Coronary Calcium as a Predictor of Coronary Events in Four Racial or Ethnic Groups
Robert Detrano, M.D., Ph.D., Alan D. Guerci, M.D., J. Jeffrey Carr, M.D., M.S.C.E., Diane E. Bild, M.D., M.P.H., Gregory Burke, M.D., Ph.D., Aaron R. Folsom, M.D., Kiang Liu, Ph.D., Steven Shea, M.D., Moyses Szklo, M.D., Dr.P.H., David A. Bluemke, M.D., Ph.D., Daniel H. O'Leary, M.D., Russell Tracy, Ph.D., Karol Watson, M.D., Ph.D., Nathan D. Wong, Ph.D., and Richard A. Kronmal, Ph.D.
Background In white populations, computed tomographic measurementsof coronary-artery calcium predict coronary heart disease independentlyof traditional coronary risk factors. However, it is not knownwhether coronary-artery calcium predicts coronary heart diseasein other racial or ethnic groups.
Methods We collected data on risk factors and performed scanningfor coronary calcium in a population-based sample of 6722 menand women, of whom 38.6% were white, 27.6% were black, 21.9%were Hispanic, and 11.9% were Chinese. The study subjects hadno clinical cardiovascular disease at entry and were followedfor a median of 3.8 years.
Results There were 162 coronary events, of which 89 were majorevents (myocardial infarction or death from coronary heart disease).In comparison with participants with no coronary calcium, theadjusted risk of a coronary event was increased by a factorof 7.73 among participants with coronary calcium scores between101 and 300 and by a factor of 9.67 among participants withscores above 300 (P<0.001 for both comparisons). Among thefour racial and ethnic groups, a doubling of the calcium scoreincreased the risk of a major coronary event by 15 to 35% andthe risk of any coronary event by 18 to 39%. The areas underthe receiver-operating-characteristic curves for the predictionof both major coronary events and any coronary event were higherwhen the calcium score was added to the standard risk factors.
Conclusions The coronary calcium score is a strong predictorof incident coronary heart disease and provides predictive informationbeyond that provided by standard risk factors in four majorracial and ethnic groups in the United States. No major differencesamong racial and ethnic groups in the predictive value of calciumscores were detected.
The Framingham risk score uses standard risk factors to estimatethe risk of coronary events in persons without previous coronaryheart disease.1,2 However, because this score predicts coronaryevents only moderately well, researchers have explored othermethods to identify patients who would benefit most from intensiveprevention efforts.3,4,5,6,7 Radiographically detectable coronary-arterycalcium is a marker of subclinical coronary heart disease andpredicts coronary events in white populations.8,9,10,11,12,13,14,15,16,17,18As a result, there has been considerable interest in the potentialuse of measurements of coronary-artery calcium in models ofrisk prediction.
The potential role of this variable as a predictor of risk iscomplicated by evidence that there are substantial differencesin the prevalence and extent of coronary calcification amongvarious ethnic groups. Bild et al.19 reported that the prevalenceof detectable coronary calcification was 22%, 15%, and 8% loweramong blacks, Hispanics, and Chinese, respectively, than amongwhites. Other studies20,21,22 have reported differences in coronarycalcification between blacks and whites, although one study23found no difference. However, the relationship between the amountof coronary calcium and the incidence of coronary events invarious ethnic groups has not been examined.
The Multi-Ethnic Study of Atherosclerosis (MESA)24 investigatesthe prevalence, correlates, and progression of subclinical cardiovasculardisease. The study cohort is a population-based sample fromsix urban communities, with oversampling of blacks, Chinese,and Hispanics. We used the data collected from the MESA cohortto study the relationship between coronary calcification andfuture coronary events in four major ethnic groups.
Methods
Study Participants
Details of the design and organization of the MESA have beenreported previously.19 Between July 2000 and September 2002,we selected 6814 persons to be members of the MESA cohort atsix field centers (Baltimore; Chicago; Forsyth County, NorthCarolina; Los Angeles; New York; and St. Paul, Minnesota). Theparticipants were required to be between 45 and 84 years ofage and to have no clinical cardiovascular disease at the timeof enrollment in the study. The participants were recruitedat each site from lists of residents, dwellings, and telephone-companycustomers. In the last few months of the recruitment period,participants were also recruited from lists of Medicare beneficiariesobtained from the Centers for Medicare and Medicaid Servicesand by referrals from other participants in order to ensurethe enrollment of adequate numbers of elderly subjects and subjectsfrom all four ethnic groups. Participants identified themselvesas white, black, Hispanic, or Chinese at the time of enrollment.The study was approved by the institutional review boards ofeach site, and all participants gave written informed consent.
