Share:
Share this content in WeChat
X
Clinical Article
Assessment of carotid artery stenosis and hemodynamic risk factors related to stroke based on 4D Flow MRI
LU Fei  SUN Mengyao  MA Yue  JIANG Yueluan  SUN Yang  TONG Dan 

Cite this article as: LU F, SUN M Y, MA Y, et al. Assessment of carotid artery stenosis and hemodynamic risk factors related to stroke based on 4D Flow MRI[J]. Chin J Magn Reson Imaging, 2024, 15(2): 14-22, 47. DOI:10.12015/issn.1674-8034.2024.02.003.


[Abstract] Objective In this study, 4D flow magnetic resonance imaging (4D Flow MRI) was employed to analyze the hemodynamics of moderate and severe atherosclerotic stenosis in unilateral carotid arteries and investigate the hemodynamic risk factors influencing carotid atherosclerotic stenosis and acute ischemic stroke.Materials and Methods A total of 20 patients diagnosed with moderate to severe unilateral carotid atherosclerosis using ultrasonography were recruited from January to December at the First Hospital of Jilin University, along with age- and vascular condition-matched normal volunteers (n=26). Clinical data and magnetic resonance data were collected. Hemodynamic parameters such as blood flow, blood flow velocity, wall shear stress (WSS), maximum pressure gradient and energy loss were obtained by CVI 42 software. Compare the measured values between groups for statistical differences using t-tests or Mann Whitney U-tests and subgroup analysis was performed on acute cerebral infarction and non-acute cerebral infarction to explore the effect of hemodynamic changes at the stenosis on the occurrence of stroke.Results The mean blood flow, maximum blood flow, total volume and mean relative pressure difference in the study group were significantly lower than those in the control group (P<0.05), while the maximum energy loss and average energy loss were higher than those in the control group (P<0.05). The mean blood flow was negatively correlated with the degree of stenosis (r=-0.420, P<0.05). There were significant differences in mean blood flow, mean velocity, minimum velocity, maximum blood flow, total volume, and verage axial wall shear stress in the upper, central and lower reaches of all stenosis vessels (P<0.05), and the maximum pressure gradient of downstream acute cerebral infarction group was lower than that of non-acute cerebral infarction group (P<0.05).Conclusions Visualization and quantitative analysis of 4D Flow MRI shows that energy loss in addition to blood flow was helpful for realistic carotid artery stenosis. Low WSS and downstream maximum pressure gradient of carotid artery stenosis may serve as potential biomarkers for stroke prediction.
[Keywords] carotid artery stenosis;ischemic stroke;risk factors;four dimensional hemodynamics;magnetic resonance imaging

LU Fei1   SUN Mengyao2   MA Yue1   JIANG Yueluan3   SUN Yang1   TONG Dan1*  

1 Department of Radiology, the First Hospital of Jilin University, Changchun 130012, China

2 Department of Ultrasound, the First Hospital of Jilin University, Changchun 130012, China

3 Beijing Branch, Siemens Medical Systems Ltd., Beijing 100102, China

Corresponding author: TONG D, E-mail: tongdan@jlu.edu.cn

Conflicts of interest   None.

Received  2023-06-13
Accepted  2024-01-21
DOI: 10.12015/issn.1674-8034.2024.02.003
Cite this article as: LU F, SUN M Y, MA Y, et al. Assessment of carotid artery stenosis and hemodynamic risk factors related to stroke based on 4D Flow MRI[J]. Chin J Magn Reson Imaging, 2024, 15(2): 14-22, 47. DOI:10.12015/issn.1674-8034.2024.02.003.

