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(Stroke. 1995;26:1774-1780.)
© 1995 American Heart Association, Inc.


Articles

Changes in the Sex Ratio of Stroke Mortality in the Period of 1955 Through 1990

Xin Hua Zhang, MD, PhD; Satoshi Sasaki, MD, PhD Hugo Kesteloot, MD, PhD

From the Department of Epidemiology, School of Public Health, University of Leuven, Leuven, Belgium.

Correspondence to Professor H. Kesteloot, Department of Epidemiology, Capucijnenvoer 33, B-3000 Leuven, Belgium.


*    Abstract
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*Abstract
down arrowIntroduction
down arrowSubjects and Methods
down arrowResults
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Background and Purpose Stroke mortality worldwide has decreased in men and women in most industrialized countries, except in eastern European countries. The purpose of this study was to compare the sex ratio of stroke mortality between populations and over time. This approach may help to determine the factors influencing this ratio.

Methods The sex ratios (men to women) of stroke mortality between ages 55 to 64, 65 to 74, and 75 to 84 years from 27 populations between 1955 and the latest available year were analyzed using World Health Organization data. The relationship between log stroke mortality and age and the relationships between alcohol, animal fat, cigarette consumption, and urinary cation excretion and the sex ratio of stroke mortality were also analyzed.

Results The mean sex ratio of stroke mortality increased 50%, 34%, and 15% in the three age classes, respectively, over 35 years. Highly significant relationships of log stroke mortality with age exist, which vary between men and women and among countries. In general, stroke mortality changed in the same direction in both sexes but decreased earlier and more rapidly in women than in men. Alcohol consumption and urinary sodium excretion correlated positively and significantly with the sex ratio. The time trends of the sex ratio also correlated positively and significantly with the time trends of cigarette consumption. No relationship with animal fat consumption was found.

Conclusions The sex ratio of stroke mortality is increasing with time and decreasing with age. Differences in lifestyle among countries and over the last three decades may contribute partially to these differences in sex ratio.


Key Words: gender • sex ratio • hypertension • mortality • risk factors


*    Introduction
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up arrowAbstract
*Introduction
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Between 1950 and 1990, stroke mortality has decreased markedly and almost linearly in nearly all industrialized countries, with the exception of the eastern European countries. The decrease occurred in men and in women.1 2 3 4 5 While the sex ratio of stroke mortality has been changing during the last 40 years, in any given population men and women live essentially under similar environmental conditions (eg, environmental pollution, climate, regional economic status, supply of food, and medical care). Therefore, these factors are unlikely to account for the changed sex ratio. The purpose of this study was to compare the sex difference of stroke mortality among countries over time and to ascertain whether any difference could be attributed to a difference between men and women in level of exposure to some of the risk factors that affect stroke mortality.


*    Subjects and Methods
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up arrowAbstract
up arrowIntroduction
*Subjects and Methods
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The data on stroke mortality in men and women in 5-year age classes from 35 to 84 years of age used in this study were provided by the World Health Organization (WHO) on a special nine-track magnetic tape (6250 bytes/in). Twenty-five countries, most industrialized, with adequate mortality data from 1955 to the latest available year (LAY) were included. Data from England, Wales, Northern Ireland, and Scotland of the United Kingdom were analyzed separately. For Hong Kong, we had data only from 1960 and for Greece only from 1956. The sex ratio of stroke mortality rates before 55 years of age were not considered because most stroke events occurred in older age classes. The mean sex ratio of stroke mortality in each of the periods (1954 to 1956, 1964 to 1966, 1974 to 1976, 1984 to 1986) and the latest available three years (either 1986-1988 or through 1989-1991) were determined as well as the percentage change of the sex ratio of stroke mortality between 1955 and the LAY. The study did not differentiate between types of stroke (ie, ischemic and hemorrhagic were combined).

The data from nine selected countries (Belgium, Cuba, Denmark, France, Hungary, Japan, the Netherlands, Sweden, and the United States), with different time trends of stroke mortality and from different geographic areas, are presented graphically to exemplify the time trends of stroke mortality (65 to 74 years) and of the sex ratio of stroke mortality for two age classes (55 to 64 and 65 to 74 years) in the period from 1950 to the LAY.

The Pearson correlation analysis was performed between male and female stroke mortality in 1969 to 1971, 1979 to 1981, and the latest available 3 years. Univariate regression analysis for log stroke mortality and age (35 to 84 years) was performed for men and women for two groups (Czechoslovakia, Hungary, and Poland, with increasing stroke mortality [CHP group]; and the United States, Canada, and Switzerland, with decreasing stroke mortality [UCS group]) as examples of the relationship between age and log stroke mortality in 1960, 1970, 1980, and 1990. The time trends of these relationships in the two groups for both sexes were also compared.

