Education, Race, and High-Density Lipoprotein Cholesterol among US Adults

HICMM

David S. Freedman, PhD, David S. Strogatz, PhD, David F. Williamson, PhD, and Ronald E. Aubert, PhD

Introdudtion Rates of coronary heart disease (CHD) in the United States are no higher among Black men than among their White counterparts'-4 despite the higher prevalence of hypertension among Blacks.5 These paradoxical findings may be due to differences in levels of high-density lipoprotein cholesterol (HDL-C): mean levels are about 20% (7 to 11 mg/dL) higher among Black men than among White men but are more similar between Black and White women.46-9 Low levels of HDL-C have been shown, in several studies of White populations,10 to increase the risk for CHD and are associated with more severe coronary artery disease among Black men.' 112 Levels of HDL-C are related positively to alcohol consumption and physical activity and inversely to obesity and cigarette smoking, but most information has been obtained from studies of White populations.13,14 Although HDL-C levels among Blacks are also related to alcohol consumption (positively) and Quetelet index (overweight) (negatively),4'7'9 associations with socioeconomic status appear to differ between races. Whereas a positive association between HDL-C and various indicators of socioeconomic status is typically observed among Whites,4'7'15 an inverse association has been reported among Blacks.4'7'9"16 The association between socioeconomic status and levels of HDL-C may, in part, be mediated by behavioral characteristics.'5 In agreement with this hypothesis, we have found that the Black/White difference in the association between educational achievement and levels of HDL-C among 31- to 45-year-old male veterans could, in part, be attributed to relative weight, cigarette smoking, and al-

cohol consumption.9 The objectives of the current study are to (1) assess these findings in an independent sample, (2) extend these observations to women and to older men, and (3) incorporate information on additional characteristics such as physical activity and body fat distribution. Data are from a representative sample of US adults who participated in the Second National Health and Nutrition Examination Survey

(NHANES II).

Materials and Methods Study Population Information concerning various risk factors for CHD and the sample of adults with HDL-C determinations in NHANES II, a multistage survey, has been described.7 Data were collected between 1976 and 1980 by the National Center for Health Statistics through standardized interviews and physical examinations. Of the 20- to 74-year-olds comprising the original sample of 17 058 persons, 88% (n = 15 080) were interviewed and 68% (n = 11 637) were interviewed and examined. An investigation of possible selection biases'7 indicated that nonresponse at the interview stage did not vary according to the sex or race of the head of household, David S. Freedman, David F. Williamson, and Ronald E. Aubert are with the Centers for Disease Control's Center for Chronic Disease Prevention and Health Promotion in Atlanta, GA. David S. Strogatz is with the New York State Department of Health and the State University of New York at Albany. Requests for reprints should be sent to David S. Freedman, PhD, Centers for Disease Control, K-26, 1600 Clifton Road, Atlanta, GA 30333. This paper was submitted to the Journal January 29, 1991, and accepted with revisions October 18, 1991.

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but participation was lower for urban subjects than for those in more rural areas (86% vs 93%). Although persons with selfperceived health problems were more likely to be examined, the assessed health status of participants was comparable to that of subjects in the National Health Interview Survey, which had a 4% nonresponse rate.17 Race, education, and income did not differ between examined and nonexamined persons in NHANES II. Of the 11 637 adults examined in NHANES II, HDL-C determinations were performed for 83% (n = 9625), yielding an overall response rate of 56.4% of the original sample. The proportion of examined persons with HDL-C levels varied by race (Whites, 83%; Blacks, 78%) but not by sex, educational achievement, income, age, alcohol consumption, cigarette smoking, or several other characteristics.7

Risk-Factor Information We used educational achievement, determined by the highest attended grade, as an indicator of socioeconomic status. As compared with indices such as income and occupation, education remains fairly constant throughout adulthood, is available for nonemployed and retired persons, and is unaffected by illness. HDL-C levels were related similarly to income and educational achievement in NHANES II.7 Race was determined by interviewers' observation or direct questioning. About 4% (n = 339) of White adults indicated they were of Hispanic descent, with Mexicans and Mexican Americans representing the largest subgroup (n = 196). Although most analyses did not distinguish between Hispanic Whites and nonHispanic Whites, the former were excluded from certain sensitivity analyses. Quetelet index (kg/m2) and skinfold thickness measurements were used as measures of overweight and obesity, respectively. The ratio of subscapular to triceps skinfold thickness, an index of central (truncal) fat, was used to describe body fat distribution. Interviewees were asked two questions conceming physical activity: (1) were they getting "much," "moderate," or "little or no" recreational exercise? and (2) aside from recreation, were they usually "very active," "moderately active," or "quite inactive"? These responses were dichotomized as very active/much exercise versus other responses in some analyses. Self-reported information was used for several prevalent diseases and medications. Diabetes mellitus was defined by 1000 American Journal of Public Health

