Differences in plaque curvature in middle cerebral artery stenosis between acute stroke and non-acute stroke

Introduction

Intracranial atherosclerotic disease (ICAD) is a leading cause of ischemic stroke worldwide, and has a high prevalence among the Asian population (1,2). ICAD contributes to 30–50% of ischemic strokes in the Chinese population, and predominantly affects the middle cerebral artery (MCA) (2). In recent years, there has been a shift in the research focus on ICAD from the extent of stenosis to the vessel wall condition and plaque stability (3,4).

High-resolution magnetic resonance imaging (HR-MRI) is a non-invasive imaging method that can simultaneously display the degree of vascular stenosis, characteristics of plaques, and local changes in the vascular wall. Traditional parameters and features of plaques have already been reported by many scholars. For example, research has shown that symptomatic patients have a larger plaque area (PA), more positive remodeling (PR) vessels, and obvious enhanced plaques than asymptomatic patients (2,5-7). Further, using HR-MRI as a follow-up examination method, research has shown that plaque enhancement has a good predictive effect on stroke recurrence in ICAD patients (8,9). However, in addition to the characteristics of plaques, changes in hemodynamics at stenotic sites also have a significant effect on the occurrence and recurrence of stroke.

The computational fluid dynamics (CFD) model is a method used to obtain the hemodynamic parameters at the sites of vascular stenosis through imaging reconstruction (10,11). CFD model can be reconstructed based on computed tomography angiography or magnetic resonance angiography (MRA), and the primary hemodynamic parameter is wall shear stress (WSS). Previous studies have reported that high WSS in stenotic coronary arteries (12), carotid arteries (13), and intracranial arteries (10) is more likely to induce PR and atherosclerotic plaque rupture, triggering a cardiovascular event. However, in a previous study (14), we found that reconstructing the CFD model was time consuming. Woo et al. (15) obtained the value of WSS using GT software to process four-dimensional flow data; however, this method has not yet been widely implemented in practice, and its use in intracranial arteries is still not generally.

WSS change in the stenotic site is related to plaque morphology. Yang et al. (8) suggested that steepness (as a geometric morphological parameter and a reflection of the plaque curvature in the longitudinal direction) is a contributing factor to recurrent stroke. We conjectured that plaque steepness may indirectly reflect the luminal curvature, and may thus be associated with WSS. Therefore, we aimed to examine the potential and value of plaque curvature in the prediction of stroke occurrence. We hypothesized that a larger plaque curvature is more likely to cause ischemic stroke. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1552/rc).

Methods

Subjects and clinical data

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The research protocol was approved by the Ethics Committee of the Nanjing Medical University (No. NMU20200320). All enrolled patients provided verbal or written informed consent before they were examined.

From January 2020 to May 2024, 107 consecutive patients with suspected MCA atherosclerotic diseases were recruited from the Department of Neurology, Nanjing First Hospital, Nanjing, China. Patients experiencing drowsiness, dizziness, or limb weakness were recruited for the study if they met the following criteria: (I) had more than two atherosclerosis risk factors; (II) had no contraindications to magnetic resonance (MR) scans; (III) had unilateral stenosis in the M1 segment of the MCA (50–99% narrowing) on enhanced MRA imaging; (IV) had no ipsilateral internal carotid artery (ICA) stenosis ≥50%; (V) had no non-atherosclerotic vascular conditions, such as brain hemorrhage, vasculitis, moyamoya disease, dissection, or tumors; (VI) had no evidence of atrial fibrillation or cardioembolism; (VII) had high-quality images suitable for diagnosis and assessment; and (VIII) had an M1 segment of the MCA that ran straight.

A power analysis was conducted, and the sample size was determined using the “PS (Power and Sample Size Calculation software, Dupont and Plummer design)” to calculate the statistical power or sample size of our clinical study.

The demographic and clinical data of the patients were gathered from their medical records, including their sex, age, history of smoking (yes/no), alcoholism (yes/no), hypertension (yes/no), diabetes (yes/no), and blood glucose, glycated hemoglobin (HbA1c), total cholesterol, low-density lipoprotein (LDL), high-density lipoprotein (HDL), triglycerides, and homocysteine values. Patients with a history of past or current smoking were considered to have a cigarette smoking history; alcoholism was defined as consuming more than 2 U/day on average for men, or more than 1 U/day on average for women over the past year; hypertension was defined by a self-reported history of high blood pressure, average blood pressure levels >140/90 mmHg, or the use of antihypertensive medication; diabetes was identified by self-reported insulin or oral hypoglycemic medication usage, or recent physician-diagnosed diabetes based on elevated HbA1c (≥6.5%) (14).