[1]
MIGDALSKI A, JAWIEN A. New insight into biology, molecular diagnostics and treatment options of unstable carotid atherosclerotic plaque: a narrative review[J/OL]. Ann Transl Med, 2021, 9(14): 1207 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/34430648/. DOI: 10.21037/atm-20-7197.
[2]
GU H Q, YANG X, WANG C J, et al. Clinical characteristics, management, and In-hospital outcomes in patients with stroke or transient ischemic attack in China[J/OL]. JAMA Netw Open, 2021, 4(8): e2120745 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/34387677/. DOI: 10.1001/jamanetworkopen.2021.20745.
[3]
PAN Y S, LI Z X, LI J J, et al. Residual risk and its risk factors for ischemic stroke with adherence to guideline-based secondary stroke prevention[J]. J Stroke, 2021, 23(1): 51-60. DOI: 10.5853/jos.2020.03391.
[4]
LI Y, REN J H. Diagnosis of carotid atherosclerotic plaque with ultrasonography and its standardized procedures[J]. Chin J Gen Pract, 2022, 21(2): 105-108. DOI: 10.3760/cma.j.cn114798-20211117-00858.
[5]
HARIRI N, RUSSELL T, KASPER G, et al. Shear rate is a better marker of symptomatic ischemic cerebrovascular events than velocity or diameter in severe carotid artery stenosis[J]. J Vasc Surg, 2019, 69(2): 448-452. DOI: 10.1016/j.jvs.2018.04.036.
[6]
TENG Z Z, WANG S, TOKGOZ A, et al. Study on the association of wall shear stress and vessel structural stress with atherosclerosis: an experimental animal study[J/OL]. Atherosclerosis, 2021, 320: 38-46 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/33524908/. DOI: 10.1016/j.atherosclerosis.2021.01.017.
[7]
NGO M T, LEE U Y, HA H, et al. Improving blood flow visualization of recirculation regions at carotid bulb in 4D flow MRI using semi-automatic segmentation with ITK-SNAP[J/OL]. Diagnostics, 2021, 11(10): 1890 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/34679588/. DOI: 10.3390/diagnostics11101890.
[8]
SECCHI F, MONTI C B, CAPRA D, et al. Carotid phase-contrast magnetic resonance before treatment: 4D-flow versus standard 2D imaging[J]. Tomography, 2021, 7(4): 513-522. DOI: 10.3390/tomography7040044.
[9]
ZHANG G L, WANG Z X, ZHANG S, et al. Age and anatomical location related hemodynamic changes assessed by 4D flow MRI in the carotid arteries of healthy adults[J/OL]. Eur J Radiol, 2020, 128: 109035 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/32413676/. DOI: 10.1016/j.ejrad.2020.109035.
[10]
TAKEHARA Y, SEKINE T, OBATA T. Why 4D flow MRI? real advantages[J]. Magn Reson Med Sci, 2022, 21(2): 253-256. DOI: 10.2463/mrms.e.2022-1000.
[11]
DYVERFELDT P, BISSELL M, BARKER A J, et al. 4D flow cardiovascular magnetic resonance consensus statement[J/OL]. J Cardiovasc Magn Reson, 2015, 17(1): 72 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/26257141/. DOI: 10.1186/s12968-015-0174-5.
[12]
MARKL M. Special issue on 4D flow MRI in magnetic resonance in medical sciences[J/OL]. Magn Reson Med Sci, 2022, 21(2): 257 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/35228484/. DOI: 10.2463/mrms.con.2022-2000.
[13]
WÅHLIN A, EKLUND A, MALM J. 4D flow MRI hemodynamic biomarkers for cerebrovascular diseases[J]. J Intern Med, 2022, 291(2): 115-127. DOI: 10.1111/joim.13392.
[14]
RIVERA-RIVERA L A, CODY K A, EISENMENGER L, et al. Assessment of vascular stiffness in the internal carotid artery proximal to the carotid canal in Alzheimer's disease using pulse wave velocity from low rank reconstructed 4D flow MRI[J]. J Cereb Blood Flow Metab, 2021, 41(2): 298-311. DOI: 10.1177/0271678X20910302.
[15]
VALI A, ARISTOVA M, VAKIL P, et al. Semi-automated analysis of 4D flow MRI to assess the hemodynamic impact of intracranial atherosclerotic disease[J]. Magn Reson Med, 2019, 82(2): 749-762. DOI: 10.1002/mrm.27747.
[16]
