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Stroke in South America

A Systematic Review of Incidence, Prevalence, and Stroke Subtypes


Gustavo Saposnik, MD; Oscar H. Del Brutto, MD; for the Iberoamerican Society of
Cerebrovascular Diseases

Background and Purpose—Stroke is a leading cause of mortality and disability in South America because of an increase
in life expectancy and changes in the lifestyle of the population. Because epidemiological and clinical characteristics of
stroke vary according to regional factors, we need to know the peculiarities of stroke on this continent.
Methods—We performed a systematic review of articles on stroke in South America, with emphasis on those providing
information on the incidence and prevalence of stroke (community-based studies) and the pattern of stroke subtypes
(hospital-based studies).
Results—Seven papers provided information on stroke epidemiology; 11 gave data on the pattern of stroke subtypes.
Community-based studies showed crude stroke prevalence rates ranging from 1.74 to 6.51 per 1000 and annual
incidence rates from 0.35 to 1.83 per 1000. Hospital-based stroke registries consistently reported a high frequency of
intracranial hemorrhages, which accounted for 26% to 46% of all strokes. Among patients with cerebral infarctions,
intracranial atherosclerotic lesions and small-vessel disease have been common pathogenic mechanisms underlying the
stroke. In most studies, hypertensive arteriolopathy was the most common cause of both infarctions and hemorrhages.
Conclusions—Stroke has been poorly studied in South America. Available data suggest that the prevalence and incidence
of stroke are lower than in developing countries. The pattern of stroke subtypes seems to be different from that reported
in other regions of the world, with a higher frequency of cerebral hemorrhages, small-vessel disease, and intracranial
atherosclerotic lesions. Such differences may be related to genetic, environmental, or sociocultural factors and to
differences in the control of stroke risk factors. (Stroke. 2003;34:2103-2108.)
Key Words: epidemiology 䡲 ethnicity 䡲 incidence 䡲 intracerebral hemorrhage 䡲 prevalence 䡲 primary prevention
䡲 South America 䡲 stroke 䡲 stroke classification
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C urrent knowledge of stroke risk factors and epidemiology is


based mostly on North American or European studies; scarce
data have been published from developing countries. Stroke will be
See Editorial Comment, page 2107
included if the design of the study was adequately described
a public health problem in South America during the next decades in the methods section and if stroke was diagnosed on the
because of an increase in life expectancy and changes in the lifestyle basis of neuroimaging findings.
of the population. Because epidemiological and clinical character-
istics of stroke vary according to environmental, racial, and socio- Results
cultural factors, we need to be aware of the peculiarities of stroke on Only 18 of more than 200 reviewed papers met inclusion
this continent to reduce the impact burden of this epidemic. Here, criteria (the Figure). Seven1–7 provided information on stroke
we review published evidence relevant to epidemiology and sub- epidemiology; 11 gave data on the pattern of stroke
types of stroke in South America. subtypes.8 –18

Methods Studies on Stroke Epidemiology


We used electronic databases to search for community- or hospital- Of the 7 community-based studies meeting inclusion criteria,
based studies including information on stroke in South America. 3 were designed primarily to assess the prevalence or inci-
Community-based studies were included if data were collected
through standarized questionnaires and if raw population numbers dence of stroke1–3; the other 4 were conducted to determine
were available for data confirmation. Age adjustments were de- the prevalence or incidence of major neurological diseases4 –7
scribed as originally reported. Hospital-based stroke registries were (Table 1).

Received May 7, 2003; final revision received May 28, 2003; accepted May 30, 2003.
From the Stroke Unit, Department of Neurology, Ramos Mejia Hospital, Buenos Aires University, Argentina (G.S.), and Stroke Unit, Department of
Neurological Sciences, Hospital-Clínica Kennedy, Guayaquil, Ecuador (O.H. Del B.).
Correspondence to Gustavo Saposnik, MD, Charcas 4431 4 “10,” Buenos Aires 1425, Argentina. E-mail gsaposnik@intramed.net.ar
© 2003 American Heart Association, Inc.
Stroke is available at http://www.strokeaha.org DOI: 10.1161/01.STR.0000088063.74250.DB

