• Users Online: 208
  • Home
  • Print this page
  • Email this page
Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 


 
 Table of Contents  
ORIGINAL ARTICLE
Year : 2013  |  Volume : 10  |  Issue : 2  |  Page : 62-67

Atherosclerosis of the intracranial carotid arteries in Nigerians: A pilot autopsy study


1 Department of Anatomy; Department of Medicine, Division of Cardiovascular Medicine, College of Medicine, University of Ibadan, Ibadan, Nigeria
2 Department of Anatomy, Division of Cardiovascular Medicine, College of Medicine, University of Ibadan, Ibadan, Nigeria
3 Department of Pathology, Division of Cardiovascular Medicine, College of Medicine, University of Ibadan, Ibadan, Nigeria

Date of Web Publication13-Feb-2014

Correspondence Address:
Olulola O Oladapo
Department of Anatomy and Medicine, Division of Cardiovascular Medicine, College of Medicine, PO Box 14259, University of Ibadan, Ibadan
Nigeria
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0189-7969.127002

Rights and Permissions
  Abstract 

Background: Evidence suggests that intracranial cerebral atherosclerosis (ICCA) occurs rarely in Caucasians, but more frequently in Asians, African-Americans, and Hispanics. Pathological studies verifying this claim are few in Africans.
Objective: This prospective study aimed at grading the extent, severity, and frequency of atherosclerosis of the circle of Willis in Nigerians, using the American Heart Association (AHA) classification.
Methods: This study is part of a descriptive, cross-sectional survey carried out on bodies referred for post-mortem to the Department of Morbid Pathology in the University College Hospital, Ibadan, Oyo State, Nigeria. The circle of Willis of 44 consecutive patients ≥20 years of age were examined for atherosclerosis using the AHA classification.
Results: Twenty (45.5%) of the 44 patients studied had atherosclerotic lesions in their intracranial cerebral vessels. The internal carotid arteries (ICAs) (10.1%) were the most frequently affected, followed by the basilar artery (BA) and the middle cerebral arteries (MCAs) (8.5% each). Fifteen (75%) of the 20 patients who had atherosclerotic lesions had at least one risk factor for atherosclerosis. Age, waist circumference, and abdominal wall thickness were strong risk factors for ICCA. A total of 188 (30.5%) atherosclerotic lesions were found in the 616 histological sections of blood vessels examined in the 44 patients. Ninety-six (51.1%) of the lesions were mild, 53 (28.2%) were moderate, and 39 (20.7%) were severe. Severe atherosclerotic lesions were most frequently observed in the Lt ICA (20.5%) and Rt MCA (15.4%). Using the AHA classification, type I lesions were found in 6.4%, type II 17.6%, type III 27.1%, type IV 10.1%, type V 18.1%, type VI 11.7%, type VII and IX 0.5%, and type VIII lesions were found in 8.0% patients.
Conclusions: The frequency of ICCA in our study was 45.5%, and this is worrisome for a population in a low-resource setting such as Nigeria, as the risk of stroke and recurrence in patients with symptomatic ICCA is high. Our findings are at variance with the other studies on ethnic or racial distribution of cerebral atherosclerosis, in which Chinese, Japanese, Hispanics, and African-Americans have higher rates of ICCA, and Caucasians have higher rates of extracranial carotid artery atherosclerosis (ECCA).

Keywords: Autopsy, cardiovascular risk factors, intracranial cerebral atherosclerosis, Nigerians, pathology


How to cite this article:
Oladapo OO, Olusakin J, Ogun GO, Akang E. Atherosclerosis of the intracranial carotid arteries in Nigerians: A pilot autopsy study. Nig J Cardiol 2013;10:62-7

How to cite this URL:
Oladapo OO, Olusakin J, Ogun GO, Akang E. Atherosclerosis of the intracranial carotid arteries in Nigerians: A pilot autopsy study. Nig J Cardiol [serial online] 2013 [cited 2019 Jan 24];10:62-7. Available from: http://www.nigjcardiol.org/text.asp?2013/10/2/62/127002