Computed Tomographic Scanning
Carr et al. have reported details of the methods used by theMESA for computed tomographic (CT) scanning and for interpretationof the scans.25 Each of the six MESA centers assessed the amountof coronary calcium with the use of either an electron-beamCT scanner (at the Chicago, Los Angeles, and New York centers)or a multidetector CT system (at the Baltimore, Forsyth County,and St. Paul centers). Certified technologists placed radiographicphantoms containing identical and known concentrations of calciumbeneath the thorax of each participant and then scanned theparticipant two times. A radiologist or cardiologist read allCT scans at a single center (the Los Angeles Biomedical ResearchInstitute at Harbor–University of California Los AngelesMedical Center, Torrance) and used an interactive scoring systemsimilar to that of Yaghoubi et al.26 The reader–work stationinterface calibrated each tomographic image according to theestimated attenuation of the calcium phantom and then identifiedand quantified the coronary calcium in each image. The coronarycalcium score (Agatston score)27 was calculated for each scan,and the mean of the two scans was used in all analyses. Intraobserverand interobserver agreement was excellent (kappa statistics,0.93 and 0.90, respectively). The participants were told eitherthat they had no coronary calcification or that the amount wasless than average, average, or greater than average and thatthey should discuss the results with their physicians.
Risk Factors
As part of the baseline examination, clinical teams at eachof the six centers collected information on cardiovascular riskfactors, including family history of coronary heart disease,a history of smoking, level of low-density lipoprotein (LDL)cholesterol, level of high-density lipoprotein (HDL) cholesterol,hypertension, and diabetes. Using a Dinamap Pro 1000 automatedoscillometric sphygmomanometer (Critikon), we measured restingblood pressure three times with the participant in the seatedposition. A central laboratory (University of Vermont, Burlington)measured levels of total and HDL cholesterol, triglycerides,plasma glucose, and high-sensitivity C-reactive protein in bloodsamples obtained after a 12-hour fast. Diabetes was definedas a fasting plasma glucose level greater than 140 mg per deciliter(7.8 mmol per liter) or a history of medical treatment for diabetes.The body-mass index was calculated as the weight in kilogramsdivided by the square of the height in meters. Family historyof coronary heart disease was obtained by asking the participantswhether any member of their immediate family (parents, siblings,and children) had had a fatal or nonfatal myocardial infarction,coronary angioplasty, or coronary-artery bypass surgery. Theparticipants were classified as current cigarette smokers, formersmokers, or persons who had never smoked.
Follow-up
We recorded new cardiovascular events for a median of 3.9 years(maximum, 5.3). At intervals of 9 to 12 months, an interviewercontacted each participant or a family member by telephone toinquire about interim hospital admissions, outpatient diagnosesof cardiovascular disease, and deaths. To verify self-reporteddiagnoses, we requested copies of medical records for participantswho had been hospitalized or received an outpatient diagnosisof cardiovascular disease. We obtained records of 98% of reportedcardiovascular events associated with hospitalization. For participantswho had died of cardiovascular causes outside the hospital,we conducted interviews with the next of kin and requested copiesof death certificates.
Trained personnel abstracted data from medical records thatreported possible cardiovascular events. Two physicians whowere members of the MESA mortality and morbidity review committeeindependently classified events and assigned incidence dates.If they disagreed, the full committee made the final classification.For the purpose of this study, we classified myocardial infarction,death from coronary heart disease, definite angina followedby coronary revascularization, definite angina not followedby coronary revascularization, and probable angina followedby coronary revascularization as coronary heart disease events.
The diagnosis of myocardial infarction was based on a combinationof symptoms, electrocardiographic findings, and levels of cardiacbiomarkers. We used hospital records and family interviews todetermine whether deaths were related to coronary heart disease.A death was considered related to coronary heart disease ifit occurred within 28 days after a myocardial infarction, ifthe participant had had chest pain within the 72 hours beforedeath, or if the participant had a history of coronary heartdisease and there was no known nonatherosclerotic, noncardiaccause of death. The adjudicators graded angina as definite,probable, or absent on the basis of their clinical judgment.A classification of definite or probable angina required clearand definite documentation of symptoms distinct from the diagnosisof myocardial infarction. A classification of definite anginaalso required objective evidence of reversible myocardial ischemiaor obstructive coronary artery disease. A more detailed descriptionof the MESA follow-up methods is available at www.mesa-nhlbi.org.
