Distributions and Trends of Serum Lipid Levels among United States Children and Adolescents Ages 4–19 Years: Data from the Third National Health and Nutrition Examination Survey

27, 879–890 (1998) PM980376

PREVENTIVE MEDICINE ARTICLE NO.

Distributions and Trends of Serum Lipid Levels among United States Children and Adolescents Ages 4–19 Years: Data from the Third National Health and Nutrition Examination Survey1 Tamy B. Hickman, M.P.H.,* Ronette R. Briefel, Dr.P.H., R.D.,*,2 Margaret D. Carroll, M.S.P.H.,* Basil M. Rifkind, M.D.,† James I. Cleeman, M.D.,† Kurt R. Maurer, Ph.D.,* and Clifford L. Johnson, M.S.P.H.* *National Center for Health Statistics, Centers for Disease Control and Prevention, Hyattsville, Maryland 20782; and †National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, Maryland 20892

Background. Atherosclerosis begins in childhood and progresses into adulthood. The reduction of cardiovascular risk factors, such as elevated serum total cholesterol and low-density lipoprotein cholesterol (LDL-C) levels, in childhood may reduce cardiovascular morbidity and mortality in adulthood. Lipid distributions among children and adolescents were examined using the most recent nationally representative data. Methods. Data from 7,499 examinees in NHANES III (1988–1994) were used to estimate mean and percentile distributions of serum total cholesterol, LDL-C, highdensity lipoprotein cholesterol (HDL-C), and triglycerides in children and adolescents aged 4 to 19 years. The estimates were analyzed by age, sex, and race/ethnic groups. Trends in mean total cholesterol were examined for 12- to 17-year-olds using data from NHES III (1966–1970), NHANES I (1971–1974), and NHANES III (1988–1994). Results. For children and adolescents 4 to 19 years of age, the 95th percentile for serum total cholesterol was 216 mg/dL and the 75th percentile was 181 mg/dL. Mean age-specific total cholesterol levels peaked at 171 mg/dL at 9–11 years of age and fell thereafter. Females had significantly higher mean total cholesterol and LDL-C levels than did males (P , 0.005). Non-Hispanic black children and adolescents had significantly higher mean total cholesterol, LDL-C, and HDL-C levels compared to non-Hispanic white and Mexican American children and adolescents. The mean total cholesterol level among 12- to 17-year-olds decreased

1 This investigation was funded and conducted by the U.S. Federal Government, MS# PM97-0143. 2 To whom correspondence and reprint requests should be addressed at 6525 Belcrest Road, Hyattsville, MD 20782. Fax: (301) 436-5431. E-mail: [email protected].

by 7 mg/dL from 1966–1970 to 1988–1994 and is consistent with, but less than, observed trends in adults. Black females have experienced the smallest decline between surveys. Conclusions. The findings provide a picture of the lipid distribution among U.S. children and adolescents and indicate that, like adults, adolescents have experienced a fall in total cholesterol levels. Total cholesterol levels in U.S. adolescents declined from the late 1960s to the early 1990s by an average of 7 mg/dL. This information is useful for planning programs targeting the prevention of cardiovascular disease beginning with the development of heathy lifestyles in childhood. q1998 American Health Foundation and Academic Press

Key Words: lipids; cholesterol; low-density lipoproteins (LDL); high-density lipoproteins (HDL); triglycerides; National Health and Nutrition Examination Survey (NHANES); children; adolescents. INTRODUCTION

Several lines of evidence relate cholesterol levels in children and adolescents to atherosclerosis in adults. Atherosclerotic changes begin in childhood and progress into adulthood. Aortic fatty streaks can be found in most children by 10 years of age, and fibrous plaques are often evident in adolescence [1,2]. These vascular changes have been shown to be directly associated with modestly elevated serum cholesterol levels as well as smoking. In the Bogalusa Heart Study of cardiovascular risk factors in children, aortic fatty streaks were found to be strongly correlated to antemortem levels of total cholesterol (TC) and low-density lipoprotein cholesterol (LDL-C) [1,3]. The Pathobiological Determinants of Atherosclerosis in Youth (PDAY) study in 15to 34-year-olds found that LDL-C plus very low-density lipoprotein cholesterol (VLDL-C) levels and smoking were positively correlated with the extent of aortic and

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0091-7435/98 $25.00 Copyright q 1998 by American Health Foundation and Academic Press All rights of reproduction in any form reserved.