  Introduction Top


There is paucity of autopsy studies of cerebral atherosclerosis in Nigerians, the last one conducted being about four decades ago. [1] The conclusions then were that the relatively low frequency of cerebrovascular disease (CVD) in Nigerians may be due to a low degree of cerebral atherosclerosis and relatively short duration of hypertension. Currently, stroke is one of the leading causes of morbidity and mortality, with a high case fatality rate. [2],[3] Stroke risk factors, especially hypertension, are prevalent. [4] The contribution of intracranial cerebral atherosclerosis (ICCA) to the burden of this disease can be further elucidated by autopsy. Previous studies have shown that larger-caliber extracranial vessels in the cerebral vasculature are more liable to atherosclerosis than smaller intracranial vessels and that extracranial atherosclerosis has been causally related to ischemic stroke, especially in Caucasians. [5] Evidence suggests that ICCA occurs rarely in Caucasians but more frequently in Asians, African-Americans, and Hispanics. [6],[7],[8] Pathological studies verifying this claim are few in Africans.

This prospective study aimed at providing useful information on grading the extent, severity, and frequency of atherosclerosis of the circle of Willis in Nigerians, using the American Heart Association (AHA) classification. An attempt was also made to correlate ICCA lesion types with some anthropometric variables and cardiovascular (CV) risk factors.


  Materials and Methods Top


This study is part of a descriptive, cross-sectional survey carried out on bodies referred for postmortem to the Department of Morbid Pathology in the University College Hospital, Ibadan, Oyo State, Nigeria between July 2009 and June 2010. Forty-four consecutive patients of ≥20 years of age were used for the study. The study protocol was approved by the institutional ethical review committee. Written or informed consent was obtained from relatives of the patients. The clinical records of the patients were retrieved to obtain their anthropometric data. Information sought included age, gender, clinical diagnosis, past medical history, and presence of CV risk factors such as hypertension, diabetes mellitus, cigarette smoking, and alcohol intake. The postmortem pathological findings including height, waist circumference (WC), and maximal abdominal wall thickness (AWT) were also recorded.

Fresh brains were harvested following exposure of the skull and removal of the calvarium. The circles of Willis at the bases of the brain were dissected out and placed on boards to examine for any gross morphological variations including presence of accessory arteries, hyperplasia or hypoplasia of arteries. The arteries were fixed in 10% buffered formalin, following which they were examined macroscopically for the presence or absence of fatty streaks, fatty plaques, fibrous plaques, complicated plaques, and thrombi. Segments of each artery were placed in disposable tissue cassettes, and for each of the 44 patients, there were 14 cassettes. These tissues were processed in Leica EM TP4C automatic tissue processor and were sectioned at about 4 mm thickness. The sections were stained using Hematoxylin and Eosin (HandE) for microscopic histology.

Atherosclerotic lesions were microscopically classified according to the AHA classification [9],[10] as follows: Normal intimal thickening was graded type 0; intima with a single layer of isolated foam cells was graded type I; intima with multiple foam cell layers usually greater than two layers was graded type II; intima with a pool of extracellular lipid was graded type III; presence of type III lesions with cholesterol crystals was graded type IV; presence of fibrous cap over extracellular lipid in the intima was graded type V; intima with surface defect and/or thrombosis was graded type VI; intima with plaque area calcified (with or without lipid core) was graded type VII; intima with hyalinized fibrous plaque with no lipid core was graded type VIII; and a completely occluded vessel lumen was graded type IX. AHA lesions I-III were described as mild, AHA lesions IV-V as moderate, and AHA lesions VI-IX as severe.

Data were reported as mean ± standard deviation (SD). The frequency distributions of atherosclerosis in each vessel of the circle of Willis were given in percentages in both male and female patients. Chi-square test was used to determine the relationship between discontinuous variables, while Student's t test was used for continuous variables. Pearson test was used to determine correlation between variables. The level of statistical significance was set at P ≤ 0.05.


