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ORIGINAL ARTICLE
Year : 2021  |  Volume : 69  |  Issue : 6  |  Page : 1663-1669

The Relationship between Patterns of Remodeling and Degree of Enhancement in Patients with Atherosclerotic Middle Cerebral Artery Stenosis: A High-Resolution MRI Study


Department of Radiology, Nanjing First Hospital, Nanjing Medical University, Nanjing 210006, China

Date of Submission18-Dec-2018
Date of Decision08-Nov-2019
Date of Acceptance25-Sep-2020
Date of Web Publication23-Dec-2021

Correspondence Address:
Dr. Yu-Chen Chen
Department of Radiology, Nanjing First Hospital, Nanjing Medical University, No. 68, Changle Road, Nanjing 210006
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.333443

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 » Abstract 


Purpose: The aim of this research was to investigate the relationship between remodeling patterns and degree of enhancement in patients with atherosclerotic middle cerebral artery (MCA) stenosis using high-resolution magnetic resonance imaging (HR-MRI).
Materials and Methods: From August 2015 to May 2016, 38 consecutive patients with unilateral MCA stenosis on time-of-flight (TOF) MR angiography were prospectively enrolled. The routine MR scan and cross-sectional images of the stenotic MCA vessel wall on HR-MRI were performed in all patients. Among them, 17 patients displayed positive remodeling (PR) and the other 21 patients displayed negative remodeling or non-remodeling (non-PR). The patients displaying hyperintense on diffusion-weighted imaging (DWI) in the territory of ipsilateral stenotic MCA were considered to have had acute stroke. Subsequently, the differences in the degree of enhancement and the number of acute stroke patients between the PR group and the non-PR group were compared. The Spearman rank correlation analysis of the enhancement degree (ED) and the remodeling index (RI) was calculated. Then, receiver operating curve (ROC) was used to evaluate diagnostic efficiency of RI and ED for acute infarction.
Results: The PR group had more obvious enhancement plaques than the non-PR group (10 versus 3, P = 0.006). The PR group also had a larger number of acute stroke patients than the non-PR group (15 versus 4, P = 0.000). The spear-man rank correlation analysis showed that the degree of enhancement had a weak positive correlation with the remodeling index (r = 0.379, P = 0.019). The area under the curve (AUC) of RI and ED was higher than that of RI (0.924: 0.842).
Conclusion: The PR, obvious enhancement predicted vulnerable plaques that were more prone to causing acute stroke. RI and ED had valuable diagnostic efficiency for acute infarction.


Keywords: Acute stroke, atherosclerosis, high-resolution MRI, remodeling pattern
Key Message: HR-MRI has emerged as a valuable method to disclose the characteristics of intracranial arteries' wall and atherosclerotic plaque. PR, obvious enhancement was risk factors which reduced plaques' stability and caused acute stroke.


How to cite this article:
Zhang DF, Wu XY, Zhang WD, Wang M, Yin X, Chen YC. The Relationship between Patterns of Remodeling and Degree of Enhancement in Patients with Atherosclerotic Middle Cerebral Artery Stenosis: A High-Resolution MRI Study. Neurol India 2021;69:1663-9

How to cite this URL:
Zhang DF, Wu XY, Zhang WD, Wang M, Yin X, Chen YC. The Relationship between Patterns of Remodeling and Degree of Enhancement in Patients with Atherosclerotic Middle Cerebral Artery Stenosis: A High-Resolution MRI Study. Neurol India [serial online] 2021 [cited 2022 Jan 18];69:1663-9. Available from: https://www.neurologyindia.com/text.asp?2021/69/6/1663/333443




Stroke is a serious threat to global public health throughout the world due to its high mortality and morbidity.[1] Intracranial atherosclerotic disease is one of the major causes of stroke, especially in Asian population.[2],[3],[4] Moreover, MCA was the most common location for atherosclerotic stenosis in intracranial arteries, accounting for 40-70% of all atherosclerotic stenosis.[5] In the past, the degree of arterial stenosis was thought to be a fundamental reflection of cerebral ischemic risk.[6] However, with the development of HR-MRI and its extensive use in intracranial arteries, some research has suggested that it was not appropriate to assess stroke risk by stenosis alone.[5],[7],[8],[9] In actuality, it was the characteristics of stenotic vessel walls and plaques that were more closely related to the incidence of ischemic stroke.[10],[11],[12],[13]

