Detection of Advanced Lesions of Atherosclerosis in Carotid Arteries Using 3-Dimensional Motion-Sensitized Driven-Equilibrium Prepared Rapid Gradient Echo (3D-MERGE) Magnetic Resonance Imaging as a Screening Tool
Abstract
Background and Purpose:
Two-dimensional high-resolution multicontrast magnetic resonance imaging (2D-MC MRI) is currently the most reliable and reproducible noninvasive carotid vessel wall imaging technique. However, the long scan time required for 2D-MC MRI restricts its practical clinical application. Alternatively, 3-dimensional motion-sensitized driven-equilibrium prepared rapid gradient echo (3D-MERGE) vessel wall MRI can provide high isotropic resolution with extensive coverage in two minutes. In this study, we sought to prove that 3D-MERGE alone can serve as a screening tool to identify advanced carotid lesions.
Methods:
Two hundred twenty-seven subjects suspected of recent ischemic stroke or transient ischemic attack were imaged using 2D-MC MRI with an imaging time of 30 minutes, then with 3D-MERGE with an imaging time of 2 minutes, on 3T-MRI scanners. Two experienced reviewers interpreted plaque components using 2D-MC MRI as the reference standard and categorized plaques using a modified American Heart Association lesion classification for MRI. Plaques of American Heart Association type IV and above were classified as advanced. Arteries of American Heart Association types I to II and III were categorized as normal or with early lesions, respectively. One radiologist independently reviewed only 3D-MERGE and labeled the plaques as advanced if they had a wall thickness of >2 mm with high or low signal intensity compared with the adjacent sternocleidomastoid muscle. Sensitivity, specificity, and accuracy for 3D-MERGE were calculated.
Results:
Four hundred forty-nine arteries from 227 participants (mean age 61.2 years old, 64% male) were included in the analysis. Sensitivity, specificity, and accuracy for identification of advanced lesions on 3D-MERGE were 95.0% (95% CI, 91.8–97.2), 86.9% (95% CI, 81.4–92.0), 93.8% (95% CI, 91.1–95.8), respectively.
Conclusions:
3D-MERGE can accurately identify advanced carotid atherosclerotic plaques in patients suspected of stroke or transient ischemic attack. It has a more extensive coverage and higher sensitivity and specificity for advanced plaque detection with a much shorter acquisition time than 2D-MC MRI.
REGISTRATION:
URL: https://www.clinicaltrials.gov; Unique identifier: NCT02017756.
Graphical Abstract
Carotid atherosclerotic plaques are identified in ≈1 in 5 patients presenting with transient ischemic attack or stroke.1–3 Determining plaque vulnerability before the onset of stroke is critical for the prevention of cerebrovascular events. Studies have demonstrated that plaque burden and specific components of plaque composition such as intraplaque hemorrhage (IPH) are predictors of increased risk for stroke.4–6 Imaging techniques that quantify luminal stenosis are the current clinical standard. However, measurement of stenosis alone underestimates the severity of plaque burden due to positive wall remodeling.7,8 In addition, plaques with high-risk features, primarily identified by multicontrast MRI, are frequently found in arteries with <50% stenosis.5,9–14 Thus, identification of both vulnerable plaques and true plaque burden is crucial for better risk assessment in the carotid arteries.
Two-dimensional high-resolution multicontrast magnetic resonance imaging (2D-MC MRI) is a reliable and reproducible imaging technique to distinguish plaque components such as irregular surface, IPH, and presence of a large lipid-rich necrotic core (LRNC) within arterial walls.12,15–17 It has been used for prospective studies that helped to establish the concept of high-risk (vulnerable) carotid plaque. However, for clinical use, this technique is limited because of its small coverage and long scan times needed for acquiring multicontrast images, restricting effective clinical usage. Although some 3D vessel wall MRI techniques can provide information on plaque characterization, degree of stenosis, luminal surface condition, and wall boundaries,12,18–21 they need long imaging times. They are thus not efficient for everyday clinical routines.
Three-dimensional motion-sensitized driven-equilibrium prepared rapid gradient echo (3D-MERGE) vessel wall imaging has recently been proven to be able to provide high isotropic resolution and extensive coverage within a short scan time.22 Plaque burden can be measured accurately with this technique.23 Intensity difference within the artery wall and irregular surface have been identified as advanced carotid lesions, and this terminology is used here rather than high-risk plaque. In this study, we sought to prove that 3D-MERGE can be used as an accurate screening tool for the identification of advanced carotid lesions.
