Jonas Schollenberger1, Luis Hernandez-Garcia1,2, and C. Alberto Figueroa1,3
1Biomedical Engineering, University of Michigan, Ann Arbor, MI, United States, 2fMRI Laboratory, University of Michigan, Ann Arbor, MI, United States, 3Surgery, University of Michigan, Ann Arbor, MI, United States
Synopsis
Collateral
flow patterns in the circle of Willis play a major role in maintaining adequate
blood supply to the brain in the presence of cerebrovascular occlusive disease.
In this work, we present a strategy to quantify collateral flow by calibrating
patient-specific computational fluid dynamic models of cerebral blood flow with
perfusion data from arterial spin labeling. For a patient with right carotid
stenosis, the collateral flow patterns in the circle of Willis obtained with
the calibrated computational model show good agreement with territorial
perfusion maps acquired with vessel-selective arterial spin labeling.
Introduction
In the
presence of cerebrovascular occlusive disease, adequate blood supply to the
brain relies on a network of collateral pathways through the circle of Willis
(CoW) and a change in distal vascular resistance through cerebral
autoregulation. Considering the high anatomical variability of the CoW, there
is a need to quantify the vasculature’s capability to compensate for a flow
reduction due to stenosis to make predictions about vascular deficits and/or
assist surgical planning.
In
vessel-selective pseudo-continuous arterial spin labeling (VS-PCASL),
individual arteries are magnetically labeled to measure the perfusion territory
in the brain. While VS-PCASL provides detailed territorial information about the
blood supply at the tissue level, a quantitative description of flow in the
large arteries supplying the brain remains unavailable. In contrast, 4D MRI
Flow can provide quantitative information on flow in large arteries but
intracranial applications have been limited by the spatial resolution necessary
to accurately capture the flow in the small cerebral arteries.
Patient-specific
computational fluid dynamic (CFD) models of blood flow have been widely used to
calculate flow and pressure in the cardiovascular system. Some of the
advantages of CFD over imaging include spatial and temporal resolution as well
as the ability to predict changes in hemodynamics following surgical
procedures. However, previous approaches of modeling patient-specific cerebral
blood flow have heavily relied on literature-based assumptions about the flow distribution
in the CoW1, limiting their applicability for clinical use.
In this work,
we present a strategy to quantify collateral flow in the CoW by combining arterial
spin labeling perfusion imaging with CFD. The CFD model is calibrated using imaging
data of global brain perfusion (non-selective PCASL), anatomy, and flow to
match patient-specific hemodynamics. The simulated collateral flow is validated
against VS-PCASL using Lagrangian particle tracking.Methods
MRI protocol:
Non-selective cardiac-triggered PCASL images are
acquired in a volume covering the entire brain cortex. A pre-scan is performed
to compensate for off-resonance in the label plane. Additionally, VS-PCASL
images are acquired for all four main brain-supplying arteries using
Super-selective PCASL2,3. The anatomy of the large arteries in the neck
and head is collected with a 3D TOF and combined with the anatomy of the aortic
arch, which is acquired with a T1-weighted SPGR. Flow measurements at the levels
of the ascending aorta, supra aortic vessels, and carotid bifurcation are acquired
with phase-contrast MRI.
Computational
Modeling:
Computational modeling is performed using the
in-house software CRIMSON (www.crimson.software), an advanced modeling environment
for patient-specific hemodynamic analysis. The large arteries are reconstructed
based on the anatomical data. Each vessel outflow is coupled with a 3-element
Windkessel model to represent the distal vascular bed. The inflow at the
ascending aorta is prescribed based on the measured flow.
Calibration:
The
parameters of each outflow Windkessel model are calibrated based on the
non-selective PCASL images. The workflow is illustrated in Figure 1 and entails
the following steps: (a) Segmentation of the cerebral perfusion territories and
calculation of the perfusion fraction of each territory to the total volume of
the cortex. (b) Calculation the cardiac-averaged
target flow splits in the CoW. (c) Tuning of the distal resistance in each
Windkessel model during the simulation to match target flow splits.
Validation:
Collateral
flow from CFD is validated against territorial perfusion maps acquired with
VS-PCASL. Lagrangian particles are seeded in the neck arteries, transported
based on the pulsatile velocity field, and counted at each outlet.Results
The combined
imaging and computational modeling approach is demonstrated for a patient with
asymptomatic right carotid stenosis (75% stenosis, female, age = 55 y/o).
The pressure
and velocity magnitude at peak systole are shown in Figure 2a. The pressure
drops significantly due to the increase in resistance in the stenosis while the
velocity increases on the contralateral side to compensate for the loss in
flow. Figure 2b shows the transport of particles through the large arteries and
quantification of collateral flow.
A qualitative
comparison between the perfusion territories based on VS-PCASL and the flow
distribution in the CoW based on CFD is shown in Figure 3. The reduction in
flow in the stenosed carotid artery (green) is compensated through the
contralateral carotid artery (blue) by supplying the right anterior perfusion
territory. The particle tracking shows both anterior cerebral arteries being
supplied by the left carotid artery. In the posterior circulation, the ASL
images show that the left vertebral artery (red) primarily supplies the right
posterior territory and the right vertebral artery (yellow) primarily supplies
the left posterior territory. This important observation is confirmed by the
CFD model showing the swirling motion of vertebral flow in the basilar artery
with little mixing. A quantitative comparison of collateral flow in the CoW is
shown in Figure 4. The percentage flow split
of right and left carotid artery based on VS-PCASL and CFD particle tracking
show good agreement.Discussion
A workflow for quantifying
collateral flow in the cerebral vasculature by combining MR imaging and CFD was
presented. Good agreement was demonstrated between calibrated CFD simulation and
VS-PCASL data. The calibrated CFD model provides quantitative, high-resolution,
and time-resolved information about the flow compensation in the cerebral
arteries due to the stenosis.Acknowledgements
No acknowledgement found.References
1. Mukherjee D, Jani ND, Selvaganesan K, Weng CL, Shadden SC.
Computational Assessment of the Relation Between Embolism Source and Embolus
Distribution to the Circle of Willis for Improved Understanding of Stroke
Etiology. J. Biomech. Eng. 2016;138:81008 doi: 10.1115/1.4033986.
2. Helle M, Norris DG, Rüfer S, Alfke K, Jansen O, Van Osch
MJP. Superselective pseudocontinuous arterial spin labeling. Magn. Reson. Med.
2010;64:777–786 doi: 10.1002/mrm.22451.
3. Schollenberger J, Figueroa CA, Garcia LH. Practical
considerations for territorial perfusion mapping in the cerebral circulation
using super ‐ selective pseudo ‐ continuous arterial spin labeling. Magn.
Reson. Med. 2020:492–504 doi: 10.1002/mrm.27936.
4. Kim DE, Park JH, Schellingerhout D, et al. Mapping the
Supratentorial Cerebral Arterial Territories Using 1160 Large Artery Infarcts.
JAMA Neurol. 2018 doi: 10.1001/jamaneurol.2018.2808.