Characteristics of atherosclerotic stenotic MCA mainly included plaque distribution, signal intensity, remodeling patterns, and degree of enhancement. Previous studies reported plaques located superiorly were more frequently observed in the symptomatic patients, possibly because they were closer to the orifices of the perforating arteries.[1],[8],[14],[15] Different plaque signals might imply different stability, and Wu et al.[4] suggested that hyperintense signals could predict artery-to-artery infarction; Natori et al.[16] found that the signal intensity of intracranial plaques was significantly higher in patients with acute stroke, which was thought to arise from intra-plaque hemorrhage and reduced plaque stability. The PR of atherosclerotic arteries caused the vessel enlargement and to some extent, alleviated vessel stenosis. However, the PR group had larger plaque area than the negative remodeling (NR) group,[6],[10] which might be more likely to lead to acute cerebral infarction. Qiao et al.[17] discovered that the contrast enhancement of intracranial atherosclerotic plaque was associated with recent ischemic events and could serve as a marker of their stability. Similarly, Lu et al.[13] thought strongly enhanced plaques played a complementary role to vessels' stenosis in determining the occurrence of acute stroke. Nevertheless, few studies have focused on the relationship between the remodeling and enhancement of plaques.

Sufficient understanding of remodeling and enhancement of plaque in atherosclerotic MCA was helpful for us to recognize the instability of plaques and then to evaluate the risk of stroke. Therefore, the present study aims to comprehensively determine the relationship between remodeling patterns and the degree enhancement in patients with atherosclerotic MCA stenosis.

Subjects and clinical data

Approval for the study was obtained by the Ethics Committee of our university. Informed consent was obtained from all the participants.

From August 2015 to May 2016, 38 consecutive patients with suspected MCA atherosclerotic disease (such as dizziness, alalia, limb weakness, or drowsiness) from the Department of Neurology were recruited. All patients underwent standard MR scan protocols including axial plain scan T1WI, T2WI, T2-fluid attenuated inversion recovery (FLAIR), DWI, time-of-flight MR angiography (TOF-MRA) within one week after admission. The criteria for patient enrollment in this study included: (1) without contraindications to MR scan; (2) two or more atherosclerotic risk factors; (3) single MCA M1 segment stenosis >30% was showed on MRA; (4) the stenosis of the ipsilateral internal carotid artery was less than 50%; (5) without non-atherosclerotic vasculopathy, such as cerebral hemorrhage, vasculitis, dissection, moyamoya disease, arterial fibrillation, cardioembolism, tumor etc.; (6) the quality of the imaging was sufficient to be used for diagnosis and analysis.

Demographic and clinical characteristics of patients were obtained from their medical record after MR scan, including sex, age, smoking, alcoholism, hypertension, diabetes, blood glucose, HbA1c, total cholesterol, low-density lipoprotein (LDL), high-density lipoprotein (HDL), triglycerides, homocysteine, phospholipase-A2, white blood cell count, and time from admission to HR-MRI examination, location of stenosis and the National Institutes of Health Stroke Scale (NIHSS).

All patients underwent the HR-MRI of stenotic MCA using a 3-Tesla MR scanner (Ingenia, Philips Medical Systems, Netherlands) with an 8-channel receiver array head coil. TOF-MRA was reconstructed to determine the blood vessel architecture, which was then used for positioning to ensure the stenosis of MCA. We performed HR-MRI scanning, including black-blood T1WI, proton density-weighted imaging (PDWI), T1WI enhancement (T1WI+C), which perpendicular to the M1 segment of stenotic MCA. The imaging sequences of HR-MRI were applied with following parameters: (1) TOF-MRA: repetition time (TR), 22 ms; echo time (TE), 3.45 ms; matrix size, 332 × 227; field of view (FOV), 200 mm × 84 mm; slice thickness, 0.6 mm; slice number, 140; number of excitation (NEX), 1. (2) T1WI: TR, 1,000 ms; TE, 9 ms; matrix size, 180 mm × 144 mm; FOV, 80 mm × 80 mm; slice thickness, 2.0 mm; slice gap, 0 mm; and slice number, 6; NEX, 2. (3) PDWI: TR, 2,000 ms; TE, 9 ms; matrix size, 180 mm × 144 mm; FOV, 80 mm × 80 mm; slice thickness, 2.0 mm; slice gap, 0 mm; and slice number, 6; NEX, 2. (4) T1WI+C: TR, 1,000 ms; TE, 9 ms; matrix size, 180 mm × 144 mm; FOV, 80 mm × 80 mm; slice thickness, 2.0 mm; slice gap, 0 mm; and slice number, 6; NEX, 2. A bolus of 15 ml gadodiamide (Kang chen, Guangzhou, China) was administered by an MRI power injector (Ingenia, Philips Medical Systems, Netherlands) at a rate of 2 ml/s. the MR images was repeated 5 minutes after contrast material administration.