Methods
The authors declare that all supporting data are available within the article and its Data Supplement. We assessed the study design and report using STARD 2015 principles; the STARD 2015 checklist and flow diagram is available in the Data Supplement.24
Study Population
This study is a subanalysis of prospectively collected data from the CARE-II study (Chinese Atherosclerosis Risk Evaluation).25–27 CARE-II is a cross-sectional, nonrandomized, observational study in which participants were recruited from five hospitals in China. In brief, inclusion criteria were as follows: (1) 18- to 80-year-old males and females, (2) anterior circulation cerebrovascular ischemic events within the previous two weeks, and (3) the presence of carotid plaque (>1.5 mm wall thickness) on carotid ultrasound. Subjects with cardioembolic stroke, history of radiation therapy on the neck, or contraindications to MR examinations were excluded from the study.27 All participants underwent MRI of bilateral carotid arteries with a standardized protocol, and the subjects were recruited if they had atherosclerotic plaque in at least one carotid artery determine by B-mode ultrasound scan (intima-media thickness ≥1.5 mm) regardless of stenosis degree.
The 3D-MERGE pulse sequence was not available on some scanners in the CARE-II study. Subjects scanned at these sites were not included in the current study. Thus, a total of 296 participants were selected among the cases who had 3D-MERGE sequences and 2D-MC MRI (Results in the Data Supplement). Institutional review boards approved the research plan, and study participants provided written consent before enrollment.
Magnetic Resonance Imaging
All patients underwent MRI on 3.0-T MRI scanners (Philips Achieva TX; Best, the Netherlands) using an 8-channel phased-array carotid artery coil on the same day. A standardized carotid MR imaging protocol was implemented for carotid plaque imaging at all participating centers. After scout scanning, the bilateral carotid arteries were imaged with 3D-MERGE8 black blood MRI. The coronally acquired images from 3D-MERGE MRI were reformatted in the axial direction for final evaluation. Imaging parameters for 3D-MERGE included repetition time ms/echo time ms, 9.3/4.4; flip angle, 6°; field of view, 252 mm (foot-to-head direction)×252 mm (right-to-left direction)×35 mm (anterior-to-posterior direction); acquired voxel resolution, 0.7×0.7×0.7 mm3; reconstruction resolution, 0.35×0.35×0.35mm3; signals averaged, one; and acquisition time, 2 minutes 42 seconds. 2D-MC MRI included T1-weighted, T2-weighted, 3D time-of-flight, and magnetization-prepared rapid acquisition with gradient echo sequences. The imaging parameters for 2D-MC MRI have previously been published27 (Data Supplement).
3D-MERGE has larger coverage of bilateral carotid arteries in the foot-head direction (150 mm) than 2D-MC MRI (32 mm), and we only compared findings from the same field of view (Figure 1). Thus, plaques outside the FOV of 2D-MC MRI were not included in the statistical analysis. Plaque slices located on the border were included only if the slices were inside the FOV of 2D-MC MRI. An illustration showing the FOV (area of interest) of 2D-MC MRI and the 3D-MERGE image is shown in Figure 1.
Figure 2. The transverse images reformatted from 3-dimensional motion-sensitized driven-equilibrium prepared rapid gradient echo (3D-MERGE) of bilateral carotid arteries were matched with 2-dimensional high-resolution multicontrast magnetic resonance (2D-MC MR). A 54-y-old man presented with right-sided cerebral ischemic stroke. The long segment of the right internal carotid artery occlusion after the bifurcation is well delineated in the coronosagittal view of the 3D-MERGE (A). The reformatted transverse image from 3D-MERGE at the level of the internal carotid artery (solid line) demonstrates high and low signal (B), which is similar in appearance seen on the matched images of the 2D-MC MR imaging (MRI; C; time-of-flight, T1 weighted images, and proton-density weighted images respectively). The corresponding region of coverage by 2D-MC MR is indicated by the dashed lines on the 3D-MERGE image.
