Association between Multiple Cardiovascular Risk Factors and Atherosclerosis in Children and Young Adults
Gerald S. Berenson, M.D., Sathanur R. Srinivasan, Ph.D., Weihang Bao, Ph.D., William P. Newman, M.D., Richard E. Tracy, M.D., Ph.D., Wendy A. Wattigney, M.S., for The Bogalusa Heart Study
Background In adults, cardiovascular risk factors reinforceeach other in their effect on cardiovascular events. However,information is scant on the relation of multiple risk factorsto the extent of asymptomatic atherosclerosis in young people.
Methods We performed autopsies on 204 young persons 2 to 39years of age, who had died from various causes, principallytrauma. Data on antemortem risk factors were available for 93of these persons, who were the focus of this study. We correlatedrisk factors with the extent of atherosclerosis in the aortaand coronary arteries.
Results The extent of fatty streaks and fibrous plaques in theaorta and coronary arteries increased with age. The associationbetween fatty streaks and fibrous plaques was much strongerin the coronary arteries (r=0.60, P<0.001) than in the aorta(r=0.23, P=0.03). Among the cardiovascular risk factors, body-massindex, systolic and diastolic blood pressure, and serum concentrationsof total cholesterol, triglycerides, low-density lipoproteincholesterol, and high-density lipoprotein cholesterol, as agroup, were strongly associated with the extent of lesions inthe aorta and coronary arteries (canonical correlation [a measureof the association between groups of variables]: r=0.70; P<0.001).In addition, cigarette smoking increased the percentage of theintimal surface involved with fibrous plaques in the aorta (1.22percent in smokers vs. 0.12 percent in nonsmokers, P=0.02) andfatty streaks in the coronary vessels (8.27 percent vs. 2.89percent, P=0.04). The effect of multiple risk factors on theextent of atherosclerosis was quite evident. Subjects with 0,1, 2, and 3 or 4 risk factors had, respectively, 19.1 percent,30.3 percent, 37.9 percent, and 35.0 percent of the intimalsurface covered with fatty streaks in the aorta (P for trend=0.01).The comparable figures for the coronary arteries were 1.3 percent,2.5 percent, 7.9 percent, and 11.0 percent, respectively, forfatty streaks (P for trend=0.01) and 0.6 percent, 0.7 percent,2.4 percent, and 7.2 percent for collagenous fibrous plaques(P for trend=0.003).
Conclusions These findings indicate that as the number of cardiovascularrisk factors increases, so does the severity of asymptomaticcoronary and aortic atherosclerosis in young people.
Atherosclerosis leading to coronary heart disease is complexin origin. Involved in the pathogenesis of atherosclerosis arehemodynamic, thrombotic, and carbohydrate–lipid metabolicvariables, along with intrinsic characteristics of the arterialwall.1 These physiologic and biochemical factors underlie theclinical events that may eventually occur. Environmental factorssuch as smoking or a sedentary lifestyle also contribute tothis process. The progression of atherosclerotic disease andthe increasing severity of atherosclerosis relate not only tothe presence and extent of cardiovascular risk factors but alsoto the persistence of risk factors over time.2,3 Sudden deathmay occur in a young person with only a single lesion complicatedby a coronary thrombus, without extensive vessel disease. Consequently,the extent of vascular lesions may not be directly related tothe occurrence of clinical events, such as myocardial infarction.Morbidity due to coronary artery disease, however, is generallyrelated to the extent of vascular lesions.4 In this regard,clinical risk factors are considered to be useful in predictingthe severity of atherosclerosis.5
Epidemiologic studies have established that multiple risk factorsincrease the probability of cardiovascular events, since cardiovascularrisk factors tend to reinforce each other in their influenceon morbidity and mortality.6 Although a specific risk factorinfluences the risk that a person will have cardiovascular disease,risk factors tend to aggregate and usually appear in combination.Furthermore, since clustering of risk factors is evident inchildhood and persists into young adulthood,7,8,9,10 the presenceof multiple risk factors could indicate the acceleration ofatherosclerosis in young people.