2103
2104 Stroke September 2003

South American map showing the geo-


graphic distribution of community-based
studies and hospital-based stroke
registries.
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The first study designed to assess stroke epidemiology was 1.83 per 1000. Age, alcohol consumption, polycythemia, and
performed in Cuzco, a Peruvian city of 210 000 inhabitants high income levels were positively associated with stroke
located 3380 m above sea level.1 Twenty-one cases of prevalence. The authors noted the importance of environmen-
first-ever stroke were found among 3246 screened individuals tal factors and lifestyle as contributors to stroke occurrence.
⬎15 years old. This gave a crude prevalence rate of 6.2 per In a Colombian study conducted in the city of Sabaneta, 76
1000 population. Six of these 21 stroke cases occurred in the of 13 588 screened people (from 17 659 inhabitants) had a
year before the study, giving a crude annual incidence rate of stroke.8 This gave a crude stroke prevalence rate of 5.6 per

TABLE 1. Community-Based Studies on Stroke Prevalence and Incidence in South America


Data Ethnic Population Crude Age-Adjusted
Collection Group,* Studied, Prevalence Prevalence Incidence
Study Year % n Rates† Rates† Rates†
Cuzco, Peru1 1988 Quechuas 97 3246 6.2 5.74‡ 1.83
Sabaneta, Colombia2 1992–1993 䡠䡠䡠 13 588 5.6 䡠䡠䡠 0.89
Santa Cruz, Bolivia3 1994 Mestizos 70, Guaranies 30 9955 1.74 3.22‡ 䡠䡠䡠
Quiroga, Ecuador4 1982 Quechuas 1113 3.6 䡠䡠䡠 䡠䡠䡠
Colombia5
Rural areas 䡠䡠䡠 7746 4.1 䡠䡠䡠 䡠䡠䡠
Urban centers 1983–1992 䡠䡠䡠 8286 9.6 䡠䡠䡠 䡠䡠䡠
Total 䡠䡠䡠 16 032 6.51 䡠䡠䡠 䡠䡠䡠
Aratoca, Colombia6 1995–1996 䡠䡠䡠 544 4.7 䡠䡠䡠 䡠䡠䡠
Chávez, Bolivia7 1995–1996 Chiquitanos 1514 䡠䡠䡠 䡠䡠䡠 0.35
*Quechuas, refers to interbreeding of the white descendants of the Hispanic population with the Amerindian
population; Mestizos, descendants of intermarriage between Spaniards and natives; Guaranies, Indians; and
Chiquitanos, native tribe from the southern Amazon region in Bolivia.
†Per 1000 population.
‡All ratios and rates were adjusted for age to the World Health Organization population according to the original
descriptions.
Saposnik and Del Brutto Stroke in South America: A Systematic Review 2105

TABLE 2. Proportion of Ischemic and Hemorrhagic Stroke Subtypes in South


American Hospital-Based Stroke Registries
Cerebral Intracranial
Strokes, Ethnic Infarction, Hemorrhage, Other,*
Stroke Registry n Group % % %
Guayaquil, Ecuador8 500 Mestizos† 62.6 37.4 䡠䡠䡠
Joinville, Brazil9 429 䡠䡠䡠 73.4 25.9 0.7
Santiago, Chile10 450 䡠䡠䡠 51 46 3
Buenos Aires, Argentina 11 361 Whites 73 27 䡠䡠䡠
Natives 66 34 䡠䡠䡠
*Includes patients with transient ischemic attacks, intracranial venous thrombosis, and unclassified
strokes.
†Mestizos⫽a racial admixture between Spaniards and Ecuadorian natives.

