|Year : 2022 | Volume
| Issue : 1 | Page : 85-92
Endovascular evaluation of intracranial atherosclerotic stenosis in a sample of Egyptian patients presented with ischemic stroke
Mahmoud M Hassan1, Khalid M Sobh2, Mahmoud Galal2, Salah I Ahmed1, Sherief M Al Shazly3, Abd Elaziz Shokry1
1 Department of Neurology, Al-Azhar University, Assiut, Egypt
2 Department of Neurology, Al-Azhar University, Cairo, Egypt
3 Department of Neurology, Al-Azhar University, Damietta, Egypt
|Date of Submission||30-Jun-2021|
|Date of Decision||06-Oct-2021|
|Date of Acceptance||13-Oct-2021|
|Date of Web Publication||4-Mar-2022|
MD Degree in Neurology Abd Elaziz Shokry
Al-Azhar University Hospitals, Assiut 08802
Source of Support: None, Conflict of Interest: None
Background and aim Intracranial atherosclerosis is an important etiology of ischemic stroke and is associated with multiple vascular risk factors. Endovascular evaluation is used for assessing patterns and distributions of intracranial atherosclerotic stenosis in a sample of Egyptian patients presented with ischemic stroke.
Patients and methods A total of 50 patients with ischemic stroke or transient ischemic attack were included. Assessment of the state of cerebral vessels before the procedure was done by duplex ultrasound, magnetic resonance angiography, and/or computed tomography angiography to confirm any stenosis in intracranial vessels. Neurological assessment was done before and after the procedure using the National Institutes of Health Stroke Scale score. Digital subtraction angiography was done to evaluate the degrees and patterns of stenosis.
Results A total of 50 participants (29 males and 21 females) were included. Their ages ranged from 30 to 78 years. The major risk factors were dyslipidemia (62.0%), hypertension (60.0%), diabetes mellitus (54.0%), smoking (48.0%), and atrial fibrillation (22.0%). The procedure was performed on 50 patients. A total of 39 (78.0%) patients had angiographic findings of vessel stenosis in either extracranial or intracranial vessels or both. In those 39 patients, 32 (64.0%) patients had arterial stenosis, and seven (14.0%) patients were found to have total occlusion. A total of 18 (36.0%) patients had angiographic findings of intracranial atherosclerotic stenosis. Of these 18 patients, 14 (28.0%) patients had arterial stenosis, and four (8.0%) patients were found to have total occlusion. The most common site of intracranial stenosis was middle cerebral artery (33.3%).
Conclusion Endovascular evaluation of patients with ischemic stroke is yielding, informative, safe, and easy to be done.
Keywords: intracranial atherosclerotic stenosis, digital subtraction angiography, ischemic stroke, endovascular evaluation, middle cerebral artery
|How to cite this article:|
Hassan MM, Sobh KM, Galal M, Ahmed SI, Al Shazly SM, Shokry AE. Endovascular evaluation of intracranial atherosclerotic stenosis in a sample of Egyptian patients presented with ischemic stroke. Al-Azhar Assiut Med J 2022;20:85-92
|How to cite this URL:|
Hassan MM, Sobh KM, Galal M, Ahmed SI, Al Shazly SM, Shokry AE. Endovascular evaluation of intracranial atherosclerotic stenosis in a sample of Egyptian patients presented with ischemic stroke. Al-Azhar Assiut Med J [serial online] 2022 [cited 2022 Jun 29];20:85-92. Available from: http://www.azmj.eg.net/text.asp?2022/20/1/85/339078
| Introduction|| |
Intracranial atherosclerotic stenosis (ICAS) of the intracranial arteries is one of the most common etiology of stroke worldwide and is associated with a high risk of recurrent stroke . Intracranial stenosis causes about 10% of strokes in white people, 20–29% of transient ischemic attacks (TIAs) or strokes in black people, and up to 40–50% of strokes in Asian people . The risk factors are broadly classified as nonmodifiable and modifiable, which are well documented, and potentially modifiable factors, which are less well documented, for example, DM and metabolic syndrome .