There is also a moderate-sized plaque in the left common carotid artery (D) in the coronosagittal view of 3D-MERGE. It’s reformatted in axial image (E) at the level of the common carotid artery (solid line) demonstrates an advanced lesion with mixed high and low signals. The multicontrast-weighted images show similar signal appearances on 2D-MC MRI (F).
Image Analysis
Two trained reviewers with >3 years of experience analyzed 2D-MC MRI data using CASCADE software (Vascular Imaging Lab, University of Washington).20 Reviewers were blinded to clinical information and the results of the 3D-MERGE review. Different contrast weighted images were matched using the carotid bifurcation of the index artery as a landmark. The index artery was defined as the artery ipsilateral to the side of the cerebral ischemic symptoms, if known, or with the more prominent plaque. The contralateral carotid artery (nonindex side) was also reviewed at the same slices as the index side.
The presence/absence and areas of calcification, LRNC, IPH, and luminal surface disruption were identified using previously published criteria.26,28 All plaques were categorized using a modified American Heart Association (AHA) lesion classification for 2D-MC MRI.15 In this study, AHA categories IV to VIII were considered as advanced carotid lesions and categories I to II and III as a normal artery or early lesions, respectively,5 on 2D-MC MRI as a reference for comparing with 3D-MERGE.
3D-MERGE was reformatted to transverse images (Figure 2) using RadiAnt DICOM Viewer (version 5.0.2 software, Medixant, Poland). A third reviewer, blinded to clinical information and the findings of the 2D-MC MRI review (D.B.G., who has 2 years of experience in carotid plaque image analysis) rated image quality using a 4-point scale (1=poor, 4=excellent) independently. Arteries with an image quality <2 or with missing contrast weightings on 2D-MC MRI were excluded from this analysis.
One reviewer (D.B.G.) reviewed 3D-MERGE images for overall plaque distribution (Figure 2) and plaque lesion type. 3D-MERGE has larger coverage and thinner slice thickness than 2D-MC MRI. Therefore, only matched slices across both imaging techniques were included for comparison (Figure 2).
For 3D-MERGE, advanced lesions were defined as having >2 mm wall thickness and having at least one of the following signal patterns: (1) low signal, presumably due to the LRNC, (2) similar in signal intensity as black blood signal within arterial wall and luminal surface, possible calcification or surface disruption, or (3) high signal intensity compared to the sternocleidomastoid muscle, presumably due to IPH.18 Early plaques were defined as a lesion with a wall thickness between 1.5 mm-2 mm and with homogenous signal intensity with respect to the sternocleidomastoid muscle (Figure 3).
Data Analysis
Categorical variables are described as counts or percentages. Proportions are presented with 95% CI. The statistical analysis was performed using STATA/SE 15.1 software (StataCorp; College Station, TX). Sensitivity, specificity, and accuracy were calculated with confidence intervals based on the exact binomial distribution. Negative and positive predictive values of the 3D-MERGE evaluation were calculated from cross-tab analysis.
Results
Five hundred ninety-two (592) arteries from 296 participants underwent 3D-MERGE and 2D-MC MRI in this study. Among them, 143 arteries in (58 from 2D-MC MRI, 108 from 3D-MERGE, 23 from both of them) were excluded due to insufficient image quality or missing at least one of the sequences on 2D-MC MRI. Thus, 449 arteries from 227 participants (mean age 61.2±9.0 years old, 64% male) were included in the analysis. Table 1 summarizes the clinical information for the study population.
| Clinical information of study population (N=227) | ||
|---|---|---|
| Mean±SD or n (%) | ||
| Sex (male) | 147 (64.8) | |
| Age, y | 61.22±9.1 | 36–87 |
| BMI, kg/m2 | 24.6±3.1 | 17.7–35.8 |
| Ever smoke | 118 (52.0) | |
| Diabetes | 55 (24.2) | |
| Hypertension | 159 (70.0) | |
| Systolic pressure, mm Hg | 147.47±23.10 | 100–240 |
| Diastolic pressure, mm Hg | 88.78±13.10 | 60–140 |
| Hyperlipidemia | 109 (48.0) | |
| Statin treatment | 56 (24.7) | |
| Cardiovascular disease | 43 (18.0) | |
| Family history of cardiovascular disease | 31 (13.0) | |
| Right carotid stenosis (NASCET) based on TOF | 13.74±29.30 | 0–100 |
| Left carotid stenosis (NASCET) based on TOF | 14.40±30.20 | 0–100 |
BMI indicates body mass index; NASCET, The North American Symptomatic Carotid Endarterectomy Trial; and TOF, time-of-flight.