Coronary arteriography has contributed considerably to elucidatingthe relation of the severity of coronary artery disease to cardiovascularrisk factors. Unfortunately, assessing the extent of atheroscleroticcoronary lesions by this invasive method in asymptomatic youngpeople is not practical, and its value is limited as comparedwith that of actual anatomical observations.11 Autopsy datafrom epidemiologic studies have shown a relation between coronaryartery disease and cardiovascular risk factors; for example,high serum total cholesterol concentrations and cigarette smokingare important contributors to the development of coronary atherosclerosis.6Autopsy studies from the Bogalusa Heart Study have demonstrateda strong association of specific antemortem risk factors withvascular lesions in children and young adults.12,13 These observationshave been extended by the findings in a larger, multicenterpostmortem study, Pathobiological Determinants of Atherosclerosisin Youth.14,15,16,17 Multiple risk-factor data collected antemortem in the Bogalusa Heart Study can be applied further toautopsy data. In this study we examined the influence of multiplerisk factors on the extent of atherosclerosis in the aorta andcoronary arteries in young people.
Methods
Study Population
The Bogalusa Heart Study is a long-term epidemiologic studyof cardiovascular risk factors from birth through the age of38 years in a biracial population (65 percent white and 35 percentblack).18,19 Seven cross-sectional surveys, each including morethan 3500 children, have been carried out since 1973. Since1978, five follow-up surveys have been conducted among youngadults who participated in previous cross-sectional surveysas children. Participation rates ranged from approximately 80percent for school-age children to approximately 60 percentfor the adult cohort. To date, data have been collected on approximately14,000 people.
For the autopsy studies, a local information system was establishedin 1978 to obtain the family's or coroner's consent to conductan autopsy after the death of a young person. For practicaland logistic reasons, an autopsy was conducted on any residentof Washington Parish in Bogalusa, Louisiana, or adjacent parisheswho died between the ages of 2 and 39 years. Not all the youngpeople who died in this area had been eligible for the BogalusaHeart Study's survey of cardiovascular risk factors, which wasrestricted to ward 4 of Washington Parish. Most deaths weredue to accidents or homicide; only about 10 percent were dueto renal, neoplastic, or infectious diseases or suicide. Autopsieswere conducted in local funeral homes or in hospitals in adjacentcommunities, and selected tissues (including the heart and coronaryarteries, aorta, and kidneys) were brought to the Departmentof Pathology at Louisiana State University Medical Center inNew Orleans for study.
As of January 1996, specimens had been collected at autopsyfrom 86 white males, 52 black males, 36 white females, and 30black females, representing more than 60 percent of all knowneligible deaths. The mean (±SD) age at death ranged from20.4±6.6 years among white females to 21.8±6.8years among black males. Of the 204 persons examined at autopsy,93 had previously been surveyed as part of the Bogalusa HeartStudy and therefore had provided data on antemortem risk factors.Among these 93 persons, the mean age at death was 19.6±5.7years for the 41 white males, 20.4±6.2 years for the19 white females, 21.7±5.2 years for the 23 black males,and 22.4±6.0 years for the 10 black females.
Characterization of Cardiovascular Risk Factors
Essentially the same protocols were used in all surveys. Themethods used to measure each risk factor have been describedin detail previously.19 Height was measured to the nearest 0.1cm and weight to the nearest 0.1 kg. Body-mass index (the weightin kilograms divided by the square of the height in meters)was used as a measure of obesity.
Blood pressure was measured in the right arm, with the subjectin a relaxed, sitting position. The average of six measurements(three taken by each of two examiners) with a mercury sphygmomanometerwas used in all analyses. The fourth Korotkoff phase was consideredthe diastolic blood pressure. Cigarette-smoking status, whichwas assessed by a questionnaire beginning at the age of eightand continuing through adulthood, was measured in terms of thenumber of cigarettes smoked per week.20 Serum total cholesterol,triglycerides, and high-density lipoprotein (HDL) and low-densitylipoprotein (LDL) cholesterol were measured by standardizedprocedures,21 which met the performance requirements of thelipid-standardization program of the Centers for Disease Controland Prevention.
Evaluation of Atherosclerotic Lesions
At autopsy, the aorta and coronary arteries were opened longitudinallyand stained with Sudan IV to localize lipid deposition. Theextent of the intimal surface that was covered with fatty streaksand raised fibrous plaques in the vessels was graded visuallyaccording to procedures developed in the International AtherosclerosisProject22; these procedures are currently used by the Departmentof Pathology at Louisiana State University Medical Center. Thepathologists grading the lesions were unaware of the subjects'risk-factor data. Briefly, the grader first estimated the percentageof the total intimal surface area involved with any atheroscleroticlesion and then estimated the percentage distribution of fattystreaks, fibrous plaques, complicated lesions (those with evidenceof hemorrhage, ulceration, necrosis, or thrombosis, with orwithout calcification), and calcified lesions within this lesion-coveredarea. The recorded percentages of individual types of lesionswithin the lesion-covered area were converted to percentagesof the total intimal surface area by multiplying each estimateby the fraction of intimal surface area covered with atheroscleroticlesions.