LENG X Y, LAN L F, IP H L, et al. Hemodynamics and stroke risk in intracranial atherosclerotic disease[J]. Ann Neurol, 2019, 85(5): 752-764. DOI: 10.1002/ana.25456.
[17]
HANNEMAN K, SIVAGNANAM M, NGUYEN E T, et al. Magnetic resonance assessment of pulmonary (QP) to systemic (QS) flows using 4D phase-contrast imaging: pilot study comparison with standard through-plane 2D phase-contrast imaging[J]. Acad Radiol, 2014, 21(8): 1002-1008. DOI: 10.1016/j.acra.2014.04.012.
[18]
WANG M X, YANG Y B, ZHANG W, et al. Risk factors for cerebrovascular events in moyamoya angiopathy using 4D flow MRI: a pilot study[J]. J Magn Reson Imaging, 2023, 58(1): 61-68. DOI: 10.1002/jmri.28522.
[19]
NGO M T, LEE U Y, HA H, et al. Comparison of hemodynamic visualization in cerebral arteries: can magnetic resonance imaging replace computational fluid dynamics?[J/OL]. J Pers Med, 2021, 11(4): 253 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/33808514/. DOI: 10.3390/jpm11040253.
[20]
JOHANSSON E, ZARRINKOOB L, WÅHLIN A, et al. Diagnosing carotid near-occlusion with phase-contrast MRI[J]. AJNR Am J Neuroradiol, 2021, 42(5): 927-929. DOI: 10.3174/ajnr.A7076.
[21]
MARKL M, WEGENT F, ZECH T, et al. In vivo wall shear stress distribution in the carotid artery: effect of bifurcation geometry, internal carotid artery stenosis, and recanalization therapy[J]. Circ Cardiovasc Imaging, 2010, 3(6): 647-655. DOI: 10.1161/CIRCIMAGING.110.958504.
[22]
SUI B B, GAO P Y, LIN Y, et al. Hemodynamic parameters distribution of upstream, stenosis center, and downstream sides of plaques in carotid artery with different stenosis: a MRI and CFD study[J]. Acta Radiol, 2015, 56(3): 347-354. DOI: 10.1177/0284185114526713.
[23]
ZHANG G L, ZHANG S, QIN Y Y, et al. Differences in wall shear stress between high-risk and low-risk plaques in patients with moderate carotid artery stenosis: a 4D flow MRI study[J/OL]. Front Neurosci, 2021, 15: 678358 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/34456667/. DOI: 10.3389/fnins.2021.678358.
[24]
ZARRINKOOB L, WÅHLIN A, AMBARKI K, et al. Quantification and mapping of cerebral hemodynamics before and after carotid endarterectomy, using four-dimensional flow magnetic resonance imaging[J/OL]. J Vasc Surg, 2021, 74(3): 910-920.e1 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/33812036/. DOI: 10.1016/j.jvs.2021.01.074.
[25]
HARLOFF A, BERG S, BARKER A J, et al. Wall shear stress distribution at the carotid bifurcation: influence of eversion carotid endarterectomy[J]. Eur Radiol, 2013, 23(12): 3361-3369. DOI: 10.1007/s00330-013-2953-4.
[26]
STRECKER C, KRAFFT A J, KAUFHOLD L, et al. Carotid geometry and wall shear stress independently predict increased wall thickness-a longitudinal 3D MRI study in high-risk patients[J/OL]. Front Cardiovasc Med, 2021, 8: 723860 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/34765650/. DOI: 10.3389/fcvm.2021.723860.
[27]
ZARRINKOOB L, WÅHLIN A, AMBARKI K, et al. Blood flow lateralization and collateral compensatory mechanisms in patients with carotid artery stenosis[J]. Stroke, 2019, 50(5): 1081-1088. DOI: 10.1161/STROKEAHA.119.024757.
[28]
HOLMGREN M, STØVERUD K H, ZARRINKOOB L, et al. Middle cerebral artery pressure laterality in patients with symptomatic ICA stenosis[J/OL]. PLoS One, 2021, 16(1): e0245337 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/33417614/. DOI: 10.1371/journal.pone.0245337.
[29]
ANDO T, SEKINE T, MURAI Y, et al. Multiparametric flow analysis using four-dimensional flow magnetic resonance imaging can detect cerebral hemodynamic impairment in patients with internal carotid artery stenosis[J]. Neuroradiology, 2020, 62(11): 1421-1431. DOI: 10.1007/s00234-020-02464-2.
[30]
SEKINE T, TAKAGI R, AMANO Y, et al. 4D flow MR imaging of ophthalmic artery flow in patients with internal carotid artery stenosis[J]. Magn Reson Med Sci, 2018, 17(1): 13-20. DOI: 10.2463/mrms.mp.2016-0074.