Plaque Distribution on 3D-MERGE
A total of 397 plaques were identified on 3D-MERGE. Among them, 381 were defined as advanced and 16 as early lesions on 3D-MERGE. Among the 381 advanced lesions, 205 (53.8%) and 96 (25.2%) were completely and partially covered by the 2D-MC MRI, respectively. Among the 96 partially covered plaques by 2D-MC MRI, 84 and 12 had more than half, and less than half, of their length within the coverage, respectively. The 2D-MC MRI did not cover the remaining 80 (20.9%) advanced plaques and 16 early plaques, so those 96 plaques were excluded from the comparison analysis between 3D-MERGE and 2D-MC MRI. Figure 1 illustrates the plaque coverage and distribution of 2D-MC MRI and 3D-MERGE.
Comparison Between 3D-MERGE and 2D-MC MRI
In traditional 2D-MC MRI review, 168 of 449 (37.4%) arteries were identified as AHA type I to II, and III (normal artery and early lesion types, respectively); 281 (62.6%) were classified as AHA type IV to VII (advanced lesion types) plaques on 2D-MC MRI.18 On the matched transverse slices between 2D-MC MR and 3D-MERGE, 289 plaques were identified as advanced lesion types on 3D-MERGE, and among them, 267 were classified as advanced lesions on the 2D-MC MRI. One hundred sixty normal arteries or early lesions were identified on 3D-MERGE, and 146 of them were interpreted as early lesions or normal on the 2D-MC MRI (Figure 3).
Carotid arteries that have a heterogeneous signal pattern on 3D-MERGE were categorized according to signal intensity and morphology in the carotid wall. Among these, 259 (89.6%) cases had low signal with lamellar shape (more likely LRNC), 79 (27.0%) had high signal intensity (possible IPH), and 26 (8%) had an irregular surface continuous with a low signal (likely surface disruption), and 126 (43%) plaques contained low black blood signal (likely calcification).
The sensitivity, specificity, positive and negative predictive values for identification of advanced plaques on 3D-MERGE were 95.0% (95% CI, 91.8–97.2), 86.9% (95% CI, 81.4–92.0), 92.4% (95% CI, 89.0–95.4), and 91.3% (95% CI, 85.8–95.1), respectively. Overall accuracy was 93.8% (95% CI, 91.1–95.8; Table 2).
| 3D-MERGE review (predictive condition) | 2D-MC MRI review (true condition) | Total | |
|---|---|---|---|
| AHA categories IV–VIII | AHA categories I–III | ||
| Advanced lesion | 267 | 22 | 289 |
| Normal and early lesion | 14 | 146 | 160 |
| Total | 281 | 168 | 449 |
| Sensitivity: (267/281)×100=95.00% [95% CI, 91.76–97.24] | |||
| Specificity: (146/168)×100=86.90% [95% CI, 81.42–92.04] | |||
| PPV: (267/289)×100=92.38% [95% CI, 89.03–95.41] | |||
| Specificity: (146/160)×100=91.25% [95% CI, 85.75–95.13] | |||
Comparison of 2D-MC MRI and 3D-MERGE results for detection of an advanced lesion. Columns show the results of 2D-MC MRI as a reference method. Rows show 3D-MERGE results using criteria described above. Sensitivity, specificity, negative, and positive predictive values are stated above. 2D-MC-MRI indicates 2-dimensional high-resolution multicontrast magnetic resonance imaging; 3D-MERGE, 3-dimensional motion-sensitized driven-equilibrium prepared rapid gradient echo; AHA, American Heart Association; and PPV, positive predictive value.