Data for animal fat and alcohol consumption were obtained from food balance sheets provided by the Food and Agricultural Organization of the United Nations (FAO)6 for 25 countries studied. The validity of FAO data for fat and alcohol consumption has been studied, and we found that the data are sufficiently correct for use in epidemiological studies.7 8 The 24-hour urinary sodium and potassium excretion data from epidemiological surveys are available for only 17 countries.9 Cigarette consumption data (per person per year) were obtained from a WHO report.10 These data were used to analyze the relationship of the sex ratio of stroke mortality with fat and alcohol consumption, with sodium and potassium excretion, and with the level of cigarette consumption between populations.


*    Results
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up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
*Results
down arrowDiscussion
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Tables 1 through 3DownDownDown show the values of the male/female (M/F) stroke mortality ratio for 27 populations in three age classes and five time periods presented as the mean of 1954-1956, 1964-1966, 1974-1976, 1984-1986, and the latest available 3 years. The mean mortality sex ratios decreased with age in all time periods studied. However, the mean value of the sex ratio of stroke mortality had increased 50% in the age class 55 to 64, 34% in the age class 65 to 74, and 15% in the age class 75 to 84 years from 1955 to the LAY, but the mean increase in the sex ratio became less marked with age. The M/F ratio of stroke mortality was below one in 6, 8, and 12 of 27 populations in the age classes 55 to 64, 65 to 74, and 75 to 84 years, respectively, in 1955 but only in 2 in the oldest age class in the LAY ({chi}2=22.84, P<.01). A decline in the M/F stroke mortality ratio occurred only exceptionally (Tables 1 through 3DownDownDown). In Japan a substantial increase occurred compared with other Asian countries. The highest increase in the M/F stroke mortality ratio occurred in Hungary (+1.04, +101%, for the difference and percentage change between 1955 and LAY, respectively) in the age class 55 to 64 years.


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Table 1. Secular Trends of Sex Ratio of Stroke Mortality From 1955 to Latest Available Year (1988-1991)1 in the Age Class 55-64 Years


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Table 2. Secular Trends of Sex Ratio of Stroke Mortality From 1955 to Latest Available Year (1988-1991)1 in the Age Class 65-74 Years


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Table 3. Secular Trends of Sex Ratio of Stroke Mortality From 1955 to Latest Available Year (1988-1991)1 in the Age Class 75-84 Years

The time trends of stroke mortality for men and women between 65 and 74 years of age in nine countries, selected on the basis of different behavior, are shown graphically in Figs 1Down and 2Down. A nearly linear decrease occurred in both sexes in most countries except Hungary. In the latter, stroke mortality increased from the early 1970s,1 but the increase occurred 5 years later in women than in men. Stroke mortality did not change much in Cuba in the last two decades. The most striking decrease of stroke mortality occurred in Japan, where it decreased about 5 years earlier in women than in men (Figs 1Down and 2Down). However, the sex ratios of the M/F stroke mortality in the nine countries considered increased steadily (Figs 3Down and 4Down) regardless of whether the stroke mortality decreased or increased. The sex ratio of stroke mortality in the United States has decreased since the 1970s; it has then leveled off in the last decade for the age class 55 to 64 and in the last years for age class 65 to 74 years, but it still remains higher than it was in 1955. France had the highest sex ratio in stroke mortality, and the Netherlands has had the highest increase over the last 40 years.



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Figure 1. Graph shows time trends of cerebrovascular accident mortality from 1950 to latest available year in Japan (JAP), Belgium (BEL), the Netherlands (NET), the United States (USA), Sweden (SWE), Hungary (HUN), Cuba (CUB), France (FRA), and Denmark (DEN) for men in the age class 65 to 74 years.



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Figure 2. Graph shows time trends of cerebrovascular accident mortality from 1950 to latest available year in nine countries for women in the age class 65 to 74 years. See Fig 1Up for explanation of abbreviations.



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Figure 3. Graph shows time trends of the sex ratio of cerebrovascular accident (CVA) mortality from 1950 to latest available year in nine countries for the age class 55 to 64 years. See Fig 1Up for explanation of abbreviations.



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Figure 4. Graph shows time trends of the sex ratio of cerebrovascular accident (CVA) mortality from 1950 to latest available year in nine countries for the age class 65 to 74 years. See Fig 1Up for explanation of abbreviations.

