Carotid-Artery Intima and Media Thickness as a Risk Factor for Myocardial Infarction and Stroke in Older Adults
Daniel H. O'Leary, M.D., Joseph F. Polak, M.D., M.P.H., Richard A. Kronmal, Ph.D., Teri A. Manolio, M.D., M.H.S., Gregory L. Burke, M.D., M.S., Sidney K. Wolfson, M.D., for The Cardiovascular Health Study Collaborative Research Group
Background The combined thickness of the intima and media ofthe carotid artery is associated with the prevalence of cardiovasculardisease. We studied the associations between the thickness ofthe carotid-artery intima and media and the incidence of newmyocardial infarction or stroke in persons without clinicalcardiovascular disease.
Methods Noninvasive measurements of the intima and media ofthe common and internal carotid artery were made with high-resolutionultrasonography in 5858 subjects 65 years of age or older. Cardiovascularevents (new myocardial infarction or stroke) served as outcomevariables in subjects without clinical cardiovascular disease(4476 subjects) over a median follow-up period of 6.2 years.
Results The incidence of cardiovascular events correlated withmeasurements of carotid-artery intima–media thickness.The relative risk of myocardial infarction or stroke increasedwith intima–media thickness (P<0.001). The relativerisk of myocardial infarction or stroke (adjusted for age andsex) for the quintile with the highest thickness as comparedwith the lowest quintile was 3.87 (95 percent confidence interval,2.72 to 5.51). The association between cardiovascular eventsand intima–media thickness remained significant afteradjustment for traditional risk factors, showing increasingrisks for each quintile of combined intima–media thickness,from the second quintile (relative risk, 1.54; 95 percent confidenceinterval, 1.04 to 2.28), to the third (relative risk, 1.84;95 percent confidence interval, 1.26 to 2.67), fourth (relativerisk, 2.01; 95 percent confidence interval, 1.38 to 2.91), andfifth (relative risk, 3.15; 95 percent confidence interval,2.19 to 4.52). The results of separate analyses of myocardialinfarction and stroke paralleled those for the combined endpoint.
Conclusions Increases in the thickness of the intima and mediaof the carotid artery, as measured noninvasively by ultrasonography,are directly associated with an increased risk of myocardialinfarction and stroke in older adults without a history of cardiovasculardisease.
High-resolution carotid ultrasonography has been used to obtainmeasurements of the thickness of the intima and media of thecarotid arteries. Previous studies have shown cross-sectionalassociations between common-carotid-artery intima–mediathickness and cardiovascular risk factors,1,2,3 the prevalenceof cardiovascular disease,2,3,4 and the involvement of otherarterial beds with atherosclerosis.5,6 Changes in common-carotid-arteryintima–media thickness have also been adopted as a surrogateend point for determining the success of interventions thatlower the levels of low-density lipoprotein cholesterol.7,8,9There are only a few studies showing an association betweenincreased carotid-artery intima–media thickness and newmyocardial infarction or stroke.10,11,12,13
We investigated the hypothesis that carotid-artery intima–mediathickness is associated with the incidence of myocardial infarctionand stroke in adults 65 years of age or older without preexistingcardiovascular disease who are living in the community. We alsohypothesized that carotid-artery intima–media thicknessis a predictor of these events after traditional cardiovascularrisk factors have been controlled for.
Methods
Subjects and Study Design
The study subjects were participants in the Cardiovascular HealthStudy, a prospective, multicenter study of men and women 65years of age or older that was sponsored by the National Heart,Lung, and Blood Institute.14 Between June 1989 and May 1990,5201 participants were enrolled from random samples of Medicareeligibility lists in Forsyth County, North Carolina; SacramentoCounty, California; Washington County, Maryland; and Pittsburgh.The study was approved by the institutional review boards atthe clinical sites and the coordinating center at the Universityof Washington, and all the participants provided written informedconsent. A detailed description of the recruitment methods hasbeen published elsewhere.15 Ninety-four percent of the membersof this first cohort were white, and most of the rest were black.A second cohort of 687 black participants was enrolled betweenJune 1992 and June 1993, three years after the enrollment ofthe original Cardiovascular Health Study cohort. Of the 5888participants, 1389 were eliminated from the analyses becausethey had cardiovascular disease at enrollment (997 with cardiacdisease, 249 with cerebrovascular disease, and 143 with both)and 30 (7 of whom also had cardiac disease) did not undergocarotid ultrasonography, leaving a sample of 4476 participants.
