1173
Cerebrovascular Disease in Saudi Arabia
Basim A. Yaqub, MRCP (UK); Abdul Rahman Shamena, MD;
Taiyewo M. Kolawole, FRCR; and Pravinchandra J. Patel, FRCR
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We studied the pattern and outcome of strokes in 200 Saudi patients. Cerebral infarction
constituted 87% of strokes, subarachnoid hemorrhage 4.5%, cerebral hemorrhage 6.5%, and
venous infarction 2%. The vessel most commonly involved was part or all of the middle cerebral
artery, constituting 52% (90) of the 174 arterial infarcts. Lacunar infarcts were seen in 21% (37)
of the patients with arterial infarcts. Among all 200 patients, 8% died and 8% had secondary
generalized seizures. Hypertension occurred in 41% of the 174 patients with arterial infarcts
and 62% of the 13 with cerebral hemorrhages. The highest incidence of hypertension as a risk
factor was among those with lacunar infarcts (81%), ganglionic cerebral hemorrhages (80%),
and infarcts of deep branches of the middle cerebral artery (57%). Embolic infarcts due to
rheumatic heart disease constituted 11% of all arterial infarcts. We conclude that our pattern
of strokes is similar to that of the west rather than that of the Japanese, but with less frequent
arteriovenous malformations and aneurysms. (Stroke 1991^22:1173-1176)
T
he Arabian Peninsula is located between latitudes 10° and 30° north. Saudi Arabia is the
largest country in the peninsula, with an area
of 2,150,000 km2 and a population of 10 million.
Riyadh is the capital of the kingdom, with a population of 1 million, and King Khalid University Hospital
is one of two main hospitals in Riyadh providing free
access and care to all Saudis. The Neurology Unit in
this hospital is the largest in the kingdom with
24-hour emergency service, but private medical care,
especially in neurology, is limited in Riyadh.
Stroke data banks and stroke registries provide the
best information about cerebrovascular diseases.1-5
However, because these methods are not yet available nationwide in Saudi Arabia, the incidence,
prevalence, and pattern of strokes are not yet known
in Saudis. We studied all patients with first-ever
stroke during the period 1984-1989 in an attempt to
establish the pattern of strokes in Saudis and to
identify the effect of different risk factors for different sites of stroke.
Subjects and Methods
During the period January 1984-December 1989,
we evaluated ah* patients admitted with a clinical
diagnosis of first-ever stroke. Two hundred thirty-one
patients were admitted from the emergency room or
From the Departments of Neurology (B.A.Y., A.R.S.) and
Radiology (T.M.K., PJ.P.), King Khalid University Hospital, King
Saud University, Riyadh, Saudi Arabia.
Address for correspondence: Dr. Basim A. Yaqub, Associate
Professor, Head of Neurology, King Khalid University Hospital,
PO Box 7805 (38), Riyadh 11472, Saudi Arabia.
Received October 3, 1990; accepted April 30, 1991.
referred from different health centers in Riyadh; few
patients were referred from hospitals outside Riyadh
for further evaluation. The patients were of different
occupations and social classes.
Two hundred patients had a definite lesion by
computed tomography (CT) of the brain performed
within 3 days, 10 days, or 1 month after the stroke.
We excluded the 20 patients whose CT scan was
negative after 1 month and the 11 patients in whom
brain CT was not done.
We defined stroke as rapidly developing clinical
symptoms and/or signs of focal and sometimes global
loss of cerebral function with symptoms lasting for
>24 hours or leading to death, with no apparent
cause other than that of vascular origin.6 Cerebral
infarct was defined as a hypodense lesion on brain
CT, with a topography corresponding to the territory
of a cerebral vessel as defined by Damasio7 and
Bories et al.8 Hemorrhagic infarct was identified as
an area of low attenuation conforming to a vascular
territory within which a single nonhomogeneous area
or multiple areas of high attenuation were present
with characteristic blood density.9 Lacunar infarct
was defined as a constellation of clinical symptoms
and signs showing a high correlation with small, deep,
rounded infarcts due to a single penetrating small
arterial occlusion as confirmed by CT.10 We recognized the four lacunar syndromes pure motor stroke,
pure sensory stroke, sensorimotor stroke, and ataxic
hemiparesis. Border zone infarcts were those occurring in border zones between two main artery territories as defined by Bogousslavsky and Regli,11 Damasio,7 and Bories et al.8 Cerebral hemorrhage was
diagnosed as a hyperdense area on brain CT with or
1174
Stroke
Vol 22, No 9 September 1991
TABLE 1.
Pattern of Strokes in 200 Saudis
Stroke type
No.