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coronary fatty streaks and raised lesions; high-density lipoprotein cholesterol (HDL-C) was negatively associated with these vascular changes [2]. In addition, coronary heart disease occurs more frequently in adult members of families in which the children’s levels of cholesterol are elevated [4]. In 1991, the National Cholesterol Education Program (NCEP) published the “Report of the Expert Panel on Blood Cholesterol Levels in Children and Adolescents” to address the importance of lowering serum cholesterol levels among U.S. children and adolescents [4]. The report underscores the role that elevated cholesterol levels in childhood play in the development of atherosclerosis in adulthood. It recommends two approaches to lowering blood cholesterol levels in children and adolescents. The first is a population-based approach which seeks to lower average cholesterol levels by urging that children from about the age of 2 or 3 years begin to participate in a low saturated fat, low cholesterol eating pattern with the rest of the family. The second is an individualized approach which involves selective screening of children from high-risk families, i.e., those with a history of premature cardiovascular disease or parental hypercholesterolemia, and treatment of elevated cholesterol levels in such children, relying primarily on dietary therapy and physical activity. This paper provides nationally representative data pertinent primarily to the NCEP population approach. Since complete information on family history of heart disease or hypercholesterolemia was not available, the data could not be used to produce meaningful estimates of the proportion of children and adolescents with high total cholesterol and LDL-C levels. The Centers for Disease Control and Prevention’s National Center for Health Statistics (NCHS) conducts the periodic National Health and Nutrition Examination Surveys (NHANES). Data from these surveys are used to produce national estimates of the nation’s health and nutritional status. The most recent survey, the third National Health and Nutrition Examination Survey (NHANES III), was completed in 1994 and provides mean and percentile distributions of serum lipid levels in children and adolescents. NHANES III data for lipid levels in adults were published earlier and indicate a downward trend in age-adjusted mean serum total cholesterol, from 220 mg/dL in 1960–1962 to 203 mg/ dL in 1988–1994 [5,6]. This is thought to contribute to the decreased death rate from coronary heart disease (CHD) which has occurred over the same time period [6]. The purpose of this current investigation is to present a comprehensive picture of the lipid status among U.S. children and adolescents 4 to 19 years of age. Furthermore, mean serum total cholesterol levels in adolescents 12 to 17 years of age are examined between 1966– 1970, 1971–1974, and 1988–1994 to determine trends

and to see if the trends in adolescents are similar to those exhibited in adults. METHODS

Sample Populations Data from three national examination surveys are used: the National Health Examination Survey III (NHES III; 1966–1970), NHANES I (1971–1974), and NHANES III (1988–1994). These surveys were selected because each provides national data on serum lipid levels in adolescents. NHES III was different from other surveys used in this investigation because it focused on the growth and development of adolescents aged 12 to 17 years only. In 1971, the survey was enhanced with the addition of a nutrition component. The first of these surveys, NHANES I, was designed to provide national estimates of the health and nutritional status of the civilian, noninstitutionalized U.S. population aged 1 to 74 years. NHANES III was designed to expand the age range and collect information on the U.S. population aged 2 months and older. Specific subpopulations, including children aged 2 months to 5 years, persons 60 years of age or older, Mexican Americans, and blacks, were oversampled in NHANES III to increase the reliability of estimates for these groups. Detailed descriptions of the plan and operation of each of the surveys have been described elsewhere [7–9]. Data Collection and Definitions Each survey employed similar methods for collection of data through household interviews and direct standardized physical examinations conducted in mobile examination centers. During the household interview, a questionnaire was administered to a proxy respondent, such as the child’s parent or guardian, for children aged 2 months to 16 years. For individuals aged 17 years or older, age was based on self-reported data. In each of the surveys, age was defined as the age at the child’s last birthday. For the purposes of this investigation, children are defined as individuals 4 to 11 years of age, and adolescents are defined as individuals 12 to 19 years of age. In NHES III and NHANES I, observed race was categorized as white, black, or other. Race and ethnic categories were based on self-reported data in NHANES III, but these variables were combined to create race/ethnic groups which included non-Hispanic white, non-Hispanic black, Mexican American, or other. The total population figures include data for race/ethnic groups not shown separately. The examination component of the survey consisted of medical tests and examinations, the collection of blood and urine specimens, and additional personal interviews. Lipid and lipoprotein measurements were obtained from venous blood serum samples collected at

