhibit cell motility and invasion and cooperates with temozolomide to reduce cell growth. PLoS One 14:e0222210. https://doi.org/10.1371/journal.pone.0222210

  6. Eichberg DG, Di L, Morell AA, Shah AH, Semonche AM, Chin CN, Bhatia RG, Jamshidi AM, Luther EM, Komotar RJ, Ivan ME (2020) Incidence of high grade gliomas presenting as radiographically non-enhancing lesions: experience in 111 surgically treated non-enhancing gliomas with tissue diagnosis. J Neurooncol 147:671–679. https://doi.org/10.1007/s11060-020-03474-z

    Article  PubMed  Google Scholar 

  7. Furnari FB, Fenton T, Bachoo RM, Mukasa A, Stommel JM, Stegh A, Hahn WC, Ligon KL, Louis DN, Brennan C, Chin L, DePinho RA, Cavenee WK (2007) Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev 21:2683–2710. https://doi.org/10.1101/gad.1596707

    Article  CAS  PubMed  Google Scholar 

  8. Gargini R, Segura-Collar B, Herranz B, Garcia-Escudero V, Romero-Bravo A, Nunez FJ,  Garcia-Perez D,  Gutierrez-Guaman J,  Ayuso-Sacido A, Seoane J, Perez-Nunez A, Sepulveda-Sanchez JM, Hernandez-Lain A, Castro MG, Garcia-Escudero R, Avila J, Sanchez-Gomez P 2020 The IDH-TAU-EGFR triad defines the neovascular landscape of diffuse gliomas SciTransl Med 12 https://doi.org/10.1126/scitranslmed.aax1501

  9. Ginsberg LE, Fuller GN, Hashmi M, Leeds NE, Schomer DF (1998) The significance of lack of MR contrast enhancement of supratentorial brain tumors in adults: histopathological evaluation of a series. Surg Neurol 49:436–440. https://doi.org/10.1016/s0090-3019(97)00360-1

    Article  CAS  PubMed  Google Scholar 

  10. Guillevin R, Herpe G, Verdier M, Guillevin C (2014) Low-grade gliomas: the challenges of imaging. Diagn Interv Imaging 95:957–963. https://doi.org/10.1016/j.diii.2014.07.005

    Article  CAS  PubMed  Google Scholar 

  11. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70

    Google Scholar 

  12. Kondziolka D, Lunsford LD, Martinez AJ (1993) Unreliability of contemporary neurodiagnostic imaging in evaluating suspected adult supratentorial (low-grade) astrocytoma. J Neurosurg 79:533–536. https://doi.org/10.3171/jns.1993.79.4.0533

    Article  CAS  PubMed  Google Scholar 

  13. Larsen J, Wharton SB, McKevitt F, Romanowski C, Bridgewater C, Zaki H, Hoggard N (2017) “Low grade glioma”: an update for radiologists. Br J Radiol 90:20160600. https://doi.org/10.1259/bjr.20160600

    Article  PubMed  PubMed Central  Google Scholar 

  14. Louis DN, Ohgaki H, Wiestler O, Cavenee WK 2016 WHO classification of tumours of the central nervous system, vol 1. Revised 4th Edition edn. International Agency for Research on Cancer,

  15. 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 131:803–820. https://doi.org/10.1007/s00401-016-1545-1

    Article  PubMed  Google Scholar 

  16. Mihara F, Numaguchi Y, Rothman M, Kristt D, Fiandaca M, Swallow L (1995) Non-enhancing supratentorial malignant astrocytomas: MR features and possible mechanisms. Radiat Med 13:11–17

    CAS  PubMed  Google Scholar 

  17. Minniti G, Lombardi G, Paolini S 2019 Glioblastoma in elderly patients: current management and future perspectives Cancers (Basel) 11 https://doi.org/10.3390/cancers11030336

  18. Montagne A, Toga AW, Zlokovic BV (2016) Blood-brain barrier permeability and gadolinium: benefits and potential pitfalls in research. JAMA Neurol 73:13–14. https://doi.org/10.1001/jamaneurol.2015.2960