Statistical Analysis
We used chi-square tests for discrete variables and one-wayanalysis-of-variance tests for continuous variables to testfor differences in demographic and risk factors between ethnicgroups and between participants with and without coronary events.To describe the frequency of coronary events according to timesince the measurement of coronary calcium, we constructed Kaplan–Meiercumulative-event curves for major coronary events (myocardialinfarction and death from coronary heart disease) and for anycoronary event. The data were stratified according to coronarycalcium score, with the use of the same cutoff points as thoseused by Greenland et al. (0, 1 to 100, 101 to 300, and >300).8
We used Cox proportional-hazards regression to estimate hazardratios for major coronary events and for any coronary eventaccording to the coronary calcium score. Tests for nonproportionalhazards using Schoenfeld residuals resulted in nonsignificantfindings in all analyses. The coronary calcium score was examinedboth as a stratified variable (with the same cutoff points asthose used by Greenland et al.) and as a continuous variable.In the analysis treating coronary calcium score as a continuousvariable, we used the base-2 logarithm of the sum of the coronarycalcium score plus 1 (log2[CAC+1]). The choice of base 2 forthe logarithm allowed us to examine how a doubling of the calciumscore affects the risk of events, since each unit differencein the log-transformed calcium score represents a doubling ofthe score. The addition of 1 to the calcium score before logarithmictransformation allowed us to include in the analysis those patientswith a calcium score of zero.
After estimating the hazard ratios for coronary events for theentire study cohort, we performed additional regression analysesfor each individual ethnic group, treating calcium score asa continuous variable. We computed receiver-operating-characteristic(ROC) curves and tested for equality of the areas under thecurves for the individual ethnic groups.
All models were adjusted for age, sex, ethnic group, cigarettesmoking, presence or absence of diabetes, total cholesterollevel, HDL cholesterol level, systolic and diastolic blood pressure,and use or nonuse of lipid-lowering or antihypertensive medication.In addition, we allowed any of the following variables to enterthe models if they were statistically significant at the P<0.05level: family history of coronary heart disease, C-reactiveprotein level, triglyceride level, creatinine level, body-massindex, waist circumference, and hip circumference. However,none of these variables met the criterion for statistical significance.We also carried out analyses that included terms for the interactionbetween ethnic group and calcium score, as well as any significantinteractions (P<0.10) between ethnic group and any of therisk factors. All analyses were performed with Stata software,version 9.2.
Results
Study Cohort
Follow-up information was not available for 35 (0.5%) of the6814 members of the MESA cohort, and 5 were discovered to havehad a cardiovascular event before enrollment in the cohort,Measurements of one or more risk factors were missing for anadditional 52 members (0.8%), none of whom had a coronary eventafter enrollment. The remaining 6722 participants are the subjectof this report. Table 1 shows the baseline characteristics ofthe study cohort. As expected, the cardiovascular risk profilewas less favorable in those in whom coronary heart disease subsequentlydeveloped than in those in whom it did not. The baseline characteristicsof the study cohort varied significantly among the four ethnicgroups, as shown in Table 2.
Table 2. Baseline Demographic Characteristics and Risk Factors According to Racial or Ethnic Group.
The prevalence of coronary calcification (coronary calcium score>0) was 70.4% for white men, 52.0% for black men, 56.6% forHispanic men, and 59.2% for Chinese men (P<0.001). The correspondingfigures for women were 44.7%, 37.0%, 34.8%, and 41.9%, respectively(P<0.001). Details of the relationship between ethnic groupand coronary calcification in the MESA have been published previously.23
A total of 162 participants had coronary events. Eighty-ninehad a major event (72 had a nonfatal myocardial infarction and17 died of coronary heart disease), and 73 had angina (13 haddefinite angina not followed by revascularization, 56 had definiteangina followed by revascularization, and 4 had probable anginafollowed by revascularization).
