Evaluation of Infarction Pattern in Patients with Symptomatic Intracranial Atherosclerosis: TCCD and MRI Study

Introduction

Intracranial atherosclerosis - or intracranial atherosclerotic disease (ICAD) - is a dynamic disease characterized by progre-ssing atherosclerotic plaques in major intracranial arteries. Risk factors for ICAD include age, ethnicity, hypertension and diabetes mellitus. Patients with ICAD have a 10 - 20% annual risk of stroke. The risk is more serious in patients with (70–99%) degree of stenosis. ICAD now considered as the commonest cause of ischemic stroke worldwide ^{(1, 2, 3, 4, 5)}.

There are five main imaging modalities for diagnosing ICAD: transcranial doppler (TCD) and transcranial color-coded duplex (TCCD) ultrasonography, computed tomo-graphy angiography (CTA), magnetic reso-nance angiography (MRA), vessel wall magnetic resonance imaging (VWMRI) and conventional angiography. The former 4 modalities are non-invasive, but conven-tional angiography is invasive.

TCCD is a bedside examination, and not expensive. With MRA brain parenchyma

can also be examined simultaneously, with no contrast or radiation exposure. But CTA still has superior spatial resolution over MRA ^{(6, 7, 8, 9, 10)}.

Four main patterns of ischemic stroke have been identified in patients with symptom-matic ICAD: perforator, territorial, border-zone and mixed ^{(11, 12)}.

This study aims at studying the demo-graphic, clinical and imaging character-ristics (emphasizing the infarction pattern) in patients with symptomatic ICAD.

Patients and Methods

This cross-sectional study was conducted during the period between November 2021 and July 2022 on patients with acute ischemic stroke recruited from the stroke units of Minia University and Kasr Alainy hospitals. Age of patients included was ≥ 40, of both sexes.  Patients presented with intracerebral hemorrhage, patients with general medical illness (e. g. liver or kidney impairment), autoimmune vasculitis and malignancies have been excluded. We also excluded patients with poor acoustic window as well as patients with extracranial stenosis ≥ 50%. Diagnosis and quantification of the extracranial stenosis followed Sabeti et al., 2004 ⁽¹³⁾.

All patients were subjected to complete history taking emphasizing stroke risk factors (e.g. hypertension, diabetes, cardiac disease, smoking and prior stroke or transient ischemic attack), general exami-nation including vital signs and cardiac examination, and meticulous neurological examination and National Institutes of Health Stroke Scale (NIHSS).

Laboratory investigations including complete blood picture, liver and kidney functions, glycated hemoglobin and fasting lipid profile have been done.

All patients were subjected to 1.5 Tesla brain MRI examination including the Diffusion-Weighted Imaging (DWI) for identification of the ischemic insult and its location and pattern; and vascular imaging of extracranial and intracranial carotid and vertebrobasilar systems. Duplex scanning was performed by qualified neuro-vascular operators using Philips iU22 machine. The acoustic windows commonly employed were the trans-temporal and the subocci-pital. Diagnosis of the intracranial stenosis followed Baumgartner et al., 1999 ⁽¹⁴⁾.

The research was conducted after the approval of the Ethical Review Committee of Faculty of Medicine, Minia University (No. dt-20-470). All patients (or their 1^st degree relatives) signed an informed consent for intervention including the advantages, disadvantages, and risks of possible complications.

Statistical Analysis

Qualitative data have been presented as number and percentages while quantitative data have been presented as mean, standard deviations and ranges when their distri-bution was parametric.  The comparison between two groups with qualitative data has been done using Fisher exact test (the expected count in any cell was less than 5). Comparison between four independent groups with quantitative data and para-metric distribution was done with One WAYANOVA Test. All statistical calcu-lations were done using computer programs SPSS (Statistical Package for the Social Science; SPSS Inc., Chicago, IL, USA) version 20 for Microsoft Windows. P-value < 0.05 = significant & P < 0.001 = highly significant.  

Results

Forty two patients have been included in this study; 22 males (52.4%) and 20 females (47.6%). Their ages ranged between 40 to 90 years (mean ± SD = 60.17 ± 13.73). Twenty patients (47.6%) were from Minia and 22(52.4%) were from Cairo.

Figure (1): Distribution of the studied cases according to Risk Factors.

HTN: Hypertension, IHD: Ischemic Heart Disease.

Hypertension was the most common risk factor (59 %), followed by dyslipidemia and diabetes.

The NIHSS ranged from 2 to 20 (with mean11.17 ± 4.75). Language impairment and motor symptoms were the most frequent (83.3% and 81% respectively), while ataxia was the least frequent symptom (14.3%).

Table (1): Distribution of the studied cases according to stenotic arteries.

Figure (2): Distribution of the studied cases according to which artery is symptomatic.

