(Stroke. 1995;26:562-568.)
© 1995 American Heart Association, Inc.
Articles |
Prevalence of Stroke at High Altitude (3380 m) in Cuzco, a Town of Peru
A Population-Based Study
From the Department of Clinical and Biological Neurosciences (A.S.J.) and the Stroke Unit (M.H.), Centre Hospitalier Universitaire de Grenoble, France; and the Instituto de Ciencias Neurologicas Oscar Trelles Montes, Hospital Santo Toribio de Mogrovejo, Lima, Peru (P.M.).
Correspondence to Marc Hommel, MD, Stroke Unit, Clinique Neurologique, Department of Clinical and Biological Neurosciences, BP 217 38043, Grenoble, Cedex 9, France.
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Abstract |
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Background and Purpose We carried out a door-to-door survey on stroke prevalence at high altitude in Cuzco City, a town in the Peruvian Andes located 3380 m above sea level.
Methods and Results Among the 3246 screened individuals over 15 years old, there were 21 cases of first-ever completed stroke, yielding a crude prevalence ratio of 6.47 per 1000 (95% confidence interval [CI], 3.71 to 8.93 per 1000). The age-adjusted to WHO population point prevalence ratio was 5.74 per 1000 (95% CI, 3.14 to 8.35 per 1000), and the age-adjusted to North American US population point prevalence ratio was 8.58 per 1000 (95% CI, 5.44 to 11.75 per 1000). Multivariate logistic regression analysis suggested that age, polycythemia, high consumption of alcohol, and area of residence were associated with stroke prevalence. Our results suggest that the stroke prevalence in the central areas of Cuzco with sedentary people having a relatively high standard of living was higher than that in the peripheral areas with people with a relatively lower standard of living and less sedentary activities (odds ratio, 5.8; 95% CI, 1.4 to 23).
Conclusions The prevalence of stroke suggests that stroke may be a public health problem in developing countries. This study suggests the importance of environmental factors such as altitude and lifestyle in stroke occurrence. The role of these factors should be confirmed and taken into account in future stroke prevalence studies.
Key Words: alcohol • altitude • lifestyle • Peru
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Introduction |
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Cerebrovascular disease (CVD) is a well-established major cause of death and disability in developed countries.1 2 3 Despite reported sizable geographic variation in stroke occurrence, only a few environmental contributors of stroke occurrence have been identified.2 At high altitude (>3000 m), people live under hypoxic conditions.4 5 Therefore, hematocrit and hemoglobin levels increase exponentially with altitude,6 7 resulting in polycythemia, which is an independent risk factor for CVD.8 9 10 11 On the other hand, studies conducted at high altitude reported low mean values of both systolic and diastolic blood pressure4 12 13 and a low prevalence rate of hypertension13 14 15 16 as well as ischemic heart disease.15 16 As hypertension and polycythemia are well-known risk factors for CVD,9 17 18 the combination of the opposite effects of the decrease in blood pressure and the increase in hematocrit observed at high altitude leads to the hypothesis of a relationship between altitude and stroke.
The few epidemiological surveys on stroke conducted at different altitudes suggest that CVD may be less frequent than at sea level. Many areas of the United States with low stroke death rates are located at high altitudes, while the highest rates are along the seacoasts.19 In the door-to-door stroke prevalence survey carried out in Kashmir at 1530 m among a rural population of 63 654 inhabitants over 15 years of age, the crude prevalence ratio was 1.43 per 1000.20 In Quiroga, Ecuador, an Andean village located at 2300 m, a survey carried out among 1135 people reported four cases of stroke, yielding a crude stroke prevalence ratio of 3.6 per 1000.21 Bancaleri22 suggested that CVD may be less frequent in Cerro de Pasco, Peru, located at 4300 m above sea level. However, no specific studies of stroke prevalence have been carried out in any town at high altitude.