positive responses to two questions: "Do you have diabetes or sugar diabetes?" and "Did a doctor tell you this?" Oral contraceptive use was ascertained through the question, "Have you taken birth control pills in the last 6 months and are you taking them now?" Women who reported taking hormones within the last week were considered to be using estrogens. Use of steroids, cholesterol-lowering drugs, and hydantoins was also determined from questions concerning use within the previous week. Subjects were asked about their usual consumption of beer, wine, and liquor over the previous 3 months, and the number of weekly dfinks (summed over the three alcohol categories) was calculated. Cigarette smoking was also assessed, and the reported number of cigarettes smoked daily was used in the analyses. Data on intake of total calories and saturated fats were collected through 24-hour dietary recalls, and subjects were asked if the foods were representative of their usual diet.

NHANES II, with variances calculated using SESUDAAN.20 After levels of various characteristics between Blacks and Whites were contrasted, associations amongvarious characteristics were examined using linear regression (SURREGR)21 and stratification. A Race [0 (Whites), 1 (Blacks)] x Education interaction term was incorporated into several analyses as an independent variable. Because education and age were inversely associated, analyses were age adjusted with age treated as a six-level categorical variable: 20-24, 25-34, 35-44, 45-54, 5564, and 65-74 years. Several analyses were performed to determine if the observed interaction between race and education could be "explained" by other characteristics. The magnitude of the Race x Education term in regression analyses was compared before and after inclusion of (1) all covariates and (2) each covariate separately. All P values and confidence intervals are twosided.

Senun L@id Detemninations About 50% of the exaninees were

Resufds

fasting at the time of examination, and in a sample of adults with an oral glucose tolerance test, mean levels of total cholesterol differed by 3 mg/dL or less between fasting and nonfasting persons.18 Serum was frozen within 1 hour of collection, and specimens were shipped (at approximately 2-week intervals) for lipid analyses to the Lipid Research Clinics Laboratory at George Washington University. Analyses were performed according to standardized protocols,19 with HDL-C assayed using a heparin and manganese chloride precipitation method.

Mean levels of age and total cholesterol varied only slightly across race-sex groups, but HDL-C levels were higher among Blacks than among Whites (Table 1), with differences of 7 mg/dLamong men and 3 mg/dL among women. Whites were more likely to have had some education beyond high school (e.g., 41% of White men vs 26% of Black men) and an income greater than $20 000 per year. Race-related differences were also observed for other characteristics. Compared with White women, Black women were more obese and had a more central distribution of body fat, as estimated by the ratio of subscapular to triceps skinfolds. Among men, Blacks also had a more central fat distribution than did Whites despite having a lower mean Quetelet index. Blacks were also more likely to smoke cigarettes, but Black smokers reported a smaller number of daily cigarettes than did White smokers. Blacks tended to be more physically active and to have lower daily intakes of total calories and saturated fats than did Whites. Differences in the prevalence of diabetes and in the use of oral contraceptives and sex hormones were also observed. The relation of educational achievement to levels of HDL-C is shown in Figure 1. (Because education and age were inversely associated [r = -0.29 to -0.55], mean levels of HDL-C have been age

Statistical Methods Of the 9625 subjects with HDL-C measurements, persons were excluded if data were missing for one or more of the following characteristics: years of education (n = 85), subscapular (n = 88) or triceps (n = 24) skinfolds, weight or height (n = 51), number of daily cigarettes (n= 14), or alcohol consumption (n = 15). These restrictions resulted in a sample size of 9386 adults (8391 White, 995 Black) for most analyses. Persons were excluded from analyses that used data from the 24-hour dietary recalls if the reported foods did not represent their usual diet (n = 3503) or if their caloric intake was less than 500 kcal or 6000 kcal or more (n = 214). All analyses incorporate the weights and complex sampling design of

