Advanced diffusion MRI provides evidence for altered axonal microstructure and gradual peritumoral infiltration in GBM in comparison to brain metastases.

Diffusion Magnetic Resonance Imaging Diffusion Tensor Imaging Glioblastoma Metastasis Radiomics

Journal

Clinical neuroradiology
ISSN: 1869-1447
Titre abrégé: Clin Neuroradiol
Pays: Germany
ID NLM: 101526693

Informations de publication

Date de publication:
29 Apr 2024
Historique:
received: 16 12 2023
accepted: 15 04 2024
medline: 29 4 2024
pubmed: 29 4 2024
entrez: 29 4 2024
Statut: aheadofprint

Résumé

In contrast to peritumoral edema in metastases, GBM is histopathologically characterized by infiltrating tumor cells within the T2 signal alterations. We hypothesized that depending on the distance from the outline of the contrast-enhancing tumor we might reveal imaging evidence of gradual peritumoral infiltration in GBM and predominantly vasogenic edema around metastases. We thus investigated the gradual change of advanced diffusion metrics with the peritumoral zone in metastases and GBM. In 30 patients with GBM and 28 with brain metastases, peritumoral T2 hyperintensity was segmented in 33% partitions based on the total volume beginning at the enhancing tumor margin and divided into inner, middle and outer zones. Diffusion Tensor Imaging (DTI)-derived fractional anisotropy and mean diffusivity as well as Diffusion Microstructure Imaging (DMI)-based parameters Dax-intra, Dax-extra, V‑CSF and V-intra were employed to assess group-wise differences between inner and outer zones as well as within-group gradients between the inner and outer zones. In metastases, fractional anisotropy and Dax-extra were significantly reduced in the inner zone compared to the outer zone (FA p = 0.01; Dax-extra p = 0.03). In GBM, we noted a reduced Dax-extra and significantly lower intraaxonal volume fraction (Dax-extra p = 0.008, V‑intra p = 0.006) accompanied by elevated axial intraaxonal diffusivity in the inner zone (p = 0.035). Between-group comparison of the outer to the inner zones revealed significantly higher gradients in metastases over GBM for FA (p = 0.04) as well as the axial diffusivity in the intra- (p = 0.02) and extraaxonal compartment (p < 0.001). Our findings provide evidence of gradual alterations within the peritumoral zone of brain tumors. These are compatible with predominant (vasogenic) edema formation in metastases, whereas our findings in GBM are in line with an axonal destructive component in the immediate peritumoral area and evidence of tumor cell infiltration with accentuation in the tumor's vicinity.

Identifiants

pubmed: 38683350
doi: 10.1007/s00062-024-01416-0
pii: 10.1007/s00062-024-01416-0
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2024. The Author(s).