A significant correlation exists between male and female stroke mortality. The Pearson correlation coefficients (r) are .90, .95, and .96 in the age class 55 to 64 years in 1970, 1980, and 1990, respectively; .91, .95, and .98 in the age class 65 to 74 years; and .93, .97, and .97 in the age class 75 to 84 years (n=27). All probability values are less than .001.

Previous work has shown a highly significant (r>.99) correlation between log mortality from all causes and age11 and between log mortality from total cancer and log age.12 The regression analysis of log mortality (per 100 000 persons per year) of stroke with age (between 35 and 84 years of age) in 1960, 1970, 1980, and 1990 indicates that log stroke mortality was significantly associated with age (r>.99) in all four time periods in both sexes (Figs 5Down and 6Down). Stroke mortality in a given country is determined by the intercept and slope of the equation. This is true both for the UCS group with decreasing stroke mortality and for the CHP group with increasing stroke mortality. In the UCS group, the intercepts and slopes of the regression equations decreased with time in men and women. These time trends indicate that the decrease of stroke mortality occurred in all age classes, but in the CHP group it also occurred in both sexes: the intercept increased and the slopes decreased with time. Whenever stroke mortality changed, it changed in the same direction but at a different rate for women and men. As a result, the overall sex ratio of stroke mortality increased.



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Figure 5. Plot shows regression analysis for log cerebrovascular accident (CVA) mortality versus age in 1960, 1970, 1980, and latest available year for men. MeanY indicates mean log CVA mortality; A, intercept; B, slope; R, correlation coefficient; UCS, United States, Canada, Switzerland; and CHP, Czechoslovakia, Hungary, Poland.



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Figure 6. Plot shows regression analysis for log cerebrovascular accident (CVA) mortality versus age in 1960, 1970, 1980, and latest available year for women. See Fig 5Up for explanation of abbreviations.

The consumption of alcohol (%E, percentage of total dietary calorie intake) in 1965, 1975, and 1985, as obtained from the FAO, correlated positively and significantly in 19 of 27 correlations with the level of the sex ratio of stroke mortality in 1965, 1975, 1985, and the LAYs among 25 countries (data on alcohol consumption only for the United Kingdom as a whole are available) in three age classes (Table 4Down). The strongest association between alcohol consumption and the sex ratio of stroke mortality is in the age class 65 to 74 years, and the correlation coefficients progressively increased with an increase of the interval between the time of alcohol consumption and the time of the sex ratio of mortality considered (Table 4Down). The trends of the sex ratio of stroke mortality between 1970 and the LAY correlated positively with the trends in cigarette smoking (per person per year) between 1970 to 1985 in the two age classes, but the correlation was significant only in the age class 55 to 64 years (n=27, r=.48, P<.05). The 24-hour urinary sodium excretion (millimoles per 24 hours) and the urinary sodium to potassium ratio (millimole to millimole) correlated positively with the sex ratio of stroke mortality, but the correlation was significant only in the age class 55 to 64 years (n=17; r=.745, P<.01, and r=.499, P<.05, for urinary sodium excretion and the sodium to potassium ratio, respectively). No consistent relationship was found between the sex ratio of stroke mortality and the consumption of animal minus fish fat (%E, reflecting saturated fat consumption7 ).


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Table 4. Correlation Coefficients of Alcohol Consumption in 1965, 1975, and 1985 With the Sex Ratio of Stroke Mortality in 1965, 1975, 1985, and Last Available Year (n=25)


*    Discussion
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
*Discussion
down arrowReferences
 
The M/F sex ratio of stroke mortality has increased almost to the same extent in both eastern European and in other industrialized countries, notwithstanding marked differences in the trends of stroke mortality. Between 1950 and 1990, three revisions of the International Classification of Diseases have been made (ICD 7 to 9). These revisions did not alter the classification of stroke mortality to any major extent.13 The reasons for the differences in stroke mortality between the sexes and the substantial increase in the sex ratio of stroke mortality over about 35 years from 1955 to 1990 (or to LAY) are not clear. The significant correlation between male and female stroke mortality suggests that similar factors influence male and female stroke mortality but to a different extent. However, stroke mortality changed at different time periods and with different rates between men and women (Figs 1Up and 2Up).

The increase of stroke mortality with age can be adequately expressed by a simple equation relating log stroke mortality to age. In all countries, substantial changes in slope and intercept occur with time (Figs 5Up and 6Up). A decrease in the intercept signals a lowering of the stroke mortality. The changes in slope over the age range of 35 to 84 years suggest that the factors influencing stroke mortality are operative at all ages after 35 years.