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Educaton, Race, and Levels of HDL-C

adjusted.) Among White men, mean HDL-C levelsvaried only slightlywith education, but there was a 7 mg/dL decrease over the five education categories among Black men. The relation also differed between Black and White women, with a positive association seen among Whites only. Within each sex, Black/White differences in mean levels of HDL-C were less than 1 mg/dL among persons with at least 16 years of education. Additional analyses treating education as a continuous variable indicated that the Black excess in HDL-C levels decreased by 0.6 mg/dL (women) to 0.7 mg/dL (men) with each additional year of education; the Race x Education interaction term was statistically significant among men (P = .004) and women (P = .02). Cross-sectional associations between levels of HDL-C and other characteristics are shown in Table 2; values represent the predicted change in HDL,C for a specified change in each variable. For example, with each additional year of education, levels of HDL-C were estimated to change by +0.8 mg/dL among White women, by +0.2 mg/dL among White men and Black women, and by -0.5 mg/dL among Black men. Levels of

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HDL-C were inversely associated with obesity and, with the exception of Black men, with the amount of centrally located body fat. As expected, HDL-C levels were positively related to alcohol consumption, but an inverse association with cigarette smokingwas seen among Whites only. Physical activity tended to be positively related to levels of HDL-C. Neither total calories nor saturated fats was associated with levels of HDL-C among men, but weak, positive associations were seen in women. Several of the dichotomous variables were also associated with HDL-C levels, with higher mean levels seen among hydantoin users and women using sex hormones. Although associations with cholesterol-lowering drugs were inconsistent, the mean level of HDL-C was 17 mg/dL lower among the two Black men who reported using these medications than among other Black men. Mean levels of HDL-C were also lower among diabetics (vs nondiabetics) and among the 10 men who reported using steroids (data not shown). Associations between education and various characteristics were then examined, and several could possibly account for the interaction between race and edu-

cation. Among men (Table 3), levels of Quetelet index and subscapular skinfold thickness increased with educational achievement among Blacks but not among Whites. In addition, associations with alcohol consumption, cigarette smoking, dietaxy intake of total calories and saturated fat, and diabetes also differed between Whites and Blacks. Among men with at least 16 years of education, Blacks were more obese, had a higher prevalence of diabetes, and consumed less alcohol than did Whites. Among women (Table 4), education showed a stronger (inverse) association with overweight and obesity among Whites than among Blacks. For example, Blackswho had completed up to 8 years of education were, on average, 2 kg/M2 heavier than their White counterparts, but the difference increased to 3.9 kg/M2 among women with at least 16 years of education. Alcohol intake was positively associated with education among White, but not Black, women. Positive associations with saturated fat intake and use of oral contraceptives and sex hormones were stronger among Blacks than among Whites.

American Journal of Public Health 1001

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s~ ~ ~ . , . - ."'-

sex group. For example, the predicted change in levels of HDL-C with each year of education was reduced from +0.8 to +0.5 mg/dL (White women) and from -0.5 to -0.3 mg/dL (Black men) after controlling for alcohol consumption and subscap-

ular skinfold thickness.

Discussion

01

..... ........ 16 9 -11 Years of Education FIGURE 1-Mean age-adjusted levels of HDL-C by sex, race, and education. Amng men, coreltins between education and levels of HDL-C were r = 0.05 (Whftes) and -0.14 (Blacks). Correlation coefficients among women were r = 0.16 (WhItes) and 0.04 (Bls). Sample sIkes raged from 34 (Black men woih at least 16 years of educaton) to 1707 (WhIte women wh 12 years of education). < 8

Analyses were then performed to determine whether the interaction between race and education was attnbutable to the covariates. Coefficients and predicted differences (Black-White) in HDL-C levels from two regression models are shown in Table 5. Independent variables in model #1 include race, education, race x education, and age; model #2 contains, in addition to these variables, obesity, alcohol

consumption, cigarette smoking, and other characteristics. Adjusting for the additional covariates reduced the coefficient of the race x education interaction term by 19% (from -0.72 [model #1] to -0.58

[model #2]) among men and by 41% (from -0.56 to -0.33) among women. Age-stratified analyses indicated that the covariates were important among both younger and older adults (less than 45 years old and 45 to 74 years old, respectively) in accounting for the Race x Education interaction.

1002 American Journal of Public Health

Most of the variability in levels of HDL-C remained unexplained, however, with the multiple correlation coefficient (R2) reaching a maximum of 0.18. Additional analyses, comparable to those shown in Table 5, were performed to examine the effects of various exclusions and individual variables (data not

shown). After the 339 Hispanic Whites excluded, reductions in the magni-

were

tude of the Race x Education interaction between the two models were similar to those shown in Table 5. As assessed by analyses in which each characteristic was added separately to model #1, subscapular skinfold thickness and alcohol con-

sumption were the most important covariates in accounting for the observed interaction. Furthermore, covariate adjustment reduced the absolute magnitude of the association between levels of HDL,C and education within each race-