Références

Sahm F, Capper D, Jeibmann A, et al. Addressing diffuse glioma as a systemic brain disease with single-cell analysis. Arch Neurol. 2012;69:523–6. https://doi.org/10.1001/archneurol.2011.2910 .
doi: 10.1001/archneurol.2011.2910 pubmed: 22158715
Venkataramani V, Schneider M, Giordano FA, et al. Disconnecting multicellular networks in brain tumours. Nat Rev Cancer. 2022;22:481–91. https://doi.org/10.1038/s41568-022-00475-0 .
doi: 10.1038/s41568-022-00475-0 pubmed: 35488036
Rapp M, Baernreuther J, Turowski B, et al. Recurrence Pattern Analysis of Primary Glioblastoma. World Neurosurg. 2017;103:733–40. https://doi.org/10.1016/j.wneu.2017.04.053 .
doi: 10.1016/j.wneu.2017.04.053 pubmed: 28434963
Haddad AF, Young JS, Morshed RA, Berger MS. FLAIRectomy: Resecting beyond the Contrast Margin for Glioblastoma. Brain Sci. 2022;12:544. https://doi.org/10.3390/brainsci12050544 .
doi: 10.3390/brainsci12050544 pubmed: 35624931 pmcid: 9139350
Lohmann P, Stavrinou P, Lipke K, et al. FET PET reveals considerable spatial differences in tumour burden compared to conventional MRI in newly diagnosed glioblastoma. Eur J Nucl Med Mol Imaging. 2019;46:591–602. https://doi.org/10.1007/s00259-018-4188-8 .
doi: 10.1007/s00259-018-4188-8 pubmed: 30327856
Aparici-Robles F, Davidhi A, Carot-Sierra JM, et al. Glioblastoma versus solitary brain metastasis: MRI differentiation using the edema perfusion gradient. J Neuroimaging. 2022;32:127–33. https://doi.org/10.1111/jon.12920 .
doi: 10.1111/jon.12920 pubmed: 34468052
Blasel S, Jurcoane A, Franz K, et al. Elevated peritumoural rCBV values as a mean to differentiate metastases from high-grade gliomas. Acta Neurochir. 2010;152:1893–9. https://doi.org/10.1007/s00701-010-0774-7 .
doi: 10.1007/s00701-010-0774-7 pubmed: 20799046
Romano A, Moltoni G, Guarnera A, et al. Single brain metastasis versus glioblastoma multiforme: a VOI-based multiparametric analysis for differential diagnosis. Radiol Med. 2022;127:490–7. https://doi.org/10.1007/s11547-022-01480-x .
doi: 10.1007/s11547-022-01480-x pubmed: 35316518 pmcid: 9098536
Lemercier P, Maya SP, Patrie JT, et al. Gradient of Apparent Diffusion Coefficient Values in Peritumoral Edema Helps in Differentiation of Glioblastoma From Solitary Metastatic Lesions. Am J Roentgenol. 2014;203:163–9. https://doi.org/10.2214/AJR.13.11186 .
doi: 10.2214/AJR.13.11186
Caravan I, Ciortea CA, Contis A, Lebovici A. Diagnostic value of apparent diffusion coefficient in differentiating between high-grade gliomas and brain metastases. Acta Radiol. 2018;59:599–605. https://doi.org/10.1177/0284185117727787 .
doi: 10.1177/0284185117727787 pubmed: 28835111
Würtemberger U, Rau A, Reisert M, et al. Differentiation of Perilesional Edema in Glioblastomas and Brain Metastases: Comparison of Diffusion Tensor Imaging, Neurite Orientation Dispersion and Density Imaging and Diffusion Microstructure Imaging. Cancers. 2022;15:129. https://doi.org/10.3390/cancers15010129 .
doi: 10.3390/cancers15010129 pubmed: 36612127 pmcid: 9817519
Novikov DS. The present and the future of microstructure MRI: From a paradigm shift to normal science. J Neurosci Methods. 2021;351:108947. https://doi.org/10.1016/j.jneumeth.2020.108947 .
doi: 10.1016/j.jneumeth.2020.108947 pubmed: 33096152
Jiang R, Du F‑Z, He C, et al. The Value of Diffusion Tensor Imaging in Differentiating High-Grade Gliomas from Brain Metastases: A Systematic Review and Meta-Analysis. Plos One. 2014;9:e112550. https://doi.org/10.1371/journal.pone.0112550 .
doi: 10.1371/journal.pone.0112550 pubmed: 25380185 pmcid: 4224505
Mao J, Zeng W, Zhang Q, et al. Differentiation between high-grade gliomas and solitary brain metastases: a comparison of five diffusion-weighted MRI models. BMC Med Imaging. 2020;20:124. https://doi.org/10.1186/s12880-020-00524-w .
doi: 10.1186/s12880-020-00524-w pubmed: 33228564 pmcid: 7684933
Byrnes TJD, Barrick TR, Bell BA, Clark CA. Diffusion tensor imaging discriminates between glioblastoma and cerebral metastases in vivo. NMR Biomed. 2011;24:54–60. https://doi.org/10.1002/nbm.1555 .
doi: 10.1002/nbm.1555 pubmed: 20665905
Tsougos I, Svolos P, Kousi E, et al. Differentiation of glioblastoma multiforme from metastatic brain tumor using proton magnetic resonance spectroscopy, diffusion and perfusion metrics at 3 T. Cancer Imaging. 2012;12:423–36. https://doi.org/10.1102/1470-7330.2012.0038 .
doi: 10.1102/1470-7330.2012.0038 pubmed: 23108208 pmcid: 3494384
Wang W, Steward CE, Desmond PM. Diffusion Tensor Imaging in Glioblastoma Multiforme and Brain Metastases: The Role of p , q , L , and Fractional Anisotropy. AJNR Am J Neuroradiol. 2009;30:203–8. https://doi.org/10.3174/ajnr.A1303 .
doi: 10.3174/ajnr.A1303 pubmed: 18842762 pmcid: 7051698
Reisert M, Kellner E, Dhital B, et al. Disentangling micro from mesostructure by diffusion MRI: A Bayesian approach. Neuroimage. 2017;147:964–75. https://doi.org/10.1016/j.neuroimage.2016.09.058 .
doi: 10.1016/j.neuroimage.2016.09.058 pubmed: 27746388
Rau A, Reisert M, Kellner E, et al. Increased interstitial fluid in periventricular and deep white matter hyperintensities in patients with suspected idiopathic normal pressure hydrocephalus. Sci Rep. 2021;11:19552. https://doi.org/10.1038/s41598-021-98054-0 .
