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Circulation. 2008;117:1526-1536
Published online before print March 17, 2008, doi: 10.1161/CIRCULATIONAHA.107.720953
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(Circulation. 2008;117:1526-1536.)
© 2008 American Heart Association, Inc.

Epidemiology

Prevalence of Angina in Women Versus Men

A Systematic Review and Meta-Analysis of International Variations Across 31 Countries

Harry Hemingway, FRCP; Claudia Langenberg, MD; Jacqueline Damant, MPhil; Chris Frost, PhD; Kalevi Pyörälä, MD; Elizabeth Barrett-Connor, MD

From the Department of Epidemiology and Public Health (H.H., J.D.), University College London Medical School, London, United Kingdom; Medical Research Council Epidemiology Unit (C.L.), Institute of Metabolic Science, Addenbrooke’s Hospital, Cambridge, UK; Medical Statistics Unit (C.F.), London School of Hygiene and Tropical Medicine, London, United Kingdom; Department of Medicine (K.P.), University of Kuopio, Kuopio, Finland; and Department of Family and Preventive Medicine (E.B.-C.), School of Medicine, University of California, San Diego.

Reprint requests to Harry Hemingway, FRCP, Professor of Clinical Epidemiology, Department of Epidemiology and Public Health, University College London Medical School, 1-19 Torrington Place, London WC1E 6BT, United Kingdom. E-mail h.hemingway{at}ucl.ac.uk

Received June 18, 2007; accepted December 31, 2007.


*    Abstract
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Background— In the absence of previous international comparisons, we sought to systematically evaluate, across time and participant age, the sex ratio in angina prevalence in countries that differ widely in the rate of mortality due to myocardial infarction.

Methods and Results— We searched MEDLINE and EMBASE until February 2006 for healthy population studies published in any language that reported the prevalence of angina (Rose questionnaire) in women and men. We obtained myocardial infarction mortality rates from the World Health Organization. A total of 74 reports of 13 331 angina cases in women and 11 511 cases in men from 31 countries were included. Angina prevalence varied widely across populations, from 0.73% to 14.4% (population weighted mean 6.7%) in women and from 0.76% to 15.1% (population weighted mean 5.7%) in men, and was strongly correlated within populations between the sexes (r=0.80, P<0.0001). Angina prevalence showed a small female excess with a pooled random-effects sex ratio of 1.20 (95% CI 1.14 to 1.28, P<0.0001). This female excess was found across countries with widely differing myocardial infarction mortality rates in women (interquartile range 12.7 to 126.5 per 100 000), was particularly high in the American studies (1.40, 95% CI 1.28 to 1.52), and was higher among nonwhite ethnic groups than among whites. This sex ratio did not differ significantly by participant’s age, the year the survey began, or the sex ratio for mortality due to myocardial infarction.

Conclusions— Over time and at different ages, independent of diagnostic and treatment practices, women have a similar or slightly higher prevalence of angina than men across countries with widely differing myocardial infarction mortality rates.


Key Words: angina • meta-analysis • population • women


*    Introduction
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The causes of angina pectoris are poorly understood. Despite stable angina being a common initial presentation of coronary disease1 and exerting a major impact on quality of life,2 ability to work, and costs to society,3 there have been few large-scale epidemiological investigations and no meta-analyses of risk factors for angina. The pathological hallmarks of myocardial infarction (MI)—plaque rupture and thrombosis—are not shared with angina,4–7 which suggests that the population causes might differ. The incidence of acute MI shows a universal excess among males across countries with widely differing absolute rates of MI mortality,8,9 and this has been taken as evidence of an inherent biological cause. By contrast, male sex was not associated with physician-defined angina occurrence in either a small (146 cases in women) healthy population study (Framingham)10 or a large (67 832 cases in women) study of primary care patients.11 Although these physician-defined angina cases were related to subsequent MI mortality in women, the lack of male excess could be biased if women with atypical symptoms were included,12,13 if women sought healthcare more often than men,12 or if physicians selected nitrates as a diagnostic test more often for women than for men.

