Whole-Brain Vascular Architecture Mapping Identifies Region-Specific Microvascular Profiles In Vivo

Abstract

Background and purpose: The novel MR imaging technique of vascular architecture mapping allows in vivo characterization of local changes in cerebral microvasculature, but reference ranges for vascular architecture mapping parameters in healthy brain tissue are lacking, limiting its potential applicability as an MR imaging biomarker in clinical practice. We conducted whole-brain vascular architecture mapping in a large cohort to establish vascular architecture mapping parameter references ranges and identify region-specific cortical and subcortical microvascular profiles.

Materials and methods: This was a single-center examination of adult patients with unifocal, stable low-grade gliomas with multiband spin- and gradient-echo EPI sequence at 3T using parallel imaging. Voxelwise plotting of resulting values for gradient-echo (R₂*) versus spin-echo (R₂) relaxation rates during contrast agent bolus administration generates vessel vortex curves that allow the extraction of vascular architecture mapping parameters representative of, eg, vessel type, vessel radius, or CBV in the underlying voxel. Averaged whole-brain parametric maps were calculated for 9 parameters, and VOI analysis was conducted on the basis of a standardized brain atlas and individual cortical GM and WM segmentation.

Results: Prevalence of vascular risk factors among subjects (n = 106; mean age, 39.2 [SD, 12.5] years; 56 women) was similar to those in the German population. Compared with WM, we found cortical GM to have larger mean vascular calibers (5.80 [SD, 0.59] versus 4.25 [SD, 0.62] P < .001), increased blood volume fraction (20.40 [SD, 4.49] s^-1 versus 11.05 [SD, 2.44] s^-1; P < .001), and a dominance of venous vessels. Distinct microvascular profiles emerged for cortical GM, where vascular architecture mapping vessel type indicator differed, eg, between the thalamus and cortical GM (mean, -2.47 [SD, 4.02] s^-2 versus -5.41 [SD, 2.84] s^-2; P < .001). Intraclass correlation coefficient values indicated overall high test-retest reliability for vascular architecture mapping parameter mean values when comparing multiple scans per subject.

Conclusions: Whole-brain vascular architecture mapping in the adult brain reveals region-specific microvascular profiles. The obtained parameter reference ranges for distinct anatomic and functional brain areas may be used for future vascular architecture mapping studies on cerebrovascular pathologies and might facilitate early discovery of microvascular changes, in, eg, neurodegeneration and neuro-oncology.

FIG 1.

Flow diagram showing the patient-selection protocol and criteria for inclusion and exclusion. The asterisk indicates that multiple scans per patient were used for further subanalyses on intrasubject test-retest reliability. VP-Shunt indicates ventriculoperitoneal shunt.

FIG 2.

Cerebral volumes of interest. Axial representation of VOIs on spatially normalized T1-weighted images displaying 6 atlas-based anatomic VOIs (female subject, 27 years of age; right-sided lesion) (A) and individually segmented gray and white matter VOIs (female subject, 38 years of age; left-sided lesion) (B). Only the hemisphere contralateral to the lesion was analyzed for each subject, with a total of 8 VOIs per subject.

FIG 3.

Color representations of distance map parameters I, VTI, and CBI. Parameters I, VTI, and CBI are shown as spatially normalized, averaged axial parametric maps. In MNI standard space, slice coordinates are as follows for all maps (from left to right, Z-axis): -40, -14, 0, 8, 24, 44. Maps of parameters I and VTI are closely correlated and depict differences between brain regions with predominantly venous outflow, eg, close to the transverse and rectus sinus, and predominantly arterial inflow, eg, in the insular cortex. Parameter CBI contrasts brain regions with increased capillary vascularization, such as the GP and hippocampus.

FIG 4.

Parametric maps for CBV fraction, VIPS, and rCBV. Parameters BVF, VIPS, and rCBV are shown as spatially normalized, averaged axial parametric maps in MNI standard space as above. Because BVF identifies regions with increased blood volume, it is similar to rCBV with moderate correlations between both parameter values in the cGM and WM, respectively (Online Supplemental Data). The parameter VIPS is highly increased in the GP and thalamus (Table 2), as well as in parts of the WM along the pyramidal tracts.

FIG 5.

Color maps of VSI, microvessel density Q, and CGI. Parameters VSI, Q, and CGI are shown as spatially normalized, averaged axial parametric maps in MNI standard space as above. Parameters VSI and CGI indicate larger vessel calibers in the cGM compared with WM (Table 2). Microvessel density Q is increased in the lenticular nucleus (GP and putamen) and thalamus, compared with WM.