The base-line examination included a medical history taking,physical examination, laboratory testing, and assessment ofcardiovascular-disease status. The study design, quality-controlprocedures, laboratory methods, and blood-pressure measurementhave been previously reported.13,16,17,18,19,20,21,22,23,24,25,26,27The algorithms for classifying new myocardial infarctions andstrokes have also been published.27,28 Myocardial infarctionsand strokes were ascertained by questions at annual visits andinterim telephone interviews every six months, reporting ofevents by participants, and use of Medicare hospital records.Discharge summaries and diagnoses were obtained for all hospitalizations.For all potential new myocardial infarctions or strokes, additionalinformation, including results of cardiac-enzyme measurements,serial electrocardiography, cranial computed tomography, andcerebral magnetic resonance imaging, was collected from medicalrecords. Interviews were conducted with surviving participantsor, for fatal events, from witnesses or proxies. All data onevents were reviewed and initially classified by local physiciansat the field centers. Final classification of all events wasdetermined by a committee of Cardiovascular Health Study investigatorsafter a review of the medical records.
The carotid arteries were evaluated with high-resolution B-modeultrasonography.29 One longitudinal image of the common carotidartery and three longitudinal images of the internal carotidartery were acquired. Measurements were made at a central readingcenter by readers blinded to all clinical information. Measurementswere made from stored digital images when the black cohort wasenrolled three years later, so that the same readers were usedfor all readings. The maximal rather than the mean intima–mediathickness was used as the key variable after a statistical investigationof the strength of the associations between risk factors andintima–media thickness.
The many measures of intima–media thickness were summarizedin two variables, one for the common carotid artery and onefor the internal carotid artery. The maximal intima–mediathickness of the common carotid artery and of the internal carotidartery was defined as the mean of the maximal intima–mediathickness of the near and far wall on both the left and rightsides. The number of measurements that were available for averagingthus ranged from 1 to 4 for the common carotid artery and 1to 12 for the internal carotid artery. A composite measure thatcombined the maximal common-carotid-artery intima–mediathickness and maximal internal-carotid-artery intima–mediathickness was obtained by averaging these two measurements afterstandardization (subtraction of the mean and division by thestandard deviation for the measurement).30 The Spearman correlationsbetween all the readings at base line and all the readings performedby separate readers three years later were 0.75, 0.86, and 0.84for the common carotid artery, internal carotid artery, andcombined measure, respectively.
Statistical Analysis
Preexisting cardiac disease was defined as documented symptomaticmyocardial infarction, angina, coronary-artery bypass surgery,or coronary-artery angioplasty. Preexisting cerebrovasculardisease was defined as a history of stroke, transient ischemicattack, or carotid endarterectomy. Participants with a historyof cardiac disease or cerebrovascular disease were excludedso that we could study asymptomatic persons without clinicalsymptoms or signs of cardiovascular disease.
All analyses were performed with SPSS/Windows statistical software.31The Cox proportional-hazards regression model was used to estimatethe relative risk of new myocardial infarction, stroke, andthe combined end point. Quintiles of carotid-artery measuresand the continuous version of these variables were used in theseanalyses. Data on subjects were censored after death from anycause and after the last follow-up visit.
We evaluated the effect of traditional risk factors on any observedassociations between carotid intima–media thickness anda given cardiovascular outcome with use of Cox proportional-hazardsmodels selected by a stepwise strategy applied to the followingvariables (with P=0.10 necessary to enter a variable into themodel): carotid-artery intima–media thickness, age, sex,race, presence or absence of atrial fibrillation, systolic anddiastolic pressure, history of diabetes, history of smoking,history of hypertension, and low-density lipoprotein and high-densitylipoprotein cholesterol levels. A variable that was enteredinto a model for a given outcome was kept in all three modelsin order to permit a direct comparison between models. The interactionbetween sex and the wall-thickness variables was tested in allthe models. We also evaluated the relative importance of intima–mediathickness (as a continuous variable) as compared with traditionalrisk factors in Cox proportional-hazards models both withoutadjustment for age and sex and with adjustment for these variables.The comparison of models was based on the Wald statistic, whichhas an asymptotic chi-square distribution.