SERUM LIPIDS AMONG U.S. CHILDREN AND ADOLESCENTS

the mobile examination center. In NHANES III, total cholesterol (N 5 7,499) and HDL-C (N 5 7,458) were measured in individuals 4 years of age or older regardless of their fasting status. A nationally representative probability sample of examinees aged 12 years or older was asked to fast and to be examined in the morning [9]. In these examinees, fasting triglyceride (TG) levels (N 5 1,099) were used to calculate LDL-C levels (N 5 1,095) using the equation developed by Friedewald et al. [10]. The lipid measurements were based on a single blood determination. Total cholesterol was the only serum lipid measurement collected in adolescents for NHES III (N 5 6,710) and NHANES I (N 5 2,126). As recommended by the second NCEP Adult Treatment Panel [11], only examinees who fasted a minimum of 9 h before the morning examination were included in the calculation of LDL-C and reported TG. Blood serum samples were frozen and shipped on dry ice to the designated laboratory conducting lipid analyses for the survey. Total cholesterol measurements for 12- to 17-year-olds in NHES III and NHANES I were made at the CDC Lipid Standardization Laboratory. The Johns Hopkins University Lipid Research Clinic (LRC) Laboratory measured cholesterol in NHANES III. All serum cholesterol measurements were standardized to the Abell–Kendall method, and a more detailed explanation of the laboratory methods has been described elsewhere [5,9,12,13]. This standardization and quality control of cholesterol measurements over time is crucial to reporting and interpreting temporal changes in serum cholesterol levels. The NCEP has recommended cut points for acceptable, borderline, and high total cholesterol and LDL-C levels among children and adolescents from high-risk families, i.e., those with premature cardiovascular disease or parental hypercholesterolemia [4]. The cut points are based on the 75th and 95th percentile estimates using LRC Prevalence Study data. Whether these same values are appropriate for children and adolescents who do not have a family history or parental hypercholesteremia is uncertain. Since the necessary information on family history or parental hypercholesterolemia was not available for NHANES III children and adolescents, the data could not be used to produce meaningful estimates of children who are “high-risk” and who therefore might require treatment. Statistical Methods All means, percentile estimates, and standard errors were generated using SUDAAN [14], a statistical program which takes into account the sampling weights and the complex sample design of the surveys. The sample weights are adjusted for nonresponse, based on the probabilities of selection, and poststratified to the

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U.S. Bureau of Census estimates of the total U.S. population. There were 10,123 children and adolescents ages 4–19 years selected for the NHANES III sample; 9,187 (91%) were interviewed and 8,636 (85%) were interviewed and examined. Of these, 7,499 had known serum total cholesterol determinations and 7,458 had known HDL-C determinations (86% of interviewed and examined sample). The sample weights are adjusted for nonresponse [15] and the estimated means and percentiles presented in this report are based on weighted data. Furthermore, analysis of characteristics of sample persons with known serum lipid values versus those with missing values with respect to selected health characteristics indicated no substantial biases. Response rates for NHES III (ages 12–17 years) and NHANES I (ages 4–17 years) were 90 and 84%, respectively. Again, estimates of mean serum total cholesterol for these surveys are based on weighted data which compenstates for nonresponse. Between 2 and 3% of youths examined in NHES III (2.6%) and 9% of children and youths examined in NHANES I had missing serum total cholesterol determinations [16,17]. The likelihood of bias due to missing data in NHES III is small due to the low percentage with missing data. Although a larger percentage of children and youths examined in NHANES I had missing serum total cholesterol data, the percentage with missing data for this survey is still low. In both surveys missing values were imputed by assigning a value of a randomly selected individual of the same gender, age, and race. Analyses focusing on current estimates use NHANES III data. The trend analysis is restricted to serum total cholesterol data in adolescents aged 12 to 17 years in NHES III, NHANES I, and NHANES III. Race, rather than race/ethnicity, was used for trend analysis because the race/ethnicity variable was not collected in NHES III and NHANES I. Crude estimates are presented because no substantial differences were found between crude and age-adjusted estimates. For the NHANES III estimates, race/ ethnic groups other than non-Hispanic white, non-Hispanic black, and Mexican American are not reported separately due to small sample sizes. Estimates of the mean, standard error, and selected percentiles for serum TC, HDL-C, LDL-C, and TG are presented in Tables 1–4. Some of these estimates include a notation that indicates that the estimate does not meet the guidelines for reliability and precision established by NCHS [9]. These guidelines give minimum sample sizes for reliability and precision which depend on the percentile being estimated and the design effect (i.e., a measure of the impact of the complex sample upon the variance of a statistic).