Arterial infarction
Venous infarction
Subarachnoid hemorrhage
Cerebral hemorrhage
174
4
9
13
Total
200
TABLE 2. Anatomic Location of Arterial Infarct in 174
Saudi Patients
87
2
4.5
6.5
100
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without intraventricular leak and classified as ganglionic when occurring in the basal ganglion (thalamic,
lenticular, or caudate) or lobar when located in the
frontal, temporal, parietal, or occipital regions. Subarachnoid hemorrhage was identified by the presence
of blood in the subarachnoid space onCTor by bloody
cerebrospinal fluid in patients with a normal CT scan.
Venous infarct was confirmed with cerebral angiography or arterial digital subtraction arteriography.
We studied the four risk factors hypertension,
diabetes mellitus, ischemic heart disease, and rheumatic heart disease. The statistical assessment of the
prevalence of hypertension and diabetes in patients
with different stroke subtypes was done by applying
the x2 test- To determine hypertension, we measured
blood pressure twice in all patients and considered
readings of ^ 150/90 mm Hg after admission from the
emergency room as abnormal. Cardiac clinical evaluation was completed in all patients, and echocardiography was done in certain patients with rheumatic
or ischemic heart disease. Diabetic patients were
defined as those whose fasting blood glucose concentration was >7.8 mmol/1.
Results
There were more men with strokes of all types than
women, with the overall male:female ratio being
1.4:1. Table 1 shows the pattern of strokes, with
cerebral infarct being the most common and venous
infarct the least common.
The anatomic location of the cerebral arterial
infarcts are shown in Table 2. Infarcts in the anterior
circulation constituted 59% while those in the posterior circulation constituted 17% of all arterial infarcts. Six patients had border zone infarcts, mainly
with Wernicke's aphasia, pure word deafness,12 partial complex seizures, and visual field defects. Lacunar infarcts constituted 18.5% of all strokes and 21%
of all arterial infarcts. Table 3 shows the frequencies
of different lacunar syndromes with the sites of the
lesions.
Venous infarcts were seen in four patients; three
were young women (two in the postpartum period, one
in the first trimester of pregnancy). These patients
presented with headache, papilledema, convulsions,
and speech problems. The one man, admitted with
carcinomatosis, had multiple venous infarcts confirmed
by brain CT and four-vessel cerebral arteriography.
Spontaneous intracranial hemorrhage was found
in 22 patients, nine (4.5%) with subarachnoid hemorrhage and 13 (6.5%) with cerebral hemorrhage.
Location
No.
ICA
Entire ICA
102
3
59
2
90
3
52
2
59
34
28
17
11
9
16
10
6
5
29
16
17
9
7
6
4
3
6
3
37
21
174
100
MCA
Entire MCA
Superficial MCA
Deep MCA
Lenticulostriate artery
Anterior choroidal artery
Anterior cerebral artery
Vertebrobasilar artery
Posterior cerebral artery
Posterior inferior cerebellar artery
Other
Border zone infarcts
Lacunes
Total
ICA, internal carotid artery; MCA, middle cerebral artery.
Ganglionic cerebral hemorrhage (10) was more common than lobar hemorrhage (three).
Table 4 compares risk factors among the 174
patients with arterial infarcts and 13 patients with
cerebral hemorrhage. The highest incidence of hypertension was in patients with lacunar infarcts
(81%), ganglionic cerebral hemorrhage (80%), or
infarcts of the deep branches of the middle cerebral
artery (57%) (/7<0.001, *26=49.12). Diabetes was
equally common among patients with infarcts in the
deep or superficial branches of the anterior or posterior circulations and patients with lacunar infarcts
(/?<0.69, ^26=3.95). Embolic infarcts due to rheumatic heart disease were seen in 11% of the patients
with arterial infarcts, equally common among those
with infarcts in the anterior or posterior circulations.
Only two patients had embolic infarcts in the territory of the lenticulostriate artery.
Among all 200 patients, 16 (8%) died in the
hospital. Ten (6%) of these were from the 174 with
arterial infarcts, one (25%) was from among the four
TABLE 3. Lacunar Syndromes: Types and Sites of Lesion in 37
Saudi Patients
Syndrome
%
Site of lesion
Pure motor stroke
No.
14
38
Sensorimotor
stroke
Pure sensory
stroke
Ataxic
hemiparesis,
dysarthriaclumsy hand,
and other
12
32
Anterior limb of internal
capsule
Posterior limb of internal
capsule
3
8
8
22
Total
37
100
Thai am us
Corona radiata or pons
Yaqub et al
Stroke in Saudi Arabia
1175
TABLE 4. Age, Sex, and Etiotogk Risk Factors in Saudi Patients With Arterial Infarcts or Cerebral Hemorrhage
Cerebral arterial infarct
Risk factor
Sex ratio
Age (mean yr)
Men
Women
Both
Hypertension
No.
