Original Article
Association between a Deletion Polymorphism of the Angiotensin-Converting-Enzyme Gene and Left Ventricular Hypertrophy
N Engl J Med 1994; 330:1634-1638June 9, 1994
- Abstract
Background
Epidemiologic studies have shown that left ventricular hypertrophy is often found in the absence of an elevated cardiac workload. To investigate whether such hypertrophy is determined in part by genetic factors, we studied the association between this condition, as assessed by electrocardiographic criteria, and a deletion (D)-insertion (I) polymorphism of the angiotensin-converting-enzyme (ACE) gene.
Methods
A population-based random sample of 711 women and 717 men 45 to 59 years of age was studied cross-sectionally in Augsburg, Germany. Electrocardiographic indexes, including the Sokolow-Lyon index, Minnesota Code 3.1, and the Rautaharju equations, were used to detect left ventricular hypertrophy. The status of the ACE gene with respect to the deletion-insertion allele was determined by the polymerase chain reaction in all subjects with left ventricular hypertrophy and an identical number of control subjects without the condition who were matched for age, sex, and blood-pressure status.
Results
We identified 141 women and 149 men with evidence of left ventricular hypertrophy. Among these subjects, an excess were homozygous for the D allele of the ACE gene (odds ratio, 1.76; 95 percent confidence interval, 1.22 to 2.53; P = 0.003). The association of the DD genotype with left ventricular hypertrophy was stronger in men (odds ratio, 2.63; 95 percent confidence interval, 1.50 to 4.64; P<0.001) than in women and was most prominent when blood-pressure measurements were normal (odds ratio, 4.05; 95 percent confidence interval, 1.76 to 9.28; P = 0.001). This association was evident for each of the scores recorded in the electrocardiographic testing for left ventricular hypertrophy.
Conclusions
The findings suggest that left ventricular hypertrophy is partially determined by genetic disposition. They identify the DD genotype of ACE as a potential genetic marker associated with an elevated risk of left ventricular hypertrophy in middle-aged men.
Media in This Article
Figure 1
Percentage of Subjects with Electrocardiographically Detected Left Ventricular Hypertrophy (LVH), According to Blood Pressure.Figure 2
Odds Ratios and 95 Percent Confidence Intervals for Left Ventricular Hypertrophy in Subjects Homozygous for the D Allele of the ACE Gene.Article Activity
- Article
Left ventricular hypertrophy, a major independent risk factor for morbidity and mortality from cardiovascular disease,1-4 is widely thought to be a consequence of left ventricular pressure overload5,6. However, the degree of such hypertrophy in patients with mildly elevated arterial pressure is not uniform and may range from normal ventricular mass to severe hypertrophy6,7. Furthermore, recent epidemiologic studies have shown that many subjects with left ventricular hypertrophy have normal blood pressure, suggesting that factors other than hemodynamic overload may contribute to the hypertrophy4.
Neuroendocrine factors such as angiotensin II and bradykinin have been implicated in the modulation of cardiac growth8,9. Experimental studies suggest that angiotensin II may stimulate cardiac protein synthesis,10-12 whereas bradykinin may have an antiproliferative effect13. Angiotensin-converting enzyme (ACE) is a key enzyme in the production of angiotensin II as well as the degradation of bradykinin and thus may participate in the modulation of cardiac growth. In addition, recent studies of experimental left ventricular hypertrophy due to pressure overload as well as studies in patients with dilated cardiomyopathy have demonstrated elevated cardiac expression of ACE messenger RNA and ACE activity14-16.
The cloning of the ACE gene has made it possible to identify a deletion (D)-insertion (I) polymorphism that appears to affect the level of serum ACE activity17-19. More important, the genotype (DD) with the highest ACE levels may be a risk factor for myocardial infarction as well as dilated and hypertrophic cardiomyopathy20-22. We explored a possible association between homozygosity of the ACE D allele (the DD genotype) and left ventricular hypertrophy identified by electrocardiography in a population-based random sample of 1428 Western Europeans.
Methods
Study Population
The cross-sectional study was carried out in Augsburg, Germany, as part of the Multinational Monitoring of Trends and Determinants in Cardiovascular Disease project of the World Health Organization23,24. Eligible participants were initially sampled at random in 1984-1985 (in a two-stage cluster sampling stratified for age and sex) from all inhabitants of a mixed urban and rural area. All who participated in the first follow-up examination in 1987-1988 (participation rate, 93.1 percent) were included after they gave informed consent to participate in the study. The study population comprised 711 women and 717 men, 45 to 59 years of age. All the subjects were whites of Western European descent.
