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 Table of Contents  
ORIGINAL ARTICLE
Year : 2016  |  Volume : 53  |  Issue : 2  |  Page : 89-95

Site and degree of intracranial arterial stenosis in acute stroke patients with metabolic syndrome among a sample of Egyptian patients


1 Department of Neurology, Faculty of Medicine, Ain Shams University, Cairo, Egypt
2 Department of Endocrinology; Department of Internal Medicine, Faculty of Medicine, Ain Shams University, Cairo, Egypt

Date of Submission21-Jun-2016
Date of Acceptance21-Feb-2016
Date of Web Publication2-Jun-2016

Correspondence Address:
Doaa A Elaidy
MD, Departments of Neurology and Psychiatry, Ain Shams University, Cairo
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/1110-1083.183409

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  Abstract 

Background
Type 2 diabetes mellitus (T2DM) has various effects on the vascular tree, both macrovascular and microvascular and both intracranial and extracranial circulation. Metabolic syndrome is a combination of medical disorders that, when occurring together, increases the risk of developing cardiovascular diseases including stroke.
Objectives
In this study, we aimed to estimate the site and degree of intracranial arterial stenosis among patients clinically diagnosed as acute ischemic stroke patients with metabolic syndrome with or without T2DM.
Patients and methods
This cross-sectional study included 100 patients admitted in Ain Shams University Specialized Hospital-Stroke Unit with the diagnosis of clinically first-ever cerebral infarction and metabolic syndrome with or without T2DM. All patients were subjected to detailed medical history, thorough general and neurological examination, full laboratory investigations, computerized tomography, MRI, and magnetic resonance angiography of the brain, carotid duplex, ECG, and echocardiography.
Results
Small vessel disease (lacune) was present more frequently in patients with T2DM than in those without T2DM, and this showed a statistically significant difference (P = 0.008). It was found that intracranial stenosis was statistically significantly higher compared with extracranial carotid stenosis in patients with T2DM with total or near-total occlusion, with P values less than 0.05. These stenoses or occlusions also tend to be multiple in the same group of patients with T2DM (P = 0.033).
Conclusion
Diabetic patients with acute ischemic stroke have a higher severity of intracranial arterial stenosis, higher incidence of multiple intracranial arterial stenoses, and lastly higher tendency to have obstructive intracranial arterial lesions.

Keywords: Acute stroke, intracranial stenosis, metabolic syndrome, type 2 diabetes mellitus


How to cite this article:
Aloush TK, Fahmy NA, Elaidy DA, Abdel-Baki RS. Site and degree of intracranial arterial stenosis in acute stroke patients with metabolic syndrome among a sample of Egyptian patients. Egypt J Neurol Psychiatry Neurosurg 2016;53:89-95

How to cite this URL:
Aloush TK, Fahmy NA, Elaidy DA, Abdel-Baki RS. Site and degree of intracranial arterial stenosis in acute stroke patients with metabolic syndrome among a sample of Egyptian patients. Egypt J Neurol Psychiatry Neurosurg [serial online] 2016 [cited 2021 Apr 23];53:89-95. Available from: http://www.ejnpn.eg.net/text.asp?2016/53/2/89/183409


  Introduction Top


Type 2 diabetes mellitus (T2DM) is a well-established risk factor for small artery occlusive disease affecting the retina, kidneys, and peripheral nerves. The role of T2DM in cerebral small vessel occlusive disease is less well characterized. Autopsy studies have yielded conflicting results, some of them suggesting a relationship between T2DM and lacunes, and others showed no significant relationship. No prospective epidemiologic studies have been conducted to examine whether or not T2DM is an independent risk factor for stroke due to small vessel occlusion [1]. T2DM has various effects on the vascular tree, both macrovascular and microvascular and both intracranial and extracranial circulation [2]. Most of the diabetic patients (78%) had microvascular complications alone, 17.5% had a combination of microvascular and macrovascular complications, and a minority of them (4.5%) had no complications [3]. The metabolic abnormalities caused by T2DM - for example, alterations in the metabolism of lipoproteins, particularly the triglyceride-rich lipoproteins - induce vascular dysfunction [2].