MR image processing

All parameter measurements were performed on Philips Intellispace Portal workstation. We magnified the short axial PDWI images to 300% and measured the vessel area (VA) of the stenotic MCA at the most narrowed lumen (MNL) and at the reference site. The reference site was the nearest plaque-free or minimally diseased segments proximal to the stenotic MCA. If a proximal reference site was not available, then the neighboring distal site was used instead.

The remodeling index (RI) = VAMNL/VAreference. We defined RI ≥ 1.05 as PR, RI ≤ 0.95 as NR, 0.95 < RI < 1.05 as non-remodeling. The measurements were completed within two days after scanning and performed by two professional radiologists, who were blinded to clinical details, and then the average value was calculated and applied. The slice for measurement was agreed upon between two observers.

Plaque contrast enhancement grade was categorized[17]: grade 0, enhancement was less than or equal to that of normal intracranial arterial walls in the same patient; grade 1, enhancement was greater than that of grade 0 but less than that of pituitary infundibulum; and grade 2, enhancement was greater than or equal to that of the pituitary infundibulum. The degree of enhancement reached a consensus between two experienced associated chief-physician.

Statistical analysis

All data were analyzed by using SPSS21.0 package (Chicago, IL, USA). Quantitative data was expressed as the mean ± standard deviation. The T test was used for quantitative data between groups. Categorical values were summarized using counts and percentages. Fisher exact test was used for categorical variables. The Spearman rank correlation analysis between RI and degree of enhancement was performed. Values of P < 0.05 were defined as statistical significance.


 » Results Top


In total, 38 consecutive patients with MCA M1 segment stenosis underwent 3.0 Tesla HR-MRI, PR was found in 17 patients, whereas the remaining 21 patients belonged to the non-PR group. The differences in sex, smoker, alcoholism, hypertension, diabetes, location of stenosis, age, blood glucose, HbA1c, HDL, LDL, total cholesterol, triglycerides, phospholipase-A2, homocysteine, white blood cell count, time from admission to HR-MRI examination between PR group and non-PR group exhibited no statistical significance, but the NIHSS score was higher in the PR group (P = 0.029) [Table 1].
Table 1: Demographic and clinical characteristics of PR group and non-PR group

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Regarding the aspect of degree of enhancement, there were 5 grade 0, 2 grade 1, and 10 grade 2 in the PR group; and 15 grade 0, 3 grade 1, and 3 grade 2 in the non-PR group. The PR group had more plaques that displayed obvious enhanced than non-PR group, the difference was statistically significant (P = 0.006). The PR group also had a larger number of acute stroke patients than the non-PR group (15 versus 4, P = 0.000) [Table 2]. [Figure 1] showed images of a symptomatic MCA stenosis in a 42-year-old male who presented with right limbs fatigue for 3 days. DWI displayed an acute ischemic stroke in the distribution of the left MCA. The M1 segment was PR, and the plaque had obvious enhancement. In contrast, [Figure 2] showed images of an asymptomatic MCA stenosis in an 83-year-old male who presented with dizziness for a half day. DWI shows normal. The M1 segment of left MCA was NR, and the plaque had no enhancement.
Figure 1: HR-MRI of a patient with symptomatic MCA stenosis. (a) Severe stenosis of the M1 segment of left MCA (white arrow). (b) An acute ischemic stroke in the distribution of the left MCA. (c) The plaque in T1WI (black arrow). (d) Measurement at the most narrowed site in PDWI. (e) Measurement at the reference site in PDWI. (f) The plaque has grade 2 enhancement (white arrow)

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Figure 2: HR-MRI of a patient with asymptomatic MCA stenosis. (a) Severe stenosis of the M1 segment of left MCA (white arrow). (b) DWI shows normal. (c) The plaque in T1WI (black arrow). (d) Measurement at the most narrowed site in PDWI. (e) Measurement at the reference site in PDWI. (f) The plaque has grade 0 enhancement (white arrow)

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Table 2: Plaque enhancement in the PR group and non-PR group

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The Spear-man rank correlation analysis displayed that degree of enhancement had a weak positive correlation with RI, value of r was 0.379, P = 0.019 [Figure 3].
Figure 3: The distribution of remodeling index and enhancement degree of plaques, there is a weak positive correlation between the two parameters

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ROC analysis revealed the AUC for RI and ED was higher than RI lonely (0.924: 0.842) [Figure 4], which indicated a better diagnostic efficiency for acute infarction.
Figure 4: Comparisons of ROC curves using RI, RI+ED to determine an occurrence of acute infarction. The AUC of RI+ED was higher than that of RI

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 » Discussion Top


The present study demonstrated that the patients with PR of atherosclerotic MCA stenosis had more obvious enhanced plaques than the patients with non-PR. A positive correlation between the remodeling index and degree of enhancement was observed. Meanwhile, the PR group had larger NIHSS scores and a higher number of acute stroke in the MCA territory than the non-PR group. Moreover, the AUC for RI and ED was higher than RI lonely. Thus, we suggested that PR and obvious plaque enhancement were risk factors that reduced plaques' stability and increased risk for acute stroke. On the other hand, this study also proved that HR-MRI can be used to display the vessel wall and plaques clearly without causing radiation damage to patients. It is considered as a promising tool to detect the features of intracranial artery walls.