[31]
ZHANG G L, ZHOU Y R, WU D, et al. Overview of 4D Flow MRI hemodynamic imaging and its clinical application[J]. Radiol Pract, 2022, 37(1): 4-9. DOI: 10.13609/j.cnki.1000-0313.2022.01.002.
[32]
FENG X Y, CHAN K L, LAN L F, et al. Stroke mechanisms in symptomatic intracranial atherosclerotic disease: classification and clinical implications[J]. Stroke, 2019, 50(10): 2692-2699. DOI: 10.1161/STROKEAHA.119.025732.
[33]
LI C H, GAO B L, WANG J W, et al. Hemodynamic factors affecting carotid sinus atherosclerotic stenosis[J/OL]. World Neurosurg, 2019, 121: e262-e276 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/30261386/. DOI: 10.1016/j.wneu.2018.09.091.
[34]
SHENG Y, LI X M, GUO X, et al. Reduction of carotid perfusion promotes inflammation of vascular endothelial cells in rabbits[J]. Basic Clin Med, 2021, 41(9): 1247-1252. DOI: 10.3969/j.issn.1001-6325.2021.09.001.
[35]
KIM J M, PARK K Y, BAE J H, et al. Intracranial arterial calcificationes can reflect cerebral atherosclerosis burden[J]. J Clin Neurol, 2019, 15(1): 38-45. DOI: 10.3988/jcn.2019.15.1.38.
[36]
Vascular Ultrasound Committee of Stroke Prevention and Treatment Expert Committee of National Health Commission, Superficial Organ and Peripheral Vascular Ultrasound Committee of Chinese Society of Ultrasound Medical Engineering, Brain and Neck Vascular Ultrasound Committee of Chinese Society of Ultrasound Medical Engineering. Expert consensus on some problems of cerebral and carotid vascular ultrasonography (Part of carotid)[J]. Chin J Cerebrovasc Dis, 2020, 17(6): 346-352. DOI: 10.3969/j.issn.1672-5921.2020.06.013.
[37]
ZHANG Y, KANG L, LIU Y A, et al. Correlation between hemodynamics, blood pressure variability and severity of carotid artery stenosis in patients with transient ischemic attack[J]. J Clin Med Pract, 2020, 24(5): 53-59. DOI: 10.7619/jcmp.202005014.
[38]
ROUSTAEI M, NIKMANESHI M R, FIROOZABADI B. Simulation of Low Density Lipoprotein (LDL) permeation into multilayer coronary arterial wall: interactive effects of wall shear stress and fluid-structure interaction in hypertension[J]. J Biomech, 2018, 67: 114-122. DOI: 10.1016/j.jbiomech.2017.11.029.
[39]
LENG X Y, WONG K S, LIEBESKIND D S. Evaluating intracranial atherosclerosis rather than intracranial stenosis[J]. Stroke, 2014, 45(2): 645-651. DOI: 10.1161/STROKEAHA.113.002491.
[40]
LIEBESKIND D S, FELDMANN E. Fractional flow in cerebrovascular disorders[J]. Interv Neurol, 2013, 1(2): 87-99. DOI: 10.1159/000346803.
[41]
KHAN A A, PATEL J, DESIKAN S, et al. Asymptomatic carotid artery stenosis is associated with cerebral hypoperfusion[J/OL]. J Vasc Surg, 2021, 73(5): 1611-1621.e2 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/33166609/. DOI: 10.1016/j.jvs.2020.10.063.
[42]
SIA S F, ZHAO X, LI R, et al. Evaluation of the carotid artery stenosis based on minimization of mechanical energy loss of the blood flow[J]. Proc Inst Mech Eng H, 2016, 230(11): 1051-1058. DOI: 10.1177/0954411916671752.
[43]
KAMPHUIS V P, ELBAZ M S M, VAN DEN BOOGAARD P J, et al. Disproportionate intraventricular viscous energy loss in Fontan patients: analysis by 4D flow MRI[J]. Eur Heart J Cardiovasc Imaging, 2019, 20(3): 323-333. DOI: 10.1093/ehjci/jey096.
[44]
ASHKIR Z, MYERSON S, NEUBAUER S, et al. Four-dimensional flow cardiac magnetic resonance assessment of left ventricular diastolic function[J/OL]. Front Cardiovasc Med, 2022, 9: 866131 [2023-06-12]. https://pubmed.ncbi.nlm.nih.gov/35935619/. DOI: 10.3389/fcvm.2022.866131.

PREV Study on MRI features of disc-condylar complex and semiquantitative evaluation of peridisc attachment in cases of temporomandibular joint disc displacement
NEXT Value of CMR feature-tracking imaging in discriminating subtypes of cardiac amyloidosis
  



Tel & Fax: +8610-67113815    E-mail: editor@cjmri.cn