1000. The annual incidence rate of stroke was 0.89 per 1000. rhagic strokes,8 –13 4 included patients with ischemic
This low incidence rate could be related to the implementa- stroke,14 –17 and 1 evaluated patients with intracranial hemor-
tion of campaigns directed at teaching the community about rhages.18 Eight of the 11 studies included adult patients of all
the hazards of stroke risk factors. Another prevalence study ages,8 –12,14,15,17 and the other 3 were restricted to young
was conducted in rural areas of Santa Cruz (Bolivia).3 Of adults.13,16,18
9955 screened inhabitants, 16 had a stroke. This gave a crude In Guayaquil, 500 Ecuadorian mestizos with stroke were
prevalence of stroke of 1.74 per 1000. The prevalence was evaluated.8 The authors found 37.4% of strokes were intra-
2-fold higher in men than in women. It was suggested that cranial hemorrhages and 62.6% were cerebral infarctions.
this low prevalence rate could be related to a high number of Hypertensive arteriolopathy was the cause of 64% of the
stroke fatalities. hemorrhages and 43% of the infarctions. Lacunar infarctions
In a study designed to assess the epidemiology of neuro- were seen in 39% of patients with ischemic stroke. This was
logical diseases in the Andean village of Quiroga (Ecuador), the first study to suggest that stroke patterns in South
4 of 1113 screened people had a stroke, yielding a crude America are different from those seen in developed countries.
prevalence rate of 3.6 per 1000.4 In a Colombian study
Subsequent studies confirmed that intracranial hemorrhages
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screening 16 032 people from 7 different rural and urban


are more prevalent (Table 2) and that the pattern of ischemic
communities, the crude stroke prevalence rate was 6.5 per
strokes is different in South America than in developed
1000, which was higher in people living in urban areas (9.6
countries (Table 3).
per 1000) compared with that found in those living in rural
In Joinville (Brazil), 73.4% of 429 stroke patients had a
areas (4.1 per 1000).5 In another Colombian study conducted
cerebral infarction, 25.9% had an intracranial hemorrhage,
in the rural area of Aratoca, 10 of 544 screened people (from
6664 inhabitants) had a stroke; this gave a crude prevalence and 0.7% had unclassified stroke.9 Arterial hypertension was
rate of 4.7 per 1000.6 In a Bolivian study on the incidence of the most common risk factor for ischemic and hemorrhagic
neurological diseases among a small Amazonian tribe, 2 of strokes. Similar figures were observed in a stroke registry
1514 individuals followed up over 1 year had a stroke, from Santiago (Chile) that included 450 patients.10 Of them,
yielding an annual incidence rate of 0.35 per 1000.7 51% had ischemic strokes, 34% had cerebral hemorrhages,
12% had subarachnoid hemorrhages, and 3% had transient
Studies on Stroke Subtypes ischemic attacks. Arterial hypertension was observed in 64%
Of the 11 hospital-based stroke registries meeting inclusion of these patients and was the most common cause of both
criteria, 6 evaluated patients with both ischemic and hemor- infarctions and hemorrhages.

TABLE 3. Proportion of Ischemic Stroke Subtypes in South American


Hospital-Based Stroke Registries
Mean Large-Artery Cerebral Small-Artery Other
Age, Disease, Embolism, Disease, Causes, Unknown,
Stroke Registry y % % % % %
Guayaquil8 (n⫽313) 58 7.4 14 43.1 6 29.5
Santiago10 (n⫽233) 64 33.5 32.6 14.1 5.2 14.6
Buenos Aires (n⫽250)
12 62 12 21 42 6 18
Whites (n⫽123) 11 20 48 5 16
Natives (n⫽126) 13 22 36 8 21
Bogota14 (n⫽119) 66 19 18 19 12 32
Santiago15 (n⫽110) 67 7 14 43 6 29
Denominators of ischemic stroke are in parentheses.
2106 Stroke September 2003