In recent decades worldwide, women have had a lower mortality from ischemic heart disease compared with men in every age class (Health Statistics Annual 1986-1993, WHO). In the earlier period of this study, women showed a stroke mortality similar to men in most countries. It was even higher than that in men in some populations (sex ratio less than 1).

The difference among countries and the increasing trends of the sex ratio of stroke mortality cannot be explained by genetic differences; for example, both the French and Japanese population had a high sex ratio. Moreover, the genetic composition of populations cannot change profoundly over a period of only 30 years.

Therefore, the differences in stroke mortality and its time trends between men and women are most likely due to environmental and lifestyle factors, as the effect of these factors acting on a genetic trail.

It is unclear whether the sex ratio of stroke mortality is different for hemorrhagic and ischemic stroke. If such a difference by stroke type exists, changes in the relative frequency of ischemic and hemorrhagic stroke could influence the sex ratio of stroke mortality. Hemorrhagic stroke is more common in Japan and ischemic stroke in western countries. The fact that the increase in the sex ratio of stroke mortality was greater in Japan compared with the United States (in the age classes 55 to 64 years and 65 to 74 years) and England and Wales (in three age classes), but lower than in other western countries, argues against this interpretation (Tables 1 through 3UpUpUp).

The fact that stroke mortalities between the sexes in the different countries are highly significantly correlated, as mentioned before, shows that basically the same risk factors are operative in men and women but at a different level. The same is true for all-cause mortality.1 14 The risk factors commonly accepted for stroke are hypertension, hypercholesterolemia, congestive heart disease, atrial fibrillation, smoking, diabetes, and alcohol intake, among others. Hypertension is the major risk factor, and its decline, due to treatment and the reduction of salt intake in a population, may be responsible for the decline in stroke mortality in men and women.15 16 17 18 19 20 21 22 Smoking frequency and alcohol consumption are lower in women than in men, and this could explain part of the difference in stroke level between men and women.23 24 25 26 27 The dietary intake of total fat and saturated fat as a percentage of energy is very similar in men and women,7 but western women have a higher high-density lipoprotein cholesterol level than men. This could be ascribable to the ability of women on a diet high in saturated fat to increase their sex hormone levels, which are important determinants of the high-density lipoprotein cholesterol levels.28 This would protect women against thrombotic stroke in the same way and by the same mechanisms that protect them against ischemic heart disease.28 29 Premenopausal and postmenopausal use of estrogen replacement therapy also could have a protective effect, but this hypothesis needs confirmation. The intake level of antioxidants and of other cations beside sodium, such as potassium and magnesium, could also influence stroke mortality, but this effect is likely to be similar in men and women.

An increase in the sex ratio of stroke mortality in the presence of its decline in men and women can only be explained by a more rapid decrease in stroke mortality among women. The level of alcohol consumption correlated significantly with the sex ratio of stroke mortality, while the time trends of cigarette smoking between 1970 and 1985 correlated significantly with the trends of sex ratio of stroke mortality during the same period, confirming their importance for the understanding of the sex ratio of stroke mortality. The higher level of stroke mortality in Japan in the early 1950s can best be explained by the high level of salt intake during that period.30 31

The higher prevalence of treatment and control of hypertension in women than in men in the last decades2 18 32 33 in some populations might partially explain the increase of the sex ratio of stroke mortality. There are exceptions, however. White women in the United States had a lesser decline in stroke mortality compared with white men during the last two decades, although white women had antihypertensive treatment more often than white men.2 In a Japanese population study,19 women and men had similar levels of antihypertensive treatment in 1960, 1970, 1980, and 1990, but the sex ratio of stroke mortality linearly increased during the last 40 years.

It would be interesting to study the sex ratio of stroke mortality and its trends for ischemic and hemorrhagic stroke separately. This may be possible in the near future because of the progress in imaging techniques. Moreover, more recent studies of stroke mortality using standard definitions and classification of stroke should remove some of the uncertainties still present in this study.

In conclusion, the differences of the sex ratio of stroke mortality among populations and their changing trends may partially be attributed to different lifestyles (such as cigarette smoking and alcohol drinking) and differences in exposure to other risk factors for stroke mortality between men and women. Most of these factors remain to be defined. Differences in the level of treatment and control of hypertension can play a role also.

Received October 12, 1994; revision received July 11, 1995; accepted July 11, 1995.


*    References
up arrowTop
up arrowAbstract
up arrowIntroduction
up arrowSubjects and Methods
up arrowResults
up arrowDiscussion
*References
 

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