Remodeling is a compensatory phenomenon occurring in arterial walls during the formation of atherosclerotic plaques.[18] It was first discovered by Glagov et al.[19] in earlier studies of coronary arteries. Subsequently, some research reported that PR was predominantly occurred in symptomatic patients in both coronary[19],[20],[21] and carotid arteries.[22],[23] Recently, with the development and application of HR-MRI in intracranial arteries, the same remodeling patterns were observed in the MCA and basilar artery.[7],[8],[24],[25] The current study was consistent with previous research. In addition, the NIHSS score was higher in the PR group. As we know, the NIHSS score reflects the severity of a stroke[26] and associated with plaque burden in symptomatic MCA stenosis.[27] Therefore, we believed that PR was a predictor of plaque stability which revealed vulnerable plaques that were more likely to cause acute ischemic stroke.

In recent years, many investigations have focused on the clinical significance of the Gadolinium enhancement of plaques in site of the intracranial arterial stenosis.[28],[29],[30],[31] Meanwhile, these studies have described that plaque enhancement on HR-MRI can help to identify the responsible plaques and can potentially sever as a marker of culprit plaques. Accordingly, pathological studies have expressed the similar viewpoints.[32] In our research, it was found that patients with obviously enhanced plaques experienced acute ischemic stroke even more often. However, there was little literature discussed of relationship between remodeling and degree of enhancement. Clarifying the association between these factors could help us to better recognize the plaques instability and to more accurately assess stroke risk. The present study revealed that PR plaques were more prone to generating obvious enhancement. There was a weak positive correlation between remodeling index and degree of enhancement. Thus, the patients exhibiting PR or showing obvious plaque enhancement should actively seek therapeutic intervention, especially in the period prior to an acute stroke. At the same time, we found that combinations of RI and ED could improve diagnostic efficiency for acute infarction.

The current study also includes some additional limitations. First, this was a prospective study with a limited number of patients. A prospective study with larger sample size should be performed to establish the relationship between vessel wall characteristics of a stenotic MCA, plaques' features and subsequent acute ischemic stroke. Second, the calculation of RI depended on the reference vessel area. We chose a proximal or distal segment as a reference site, which might cause an underestimation or overestimation of the RI due to the natural tapering of the MCA. However, using the average of distal and proximal to the stenosis for the remodeling calculation might result in measurement error mainly due to times of measurements were performed. Therefore, we should further develop more accurate tools for measurement. Third, the degree of enhancement of atherosclerotic plaques was a subjective judgement made by two radiological associate chief-physicians rather than an accurate measurement. Quantifying the degree of enhancement should be taken in future research. Fourth, the entire population of our study had moderate or severe MCA stenosis. Since we did not include the patients with mild stenotic MCA (<30%), this implied that our findings were not applicable to all patients with MCA stenosis. Fifth, although patients with ipsilateral carotid stenosis greater than 50% were excluded, we could not completely exclude the influence from carotid plaques with stenosis of less than 50%. Fortunately, the ultrasound can be used to monitor carotid plaques and thus minimize the impact of carotid plaques on the study's limitations. Sixth, our study was lack of pathological information to differentiate blood products within the plaques. Lastly, we performed HR-MRI scanning perpendicular to the M1 segment of stenotic MCA as much as we can, however, the scanning vessels were not perfectly straight. This might have a slight influence for observation. We would choose the most standard cross-sectional images in research, to our best. The above factors should be taken into consideration in future research.


 » Conclusion Top


In summary, there were more patients with obvious plaque enhancement in the PR group than that in the non-PR group regarding atherosclerotic MCA stenosis. The degree of enhancement had a positive correlation with the remodeling index. The current study also proved that HR-MRI was a valuable method to depict the characteristics of intracranial vessel wall and their plaques.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Acknowledgements

This work was funded by Jiangsu Provincial Special Program of Medical Science (No. BE2017614), Youth Medical Talents of Jiangsu Province (No. QNRC2016062), and 14th “Six Talent Peaks” Project of Jiangsu Province (No. YY-079).

Financial support and sponsorship

Yu-Chen Chen.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2]



 

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