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HICKMAN ET AL. RESULTS

Current National Estimates Serum total cholesterol means and selected percentiles by age, sex, and race/ethnicity are shown in Table 1. For children and adolescents 4 to 19 years of age, the 95th percentile for total cholesterol was 216 mg/dL and the 75th percentile was 181 mg/dL. Children aged 9 to 11 years had a mean total cholesterol level of 171 mg/dL which was significantly higher than the means for other age groups (P , 0.005). Overall, females ages 4 to 19 years had a higher mean total cholesterol (167 mg/dL) than males (163 mg/dL) (P , 0.0005). Furthermore, there was a significant mean decrease in TC in males from ages 9 to 11 years to 12 to 15 years (P , 0.0001). For females ages 16–19 years, the 95th percentile for total cholesterol (237 mg/dL) was the highest estimate for all age groups and both sexes. For children and adolescents 4 to 19 years of age, non-Hispanic blacks had a significantly higher mean total cholesterol level (170 mg/dL) than non-Hispanic whites (164 mg/ dL) (P , 0.0001) or Mexican Americans (164 mg/dL) (P , 0.0001). As shown in Table 2, mean HDL-C levels were relatively constant among age groups for children aged 4 to 19 years except that in boys mean HDL-C levels fell 6 mg/dL from ages 9 to 11 years to 12 to 15 years (P , 0.0001). In addition, the 5th percentile for these children and adolescents was an HDL-C of 32 mg/dL. Although the overall mean HDL-C was similar for both sexes, the mean was higher in males among the younger children, whereas the mean was higher in female adolescents. Table 2 shows that non-Hispanic black children had the highest mean HDL-C. Mean LDL-C and percentile distributions are presented in Table 3. Adolescents 16 to 19 years of age had significantly higher mean LDL-C levels than 12- to 15year-olds (P , 0.05). Female adolescents had a higher mean level (99 mg/dL) than males (91 mg/dL) (P , 0.01), and the mean LDL-C increased with age in both sexes. Non-Hispanic black adolescents ages 12 to 15 years had a higher mean LDL-C than non-Hispanic white (P , 0.001) or Mexican American adolescents (P , 0.01). As shown in Table 4, the mean triglycerides level for adolescents aged 12 to 19 years was 93 mg/dL. There was no difference in the mean among sex and age groups. Similar to the findings in Tables 1 through 3, a significant race/ethnicity difference was found in mean triglycerides. The mean was significantly lower among the non-Hispanic black adolescents than non-Hispanic white (P , 0.0001) and Mexican American (P , 0.0001) adolescents.

Trends in Total Cholesterol Data from NHES III (1966–1970), NHANES I (1971– 1974), and NHANES III (1988–1994) indicate that there was a downward trend in mean total cholesterol among race-sex groups aged 12 to 17 years (Table 5). The mean serum cholesterol level decreased by 7 mg/ dL (P , 0.0001) from 1966–1970 to 1988–1994. For both sexes, the mean total cholesterol declined slightly, but was not statistically different, between NHES III and NHANES I which were conducted in adjacent time periods. The mean total cholesterol level decreased by 8 mg/dL (P , 0.0001) in white adolescents and 5 mg/ dL (P , 0.005) in black adolescents from 1966–1970 to 1988–1994. As shown in Fig. 1, there has been a downward trend in mean total cholesterol among race-sex groups aged 12 to 17 years. Black females have maintained a higher mean than black males, white males, or white females. In addition, black females have experienced the smallest decline in mean total cholesterol, a drop of 4 mg/dL from 1966–1970 to 1988–1994. DISCUSSION

This investigation provides current national reference data on the distribution of lipid levels in U.S. children and adolescents and examines these distributions by age, sex, and race/ethnicity. This study is consistent with findings from previous studies on serum lipid levels by age, sex, and race [18–21]. The LRC Prevalence Study and NHANES I found that mean total cholesterol was higher among females than males [18,19]. In NHANES III, female adolescents had higher mean total cholesterol and LDL-C levels than did male adolescents, and 9- to 11-year-olds had the highest mean total cholesterol among all age groups. LRC data have also shown a decrease in total cholesterol among males during puberty as a result of a decrease in HDLC [19]. It is believed that this decrease probably stems from hormonal changes experienced by males during puberty [19]. Freedman et al. [20] reported that mean total cholesterol, LDL-C, and HDL-C levels were higher in black children than white children in the Bogalusa Heart Study, which was designed to examine racial differences in lipid levels in children. The NHANES III data confirm that non-Hispanic black children and adolescents have higher mean total cholesterol, LDL-C, and HDL-C levels compared with non-Hispanic white and Mexican American children and adolescents. In general, lower LDL-C levels in non-Hispanic whites and Mexican Americans were associated with lower total cholesterol, lower HDL-C, and higher triglycerides. Using the Friedewald equation, higher triglycerides accounted for about 5 mg/dL of VLDL-C in non-Hispanic white and

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SERUM LIPIDS AMONG U.S. CHILDREN AND ADOLESCENTS

TABLE 1 Serum Total Cholesterol Levels among U.S. Children and Adolescents 4 to 19 Years of Age by Age, Sex, and Race/Ethnicity: NHANES III, 1988–1994 Percentiles Population group

N

Mean (SE)

a

5

10

25

50

75

90

95

b

Age (years) 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Sex and ageb (years) Male 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Female 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Race/ethnicity and sex Non-Hispanic black Male Female Non-Hispanic white Male Female Mexican American Male Female Race/ethnicity and age (years) Non-Hispanic black 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Non-Hispanic white 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Mexican American 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) a b

1,707 1,367 1,488 1,502 1,435 2,937 7,499

162 166 171 161 165 163 165

(0.9) (1.0) (1.0) (1.2) (1.6) (1.0) (0.6)