Like other developing countries, Peru lacks funds and has too few hospitals and physicians to attend to the whole population. Thus, only a minority of stroke victims can be examined by a physician or admitted to a hospital. In such countries, prevalence studies are often door-to-door surveys; hospital-based studies are difficult because of the incomplete data of hospital medical records and the very small proportion of patients hospitalized. The present survey in a high-altitude town (Cuzco, Peru) was undertaken to study the prevalence of stroke and its association with cerebrovascular risk factors.
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Subjects and Methods |
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This study was a territory-based door-to-door survey carried out in Cuzco, Peru, from July 1 to August 31, 1988.
Study Area and Population
The city of Cuzco is a large urban community of 210 000
inhabitants, located in the southern Peruvian Andes, 3400 m above sea
level (latitude, 13.31; longitude, 71.59; Figure
). This
town was chosen because it is representative of the highland
regions and has a homogeneous population. The Cuzco area is a temperate
region with a wet season during austral winter and a dry season during
austral summer. It is a university and business town; activities are
based on tourism, farming, and some industry, but there are no mines.
Most inhabitants are the result of interbreeding of the white
descendants of the Hispanic population with the Amerindian population
(Quechuas and to a lesser extent Aymaras).23 24 There is
no black population.
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The town can be divided into two areas: (1) The central area is characterized by inhabitants who are sedentary and have a "relatively high" standard of living and a hypercaloric diet, rich in sugars and fats in comparison to that of the peripheral area.24 However, it must be stressed that, if compared with developed countries, the whole city of Cuzco is classified as economically very poor. (2) The peripheral area is characterized by inhabitants who have a "lower" standard of living and whose jobs require more physical activity. The diet is normocaloric and based on carbohydrates of long absorption. This population generally consumes local products such as potatoes, maize, and quinoa.24 25 26
The healthcare system consists of two 350-bed district hospitals, one health center for children, and fewer than 10 general practitioners in private practice. Medical records of hospitalized patients are incomplete, and death certificates are unreliable. There is no long-term care facility in the Cuzco area in which stroke survivors could be hospitalized. The nearest town with equipment for computed tomography (CT) and electroencephalography is Lima, 1200 km away by road. Medical care is very expensive for the population because of the lack of national insurance services. Furthermore, because of the scarcity of physicians, it is difficult to attend correctly to the medical needs of the population. In most cases, ill adults stay at home without reliable diagnosis or suitable medical care.
When designing the study, the area of Cuzco was divided into 28 sectors of 1 km2 each on the basis of an existing map that was updated by the field study team. Initial predictions concerning the demographic data were based on the 1981 Peruvian national census.
Data Collection
A two-step survey design was used.
Step 1
To identify all people with a possible history of neurological
disease, a screening examination was conducted by eight pairs of
medical students and two neurologists. In each street, we randomly
selected two households in which we interviewed all the people over 15
years of age. The medical history of absent people was obtained by
questioning those present at home. People living at high altitude
for less than 2 years were excluded.
The interview concerned demographic and social data, personal and
family medical history, medical treatments, and the presence or history
of neurological signs and symptoms. The following demographic data were
explored: place and altitude of birth, lifetime residence in
high-altitude areas and in Cuzco, age, sex, race, language, civil
status, education, profession, and number and age of children below 15
years. Moreover, the following medical data were recorded: presence of
diabetes mellitus; history of cardiac, psychiatric, or general
disorders; history of diagnosed neurological disorder; and history of
neurological and vascular disease in first-degree relatives. Current
alcohol consumption was recorded in three categories: <120 g/wk,
between 120 and 300 g/wk, and >300 g/wk. Current tobacco use was
recorded when the average amount of tobacco smoked was 
1 cigarette
per day. Cocoa leaf consumption habits were also noted. The
questionnaires, provided by the World Health Organization
(WHO)27 and from the survey of Li et al,28
were translated into Spanish. These questionnaires had been designed to
obtain information on neurological signs and symptoms such as the
presence or history of episodes of motor paralysis, disorder of stance
and gait, uncoordination, involuntary movements, tremor, pain and
disorders of body sensation, headache, vertigo, disturbance of speech
and language, disturbance of vision, trauma, loss of consciousness,
convulsions, seizures, episodic confusion, and dementia. This interview
was supplemented by the examination and evaluation of blood pressure
and radial pulse, weight, and clinical signs of polycythemia.
