Anatomical location-related hemodynamic variations are associated with atherosclerosis in the middle cerebral artery: a preliminary cross-sectional 4D flow and 3D vessel wall MRI study

Abstract

Background: Hemodynamics is crucial for the assessment of atherosclerotic development. However, flow alterations due to plaque existence and increased plaque number in different intracranial arterial segments have not been fully understood. This study aimed to investigate the relationship of wall shear stress (WSS) parameters between middle cerebral arteries (MCAs) with and without plaque and explore the potential discrepancy between multiple- and single-plaque existence.

Methods: Consecutive patients with MCA atherosclerosis were recruited and underwent four-dimensional (4D) flow magnetic resonance imaging (MRI) and three-dimensional (3D) vessel wall imaging (VWI). Time-averaged WSS (TAWSS), time-averaged WSS coefficient variation (TAWSSCV), and oscillatory shear index (OSI) were measured at five cross-sectional slices [initial, upstream, the most narrowed lumen (MNL), downstream, and terminal] of plaque and reference (REF) sites to describe lesion-level hemodynamics. Segment-level hemodynamics of M1 and M2 segments were also analyzed. MCA geometry and plaque characteristics were calculated. The MCAs were then classified into four groups according to plaque presence in different segments: Group I, without plaque; Group II, with plaque only in M1; Group III, with plaque in both M1 and M2; Group IV, with plaque only in M2. The above parameters were compared in MCA with and without plaque as well as single- and multiple-plaque (≥2) MCAs.

Results: A total of 150 MCAs with 231 plaques from 79 patients were investigated. TAWSS_min showed a relatively larger value at the proximal portion compared to the distal portion across plaque in both M1 and M2 segments. Lower lesion-level TAWSS_min was found in the M1 plaque presence of Group III compared to Group I and Group II (P=0.026 and P=0.014). Similar association was also observed in the M2 plaque presence of Groups III and IV compared to Group I (P=0.010 and P=0.008), whereas lower segment-level TAWSS_min was only seen in the M2 segment of Group III compared to Group I (P=0.039). Lower OSI_mean was found both in the M1 presence of Group II and III compared to Group I (P=0.013 and P=0.048) and OSI_max was found in the M1 plaque presence of Group II compared to Group I (P=0.036). Lower stenosis was found in single-plaque compared to multiple-plaque groups (P=0.045 and P=0.049). Lower lesion-level highest/initial TAWSS_mean ratio (P=0.037) and highest/initial TAWSS_max ratio (P=0.013) were found in the single-plaque M1 group compared to the multiple-plaque M1 group. The M1 geometry and positive remodeling (PR) were different between single- and multiple-plaque M1 groups whereas maximum wall thickness (maxWT) and normalized wall index (NWI) showed differences between the single- and multiple-plaque M2 groups (all P<0.05).

Conclusions: Hemodynamic alterations are observed under the impacts of atherosclerosis and are different between M1 plaque and M2 plaque. Single- and multiple-plaque MCAs exhibit different geometry, plaque characteristics, and hemodynamics, and these vary according to segments. The interplay of arterial segment, plaque number, and characteristics as well as hemodynamics could provide insight for the mechanisms of atherosclerotic existence.

Keywords: Four-dimensional flow magnetic resonance imaging (4D flow MRI); atherosclerosis; middle cerebral artery (MCA); three-dimensional vessel wall imaging (3D VWI); wall shear stress (WSS).

Figure 1

Plaque and hemodynamic measurements of a mild stenotic right MCA. (A) The axial MIP images of 3D TOF MRA with yellow lines indicating slices with 1 mm intervals to calculate segment-level hemodynamics. (B,C) The coronal and cross-sectional MPR images of 3D HR-VWI show five slices across plaque to generate plaque and lesion-level hemodynamic characteristics. Yellow line, initial slice; green line, upstream slice; red line, MNL slice; blue line, downstream slice; orange line, terminal slice. (C) The cross-sectional image of red slice in (B). (D,E) TAWSS and OSI distribution maps. The red boxes in the distribution maps indicate the regional TAWSS and OSI of M1 plaque in (B). The red boxes in the upper right corner show the maps of regional TAWSS and OSI in different orientations. 3D, three-dimensional; HR-VWI, high-resolution vessel wall imaging; MCA, middle cerebral artery; MIP, maximum intensity projection; MNL, the most narrowed lumen; MPR, multiplanar reformation; MRA, magnetic resonance angiography; OSI, oscillatory shear index; TAWSS, time-averaged wall shear stress; TOF, time-of-flight.

Figure 2

The flowchart of patient enrollment. MCA, middle cerebral artery.

Figure 3

Plaque location and hemodynamic characteristics of MCAs with and without plaque. (A) A right MCA without plaque. Left to right, axial and coronal MIP images of 3D TOF MRA, a coronal MPR image of 3D HR-VWI and maps of TAWSS and OSI distributions. White brackets show the M1 and M2 segments. (B) A right atherosclerotic MCA with a single plaque in M1. Left to right, axial and coronal MIP images of 3D TOF MRA, a coronal MPR image of 3D HR-VWI and maps of TAWSS and OSI distributions. Yellow arrow shows the location of the plaque. (C) A right atherosclerotic MCA with multiple plaques in M1 (N=2). Left to right, an MIP images of 3D TOF MRA, cross-sectional images of 3D HR-VWI and maps of TAWSS and OSI distributions. Yellow and red arrows respectively show the locations of the plaques while yellow one indicated the most stenotic plaque. (D) A right atherosclerotic MCA with plaques in both M1 and M2. Left to right, an MIP images of 3D TOF MRA, cross-sectional images of 3D HR-VWI and maps of TAWSS and OSI distributions. Yellow and white arrows respectively show the locations of the most stenotic plaques in M1 and M2 segments. The red boxes in the distribution maps indicate the regional TAWSS and OSI of M1 plaques (yellow arrows). The red boxes in the upper right corner show the maps of regional TAWSS and OSI in different orientations. 3D, three-dimensional; HR-VWI, high-resolution vessel wall imaging; MCA, middle cerebral artery; MIP, maximum intensity projection; MNL, the most narrowed lumen; MPR, multiplanar reformation; MRA, magnetic resonance angiography; OSI, oscillatory shear index; TAWSS, time-averaged wall shear stress; TOF, time-of-flight.