124 126 131 118 118 118 121

132 134 139 126 124 125 130

144 149 151 141 141 141 145

161 165 168 158 158 158 162

177 182 187 178 182 180 181

194 197 206 197 207 201 200

204 209 222 209 222 217 216

161 166 172 158 158 158 163

(1.5) (1.7) (2.0) (1.6) (1.8) (1.2) (1.0)

122 126 135 116 116 116 119

132 134 140 124 122 123 127

143 146 153 140 138 139 143

159 164 170 157 155 156 161

175 183 188 174 174 174 179

191 202 208 192 199 195 198

202 212 226 203 213 206 212

164 166 169 164 171 167 167

(1.3) (1.4) (1.5) (1.9) (2.3) (1.3) (0.8)

125 126 130 122 118 119 124

133 135 137 129 128 128 132

145 149 148 142 145 144 147

162 165 166 159 163 161 163

178 180 185 181 189 185 184

196 196 204 201 217 209 202

206 203 218 218 237 225 220

168 (1.0) 171 (1.2)

122 122

132 134

148 149

165 167

186 189

204 213

219 226

162 (1.2) 166 (1.1)

118 123

126 132

143 146

160 163

178 182

195 200

207 217

163 (1.0) 165 (1.1)

121 121

129 128

143 144

159 161

180 183

202 201

213 216

166 172 173 169 168 168 170

(1.3) (1.7) (1.8) (1.2) (1.7) (1.1) (0.9)

121 128 131 119 120 119 122

128 138 138 127 131 130 133

147 150 152 147 147 147 148

164 168 168 166 163 164 166

182 190 191 186 186 186 187

200 210 212 208 214 211 209

214 219 226 222 226 224 223

162 166 170 159 163 161 164

(1.5) (1.3) (1.2) (1.4) (2.1) (1.4) (0.8)

128 125 131 117 117 117 119

134 133 140 126 123 124 129

144 149 151 140 139 139 144

160 165 168 157 157 157 162

175 181 186 176 182 179 180

188 196 201 193 205 199 198

202 204 219 203 221 215 212

161 164 168 160 168 163 164

(1.7) (1.8) (1.2) (1.7) (2.3) (1.6) (0.9)

120 126 126 118 121 119 121

127 134 135 123 129 126 129

143 145 147 139 145 141 144

159 162 163 155 162 157 160

177 179 186 176 186 181 182

197 192 206 198 211 204 201

204 208 216 212 227 218 214

Standard error of the mean. Includes other race/ethnicity groups in addition to non-Hispanic white, non-Hispanic black, and Mexican American.

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HICKMAN ET AL.

TABLE 2 Serum High-Density Lipoprotein Cholesterol (HDL-C) Levels among U.S. Children and Adolescents 4 to 19 Years of Age by Age, Sex, and Race/Ethnicity: NHANES III, 1988–1994 Percentiles Population group

N

Mean (SE)

a

5

10

25

50

75

90

95

b

Age (years) 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Sex and ageb (years) Male 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Female 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Race/ethnicity and sex Non-Hispanic black Male Female Non-Hispanic white Male Female Mexican American Male Female Race/ethnicity and age (years) Non-Hispanic black 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Non-Hispanic white 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) Mexican American 4–5 6–8 9–11 12–15 16–19 12–19 Total (4–19) a b

1,697 1,362 1,479 1,494 1,426 2,920 7,458

49 52 52 50 49 49 50

(0.5) (0.6) (0.5) (0.6) (0.5) (0.4) (0.3)

30 33 35 33 31 32 32

35 37 38 35 34 35 36

40 43 43 41 40 40 41

47 50 51 48 48 48 49

55 59 59 57 56 56 57

64 67 68 64 64 64 65

70 71 74 69 70 69 71

50 53 54 48 46 47 50

(0.7) (0.6) (0.6) (0.7) (0.9) (0.6) (0.4)

31 33 37 32 30 31 32

35 37 39 35 33 34 35

41 43 44 39 38 38 40

49 51 52 46 45 46 48

56 60 61 55 51 53 57

65 68 71 62 61 62 65

71 73 76 67 67 67 71

48 50 51 51 52 52 51

(0.6) (0.9) (0.7) (0.8) (0.7) (0.5) (0.4)

30 33 33 33 33 33 33

34 37 38 36 37 37 36

39 43 42 42 43 43 42

46 49 50 50 52 51 50

55 57 57 58 59 59 58

62 64 65 66 66 66 65

68 70 69 70 72 71 70

55 (0.5) 56 (0.4)

37 36

39 40

46 46

53 54

63 63

72 72

77 78

48 (0.5) 50 (0.5)

31 32

35 36

39 41

47 49

55 56

63 63

68 68

51 (0.5) 52 (0.4)