Metabolic syndrome is a combination of medical disorders that, when occurring together, increase the risk of developing cardiovascular diseases including strokes. Components of the so-called metabolic syndrome were frequently found in stroke patients and patients with intracranial stenosis (ICS). Metabolic syndrome is present in about half of the individuals with symptomatic intracranial atherosclerotic disease and is associated with a substantially higher risk for major vascular events [4].

Only six of 19 studies found T2DM to be a risk factor for small vessel disease-related brain abnormalities, including white matter lesions or lacunes. Interactive effects between diabetes and other major vascular risk factors, particularly metabolic syndrome components, have been implicated in the development of diabetes-related complications. The importance of such interactions for the development of brain abnormalities in diabetic patients is unclear [5].


  Aim of the work Top


The aim of this study was to estimate the site and degree of intracranial arterial stenosis among patients clinically diagnosed as acute ischemic stroke patients with metabolic syndrome with or without T2DM.


  Patients and methods Top


This cross-sectional study included 100 patients admitted in Ain Shams University Specialized Hospital-Stroke Unit with the diagnosis of clinically first-ever cerebral infarction and metabolic syndrome (according to the joint statement of criteria for the diagnosis of metabolic syndrome of International Diabetes Federation, American Heart Association/National Heart, Lung, and Blood Institute, World Heart Federation, International Atherosclerosis Society, and International Association for the Study of Obesity) [6], who were selected on the basis of the presence of at least three of the following five criteria: increased waist circumference (΃94 cm in men and ≥80 cm in women); elevated triglycerides of 150 mg/dl or more (drug therapy for elevated triglycerides is an alternate indicator); third, reduced high-density lipoproteins (HDL)-c [≤40 mg/dl in men or ≤50 mg/dl in women; fourth, elevated systolic blood pressure of 130 or greater and/or diastolic of 85 mmHg or greater (antihypertensive drug treatment in a patient with a history of hypertension is an alternate indicator)]; and fifth, fasting glucose of 100 mg/dl or greater, or being on drug treatment for hyperglycemia. Egyptian waist circumference cutoff points for abdominal obesity was based on data from the Egyptian National Hypertension Project (ENHP), 97.5 cm for men and 92.3 cm for women [7].

All of the patients were divided into two groups. Group I included T2DM patients with a history of diabetes or newly diagnosed during the presentation, according to the criteria of the American Diabetes Association, 2004, [8] for the diagnosis of T2DM, which would be either of symptoms of diabetes, including polyuria, polydipsia, and unexplained weight loss plus random plasma glucose concentration of 200 mg/dl or greater, or fasting plasma glucose of 126 mg/dl or greater, or 2 h postload glucose of 200 mg/dl or greater during an oral glucose tolerance test using a glucose load containing the equivalent of 75 g anhydrous glucose dissolved in water. Group II included patients who did not have a diagnosis of T2DM.

Inclusion criteria were as follows: both sexes, age ranges from 40 to 65 years, with clinically first-ever cerebral infarction verified using MRI of the brain. All patients who met the joint statement of criteria for the diagnosis of metabolic syndrome, patients who met the criteria of the American Diabetes Association for diagnosis of T2DM, newly diagnosed diabetic patients, or known diabetic patients were also included in the study regardless of whether or not the blood sugar levels were controlled.

Exclusion criteria were as follows: spontaneous or traumatic intracerebral hemorrhage, subarachnoid hemorrhage, hemorrhagic transformation of ischemic infarct, cerebral venous thrombosis, hematological diseases and coagulopathies, recurrent stroke, atrial fibrillation, rheumatic heart disease or any other definite cardioembolic stroke, having type 1 diabetes mellitus, organ failure or coma. Ethical consideration with a prior written consent was taken from each patient or the guardians.