Discussion
To the best of our knowledge, this study is one of the first studies using 3D-MERGE alone as a screening tool for identification of advanced atherosclerotic lesions in the extracranial carotid arteries. Murata et al29 used the same dataset in a study to investigate carotid plaque distribution and length to determine their relationship with clinical information and stroke risk. However, we sought to use 3D-MERGE as the sole sequence to screen for advanced plaque using different signal intensities in the arterial wall and luminal surface. Our study showed that 3D-MERGE is an accurate imaging technique for severity of plaque lesion types using modified AHA criteria, compared with 2D-MC MRI as the reference. Its high positive and negative predictive values indicate that it is a reliable tool for identification and categorization of carotid atherosclerotic plaques. Its large coverage of the bilateral carotid arteries (15 cm in the foot-head direction), provides more extensive coverage than traditional 2D multicontrast techniques, and its shorter imaging duration (2 minutes 42 seconds) makes 3D-MERGE MRI more readily applicable for clinical use. Furthermore, no contrast agents are needed for 3D-MERGE, making it useful for patients with renal dysfunction or in emergent situations as a fast diagnostic tool. It is, therefore, a promising tool for rapid assessment of the extracranial carotid arteries in patients suspected of acute ischemic stroke or transient ischemic attacks.
In this study, we used conventional 2D-MC MRI as the reference standard to validate 3D-MERGE. Previously, we have demonstrated that 2D-MC MRI is capable of classifying intermediate to high-risk atherosclerotic plaques of the carotid artery according to a modified AHA classification.15,21 This capability is built on comparison studies between 2D-MC MRI and histology, which validated characteristics of the high-risk plaques in MRI, such as fibrous cap rupture, IPH, and LRNC characteristics, that have been shown to be associated with an increased risk for stroke or transient ischemic attack.14,30,31
In this study, we observed that 20.9 % of plaques identified on 3D-MERGE were entirely outside of the coverage of 2D-MC MRI. Our results are similar to a study by Murata et al29 who reported that 16% of carotid plaques were entirely outside the 2D field of view. These lesions potentially may represent the culprit plaque in patients with ischemic neurological events, supporting the need for MRI techniques with larger field of view, such as 3D-MERGE, for plaque screening. 3D-MERGE provides more information than traditional 2D methods by providing the extent and length of plaque and plaque distribution that are correlated with stroke risk factors.29
We investigated the cause of the false-positive and the false-negative cases by 3D-MERGE. The majority of the disagreements were caused by plaque mimicking flow artifacts or partial volume effects on 2D-MC MRI. In our study, 3D-MERGE achieved better blood suppression than the 2D-MC MRI using the improved motion-sensitized driven-equilibrium flow suppression method, which reduces plaque mimicking artifacts.32 If flow artifacts appear on 3D-MERGE, they can be separated from the vessel wall by the presence of a layer of thin low signal between the wall and lumen boundary.29 In addition, 3D-MERGE has a thinner slice thickness than 2D-MC MRI to avoid partial volume artifacts. These results indicate that 3D-MERGE has more clinical strength than 2D-MC MRI.
There are some limitations to this study. First, we used 2D-MC MRI as standard reference. Although 2D-MC MRI can detect carotid plaque composition with high accuracy and reproducibility,33–35 it is susceptible to partial volume effects and flow artifacts as described above. Therefore, it would be ideal to conduct a study using histology to validate 3D-MERGE for plaque lesion type classification. Second, this study looked at the heterogeneous signal patterns within the artery wall on 3D-MERGE imaging as representative of advanced lesions, but without definitive identification of high-risk plaque components. The advanced lesion, whether it is IPH, LRNC, or irregular surface, is itself a high-risk feature of plaque, so accurate discrimination between exact histological elements may not be essential for assessing increased risk. Third, 2D-MC MRI has smaller coverage than 3D-MERGE. We could not classify the plaques outside of the coverage of 2D-MC MRI. Fourth, we excluded cardiogenic stroke using echocardiography and ECG. However, it is possible that some patients may have had cardioembolic stroke due to lack of extended cardiac monitoring.
Conclusions
3D-MERGE MRI can be used as a single sequence for rapid screening of patients presenting with symptoms of acute stroke or transient ischemic attack to detect advanced plaques in carotid arteries with good accuracy and a short imaging time compared to well-established 2D multicontrast-weighted MRI. Further study is warranted to validate 3D-MERGE against histology.
Article Information
Supplemental Materials
Online Figure I
Online Tables I–II
Acknowledgments
Zach Miller at the University of Washington helped edit this article for language and grammar. Dr Jie Sun provided invaluable support in submitting the article. We also thank the other investigators, staff, and participants of the CARE-II study (Chinese Atherosclerosis Risk Evaluation) for their valuable contributions. A full list of participating CARE-II investigators and institutions can be found at URL: https://www.clinicaltrials.gov.