Transcranial Doppler ultrasound, magnetic resonance angiography, computed tomography angiography (CTA), conventional cerebral angiography, and high-resolution MRI were used as a diagnostic method to identify ICAS. Digital subtraction angiography is considered to be the ideal method for diagnosis of ICAS. Catheter cerebral angiography (CCA) is a safe and effective procedure for diagnosis of various intracranial and extracranial disorders and can be performed when the results of noninvasive imaging are unsatisfactory or when anatomical or hemodynamic information is needed and to simplify therapeutic interventions. The information gained by CCA, combined with clinical and noninvasive imaging results, can be used for diagnosis and follow-up of the results of a therapeutic intervention .
Intracranial stenosis presents with one or recurrent ischemic strokes and TIA . High-grade stenosis contributes to both the occurrence and magnitude of ischemic injury. Overall, 50% of patients have either lacunar, subcortical, or cortical infarction . The remaining patients with intracranial stenosis have multiple lesions involving a combination of cortical, subcortical, and lacunar infarctions . Endovascular treatment is a special challenge, and the selection of interventional techniques essentially differs from the treatment of extracranial stenosis. New technical approaches can be applied to avoid complications .
The aim of the study was to evaluate the pattern and distribution of ICAS in a sample of Egyptian patients presented with ischemic stroke using CCA.
| Patients and methods|| |
The study was carried out on the first 50 patients presented with acute ischemic cerebrovascular stroke and/or TIA. All of them underwent diagnostic cerebral angiography at the neurointerventional unit in our Neurology Department of El-Hussein University Hospital. The following patients were excluded from the study: patients with modified Rankin Scale more than or equal to 3, patients with major stroke within 4 weeks (National Institutes of Health Stroke Scale score ≥15), and/or with severe renal impairment precluding safe contrast medium administration, severe hypertension (blood pressure ≥180/100), uncorrectable coagulopathy, inability to achieve safe vascular access, severe tortuosity of aortic arch, common carotid artery or vertebral artery, intracranial hemorrhage, patients with other causes mimicking stroke (trauma, infection, or an intracranial malignancy), premorbid neurological disorders (peripheral neuropathy, myopathy, multiple sclerosis, dementia, and ataxia), and patients who refuse to participate in the study.
| Methods|| |
All of the patients underwent the following:
- Medical and neurological history, including history of comorbidities and risk factors.
- Neurological examination to diagnose the presence of a stroke and computed tomography brain to confirm the diagnoses.
- Assessment of cerebral vessels before the procedure; by using duplex ultrasound, magnetic resonance angiography and CTA on the arch and supra-aortic vessels may be used to confirm site of stenosis.
- Neurological examination before and after the procedure with assessment of any neurological insult (headache, altered of consciousness, TIA, or stroke).
- Laboratory investigations: CBC, PT, PTT, liver and kidney function tests, random blood sugar, lipid profile, and serum uric acid.
- ECG before the procedure.
- Diagnostic cerebral angiography, where the degree of stenosis is determined according to North American Symptomatic Carotid Endarterectomy Trial (NASCET) criteria. The luminal diameter at the point of greatest stenosis (D sten) (A) and at the normal part of the artery (D dist) (B) was measured, and the degree of stenosis was calculated as follows :
- No oral intake was allowed except medications for 6 h before the procedure.
- Placement of a peripheral intravenous access was done.
- In all patients recruited for diagnostic cerebral angiography, the procedure was done with regional anesthesia in the femoral puncture site or axillary region in the brachial approach, and appropriate cardiac monitoring was done; general anesthesia was done for patients who were not compliant.
- An 18-G puncture needle was used. A 5 F sheath (Check-Flo Performer Introducer set; Cook,
Bloomington, Indiana, USA) was slowly and continuously perfused with heparinized saline (10 000 U heparin per liter of saline) under arterial pressure, and a 0.035 ‘J-tipped hydrophilic
guide wire with puncture was inserted (Seldinger technique).