Hypertension was defined as history of hypertension and/or high blood
pressure 160 mm Hg systolic and/or 95 mm Hg
diastolic.29 Obesity was defined as weight >110% of the
theoretical weight calculated with the formula of Lorentz (Gross et
al30 ). Polycythemia was defined by the presence of
hyperemia of the conjunctivas and cutaneous or mucous
erythrosis.5 If a family member had died during the last
year of study, a thorough inquiry into the circumstances of death was
carried out. The interviewers asked if, before the date of the survery,
anyone living in the selected households had developed neurological
signs and symptoms of the type detailed in the questionnaire and had
subsequently died. When such a case was identified, the medical records
were reviewed, and the relatives were interviewed by the neurologist.
If the diagnosis of stroke was established, it was considered
separately and included in the incidence rates and not in the
prevalence rates.
Step 2
The patients who screened positive for stroke at Step 1 were
clinically examined by one of the two neurologists. Present and absent
people screened during step 1 were invited to the outpatient clinic by
the neurologists, who examined 120 screened people.
For the diagnosis of stroke, we used the clinical criteria of the Ad Hoc Committee on Cerebrovascular Diseases and of the National Survey of Stroke31 32 ; only first-ever strokes were considered. As CT was available in only a few cases, the diagnosis was established on clinical criteria, and no attempt was made to distinguish hemorrhagic from ischemic strokes. We reviewed and examined 37 patients suspected of stroke at step 1 and classified 21 as having had completed strokes at step 2. Among the 120 people who went to the outpatient clinic, none of the stroke-negative screened patients at step 1 were classified as stroke-positive at step 2. Among the 37 cases of suspected stroke at step 1, 13 had occurred in people who were absent and 24 in subjects who were present. At step 2, among the 21 patients with definite stroke, 6 were initially absent and 5 were present. The screeners were two neurologists and 16 medical students from Cuzco and Lima Universities who had received theoretical and practical neurological training. The two neurologists, one Peruvian (P.M.) and the other French (A.S.J.), stayed in Cuzco throughout the survey and carried out all the step 2 examinations. The physicians of Cuzco were informed of but were not involved in the study. To maximize population cooperation, we used local radio and newspapers to inform people and to emphasize the importance of this study for the prevention of CVD. In about 80% of the randomly selected homes, there was at least one person who was able to answer the questionnaire. The cooperation of the people present reached 90%.
Data Sets and Statistical Analysis
Data were recorded in the field onto specific index card files
and then entered into a database. The statistical analysis was
carried out with SPSS/PC+ 4.0
software.33 The frequency of CVD was expressed in terms of
point prevalence and incidence rates of completed stroke and of
cerebrovascular mortality rates.34 All ratios and rates
were adjusted for age to the WHO population and to the 1971 total US
population over 15 years old.34 35 Confidence intervals
(95% CI) were calculated to describe the precision of the estimates.
Differences in rates were tested with the 
2 test,
and bivariate comparisons of means were performed with Student's
t test. The link between the factors studied and the
subsequent development of stroke was estimated using multivariate
logistic regression and was expressed in adjusted odds ratio (OR) and
95% CI.33
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Results |
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The screeners personally interviewed and took the blood pressure of 1904 people and collected data from 3246 people. Fifty-four people who had not lived at high altitudes for 2 years were not included in the study. We were not able to collect reliable medical information for an estimated 2.7% of the people. The distribution according to age and sex was similar between the 1981 national census population and our sample.