Editorial p 1505

Clinical Perspective p 1536

Thus, it is not known whether male sex is a risk factor for angina in unselected populations, independent of diagnostic and treatment practices.14 Addressing this question is fundamental both to etiological understanding of the complex phenotypes aggregated in the term "coronary heart disease" and to the development of appropriate clinical services, which have been beset by inequitable underuse of investigation and treatment among women.15 The 7-item Rose angina questionnaire16 is largely free of biases due to the diagnostic practices of physicians and is the only standardized instrument for assessing typical angina that has been used in different countries. In women, Rose-determined angina is associated with coronary risk factors,17 resting ECG abnormalities,17 carotid intima-media thickness,18 and coronary artery calcification.19 Women with angina ascertained by use of the Rose questionnaire have greater cardiovascular20 and coronary21–24 mortality than women without angina, with relative risks similar to those of men.20–24 Clinical studies suggest that angina in women is more commonly microvascular in origin than is the case in men,25 and in the general population, microvascular disease is associated with increased risk of MI and coronary death in women but not men.26

We hypothesized that if male sex is a cause of angina, this would be reflected in its population prevalence across countries that differ widely in MI mortality rates, risk factors, cultural factors, and healthcare systems, and it would be robust across both participant age and study year. In the absence of any previous studies on this hypothesis, we performed a meta-analysis according to the standards proposed by the Meta-analysis Of Observational Studies in Epidemiology (MOOSE) Investigators.27


*    Methods
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Study Eligibility
The review included reports of angina prevalence that used the Rose angina questionnaire in population-based surveys of women and men. We included cross-sectional and prospective cohort study designs and articles in any language; there were no exclusion criteria.

Search of Data Sources
We searched MEDLINE and EMBASE for articles published up to February 27, 2006, using a search strategy developed with an experienced librarian. The strategy used search terms (including MeSH [Medical Subject Headings]) most sensitive for identifying epidemiological studies of prevalence: "angina pectoris/epidemiology [MAJR:NoExp] OR angina [tw] AND prevalence [tw]." We individually searched on each of the 70 unique countries included in previous international comparisons of MI in women and men.8,28,29 We hand-searched the bibliography of each eligible study. We obtained unpublished tabular data for countries with particularly high (Russia, Poland, and Czech Republic) or particularly low (Japan) MI mortality rates and obtained data from India and Sri Lanka from investigators when their surveys had measured but not yet reported angina prevalence.

Selecting Studies and Data Abstraction
A total of 2068 titles, and abstracts if available, and 136 full-text papers (25 of which were written in languages other than English) were reviewed against the eligibility criteria, and 53 unique articles were included. We excluded 83 full-text papers because they did not report angina prevalence (n=26 papers), did not use the Rose questionnaire (n=26), did not report separate estimates for women and men (n=15), and other reasons. From each article, we abstracted the following information: definition of angina (classified as "definite" if cases met all 7 Rose criteria30 [Table 1] or "other" if fewer than 7 items were used to define a case, or if it was not stated explicitly), prevalence of angina in women and men, language of administration (English versus non-English), survey response rate, country, year the study began, and age range. Where mean age was not stated, the population weighted mean or midpoint of the range was derived (in the 14 studies for which both were available, the mean difference was 1.9 years). The mean age of women and men was similar in all studies, differing by a mean of 0.11 years. With the exception of the British-Norwegian Migrant Study,20 all articles reported estimates within 1 country. Of the 52 articles investigating a single country, 10 gave more than 1 report according to ethnicity or geographic region. Because of this and the use of unpublished data, there were a total of 74 populations (separate reports) from 53 unique articles that contributed data for 31 countries for the present analyses. Interreader correlation for angina prevalence was high (reliability coefficient of 0.973 for women and 0.978 for men).


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  		Table 1. Angina Questionnaire Items*

Country-Level Mortality Data
We obtained country- and sex-specific mortality rates for acute MI from the World Health Organization (WHO) mortality database (http://www3.who.int/whosis/mort/table1.cfm?path=whosis,mort,mort_table 1&language=english). Acute MI was defined by the International Classification of Diseases (ICD), 9th revision (ICD-9; code 410) or, when available, the 10th revision (ICD-10; codes I21 and I22). For the Russian Federation and Switzerland, only the aggregated term "ischemic heart diseases" (ICD-10 I20 to I25) was available. Masked to angina prevalence, 2 reviewers independently selected MI mortality rates that were closest in time to the start year of each survey and that corresponded to the mean age of survey participants. The interreader agreement between 2 independent reviewers for acute MI mortality was high, with a reliability coefficient of 0.978 for women and 0.976 for men. To assess whether the level of economic development influenced the sex ratio in angina, we classified each country according to the 6 WHO geographic regions and according to 5 mortality strata based on mortality in children younger than 5 years and in males between the ages of 15 and 59 years31: A, very low child and adult mortality; B, low child and adult mortality; C, low child and high adult mortality; D, high child and adult mortality; and E, very high child and adult mortality.