All the subjects responded to a questionnaire on their medical history and lifestyle. Laboratory evaluations for the determination of blood count and cholesterol were carried out with standard methods. Blood pressure was measured three times with a random-zero device (Hawksley, Lancing, United Kingdom), and strict quality control was applied. The mean of the last two measurements was used. Hypertension was defined as a systolic blood pressure of 160 mm Hg or higher, a diastolic blood pressure of 95 mm Hg or higher, or both. The status of antihypertensive treatment was assessed on the basis of the prescriptions used during the week before the interview. Standard 12-lead electrocardiograms were recorded in all patients and analyzed with a digital system. Left ventricular hypertrophy was defined according to published criteria, with the Sokolow-Lyon index,25 Minnesota Code 3.1,26 and Rautaharju equations (for both men and women)27. Subjects with evidence of bundle-branch block or Wolff-Parkinson-White syndrome were excluded from the analysis.
Extraction and Amplification of Genomic DNA
DNA was prepared from frozen peripheral blood with standard procedures28. Briefly, 500 microliters of blood was diluted in 4.5 ml of buffer (155 mM ammonium chloride, 10 mM potassium carbonate, and 0.1 mM EDTA; pH 8.0), vortexed, and centrifuged. The pellets were resuspended in 100 microliters of buffer (10 mM TRIS-hydrochloric acid and 1 mM EDTA; pH 8.0) to which 300 microliters of lysis buffer (400 mM sodium chloride, 10 mM TRIS-hydrochloric acid, and 2 mM EDTA; pH 8.0), 15 microliters of sodium dodecyl sulfate (20 percent), and 30 microliters of proteinase K (10 mg per milliliter of solution) were added. Overnight digestion with proteinase K at 55 °C was followed by centrifugation and precipitation of the supernatant in ethanol. The polymerase chain reaction (PCR) was carried out as described elsewhere,29 except that glycerine (2.5 microliters) was added to the reaction mixture. The PCR products were denatured and separated by agarose-gel electrophoresis21.
Statistical Analysis
Subjects were considered to have left ventricular hypertrophy if they fulfilled any of the three electrocardiographic criteria. Controls were selected from the remaining subjects and matched one-to-one for age, sex, and blood-pressure status (i.e., normotensive, normotensive with antihypertensive treatment, hypertensive with antihypertensive treatment, or hypertensive without treatment).
The statistical analyses were based on the calculation of odds ratios to provide an estimate of the relative risk of left ventricular hypertrophy in groups of subjects with different genotypes. To account for the influence of matching, odds ratios were calculated for all pairs, for men and women separately, and for prespecified subgroups defined according to blood-pressure status30. The analyses were performed by means of conditional logistic-regression models that, in the final stage, also included potential confounding variables such as body-mass index, blood pressure, and heart rate as a continuous variable.
Results
The screening of this large, population-based sample identified electrocardiographic evidence of left ventricular hypertrophy in 141 women and 149 men. The demographic characteristics of the subjects with left ventricular hypertrophy and the matched controls did not differ significantly with regard to systolic and diastolic blood pressure, heart rate, body-mass index, hematocrit, total and high-density lipoprotein cholesterol, or smoking behavior (data not shown).
The distribution of the DD, ID, and II genotypes in the control group was 24.8 percent, 58.6 percent, and 16.6 percent, respectively; there was an overall frequency of 54 percent for the D allele and 46 percent for the I allele (Table 1Table 1
Distribution of ACE Genotypes among Middle-Aged Subjects with Left Ventricular Hypertrophy and Matched Controls.), which compares closely with other white populations studied19,20. In contrast, the group with left ventricular hypertrophy was characterized by an excess of subjects homozygous for the D allele (Table 1). Analyses of the matched pairs revealed that the DD genotype was associated with a significantly increased risk of left ventricular hypertrophy, as detected by electrocardiography (Table 1).The DD genotype was not associated with a significant increase in the risk of left ventricular hypertrophy in women (odds ratio, 1.22; 95 percent confidence interval, 0.84 to 1.77; P = 0.42). In contrast, men who were homozygous for the D allele (i.e., who had the DD genotype) more often had electrocardiographic evidence of left ventricular hypertrophy than did those with the ID and II genotypes (odds ratio, 2.63; 95 percent confidence interval, 1.50 to 4.64; P<0.001) (Table 1).