31 34

35 37

41 43

49 50

58 58

66 67

72 73

53 58 58 55 53 54 55

(0.7) (0.7) (0.7) (0.8) (0.5) (0.5) (0.4)

35 39 35 36 36 36 36

38 42 41 39 38 39 40

45 49 47 46 45 45 46

52 57 57 54 51 52 54

59 66 66 63 59 61 63

68 73 76 72 69 71 72

75 80 83 77 74 76 78

47 50 51 48 48 48 49

(0.8) (0.8) (0.8) (0.7) (0.6) (0.5) (0.4)

29 32 35 32 30 31 32

34 36 38 35 33 34 35

39 42 42 40 39 40 41

46 49 50 47 47 47 48

53 56 58 54 54 54 55

63 65 66 61 61 61 63

67 69 71 65 67 66 68

50 53 52 50 50 50 51

(0.6) (0.6) (1.0) (0.9) (0.6) (0.6) (0.4)

29 35 33 32 32 32 32

35 38 37 35 36 36 36

41 44 42 42 42 42 42

49 52 51 49 48 49 50

57 59 60 57 57 57 58

64 66 70 65 65 65 66

69 72 76 70 72 71 72

Standard error of the mean. Includes other race/ethnicity groups in addition to non-Hispanic white, non-Hispanic black, and Mexican American.

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SERUM LIPIDS AMONG U.S. CHILDREN AND ADOLESCENTS

TABLE 3 Serum Low-Density Lipoprotein Cholesterol (LDL-C)a Levels among U.S. Adolescents 12 to 19 Years of Age by Age, Sex, and Race/Ethnicity: NHANES III, 1988–1994 Percentiles Population group

N

Mean(SE)

b

5

10

25

50

75

90

95

91 (2.0) 99 (2.8) 95 (1.6)

51 56 53

56 63 61

73 78 76

88 90 89

106 113 109

125 146 132

135 162 152

88 (2.4) 94 (3.8) 91 (2.1)

50d 54d 52

54d 64d 60

68 76 73

83 89 88

103 103 103

119d 132d 126

131d 153d 149

94 (2.8) 103 (4.4) 99 (2.4)

54d 59d 54

59 63 62

77 79 78

90 94 92

110 123 115

127 147 139

145d 167d 161

99 (2.4) 102 (1.9)

60 58

68 71

80 81

98 96

115 123

127 142

138 154

91 (3.2) 100 (3.4)

48d 54d

58 60

72 76

87 90

102 115

131 145

152d 161d

93 (2.2) 92 (3.1)

56d 52d

63d 57

74 74

93 88

107 108

123d 124

135d 139d

101 (2.1) 100 (2.0) 101 (1.4)

57 60 59

70 69 69

81 80 81

99 96 97

119 116 119

133 134 134

142 156 146

89 (2.7) 101 (3.9) 95 (2.6)

46d 58d 51

53 65 59

70 78 75

86 90 88

105 113 107

122 151 135

133d 163d 155

91 (3.0) 95 (2.1) 93 (2.1)

53d 57d 54

57 63 61

73 76 74

90 91 91

106 109 107

123 126 123

130d 140d 136

c

Age (years) 12–15 16–19 Total (12–19) Sex and agec (years) Male 12–15 years 16–19 years Total (12–19) Female 12–15 16–19 Total (12–19) Race/ethnicity and sex Non-Hispanic black Male Female Non-Hispanic white Male Female Mexican American Male Female Race/ethnicity and age (years) Non-Hispanic black 12–15 16–19 Total (12–19) Non-Hispanic white 12–15 16–19 Total (12–19) Mexican American 12–15 16–19 Total (12–19)

551 544 1,095

a LDL-C was calculated from adolescents in the morning fasting subsample who fasted 9 h or more and whose triglycerides levels were less than or equal to 400 mg/dL. LDL-C was then calculated using the equation developed by Friedewald et al. [10]: (LDL-C) 5 (Total Cholesterol -(HDL-C)) - (Triglycerides/5). b Standard error of the mean. c Includes other race/ethnicity groups in addition to non-Hispanic white, non-Hispanic black, and Mexican American. d Estimate may be unstable due to small sample size relative to the complex survey design effect.

Mexican American adolescents compared to non-Hispanic black adolescents. Mean LDL-C plus VLDL-C values, which some consider a measure of the total atherogenic lipoproteins, were relatively similar in the three groups: 115, 114, and 112 mg/dL in non-Hispanic black, non-Hispanic white, and Mexican American 12- to 19year-olds, respectively. Mean total cholesterol levels were about 5–7 mg/dL higher in the non-Hispanic black adolescents compared to the other two groups. This

race/ethnicity pattern in children and adolescents is different from that observed for adults in NHANES III. In adults aged 20–74 years, non-Hispanic black men had the lowest age-adjusted mean total cholesterol (200 mg/dL) while non-Hispanic white women had the highest age-adjusted mean total cholesterol (205 mg/dL) [5,6]. Data from NHES III (1966–1970), NHANES I (1971– 1974), and NHANES III (1988–1994) indicate that the

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HICKMAN ET AL.