%
Entire ICA or
MCA/superficial
MCA/ACA (TI=74)
1.4
Deep
r
MCA
(II=28)
1.1
Border
zone
(«=6)
2
Lacune
("=37)
Total
(* = 174)
1.9
2.4
1.5
54
67
47
51
31
30
81
72
41
2
33
8
28
11
30
44
25
2
7
0
0
2
7
3
8
2
7
0
0
5
17
0
0
15
20
16
57
15
20
8
29
9
12
12
16
69
64
58
2
9
33
1.5
63
59
59
59
60
54
Cerebral hemorrhage
Ganglion ic
Total
Lobar
(n = 10)
("=3)
(" = 13)
59
61
61
59
60
65
Vertebrobasilar
("=29)
60
63
0.5
45
42
1.2
43
53
45
49
8
80
0
0
8
62
1
0
0
1
10
8
17
10
0
0
0
0
0
0
19
11
0
0
0
0
0
0
Diabetes
No.
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%
IHD
No.
%
RHD
No.
%
ICA, internal carotid artery, MCA, middle cerebral artery, ACA, anterior cerebral artery, IHD, ischemic heart disease; RHD, rheumatic
heart disease.
with venous infarcts, and five (23%) were from
among the 22 patients with cerebral or subarachnoid
hemorrhage. Epilepsy developed in 16 patients (8%)
during a follow-up of 1-4 years.
Discussion
Rather than being population-based, our study
consists of patients with first-ever stroke and is
negatively biased toward certain categories such as
rapidly lethal strokes or those with rapidly reversible
symptoms. However, our study is very important in
defining the pattern and outcome of strokes in a
particular ethnic group not studied before.
Our study agrees with others in finding a male
preponderance.8"18 The overall male:female ratio
was consistent in all types of arterial infarcts, but not
in venous infarcts.
We studied only a few risk factors but found the
incidence of embolic infarction of cardiac origin to be
higher than that reported in the west because the
incidence of rheumatic valvular lesions is still high in
Saudi Arabia and other developing countries.19 We
found diabetes and hypertension to have the same
frequencies as reported in the literature.20'21 However, the frequency of hypertension was not the same
in all stroke subtypes, as it was for diabetes mellitus.
The pattern of strokes in Saudis was more like that
in Europeans13-15-22-25 than like that in Chinese26 and
Japanese.16^7-28 Ganglionic hemorrhage related to
hypertension had the same frequency as in the west,
but subarachnoid hemorrhage and lobar intracerebral hemorrhage due to arteriovenous malformations
had lower incidences, suggesting that aneurysm and
arteriovenous malformations are less common in this
ethnic group.29 Our findings on lacunar infarcts are
comparable to those in other studies, which indicate
that lacunar syndromes are more common in the
elderly, in hypertensive persons, and in males.10 The
frequency of venous infarcts was higher in our study
than in others8-30 but reflects a certain bias because
most such cases are referred to our institutes for
specific investigations not available in small hospitals
in the kingdom.
In conclusion, our study, though not communitybased, reflects the pattern of strokes in Saudis and
outlines some of the risk factors.
Acknowledgments
We thank Dr. Tahir Obeid and AbdulKader Daif
for allowing us to study their patients. We are also
grateful to Dr. Bamgboye for statistical advice and
analysis and to Ms. Lydia Gallardo and Joan Beleno
for excellent secretarial help.
References
1. Mohr JP: Stroke data banks (editorial). Stroke 1986;17:
171-172
2. Kunitz SC, Gross CR, Heyman A, Kase CS, Mohr JP, Price
TR, Wolf PA: The Pilot Stroke Data Bank: Definition, design,
and data. Stroke 1984;15:740-746
3. Sandercock P, Molyneux A, Warlow C: Value of CT in
patients with stroke: Oxfordshire Community Stroke Project.