Statistical Analyses
Prevalence ratios comparing women with men were calculated and logarithmically transformed for each study. As is standard practice for ratios, all analyses were performed on these logarithmically transformed values, with back-transformation for reported results. Standard errors for each (log) prevalence ratio were calculated. Pooled (log) prevalence ratios with 95% CIs were calculated with the STATA (version 9.2) meta-analysis program (Stata Corp, College Station, Tex; http://www.stata.com), and a forest plot was obtained. Heterogeneity of effects across studies was assessed by the Cochran Q statistic. Because this was significant, and to allow for clustering of data from the same country, a random-effects model was used. Stratified meta-regression analyses were performed according to participants’ mean age, start year of the survey, absolute levels of MI mortality in women (categorized by quartiles), the sex ratio in MI mortality (quartiles), birth cohorts, WHO region and subregion, angina definition, language, and response rate of the study. The statistical significance of differences between estimates in these subgroup analyses was assessed with random-effects meta-regression models. Global tests of heterogeneity were used to investigate differences when the source of variability under investigation was unordered, and trend tests were used for ordered sources. We calculated {tau}-squared, a moment-based estimate of the residual between-studies variance, as part of the random-effects meta-regression analysis.32

The authors had full access to the data and take full responsibility for its integrity. All authors have read and agree to the manuscript as written.


*    Results
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Individual Study Estimates
We included a total of 74 population samples of 13 331 angina cases in 199 494 women and 11 511 cases in 201 821 men from 31 countries, 5 countries being English speaking (Table 2DownDown) (I. Nazareth, G. D’Costa, G. Levy, D. Naik, R. Vaidya, M. King, unpublished data, 2007).17,18,20,22,23,24,33–74,76–80 Mortality estimates for acute MI were available for 66 of the 74 studies. Angina prevalence varied widely, from 0.73% to 14.4% (population weighted mean 6.7%) in women and from 0.76% to 15.1% (population weighted mean 5.7%) in men. There was a strong and significant correlation between female and male angina prevalence across studies (correlation coefficient 0.80, 95% CI 0.70 to 0.87, P<0.0001; Figure 1). Figure 1 illustrates that most studies lie above the line of equality between the sexes, which denotes a female excess. There were significant ecological correlations between study-level angina prevalence and country-level MI mortality rates in women (r=0.27, 95% CI 0.03 to 0.48, P=0.03) and men (r=0.42, 95% CI 0.20 to 0.60, P=0.0005).


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  		Table 2. Angina Prevalence Studies Included in the Meta-Analysis (74 Reports, 31 Countries)


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  		Table 2. Continued


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  		Table 2. Continued


Figure 1189128
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  		Figure 1. Angina prevalence in women vs men. Labels are given for populations in which the prevalence differs by at least 2.5% between women and men.

Pooled Results From Meta-Analysis
The pooled sex ratio of angina prevalence from the random-effects model was 1.20 (95% CI 1.14 to 1.28, P<0.0001), with significant heterogeneity between studies (P<0.0001; Figure 2); the between-studies variance of the log (prevalence ratio) was 0.0347, which corresponds to a geometric SD of 1.20 [1.20=exp(square root of 0.0347)] acting in a multiplicative fashion. In other words, the average weighted prevalence ratio was 1.20, with a geometric SD of 1.21 (exponentiated value of the SD of the log-transformed values). The British sample in the Norwegian Migrant Study, performed in 1962, was the largest study that differed from the pooled estimate; 2 of the 3 estimates from India showed a male excess. The sex ratio in angina was similar in the subset of studies with complete information on MI mortality rates (n=66, sex ratio 1.20, 95% CI 1.12 to 1.27).


Figure 2189128
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  		Figure 2. Sex ratios in Rose angina prevalence ([PR] 95% CIs) ordered by study weight and pooled estimate from a random-effects model. Numbers in parentheses denote patients’ ages or year of study.