TABLE 4 Serum Triglyceridesa among U.S. Adolescents 12 to 19 Years of Age by Age, Sex, and Race/Ethnicity: NHANES III, 1988–1994 Percentiles Population group

N

Mean (SE)

554 545 1,099

b

5

10

25

50

75

90

95

91 (4.4) 95 (3.7) 93 (2.4)

38 39 38

44 45 45

56 58 57

74 78 76

108 119 110

147 173 160

208 207 207

87 (7.0) 94 (6.1) 91 (4.0)

35d 36d 36

41d 45d 42

54 56 55

72 79 74

101 119 107

135d 165d 150

178d 200d 196

96 (5.6) 96 (5.9) 96 (3.9)

41d 43d 43

48 46 47

59 60 60

81 76 77

110 118 115

170 168 171

213d 207d 208

72 (4.5) 72 (3.2)

35d 36d

39 40

48 50

63 63

84 81

99 110

117d 144d

95 (6.5) 99 (5.0)

37d 41d

43 47

56 60

76 80

109 118

164 172

205d 218d

95 (5.5) 98 (4.6)

37d 45d

44 53

55 62

79 85

109 111

146 156

203d 202d

74 (5.2) 70 (2.7) 72 (3.0)

35d 35d 35

39 41 39

49 48 49

64 63 63

82 83 82

103 100 101

151d 120d 126

94 (6.7) 99 (4.6) 97 (3.4)

38d 39d 39

43 48 35

57 59 57

74 81 78

108 123 115

168 173 171

211d 223d 216

95 (4.0) 98 (6.2) 96 (3.7)

43d 38d 42

48 46 47

60 60 60

83 82 83

109 112 111

144 158 150

191d 210d 205

c

Age (years) 12–15 16–19 Total (12–19) Sex and agec (years) Male 12–15 16–19 Total (12–19) Female 12–15 16–19 Total (12–19) Race/ethnicity and sex Non-Hispanic black Male Female Non-Hispanic white Male Female Mexican American Male Female Race/ethnicity and age (years) Non-Hispanic black 12–15 16–19 Total (12–19) Non-Hispanic white 12–15 16–19 Total (12–19) Mexican American 12–15 16–19 Total (12–19) a

Reported triglycerides include only adolescents in the morning fasting subsample who fasted 9 hours or more. Standard error of the mean. c Includes other race/ethnicity groups in addition to non-Hispanic white, non-Hispanic black, and Mexican American. d Estimate may be unstable due to small sample size relative to the complex survey design effect. b

mean serum total cholesterol levels have decreased 7 mg/dL, on average, among 12- to 17-year-olds. This trend was observed in males and females, as well as white and black children. However, black females continue to have the highest mean total cholesterol (168 mg/dL) of the four race/sex groups and experienced the smallest decrease (4 mg/dL) over time. These trends parallel overall decreases in mean total cholesterol observed for adults during a similar time period, although to a lesser extent. The age-adjusted mean serum cholesterol level declined 15 mg/dL in adults from 1960–1962

to 1988–1991 [5] and 17 mg/dL (220 to 203 mg/dL) from 1960–1962 to 1988–1994 [6] compared with a 7 mg/dL decline (167 to 160 mg/dL) in adolescents from 1966– 1970 to 1988–1994. Differences in the magnitude of the decline in total serum cholesterol levels in adolescents compared to adults may be due to a variety of factors that make the pattern of adolescents’ lipid levels different than adults; e.g., they start at lower total cholesterol levels and experience HDL-C and lipid changes associated with puberty. In addition, other factors such as dietary patterns and the relationships between obesity,

887

SERUM LIPIDS AMONG U.S. CHILDREN AND ADOLESCENTS

TABLE 5 Trends in Mean Serum Total Cholesterol Levels Among U.S. Adolescents 12 to 17 Years of Age by Sex and Race: 1966–1970, 1971–1974, and 1988–1994 NHES IIIa (1966–1970)

NHANES Ib (1971–1974)

NHANES IIIc (1988–1994)

N

Mean

(SE)d

N

Mean

(SE)d

N

Mean

(SE)d

Male Black White Totale

471 3,024 3,514

171 163 165

(1.8) (0.7) (0.8)

250 806 1,064

165 163 164

(2.5) (1.4) (1.3)

389 622 1,055

166 155 157

(1.5) (1.6) (1.3)