- During the first placement of the diagnostic catheter in the aortic arch, a 0.035 hydrophilic wire was used to proceed the diagnostic catheter into the vessels. The used catheter is a 5-Fr diagnostic catheter (Vertebral or Simmon II catheter; Boston Scientific or Cordis, Marlborough, Massachusetts, United States).
- Diagnostic cerebral angiography consists of visualization of both common carotid arteries including the external and the internal carotid artery, the carotid bulb, the siphon, the extracranial part, the intracranial part, and the T-carotid in several projections. Moreover, it includes both vertebral arteries and the basilar artery.
- Several projections should be considered such as the AP, lateral, oblique, and Towne views according to each case to visualize any pathology accurately.
- Catheter sheath removal and puncture site hemostasis were performed.
The study was approved by the ethical committee of Al-Azhar Assuit Faculty of Medicine. All steps of the study were clearly explained to all of the patients and/or family before doing the procedure, and written consents were obtained from all of the participants. The study was conducted in accordance with the Helsinki standards as revised in 2013.
The collected data were revised, organized, tabulated, and statistically analyzed using Statistical Package for the Social Sciences (SPSS), version 22.0 (SPSS Inc., Chicago, Illinois, USA) for Windows. Data are presented as mean±SD, frequency, and percentage. Categorical variables were compared using χ2 and Fisher’s exact tests (if required). Continuous variables were compared by Student t test (two-tailed). The level of significance was accepted if P value was less than 0.05. The sample size was not calculated before the study. We took the cases that fulfilled the inclusion criteria based on the available economic requirement.
| Results|| |
Patient demographics and clinical characteristics
A total of 50 patients with confirmed stroke and/or TIA who underwent diagnostic catheter angiography were included in the study. The patients had a mean±SD age of 57.7±10.7 years; 29 (58%) of them were males and 21 (42%) were females. The major risk factors were dyslipidemia in 31 (62.0%) patients, hypertension in 30 (60.0%) patients, diabetes mellitus (DM) in 27 (54.0%), smoking in 24 (48.0%) patients, atrial fibrillation (AF) in 11 (22.0%) patients, and eight (16.0%) patients had elevated uric acid ([Table 1]).
|Table 1 Assessment of risk factors in patients with intracranial atherosclerotic stenosis|
Click here to view
A total of 25 (50.0%) patients presented with left-side weakness and 20 (40.2%) patients with right-side weakness. Duplex ultrasound showed atherosclerotic changes with no significant stenosis in 33 (66.0%) patients. Moreover, CTA was done in 20 patients only with findings consistent with the catheter angiography in 13 (26.0%) patients, whereas it was inconsistent in seven (14.0%) patients. Distribution of patients according to National Institutes of Health Stroke Scale showing that moderate ischemic stroke was present in 34 (68%) patients ([Table 2]).
Complete blood count showed a low hemoglobin range (mean±SD=12.89±1.48), whereas a high platelet count (mean±SD=260.71±78.04). The bleeding profile and the renal function are crucial preprocedural, with normal ranges in both tests. The viral markers were done for all of the patients to ensure the proper infection control measures to be taken, and it showed four HCV-positive patients ([Table 3]).
A total of 39 (78.0%) patients had angiographic findings of vessel stenosis in either extracranial vessels or intracranial ones or both. In these 39 patients, 32 (64.0%) patients had arterial stenosis, and seven (14.0%) patients of them were found to have total occlusion. Cerebral catheter angiography was performed on 50 patients, of whom 18 (36.0%) had angiographic findings of ICAS in either anterior vessels or posterior ones or both. In these 18 patients, 14 (28.0%) patients had arterial stenosis, and four (8.0%) patients of them were found to have total occlusion. It was obvious that the extracranial vessels (carotid a. and vertebral a.) are more affected, whereas the intracranial anterior part, which includes the supraclinoid part of the ICA together with the middle cerebral artery (MCA) and the anterior cerebral artery (ACA), is affected in only 12 (24%) patients from the 50 patients who underwent diagnostic catheter angiography. On the contrary, the intracranial posterior part includes the intracranial part of the vertebral artery (V4) together with the basilar artery and the posterior cerebral artery (PCA), with stenosis documented in nine (18%) patients ([Table 4]).