Another study conducted in Buenos Aires (Argentina) Stroke incidence is more difficult to assess than preva-
identified differences in risk factors and stroke subtypes lence when resources that allow prospective follow-up of a
between Argentinian natives and whites.11 The authors found community are limited. The 3 studies on stroke incidence
a high frequency of hemorrhagic strokes and small-vessel in South America yielded rates ranging from 0.35 to 1.83
disease in both ethnic groups. Hemorrhages were signifi- per 1000 population,1,2,5 which are lower than that of
cantly higher in Argentinian natives than in whites (34% developed countries. However, those geographically re-
versus 27%), and whites had a nonsignificantly higher ten- stricted studies may not reflect the situation of the entire
dency of penetrating artery disease than natives (35% versus continent.
24%). The same authors compared the frequency of stroke Another conclusion that can be drawn from South
subtypes among whites living in Buenos Aires and Boston American studies is the consistently reported high percent-
and found that the former had a higher frequency of hemor- age of patients with intracranial hemorrhages among stroke
rhagic strokes (27% versus 15%) and small-vessel disease sufferers, which is 2 to 3 times higher than that seen in
(35% versus 21%).12 people living in developed countries.8 –12 Several factors
Among 119 patients with cerebral infarction studied in may explain such differences, including a higher preva-
Bogota (Colombia), only 19% had large-vessel atherosclero- lence of uncontrolled arterial hypertension, dietary habits,
sis as the cause of stroke.14 In Santiago, 2 study of 110 widespread abuse of over-the-counter medications that
patients with ischemic stroke suggested that the prevalence of predispose to bleeding, and alcohol abuse. Among patients
extracranial carotid artery atherosclerosis is low among Chil- with ischemic strokes, stroke registries suggest that intra-
ean patients with cerebral infarctions,15 and other study from cranial atherosclerotic lesions and penetrating small-vessel
Guayaquil showed that 60% of Ecuadorian mestizos with disease are more common in South America than in
cerebral infarctions related to large-artery atherosclerosis had developed countries.8,10 –12,14 –16
intracranial lesions, located mostly in the middle cerebral An unsolved puzzle is the contribution of racial-ethnic
artery stem.17 factors to the particular expression of stroke patterns. The
Stroke subtypes in young adults have also been evaluated South American population is heterogeneous and includes
in some studies. In a series from Sao Paolo (Brazil) that native Indians, immigrants of all races, and a number of racial
included 106 patients 15 to 40 years of age with cerebral admixtures. Therefore, it is difficult to group the patients
infarction, cardioembolism was the most common pathoge- according to race or ethnic group even after considering skin
netic mechanism of stroke in the subgroup of patients 30 to 40 color or last names. Likewise, lifestyles, dietary habits, and
years of age, whereas other determined causes of stroke were environmental conditions are not uniform in South America,
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most often seen among patients ⬍29 years of age. Lacunar and results from a given study may not extrapolate to the
infarctions were more common in patients ⬎30 years of entire region. It is important to describe ethnic subgroups to
age.16 There was a predominance of women among patients better understand stroke differences among different popula-
⬍29 years of age and of men in patients 30 to 40 years of age. tions. The term “Hispanic,” used in US stroke studies to refer
The authors concluded that the pathogenesis of ischemic to people coming from Latin America, should be banned from
stroke in young adults varies according to age and sex. In a South American studies attempting to evaluate the role of
series of 151 young adults (15 to 44 years of age) with race-ethnicity in the pattern of disease expression. A more
intracranial hemorrhage from Guayaquil, hypertensive arte- specific classification using terms such as whites, blacks,
riolopathy was the leading cause of bleeding (39.7% of mestizos, mulattos, and natives may be of more value in this
cases).18 In Curitiba (Brazil), another series of 164 young setting.
adults with stroke (86% ischemic) also showed that arterial In summary, much has to be learned about stroke in South
hypertension was the most common risk factor for the America. Large-scale, multicentric community- and hospital-
based studies with standarized designs that make them
occurrence of both ischemic and hemorrhagic strokes.13
comparable to each other are urgently needed to increase our
knowledge of the epidemiology and patterns of stroke sub-
Discussion
types in South America.
Valuable information can be extracted from the scarce pub-
lications of stroke in South America. Stroke prevalence is
lower than that in developed countries, probably because of
Acknowledgments
Drs Mario Muñoz (Bogotá, Colombia) and Ayrton Massaro (Sao
some unknown protective ethnic factors or differences in Paulo, Brazil) provided useful information for inclusion in this
