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Proton MR spectroscopy shows improved performance to segregate high-grade astrocytoma subgroups when defined with the new 2021 World Health Organization classification of central nervous system tumors

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Abstract

Objectives

The 2021 World Health Organization (WHO) classification of central nervous system (CNS) tumors prioritizes isocitrate dehydrogenase (IDH) mutation to define tumor types in diffuse gliomas, in contrast to the 2016 classification, which prioritized histological features. Our objective was to investigate the influence of this change in the performance of proton MR spectroscopy (1H-MRS) in segregating high-grade diffuse astrocytoma subgroups.

Methods

Patients with CNS WHO grade 3 and 4 diffuse astrocytoma, known IDH mutation status, and available 1H-MRS were retrospectively retrieved and divided into 4 groups based on IDH mutation status and histological grade. Differences in 1H-MRS between groups were analyzed with the Kruskal–Wallis test. The points on the spectrum that showed the greatest differences were chosen to evaluate the performance of 1H-MRS in discriminating between grades 3 and 4 tumors (WHO 2016 defined), and between IDH-mutant and IDH-wildtype tumors (WHO 2021). ROC curves were constructed with these points, and AUC values were calculated and compared.

Results

The study included 223 patients with high-grade diffuse astrocytoma. Discrimination between IDH-mutant and IDH-wildtype tumors showed higher AUC values (highest AUC short TE, 0.943; long TE, 0.864) and more noticeable visual differences than the discrimination between grade 3 and 4 tumors (short TE, 0.885; long TE, 0.838).

Conclusion

Our findings suggest that 1H-MRS is more applicable to classify high-grade astrocytomas defined with the 2021 criteria. Improved metabolomic robustness and more homogeneous groups yielded better tumor type discrimination by 1H-MRS with the new criteria.

Clinical relevance statement

The 2021 World Health Organization classification of brain tumors empowers molecular criteria to improve tumor characterization. This derives in greater segregation of high-grade diffuse astrocytoma subgroups by MR spectroscopy and warrants further development of brain tumor classification tools with spectroscopy.

Key Points

• The new 2021 updated World Health Organization classification of central nervous system tumors maximizes the role of molecular diagnosis in the classification of brain tumors.

• Proton MR spectroscopy performs better to segregate high-grade astrocytoma subgroups when defined with the new criteria.

• The study provides additional evidence of improved metabolic characterization of brain tumor subgroups with the new criteria.

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Abbreviations

1H-MRS:

Proton MR spectroscopy

CNS:

Central nervous system

IDH:

Isocitrate dehydrogenase

WHO:

World Health Organization

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Acknowledgements

Co-funded by European Regional Development Fund. ERDF, a way to build Europe. We thank CERCA Programme/Generalitat de Catalunya for institutional support.

Funding

This work has received funding by the Spanish Ministry of Health, Instituto de Salud Carlos III (ISCIII) (PI20/00360).

Author information

Authors and Affiliations

  1. Radiology Department, Institut deDiagnòstic Per LaImatge (IDI), Hospital Universitari de Bellvitge, L’Hospitalet de Llobregat, Barcelona, Spain

    Carles Majós, Albert Pons-Escoda, Pablo Naval, Anna Güell & Mònica Cos

  2. Neurooncology Unit, Institutd’InvestigacióBiomèdica deBellvitge-IDIBELL, L’Hospitalet de Llobregat, Barcelona, Spain

    Carles Majós, Albert Pons-Escoda, Anna Lucas, Noemí Vidal & Jordi Bruna

  3. Centro de Investigación Biomédica en Red, BioingenieríaBiomateriales y Nanomedicina (CIBER-BBN), Cerdanyola del Vallès, Spain

    Carles Majós

  4. Radiation Oncology Department, Institut Català d’Oncologia (ICO), Hospital Universitari de Bellvitge, L’Hospitalet de Llobregat, Barcelona, Spain

    Anna Lucas

  5. Pathology Department, Hospital Universitari de Bellvitge, L’Hospitalet de Llobregat, Barcelona, Spain

    Noemí Vidal

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  1. Carles Majós
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  2. Albert Pons-Escoda
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Corresponding author

Correspondence to Carles Majós.

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Guarantor

The scientific guarantor of this publication is Carles Majós.

Conflict of interest

Albert Pons-Escoda is a member of the European Radiology Editorial Board. They have not taken part in the review or selection process of this article.

The other authors of this manuscript declare no relationships with any companies, whose products or services may be related to the subject matter of the article.

Statistics and biometry

No complex statistical methods were necessary for this paper.

Informed consent

Written informed consent was waived by the Institutional Review Board.

Ethical approval

Institutional Review Board approval was obtained.

Study subjects or cohorts overlap

Some study subjects or cohorts have been previously reported in:

1. Majós C, Bruna J, Julià-Sapé M, Cos M, Camins A, Gil M, Acebes JJ, Aguilera C, Arús C (2011) Proton magnetic resonance spectroscopy provides relevant prognostic information in high-grade astrocytomas. AJNR Am J Neuroradiol 32:74–80.

2. Julià-Sapé M, Coronel I, Majós C, Candiota AP, Serrallonga M, Cos M, Aguilera C, Acebes JJ, Griffiths JR, Arús C (2012) Prospective diagnostic performance evaluation of SV-1H-MRS for ty** and grading brain tumours. NMR Biomed 25:661–673.

3. Julià-Sapé M, Majós C, Camins A, Samitier A, Baquero M, Serrallonga M, Domènech S, Grivé E, Howe F, Opstad K, Calvar J, Aguilera C, Arús C (2014) Multicentre evaluation of the INTERPRET decisión-support system 2.0 for brain tumour classification. NMR Biomed 27:1009–1028.

4. Mora P, Majós C, Castañer S, Sánchez JJ, Gabarrós A, Muntané A, Aguilera C, Arús C (2014) 1H-MRS can be used to reinforce the suspicion of primary central nervous system lymphoma prior to surgery. Eur Radiol 24:2895–2905.

Methodology

• retrospective

• observational

• performed at one institution

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Carles Majós and Albert Pons-Escoda have contributed equally and are co-first authors of the manuscript.

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Majós, C., Pons-Escoda, A., Naval, P. et al. Proton MR spectroscopy shows improved performance to segregate high-grade astrocytoma subgroups when defined with the new 2021 World Health Organization classification of central nervous system tumors. Eur Radiol 34, 2174–2182 (2024). https://doi.org/10.1007/s00330-023-10138-9

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