  Results Top


The anthropometric variables of the studied patients are shown in [Table 1]. The study population consisted of 24 (54.5%) males and 20 (45.5%) females, and apart from height, there was no significant difference between them. The medical records of the patients studied showed that 26 (59.1%) had no identifiable risk factors for atherosclerosis whilst 18 (40.9%) had at least one risk factor for atherosclerosis. The risk factors identified were hypertension in 16 (36.4%) patients, alcohol consumption in 6 (13.6%) patients, hypertension combined with alcohol consumption in 3 (6.8%) patients, and hypertension combined with diabetes mellitus in 3 (6.8%) patients. All of the three patients with diabetes were females. The only patient (2.3%) who smoked cigarettes also drank alcohol and had hypertension. The comparison of anthropometric variables of patients with and without risk factors for atherosclerosis is shown in [Table 2]. The mean age, WC, and AWT of patients with at least one risk factor were significantly greater than those of patients with no identifiable risk factor.
Table 1: Anthropometric variables in the 44 patients studied

Click here to view
Table 2: Comparison of anthropometric variables of patients with no risk factor and of patients with at least one risk factor for atherosclerosis

Click here to view


Twenty (45.5%) of the 44 patients studied had atherosclerotic lesions in their intracranial cerebral vessels. Thirteen (54.2%) of these were males and 7 (35%) were females. The gender distribution was not statistically significant (P = 0.2). The mean age of patients who had atherosclerotic lesions (51.4 ± 15.1 years) was significantly greater than that of those who did not have atherosclerotic lesions (37.0 ± 11.1 years) (P = 0.001). Fifteen (75%) of the 20 patients who had atherosclerotic lesions had at least one risk factor for atherosclerosis. By contrast, 21 (87.5%) of the 24 patients who did not have atherosclerosis had no underlying risk factors for atherosclerosis, and this was statistically significant (P < 0.001).

[Figure 1] shows the anatomical distribution of ICCA in the 44 patients studied. The internal carotid arteries (ICAs) (10.1%) were the most frequently affected by atherosclerosis, followed by the basilar artery (BA) and the middle cerebral arteries (MCAs) (8.5% each). A total of 188 (30.5%) atherosclerotic lesions were found in the 616 histological sections of blood vessels examined in the 44 patients. [Figure 2] shows the anatomical distribution of these histological atherosclerotic lesions. Ninety-six (51.1%) of the lesions were mild, 53 (28.2%) were moderate, and 39 (20.7%) were severe. Severe atherosclerotic lesions were most frequently observed in the Lt ICA (20.5%), Rt MCA (15.4%), BA (12.8%), Rt ICA (12.8%), and Lt MCA (10.3%).
Figure 1: Percentage distribution of atherosclerotic lesions in specific vessels of the circle of Willis in the 44 patients studied

Click here to view
Figure 2: The anatomical distribution of atherosclerotic lesions in H and E histological sections of intracranial carotid arteries (BA – Basilar artery; MCA – Middle cerebral artery; ACA – Anterior cerebral artery; PCA – Posterior cerebral artery; VA – Vertebral artery; AcmA – Anterior communicating artery; ICA – Internal carotid artery; PcmA – Posterior communicating artery)

Click here to view


The classification of the lesions using the AHA classification of atherosclerosis is shown in [Table 3]. The type I lesions were found in 6.4%, type II 17.6%, type III 27.1%, type IV 10.1%, type V 18.1%, type VI 11.7%, type VII and IX 0.5% each and type VIII lesions were found in 8.0% of patients. Representative photomicrographs of these lesions are shown in [Figure 3] and [Figure 4].
Figure 3: Type VI lesion in a 40‑year‑old female (H and E, ×100). Arrows show calcifications at the periphery of disrupted intima. Arrowhead points at old thrombi in the intima of the vessel