Br Med J 1985;290:193-197
4. Oxfordshire Community Stroke Project: Incidence of stroke in
Oxfordshire: First year's experience of a community stroke
register. Br Med J 1983;287:713-717
1176
Stroke
Vol 22, No 9 September 1991
Downloaded from http://stroke.ahajournals.org/ by guest on June 17, 2017
5. Mohr JP, Caplan LR, Melski JW: The Harvard Cooperative
Stroke Registry: A prospective registry. Neurology 1978;28:
754-762
6. Hatano S: Experience from a multicentre stroke register: A
preliminary report. Bull WHO 1976^4^41-553
7. Damasio H: A computed tomographic guide to identification
of cerebral vascular territories. Arch Neurol 1983;40:132-142
8. Bories J, Derhy S, Chris J: Roles of scanning: CT, PET and
MRI: CT in hemispheric ischaemic attacks. Neuroradiology
1985;27:468-483
9. Ott BR, Zamani A, Kleefield J, Funkenstein HH: The clinical
spectrum of hemorrhagic infarction. Stroke 1986;17:630-637
10. Bamford J, Sandercock P, Jones L, Warlow C: The natural
history of lacunar infarction: The Oxfordshire Community
Stroke Project. Stroke 1987;18:545-551
11. Bogousslavsky J, Regli F: Unilateral watershed cerebral infarcts. Neurology 1986^36:373-377
12. Yaqub B, Gascon G, Al-Nozha M, Whitaker H: Pure word
deafness (acquired verbal auditory agnosia) in an Arabic
speaking patient. Brain 1988;lll:457-466
13. Whisnant JP, Fitzgibbon JP, Kurland LT, Sayre GP: Natural
history of stroke in Rochester, Minnesota: 1954 through 1954.
Stroke 1971;2:ll-22
14. Matsumoto N, Whisnant JP, Kurland LT, Okazaki H: Natural
history of stroke in Rochester, Minnesota: 1955 through 1969:
An extension of a previous study, 1945 through 1954. Stroke
1973;4:2O-29
15. Kannel WB, Wolf PA; Epidemiology of cerebrovascular disease, in Ross Russell RW (ed): Vascular Disease of the Central
Nervous System. Edinburgh, UK, Churchill Livingstone, Inc,
1983
16. Ueda K, Omae T, Hirota Y, Takeshita M, Katsuki S, Tanaka
K, Enjoji M: Decreasing trend in incidence and mortality from
stroke in Hisayama residents, Japan. Stroke 1981;12:154-160
17. Herman B, Leyten ACM, van Luijk JH, Frenken CWGM, de
Coul O, Schulte BPM: Epidemiology of stroke in Tilburg, The
Netherlands: The population-based stroke incidence register:
Incidence, initial clinical picture and medical care, and three
week case fatality. Stroke 1982;13:334-339
18. Tanaka H, Ueda Y, Date H, Baba T, Yamashita H, Hayashi
M, Shoji H, Owada K, Baba K-I, Shibuya M, Kon T, Detels R:
Incidence of stroke in Shibata, Japan: 1976-1978. Stroke
1981;12:460-466
19. Milikan C, McDowell F, Easton J: Editorial. Stroke. Philadelphia, Lea & Febiger, 1987, pp 191-220
20. Riddle MC, Hart J: Hypergrycemia, recognized and unrecognized, as a risk factor for stroke and transient ischemic attacks.
Stroke 1982;13:356-359
21. Barrett-Connor E, Khaw KT: Diabetes mellitus: An independent risk factor for stroke? Am J Epidemiol 1988;128:116-123
22. Weinfeld FD (ed): The National Survey of Stroke. Stroke
1981;12(suppl 1):1-31
23. Kotila M: Declining incidence and mortality of stroke? Stroke
1984;15:255-259
24. Gross CR, Kase CS, Mohr JP, Cunningham SC, Baker WE:
Stroke in South Alabama: Incidence and diagnostic features-A population-based study. Stroke 1984;15:249-255
25. Sivenius J, Heinonen OP, Pyorala K, Salonen J, Riekken P:
The incidence of stroke in the Kuopio area of east Finland.
Stroke 1985;16:188-192
26. Huang CY, Chan FL, Yu YL, Woo E, Chin D: Cerebrovascular disease in Hong Kong Chinese. Stroke 1990^1:230-235
27. Katsuki S: Epidemiological and clinicopathological study on
cerebrovascular disease in Japan. Prog Brain Res 1966;21B:
64-89
28. Ueda K, Hasuo Y, Kiyohara Y, Wada J, Kawano H, Kato I,
Fujii I, Yanai T, Omae T, Fujishima M: Intracerebral hemorrhage in a Japanese community, Hisayama: Incidence, changing pattern during long-term follow-up, and related factors.
Stroke 1988;19:48-52
29. Al-Mefty O, Al-Rodhan N, Fox J: The low incidence of
cerebral aneurysms in the Middle East: Is it a myth? Neurosurgery 1988;22:951-954
30. Chiras J, Dubs M, Bories J: Venous infarctions. Neuroradiology 1985;27:593-600
KEY WORDS • cerebrovascular disorders • Saudi Arabia
Cerebrovascular disease in Saudi Arabia.
B A Yaqub, A R Shamena, T M Kolawole and P J Patel
Stroke. 1991;22:1173-1176
doi: 10.1161/01.STR.22.9.1173
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