    Article  PubMed  PubMed Central  Google Scholar 

  19. Olar A, Wani KM, Alfaro-Munoz KD, Heathcock LE, van Thuijl HF, Gilbert MR, Armstrong TS, Sulman EP, Cahill DP, Vera-Bolanos E, Yuan Y, Reijneveld JC, Ylstra B, Wesseling P, Aldape KD (2015) IDH mutation status and role of WHO grade and mitotic index in overall survival in grade II-III diffuse gliomas. Acta Neuropathol 129:585–596. https://doi.org/10.1007/s00401-015-1398-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ostrom QT, Patil N, Cioffi G, Waite K, Kruchko C, Barnholtz-Sloan JS 2020 CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2013–2017. Neuro Oncol 22:iv1-iv96. https://doi.org/10.1093/neuonc/noaa200

  21. Pallud J, Capelle L, Taillandier L, Fontaine D, Mandonnet E, Guillevin R, Bauchet L, Peruzzi P, Laigle-Donadey F, Kujas M, Guyotat J, Baron MH, Mokhtari K, Duffau H (2009) Prognostic significance of imaging contrast enhancement for WHO grade II gliomas. Neuro Oncol 11:176–182. https://doi.org/10.1215/15228517-2008-066

    Article  PubMed  PubMed Central  Google Scholar 

  22. Provenzale JM, Mukundan S, Dewhirst M (2005) The role of blood-brain barrier permeability in brain tumor imaging and therapeutics. AJR Am J Roentgenol 185:763–767. https://doi.org/10.2214/ajr.185.3.01850763

    Article  PubMed  Google Scholar 

  23. Qi S, Yu L, Li H, Ou Y, Qiu X, Ding Y, Han H, Zhang X (2014) Isocitrate dehydrogenase mutation is associated with tumor location and magnetic resonance imaging characteristics in astrocytic neoplasms. Oncol Lett 7:1895–1902. https://doi.org/10.3892/ol.2014.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Reuss DE, Mamatjan Y, Schrimpf D, Capper D, Hovestadt V, Kratz A, Sahm F, Koelsche C, Korshunov A, Olar A, Hartmann C, Reijneveld JC, Wesseling P, Unterberg A, Platten M, Wick W, Herold-Mende C, Aldape K, von Deimling A (2015) IDH mutant diffuse and anaplastic astrocytomas have similar age at presentation and little difference in survival: a grading problem for WHO. Acta Neuropathol 129:867–873. https://doi.org/10.1007/s00401-015-1438-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Scott JN, Brasher PM, Sevick RJ, Rewcastle NB, Forsyth PA (2002) How often are nonenhancing supratentorial gliomas malignant? A population study. Neurology 59:947–949. https://doi.org/10.1212/wnl.59.6.947

    Article  CAS  PubMed  Google Scholar 

  26. Segura-Collar B, Gargini R, Tovar-Ambel E, Hernandez-SanMiguel E, Epifano C, Perez de Castro I, Hernandez-Lain A, Casas-Tinto S, Sanchez-Gomez P 2020 The EGFR-TMEM167A-p53 axis defines the aggressiveness of gliomas Cancers (Basel) 12 https://doi.org/10.3390/cancers12010208

  27. Sharma HS, Muresanu DF, Castellani RJ, Nozari A, Lafuente JV, Tian ZR, Sahib S, Bryukhovetskiy I, Bryukhovetskiy A, Buzoianu AD, Patnaik R, Wiklund L, Sharma A (2020) Pathophysiology of blood-brain barrier in brain tumor. Novel therapeutic advances using nanomedicine. Int Rev Neurobiol 151:1–66. https://doi.org/10.1016/bs.irn.2020.03.001

