Rui Shen1, Xinyu Tong1, Huiyu Qiao1, Ran Huo2, Tao Wang3, Zuoguan Chen4, Ning Xu1, Jiachen Liu1, Shuwan Yu1, and Xihai Zhao1
1Center for Biomedical Imaging Research, Department of Biomedical Engineering, School of Medicine, Tsinghua University, Beijing, China, 2Department of Radiology, Peking University Third Hospital, Beijing, China, 3Department of Neurosurgery, Peking University Third Hospital, Beijing, China, 4Department of Vascular Surgery, Beijing Hospital, National Center of Gerontology, Institute of Geriatric Medicine, Chinese Academy of Medical Sciences, Beijing, China
Synopsis
Keywords: Vessel Wall, Atherosclerosis, mechanical constitutive property, inverse problem
Motivation: Beyond structural features of carotid plaque and hemodynamic parameters, the hemodynamic and structural metrics were determined by image-based computer simulations and the constitutive characteristics of carotid plaques were ignored.
Goal(s): We aimed to propose a method for identification of carotid plaque constitutive parameters using CINE MR images.
Approach: A novel MRI-based method to identify constitutive parameters of carotid plaque compositions was proposed and the calculated values from the proposed method were compared with the reference and ex-vivo validation.
Results: We found that calculated values were consistent with the reference and experimental results. The constant D2 could identify plaque compositions with different stiffness.
Impact: Our study proposed a novel MRI-based method for
identifying constitutive parameters of carotid plaque compositions. The
constant D2 could indicate different components of carotid plaques.
Introduction
Carotid atherosclerotic disease is known as one
of the major etiologies for ischemic stroke1, 2. A number of studies
demonstrated that the key features of carotid vulnerable plaques are associated
with cerebrovascular events3. Beyond structural features of carotid
plaque and hemodynamic parameters4-6, the structural mechanical characteristics
are also essential for indicating the vulnerability of carotid plaques7.
Nevertheless, the hemodynamic and structural metrics were determined by
image-based computer simulations5-7 and the constitutive
characteristics of carotid plaques were ignored8, 9. In this study,
we proposed a method for identification of carotid plaque constitutive
parameters to determine different compositions of carotid plaques using CINE MR
images.Methods
Study population: Thirty-six patients
with moderate-to-severe carotid atherosclerotic stenosis who were scheduled for
carotid endarterectomy (CEA) were recruited. The study protocol was approved by
institutional review board and written consent form was obtained from all
subjects. MR imaging protocol:
Multi-contrast carotid MRI and CINE MRI were conducted on a whole-body 3.0T MR
scanner (Ingenia TX, Philips Healthcare) with 8-channel carotid coil within one
week before CEA. The detailed imaging parameters are listed in Table 1. MR image analysis: The
lumen and outer wall boundaries of carotid arteries were outlined on MR images
which were matched to the CINE MR images. The carotid plaque compositions were identified
according to multi-contrast MR images by two experienced radiologists. Image
post-processing and property identification: The contours of lumen, outer
wall and different plaque compositions were mapped onto different frames of
CINE MR images. To calculate the displacement field of carotid plaque contour,
different frames of CINE MR images were registered by
using an open-source toolkit Elastix. The blood pressure utilized in the 2D finite
element (FE) model was presented in Figure 1(b). In the FE procedure, the modified Mooney-Rivlin strain energy density function (as
Eq 1) was utilized to describe the stress-stretch relationship and the arterial
wall and plaque components were assumed as hyper-elastic, isotropic and incompressible.
With the specific strain and pressure, the zero-pressure algorithm by Huang
et al was implemented10. The constitutive parameters of carotid
plaques were determined by the FE analysis. Ex-vivo validation
analysis: The ex-vivo carotid plaques samples of 6
patients from CEA surgery within 24 hours were segmented into stripes for
uniaxial tensile test (Figure 1(d)). The stress-stretch curve of each
stripe was fitted by using ordinary least square fitting method to obtain
constitutive parameters11.