Meta-Regression of Influence of Country, Study, and Participant Characteristics on the Sex Ratio of Angina
Stratified analyses showed that the angina sex ratio did not differ significantly according to participant’s age (P=0.12), start year of the survey (P=0.89), the sex ratio in MI (P=0.09), or birth cohort (P=0.15; Table 3). A female excess was found across countries with MI mortality rates in women that ranged from 1 to 1764.4 per 100 000, with some evidence that the excess declined as MI mortality increased. This female excess was particularly high among American studies (1.40, 95% CI 1.28 to 1.52) and was higher among nonwhite ethnic groups than among whites. Estimates differed according to WHO region (P=0.0004), with Southeast Asia (4 studies from India, 1 from Sri Lanka) being the only region that did not show an overall female excess (sex ratio 0.88, 95% CI 0.56 to 1.38). The female excess effect did not differ according to definition of angina (P=0.83), questionnaire language (P=0.10), administration method (P=0.43), or response rate to survey (P=0.09). In meta-regression analyses of the subset of studies with complete information on all covariates (n=66), adjustment for all factors mentioned above reduced the residual variance between studies by 8%, which indicates that these factors explained only a small proportion of the heterogeneity between studies.


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  		Table 3. Sex Ratio in Angina Prevalence in Specified Subgroups (Random Effects Models)


*    Discussion
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Objective Addressed
In the present meta-analysis, which was based on almost 25 000 angina cases in women and men from 31 countries, we found that women had a slightly higher prevalence of stable angina pectoris than men, with a pooled sex ratio of 1.20. The present study adds to current understanding by demonstrating for the first time that the female excess is remarkably consistent across countries with widely differing MI mortality rates, spanning 4 decades of study period and 4 decades of participant age. Such generalizability suggests an inherent biological basis rather than artifactual explanations. The sex ratio of angina contrasts with the male excess of MI, is unexplained, and warrants further study. There have been no previous international comparisons focusing on angina in women and men, and as far as we are aware, this is the first systematic review of any etiological risk factor for stable angina, as distinct from aggregate end points of nonfatal MI and coronary death. The male focus of randomized trials and clinical guidelines in angina is at odds with the global public health burden and should be addressed.

Lack of Male Excess
Clinicians have been faced with a paradox, with the male preponderance of patients who reach coronary angiography contrasting with individually small reports from epidemiological studies that suggest that male sex may not be a risk factor for angina in the general population. The contribution of the present meta-analysis is to provide large-scale evidence that this lack of male excess in angina prevalence is highly robust across countries that differ markedly in rates of MI mortality (interquartile range 12.7 to 126.5 per 100 000 in women) and in angina prevalence. This contrasts with the male excess in MI that is present and of similar magnitude among countries with low, medium, and high rates of coronary death. The countries included in the present review span widely differing social conditions and smoking, diet, physical activity, and other health-related behaviors that influence MI mortality.81 Furthermore, we found a lack of male excess in angina at all ages, including women before and after menopause. This suggests that the changes in hormone, lipid, hemostatic, hemodynamic, and inflammatory factors9 at the time of the menopause are not important modifiers of the angina sex ratio. So why, then, do women have lower rates of MI than men but not of angina? Neither the observational studies on women’s reproductive history nor the trials of exogenous estrogens82 have addressed the development of stable angina, with all such studies focusing on MI. Further research is required to establish whether risk factors that are unique to women (eg, cyclic hormones with menses, pregnancy-associated remodeling of the coronary arteries, pregnancy-induced hypertension, and gestational diabetes), that are more common in women (eg, clustering of risk factors, lower levels of physical exercise, and higher mean heart rates), or that have stronger effects in women (eg, diabetes mellitus11,83), as well as their underlying genetic basis,84 differentially predict angina compared with MI.

Vasculopathy in Women With Angina
Angina in women is associated with myocardial ischemia through mechanisms that both overlap with and differ from those in men.25 The prevalence of atherosclerosis in the large epicardial coronary arteries in unbiased samples of women has been difficult to study. In a large primary care study (7906 coronary deaths), women with angina were at markedly increased risk of subsequent coronary mortality, even among women not known to have abnormal angiography findings.11 Intracoronary ultrasound studies of young heart transplant recipients shows a similar prevalence (52%) of intimal thickening in women and men.85 Studies in heart transplant86 and transsexual87 patients show that large arteries are inherently smaller in women, independent of body size, and such smaller coronary arteries may be associated with ischemia at a lower plaque burden.88 Many women with unobstructed coronary arteries have magnetic resonance spectroscopy changes consistent with ischemia,89 and these are associated with an increased risk of subsequent coronary events.90 Microvascular disease of the coronary arteries is more common in women than men and is associated with anginal symptoms and ischemia.91 Although some studies have suggested that retinal markers of microvascular disease might be stronger predictors of coronary events in women than men,26,92,93 this has not been found in other studies.94,95 Moreover, in the Multi-Ethnic Study of Atherosclerosis (MESA), retinal microvascular abnormalities showed similar associations in women and men in concentric left ventricular remodeling,96 aortic distensibility,97 and coronary artery calcification.98