Results
The base-line characteristics of the 4476 study participantsare given in Table 1. The mean age of the participants at entrywas 72.5 years, and 38.8 percent were men. Blacks made up 15.2percent of the sample. The median follow-up was 6.2 years (maximum,7). There were 267 new myocardial infarctions, 284 new strokes,and 496 participants who had a new myocardial infarction orstroke. Fifty-five participants had both a myocardial infarctionand a stroke, but only the event that occurred first was usedfor the analysis of the combined end point.
Table 1. Characteristics of the 4476 Study Participants at Enrollment.
Figure 1 shows the cumulative event-free rates with respectto the combined end point according to quintiles of intima–mediathickness. The estimated cumulative rate of the combined endpoint for the highest quintile of the combined wall-thicknessmeasure was over 25 percent at seven years, as compared witha cumulative rate of less than 5 percent for the lowest quintile.The yearly incidence of the combined end point of myocardialinfarction or stroke increased with increasing quintiles foreach of the measures of intima–media thickness (Figure 2).The rates were similar for quintiles of common-carotid-arteryintima–media thickness and internal-carotid-artery intima–mediathickness, but the gradient of increasing risk was slightlyless pronounced than for the combined measure.
Figure 1. Unadjusted Cumulative Event-free Rates for the Combined End Point of Myocardial Infarction or Stroke, According to Quintile of Combined Intima–Media Thickness.
The estimated cumulative rate of the combined end point for the fifth quintile of the combined measure was over 25 percent at seven years, as compared with a cumulative rate of less than 5 percent for the first quintile.
Figure 2. Unadjusted Incidence of Myocardial Infarction or Stroke According to Quintile of Carotid-Artery Intima–Media Thickness.
The yearly incidence of the combined end point of myocardial infarction or stroke increased with increasing quintiles of each of the measures of intima–media thickness (IMT). The rates were similar for quintiles of common-carotid-artery (CCA) intima–media thickness and internal-carotid-artery (ICA) intima–media thickness, but the gradient of increasing risk was slightly less pronounced than for the combined measure.
In a Cox proportional-hazards regression, the combined measureof intima–media thickness was significantly associatedwith the risk of the combined end point after adjustment forage and sex (P<0.001 by the test for trend), with personsin the highest quintile having a risk that was 3.9 times asgreat as that of persons in the lowest quintile (Table 2). Therisk associated with the combined measure of intima–mediathickness remained significant (P< 0.001 by the test fortrend), although slightly reduced in magnitude, after adjustmentfor systolic and diastolic blood pressure, pack-years of smoking,and the presence or absence of atrial fibrillation and diabetes.Similar results were observed for the individual measures ofintima–media thickness, but with somewhat smaller relativerisks (Table 2).
Table 2. Relative Risk of the Combined End Point of Stroke or Myocardial Infarction as a Function of the Common-Carotid-Artery and Internal-Carotid-Artery Intima–Media Thickness Expressed as Quintiles and as a Continuous Variable.
Cox proportional-hazards models using the intima–mediathickness as a continuous variable also showed strong associationswith the combined event. The age- and sex-adjusted relativerisks associated with a change of 1 SD in the intima–mediathickness of the common carotid artery, internal carotid artery,and the two combined were similar, with a 35 to 44 percent increasein risk, and remained significant after adjustment for riskfactors. Comparison of the chi-square statistics showed thatthe combined measure of intima–media thickness was a strongerpredictor than the individual measures.
We examined the strength of the associations with myocardialinfarction alone as the outcome. The results for myocardialinfarction paralleled those for the combined end point. Althoughthe intima–media thickness of both the common and internalcarotid arteries was associated with the risk of myocardialinfarction, the relative risks associated with greater common-carotid-arteryintima–media thickness tended to be lower than those associatedwith greater internal-carotid-artery intima–media thicknessand with greater combined intima–media thickness (Table 3).Increases of 1 SD in common-carotid-artery, internal-carotid-artery,and combined thickness were associated with 33 to 46 percentincreases in risk after adjustment for age and sex.
Table 3. Relative Risk of Myocardial Infarction as a Function of the Common-Carotid-Artery and Internal-Carotid-Artery Intima–Media Thickness Expressed as Quintiles and as a Continuous Variable.
In contrast, the common-carotid-artery intima–media thicknessand the combined measure were better predictors of stroke thanthe internal-carotid-artery intima–media thickness (Table 4).An increment of 1 SD in wall thickness was associated witha 33 to 43 percent increase in risk after adjustment for ageand sex and a 25 to 33 percent increase in risk after adjustmentfor additional factors (P<0.001 for all comparisons).