Three pathologists evaluated the vessels independently; theextent of atherosclerosis was expressed as the mean of the threevalues assigned by these pathologists for the percentage ofthe intimal surface covered by lesions. The prevalence of atheroscleroticlesions was defined as the percentage of persons studied whohad at least minimal sudanophilic intimal deposits.
Statistical Analysis
We used z scores (standardized values) specific for the studyperiod, race, sex, and age to eliminate the effects of age,race, sex, and potential variations in laboratory measurementson the antemortem risk-factor variables. For the 65 personswhose risk-factor status was assessed more than once, we usedthe average of the adjusted levels. Risk factors were definedas values above the 75th percentile (specific for study period,race, age, and sex) for the group as a whole. Antemortem valuesfor very-low-density lipoprotein cholesterol and triglyceridevalues in nonfasting subjects were not included in the analyses.
Spearman correlation analysis was used to examine the associationbetween the extent of fatty-streak or fibrous-plaque lesionsin the aorta and coronary arteries and age at death and thez scores of individual risk-factor variables. A multivariatetechnique, referred to as canonical correlation analysis, wasthen used to examine the association between the two sets ofvariables — that is, the antemortem risk-factor variablesand the extent of fatty-streak and fibrous-plaque lesions inthe aorta and coronary arteries. The prevalence of atherosclerosisin various age groups was evaluated with a chi-square test.The influence of cigarette smoking on the extent of atherosclerosisand the effect of multiple risk factors on the extent of atherosclerosiswere evaluated with analysis of covariance after the extentof lesions was adjusted for race, sex, and age at death; subjectswith no risk factors were compared with those with one, two,and three or four risk factors. All statistical tests were two-sided.SAS software was used for all analyses.23
Results
Prevalence, Extent, and Interrelations of Lesions
Essentially all persons in the age groups we studied had fattystreaks in the aorta. In contrast, the prevalence of fatty streaksin the coronary arteries increased with age from approximately50 percent at 2 to 15 years of age to 85 percent at 21 to 39years (P=0.01). The prevalence of raised fibrous-plaque lesionsin the aorta and coronary arteries is shown in Figure 1. Inthe aorta, there was a trend toward increasing prevalence withage (P=0.001), especially after the age of 15 years; prevalenceincreased to 60 percent by the age of 26 to 39 years. In thecoronary vessels, this age-related trend was even more consistent(P=0.001), with the prevalence increasing from 8 percent at2 to 15 years to 69 percent at 26 to 39 years.
Figure 1. The Prevalence of Fibrous-Plaque Lesions in the Aorta and Coronary Arteries in 204 Children and Young Adults, According to Age.
There is a consistent trend toward a greater prevalence of coronary-artery lesions with increasing age (P=0.001).
For each type of lesion, there was a trend toward involvementof an increasing percentage of the intimal surface with increasingage. In the aorta, the mean (±SD) percentage of the surfaceinvolved with fatty streaks increased from 13.8±15.5percent at 2 to 15 years of age to 28.8±15.3 percentat 26 to 39 years (P<0.001), and the percentage involvedwith fibrous plaques increased from 0.2±0.5 percent to4.0±7.4 percent, respectively (P<0.001). In the coronaryarteries, the percentage of the surface involved with fattystreaks increased from 0.5±0.7 percent to 7.1±8.2percent (P<0.001), and the percentage involved with fibrousplaques increased from 0.2±0.9 percent to 6.9±11.4percent (P<0.001).
With respect to the interrelation of types of lesions in theaorta and coronary arteries, the correlation of the extent offatty streaks and fibrous plaques in the aorta with the extentof lesions of the same type in the coronary arteries was onlymoderate (r=0.36 to 0.37, P=0.001). Furthermore, the correlationbetween the extent of fatty streaks and that of fibrous plaqueswas much greater in the coronary arteries (r=0.60, P<0.001)than in the aorta (r= 0.23, P=0.03).