A substantial proportion of women and men with electrocardiographic evidence of left ventricular hypertrophy were found to be normotensive. Figure 1Figure 1
Percentage of Subjects with Electrocardiographically Detected Left Ventricular Hypertrophy (LVH), According to Blood Pressure. shows the increasing prevalence of left ventricular hypertrophy in subjects with borderline blood-pressure readings or readings indicating hypertension; in absolute numbers, however, the majority of subjects with left ventricular hypertrophy (as defined by all the electrocardiographic criteria combined) had normal blood-pressure readings (Figure 1). Therefore, we studied prespecified subgroups to determine whether the association between the DD genotype of the ACE gene and left ventricular hypertrophy was influenced by blood-pressure levels. Interestingly, the strongest association was found when blood pressure was normal (Figure 2Figure 2Odds Ratios and 95 Percent Confidence Intervals for Left Ventricular Hypertrophy in Subjects Homozygous for the D Allele of the ACE Gene. and Table 2Table 2
Distribution of ACE Genotypes among Normotensive and Hypertensive Men with Left Ventricular Hypertrophy and Matched Controls.). The association of the DD genotype with left ventricular hypertrophy was evident in groups of normotensive middle-aged men with the condition as identified by the Sokolow-Lyon index, Minnesota Code 3.1, or the Rautaharju equations, as well as in the combined group, for which the odds ratio reached 4.05 (P = 0.001) (Table 2).Additional covariables were not related to the ACE genotype. Conditional logistic-regression analyses demonstrated that the significant association of the DD genotype with electrocardiographic evidence of left ventricular hypertrophy was independent of possible confounding variables, such as blood pressure, heart rate, body-mass index, lipid profile, hematocrit, and cigarette consumption (data not shown). Likewise, excluding subjects with electrocardiographic evidence of myocardial infarction (12 men and 1 woman) or ischemia at rest (9 men and 3 women) did not affect the observed association between the DD genotype and left ventricular hypertrophy detected by electrocardiography.
Discussion
Our results strongly suggest that genetic background, in addition to hemodynamic overload,5,6 obesity,31 and certain environmental factors,32 may influence the development of left ventricular hypertrophy. The idea that genetic background contributes to the regulation of cardiac hypertrophy originated in studies of twins. The investigation by Adams et al. suggested that left ventricular mass is partly determined by familial influences33. Verhaaren et al. concluded that over 60 percent of the variability in left ventricular mass can be explained by heritable factors34. Our study extends these findings by identifying a molecular genetic marker, a deletion polymorphism in intron 16 of the ACE gene, that is associated with electrocardiographic evidence of left ventricular hypertrophy.
Further analyses identified two factors that affected the association between the ACE DD genotype and left ventricular hypertrophy. First, among men homozygous for the deletion allele of the ACE gene, the odds of meeting the electrocardiographic criteria for left ventricular hypertrophy were 2.63 times greater than among the other men, whereas no significant association was seen among women. Interestingly, previous epidemiologic studies pointed out that the heritability of left ventricular mass as well as the incidence of left ventricular hypertrophy may differ between men and women, suggesting sex-related differences in the pathogenesis of the condition4,34.
Second, 62 percent of the subjects with electrocardiographic evidence of left ventricular hypertrophy in this study were found not to have hypertension. This finding, although surprising, agrees with prior population-based studies. In particular, Levy et al. reported for the Framingham Heart Study that 56 percent of middle-aged women and 57 percent of middle-aged men with left ventricular hypertrophy identified by echocardiography had systolic blood-pressure readings below 140 mm Hg4. In the present study, the large number of normotensive subjects with left ventricular hypertrophy allowed us to test whether the association of that condition with the ACE deletion-insertion polymorphism was influenced by blood pressure. Interestingly, the strongest association between the ACE DD genotype and left ventricular hypertrophy was identified when blood pressure was normal. We postulate that the effect of the DD genotype on the development of left ventricular hypertrophy may be stronger when no other causative factors are present, such as left ventricular pressure overload.
