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

Clinical Neuroradiology, vol. 34, pp. 703–711

Abstract

PURPOSE: 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. METHODS: 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. RESULTS: 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). CONCLUSION: 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.

Authors 11

1. Urs Würtemberger corresponding

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

   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

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

2. Alexander Rau

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

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

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

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

3. Martin Diebold

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

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

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

4. L. E. Becker

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

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

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

5. Marc Hohenhaus

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

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

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

6. Jürgen Beck

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

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

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

7. Peter Christoph Reinacher Aachen Fraunhofer Institute for Laser Technology (ILT)

   University of Freiburg · University Medical Center Freiburg · Fraunhofer Institute for Laser Technology

   Affiliation as printed

   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

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

8. Daniel Erny

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

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

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

9. Marco Reisert

   University of Freiburg · University Medical Center Freiburg

   Affiliation as printed

   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

   Department of Medical Physics, Medical Center—University of Freiburg, Faculty of Medicine, University of Freiburg, 79106, Freiburg, Germany

10. Horst Urbach

    University of Freiburg · University Medical Center Freiburg

    Affiliation as printed

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

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

11. Theo Demerath

    University of Freiburg · University Medical Center Freiburg

    Affiliation as printed

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

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