|Table 4 Degree of stenosis in intracranial cerebral vessels by catheter angiography|
Click here to view
Extracranial part of ICA is the most affected artery in both sides; each of them was affected in 17 (34%) patients, whereas the least affected artery was the right extracranial part of vertebral artery in five (10%) patients. A total of 30 (60%) patients experienced significant stenosis more than 50%; seven (14.0%) of them had total occlusion, whereas the other 23 patients had stenosis ranging from more than 50% to subtotal occlusion (99%). The highest rate of significant stenosis was noted in the right and left extracranial parts of the ICA, whereas the least significant stenosis was noted in the right and left intracranial posterior circulation.
There were 44 cerebral vessels that had significant stenosis in 30 patients. Overall, eight patients experienced combined intracranial and extracranial significant stenoses. Of 50 patients, 18 (36%) patients had ICAS, ranging from 20% to total occlusion. Of whom, 14 (28%) had significant stenotic segments (>50%). Total occlusion was found in four (8%) patients ([Table 5]).
|Table 5 Degree of stenosis in extracranial cerebral vessels by catheter angiography|
Click here to view
In [Table 6], the distribution of 21 intracranial stenosis cases was as follows: MCA in seven (33.3%), basilar in four (19%), supraclenoid ICA in three (14.2%), PCA in three (14.2%), VA in two (9.5%), and ACA in two (9.5%) patients. The most common site of intracranial stenosis was MCA. There is a high significance of affection in intracranial vessels with total occlusion. MCA was totally occluded in three arteries, and PCA was occluded in one artery.
|Table 6 Number of vessels and distribution of intracranial vessel stenosis|
Click here to view
The distribution of vessel affection in total occlusion was significant in anterior circulation than posterior circulation either intracranial or extracranial. The posterior circulation is less affected with two vessels in extracranial and one in intracranial. In cases of a single stenosis, the total number of stenotic sites was 19 (48.7%). In cases of multiple stenosis, the total number of stenotic sites was 14 (35.9%) in two segments in the same patients, whereas three segments of stenosis were found in five (12.8%) patients. This means that multiple stenosis is important to identify and search for, as the percentage of multiple stenosis in patients is 52.3%, which is nearly half of the patients ([Table 7]).
| Discussion|| |
In our study, the mean age of patients was 57.7±10.7 years. There were 29 (58%) males and 21 (42%) females. Patients with ICAS had a mean age of 56.1±9.6 years, and this was consistent with the studies by Haghighi et al. ; Ssi-Yan-Kai et al. ; Shariat et al. ; Cancio et al. ; Homburg et al. ; Akins et al. ; and Moustafa et al. , where the mean ages were 66, 67.9, 66.7, 69.9, 68, 62, and 64.6 years, respectively. However, in the study by Suri et al. , the mean age was 76.2 years.
In the current study, the major risk factors of ICAS were as follows: hypertension presented in 13 (72.2%) patients, dyslipidemia in 12 (66.7%) patients, DM in 11 (61.1%) patients, smoking in 11 (61.1%) patients, AF in four (22.2%) patients, and uric acid in three (16.7%) patients at the time of intervention.