Click here to view
Figure 4: Type IV lesion in a 40‑year‑old male (H and E, ×100). Arrows point at cholesterol clefts in the intima of vessel

Click here to view
Table 3: Distribution of atherosclerotic lesion types in the circle of Willis

Click here to view


The distribution of ICCA was age related, with increase in severity as the age increased [Table 4]. Mild atherosclerosis first appeared in the age group 25-34 years and severe forms were found in 35-44 years. The most severe form occurred at age ≥ 55 years. Of the 188 atherosclerotic lesions, 146 (77.7%) were found in patients with risk factors for atherosclerosis, especially those who had hypertension or hypertension with diabetes [Table 5]. Moderate and severe atherosclerosis were proportionately more common in patients who had combined hypertension and diabetes mellitus than in patients who had hypertension alone (P = 0.006). The patients who used alcohol had only mild lesions in their vessels. A history of previous alcohol use showed significant negative association with moderate and severe atherosclerosis (P < 0.001).
Table 4: Distribution of atherosclerotic lesion types in the circle of Willis by age groups

Click here to view
Table 5: Distribution of atherosclerotic lesions in the patients having risk factors of atherosclerosis

Click here to view


The correlation of atherosclerotic lesions and biological variables is shown in [Table 6]. There was a positive correlation of ICCA with age (P < 0.01), WC (P < 0.05), and AWT (P < 0.05), but not height.
Table 6: Correlation between atherosclerotic lesion scores and anthropometric variables

Click here to view


During the course of the study, some anatomical variations were found in the vessels of the circle of Willis. Two patients had incidental asymptomatic berry aneurysms. A 61-year-old male had a single berry aneurysm located at the anterior communicating artery (AcmA) associated with an anomalous Rt MCA. The second patient, a 60-year-old female, had a single berry aneurysm of the Rt ICA. Two (4.5%) other patients had hypoplastic cerebral vessels. One of them had hypoplasia of the Lt posterior communicating artery (PcmA). The second patient had a hypoplastic Lt ACA, with fusion of the distal segment of the Rt and Lt ACAs. There was also early bifurcation of the second segment of the Lt ACA.


  Discussion Top


The present study showed the frequency of ICCA to be 45.5%. This figure is more than three times what was recorded in the same hospital four decades ago. [1] We also reported an increase in frequency of extracranial carotid artery atherosclerosis (ECCA) in the same hospital, which was 73.3%. [11] The epidemiological transition may be occurring at a faster rate than previously envisaged, and this will increase the burden of stroke and other atherosclerotic vascular diseases which a resource-poor country such as ours is ill-prepared for. [12] In the Japanese population, a frequency of 75.8% of cerebrovascular atherosclerosis was observed. [13] In our patients, ICCA was first seen in the age group 25-34 years and increased progressively with age, with peak frequency seen in the sixth decade of life. This finding is similar to other studies where atherosclerosis first appears in the circle of Willis in the third decade and increases progressively. [14] A study on 50 cadavers above the age of 30 years recorded a sudden spurt in the extent of fibrous plaques and complicated lesions in the aorta, carotids, and circle of Willis in the sixth decade. [15] In the present study also, the most severe type IX lesion was recorded in age above 64 years, and this can be easily explained by the natural history and progression of atherosclerosis with increasing age. What we could not explain readily in our findings was the drastic decline of lesions in the age group 45-54 years to 5.1%. The relatively short lifespan of Nigerians may be contributory.