Coronary Calcium as a Predictor of Coronary Heart Disease
Figure 1 shows the unadjusted Kaplan–Meier cumulative-eventcurves for major coronary events and for any coronary eventaccording to coronary calcium score. The differences among thesecurves were statistically significant (P<0.001).
Figure 1. Unadjusted Kaplan–Meier Cumulative-Event Curves for Coronary Events among Participants with Coronary-Artery Calcium Scores of 0, 1 to 100, 101 to 300, and More Than 300.
Panel A shows the rates for major coronary events (myocardial infarction and death from coronary heart disease), and Panel B shows the rates for any coronary event. The differences among all curves are statistically significant (P<0.001).
Table 3 shows the risk of major events and of any event associatedwith higher calcium score after adjustment for standard riskfactors. The hazard ratio increases with an increase in stratumof calcium score. The largest increase in hazard ratio occursfor calcium scores greater than 100. The risk of both majorcoronary events and any event was increased by a factor of atleast seven among participants with scores over 100 as comparedwith those without any coronary calcium. Table 3 also showsthe increase in the risk of a major coronary event and of anycoronary event associated with a doubling of the coronary calciumscore (a 1-unit increase in log2[CAC+1]). After adjustment forstandard risk factors, a doubling of the calcium score resultedin a 20% increase in the risk of a major event and a 26% increasein the risk of any event.
Table 3. Risk of Coronary Events Associated with Increasing Coronary-Artery Calcium Score after Adjustment for Standard Risk Factors.
Predicting Coronary Heart Disease in Individual Ethnic Groups
Table 4 shows the risk of coronary heart disease associatedwith increasing calcium score in each of the four ethnic groups,adjusted for standard risk factors and interactions. For eachethnic group, the risk associated with a doubling of the calciumscore increased by 15 to 35% for a major event and by 18 to39% for any event. All adjusted hazard ratios are significant(P<0.02), except for the hazard ratio for major coronaryevents among Chinese participants, who had only six such events.There was no interaction between ethnic group and the risk associatedwith increasing calcium score.
Table 4. Risk of Coronary Heart Disease Associated with Coronary-Artery Calcium Score in Four Racial or Ethnic Groups.
Table 5 shows the areas under the ROC curves for the predictionof major coronary events and of any coronary event accordingto ethnic group, calculated on the basis of the standard riskfactors alone and on the basis of the standard risk factorsplus the coronary calcium score. The areas under the curve forthe prediction of major events and those for the predictionof any event were greater when the calcium score was added tothe standard risk factors. These increases were statisticallysignificant for each ethnic group, except for the predictionof any event in Hispanics and of major events in Hispanics andwhites.
Table 5. Use of Area under the Curve for Risk Factors Alone and for Risk Factors plus Coronary-Artery Calcium Score to Predict Major Coronary Events and Any Coronary Event, According to Racial or Ethnic Group.
Discussion
We examined the predictive value of measurements of coronary-arterycalcium in a multiethnic U.S. population. We found that a doublingof the calcium score increased the estimated probability ofboth major coronary events (myocardial infarction and deathfrom coronary heart disease) and any coronary event by approximately25% during a median follow-up period of 3.8 years. Moreover,the coronary calcium score contributed to the risk of both majorevents and any event in four major ethnic groups independentlyof other risk factors.
Other studies evaluating the prognostic accuracy of the measurementof coronary calcium by CT have shown that coronary calcificationis predictive of coronary events independently of standard riskfactors or risk-factor scores.8,9,10,11,12,13,14,15,16,17,18For example, a study by LaMonte et al. of nearly 11,000 adultsfrom 22 to 96 years of age who underwent a screening medicalexamination reported hazard ratios for major coronary eventsof 8.7 among men and 6.3 among women with coronary calcium scoresof 400 or more during a mean follow-up of 3.5 years.15 Amongmen and women 40 to 45 years of age in the Prospective ArmyCoronary Calcium Project, the presence of coronary calcium wasassociated with an increase in the risk of coronary events bya factor of 12 during 3 years of follow-up.17 Finally, in thepopulation-based Rotterdam Study of elderly asymptomatic subjects,during a mean follow-up of 3.3 years, the adjusted relativerisks of coronary events associated with calcium scores of 101to 400, 401 to 1000, and more than 1000 (as compared with scoresof 0 to 100) were 3.1, 4.6, and 8.3, respectively.18 However,many previous studies included participants who were referredby themselves or their physicians or who were chosen becausethey were at high risk. In addition, previous analyses did notattempt to evaluate the effect of ethnic group on the predictivevalue of coronary calcification.