ICA: internal carotid artery. MCA: middle cerebral artery. ACA:  anterior cerebral artery.

PCA: posterior cerebral artery.

Most of our patients (71.4%) had stenosis in more than one artery. MCA was the commonest artery to be stenotic (25 patients i.e. 69.6%), among them 18 patient (42.9%) were symptomatic.

On the other hand, ACA was the least artery to be stenotic (7 patients i.e. 16.7%), among them only 2 patients (4.2%) were symptomatic.

Table (2): Distribution of the studied cases according to Parenchymal imaging findings.

SVD: small vessel disease

Figure (3): Distribution of the studied cases according to Infarction pattern.

Regarding the infarction site, 20 (47.6%) cases had subcortical infarcts and 21 (50.0%) cases had combined cortical and subcortical infarcts. Only one patient had

an isolated cortical infarction. Territorial infarction was the most common pattern (59.5%) followed by perforator, border-zone and the mixed pattern. 

Table (3): Comparison between infarction patterns of anterior vs. posterior circulation.

Territorial pattern was the dominant pattern among those with anterior circulation symptomatic stenosis. But in patients with posterior circulation symptomatic stenosis both territorial and perforator patterns were the most prevalent.

Table (4): Relation between NIHSS and infarction pattern.

There was a statistically significant difference between NIHSS scores in different patterns of infarctions; the lowest scores were among those with perforator infarction patterns, while those with territorial pattern had the highest scores.

Discussion

Forty two patients have been included in this study; 22 males and 20 females. Their ages ranged between 40 to 90 years. The most common risk factors seen in our patients were hypertension, dyslipidemia and diabetes. That was in agreement with López-Cancio et al., 2012 who studied risk factors in patients with asymptomatic ICAD in Spanish population; and Tsivgoulis et al., 2014 who did the same but in patients with symptomatic ICAD in Caucasian population ^{(15, 16)}. It was also in agreement with Zürcher et al., 2019 who studied patients with both anterior and posterior circulation ischemic strokes ⁽¹⁷⁾.  

The NIHSS score ranged from 2 to 20 in our sample. Language impairment and motor symptoms were the most frequent, while ataxia was the least frequent symptom. That could be explained by our results in which MCA was the commonest artery to have symptomatic stenosis; and that was also consistent with  Yew and  Cheng 2009, who found that dysphasia, dysarthria and hemiparesis were the most common presenting features in patients with ischemic strokes ⁽¹⁸⁾. 

Regarding the distribution of studied patients according to stenotic arteries, MCA was the commonest artery to be symptomatically stenotic (18 patients); followed by basilar artery (11 patients), and then both the vertebral and internal carotid arteries. That was exactly the same order reported by Banerjee and Chimowitz, 2017 in their review about stroke caused by atherosc-lerosis of major intracranial arteries ⁽²⁾.   

Regarding the infarction pattern, territorial infarction was the most common (59.5%) followed by perforator, borderzone and the mixed pattern. That was in agreement with Kim et al., 2012 who studied 657 patients with ischemic stroke caused by ICAD in a 9-center Korean study.  Territorial pattern has been seen in 65.3% of patients, followed by the perforator pattern in 21.0%, then the borderzone and mixed patterns⁽¹⁹⁾.  López-Cancio et al., 2014 also studied 136 patients with symptomatic ICAD. Territorial pattern was the most prevalent in 50.7% of patients, followed by the perforator pattern in 25%, then the borderzone and mixed patterns ⁽¹²⁾.

In our sample, territorial pattern was the dominant pattern among those with anterior circulation symptomatic stenosis. But in patients with posterior circulation sympto-matic stenosis both territorial and perfo-rator patterns were the most prevalent. The higher prevalence of perforator pattern in patient’s posterior circulation symptom-matic stenosis was also in agreement with the results obtained by López-Cancio et al., 2014 who describes the extension of atherosclerotic plaques to perforators as an important mechanism of ischemia in the posterior circulation ⁽¹²⁾.

In our study, there was a statistically significant difference between NIHSS scores in different patterns of infarctions; the lowest scores were among those with perforator infarction patterns, while those with territorial pattern had the highest scores. That can be simply explained by larger size of the territorial pattern caused by occlusion of the main intracranial arteries. These results augment findings by Hussain et al., 2018 who studied the correlation between clinical and radiolo-gical features of different infarcts patterns. Territorial infarcts were associated with the poorest clinical outcome ⁽²⁰⁾.  

Conclusions

MCA was the commonest to have symptomatic ICAD, followed by basilar artery, and then both the vertebral and internal carotid arteries. Territorial pattern was the dominant pattern among those with anterior circulation symptomatic stenosis. But in patients with posterior circulation symptomatic stenosis both territorial and perforator patterns were the most prevalent. Territorial pattern had the highest NIHSS scores.