However, in the study by Haghighi et al. , hypertension presented in 78.3%, dyslipidemia in 43.3%, DM in 62.2%, and smoking in 27% of patients. Ssi-Yan-Kai et al. , reported that hypertension was present in 56.3%, dyslipidemia in 37.5%, DM in 25%, smoking in 18.8%, and AF in 6.3% of patients. Shariat et al. , reported that hypertension was present in 76.2%, dyslipidemia in 59.5%, DM in 57.8%, and smoking in 31% of patients. Cancio et al. , reported that hypertension was present in 75.9%, dyslipidemia in 66.3%, DM in 55.1%, and smoking in 18.8% of patients. Homburg et al. , reported that hypertension was present in 82%, dyslipidemia in 76%, DM in 30%, smoking in 31%, and AF in 8% of patients. Moustafa et al. , reported that hypertension was present in 75.8%, dyslipidemia in 60%, DM in 56.5%, and AF in 21% of patients. The most presenting symptom was hemiparesis, which was present in 46 (92%) patients. Of 50 patient, 18 (36%) patients had ICAS ranging from 20% to total occlusion; of whom, 14 (28%) had significant stenotic segments (>50%) and four (8%) had total occlusion.
ICAS was present in 18 (36%) of all patients, and this is consistent with the studies by Wong et al. , who reported that 37% of their studied patients with stroke had intracranial stenosis; Huang et al. , who reported that 51% of 96 patients presented with stroke had ICAS; Silva et al. , who reported that 54% of their studied patients with acute ischemic stroke had ICAS; and Suwanwela and Chutinetr , who reported that ICAS was seen in 47% of the studied patients with stroke.
However, this was inconsistent with the findings of White et al. , who reported intracranial stenosis was seen in 9, 15, and 17% of white, Hispanic, and African-American individuals with ischemic strokes, respectively; Markus et al. , who reported that intracranial stenosis was found in 17.9 and 2.1% of black and white patients with ischemic stroke, respectively, Weimer et al. , who reported that intracranial steno-occlusion was found in 11.4% of their studied patients; and Moustafa et al. , who reported that intracranial stenosis was present in 27% of Egyptian patients.
In intracranial stenosis, anterior circulation affection was present in the ICA (intracranial part). ACA and MCA affection was seen in 12 (24%) patients. However, in the posterior circulation, the affection was seen in nine (18%) patients. The distribution of 21 intracranial stenosis cases was as follows: MCA in seven (33.3%), basilar in four (19%), supraclenoid ICA in three (14.2%), PCA in three (14.2%), VA in two (9.5%), and ACA in two (9.5%) patients. The most common site of stenosis was MCA, which is supported by Dae et al. . The M1 segment of the middle cerebral artery was the most commonly involved one.
However, in the study by Moustafa et al. , it was reported that MCA was seen in 30.8%, basilar in 9.1%, supraclenoid ICA in 25.9%, PCA in 42%, VA in 7.7%, and ACA in 3.5% of patients. However, the study by Homburg et al. , reported that MCA was seen in 16%, basilar in 11%, supraclenoid ICA in 10%, PCA in 26%, VA in 30%, and ACA in 6% of patients. In our study, there was no significant difference between male and female affection with ICAS, and this is consistent with the study by Haghighi et al. ; Ssi-Yan-Kai et al. ; Shariat et al.  and Suri et al. . This finding disagrees with Cancio et al. ; Homburg et al. ; Akins et al.  and Moustafa et al. , who reported that males more than females are seen to have ICAS affection.
In our study, extracranial significant stenosis (46 arteries, 68.6%) was more common than intracranial significant stenosis (21 arteries, 31.4%). This was in agreement with the studies carried out on a white population by Wityk et al.  and Iranian population by Hossein et al. , where extracranial stenosis (58 and 57%, respectively) was seen more than intracranial stenosis (42 and 43%, respectively).
However, this was in contrast to the studies done in the South Korean Population and Chinese population (52% intracranial and 48% extracranial stenosis) . The high prevalence of extracranial stenosis may be owing to the easily accessible duplex ultrasound as a part of the initial investigations in stroke and owing to its limitation in examining the intracranial vasculature . Hence, Egyptian patients do not reach the advanced level of investigations that is required to assess the intracranial vessels after stroke. The most frequent intracranial stenosis was MCA, seen in seven (33.3%) of 21 intracranial segments. Anterior intracranial stenosis was seen in 12 (57.2%) as compared with the posterior intracranial stenosis seen in nine (42.8%). These findings are in agreement with the GESICA study .