Table 4. Relative Risk of Incident Stroke as a Function of the Common-Carotid-Artery and Internal-Carotid-Artery Intima–Media Thickness Expressed as Quintiles and as a Continuous Variable.
Adding a term for interaction between intima–media thicknessand sex to the above models did not result in any significanteffect in any of the models (P>0.20 for all comparisons).
Cox proportional-hazards models, with the intima–mediathickness as a continuous variable, showed strong associationsbetween the combined outcome and traditional risk factors aswell as the intima–media thickness (Table 5). The age-and sex-adjusted relative risks associated with an increaseof 1 SD in the combined measure of intima–media thicknesswere at least as strong as those associated with traditionalrisk factors (Table 5).
Table 5. Comparison of the Associations of Individual Risk Factors with the Combined Event of Stroke or Myocardial Infarction in Cox Proportional-Hazards Models with and without Adjustment for Age and Sex.
Discussion
We have previously reported on the positive associations betweencardiovascular risk factors and carotid-artery intima–mediathickness.2,29 We have also shown that a measurement that combinedcommon-carotid-artery and internal-carotid-artery intima–mediathicknesses was more strongly associated with the prevalenceof cardiovascular disease and with traditional risk factorsthan either variable used alone.30 We now report a positiveassociation between carotid-artery intima–media thicknessand the incidence of new myocardial infarction and stroke inadults 65 years of age or older who did not have a history ofcardiovascular disease. We have shown that the intima–mediathickness is a strong predictor of both myocardial infarctionand stroke and that the risk gradients are similar. The combinedmeasure of common-carotid-artery and internal-carotid-arteryintima–media thickness was a better predictor of eventsthan either thickness measure taken alone. When statisticaladjustment was made for traditional cardiovascular risk factors,carotid-artery intima–media thickness remained a significantpredictor of cardiovascular events. The strength of the associationsbetween intima–media thickness and outcome was at leastas strong as the associations seen with traditional risk factors.
Four other studies have explored the possible association betweencarotid-artery intima–media thickness and the incidenceof cardiovascular events.10,11,12,13 Three of these studiesreported results using measurements of the common carotid artery.Salonen and Salonen, in a study of 1257 middle-aged Finnishmen, observed an association between common-carotid-artery intima–mediathickness and cardiac events. This observation was based ona one-year follow-up and a total of 24 events.10 Because thedefinitions of high-risk categories in their study were differentfrom those we used, direct comparison of our results with theirsis not possible.
The Rotterdam Elderly Study was a single-center, prospectivestudy of disease and disability in the elderly involving 7983subjects 55 years of age or older.32 They performed a case–controlstudy in a subgroup of their population that showed an associationbetween common-carotid-artery intima–media thickness andthe risk of myocardial infarction and stroke.11 The Rotterdaminvestigators did not find a consistent relative risk of myocardialinfarction, whereas we found that the risk of myocardial infarctionincreased in a monotonic fashion with increasing intima–mediathickness. They included subjects with angina, transient ischemicattack, and other manifestations of cardiovascular disease atentry, whereas we excluded such subjects. The inclusion of subjectswith symptomatic cardiovascular disease may explain why theRotterdam investigators were unable to show a strong associationbetween common-carotid-artery intima–media thickness andthe risk of myocardial infarction, whereas we show a strongrisk gradient. The differences between their study and oursmay be explained by the larger number of subjects and the longerduration of follow-up in our study. Moreover, our results extendtheir findings by showing that internal-carotid-artery intima–mediathickness is as good a predictor as common-carotid-artery intima–mediathickness, and the combination of the two is statistically superiorto either one.