Footnote
Nonstandard Abbreviations and Acronyms
- 2D-MC MRI
- 2D high-resolution multicontrast MRI
- 3D-MERGE
- 3-dimensional motion-sensitized driven-equilibrium prepared rapid gradient echo
- AHA
- American Heart Association
- IPH
- intraplaque hemorrhage
- LRNC
- lipid-rich necrotic core
- MRI
- magnetic resonance imaging
Supplemental Material
File (str_stroke-2020-032505_supp2.pdf)
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- 273.64 KB
References
1.
Cheng SF, Brown MM, Simister RJ, Richards T. Contemporary prevalence of carotid stenosis in patients presenting with ischaemic stroke. Br J Surg. 2019;106:872–878. doi: 10.1002/bjs.11136
2.
Ooi YC, Gonzalez NR. Management of extracranial carotid artery disease. Cardiol Clin. 2015;33:1–35. doi: 10.1016/j.ccl.2014.09.001
3.
Chaturvedi S, Bruno A, Feasby T, Holloway R, Benavente O, Cohen SN, Cote R, Hess D, Saver J, Spence JDet al; Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Carotid endarterectomy–an evidence-based review: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology. 2005;65:794–801. doi: 10.1212/01.wnl.0000176036.07558.82
4.
Halliday A, Harrison M, Hayter E, Kong X, Mansfield A, Marro J, Pan H, Peto R, Potter J, Rahimi Ket al; Asymptomatic Carotid Surgery Trial (ACST) Collaborative Group. 10-year stroke prevention after successful carotid endarterectomy for asymptomatic stenosis (ACST-1): a multicentre randomised trial. Lancet. 2010;376:1074–1084. doi: 10.1016/S0140-6736(10)61197-X
5.
Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 1995;92:1355–1374. doi: 10.1161/01.cir.92.5.1355
6.
Sun J, Hatsukami TS. Plaque imaging to decide on optimal treatment: medical versus carotid endarterectomy versus carotid artery stenting. Neuroimaging Clin N Am. 2016;26:165–173. doi: 10.1016/j.nic.2015.09.011
7.
Dong L, Kerwin WS, Ferguson MS, Li R, Wang J, Chen H, Canton G, Hatsukami TS, Yuan C. Cardiovascular magnetic resonance in carotid atherosclerotic disease. J Cardiovasc Magn Reson. 2009;11:53. doi: 10.1186/1532-429X-11-53
8.
Mossa-Basha M, Wasserman BA. Low-grade carotid stenosis: implications of MR imaging. Neuroimaging Clin N Am. 2016;26:129–145. doi: 10.1016/j.nic.2015.09.010
9.
Moody AR, Murphy RE, Morgan PS, Martel AL, Delay GS, Allder S, MacSweeney ST, Tennant WG, Gladman J, Lowe Jet al. Characterization of complicated carotid plaque with magnetic resonance direct thrombus imaging in patients with cerebral ischemia. Circulation. 2003;107:3047–3052. doi: 10.1161/01.CIR.0000074222.61572.44
10.
Singh N, Moody AR, Gladstone DJ, Leung G, Ravikumar R, Zhan J, Maggisano R. Moderate carotid artery stenosis: MR imaging-depicted intraplaque hemorrhage predicts risk of cerebrovascular ischemic events in asymptomatic men. Radiology. 2009;252:502–508. doi: 10.1148/radiol.2522080792
11.
Yuan C, Mitsumori LM, Beach KW, Maravilla KR. Carotid atherosclerotic plaque: noninvasive MR characterization and identification of vulnerable lesions. Radiology. 2001;221:285–299. doi: 10.1148/radiol.2212001612
12.
Saam T, Hatsukami TS, Takaya N, Chu B, Underhill H, Kerwin WS, Cai J, Ferguson MS, Yuan C. The vulnerable, or high-risk, atherosclerotic plaque: noninvasive MR imaging for characterization and assessment. Radiology. 2007;244:64–77. doi: 10.1148/radiol.2441051769
13.