dietary habits or lifestyles.1,2 This hypothesis is supported by review. We thank Dr Exuperio Diez Tejedor for his kind support.
the finding that stroke prevalence is even lower in rural than
in urban areas. It has also been suggested that low prevalence References
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Editorial Comment
Stroke Incidence and Quality Standard for Comparison
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Stroke is one of the leading causes of death in many In the early 1980s, the WHO MONICA (World Health
countries. Accordingly, the frequency of occurrence of stroke Organization Monitoring Trends and Determinants in Cardio-
provides essential information when planning community- vascular Disease) project was initiated to continuously regis-
based programs intended for reduction of mortality. In ter the occurrence of stroke and myocardial infarction among
epidemiology, incidence is widely used as the measure of the many populations by use of uniform procedures and methods
frequency of occurrence in populations. The measure is in 16 European and 2 Asian populations. Briefly, the protocol
potential of community-based studies to answer additional for the stroke registers provided detailed instructions for
questions based on an unbiased sample of incident cases event registration. It included guidelines for case ascertain-
when understanding disease etiology. In addition, the inci- ment, outlined validation procedures, and gave specific cod-
dence also measures the density of events occurring during ing rules for diagnostic category (definite stroke, unclassifi-
the observation period. Because the differences in registration able, or not stroke), order of event (first or recurrent), and
procedures, case ascertainment, and diagnostic procedures1 case-fatality rate. Diagnostic criteria were applied to symp-
could result in inaccurate measure of incidence, more accu-
toms, clinical findings, and investigations undertaken within
rate ascertainment of the incidence is required. It needs to
28 days of onset.13
define clearly for whom and what it uses when measuring the
WHO MONICA provides the most reliable and multina-
incidence. If it applies to stroke, the numerator should use the
tional compatible information on stroke incidence and case
individuals defined by characteristic and background who
fatality by using stroke registers, which can provide more
met the standardized criteria of stroke (including stroke
subtypes), and denominator should use those who become ill accurate estimates of incidence and mortality rates than
(ie, population at risk). official routine statistics can.14 In addition, suspected stroke
Recently, stroke incidence has ranged widely among re- events could be also classified through strictly standardized
ports from different regions of the world and at different methods and criteria.
points in time using community-based stroke studies and Several studies have compared a population-based
cohort studies in many countries.2–12 Among these reports, MONICA stroke registry with hospital discharge registry.
there was no research for which the same diagnostic criteria, According to Asplund et al,15 compared using the ratio of the
diagnostic method, and population denominator were used. number of fatal stroke events in the MONICA registers to the
Comparison of stroke incidence is only meaningful when number of stroke deaths in routine mortality statistics, a
based on the same diagnostic criteria and procedures in MONICA stroke register-to-routine mortality statistics ratio
various parts of the world. Definitions (standard criteria) and ⬍1.0 and ⱖ1 were found in 10 of the 21 populations. This
methods must be standardized for comparison. indicates that the official statistics may greatly underestimate
2108 Stroke September 2003

or overestimate stroke mortality in many other areas. In 3. Bamford J, Sandercock P, Dennis M, Warlow C, Jones L, McPherson K,
Swedish16 and Finnish17 MONICA populations, moreover, Vessey M, Fowler G, Molyneux A, Hughes T, et al. A prospective study
of acute cerebrovascular disease in the community: the Oxfordshire
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of false-negative in nonfatal cases was slightly lower in the 51:1373–1380.
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incidence, prevalence, and survival: secular trends in Rochester, Min-
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(17%).16 Stegmayr et al18 stated, “The quality of official 5. Giroud M, Beuriat P, Vion P, D’Athis PH, Dusserre L, Dumas R. Stroke
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Blanc S, Bottacchi E. Incidence and prognosis of stroke in the Valle
This study provided some interesting information on epi- d’Aosta Italy. Stroke. 1992;23:1712–1715.
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study is a review based on published evidence of epidemio- stroke incidence in men between 1972 and 1990 in Frederiksberg,
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used in this study was selected on the basis of prepared epidemiology in Novosibirsk, Russia: a population-based study. Mayo
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the best of our knowledge, this is the first study that has Huang YN, Chen J. The incidence of ischemic and hemorrhagic stroke in
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