The subjects of the Atherosclerosis Risk in Communities Studywere 15,792 middle-aged men and women, 45 to 64 years of ageand living in four separate areas of the United States, whowere followed for four to seven years for the incidence of cardiacdisease.12 Although it reported only far-wall measurements,the Atherosclerosis Risk in Communities Study also used a combinedmeasure of common-carotid-artery and internal-carotid-arteryintima–media thicknesses. Although they did not reporton the associations with stroke, the investigators found a similarassociation between intima–media thickness and cardiacdisease in a younger population.12 Hodis et al. also found anassociation between intima–media thickness and coronaryevents in a study of men who had undergone coronary-artery bypassgraft surgery and were followed for an average of 8.8 years.13
In our study, which assessed whether noninvasive measurementshave any predictive power with respect to subsequent cardiovascularevents, we were aware that carotid-artery intima–mediathickness is strongly associated with cardiovascular risk factors.2,3,4,5,29,33,34Despite this association, we have shown that the carotid-arteryintima–media thickness is a strong predictor of new cardiovascularevents even after statistical adjustment for other risk factors.This finding has clinical significance, particularly with regardto the elderly. Calculated risk profiles have been proposedfor use in identifying persons at high risk for myocardial infarction35and for stroke.36 However, borderline elevation of multiplerisk factors is common in the elderly, and the association betweenrisk factors and cardiovascular disease may weaken in the lateryears of life.37,38 Therefore, it may be difficult for cliniciansto identify older patients with subclinical cardiovascular diseaseon the basis of classic risk factors. Increased intima–mediathickness, an indicator of subclinical disease, may reflectthe consequences of past exposure to risk factors. The additionof measurements of intima–media thickness to cardiovascularrisk equations may help identify asymptomatic persons who wouldbenefit from aggressive preventive measures.
This strategy, if applied to populations similar to our cohort,would require combined measurements of common-carotid-arteryand internal-carotid-artery intima–media thickness atthe far and near walls of the arteries. The internal-carotid-arteryintima–media measurements, because of the way they areperformed, probably reflect the presence of focal plaque andmay thus be more representative of risk-factor exposure.39 Thismay explain in part the added predictive power of combined measurementsof the common and internal carotid arteries. Similarly, near-wallmeasurements are also useful, since far-wall measurements hada significantly weaker association with outcomes (P<0.001)than the combined near- and far-wall measurements (analysesnot shown).
Measurements of carotid-artery intima–media thicknesswere as strong predictors of events as the traditional riskfactors. After adjustment for conventional risk factors, thecombined measure of intima–media thickness was the variablemost strongly associated with the risk of cardiovascular events.An increase of 1 SD in combined intima–media thicknesswas associated with a relative risk of 1.36 for the combinedend point of myocardial infarction or stroke after adjustmentfor age, sex, and the other risk factors. In contrast, in thesame model an increase in age of 1 SD (5.5 years) was associatedwith a relative risk of 1.34, and an increase in systolic bloodpressure of 1 SD (21.5 mm Hg) with a relative risk of 1.21.The relative strength of the associations between events andintima–media thickness, as compared with the associationbetween events and other traditional risk factors, suggeststhat intima–media thickness is by itself as powerful apredictor of cardiovascular events as the traditional risk factors.
Variability in measurement of the intima–media thicknessmight have affected our results. The strong correlations betweenreplicate readings of the intima–media thickness (Spearmancoefficients of 0.75 to 0.86) are similar to those already published.2,4,5,11,12,13,30Any increase in the precision of the measurements as a resultof technological improvements might increase their predictivepower for cardiovascular events.
We conclude that the intima–media thickness of the commoncarotid artery and the internal carotid artery is strongly associatedwith the risk of myocardial infarction and stroke in asymptomaticolder adults. Measurements of carotid-artery intima–mediathickness retain predictive power with respect to new cardiovascularevents even after traditional risk factors for cardiovascularevents have been taken into consideration; moreover, such measurementsseem more powerful predictors than these same risk factors.
Supported in part by contracts (NO1-HC85079 through NO1-HC85086)with the National Heart, Lung, and Blood Institute.
Source Information
From the Department of Radiology, Tufts–New England Medical Center, Boston (D.H.O.); the Department of Radiology, Brigham and Women's Hospital, Boston (J.F.P.); the Department of Biostatistics, University of Washington, Seattle (R.A.K.); the Division of Epidemiology and Clinical Applications, National Heart, Lung, and Blood Institute, Bethesda, Md. (T.A.M.); the Department of Public Health Sciences, Bowman Gray School of Medicine, Winston-Salem, N.C. (G.L.B.); and the Department of Surgery, University of Pittsburgh, Pittsburgh (S.K.W.).
Address reprint requests to the CHS Coordinating Center, Century Sq., 1501 4th Ave., Suite 2025, Seattle, WA 98101, or to daniel.oleary{at}es.nemc.org.
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