    Article  CAS  PubMed  Google Scholar 

  28. Suchorska B, Schuller U, Biczok A, Lenski M, Albert NL, Giese A, Kreth FW, Ertl-Wagner B, Tonn JC, Ingrisch M (2019) Contrast enhancement is a prognostic factor in IDH1/2 mutant, but not in wild-type WHO grade II/III glioma as confirmed by machine learning. Eur J Cancer 107:15–27. https://doi.org/10.1016/j.ejca.2018.10.019

    Article  CAS  PubMed  Google Scholar 

  29. Wang YY, Wang K, Li SW, Wang JF, Ma J, Jiang T, Dai JP (2015) Patterns of tumor contrast enhancement predict the prognosis of anaplastic gliomas with IDH1 mutation. AJNR Am J Neuroradiol 36:2023–2029. https://doi.org/10.3174/ajnr.A4407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Weller M, van den Bent M, Preusser M, Le Rhun E, Tonn JC, Minniti G, Bendszus M, Balana C, Chinot O, Dirven L, French P, Hegi ME, Jakola AS, Platten M, Roth P, Ruda R, Short S, Smits M, Taphoorn MJB, von Deimling A, Westphal M, Soffietti R, Reifenberger G, Wick W (2020) EANO guidelines on the diagnosis and treatment of diffuse gliomas of adulthood. Nat Rev Clin Oncol. https://doi.org/10.1038/s41571-020-00447-z

    Article  PubMed  PubMed Central  Google Scholar 

  31. White ML, Zhang Y, Kirby P, Ryken TC (2005) Can tumor contrast enhancement be used as a criterion for differentiating tumor grades of oligodendrogliomas? Am J Neuroradiol 26:784–790

    PubMed  PubMed Central  Google Scholar 

  32. Wiestler B, Capper D, Holland-Letz T, Korshunov A, von Deimling A, Pfister SM, Platten M, Weller M, Wick W (2013) ATRX loss refines the classification of anaplastic gliomas and identifies a subgroup of IDH mutant astrocytic tumors with better prognosis. Acta Neuropathol 126:443–451. https://doi.org/10.1007/s00401-013-1156-z

    Article  CAS  PubMed  Google Scholar 

  33. Yushkevich PA, Pashchinskiy A, Oguz I, Mohan S, Schmitt JE, Stein JM, Zukic D, Vicory J, McCormick M, Yushkevich N, Schwartz N, Gao Y, Gerig G (2019) User-guided segmentation of multi-modality medical imaging datasets with ITK-SNAP. Neuroinformatics 17:83–102. https://doi.org/10.1007/s12021-018-9385-x

    Article  PubMed  PubMed Central  Google Scholar 

  34. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G (2006) User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31:1116–1128. https://doi.org/10.1016/j.neuroimage.2006.01.015

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization, A.K. and C.F.F.; methodology, A.K. and C.F.F.; software, M.D. and A.K.; validation, A.K. and C.F.F..; formal analysis, A.K.; investigation, A.K. and M.D.; resources, C.F.F., C.T. and A.G.; data curation, A.K. and M.D.; writing—original draft preparation, A.K. and M.D.; writing—review and editing, C.F.F, C.T and A.G.; supervision, C.F.F and C.T.; project administration, A.K. and C.F.F. All the authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Aleksandrs Krigers.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethics approval

All the 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. The study was approved by the Bioethics Committee of the Medical University of Innsbruck (AN5220 329/4.4, EK Nr. 1333/2021).

Consent to participate

Informed consent was obtained from all individual participants included in the study (AN5220 329/4.4).

Consent to publication

No individual data is showed separately in the manuscript. All data are used only after anonymized statistical processing and are described with pool results.

Additional information

Publisher’s note

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

This article is part of the Topical Collection on Tumor - Glioma

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Krigers, A., Demetz, M., Grams, A.E. et al. The diagnostic value of contrast enhancement on MRI in diffuse and anaplastic gliomas. Acta Neurochir 164, 2035–2040 (2022). https://doi.org/10.1007/s00701-021-05103-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-021-05103-8

Keywords

Navigation