The proportion of male patients with ICCA in this study was higher than in females, although this was not statistically significant, probably due to the small sample size. Autopsy-based epidemiological and cross-sectional population-based studies have observed an increased odds ratio for men developing the disease. [16],[17] A study of arterial circles of Willis from a series of consecutive autopsies in Ugandan Africans showed no significant difference in the severity of atherosclerosis between men and women, although the severity increased with age. [18]

Autopsy studies and clinical carotid intima-media thickness indicate that carotid atherosclerosis develops asymmetrically in regions of low shear stress. [19] This was found to be similar across populations, race, gender, and age. Our findings showed that atherosclerosis was most frequent in the ICAs, MCAs, and BAs, supporting the fact that turbulence is most common at the origin of larger arterial branches. [20] Clinical studies in other races have shown that the MCA is the most commonly affected artery, followed by ICA, vertebral artery (VA), and BA. [21],[22] Using the AHA classification, the predominant lesions that we found were type III lesions (27.1%). In a pathological study among young people in Brazil suffering from violent death, type I lesion ranged between 48 and 55% and type II between 40 and 41%. [23] Our patients had a lower frequency, with type I being 6.4% and type II being 17.6%. Brazil has a more advanced economy than Nigeria and it is not surprising that it has a higher prevalence of atherosclerotic lesions at an early age. For ease of reference, we grouped the lesions as mild (54.8%), moderate (28.2%), and severe (20.7%). Mild lesions were most frequent in the ACAs and PCAs, while moderate to severe lesions were most frequent in the ICAs, MCAs, and BAs in both genders. In contrast, the Japanese had mild lesions mostly in the ICAs, MCAs, and BAs, whilst severe lesions were found in the PCAs, MCAs, and VAs. [13]

With respect to the risk factors for atherosclerosis, the patients who had history of hypertension and hypertension combined with diabetes mellitus had higher frequency and greater severity of ICCA than others. The LaPlace's law states that an increase in vessel radius and/or pressure increases the tension which produces injury to the vessel wall. [20] Transvascular low density lipoprotein (LDL) transport is increased in patients with diabetes mellitus, especially if hypertension is present. [24] Therefore, lipoprotein flux into the arterial wall could be increased in these patients, possibly explaining accelerated development of atherosclerosis. We found a positive correlation between ICCA, WC, and AWT. This is not surprising as obesity plays a role in the development of atherosclerosis. [25]

The frequency of anomalies of the circle of Willis in our study was 6.8%, which is far less than 16.7% found in a study in India. [26] It has been postulated that variations in the circle of Willis play an important role in the development of cerebral aneurysm, and we found an anomalous MCA in a subject with berry aneurysm.

Limitation of the study

Autopsy studies are usually limited by recruitment biases and our study is not an exception.


  Conclusions Top


The frequency of ICCA in our study was 45.5%, and this is worrisome for a population in a low-resource setting such as Nigeria, as the risk of stroke and recurrence in patients with symptomatic ICCA is high in spite of treatment. [27] The frequency of ECCA in the same hospital was 73.3%. [11] Our findings are at variance with the other studies on ethnic or racial distribution of cerebral atherosclerosis in which Chinese, Japanese, Hispanics, and African-Americans have higher rates of ICCA, and Caucasians have higher rates of ECCA. [6],[16],[28],[29],[30]

Institution to which the work should be attributed: Department of Pathology, University College Hospital, College of Medicine, University of Ibadan, Nigeria.


  Acknowledgments Top


We are grateful to all the academic, technical staff and resident doctors of the Department of Pathology of University College Hospital, Ibadan, who gave their time and support and were enthusiastic in making this study a success.

 
  References Top

1.Williams AO, Loewenson RB, Lippert DM, Resch JA. Cerebral atherosclerosis and its relationship to selected diseases in Nigerians: A pathological study. Stroke 1975;6:395-401.  Back to cited text no. 1
[PUBMED]    
2.Wahab KW. The burden of stroke in Nigeria. Int J Stroke 2008;3:290-2.  Back to cited text no. 2
[PUBMED]    
3.Mbakwem AC, Oke DA, Ajuluchukwu JN, Abdulkareem FB, Ale O, Odunlami K. Trends in acute emergency room hypertension related deaths: An autopsy study. Niger J Clin Pract 2009;12:15-9.  Back to cited text no. 3
[PUBMED]    
4.Owolabi MO, Ugoya S, Platz T. Racial disparity in stroke risk factors: The Berlin-Ibadan experience; a retrospective study. Acta Neurol Scand 2009;119:81-7.  Back to cited text no. 4
[PUBMED]    
5.Fisher CM, Gore I, Okabe N, White PD. Atherosclerosis of the carotid and vertebral arteries - extracranial and intracranial. J Neuropathol Exp Neurol 1965;24:455-76.  Back to cited text no. 5
    