Demographic Data
Among 3246 screened people, 97% were interbred Quechua/Hispanic,
1.3% were white, 1.1% were Quechua, 0.1% were Aymara, and 0.2% were
of other racial groups. Concerning language, 99.2% of the people spoke
Spanish and 0.8% spoke only Quechua. Within the 3246 screened people,
those over 15 years of age represented 62.5% of the
population. Their mean age was 36 years (SD=16). The ratio of male to
female was 0.85. Regarding lifetime residence in high-altitude areas
(between 2800 and 5000 m), 86.6% of the people had lived in
high-altitude areas since their birth, 8.6% for 10 years or more, and
4.7% had spent less than 10 years and more than 2 years in
high-altitude areas. Concerning lifetime residence in Cuzco, 54.9% of
the people were born in Cuzco, 34.4% lived in Cuzco for more than 10
years, and 10.7% for less than 10 but more than 2 years. Concerning
education, 34% of the people were classified at university level and
58.6% at primary or secondary level, and 7.4% were illiterate.
The occupations of the population were classified as skilled
(students, 23.8%; civil servants and scientific and technical
workers, 12.2%), unskilled (business, 25.6%; employees, 7.8%;
farmers, 4.5%), and unemployed (homemakers, 22.2%; pensioners,
3.8%).
Specific rates for the urban and peripheral populations are shown in
Table 1.
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Stroke Prevalence Rates
Among the 3246 screened people, there were 21 cases of completed
stroke (12 men and 9 women; sex ratio, 0.57). The crude point
prevalence ratios were 6.2 per 1000 (95% CI, 3.5 to 8.9 per 1000). The
point prevalence ratio adjusted for age to the WHO population was 5.74
per 1000 (95% CI, 3.14 to 8.35 per 1000), and the age-adjusted point
prevalence ratio to the North American US population was 8.58 per 1000
(95% CI, 5.44 to 11.75 per 1000). The prevalence ratio of stroke was
higher in men than in women, but it had no statistical significance
(sex ratio=1.27; P=.3) and increased dramatically with age.
The age-adjusted prevalence ratio was higher in central areas (2017
people; 8.08 per 1000; 95% CI, 4.17 to 12.0 per 1000) than in
peripheral areas (1272 people; 1.13 per 1000; 95% CI, 0.71 to 3.0 per
1000), P<.001.
Six cases of first-completed stroke occurred during the year before the survey. Among the six patients with completed stroke, two died before September 1, 1988. The crude annual incidence rate for completed stroke was 1.83 per 1000 (95% CI, 0.36 to 3.30 per 1000). All cases of stroke occurred in the central area.
Risk Factors of Stroke
The prevalences of risk factors for stroke in Cuzco and in stroke
populations are reported in Table 2. Multivariate
logistic regression analysis of stroke showed that the prevalence
ratios increased with age, polycythemia, and high consumption of
alcohol (>300 g/wk) and in the central areas (Table 3).
Polycythemia was correlated positively with age, professional level of
employment, and overweight. High consumption of alcohol was correlated
positively with age, male sex, professional level of employment,
peripheral area of residence, and tobacco. Significant differences in
bivariate analysis between the central and peripheral areas were
noted regarding age, education level, profession, alcohol, tobacco,
polycythemia, obesity, and hypertension (Tables 1
and 2). Multivariate
logistic regression of the area of residence showed that the urban
areas had higher prevalences of older people, hypertension, high
consumption of tobacco, low consumption of alcohol, and obesity.
Although prevalence of stroke was higher in bivariate comparison in
patients with hypertension and heart disease and in those taking
contraceptive pills, the adjusted ORs of these risk factors were not
kept in the multivariate forward stepwise selected model of stroke
prediction. Although hypertension had a high OR in bivariate
analysis, it was not retained in the model (Table 3). Prevalence of
hypertension was significantly higher in the central area population
than in that of the peripheral area and increased with age, consumption
of tobacco, and obesity. No significant relation could be established
between stroke prevalence and sex, education, profession, obesity, or
diabetes.