Study limitations and conclusion
Intracranial stenosis is a common cause for ischemic stroke. Owing to the limitations of imaging studies, there are limited data on the prevalence of intracranial stenosis.
The prevalence of hypertension, dyslipidemia, and DM was more prevalent in intracranial stenosis.
ICAS is prevalent in the Egyptian stroke population (36%), similar to most non-white populations.
Middle cerebral artery is the most common site (33.3%) of intracranial stenosis in the Egyptian population.
Extracranial stenosis was even more prevalent than intracranial carotid artery disease, which should encourage future stroke prevention to target risk factor modification.
Follow-up research on symptomatic intracranial artery stenosis would provide a feasible basis for secondary prevention of patients with stroke.
The use of a risk-assessment tools should be considered as these tools can help identify individuals who could benefit from therapeutic interventions.
The authors would like to acknowledge the nurses and workers of the neurointerventional unit.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Gorelick PB, Wong KS, Bae HJ, Pandey DK. Large artery intracranial occlusive disease: a large worldwide burden but a relatively neglected frontier. Stroke 2008; 39:2396–2399.
Christine A, Holmstedt DO, Tanya N, Turan MD, Chimowitz MI. Atherosclerotic intracranial arterial stenosis: risk factors, diagnosis, and treatment. Lancet Neurol 2013; 12:1106–1114.
Qureshi AI, Feldmann E, Gomez CR, Johnston SC, Kasner SE, Quick DC et al.
Intracranial atherosclerotic disease: an update. Ann Neurol 2009; 66:730–738.
Wojak Joan C, Abruzzo TA, Bello JA, Blackham KA, Hirsch JA, Jayaraman MV et al.
Quality improvement guidelines for adult diagnostic cervicocerebral angiography. J Vasc Interv Radiol 2015; 26:1596–1608.
Ois A, Gomis M, Rodríguez-Campello A, Cuadrado-Godia E, Jiménez-Conde J, Pont-Sunyer C et al.
Factors associated with a high risk of recurrence in patients with transient ischemic attack or minor stroke. Stroke 2008; 39:1717–1721.
Khan A, Kasner SE, Lynn MJ, Chimowitz MI, and the Warfarin Aspirin Symptomatic Intracranial Disease (WASID) Trial Investigators. Risk factors and outcome of patients with symptomatic intracranial stenosis presenting with lacunar stroke. Stroke 2012; 43:1230–1233.
Cho KH, Kang DW, Kwon SU, Kim JS. Location of single subcortical infarction due to middle cerebral artery atherosclerosis: proximal versus distal arterial stenosis. J Neurol Neurosurg Psychiatry 2009; 80:48–52.
Nordmeyer H, Chapot R, Haage P. Endovascular treatment of intracranial atherosclerotic stenosis. Fortschr Röntgenstr 2019; 191:643–652.
Yan Y, Liang L, Chen T, Zhong C, Li P. Treatment of symptomatic vertebrobasilar artery stenosis with stent-assistant angioplasty in the elderly. Rev Assoc Med Bras 2012; 58:422–426.
Haghighi B, Mehrdad E, Amin SV, Shariat A, Banihashemi MA, Nikseresht A et al.
Large-vessel stenosis in the patients with ischemic stroke in Iran: prevalence, pattern, and risk factors. J Vasc Interv Neurol 2015; 8:12–19.
Ssi-Yan-Kai G, Nasr N, Faury A, Catalaa I, Cognard C, Larrue V, Bonneville F. Intracranial artery stenosis or occlusion predicts ischemic recurrence after transient ischemic attack. Am J Neuroradiol 2013; 34:185–190.
Shariat A, Niknam L, Izadi S, Salehi A. Prevalence of intracranial artery stenosis in Iranian patients with acute ischemic stroke using transcranial Doppler ultrasonography. Iran J Neurol 2016; 15:133–139.