According to the stroke protocol of Stroke Unit of Ain Shams University Specialized Hospital, all patients were subjected to detailed medical history taking including age, sex, and screening of recognized risk factors for ischemic stroke such as arterial hypertension, diabetes mellitus, dyslipidemia, history of ischemic or rheumatic heart disease, alcohol intake, and smoking. Thorough general and neurological examination and full metabolic profile evaluation were carried out on admission, including fasting serum glucose level, 2 h postprandial serum glucose level, HbA1c, renal functions, liver functions, coagulation profile, complete lipid profile, and complete blood count. ECG, transthoracic echocardiography, and transesophageal echocardiography (if indicated) were performed. Computerized topography of the brain was performed to exclude intracerebral hemorrhage. MRI of the brain was performed on 1.5 T. Carotid duplex study and three-dimensional time-of-flight magnetic resonance angiography (MRA) of the cerebral vessels were performed on a 1.5 T General Electric machine (Little Chalfont, UK). Images were calibrated and visually inspected for the presence of stenosis or occlusion of the major arteries on both sides [middle cerebral artery (MCA) horizontal segment, anterior cerebral artery (ACA), internal carotid artery (ICA), posterior cerebral artery (PCA), and basilar artery (BA)]. Stenotic segments were measured by comparing the diameter of the vessel at the site of stenosis with the normal diameter of the vessel just proximal to the stenosis according to the warfarin-aspirin symptomatic intracranial disease study method that is calculated as follows: percent stenosis = [1-(D stenosis/D normal)]×100% [9]. When measurement of the proximal portion was not feasible, the diameter of the vessel distal to the stenosis (second choice), or the diameter of the feeding vessel (third choice) was used. Stenosis less than 25% was considered normal and was not counted. Grading of stenosis was carried out according to the method of Uehara et al. (2001) [10] as follows: normal = 0-24%; mild = 25-49%; moderate = 50-74%; severe = 75-99%; and occlusion = 100%. The site of the lesion was recorded and the frequencies were calculated. A cumulative analysis of distribution of lesions was performed to compare the anterior and posterior cerebral circulations.

Statistical analysis

Statistical presentation and analysis of the present study was conducted using mean, standard error, Student's t-test, and χ2 -test using SPSS V17 (IBM Corp., Chicago, Illinois, USA). Unpaired Student's t-test was used to compare the two groups in quantitative data. χ2 hypothesis states that the row and column variables are independent, without indicating the strength or direction of the relationship. All P values were two-tailed, and statistical significance was set at 0.008 level. Otherwise, P value less than 0.05 was considered statistically significant.


  Results Top


A total of 100 first-ever ischemic stroke and metabolic syndrome patients were enrolled in a hospital-based study [Table 1]. They were divided into two groups: group I included T2DM patients either with a history of diabetes or newly diagnosed diabetes during the presentation, and group II included patients who did not have a diagnosis of T2DM. We compared the two groups with regard to their risk factor profiles, as shown in [Table 2].
Table 1: Demographic and baseline characteristics of the study population

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Table 2: Comparison between the two groups with regard to risk factor profiles

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On comparing the two groups with regard to the localization of stroke within either anterior or posterior circulation, no statistically significant difference was found (P = 0.689).

Small vessel disease (lacune) was present more frequently in group I patients than in group II patients, and this showed a statistically significant difference (P = 0.008), as shown in [Table 3].
Table 3: Comparison between the two groups with regard to stroke subtype

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MRA studies showed evidence of ICS and/or total occlusion in 37 patients of group I and 22 patients of group II. Carotid duplex studies showed evidence of extracranial carotid stenosis in 12 patients of group I and in six patients of group II. This difference was statistically nonsignificant (P = 0.118). On comparing ICS and extracranial carotid stenosis in each group, it was found that the number of patients with ICS was significantly higher than that for extracranial carotid stenosis; the difference was statistically significant. P values of all results were less than 0.05, as shown in [Table 4]. The difference in degrees of the ICS showed a statistical significance between the two groups, with P value less than 0.001 [Table 5].
Table 4: The difference in intracranial stenosis between the two groups with comparison between the intracranial stenosis and the extracranial carotid stenosis in each group

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Table 5: The distribution of the degree of intracranial stenosis among patients of the two groups

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Nevertheless, on analysis of the sites of the lesions within the intracranial arteries MCA, ACA, PCA, ICA, and BA according to the MRA studies, it revealed no statistically significant difference between the two groups, with all P values being more than 0.05.