Study Strengths and Limitations
A key strength of the present study is the use of a standard questionnaire to detect typical symptoms of angina pectoris, which is largely free of the potential underrecognition and selection biases that might affect angina diagnosed by physicians.11,12 However, several limitations require consideration. The first limitation is reporting bias. Importantly, the sex ratio we observed (1.2, small female excess) is identical to that observed when angina is defined clinically by the initiation of antianginal therapy in an entire country (Finland; sex ratio 1.2).11 This strongly suggests that the sex ratio is not an artifact of reporting on the Rose questionnaire. Second, the Rose angina questionnaire was originally developed and validated in men99 in western Europe and the United States; however, we found that angina prevalence in women was associated with country-level MI mortality rate, consistent with the impact of angina on mortality in individual women in cohort studies.20–24 Misdiagnosis of MI in women might explain why these associations were stronger in men. The lack of male excess in angina was found in each of the 31 countries studied, with their attending differences in public and professional awareness of heart disease in women and healthcare provision. Such a stable finding supports an inherent, valid underlying association. Third, the only available data for meta-analysis concerned prevalent rather than incident (new) cases. Although women with incident angina might have a better survival than men, the small size of this difference cannot account for the lack of male excess in angina occurrence. Furthermore, the present results are in accordance with studies of new cases of angina without a previous history of MI.10,11 Lastly, although we may have missed data sets, we estimate that 35 larger studies (with the 75th centile in study weight) each reporting the most extreme observed male excess (sex ratio 0.30) would be required to change the pooled estimate to 0.77 (the least extreme male excess in MI mortality). It is unlikely that such a volume of such extreme data would not have been reported or would have been reported but not found.

Clinical Implications
The present finding of the global phenomenon of a female excess in angina, independent of diagnostic and treatment practices, has clinical implications for understanding quality of care in women. First, inequities in management of women may be underestimates, because studies begin with populations that are selected by clinical contact rather than because of the presence of typical anginal symptoms in the general population. With each step in the presentation, investigation, and referral cascade, the ratio of women to men declines. Second, clinical guidelines should consider the population perspective. Recent guidelines specific to women recommend investigation among those with typical symptoms,100 but these and other guidelines are silent on the issue of whether women with typical symptoms present to a physician and, if so, whether their physician will label their symptoms as typical. Women with typical symptoms on Rose questionnaire who are not diagnosed with angina by a doctor have an increased mortality compared with women with no symptoms.12,101

Conclusions
Women have a similar or slightly higher prevalence of angina across countries that differ widely in MI mortality. Understanding the dichotomy of why men, who have a universal excess of fatal MI, do not have an excess of angina presents an important challenge for further research.


*    Acknowledgments
 
We would like to thank Dr M. Bobak, Professor R. Mohideen, and Professor M. Sekine for kindly permitting us to use angina estimates from their unpublished data.

Sources of Funding

Dr Hemingway is supported by a public health career scientist award from the Department of Health. Dr Langenberg is supported by a Health of the Public PhD Fellowship from the Medical Research Council.

Disclosures

None.


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CLINICAL PERSPECTIVE

Is male sex a risk factor for stable angina pectoris in the same way that it is for acute coronary syndromes? In this meta-analysis based on almost 25 000 angina cases in women and men from 31 countries, we found that women had a slightly higher prevalence of stable angina pectoris than men. This study adds to current understanding by demonstrating for the first time that the female excess of angina is remarkably consistent across countries with widely differing myocardial infarction mortality rates, spanning 4 decades of study period and 4 decades of participant age. Such generalizability may suggest an inherent biological basis rather than artifactual explanations. The sex ratio of angina contrasts with the ubiquitous male excess of myocardial infarction, is unexplained, and warrants further study. The observation of a female excess of angina, independent of diagnostic and treatment practices, has clinical implications for understanding the quality of care in women.