Original Article
Genetic Susceptibility to Death from Coronary Heart Disease in a Study of Twins
N Engl J Med 1994; 330:1041-1046April 14, 1994
- Abstract
Background
A family history of premature coronary heart disease has long been thought to be a risk factor for coronary heart disease. Using data from 26 years of follow-up of 21,004 Swedish twins born between 1886 and 1925, we investigated this issue further by assessing the risk of death from coronary heart disease in pairs of monozygotic and dizygotic twins.
Methods
The study population consisted of 3298 monozygotic and 5964 dizygotic male twins and 4012 monozygotic and 7730 dizygotic female twins. The age at which one twin died of coronary heart disease was used as the primary independent variable to predict the risk of death from coronary heart disease in the other twin. Information about other risk factors was obtained from questionnaires administered in 1961 and 1963. Actuarial life-table analysis was used to estimate the cumulative probability of death from coronary heart disease. Relative-hazard estimates were obtained from a multivariate survival analysis.
Results
Among the men, the relative hazard of death from coronary heart disease when one's twin died of coronary heart disease before the age of 55 years, as compared with the hazard when one's twin did not die before 55, was 8.1 (95 percent confidence interval, 2.7 to 24.5) for monozygotic twins and 3.8 (1.4 to 10.5) for dizygotic twins. Among the women, when one's twin died of coronary heart disease before the age of 65 years, the relative hazard was 15.0 (95 percent confidence interval, 7.1 to 31.9) for monozygotic twins and 2.6 (1.0 to 7.1) for dizygotic twins. Among both the men and the women, whether monozygotic or dizygotic twins, the magnitude of the relative hazard decreased as the age at which one's twin died of coronary heart disease increased. The ratio of the relative-hazard estimate for the monozygotic twins to the estimate for the dizygotic twins approached 1 with increasing age. These relative hazards were little influenced by other risk factors for coronary heart disease.
Conclusions
Our findings suggest that at younger ages, death from coronary heart disease is influenced by genetic factors in both women and men. The results also imply that the genetic effect decreases at older ages. .
Media in This Article
Figure 1
Age-Specific Probabilities of Death from Coronary Heart Disease in Subjects Whose Twins Died of the Disease.Table 1
Mortality Due to Coronary Heart Disease among Twins in the Study Sample of the Swedish Twin Registry.Article Activity
- Article
During the past 20 years, the role of family history in early-onset coronary heart disease in men has been well established1-14. However, only a few prospective studies have investigated the influence of familial factors on this disease in women15,16. Furthermore, the effect of a family history of coronary heart disease in older subjects, either men or women, has been examined in only one recent study17.
The extent to which the familial occurrence of coronary heart disease is due to genetic mechanisms can be assessed in twin or adoption studies. Early studies from the Swedish and Danish twin registries18,19 found a genetic influence on the risk of death from coronary heart disease in men by comparing concordance between monozygotic and dizygotic twins. A recent adoption study20 showed a genetic influence of mortality due to all cardiovascular and cerebrovascular diseases. None of these studies, however, specifically investigated the extent to which the genetic risk of coronary heart disease varied according to age at death. This is important because in several other chronic diseases, an early age at onset and an early age at death have been suggested to indicate genetic susceptibility21,22.
Using the Swedish Twin Registry, we performed a large prospective study examining the influence of genetic factors on mortality due to coronary heart disease at different ages, among both women and men.
Methods
Swedish Twin Registry
The cohort drawn from the Swedish Twin Registry for this study contained 10,944 pairs of twins (21,888 twins) of the same sex who were born between 1886 and 1925; both members of each pair were alive in 196123. The details of the compilation of the twin registry are presented elsewhere24.
The present study was based on a follow-up of mortality during 26 years, from 1961 through 1987. The information in the twin registry is matched annually with information about causes of death obtained from death certificates and coded according to the standards of the International Classification of Diseases (seventh, eighth, and ninth editions). Medical certification is carried out by the attending physician or coroner, with use of both clinical records and autopsy reports25. In this study, the listing of the underlying cause of death was used to identify deaths from coronary heart disease.
Study Population
The study population totaled 21,004 twins (10,502 pairs) after the exclusion of 439 pairs whose zygosity could not be determined and 3 other pairs for whom information about the cause of death was missing. The final sample included 3298 monozygotic and 5964 dizygotic male twins and 4012 monozygotic and 7730 dizygotic female twins.
Study Variables
Age at Death from Coronary Heart Disease
Since the twin registry is population-based and the study sample was identified (in 1961) before any twin had died of coronary heart disease, both twins of each pair were included as subjects in this study. The age at which a subject died of coronary heart disease was the primary variable used to predict the risk of death from coronary heart disease in that person's twin. Age at death was determined from the year of birth and year of death listed in the national population and death registries.