It has been reported previously that the prevalence and extentof coronary calcification differ substantially among ethnicgroups.19,20,21,22 Our study suggests that these differencesdo not decrease the predictive value of this subclinical markerin American minority groups. Our results, in fact, suggest thatthe coronary calcium score is valuable for the prediction offuture events even in ethnic groups in which coronary calcificationis less prevalent.
Our study has several limitations. CT acquisition and readingmethods differ among studies and clinical scanning centers.We calibrated images with the use of a calcium phantom to controlfor variability in some of the physical characteristics of thescanners.28 We also chose a large field of view to include thephantom in all images, and we set the minimum lesion size usedto define a calcified plaque conservatively large to reducevariability among scanners resulting from differences in thesignal-to-noise ratio. These and other differences from theusual clinical scanning protocols are expected to have someeffect on the absolute values of calcium measurements but willonly minimally affect the ranking of participants' calcium scores.We suggest caution in using the absolute calcium-score numbersfrom our study in settings in which scanning and reading protocolsdiffer greatly from those used in the MESA.
In our study, the participants and their physicians were informedof the coronary calcium scores. This might have influenced ourresults in two ways. First, participants with high coronarycalcium scores might have changed their behavior or receivedpreventive treatment that would have lowered their risk of coronaryevents. This would have biased our results toward the null hypothesisfor the relationship between coronary calcium and coronary disease.Second, knowledge of the calcium score might have influencedthe diagnosis of angina, potentially biasing the results towardshowing a stronger relationship between coronary calcium andcoronary disease. However, the relationship between coronarycalcium and major coronary events would not have been affectedby this bias.
Although our findings suggest that coronary calcium predictscoronary heart disease in four ethnic groups, ethnic-specificcalibration of calcium measures may be needed to adjust forbaseline differences among the ethnic groups. Finally, our studywas limited by the small number of clinical events. Furtherfollow-up of the MESA cohort will allow refinement of our riskestimates.
In conclusion, we found that measurement of coronary-arterycalcium in a multiethnic American cohort added incremental valueto the prediction of coronary heart disease over that of thestandard coronary risk factors in each of four ethnic groups.
Supported by grants (N01-HC-95159 to N01-HC-95166 and N01-HC-95169)from the National Heart, Lung, and Blood Institute.
Dr. Guerci reports receiving grant support from Pfizer. Dr.O'Leary reports receiving consulting fees from Schering, SanofiAventis, Eli Lilly, and Pfizer, receiving lecture fees fromAstraZeneca, and owning stock in Medpace. Dr. Watson reportsreceiving consulting fees from Merck and lecture fees from Merck,Abbott, and Schering. No other potential conflict of interestrelevant to this article was reported.
We thank the other investigators, the staff, and the participantsin the MESA (www.mesa-nhlbi.org) for their valuable contributions.
Source Information
From the University of California at Irvine, Irvine (R.D., N.D.W.); Saint Francis Hospital, Roslyn, NY (A.D.G.); Wake Forest Baptist Medical Center, Winston-Salem, NC (J.J.C., G.B.); the Division of Prevention and Population Sciences, National Heart, Lung, and Blood Institute, Bethesda, MD (D.E.B.); the University of Minnesota, Minneapolis (A.R.F.); Northwestern University, Chicago (K.L.); Columbia University, New York (S.S.); Johns Hopkins University, Baltimore (M.S., D.A.B.); Caritas Carney Hospital, Dorchester, MA (D.H.O.); the University of Vermont, Burlington (R.T.); the University of California at Los Angeles, Los Angeles (K.W.); and the University of Washington, Seattle (R.A.K.).
Address reprint requests to Dr. Detrano at the Department of Radiological Sciences, University of California at Irvine, Medical Sciences Bldg., Irvine, CA 92697, or at robert{at}chinacal.org.
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Coronary Calcium and Events in Four Ethnic Groups
Payne P. W. Jr., Littmann L., Burtey S., Dussol B., Brunet P., Goyal S. K., Punnam S. R., Nasir K., Budoff M. J., Blumenthal R., Guerci A. D., Bild D. E., Kronmal R. A., Weintraub W. S., Diamond G. A.