Relation of Lesions to Specific Risk Factors
Correlations between the extent of lesions and specific antemortemrisk factors are shown in Table 1. The extent of atheroscleroticlesions correlated positively and significantly with body-massindex, systolic blood pressure (except in the case of fibrousplaques in the aorta), diastolic blood pressure (this was trueonly for fibrous plaques in the coronary arteries), serum totalcholesterol concentrations (except for fibrous plaques in theaorta and coronary artery), serum LDL cholesterol concentrations(except for fibrous plaques in the aorta), and serum triglycerideconcentrations (except for fatty streaks in the aorta). Furthermore,canonical correlation analysis showed that the extent of fatty-streakand fibrous-plaque lesions in the aorta and coronary vesselsas a group were associated moderately strongly with body-massindex (r=0.48), systolic blood pressure (r=0.55), serum triglycerideconcentrations (r= 0.50), and LDL cholesterol concentrations(r=0.43) and associated weakly with diastolic blood pressure(r=0.22) and HDL cholesterol concentrations (r= –0.16).On the other hand, antemortem risk-factor variables as a groupwere most strongly associated with the extent of fatty streaksin the coronary arteries (r=0.55), followed by the extent offibrous plaques in the coronary arteries (r=0.52), fibrous plaquesin the aorta (r=0.40), and fatty streaks in the aorta (r=0.38).Overall, the highest canonical correlation between antemortemrisk-factor variables and the extent of lesions in the aortaand coronary arteries was 0.70 (P<0.001).
Table 1. Correlation between the Extent of Lesions in the Aorta and Coronary Arteries and Antemortem Risk-Factor Variables.
The influence of cigarette smoking on the prevalence and extentof aortic and coronary-artery lesions is shown in Figure 2.The prevalence of lesions in these vessels was similar in the15 smokers and the 34 nonsmokers (for the remaining subjects,smoking status was unknown). The mean (±SE) percentageof the intimal surface involved with fibrous-plaque lesionsin the aorta was higher in smokers than in nonsmokers (1.22±0.62percent vs. 0.12±0.07 percent, P=0.02), as was the percentageinvolved in fatty-streak lesions in the coronary vessels (8.27±3.43percent vs. 2.89±0.83 percent, P=0.04).
Figure 2. The Influence of Cigarette Smoking on the Prevalence (Top Panels) and Extent (Bottom Panels) of Atherosclerosis in the Aorta and Coronary Arteries in Children and Young Adults.
There were 34 nonsmokers and 15 smokers among the 93 subjects; for the remaining subjects, smoking status was unknown. Even though the lifetime amount of smoking may be relatively low at young ages, its adverse effects are obvious.
Relation of Lesions to Multiple Risk Factors
The mean percentage of the intimal surface covered by lesionsin patients with different numbers of risk factors (0, 1, 2,and 3 or 4) is shown in Figure 3. The risk factors we evaluatedincluded body-mass index, systolic blood pressure, serum triglycerideconcentration, and serum LDL cholesterol concentration. In subjectswith 0, 1, 2, and 3 or 4 risk factors, 19.1 percent, 30.3 percent,37.9 percent, and 35.0 percent, respectively, of the intimalsurface area was involved with fatty streaks in the aorta (Pfor trend=0.01). In the coronary arteries, 1.3 percent, 2.5percent, 7.9 percent, and 11.0 percent, respectively, of theintimal surface was involved with fatty streaks (P for trend=0.01),and 0.6 percent, 0.7 percent, 2.4 percent, and 7.2 percent wasinvolved with collagenous fibrous plaques (P for trend=0.003).The extent of fatty-streak lesions in the coronary arterieswas 8.5 times as great in persons with three or four risk factorsas in those with none (P=0.03), and the extent of fibrous-plaquelesions in the coronary arteries was 12 times as great (P=0.006).
Figure 3. The Effect of Multiple Risk Factors on the Extent of Atherosclerosis in the Aorta and Coronary Arteries in Children and Young Adults.
Values shown are the percentages of the intimal surface covered with lesions in subjects with 0, 1, 2, and 3 or 4 risk factors. Risk factors were elevated values for body-mass index, systolic blood pressure, and serum triglyceride and LDL cholesterol concentrations, defined as values above the 75th percentile for the study group (specific for study period, race, sex, and age). There were 52 subjects with no risk factors, 20 with one, 14 with two, and 7 with three or four. The P value is based on the analysis of trend. A marked increase in the percentage of the intimal surface covered by fibrous plaques is evident in the coronary vessels of subjects with multiple risk factors.