We divided the men who died of coronary heart disease into five age groups and the women into four groups, as shown in Table 1Table 1
Mortality Due to Coronary Heart Disease among Twins in the Study Sample of the Swedish Twin Registry.. All women who died of coronary heart disease before the age of 66 were included in one age group because of the small number of these subjects. In the survival analyses, the variable of death from coronary heart disease in one's twin was categorized according to age interval. The reference category for each variable was defined as the group of subjects whose twins did not die of coronary heart disease in that age interval.Other Risk Factors
Questionnaires had been sent to all twins in the study cohort in 1961 and 1963, to obtain information about their health status and health-related habits. All risk factors assessed in these questionnaires and known to be associated with coronary heart disease were chosen as covariates. These included cigarette smoking, body-mass index, diabetes, hypertension, level of education, and marital status.
In the 1961 questionnaire, subjects were asked whether they smoked then, had formerly smoked, or had ever smoked at all. Those who had never smoked served as the reference group in survival analyses. Body-mass index (calculated by dividing the weight in kilograms by the square of the height in meters) was determined from the weight and height listed on the 1963 questionnaire. This variable was categorized as less than 24, 24.0 to 27.9, and 28 or more.
The subjects' status with regard to hypertension and diabetes was assessed from their own replies; these variables were regarded as dichotomous. Educational status was treated dichotomously, with a grade-school education serving as the reference category. With respect to marital status, subjects were categorized as unmarried, married, or divorced. Unmarried subjects served as the reference group.
A variable for birth cohort was created for discrete-time survival analysis, with four birth periods: 1886 through 1895, 1896 through 1905, 1906 through 1915, and 1916 through 1925. Finally, zygosity was included as a dichotomous variable, with monozygosity serving as the base line.
Statistical Analysis
Correction for Left Censoring
All analyses were corrected for the left truncation due to staggering of the age at which each pair of twins was entered in the registry26. Furthermore, correcting for left truncation also adjusted for the effect of left censoring inherent in the registry, which was due to the study requirement that both twins be alive in 1961.
Life-Table Analysis
Life tables of mortality due to coronary heart disease were used to construct survival curves in order to examine the risk of death from coronary heart disease among the subjects whose twins had died of this disorder. Survival probabilities were calculated separately according to the age interval in which one's twin died of coronary heart disease.
The actuarial approach was used to estimate the cumulative probability of death from coronary heart disease, with correction for left censoring. This adjustment required staggered entry of the subjects into the life table according to their ages27.
Discrete-Time Survival Analysis
We performed a discrete-time survival analysis to obtain relative-hazard estimates for the effect of death from coronary heart disease in one's twin. We chose this approach because it corrected for the left censoring inherent in the registry, in addition to allowing for the effects of other covariates. Discrete-time survival analysis uses logistic regression to model hazard estimates when survival time is measured in discrete intervals28. With this method, the logarithm of the odds of death from coronary heart disease during an interval, which is conditional on survival until the beginning of that interval, is the dependent variable. The registry data were modified in a manner outlined by Hosmer and Lemeshow28 in order to use the model for discrete-time survival. The period of follow-up was 26 years; the earliest age at which a subject was considered to be at risk was 36 years, and the latest was 102 years. Survival analysis was performed for each year of risk for each subject.
Separate variables for the age at which one's twin died of coronary heart disease were created for the monozygotic twins and the dizygotic twins. The relative-hazard estimates for these variables in the monozygotic twins were then directly compared with the estimates in the dizygotic twins.
The covariates described above were also included in the discrete-time survival analyses. Since some information was lacking for each risk factor recorded in the registry, all multivariate analyses included only subjects for whom information about risk factors was complete (7715 men and 7748 women). The analyses evaluating the effect of the age of death from coronary heart disease in one's twin were also performed in the reduced sample, without the covariates; the results were very similar to those of the analysis of the full sample.
To correct for the fact that deaths from coronary heart disease in each pair of twins did not represent independent observations, the variances of the beta coefficients for the mortality-related variables were doubled in all analyses. This approximated an approach designed by Bonney29 for dependent observations in logistic regression.
Results
Concordance
Among the 1649 pairs of monozygotic male twins, 114 were concordant and 335 were discordant for death from coronary heart disease, as compared with 164 concordant and 705 discordant pairs among the 2982 pairs of dizygotic male twins. Among the 2006 pairs of monozygotic female twins, 66 were concordant and 273 were discordant for death from coronary heart disease, as compared with 99 concordant and 611 discordant pairs among the 3865 pairs of dizygotic female twins. There was thus a greater proportion of concordant pairs among the monozygotic twins than among the dizygotic twins in both men and women, suggesting a genetic component to death from coronary heart disease in the Swedish Twin Registry.