A total of 22 (59.46%) patients from group I with ICS had multiple ICS, whereas six (27.27%) patients from group II had multiple ICS, and this difference was statistically significant (P = 0.033) [Table 6].
Table 6: The difference between the two groups as regards single and multiple intracranial stenosis

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  Discussion Top


T2DM increases the risk for ischemic stroke. Considering the role of T2DM in metabolic syndrome, Athyros and colleagues (2009) concluded that those with both metabolic syndrome and T2DM had the highest prevalence of vascular diseases (coronary heart disease/stroke/peripheral arterial disease), followed by those with metabolic syndrome without T2DM [11-13]. On this basis, the aim of our study was to analyze the stroke subtype and the site and the degree of the intracranial arterial stenosis in metabolic syndrome patients on first presentation of ischemic stroke, with or without T2DM.

In the current study, there was a significant difference between the two groups as regards the demographic data and risk factor profiles. The incidence of male sex, smoking, past history of dyslipidemia, and prior intake of lipid-lowering agents was significantly higher in patients with metabolic syndrome and T2DM, compared with patients with metabolic syndrome without T2DM. We attribute these findings to the association of T2DM with accelerated lipolysis and diminished uptake by skeletal muscle, leading to excess plasma levels of free fatty acids. Furthermore, increased flux of free fatty acids to the liver results in triglyceride synthesis stimulation, assembly, and secretion of very low-density lipoproteins cholesterol. Hypertriglyceridemia and low HDL due to cholesterol transport from HDL to very low-density lipoproteins have been associated with atherosclerosis. However, our results showed no statistically significant difference between the two groups as regards the presence of hypertension and, consequently, left ventricular hypertrophy in echocardiography.

This is in contrast to the results of studies by Schulz and Rothwell (2008) [14], Tuttolomondo et al. (2008) [15], and Arboix et al. (2009) [16], who found a higher association between hypertension as a vascular risk factor and diabetic patients with ischemic stroke compared with nondiabetic patients. These differences in results can be attributed to the presence of metabolic syndrome components including hypertension in all our study population.

In addition, this statistically insignificant difference between the two study groups as regards a major vascular risk factor like hypertension makes the other comparable results independent of it. Past history of ischemic heart disease, myocardial infarction, increased left atrial diameter, decreased ejection fraction, and transient ischemic attacks, as risk factors for embolic stroke, showed a nonsignificant statistical difference between the two groups. These results are in accordance with study by Holzer et al. (2010) [17], who reported that much less frequently diabetic patients present with cerebral embolism. These results are also in agreement with our study subject selection by excluding any definite embolic stroke. In addition, this statistically insignificant difference between the two study groups as regards the vascular risk factors for cerebral embolism makes the other comparable results independent of it.

Our study also showed that the incidence of ICS in diabetic patients was higher than that in the nondiabetic patients. This difference was statistically significant (P = 0.004). In addition, on comparing ICS and extracranial carotid stenosis in each group, it was found that the number of patients with ICS was statistically significantly higher compared with the number of patients with extracranial carotid stenosis; the difference was statistically significant in the diabetic group (P < 0.001), whereas in the nondiabetic group the difference was less statistically significant (P = 0.008).

We attribute these findings to diabetes-related cerebral histopathological changes in human brains. It has been found that arteriolosclerosis of intracranial arteries is likely to be more severe and extensive in diabetic patients. This pathology reflects small-vessel disease, lacunar infarcts, and ICS that are definitely greater in T2DM. Our results are in agreement with a study conducted in Korea, which included 1436 diabetic patients who underwent intra-arterial four-vessel cerebral angiography. In that study, lesions were located in the intracranial area in 66% and in the extracranial area in 34% [18]. Similarly, T2DM was found to be more significantly prevalent in patients with ICS [19]. To describe vascular risk factors of patients harboring intracranial arterial stenosis, clinical reports of all patients admitted to Unitat de Neurologia, Hospital de Mataro, Barcelona Institute, with the diagnosis of intracranial arterial stenosis were reviewed. They concluded that T2DM was the most specific risk factor for intracranial arterial stenosis [20].