Sun J, Zhao XQ, Balu N, Neradilek MB, Isquith DA, Yamada K, Cantón G, Crouse JR, Anderson TJ, Huston Jet al. Carotid plaque lipid content and fibrous cap status predict systemic CV outcomes: The MRI Substudy in AIM-HIGH. JACC Cardiovasc Imaging. 2017;10:241–249. doi: 10.1016/j.jcmg.2016.06.017
14.
Gupta A, Baradaran H, Schweitzer AD, Kamel H, Pandya A, Delgado D, Dunning A, Mushlin AI, Sanelli PC. Carotid plaque MRI and stroke risk: a systematic review and meta-analysis. Stroke. 2013;44:3071–3077. doi: 10.1161/STROKEAHA.113.002551
15.
Cai JM, Hatsukami TS, Ferguson MS, Small R, Polissar NL, Yuan C. Classification of human carotid atherosclerotic lesions with in vivo multicontrast magnetic resonance imaging. Circulation. 2002;106:1368–1373. doi: 10.1161/01.cir.0000028591.44554.f9
16.
Yuan C, Parker DL. Three-dimensional carotid plaque MR imaging. Neuroimaging Clin N Am. 2016;26:1–12. doi: 10.1016/j.nic.2015.09.001
17.
Yuan C, Kerwin WS. MRI of atherosclerosis. J Magn Reson Imaging. 2004;19:710–719. doi: 10.1002/jmri.20070
18.
Cai Y, He L, Yuan C, Chen H, Zhang Q, Li R, Li C, Zhao X. Atherosclerotic plaque features and distribution in bilateral carotid arteries of asymptomatic elderly population: A 3D Multicontrast MR Vessel Wall Imaging Study. Eur J Radiol. 2017;96:6–11. doi: 10.1016/j.ejrad.2017.09.004
19.
Esposito-Bauer L, Saam T, Ghodrati I, Pelisek J, Heider P, Bauer M, Wolf P, Bockelbrink A, Feurer R, Sepp Det al. MRI plaque imaging detects carotid plaques with a high risk for future cerebrovascular events in asymptomatic patients. PLoS One. 2013;8:e67927. doi: 10.1371/journal.pone.0067927
20.
Kerwin W, Xu D, Liu F, Saam T, Underhill H, Takaya N, Chu B, Hatsukami T, Yuan C. Magnetic resonance imaging of carotid atherosclerosis: plaque analysis. Top Magn Reson Imaging. 2007;18:371–378. doi: 10.1097/rmr.0b013e3181598d9d
21.
Saam T, Ferguson MS, Yarnykh VL, Takaya N, Xu D, Polissar NL, Hatsukami TS, Yuan C. Quantitative evaluation of carotid plaque composition by in vivo MRI. Arterioscler Thromb Vasc Biol. 2005;25:234–239. doi: 10.1161/01.ATV.0000149867.61851.31
22.
Balu N, Yarnykh VL, Chu B, Wang J, Hatsukami T, Yuan C. Carotid plaque assessment using fast 3D isotropic resolution black-blood MRI. Magn Reson Med. 2011;65:627–637. doi: 10.1002/mrm.22642
23.
Zhao H, Wang J, Liu X, Zhao X, Hippe DS, Cao Y, Wan J, Yuan C, Xu J. Assessment of carotid artery atherosclerotic disease by using three-dimensional fast black-blood MR imaging: comparison with DSA. Radiology. 2015;274:508–516. doi: 10.1148/radiol.14132687
24.
Cohen JF, Korevaar DA, Altman DG, Bruns DE, Gatsonis CA, Hooft L, Irwig L, Levine D, Reitsma JB, De Vet HC. STARD 2015 guidelines for reporting diagnostic accuracy studies: explanation and elaboration. BMJ Open. 2016;6:e012799. doi: 10.1136/bmjopen-2016-012799
25.
Watase H, Canton G, Sun J, Zhao X, Hatsukami TS, Yuan C. Four different carotid atherosclerotic behaviors based on luminal stenosis and plaque characteristics in symptomatic patients: An In Vivo Study. Diagnostics (Basel). 2019;9:E137. doi: 10.3390/diagnostics9040137
26.