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Discussion |
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Although epidemiological research on CVD has been carefully studied in developed countries,2 3 36 37 it has been poorly studied in developing countries, except in China.28 38 However, recent studies suggest that stroke is also a major health problem in these latter countries.28 39 In developing countries, the data collected in epidemiological studies cannot be validated according to existing medical records or previous medical information. There is a lack of medical equipment, and the trained specialists are concentrated in the largest and wealthiest areas. Moreover, it is often difficult to contact people directly because of the lack of postal addresses in certain parts of cities where rapid growth remains uncontrolled. Additionally, due to social insecurity, some people are reluctant to give precise answers on a questionnaire. Moreover, demographic data are frequently unreliable, especially for indigent populations. Therefore, the design of this study deliberately addresses these aims; case ascertainment was achieved by a territory-based house-to-house survey. We tried to solve the problem of reliability of medical data for the 1342 (41.3%) absentees, which was obtained from the people present. There were more young employed men who lived in the peripheral area and drank alcohol among the absentees than among those present. At step 1, among the people who screened positive for stroke, the proportion of absentees was lower than the proportion of people present, but this might be because the population of absentees have fewer risk factors than the population of people present. Among the 13 absentees who screened positive for stroke, 6 completed strokes were finally diagnosed; among the 24 people present and positive for stroke, 15 completed strokes were finally diagnosed. No stroke was diagnosed at the step 2 outpatient clinic in the people who were stroke-negative at step 1. Therefore, although the medical data of absent people may have lacked accuracy, we had no proof of erroneous screening.
The prevalence ratios for CVD vary markedly throughout the world from 1.43 to 20 per 1000, with the highest rates in the Far East. In developed countries, most studies carried out after 1970 reported age-adjusted prevalence ratios for CVD ranging from 4.4 to 10 per 1000.2 8 36 37 40 41 42 Higher rates up to 20 per 1000 were reported in Japan.38 43 In developing countries, the crude prevalence ratios for CVD ranged from 1.43 to 14 per 1000.20 38 39 44 45 In these latter countries, many epidemiological studies reported crude prevalence rates and not age-adjusted rates. Differences in age distribution of the screened populations and differences in the methodology used to estimate the prevalence make comparisons difficult. Nevertheless, our data of prevalence ratios for CVD may be regarded as close to those of the world-wide average.
The high mortality rates in developing countries, yielding an average life expectancy of 62 years in Peru, might have modified our stroke prevalence rates for disease that concern almost only the elderly population. Consequently, we calculated age-adjusted rates to the WHO and North American US populations. Moreover, a high case fatality rate after acute stroke could induce a bias in the evaluation of our prevalence rates. To evaluate the stroke case fatality rate in Cuzco, we checked the medical records of the patients admitted to the hospital during the preceding year. The in-hospital 30-day case fatality rate for stroke was 23% (9 deaths for 40 strokes in 1987; 95% CI, 10% to 34%), which is similar to the rate determined by the population-based Oxfordshire Community Stroke Project46 and to the average world death rates.1 3 The mortality rate in Cuzco and the special care given to determining the causes of deaths occurring during the year preceding the survey allow us to suggest that this bias, if any, was reduced to a minimum. In Cuzco, there are two small hospitals and few physicians, and it is not possible to attend to the medical needs of a whole population. Therefore, only a small proportion of people who suffered a stroke could be hospitalized, and surveys carried out according to hospital data did not correspond to stroke incidence.
The prevalence rates of stroke observed in our study could be modified by differences in the frequency of risk factors for stroke between our sample population and other world populations. Among the well-established risk factors for stroke,2 19 47 48 49 50 51 factors such as hypertension, tobacco, diabetes mellitus, and cardiac disease were not taken into account by the multivariate statistical model, while the roles of age, high alcohol consumption, and polycythemia as stroke risk factors have been correlated positively with stroke occurrence in our study. This may be explained by the low number of strokes in our sample. Although hypertension had a high OR in bivariate analysis, it was not retained in the model, probably because it was correlated with age and the area of residence.