Our results indicate that differences between Blacks and Whites in the crosssectional association between educational achievement and levels of HDL-C can, in part, be attributed to behavioral characteristics. Consistent with the results of other investigations,46'9 mean levels of HDL-C were 3 mg/dL (women) to 7 mg/dL (men) higher among Blacks than among Whites. The largest Black/White differences in HDL-C levels were seen among adults with up to 8 years of education, whereas no difference was evident among persons with at least 16 years of education. With each additional year of education, mean HDL-C levels decreased by 0.5 mg/dL among Black men but not among White men (1 = +0.2 mg/dL per year of educational achievement); among women, the association was positive among Whites (1B = +0.8) but very weak among Blacks (13= +0.2). About 20% (men) to 40% (women) of the interactions between race and education could be accounted for by other correlates of HDL-C levels, particularly obesity and alcohol

consumption. Although only 56% of the original sample for NHANES II had an HDL-C determination, there were no differences in (1) interview status according to race or sex of the head of household,17 (2) participation in the examinations by education or income,17 or (3) obtainment of an HDL-C measurement according to levels of education, Quetelet index, alcohol consumption, or smoking status.7 It is possible, however, that associations among race, educational achievement, HDL-C levels, and the explanatory variable may be biased by other factors related to participation. The similarity of many of our findings with those from other studies, however, makes this less likely. With increasing industrialization, the

burden of CHD appears to shift to lower social strata,77 and persons with high socioeconomic status are no longer at the greatest risk. 123-26 It has been suggested27 that these temporal changes occur because persons with high socioeconomic status can more

quickly adopt detrimental

behaviors that influence CHD risk and are

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1004 American Journal of Public Health

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Educaion, Race, and Levels of HDL-C

then able to modify these behaviors more rapidly. Consistent with this hypothesis, the relation of socioeconomic status to levels of total cholesterol, cigarette smoking, and consumption of various foods has changed between the 1950s and 1980s.23 28 Inverse associations between indicators of socioeconomic status and several CHD risk factors have been found,15'23'28-30 and a positive association between educational achievement and levels of HDL-C has been reported in studies of White adults 15,30

In contrast, socioeconomic status was recently found to bepositively related to CHD incidence among urban men in Puerto Rico, possibly due to the relatively recent economic development of this area.31 Even within industrialized societies, however, the relation of socioeconomic status to CHD mayvaiy across ethnic groups.32 A study from one center in the Multiple Risk Factor Intervention Trial, for example, found that socioeconomic status was inversely related to a composite risk-factor score for CHD among White, Asian, and Hispanic men, but not among Black men.33 Furthermore, a recent survey of adults from New York City found an inverse association between educational achievement and several CHD risk factors (smoking, sedentary behavior, obesity, and atherogenic diet) that was stronger among Whites than among Blacks.34 Our findings concerning the inverse association between educational achievement and levels of HDL-C among Black men agree with the results of other investigations. Mean HDL-C levels among Black adults from Framingham, Mass (50% of whom had completed college), were 6 to 7 mg/dL lower than those among Whites.35 Black/White differences in the association between socioeconomic status indicators and levels of HDL-C have also been found in the Multiple Risk Factor Intervention Trial4 and among US Armyveterans.9 With the exception ofeducation, we found that associations between levels of HDL,C and most characteristics did not differ between Blacks and

Whites. Although cigarette smoking was inversely associated with levels ofHDL-C among Whites only, other studies of smokingand HDL-C levels in Blacks have yielded conflicting results, with the observed associations ranging from inverse4 to weakly positive.35

Few studies have examiined characteristics that might mediate the relation of educational achievement to levels of HDL-C. Heiss et al.,'5 however, in an

July 1992, Vol. 82, No. 7

analysis of White adults, found that most of the positive association between education and HtDL-C levels among women could be attributed to obesity, alcohol consumption, smoking, and use of sex hormones. (Associations between education and these characteristics were similar to those seen in the current study.) Furthermore, about 40% of the interaction between race and educational achievement for levels of HDL-C could be attributed to Quetelet index, alcohol consumption, and cigarette smoking among 31- to 45-yearold men.9 Our results, based on a national probability survey, extend these findings to women and older men. The persistence of a large proportion of the interaction even after covariate adjustment could result from (1) unmeasured characteristics that are associated with levels of HDL-C and educational achievement, or (2) misclassification of HDL-C levels and other characteristics. Because of the large dayto-dayvariability in dietaxy intake, our assessed intakes of total calories and saturated fat may be particularly inaccurate. When one considers the differences in job opportunities, income, and physical environment that exist between Blacks and Whites at any specified level of education,36 racial differences in the association between socioeconomic status and measures of health and health-related behaviors37-0 are not surprising. A full explanation of Black/White differences in the association between educational achievement and levels of HDL-C remains to be resolved. Our findings, however, suggest that preventing obesity may be a useful goal for maintaining the relatively high levels of HDL-C seen among Blacks in the United States. []

5. 6.