A potential limitation of this study is that the identification of left ventricular hypertrophy by electrocardiography may have influenced the results. Electrocardiography is less sensitive than echocardiography for the estimation of left ventricular mass2; however, digital and automated electrocardiographic interpretation carries the advantage of unbiased classification of left ventricular hypertrophy and allows screening in large populations such as ours3. The clinical relevance of the electrocardiographic indexes used may be underscored by an increased mortality from cardiovascular causes among subjects with electrocardiographic evidence of left ventricular hypertrophy1,3,27. Finally, to reduce further any potential bias created by the use of electrocardiographic criteria, we carried out three analyses with different electrocardiographic scores for left ventricular hypertrophy. All the electrocardiographic indexes used identified an increased risk of left ventricular hypertrophy among normotensive men homozygous for the D allele of ACE.
Our study does not identify the mechanism by which the DD genotype of the ACE gene may affect cardiac hypertrophy. Since some components of the renin-angiotensin system have been genetically linked to arterial hypertension,35-37 elevation of blood pressure in itself could potentially account for the increased incidence of left ventricular hypertrophy in subjects homozygous for the ACE D allele. This explanation seems unlikely. First, the ACE polymorphism did not show linkage with blood pressure in two previous studies19,38 or in this one (data not shown). Second, in the present study, the subjects with left ventricular hypertrophy and the control subjects were matched by the study design for the presence (or absence) of hypertension and antihypertensive treatment. Finally, the association of the ACE DD genotype was most prominent when blood pressure was normal. Thus, even if a potential interaction of exercise-related or situational hypertension cannot be fully excluded, the association of the ACE DD genotype and left ventricular hypertrophy seems to involve other mechanisms than blood-pressure levels. In this regard, it may be of interest that a meta-analysis of multiple clinical studies has suggested that pharmacologic inhibitors of ACE may be superior to some other antihypertensive agents in inducing regression of cardiac hypertrophy, even though they have similar effects on blood pressure39. Furthermore, ACE inhibitors promote better survival in heart failure than do other vasodilators40. Therefore, clinical data support the hypothesis that the inhibition of ACE may affect cardiac structure and function by mechanisms other than simple reduction in blood pressure.
The data do not permit us to conclude definitely that the D allele of ACE mediates the development of left ventricular hypertrophy. Alternatively, the DD genotype may serve as a marker of a critical gene in close proximity. Thus, it is certainly premature to speculate whether the association of the ACE DD genotype and left ventricular hypertrophy may affect outcomes for patients treated with ACE inhibitors. A final limitation is that this study examined a Western European population composed of white adults. Further population-based studies are needed to determine whether homozygosity for the ACE D allele is associated with an increased risk of hypertrophy in normotensive adults from other geographic areas and racial backgrounds. However, this study suggests that genetic disposition may substantially contribute to the development of left ventricular hypertrophy in normotensive subjects.
Presented in part at the 66th scientific sessions of the American Heart Association, Atlanta, November 8-11, 1993.
Supported by a grant (DFG Schu 617/3-1) from the Deutsche Forschungsgemeinschaft, by an Astra Award for Cardiovascular Research, and by the Bundesministerium fur Forschung und Technologie. Dr. Lorell is an Established Investigator of the American Heart Association.
We are indebted to Ingrid Kirst, Peter Schickling, and Gunther Bruckschlegel for technical assistance, and to Dr. Charalampos Aslanidis for critical discussion of this work.
Source Information
From the Medizinische Klinik II, University of Regensburg, Regensburg, Germany (H.S., S.R.H., G.A.J.R.); the Institut fur Epidemiologie (H.-W.H., M.S., U.K.) and the MEDIS Institut (S.P.), GSF Forschungszentrum, Munchen-Neuherberg, Germany; the Institut fur Epidemiologie und Sozialmedizin (H.-W.H., U.K.), University of Munster, Munster, Germany; and the Charles A. Dana Research Institute and Harvard-Thorndike Laboratory of Beth Israel Hospital, Department of Internal Medicine, Cardiovascular Division, Beth Israel Hospital and Harvard Medical School, Boston (B.H.L.).
Address reprint requests to Dr. Schunkert at the Klinik and Poliklinik fur Innere Medizin II, Universitat Regensburg, Franz-Josef Strauss Allee, D-93053 Regensburg, Germany.
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