6.Gorelick PB. Distribution of atherosclerotic cerebrovascular lesions. Effects of age, race, and sex. Stroke 1993;24:116-21.  Back to cited text no. 6
    
7.Sacco RL, Kargman DE, Gu Q, Zamanillo MC. Race-ethnicity and determinants of intracranial atherosclerotic cerebral infarction. The Northern Manhattan Stroke Study. Stroke 1995;26:14-20.  Back to cited text no. 7
[PUBMED]    
8.Qureshi AI, Safdar K, Patel M, Janssen RS, Frankel MR. Stroke in young black patients. Risk factors, subtypes, and prognosis. Stroke 1995;26:1995-8.  Back to cited text no. 8
[PUBMED]    
9.Dalager S, Paaske WP, Kristensen IB, Laurberg JM, Falk E. Artery-related differences in atherosclerosis expression implication for atherogenesis and dynamics in intima-media thickness. Stroke 2007;38:2698-705.  Back to cited text no. 9
[PUBMED]    
10.Virmmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: A comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Throm Vasc Biol 2000;20:1262-75.  Back to cited text no. 10
    
11.Erete IE, Ogun OG, Oladapo OO, Akang EE. Prevalence and severity of atherosclerosis in extracranial carotid arteries in Nigeria: An autopsy study. BMC Cardiovasc Dis 2012;12:106.  Back to cited text no. 11
    
12.Forrester T, Cooper RS, Weatherall D. Emergence of Western diseases in the tropical world: The experience with chronic cardiovascular diseases. Br Med Bull 1998;54:463-73.  Back to cited text no. 12
[PUBMED]    
13.Nakamura M, Yamamoto H, Kikuchi Y, Ishihara Y, Sata T, Yoshimura S. Cerebral atherosclerosis in Japanese. I. Age related to atherosclerosis. Stroke 1977;2:400-8.  Back to cited text no. 13
    
14.Patwardhan JR, Gadgil RK, Pandit Y, Velankar BB. Comparative histopathological study of arteriosclerosis of the retina, the brain and the circle of Willis. Indian J Ophthalmol 1970;18:155-61.  Back to cited text no. 14
  Medknow Journal  
15.Kopoor K, Kak VK, Singh B. An autopsy study of atherosclerosis in aorta, common carotid arteries and circle of Willis. Nepal Med Coll J 2004;6:69-77.  Back to cited text no. 15
[PUBMED]    
16.Suri MK, Johnston SC. Epidemiology of intracranial stenosis. J Neuroimaging 2009;19(Suppl 1):11-16S.  Back to cited text no. 16
    