7.

8.

9.

10.

11.

12.

13.

14.

Acknowledgments The authors acknowledge the support of Tim Byers at the Centers for Disease Control. We also thank Robinson Fuiwood, of the National Heart, Lung, and Blood Institute, and Margaret Carroll, of the National Center for Health Statistics, for their advice and encouragement in analyzing these data.

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mioL 1983;117:507-515. 18. National Center for Health Statistics, National Heart, Lung, and Blood Institute Coilaborative Lipid Group. Trends in serum cholesterol levels among US adults aged 20 to 74 years.IJAMA. 1987;257:937942. 19. Manual of Laboratory Operation.~Lipid Research Clinics Program. Vol 1. Bethesda, Md: National Institutes of Health;

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Fmdnuan et aL 1974. US Dept of Health, Education, and Wefre publication NIH 75-628. 20. Shah BV. SESUDAAN.: Standad E,ros Pf =m for Copaig of Standanld Rates from Sampe Data. Research Triangle Park, NC: Research Triangle Institute; 1981. 21. Shah BV. SURREGR Starud Emor of Regnsion Coeients from Sample Survey Data. ResearchTriangle Park, NC: Research Triangle Institute; 1982. 22. Jenkins CD. Recent evidence supporting psychologic and social risk factors for coronary disea. N Engi J Med 1976;294: 987-994. 23. Marmot MG, Adelstein AM, Robinson N, et al. Changing social-class distnbution of heart disease.BrMedJ. 1978;2:1109-1112. 24. Rose G, Marmot MG. Social class and coronary heart disease. Br Heart J. 1981;45: 13-19. 25. Rosenman RH, Brand RJ, Jenkins CD, et al. Coronary heart disease in the Western Collaborative Group Study: final follow-up experience of 8½ years. JAMA 1975;233:

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findings of the three Chicago epidemiologic studies. Circulton. 1982;66:13081314. 27. Morgenstern H. The chanmig association between social status and coronary heart dise in a rural popuation. Soc Sci MedL

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28. Stamler J. Primary prevention of coronary heart disease: the last 20 years.AmJ CardioL 1981;47:722-735. 29. Jacobsen BK, Thelle DS. Risk factors for coronaly heart disease and level of education: the Tromso Heart Study. Am J EpidemioL 1988;127:923-932. 30. Helmert U, Herman B, Joeckel KH, Greiser E, Madans J. Social class and risk factors for coronary heart disease in the Federal Republic of Germany: results of the baseline survey of the German Cardiovascular Prevention Study (GCP). J Epidemdol Community Healt 1989;43: 37-42. 31. Sorlie PD, Garcia-Palmieri MR. Educational status and coronary heart disease in Puerto Rico: the Puerto Rico Heart Health Program.IntJEpidemioL 1990;19: 59-65. 32. Marmot MG, Kogevinas M, Elston MA. Social/economic status and disease. Ann Rev Puibic Health. 1987;8:111-135. 33. Kraus JF, Borhani NO, Franti CE. Socioeconomic status, ethnicity, and risk of cor-

onaiy heart disease.AmJEpidemioL 1980, 111:407-414. 34. Shea F, Stein AD, Basch CE, et al. Independent assocations of educational attainment and ethnicitywith behavkal risk factors for cardiovascular disease. Am J EpidemioL 1991;134:567-582. 35. Wilson PWF, Savage DD, Castelli WP, et al. HDL-cholesterol in a sample of Black adults: the Framingham Minority Study. Metabolsm 1983;32:328-332. Ab36. US Bureau of the Census. S stract of the United States: 1982-1983. Washigton, DC: US Govt Printmng Office; 1984. 37. Kessler RC, Neighbors HW. A new perspective on the relationships among race, social class, and psychoogical distress. J Heah Soc Behav. 1986;27:107-115. 38. Stogatz DS. Use of medical care for chest pain: differences between Blacks and Whites. Am J Pubfic Healk 199080:.290294. 39. Cooper R. A note on the biologic concept of race and its application in epidemioogic research. Am Heat J. 1984;108:715-723. 40. Caspar ML, Wing S, Strogtz DS. Variation in the magnitude of Black-White differences in stroke mortality by counity occupational structure. J Epidm Community Heath In press.

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