$$$W=c_1 (I ̅_1-2)+D_1(exp(D_2 (I ̅_1-3))-1)+κ (J-1) $$$ Eq 1Results
Of 36 patients (mean age: 63.9±8.1 years; 27
males) enrolled in this study, 52 slices with CINE MR images were matched with
the multi-contrast MR images. The clinical characteristics of the study
population are summarized in Table 2. The constitutive parameters of each
tissue type were: media, c1 = 0.15 [0.11, 0.19] kPa, D1 = 4.02 [3.88, 4.18] kPa and D2
= 20.01 [19.43, 21.17]; fibrous cap, c1
= 0.19 [0.12, 0.24] kPa, D1 =
5.82 [5.52, 6.16] kPa and D2
= 19.82 [18.22, 21.06]; lipid, c1
= 0.05 [0.03, 0.09] kPa, D1 =
5.01 [4.91, 5.13] kPa and D2
= 5.52 [5.20, 5.72]; and intraplaque
hemorrhage (IPH), c1 = 0.31 [0.17, 0.44] kPa, D1 =
4.51 [4.34, 4.71] kPa and D2
= 5.63 [5.33, 5.74]. Of all the parameters, the D2 of media and fibrous cap is much
larger than those of the lipid and intraplaque hemorrhage. In the validation experiment,
the fresh carotid plaque samples of 6 patients were segmented into 11 media stripes,
10 fibrous cap stripes, 8 lipid stripes and 6 IPH stripes. The
ex-vivo validation demonstrated that the identified parameters of different
compositions are consistent with the averaged values from the uniaxial tensile
test.Discussion and Conclusion
In this study, we proposed a new MRI-based
method to identify carotid plaque constitutive property and found that the
constitutive parameters could identify
carotid plaque compositions with different stiffness. All the calculated values
of different compositions of all slices were consistent with both experimental
results in the validation and a previous study12. In
addition, the value of D2 indicates that the media and fibrous cap
are stiffer than the lipid and IPH. This finding suggests that the D2 constant is an effective indicator
for composition identification. However, there are still some limitations: (1) some tissue stripes may contain more than one tissue types; (2) the 2D FE model
only determined the material property in the
circumferential direction. In conclusion, a novel MRI-based method for carotid
plaque constitutive parameters identification was proposed and validated with
ex-vivo uniaxial tensile test and the constant D2 could identify
compositions of different stiffness in carotid atherosclerotic plaques.Acknowledgements
NoneReferences
1. Benjamin,
E. J., Muntner, P., Alonso, A., et al. Heart disease and stroke statistics-2019
update: a report from the American Heart Association. Circulation. 2019, 139,
e56–528.
2. Markus,
H. Stroke: causes and clinical features. Medicine. 2016, 44, 515–520.
3. Michel
JB, Virmani R, Arbustini E, Pasterkamp G. Intra-plaque hemorrhages as the
trigger of plaque vulnerability. European Heart Journal. 2011, 32:1977–1985.
4. Zhao
X , Miller Z E , Yuan C . Atherosclerotic plaque imaging by carotid MRI.
Current Cardiology Reports. 2009, 11(1):70-77.
5. Wang
J., Paritala P. K., Mendieta J. B., et al. Carotid Bifurcation with tandem stenosis—a
patient-specific case study combined in vivo imaging, in vitro Histology and in
silico Simulation. Frontiers in Bioengineering and Biotechnology. 2019,
7(349):1-11.
6. Shen
R., Tong X., Li D., et al. Slice-based and time-specific hemodynamic
measurements discriminate carotid artery vulnerable atherosclerotic plaques.
Comput Methods Programs Biomed. 2022, Oct;225:107050.
7. Huang
Y, Teng Z, Sadat U, et al. The influence of computational strategy on
prediction of mechanical stress in carotid atherosclerotic plaques: comparison
of 2D structure-only, 3D structure-only, one-way and fully coupled
fluid-structure interaction analyses. J Biomech. 2014 Apr 11;47(6):1465-71.
8. Teng
Z, Yuan J, Feng J, et al. The influence of constitutive law choice used to
characterise atherosclerotic tissue material properties on computing stress
values in human carotid plaques. J Biomech. 2015 Nov 5;48(14):3912-21.
9. Yuan
J, Teng Z, Feng J, et al. Influence of material property variability on the
mechanical behaviour of carotid atherosclerotic plaques: a 3D fluid-structure
interaction analysis. Int J Numer Method Biomed Eng. 2015 Aug;31(8):e02722.
10. Huang
Y, Wang S, Luo T, et al. Estimation of the zero-pressure computational start
shape of atherosclerotic plaques: Improving the backward displacement method
with deformation gradient tensor. J Biomech. 2022 Jan;131:110910.
11. Wang
S, Tokgoz A, Huang Y, et al. Bayesian Inference-Based Estimation of Normal
Aortic, Aneurysmal and Atherosclerotic Tissue Mechanical Properties: From
Material Testing, Modeling and Histology. IEEE Trans Biomed Eng. 2019
Aug;66(8):2269-2278.
12. Teng
Z, Zhang Y, Huang Y, et al. Material properties of components in human carotid
atherosclerotic plaques: a uniaxial extension study. Acta Biomater. 2014
Dec;10(12):5055-5063