17.Wityk RJ, Lehman D, Klag M, Coresh J, Ahn H, Litt B. Race and sex differences in the distribution of cerebral atherosclerosis. Stroke 1996;27:1974-80.  Back to cited text no. 17
[PUBMED]    
18.Owor R, Resch JA, Loewenson RB. Cerebral atherosclerosis in Uganda. Stroke 1976;7:404-6.  Back to cited text no. 18
[PUBMED]    
19.Tajik P, Meijer R, Duivenvoorden R, Peters SA, Kastelein JJ, Visseren FJ, et al. Asymmetrical distribution of atherosclerosis in the carotid artery: Identical patterns across age, race, and gender. Eur J Prev Cardiol 2012;19:687-97.  Back to cited text no. 19
[PUBMED]    
20.Resch JA, Loewenson RB, Baker AB. Physical factors in the pathogenesis of cerebral atherosclerosis. Stroke 1970;1:77-85.  Back to cited text no. 20
[PUBMED]    
21.Caplan LR, Gorelick PB, Hier DB. Race, sex and occlusive cerebrovascular disease: A review. Stroke 1986;17:648-55.  Back to cited text no. 21
[PUBMED]    
22.Wong KS, Ng PW, Tang A, Liu R, Yeung V, Tomlinson B. Prevalence of asymptomatic intracranial atherosclerosis in high risk patients. Neurology 2007;68:2035-8.  Back to cited text no. 22
[PUBMED]    
23.Modelli ME, Cherulli AS, Gandolfi L, Pratesi R. Atherosclerosis in young Brazilians suffering violent deaths: A pathological study. BMC Res Notes 2011;4:531.  Back to cited text no. 23
    
24.Jensen JS, Feldt-Rasmussen B, Borch-Johnsen K, Jensen KS, Nordestgaard BG. Increased transvascular lipoprotein transport in diabetes: Association with albuminuria and systolic hypertension. J Clin Endocrinol Metab 2005;90:441-5.  Back to cited text no. 24
    
25.Weinbrenner T, Schroder H, Escurriol V, Fito M, Elosua R, Vila J, et al. Circulating oxidized LDL is associated with increased waist circumference independent of body mass index in men and women. Am J Clin Nutr 2006;83:30-5.  Back to cited text no. 25
    
26.Kapoor K, Singh B, Dewan IJ. Variations in the configuration of the circle of Willis. Anat Sci Int 2008;83:96-106.  Back to cited text no. 26
    
27.Sacco RL, Adams R, Albers G, Alberts MJ, Benavente O, Furie K, et al. American Heart Association; American Stroke Association Council on Stroke; Council on Cardiovascular Radiology and Intervention; American Academy of Neurology. Guidelines for prevention of stroke in patients with ischemic stroke or transient ischemic attack: A statement for healthcare professionals from the American Heart Association/American Stroke Association Council on Stroke: Co-sponsored by the Council on Cardiovascular Radiology and Intervention: The American Academy of Neurology affirms the value of this guideline. Stroke 2006;37:577-617.  Back to cited text no. 27
[PUBMED]    
28.Kuller L, Resiler DM. An explanation for variations in distribution of stroke and arteriosclerotic heart disease among populations and racial groups. Am J Epidemiol 1971;93:1-9.  Back to cited text no. 28
    
29.Feldmann E, Daneault N, Kwan E, Ho KJ, Pessin MS, Langenberg P, et al. Chinese-white differences in the distribution of occlusive cerebrovascular disease. Neurology 1990;40:1541-5.  Back to cited text no. 29
[PUBMED]    
30.Fields WS, Lemak NA. Joint study of extracranial arterial occlusion. X. Internal carotid artery occlusion. JAMA 1976;235:2734-8.  Back to cited text no. 30
    


    Figures

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

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


This article has been cited by
1 Intracranial Arterial Calcification in Black Africans with Acute Ischaemic Stroke
Richard B. Olatunji,Ademola J. Adekanmi,Ayotunde O. Ogunseyinde
Cerebrovascular Diseases Extra. 2018; : 26
[Pubmed] | [DOI]
2 Vertebral Artery Hypoplasia in a Black Kenyan Population
Julius Ogeng’o,Beda Olabu,Rankeet Sinkeet,Nafula M. Ogeng’o,Hemedi Elbusaid
International Scholarly Research Notices. 2014; 2014: 1
[Pubmed] | [DOI]



 

Top
 
 
  Search
 
Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusions
Acknowledgments
References
Article Figures
Article Tables

 Article Access Statistics
    Viewed2855    
    Printed62    
    Emailed0    
    PDF Downloaded223    
    Comments [Add]    
    Cited by others 2    

Recommend this journal


[TAG2]
[TAG3]
[TAG4]