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(2009). Pattern of Arterial Calcification in Patients with Systemic Lupus Erythematosus. The Journal of Rheumatology
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(2009). ACCF/AHA/ACP 2009 competence and training statement: a curriculum on prevention of cardiovascular disease.. J Am Coll Cardiol
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(2009). ACCF/AHA/ACP 2009 Competence and Training Statement: A Curriculum on Prevention of Cardiovascular Disease: A Report of the American College of Cardiology Foundation/American Heart Association/American College of Physicians Task Force on Competence and Training (Writing Committee to Develop a Competence and Training Statement on Prevention of Cardiovascular Disease): Developed in Collaboration With the American Academy of Neurology; American Association of Cardiovascular and Pulmonary Rehabilitation; American College of Preventive Medicine; American College of Sports Medicine; American Diabetes Association; American Society of Hypertension; Association of Black Cardiologists; Centers for Disease Control and Prevention; National Heart, Lung, and Blood Institute; National Lipid Association; and Preventive Cardiovascular Nurses Association. Circulation
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(2009). Myeloperoxidase, Subclinical Atherosclerosis, and Cardiovascular Disease Events. J Am Coll Cardiol Img
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(2009). The association of pericardial fat with incident coronary heart disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Am. J. Clin. Nutr.
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(2009). Traffic exposure and subclinical cardiovascular disease: is the association modified by socioeconomic characteristics of individuals and neighbourhoods? Results from a multilevel study in an urban region. Occup. Environ. Med.
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(2009). Primary and Secondary Prevention of Cardiovascular Diseases: A Practical Evidence-Based Approach. Mayo Clin Proc.
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(2009). 25-Hydroxyvitamin D Levels Inversely Associate with Risk for Developing Coronary Artery Calcification. J. Am. Soc. Nephrol.
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(2009). Association of kidney function and uncarboxylated matrix Gla protein: Data from the Heart and Soul Study. Nephrol Dial Transplant
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(2009). Thoracic aortic calcium versus coronary artery calcium for the prediction of coronary heart disease and cardiovascular disease events.. J Am Coll Cardiol Img
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(2009). Prognostic value of multislice computed tomography and gated single-photon emission computed tomography in patients with suspected coronary artery disease.. J Am Coll Cardiol
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WRITING GROUP MEMBERS, , Lloyd-Jones, D., Adams, R., Carnethon, M., De Simone, G., Ferguson, T. B., Flegal, K., Ford, E., Furie, K., Go, A., Greenlund, K., Haase, N., Hailpern, S., Ho, M., Howard, V., Kissela, B., Kittner, S., Lackland, D., Lisabeth, L., Marelli, A., McDermott, M., Meigs, J., Mozaffarian, D., Nichol, G., O'Donnell, C., Roger, V., Rosamond, W., Sacco, R., Sorlie, P., Stafford, R., Steinberger, J., Thom, T., Wasserthiel-Smoller, S., Wong, N., Wylie-Rosett, J., Hong, Y., for the American Heart Association Statistics Comm,
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(2008). Short Sleep Duration and Incident Coronary Artery Calcification. JAMA
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Pollin, T. I., Damcott, C. M., Shen, H., Ott, S. H., Shelton, J., Horenstein, R. B., Post, W., McLenithan, J. C., Bielak, L. F., Peyser, P. A., Mitchell, B. D., Miller, M., O'Connell, J. R., Shuldiner, A. R.
(2008). A Null Mutation in Human APOC3 Confers a Favorable Plasma Lipid Profile and Apparent Cardioprotection. Science
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(2008). Signs of subclinical coronary atherosclerosis in relation to risk factor distribution in the Multi-Ethnic Study of Atherosclerosis (MESA) and the Heinz Nixdorf Recall Study (HNR). Eur Heart J
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Ostrom, M. P., Gopal, A., Ahmadi, N., Nasir, K., Yang, E., Kakadiaris, I., Flores, F., Mao, S. S., Budoff, M. J.
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Payne, P. W. Jr., Littmann, L., Burtey, S., Dussol, B., Brunet, P., Goyal, S. K., Punnam, S. R., Nasir, K., Budoff, M. J., Blumenthal, R., Guerci, A. D., Bild, D. E., Kronmal, R. A., Weintraub, W. S., Diamond, G. A.
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