Magnetic resonance imaging (MRI) process

After being admitted for a week, the enrolled patients underwent standard MRI procedures, including axial T1-weighted imaging (T1WI), T2-weighted imaging, T2-fluid attenuated inversion recovery, diffusion-weighted imaging (DWI), apparent diffusion coefficient (ADC) imaging, and enhanced MRA. The HR-MRI scans were performed on the stenotic MCA using a 3-Tesla MR scanner (Ingenia, Philips Medical Systems, Netherlands) with an 8-channel head coil. Subsequently, the following scan parameters were used to perform black-blood pre-contrast T1WI and contrast-enhanced T1WI (T1WI + C) imaging perpendicular to the M1 segment of the MCA: (I) pre-contrast T1WI: echo time (TE), 9 ms; repetition time (TR), 1,000 ms; slice thickness, 0.6 mm; slice gap, 0 mm; slice number, 10; number of excitions (NEX), 2; matrix size, 180 mm × 144 mm; field of view (FOV), 80 mm × 80 mm; and acquisition time, 192 s; and (II) T1WI + C: TE, 9 ms; TR, 1,000 ms; slice thickness, 0.6 mm; slice gap, 0 mm; slice number, 10; NEX, 2; matrix size, 180 mm × 144 mm; FOV, 80 mm × 80 mm; and acquisition time, 192 s. A 15 mL bolus of gadodiamide (Kang Chen, Guangzhou, China) was injected intravenously at a speed of 2 mL/s, T1WI+C was performed 5 minutes after the administration of the contrast agent.

Analysis of MR images

The vessel wall parameters were measured based on the images on a Philips Intellispace Portal workstation. The short axial T1WI images were enlarged to 300%, and manual measurements of the lumen area (LA) and vessel area (VA) at both the reference location and the most narrowed lumen (MNL) of the MCA were performed. The reference site was chosen as the nearest segment free of plaques or with minimal disease proximal to the stenosis in the MCA. In cases in which a proximal reference site was unavailable, the adjacent distal site was used. The following formulas were used: wall area (WA) = VA − LA; PA = WA_MNL − WA_reference; remodeling index (RI) = VA_MNL/VA_reference; normalized wall index (NWI) = WA/VA; degree of stenosis = (1 − LA_MNL/LA_reference) × 100%. The parameters were calculated according to previous studies (3,16).

Patients showing hyperintense signals on DWI and hypointense signals on the ADC in the stenotic MCA region were categorized as experiencing acute stroke, and assigned to the symptomatic group, while the remaining patients were assigned to the asymptomatic group. Patients with scattered cortical acute stroke lesions were allocated to the artery-to-artery embolism (AAE) group, and patients with a single subcortical lesion with a spatial relationship between the perforating arteries and the margin of plaque on HR-MRI were allocated to the local branch occlusion (LBO) group (15,17). A RI ≥1.05 was defined as PR, 0.95< RI <1.05 was defined as non-remodeling, and a RI ≤0.95 was defined as negative remodeling (NR) (3,16). Plaque enhancement was graded as follows: grade 0: enhancement equal to or less than normal arterial walls; grade 1: enhancement greater than grade 0 but less than the pituitary infundibulum; and grade 2: enhancement equal to or greater than that of the pituitary infundibulum. Grades 1 and 2 were considered enhanced in this study (17,18).

The height of plaques in most stenotic sites was defined as H₂, the midpoint from the beginning of the plaques to H₂ was H₁, and the midpoint from H₂ to the ending of the plaques was H₃. R₁₂ and R₃₂ are the ratio of H₁/H₂ and H₃/H₂, respectively. Two experienced radiologists, who were blinded to the clinical information of the patients, conducted the measurements. Subsequently, the average value was determined and applied. Both observers reached a consensus on the slices selected for measurement and the degree of plaque enhancement. In cases of disagreement, a joint reading was performed to reach a consensus.