Life-Table Analysis
The age-specific risks derived from the life-table analysis presented in Figure 1Figure 1
Age-Specific Probabilities of Death from Coronary Heart Disease in Subjects Whose Twins Died of the Disease. demonstrate the influence of the age of one's twin at death from coronary heart disease on the probability of death from this disease. Both male and female twins died of coronary heart disease at earlier ages than did the whole population of the twin registry if their respective twins had died of this disease before the age of 76 years. Furthermore, the monozygotic twins died earlier of coronary heart disease than the dizygotic twins if their respective twins died in the early age intervals. The fact that the influence of having a monozygotic twin who died of coronary heart disease was greater than that of having a dizygotic twin suggests that there may be a genetic component to the risk that a twin may die of coronary heart disease before the age of 76. As the age at death from coronary heart disease in one's twin increased, the difference between the survival probability of the monozygotic twins and that of the dizygotic twins became smaller. This finding applied to both men and women (Figure 1). Also, the probability of death from coronary heart disease moved closer to that in the general twin population.If one's twin died after the age of 85 years, the probability of death from coronary heart disease was less than that in the general twin population, most likely because this general population included subjects whose twins had died at earlier ages.
Discrete-Time Survival Analysis
The results of the discrete-time survival analyses are presented in Table 2Table 2
Relative Hazard of Death from Coronary Heart Disease in Subjects According to the Age of Their Twins at Death from Coronary Heart Disease. for both men and women. The relative hazard of death from coronary heart disease for monozygotic male twins whose respective twins had died of coronary heart disease when 36 to 65 years old was approximately three times greater than the hazard for dizygotic twins. As the age at which one's twin died of coronary heart disease increased, the relative hazards for both the monozygotic and dizygotic twins decreased in magnitude. These results parallel the findings reflected by the survival curves.The relative hazards for monozygotic and dizygotic male twins whose respective twins had died of coronary heart disease when 56 to 75 years old were significantly different from each other. The finding that there was no significant difference between the estimates for monozygotic and dizygotic twins whose respective twins had died when 36 to 55 years old was most probably due to the small number of deaths from coronary heart disease in this age group, since the difference in the relative hazard in this group was the largest of such differences among all the age groups.
Among women, the relative hazard for twins whose respective twins had died of coronary heart disease before the age of 66 was 14.9 for monozygotic twins and 2.2 for dizygotic twins. As in the men, the hazards in both zygosity groups decreased as the age at which the twin had died of heart disease increased. Among women whose twins had died of coronary heart disease at 36 to 75 years of age, the relative hazard for monozygotic twins differed significantly from the relative hazard for dizygotic twins.
We next examined the extent to which other standard risk factors measured in the registry might confound the effect of early death from coronary heart disease in one's twin (Table 3Table 3
Relative Hazard of Death from Coronary Heart Disease in Subjects According to the Age of Their Twins at Death from Coronary Heart Disease, with Control for Risk Factors.). All covariates shown by univariate analysis to be significant predictors of death from coronary heart disease were included in a multivariate analysis along with variables related to the age at death. For the men these covariates were hypertension, diabetes, smoking, birth cohort, body-mass index, marital status, and education, and for women they were hypertension, diabetes, smoking, birth cohort, and body-mass index. All these covariates were also shown to be significant predictors in the multivariate analysis (Table 3).Among the men, the relative hazard when one's twin died at 36 to 55 years of age was reduced (from 13.4 to 8.1) only in the monozygotic twins, after other risk factors were included. To determine which variable most influenced this reduction in the relative hazard, each risk factor was individually included in a separate analysis with the variable for the age at which one's twin died of coronary heart disease. The reduction in risk was most strongly influenced by control for the effect of the birth cohort, which probably reflected temporal trends in mortality due to coronary heart disease among all subjects in the Swedish Twin Registry. To a smaller degree, controlling for diabetes also reduced the effect of having a twin who had died of coronary heart disease before the age of 56 years.
Among the dizygotic male twins and all female twins, there was little reduction in the relative hazard according to the age at which the first twin died of coronary heart disease when this variable was analyzed together with other covariates. Therefore, the effect of one's twin's death from coronary heart disease was largely uninfluenced by the other covariates.
Discussion
We found that among both women and men, death from coronary heart disease at an early age in one's twin was a strong predictor of the risk of death from this disorder. This risk was greater in monozygotic twins than in dizygotic twins and was largely independent of other personal risk factors for coronary heart disease.
Both the Nurses' Health Study16 and the Framingham Offspring Study17 found that a family history of coronary heart disease was an independent risk factor for coronary disease in women. The Danish Twin Concordance Study18 found that concordance for coronary heart disease was higher among monozygotic than among dizygotic twins, but the investigators did not stratify the subjects according to age or examine the effects of other risk factors. In our study, we have demonstrated that in both men and women a family history of early death from coronary heart disease is associated with an increased risk of death from the disease. Our data also suggest that this increased risk is, at least in part, genetic in nature.