Some studies have put forward the role of racial
factors,17 40 52 53 54 environmental
factors,54 55 lifestyle,51 56 57 58 59 60 61 62 63 64 and
altitude.19 The influence of a racial factor in this study
is difficult to evaluate because the population of Cuzco is descended
from white, Hispanic, and Quechua Amerindian populations, which have
Mongolian and maybe also Melanesian origins.23 65 The
reported prevalence rates of stroke in developing countries vary
according to the different studies and may be lower in rural than in
urban zones.20 39 Some authors thus emphasized the role of
lifestyle as a risk factor for CVD.39 47 48 58 59 60 61 62 63 64 When
comparing the prevalence ratios of the peripheral and central areas of
Cuzco, there was a statistically significant lower prevalence in the
peripheral area. Multivariate analysis suggested an association
between stroke and area of residence when adjusted for age,
polycythemia, and high alcohol consumption (Table 3). The inhabitants
of the urban areas were characterized by a sedentary lifestyle and
obesity attributable to professional activity and a hypercaloric diet
too rich in fried carbohydrates. In contrast, the inhabitants of the
peripheral areas were of normal weight relating to a normocaloric diet
based on carbohydrates of long absorption and extensive physical
activity.24 Despite the controversy about the role of
overweight and sedentary lifestyle as independent risk
factors,2 17 19 66 67 these factors have been related to
stroke in more recent studies.47 57 58 59 60 61 62 63 64
We also considered the possibility that the observed differences between the two areas could be due to the consumption of coca leaves in the peripheral areas. However, the traditional habit of chewing coca leaves is disappearing, and the people of Cuzco only occasionally consume coca leaf infusions. Moreover, there is no reported relationship between the consumption of coca leaves and stroke occurrence. Although coca leaf is reputedly produced in Peru, it is not purified into cocaine. People in Cuzco did not admit to consuming cocaine and probably did not consume it.
Although the role of altitude in stroke has not been established, studies report a possible relationship between altitude and stroke, with a lower prevalence of stroke at higher altitudes.19 20 21 22 The stroke prevalence rates of our study should be compared with stroke prevalence in the same population at sea level before they can lead to the hypothesis that altitude may have a beneficial effect in stroke occurrence. Because blood pressure decreases and may reach a plateau above 3000 m13 and hematocrit and hemoglobin levels increase exponentially with altitude,6 7 16 one can hypothesize that the combination of the opposite effects of the decrease in blood pressure and the increase in hematocrit may vary in relation to different altitudes.
This study suggests the importance of environmental factors and lifestyle as possible contributors to stroke occurrence. These factors should be taken into account in future stroke prevalence studies. The present study agrees with most studies that have shown that age, high consumption of alcohol, and polycythemia are independent risk factors for stroke. Moreover, this study suggests a relationship between stroke and overweight and/or sedentary lifestyle. The obtained value of the stroke prevalence rate is close to that of developed countries, suggesting that CVD is a healthcare problem in Peru. To demonstrate a possible protective role of altitude in stroke, further studies should be carried out at sea level, among a population presenting similar racial characteristics and lifestyle, and at different altitudes.
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Acknowledgments |
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We thank Pr Cuba for his vital contribution to the setup of this study and the medical students of Lima and Cuzco, who participated in the field work. We thank Jean-Pierre Jeremencko and the Alliance Française for their material assistance. We are also grateful to Yves Saint Geours, the Institut Français des Etudes Andines, and the French Embassy, which provided administrative support during the study. We acknowledge Ralph Sacco, MD, MS, for his critical review of the manuscript.
Received June 2, 1994; revision received December 26, 1994; accepted December 26, 1994.
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