Statistical analysis

The statistical analyses were performed using the SPSS 21.0 software package (Chicago, IL, USA). The normality of the distribution of the quantitative data was assessed using the Kolmogorov-Smirnov test. Normally distributed continuous data are expressed as the mean ± standard deviation, while non-normally distributed data are presented as the median and inter-quartile range. The continuous variables were compared between groups using the t-test, while the categorical variables were compared using the Pearson chi-square test. Non-normally distributed data were analyzed using the Mann-Whitney U test. Subsequently, the statistically significant indicators underwent multivariate logistic regression analyses for further examination. A P value less than 0.05 was considered statistically significant. The degree of inter-observer consistency in measurements was assessed using intraclass correlation coefficients (ICC) with a two-way random effects model for continuous variables across different observers. An ICC exceeding 0.75 indicated robust reproducibility among the observers (7).

Results

Demographic and clinical characteristics of patients

After 35 patients were excluded (12 patients with moving artifacts; 18 patients with ipsilateral ICA stenosis ≥50%; 3 patients with brain tumors; and 2 patients with brain hemorrhages), 107 patients were enrolled in the study (Figure 1). There were 43 patients in the asymptomatic group (25 men, 18 women; mean age: 57±12 years), and 64 patients in the symptomatic group (33 men, 31 women; mean age: 68±10 years). No statistically significant differences were observed between the asymptomatic and symptomatic groups in terms of sex, smoking status, alcoholism, hypertension, diabetes mellitus, age, blood glucose levels, total cholesterol, triglycerides, HDL, LDL, HbA1c, and homocysteine levels (Table 1). More enhanced plaques were observed in the symptomatic group than the asymptomatic group (52 vs. 14, P=0.001). Of the patients in the symptomatic group, 31 were allocated to the AAE group, 25 to the LBO group, and 8 to the mixed-mechanism group.

Figure 1 The flow chart for the study. MCA, middle cerebral artery; ICA, internal carotid artery.

Vessel wall and plaque quantitative data for the asymptomatic and symptomatic groups

The inter-observer agreement for the manual measurements and judgement of enhancement was strong, and exhibited a robust level of consistency, as reflected by an ICC ranging from 0.907–0.964 (P<0.001). The symptomatic group (Figure 2) had a larger PA (5.79±2.16 vs. 4.74±1.58, P=0.007), a larger RI (1.08±0.10 vs. 0.94±0.10, P<0.001), and more enhanced plaques (52 vs. 14, P=0.001) in most narrowed sites than the asymptomatic group (Figure 3). Additionally, the symptomatic group had a smaller H₁ (1.42±0.33 vs. 1.96±0.49, P<0.001), H₃ (1.57±0.36 vs. 1.95±0.42, P<0.001), R₁₂ (P<0.001), and R₃₂ (P<0.001) (Table 2 and Figure 4).

Figure 2 The HR-MRI of a patient who had right MCA atherosclerotic stenosis and scattered cortical acute stroke lesions. (A) Scattered cortical acute stroke lesions on DWI. (B) MRA showed the stenotic site of the right MCA. The arrow indicates the stenosis site. (C) Plaque imaging at the midpoint between the beginning and the most stenotic site on T1WI. (D) Plaque imaging at the most stenotic site on T1WI. (E) Plaque imaging at the midpoint between the most stenotic site and the ending. (F) The plaque had obvious enhancement on enhanced T1WI. The arrow indicates the enhanced plaque. HR-MRI, high-resolution magnetic resonance imaging; MCA, middle cerebral artery; DWI, diffusion-weighted imaging; MRA, magnetic resonance angiography; T1WI, T1-weighted imaging.

Figure 3 HR-MRI of a patient who had left MCA atherosclerotic stenosis and a single infarction in the basal ganglia. (A) Single infarction in the basal ganglia on DWI. (B) MRA showed the stenotic site of the left MCA. The arrow indicates the stenosis site. (C) Plaque imaging at the midpoint between the beginning and the most stenotic site on T1WI. (D) Plaque imaging at the most stenotic site on T1WI. (E) Plaque imaging at the midpoint between the most stenotic site and the ending. (F) The plaque had enhancement on enhanced T1WI. The arrow indicates the plaque without enhancement. HR-MRI, high-resolution magnetic resonance imaging; MCA, middle cerebral artery; DWI, diffusion-weighted imaging; MRA, magnetic resonance angiography; T1WI, T1-weighted imaging.

