Changes in fiber integrity, diffusivity, and metabolism of the pyramidal tract adjacent to gliomas: a quantitative diffusion tensor fiber tracking and MR spectroscopic imaging study

Abstract

Background and purpose: The underlying changes in the neuronal connectivity adjacent to brain tumors cannot always be depicted by conventional MR imaging. The hypothesis of this study was that preoperative sensorimotor deficits are associated with impairment in pyramidal fiber bundles. Hence, we investigated the potential of combined quantitative diffusion tensor (DT) fiber tracking and MR spectroscopic imaging (MRSI) to determine changes in the pyramidal tract adjacent to gliomas.

Materials and methods: Quantitative DT fiber tracking and proton MRSI were performed in 20 patients with gliomas with WHO grades II-IV. Eight patients experienced preoperative sensorimotor deficits. Mean diffusivity (MD), fractional anisotropy (FA), and number of fibers per voxel (FpV) were calculated for the pyramidal tract of the ipsilateral and contralateral hemisphere. Metabolite concentrations for choline-containing compounds (Cho), creatine (Cr), and N-acetylaspartate (NAA) were computed, using LCModel, for all voxels located at the pyramidal tracts.

Results: For the whole pyramidal tract, quantitative DT fiber tracking resulted in significantly lower FpV and FA values (P < .001), but not MD values, for the ipsilateral hemisphere. For the section of the fiber bundle closest to the lesion, we found significantly decreased FpV and FA (P < .001) and increased MD (P = .002). MRSI showed, for the same volumes of interest, significantly decreased NAA (P = .001), increased Cho (P = .034) and Cho/NAA (P = .001) for the ipsilateral pyramidal tract. In patients suffering sensorimotor deficits, we found significantly lower FA (P = .022) and higher MD values (P = .026) and a strongly negative correlation between FA and MD (R = -0.710, P = .024) but no correlation in patients without deficits (R = 0.078, ns).

Conclusion: Quantitative DTI was able to show significant differences in diffusivity of the pyramidal tract in patients with sensorimotor deficits in relation to patients without them. The additional use of proton MRSI may be helpful to discern whether these diffusivity changes in fiber tracts are caused by tumor infiltration or peritumoral edema.

Fig 1.

Results of the fiber-tracking procedure of the DTI data and the spectral analysis of the MRSI data for a patient having no sensorimotor deficits (patient 17 in Table 1). Screenshot from the planning workstation of a navigation system of an axial T2-weighted MR imaging (A) coregistered with a segmented metabolic Cho/NAA map (C). Overlaid on these images are the cross sections of the ipsilateral (blue) and contralateral (magenta) pyramidal tracts, the tumor segmented manually by a neurosurgeron (yellow), and the VOI (PRESS-box) of the MRSI experiment (white rectangle). B, a 3D reconstruction of the ipsilateral (blue) and contralateral (magenta) pyramidal tracts depicted on the axial sections of the DTI dataset measured with a b-value = 0 s/mm². LCModel fits (red line) of the MRSI data of voxel position 1 (D) and 2 (E) as depicted in C as white squares. Overlaid on these images are the molar concentrations for Cho, Cr, and NAA calculated by LCModel.

Fig 2.

Results of the fiber-tracking procedure of the DTI data and the spectral analysis of the MRSI data for a patient with a hypesthesia in right arm (patient 14 in Table 1). Screenshot from the planning workstation of a navigation system of an axial T2-weighted MR imaging (A) coregistred with a segmented metabolic Cho/NAA map (C). Overlaid on these images are the cross sections of the ipsilateral (blue) and contralateral (magenta) pyramidal tracts, the tumor segmented manually by a neurosurgeon (green), and the PRESS-box of the MRSI experiment (white rectangle). B, a 3D reconstruction of the ipsilateral (blue) and contralateral (magenta) pyramidal tracts depicted on the axial sections of the DTI dataset measured with a b-value = 0 s/mm². LCModel fits (red line) of the MRSI data of voxel positions 1 (D) and 2 (E) as depicted in C as white squares. Overlaid on these images are the molar concentrations for Cho, Cr, and NAA calculated by LCModel.

Fig 3.

Shown are boxplots of FpV, FA, and MD values of the whole ipsilateral and contralateral pyramidal tracts (A, B, and C, respectively). The horizontal lines are the medians, and the ends of the boxes are the lower and upper quartiles (25th and 75th percentiles). MD values are expressed in units × 10⁻³ mm²/s. The error bars depict the SD. Overlaid are the P values calculated from a 2-sided paired t test (ns = not significant).

Fig 4.

Shown are boxplots of FpV, FA, and MD values for the section of the ipsilateral and contralateral pyramidal tracts (A, B, and C, respectively) corresponding with the MRSI section, respectively. Boxplots of molar concentrations of NAA, Cho, and the Cho/NAA ratio averaged over voxel positions located at the ipsilateral and contralateral pyramidal tract cross sections (D, E, and F, respectively). MD values are expressed in units × 10⁻³ mm²/s. NAA and Cho values are are expressed in millimoles per liter. Overlaid are the P values calculated from a 2-sided paired t test.

Fig 5.

Boxplots of FpV, FA, and MD values of the section of the ipsilateral pyramidal tracts corresponding with the MRSI section for subgroups of patients without sensorimotor deficits, “no,” and patients with sensorimotor deficits, “yes” (A, B, and C, respectively). MD values are expressed in units × 10⁻³ mm²/s. Overlaid are the P values calculated from a 2-sided unpaired t test (ns = not significant).