In a prospective study by Logallo et al. (2014) [21], 607 ischemic stroke or transient ischemic attack patients were screened for ICS using transcranial color-coded sonography, MRA, and/or computerized tomographic angiography during an 18-month study period. T2DM was the only risk factor significantly associated with symptomatic ICS (P = 0.04).

On a similar note, a 5-year retrospective analysis of 4733 Egyptians was carried out by Abd Allah et al. (2010) [22], who concluded that hemodynamically significant and clinically relevant extracranial atherosclerotic carotid disease is rare among Egyptians.

Similar results were obtained by Abdel-Nasser et al. (1997) [23], Zakaria et al. (1998) [24], Zaki-Eldine et al. (2002) [25], Abdel Moniem et al. (2008) [26], and Essa et al. (2011) [27].

In the current study, on comparing the carotid duplex results of the two study groups, it showed evidence of extracranial carotid stenosis in both groups, yet with no statistical significance. This is in agreement with a study by Shahar and colleagues (2011), in which the extracranial carotid stenosis was assessed using Doppler ultrasound. A nonsignificant difference was found between patients with T2DM and those with metabolic syndrome or insulin resistance as verified through impaired glucose tolerance test [28].

These results had been previously mentioned by Park et al. (2007) [29] and Zoungas et al. (2012) [30]. Thus, the metabolic syndrome with the included vascular risk factors have been shown to be an important cause of macrovascular stroke disease independent of T2DM [29],[30].

In the current study, analysis of the sites of the lesions in the intracranial arteries according to the MRA studies did not show statistically significant difference between diabetic and nondiabetic patients. Moreover, there was no statistically significant difference between the two groups with regard to the localization of stroke within either the anterior or the posterior circulation.

Our results are in agreement with a recent retrospective study by Yang and colleagues (2014), which was conducted on 1137 patients enrolled in the Nanjing Stroke Registry Program between June 2004 and March 2011. Cerebrovascular artery stenoses were measured in 383 patients with T2DM and 754 nondiabetic patients using digital subtraction angiography. They found no difference in the distribution of stenosis in the anterior and posterior circulation vessels between these two groups (P = 0.628) [31]. Moreover, this nonsignificant difference in stroke localization between diabetic and nondiabetic patients had been described before by Laakso and Kuusisto (2007) [32].

As regards the degrees of the ICS, our results showed that the severity of intracranial arterial stenosis was significantly associated with T2DM (P < 0.001); moreover, the obstructive intracranial lesions was significantly higher in diabetic patients compared with nondiabetic patients (P < 0.001). The current study also showed that diabetic patients had a greater tendency of having multiple intracranial stenoses compared with nondiabetic patients. This difference showed a statistically significance (P = 0.033).

These results are in accordance with that obtained by Tawfik et al. (2009) [33], who concluded that the degree of ICS had a statistically significant positive correlations with T2DM. In addition, Abdel Moniem and colleagues (2008) had nearly similar results. They concluded that T2DM was the most statistically significant factor affecting the degree of intracranial vessel stenosis (P < 0.007) [24].

More recently, similar results were obtained by Yang and colleagues (2014), and, besides, they found that diabetic patients had tendency of a higher incidence of multiple ICS. In contrast to our results, they found that the nonobstructive intracranial arterial lesions occurred more often in diabetic than in nondiabetic patients (P = 0.002) [31].


  Conclusion Top


Our study showed that diabetic patients with acute ischemic stroke have higher severity of intracranial arterial stenosis, higher incidence of multiple intracranial arterial stenoses, and lastly higher tendency to the obstructive intracranial arterial lesions. Consequently, as the metabolic syndrome is predominantly associated with macrovascular disease, our results suggest that the presence of T2DM may independently alter the pathophysiological mechanisms of cerebrovascular disease. We also concluded that the metabolic syndrome is associated with a greater risk for ischemic stroke, but with T2DM cerebrovascular risk increases even more.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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Abstract
Introduction
Aim of the work
Patients and methods
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