Figure 4 Schematic drawing of the plaque curvature. H₂ represents the height of plaque at the most stenotic site; H₁ denotes the midpoint from beginning of the plaques to H₂; H₃ indicates the midpoint from H₂ to the ending of the plaques; R₁₂ = H₁/H₂; R₃₂ = H₃/H₂. MCA, middle cerebral artery.

Multivariate logistic regression analyses of plaque characteristics

The multivariate logistic regression analysis showed that the three models demonstrated excellent predictive performance with area under the curve (AUC) values of 0.878 [95% confidence interval (CI): 0.807–0.949, P<0.001], 0.925 (95% CI: 0.874–0.976, P<0.001), and 0.961 (95% CI: 0.952–0.994, P<0.001), respectively. Model 3 (RI + PA + enhancement + H₁ + H₂ + H₃ + R₁₂ + R₃₂), which was a combination of Models 1 and 2, showed the best predictive efficacy (Table 3 and Figure 5).

Figure 5 Receiver operating characteristic curves were constructed to predict stroke occurrence. The AUC values were 0.878, 0.925, and 0.961 for Model 1, Model 2, and Model 3, respectively. Model 1 = RI + PA + EP; Model 2, H₁ + H₂ + H₃ + R₁₂ + R₃₂; Model 3, Model 1 + Model 2. H₂ represents the height of plaque at the most stenotic site; H₁ denotes the midpoint from beginning of the plaques to H₂; H₃ indicates the midpoint from H₂ to the ending of the plaques; R₁₂, H₁/H₂; R₃₂, H₃/H₂. RI, remodeling index; PA, plaque area; EP, enhanced plaque; AUC, area under the curve.

Quantitative data of the vessel wall and plaques in the AAE and LBO groups

The number of superior/posterior plaques in the LBO group was greater than that in the AAE group (16 vs. 10, P=0.018). Other quantitative data such as the VA, LA, WA, NWI, PA, degree of stenosis, RI, H₁, H₂, H₃, R₁₂, and R₃₂ showed no significant differences (Table 4).

Discussion

This appears to be the first study to explore the relationship between plaques and acute ischemic stroke from the perspective of plaque curvature. We found that the symptomatic group had a larger PA, RI, and NWI_MNL, more enhanced plaques, and a smaller H₁, H₃, R₁₂, and R₃₂ than the asymptomatic group. The multivariate logistic regression analysis showed that the RI + PA + enhancement + H₁ + H₂ + H₃ + R₁₂ + R₃₂ model had the best predictive efficacy. Meanwhile, the AAE group had a greater number of superior/posterior plaques than the LBO group.

The application of HR-MRI in ICAD is advanced and widely employed, and has been the subject of a relatively large amount of research. The VA, LA, WA, and PA were measurement parameters commonly used in early research (19,20). Similar to a previous study (16,19,20), we found that the symptomatic group had a larger PA; however, the LA_MNL, VA_reference, and LA_reference were smaller in the symptomatic group than the asymptomatic group, and there were also some differences between other studies (14,21). To reduce the differences caused by individualization between the VA and LA, scholars have used the NWI to enhance comparability among vascular wall measurement parameters (22). We also found differences in the VA_reference and LA_reference between the two groups; however, the lack of a statistically significant difference in the NWI_reference indicated that the differences might not be clinically significant, and might have been caused by individual variations. Similar to previous studies (3,22), we found that the NWI_MNL, which reflects the plaque burden in the stenotic site, was larger in the symptomatic group than the asymptomatic group. Enhancement in plaques is believed to indicate localized active inflammation stemming from the accumulation of macrophages and neutrophils. This phenomenon has been acknowledged to be a sign of plaque vulnerability in MCA (8,9,17,23). Thus, our results were consistent with previous findings (8,9,17,23).