Discussion
Observations from autopsy studies by the Bogalusa Heart Studyand the multicenter Pathobiological Determinants of Atherosclerosisin Youth study clearly documented a strong relation betweencoronary atherosclerosis and cardiovascular risk factors inyoung people.12,13,14,15,16,17 Our observation that specificantemortem risk factors such as elevations in body-mass index,systolic blood pressure, serum LDL cholesterol concentration,and serum triglyceride concentration and cigarette smoking aresignificantly related to the extent of atherosclerotic lesionsin young people is in agreement with the findings in those studies.Furthermore, the prevalence and extent of lesions in the coronaryarteries, especially fibrous-plaque lesions that encroach onthe lumen, increased with age in the young people we studied.Previous studies of the natural history of atherosclerosis indicatedthat in populations with high rates of premature coronary arterydisease, advanced lesions begin to appear with greater frequencyduring childhood and young adulthood.24 Although there has beensome question about the clinical significance of fatty streaksin the aorta, which some suggest are evanescent, their presencein association with fibrous plaques in coronary vessels is consideredto indicate that atherosclerosis is progressive and severe.25In the current study, the correlation between the extent offatty streaks and that of fibrous plaques was much greater inthe coronary arteries than in the aorta. Also, the proportionof collagenous fibrous plaques in relation to fatty streakswas greater in the coronary vessels than in the aorta.
We found that the extent of atherosclerotic lesions in the coronaryvessels increased markedly in young people with multiple riskfactors. This finding supports the concept that multiple riskfactors have a synergistic effect on morbidity and mortalityfrom coronary heart disease in middle age and later, as hasbeen demonstrated by epidemiologic studies such as the FraminghamStudy.26 We could not examine the effect of multiple risk factorson the extent of atherosclerosis separately according to raceand sex because of the small numbers of persons in each groupwithin our sample.
The multiple risk factors we evaluated included high valuesfor body-mass index, systolic blood pressure, and LDL cholesteroland triglycerides in serum. Cardiovascular risk factors suchas dyslipidemia, hypertension, hyperinsulinemia or insulin resistance,and obesity often coexist in both children and young adults.9,10Since the clustering of these conditions — termed syndromeX,27 the deadly quartet,28 or insulin-resistance syndrome29— is seen so frequently, a common pathophysiologic mechanisminvolving insulin resistance has been suggested. Although wedid not measure plasma insulin and glucose concentrations asindicators of carbohydrate–lipid metabolism, it is reasonableto suggest that these variables may be part of the cluster ofrisk factors in the study population, as we have shown previously.9,10,30In this regard, the effects of elevated glycosylated hemoglobinconcentrations and of obesity on atherosclerosis are evidentthroughout the group of 15-to-34-year-old subjects in the PathobiologicalDeterminants of Atherosclerosis in Youth study.16
Our observation that the extent of fatty-streak lesions in thecoronary vessels of children and young adults was higher incigarette smokers than in nonsmokers is in agreement with thefindings of the Pathobiological Determinants of Atherosclerosisin Youth study.14,17 Therefore, it is to be expected that cigarettesmoking by young people who have multiple other risk factorswill adversely influence the extent of coronary atherosclerosis.
The effects of multiple risk factors on coronary atherosclerosisgive further justification for the evaluation of cardiovascularrisk in young people and provide a rationale for both preventionand intervention. It may be important to focus on multiple cardiovascularrisk factors early in life, rather than on a specific risk factor,such as hypercholesterolemia. Interventions related to modifiablerisk factors, such as the prevention of smoking, weight control,and encouragement of physical exercise and a prudent diet, ifundertaken early in life, may retard the development of atherosclerosis.
Supported by grants from the National Heart, Lung, and BloodInstitute (HL-38844) and the National Institute of Child Healthand Human Development (HD-32194).
We are indebted to the many people who collaborated with theBogalusa Heart Study for their cooperation, to Bettye Seal forher work as community coordinator, and to the children and youngadults of Bogalusa, Louisiana, without whom this study wouldnot have been possible.
Source Information
From the Tulane Center for Cardiovascular Health, Tulane School of Public Health and Tropical Medicine (G.S.B., S.R.S., W.B., W.A.W.); and the Department of Pathology, Louisiana State University Medical Center (W.P.N., R.E.T.) — both in New Orleans.
Address reprint requests to Dr. Berenson at the Tulane Center for Cardiovascular Health, Tulane School of Public Health and Tropical Medicine, 1501 Canal St., 14th Fl., New Orleans, LA 70112-2824.
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Psychological Factors and Coronary Artery Disease
Pickering T., Davidson K., Chaplin W., Soteriades E. S., Olson J. C., Edmundowicz D., Orchard T. J., Markovitz J. H., Iribarren C., Bild D. E., O'Malley P. G., Taylor A. J.
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