Zhao X, Hippe DS, Li R, Canton GM, Sui B, Song Y, Li F, Xue Y, Sun J, Yamada Ket al; CARE-II Study Collaborators. Prevalence and characteristics of carotid artery high-risk atherosclerotic plaques in Chinese patients with cerebrovascular symptoms: A Chinese Atherosclerosis Risk Evaluation II Study. J Am Heart Assoc. 2017;6:e005831. doi: 10.1161/JAHA.117.005831
27.
Zhao X, Li R, Hippe DS, Hatsukami TS, Yuan C; CARE-II Investigators. Chinese Atherosclerosis Risk Evaluation (CARE II) study: a novel cross-sectional, multicentre study of the prevalence of high-risk atherosclerotic carotid plaque in Chinese patients with ischaemic cerebrovascular events-design and rationale. Stroke Vasc Neurol. 2017;2:15–20. doi: 10.1136/svn-2016-000053
28.
Xu WH, Li ML, Gao S, Ni J, Yao M, Zhou LX, Peng B, Feng F, Jin ZY, Cui LY. Middle cerebral artery intraplaque hemorrhage: prevalence and clinical relevance. Ann Neurol. 2012;71:195–198. doi: 10.1002/ana.22626
29.
Murata K, Murata N, Chu B, Watase H, Hippe DS, Balu N, Sun J, Zhao X, Hatsukami TS, Yuan C. Characterization of carotid atherosclerotic plaques using 3D-MERGE magnetic resonance imaging and correlation with stroke risk factors. Stroke. 2020;51:475–480. doi: 10.1161/STROKEAHA.119.027779
30.
Xu D, Hippe DS, Underhill HR, Oikawa-Wakayama M, Dong L, Yamada K, Yuan C, Hatsukami TS. Prediction of high-risk plaque development and plaque progression with the carotid atherosclerosis score. JACC Cardiovasc Imaging. 2014;7:366–373. doi: 10.1016/j.jcmg.2013.09.022
31.
Underhill HR, Hatsukami TS, Cai J, Yu W, DeMarco JK, Polissar NL, Ota H, Zhao X, Dong L, Oikawa Met al. A noninvasive imaging approach to assess plaque severity: the carotid atherosclerosis score. AJNR Am J Neuroradiol. 2010;31:1068–1075. doi: 10.3174/ajnr.A2007
32.
Wang J, Yarnykh VL, Hatsukami T, Chu B, Balu N, Yuan C. Improved suppression of plaque-mimicking artifacts in black-blood carotid atherosclerosis imaging using a multislice motion-sensitized driven-equilibrium (MSDE) turbo spin-echo (TSE) sequence. Magn Reson Med. 2007;58:973–981. doi: 10.1002/mrm.21385
33.
Zhao X, Underhill HR, Zhao Q, Cai J, Li F, Oikawa M, Dong L, Ota H, Hatsukami TS, Chu Bet al. Discriminating carotid atherosclerotic lesion severity by luminal stenosis and plaque burden: a comparison utilizing high-resolution magnetic resonance imaging at 3.0 Tesla. Stroke. 2011;42:347–353. doi: 10.1161/STROKEAHA.110.597328
34.
Zhao X, Underhill HR, Yuan C, Oikawa M, Dong L, Ota H, Hatsukami TS, Wang Q, Ma L, Cai J. Minimization of MR contrast weightings for the comprehensive evaluation of carotid atherosclerotic disease. Invest Radiol. 2010;45:36–41. doi: 10.1097/RLI.0b013e3181beada7
35.
Ota H, Yarnykh VL, Ferguson MS, Underhill HR, Demarco JK, Zhu DC, Oikawa M, Dong L, Zhao X, Collar Aet al. Carotid intraplaque hemorrhage imaging at 3.0-T MR imaging: comparison of the diagnostic performance of three T1-weighted sequences. Radiology. 2010;254:551–563. doi: 10.1148/radiol.09090535
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© 2021 American Heart Association, Inc.
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Received: 1 September 2020
Revision received: 30 April 2021
Accepted: 14 May 2021
Published online: 30 September 2021
Published in print: January 2022
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Disclosures Dr Yuan has also received research grants from the National Institutes of Health (NIH). Drs Yuan and Hatsukami have received research grants from Philips Healthcare. The other authors report no conflicts.
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Philips Healthcare assisted in training and implementation of the magnetic resonance imaging (MRI) techniques at different participating image centers.
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