Vascular stenosis can lead to alterations in local hemodynamics, and the effect on hemodynamic parameters is particularly pronounced when the stenosis severity exceeds 50% (24). WSS is the principal parameter of hemodynamics, represents the tangential stress exerted by blood flow on the arterial wall, and is the primary force acting on the endothelial surface (25). In addition to the characteristics of plaques at the site of vascular stenosis, the local features of WSS are also related to the occurrence and recurrence of strokes (10,14,15). Meanwhile, the luminal curvature is a crucial factor influencing the local VSS (26), and the luminal curvature in the stenotic site depends on the plaque morphology. Thus, we conjectured that plaque curvature may reflect the luminal curvature. The surface morphology of plaques is complex and varied, and can currently only be represented using relatively simple parameters. Yang et al. (8) suggested that steepness is a geometric morphometric parameter that indicates the luminal curvature along the longitudinal axis, and used height/length to represent steepness.

In the present study, we used the height of plaques in the most stenotic site (H₂), the middle point from the beginning of the plaques to H₂ (H₁), and the middle point from H₂ to the ending of the plaques (H₃) to reflect the curvature of the plaque as much as possible. To reduce the diversity in the absolute height differences between the plaques and increase comparability, we also used ratios like R₁₂ (H₁/H₂) and R₃₂ (H₃/H₂) to compare the symptomatic and asymptomatic groups. We found that the symptomatic group had a smaller H₁, H₃, R₁₂, and R₃₂ than the asymptomatic group, but found no statistically significant difference in the H₂ between the two groups. A large R₁₂ and R₃₂ indicated that the plaque curvature was small; conversely, a small R₁₂ and R₃₂ indicated that the plaque curvature was large. The results of our study supported our hypothesis that a larger plaque curvature is more likely to cause ischemic stroke.

We also extracted more imaging information from traditional HR-MRI. The use of these three-point measurements and the plaque height ratio can indirectly demonstrate variations in WSS at the stenosis MCA, especially in hospitals lacking advanced WSS measurement capabilities. We had hoped to find some convenient and quick parameters to evaluate the risk of plaque in patients more quickly; although these parameters are simple and not comprehensive. We sought to provide parameters with as much diagnostic value as possible to clinicians and patients with limited images.

Various mechanisms contributed to ischemic stroke resulting from MCA atherosclerosis, including AAE (which is most common in patients with intracranial arterial stenosis), LBO, in situ thrombosis, and a combination of these mechanisms. AAE is thought to be caused by the instability or surface rupture of plaques, leading to the formation of microemboli that block downstream microcirculation; while LBO is thought to be caused by plaques blocking the opening of a branch artery or by disease of the branch artery (15,17). In our study, the AAE group had more enhanced plaques than the LBO group, but the difference was not statistically significant; however, this might be due to the small sample size of our study. The LBO group had more superior/posterior plaques than the AAE group, which is consistent with the findings of previous studies (3,19,20,27).

Our study had several limitations. First, it had a small sample size; thus, future studies with a larger number of subjects need to be conducted. Our research is still ongoing, and more cases will be examined in the future to further validate our research findings. Second, the exclusion of patients with MCA stenosis less than 50% limits the generalizability of our results. Third, the manual assessment of vessel wall and plaque parameters led to unavoidable measurement errors. Imaging experts in plaque analysis performed the measurements to minimize any measurement errors as much as possible. The future promotion and application of automatic measurement software will enable the resolution of manual measurement issues. Fourth, our study did not analyze plaque signal, pathological information and the length of plaque, which should be examined in future research. Fifth, we only analyzed two types of ischemic stroke resulting from MCA atherosclerosis. More types and mechanisms of infarction, and more cases need to be further investigated in the future. Sixth, the M1 segment of the MCA cannot be absolutely straight, which would inevitably have had some effect on our measurements. We hope that more precise parameters can be discovered in the future. Finally, measuring plaque height at three points and calculating their ratio may not fully capture the morphological features of the plaques. These factors should be addressed in future research.

Conclusions

The symptomatic group had a larger PA, RI, and NWI_MNL, more enhanced plaques, and a smaller H₁, H₃, R₁₂, and R₃₂ than the asymptomatic group. An association was found between plaque curvature and ischemic stroke, such that larger plaque curvature was more likely to cause ischemic stroke. Ischemic stroke resulting from MCA atherosclerosis had different mechanisms. The LBO group had more superior/posterior plaques than the AAE group.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-1552/rc

Funding: This study was funded by the National Natural Science Foundation of China (No. 82202128).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1552/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). The research protocol was approved by the Ethics Committee of the Nanjing Medical University (No. NMU20200320). All recruited patients provided verbal or written informed consent before they were examined.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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