We found that the difference in relative hazard between the monozygotic and dizygotic twins remained statistically significant except among subjects whose twins died of coronary heart disease after the age of 75. Our findings also indicate that genetic susceptibility to death from coronary heart disease becomes less pronounced in older age. The Danish Adoption Register study,20 however, revealed a genetic component only in subjects whose parents died of cardiovascular causes before the age of 50. The results of our study do not necessarily contradict those of the adoption study, since the larger size of our study population and the long period of follow-up allowed us to detect these associations at later ages (up to age 75) more readily.
There were several risk factors for coronary heart disease that were not measured in this study. In interpreting our results, we cannot ignore the possibility that monozygotic twins shared more environmental risk factors, such as dietary variables and physical inactivity, than the dizygotic twins. However, it is known that at least one primary variable for coronary heart disease, the total cholesterol level, is influenced in large part by genetic mechanisms, as shown in a recent study of Swedish twins reared apart30.
Since all the risk factors in the present study were determined from the subjects' responses, some cases of hypertension and diabetes mellitus may have been missed. Furthermore, information about risk factors was obtained only at the beginning of the follow-up period; therefore, both misclassification and changes in status for risk factors could have led to underestimation of their effect. Nevertheless, the risk factors of smoking, hypertension, diabetes, unmarried status, limited education, and obesity were still predictive of death from coronary heart disease.
One of the primary concerns in research into mortality is whether causes of death have been reliably identified. A study of death certificates entered in the Swedish Twin Registry from 1970 to 1975 found that they had a positive predictive value of 92 percent for death from coronary heart disease31. The authors of that study concluded that categorization of coronary heart disease as a cause of death on death certificates was reliable. Other studies of death certificates in Sweden have also shown the positive predictive value for such mortality to be more than 90 percent32,33.
The high preponderance of monozygotic as compared with dizygotic twins among the pairs of twins who both died of coronary heart disease at an early age suggests that multiple genetic factors interact to produce susceptibility to death from coronary disease34. The interaction may be due to the effects of several monogenic mechanisms, genes of small effect, or a combination of both. Since coronary heart disease has long been thought to have complex multifactorial causes, it is not surprising that our results support this view.
Many of the genetic mechanisms that predispose people to coronary heart disease remain unknown. Most of the research leading to an understanding of the genetic factors underlying coronary heart disease, which has been recently reviewed,35-38 has focused on the genetic variability of quantitative traits associated with the disease. The candidate genes and defects that underlie abnormal levels of lipoprotein gene products found in the plasma have also been carefully studied and reviewed in recent years39,40. It is unlikely, however, that abnormalities in lipoproteins account for all genetic risk of coronary heart disease. It has been suggested35,36,38,40 that the genetics of coronary heart disease would be better understood if studies included factors directly related to the pathogenesis of atherosclerotic plaques, such as the reactivity of the blood-vessel wall to injury, the role of scavenger cells, and the influence of the blood-clotting system. Also, specific polymorphisms in the gene encoding the angiotensin-converting enzyme may be involved41.
Our study suggests that it is important to identify both men and women whose first-degree relatives have died of coronary heart disease at any age, particularly when young, so that their modifiable risk factors for coronary disease can be addressed. Further research is clearly needed to determine the molecular mechanisms that underlie genetic susceptibility to coronary heart disease and how these mechanisms may vary with age.
Presented in part at the American Heart Association Cardiovascular Epidemiology Meetings, Memphis, Tenn., March 18-19, 1992.
Supported in part by the MacArthur Research Network on Successful Aging through a grant from the John D. and Catherine T. MacArthur Foundation, by a training grant (2-T32-MH-14235) from the National Institute of Mental Health, by a grant (HG-00348) from the National Institutes of Health, by a grant (09533) from the Medical Research Council of Sweden, by the Swedish Heart and Lung Foundation, and by King Gustav V and Queen Victoria's Foundation.
We are indebted to Drs. Nancy Pedersen and Larry Gall for their valuable input and to the Steering Committee of the Swedish Twin Registry for permitting us access to the registry.
Source Information
From the Departments of Epidemiology and Public Health (M.E.M., N.R., L.F.B.) and Genetics (N.R.), Yale University School of Medicine, New Haven, Conn.; and the Department of Environmental Hygiene, Karolinska Institute (B.F.), and the Division of Cardiovascular Medicine, Department of Internal Medicine, Karolinska Hospital, and Division of Epidemiology, Institute of Environmental Medicine, Karolinska Institute (U.F.), Stockholm, Sweden.
Address reprint requests to Dr. Marenberg at the Department of Epidemiology and Public Health, Yale University School of Medicine, 60 College St., New Haven, CT 06510.
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