Cancio E, Dorado L, Millán M, Reverté S, Suñol A, Massuet A et al.
The Barcelona-Asymptomatic Intracranial Atherosclerosis (AsIA) study: prevalence and risk factors. Atherosclerosis 2012; 221:221–225.
Homburg PJ, Plas GJJ, Sietske R, Lugt AV, Dippel DWJ. Prevalence and calcification of intracranial arterial stenotic lesions as assessed with multi-detector computed tomography angiography. Stroke 2011; 42:1244–1250.
Akins PT, Pilgram TK, Cross DTIII, Moran CJ. Natural history of stenosis from intracranial atherosclerosis by serial angiography. Stroke 1998; 29:433–438.
Moustafa RR, Moneim AA, Salem HH, Shalash AS, Azmy HA. Intracranial steno-occlusive arterial disease and its associations in Egyptian ischemic stroke patients. Stroke 2013; 44:538–541.
Suri MF, Qiao Y, Ma X, Guallar E, Zhou J, Zhang Y et al.
Prevalence of intracranial atherosclerotic stenosis using high-resolution magnetic resonance angiography in the general population: the atherosclerosis risk in communities study. Stroke 2016; 47:1187–1193.
Wong KS, Li H, Chan YL, Ahuja A, Lam WW, Wong A, Kay R. Use of transcranial Doppler ultrasound to predict outcome in patients with intracranial large-artery occlusive disease. Stroke 2000; 31:2641–2647.
Huang YN, Gao S, Li SW, Wong KS, Kay R. Vascular lesions in Chinese patients with transient ischemic attacks. Neurology 1997; 48:524–525.
Silva DA, Woon FP, Lee MP, Chen C, Chang H, Wong M. South Asia patients with ischemic stroke. Intracranial large arteries are the predominant site of disease. Stroke 2007; 38:2592–2594.
Suwanwela NC, Chutinetr A. Risk factors for atherosclerosis of cervicocerebral arteries: intracranial versus extracranial. Neuroepidemiology 2003; 22:37–40.
White H, Boden-Albala B, Wang C, Elkind MS, Rundek T, Wright CB, Sacco RL. Ischemic stroke subtype incidence among whites, blacks, and Hispanics: the Northern ManhaHan Study. Circulation 2005; 111:1327–1331.
Markus HS, Khan U, Birns J, Evans A, Kalra L, Rudd AG, Wolfe CD. Differences in stroke subtypes between black and white patients with stroke. The South London Ethnicity and Stroke Study. Circulation 2007; 116:2157–2164.
Weimer C, Goertler M, Harms L, Diener HC. for the German Stroke Study Collaboration. Distribution and outcome of symptomatic stenoses and occlusions in patients with acute cerebral ischemia. Arch Neurol 2006; 63:1287–1291.
Dae CH, Lee SH, Kim KR, Park ST, Lim SM, Kim SJ et al.
Pattern of atherosclerotic carotid stenosis in Korean patients with stroke: Different involvement of intracranial versus extracranial vessels. Am J Neuroradiol 2003; 24:239–244.
Wityk RJ, Lehman D, Klag M, Coresh J, Ahn H, Litt B. Race and sex differences in the distribution of cerebral atherosclerosis. Stroke 1996; 27:1274–1980.
Hossein Z, Ebrahimi H, Shafiee K. Intracranial stenosis in patients with acute cerebrovascular accidents. ARYA Atherosc J 2008; 3:206–210.
Wong KSL, Chen C, Fu J, Chang HM, Suwanwela NC, Huang YN et al.
Association between CYP2C19 loss-of-function allele status and efficacy of clopidogrel for risk reduction among patients with minor stroke or transient ischemic attack. JAMA 2016; 316:70–78.
Mazighi M, Tanasescu R, Ducrocq X, Vicaut E, Bracard S, Houdart E, Woimant F. Prospective study of symptomatic atherothrombotic intracranial stenosis: the GESICA study. Neurology 2006; 66:1187–1191.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7]