doi: 10.1038/s41598-021-98054-0 pubmed: 34599204 pmcid: 8486779
Würtemberger U, Diebold M, Erny D, et al. Diffusion Microstructure Imaging to Analyze Perilesional T2 Signal Changes in Brain Metastases and Glioblastomas. Cancers. 2022;14:1155. https://doi.org/10.3390/cancers14051155 .
doi: 10.3390/cancers14051155 pubmed: 35267463 pmcid: 8908999
Demerath T, Donkels C, Reisert M, et al. Gray-White Matter Blurring of the Temporal Pole Associated With Hippocampal Sclerosis: A Microstructural Study Involving 3 T MRI and Ultrastructural Histopathology. Cerebral Cortex bhab320. 2021. https://doi.org/10.1093/cercor/bhab320 ..
Rau A, Schroeter N, Blazhenets G, et al. Widespread white matter oedema in subacute COVID-19 patients with neurological symptoms. Brain. 2022;145:3203–13. https://doi.org/10.1093/brain/awac045 .
doi: 10.1093/brain/awac045 pubmed: 35675908
Rau A, Jost WH, Demerath T, et al. Diffusion microstructure imaging in progressive supranuclear palsy: reduced axonal volumes in the superior cerebellar peduncles, dentato-rubro-thalamic tracts, ventromedial thalami, and frontomesial white matter. Cerebral Cortex. bhac, Vol. 041. 2022. https://doi.org/10.1093/cercor/bhac041 .
doi: 10.1093/cercor/bhac041
Veraart J, Novikov DS, Christiaens D, et al. Denoising of diffusion MRI using random matrix theory. Neuroimage. 2016;142:394–406. https://doi.org/10.1016/j.neuroimage.2016.08.016 .
doi: 10.1016/j.neuroimage.2016.08.016 pubmed: 27523449
Kellner E, Dhital B, Kiselev VG, Reisert M. Gibbs-ringing artifact removal based on local subvoxel-shifts: Gibbs-Ringing Artifact Removal. Magn Reson. Med, Vol. 76. 2016. pp. 1574–81. https://doi.org/10.1002/mrm.26054 .
doi: 10.1002/mrm.26054
Latysheva A, Geier OM, Hope TR, et al. Diagnostic utility of Restriction Spectrum Imaging in the characterization of the peritumoral brain zone in glioblastoma: Analysis of overall and progression-free survival. Eur J Radiol. 2020;132:109289. https://doi.org/10.1016/j.ejrad.2020.109289 .
doi: 10.1016/j.ejrad.2020.109289 pubmed: 33002815
Rees JH, Smirniotopoulos JG, Jones RV, Wong K. Glioblastoma multiforme: radiologic-pathologic correlation. Radiographics. 1996;16:1413–38.
doi: 10.1148/radiographics.16.6.8946545 pubmed: 8946545
Berghoff AS, Rajky O, Winkler F, et al. Invasion patterns in brain metastases of solid cancers. Neuro Oncol. 2013;15:1664–72. https://doi.org/10.1093/neuonc/not112 .
doi: 10.1093/neuonc/not112 pubmed: 24084410 pmcid: 3829586
Fisher E, Chang A, Fox RJ, et al. Imaging correlates of axonal swelling in chronic multiple sclerosis brains. Ann Neurol. 2007;62:219–28. https://doi.org/10.1002/ana.21113 .
doi: 10.1002/ana.21113 pubmed: 17427920
Kellner E, Reisert M, Rau A, et al. Clinical feasibility of diffusion microstructure imaging (DMI) in acute ischemic stroke. Neuroimage: Clin. 2022;36:103189. https://doi.org/10.1016/j.nicl.2022.103189 .
doi: 10.1016/j.nicl.2022.103189 pubmed: 36126516
Ware AL, Yeates KO, Tang K, et al. Longitudinal white matter microstructural changes in pediatric mild traumatic brain injury: An A‑CAP study. Hum Brain Mapp. 2022;43:3809–23. https://doi.org/10.1002/hbm.25885 .
doi: 10.1002/hbm.25885 pubmed: 35467058 pmcid: 9294335
Tamura R, Ohara K, Sasaki H, et al. Histopathological vascular investigation of the peritumoral brain zone of glioblastomas. J Neurooncol. 2018;136:233–41. https://doi.org/10.1007/s11060-017-2648-9 .
doi: 10.1007/s11060-017-2648-9 pubmed: 29188530
De Gooijer MC, Guillén Navarro M, Bernards R, et al. An Experimenter’s Guide to Glioblastoma Invasion Pathways. Trends Mol Med. 2018;24:763–80. https://doi.org/10.1016/j.molmed.2018.07.003 .
doi: 10.1016/j.molmed.2018.07.003 pubmed: 30072121

Auteurs

U Würtemberger (U)

Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany. urs.wuertemberger@uniklinik-freiburg.de.
Dept. of Neuroradiology, University Medical Center Freiburg, Breisacher Str. 64, 79106, Freiburg, Germany. urs.wuertemberger@uniklinik-freiburg.de.

A Rau (A)

Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.
Department of Diagnostic and Interventional Radiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

M Diebold (M)

Institute of Neuropathology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

L Becker (L)

Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

M Hohenhaus (M)

Department of Neurosurgery, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

J Beck (J)

Department of Neurosurgery, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

P C Reinacher (PC)

Department of Neurosurgery, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.
Fraunhofer Institute for Laser Technology, 52074, Aachen, Germany.

D Erny (D)

Institute of Neuropathology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

M Reisert (M)

Department of Medical Physics, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.
Department of Stereotactic and Functional Neurosurgery, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

H Urbach (H)

Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

T Demerath (T)

Department of Neuroradiology, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany.

Classifications MeSH