Female Black White Totale

513 2,668 3,196

172 170 170

(1.6) (0.9) (0.8)

259 796 1,062

174 166 167

(3.5) (1.4) (1.3)

456 714 1,222

168 163 164

(1.4) (1.5) (1.3)

Totale

6,710

167

(0.7)

2,126

165

(1.0)

2,277

160

(1.1)

Population

a

National Health Examination Survey III. First National Health and Nutrition Examination Survey. c Third National Health and Nutrition Examination Survey. d Standard error of the mean. e Includes other race groups in addition to white and black. b

physical activity, and lipids may be different in adolescents compared with adults. Blacks experienced a smaller decline in mean serum cholesterol levels compared with whites for both male and female adolescents and adults [5,6]. The trend data indicate that, at a time when CHD death rates were falling, both U.S. adults and U.S. adolescents were experiencing reductions in mean serum

cholesterol levels. Although variables such as race/ ethnicity, age, and gender are not modifiable, many of the risk factors that are strongly associated with elevated cholesterol levels are modifiable. As part of NCEP’s population approach, several health and dietary recommendations have been proposed for all healthy children over 2 years of age [4]. This approach is also consistent with the 1995 “Dietary Guidelines

FIG. 1. Trends in mean serum total cholesterol levels among adolescents aged 12 to 17 years by race-sex group in three national surveys: NHES III (1966–1970), NHANES I (1971–1974), and NHANES III (1988–1994).

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HICKMAN ET AL.

for Americans” [22]. These guidelines and the NCEP suggest that children eat a wide variety of foods to meet their nutritional needs and consume an adequate amount of calories to support normal growth and development. It is also recommended that total fat intake not exceed 30% of calories, that saturated fat intake be limited to less than 10% of the total calories, and that cholesterol be limited to less than 300 mg per day [4,22]. Dietary intake data indicate that mean fat intake in 12- to 17-year-olds decreased from about 37% of calories in NHANES I (1971–1974) and NHANES II (1976– 1980) to about 34% of calories in NHANES III (1988– 1994) [23,24]. Saturated fat declined from about 14 to 12% of calories over this same time period. Mean daily dietary cholesterol intakes declined from 350 mg in NHANES I to 265 mg in NHANES III. Dietary changes in adolescents are similar to those in adults for the same surveys [23–25]. NHANES data for adolescents indicate that although total fat and saturated fat as a percentage of calories and cholesterol intakes have decreased, mean intake levels are still above current dietary recommendations. More progress is needed to further improve dietary profiles in American children ages 2 years and older. Only about one in six children and adolescents currently meet dietary recommendations for fat and cholesterol [24]. Non-Hispanic black adolescents have a higher prevalence of overweight compared with non-Hispanic white and Mexican American children and adolescents, especially adolescent females [24,26]. Furthermore, non-Hispanic black females aged 6 to 17 years had the highest prevalence of overweight, as compared to nonHispanic white and Mexican American females in similar age groups [26]. The recent “Surgeon General’s Report on Physical Activity” reported that nearly half of American adolescents are not vigorously active on a regular basis and that physical activity declines dramatically in adolescence [27]. Based on NHANES, Troiano et al. [26] found an increase in the prevalence of overweight among children and adolescents from 1963 to 1991. Increases in overweight further emphasize the need to balance food intake with physical activity in children and adolescents. Since elevated total cholesterol and LDL-C levels increase the risk of cardiovascular disease in adults and higher HDL-C levels may lower the risk, it is unclear whether non-Hispanic black children and adolescents are at greater future risk of cardiovascular disease than other race/ethnic groups. In the PDAY study, young blacks had significantly more extensive fatty streaks than whites and similar extent of raised lesions and associations of lesions with age compared with whites [2]. However, race and sex differences in atherosclerotic lesions were not explained by the risk factors studied.

The PDAY study found that the effects of VLDLC1LDL-C levels, HDL-C levels, and smoking were similar in blacks and whites, and in men and women, suggesting that risk factor modification in all race-sex groups in adolescence is appropriate for the prevention of cardiovascular disease in adulthood. Tracking of cholesterol levels in childhood into adulthood has been described in several studies. Total cholesterol and LDL-C levels appear to track to a greater degree than other lipids [19,20]. In the Muscatine Study, it was found that childhood cholesterol measurements are generally predictive of adult levels of total and LDL-C [21]. However, of those children in kindergarten through the 12th grade who were found to have cholesterol levels greater than the 90th percentile, only about 43% were found to have levels greater than the 90th percentile by 20 to 30 years of age. In the Bogalusa Heart Study, the issue of tracking was explored by taking single lipid measurements 12 years apart [28]. Researchers found that the correlation between measurements was highly statistically significant for serum total cholesterol for each age, race, and sex group. Overall, the data on tracking of cholesterol from childhood to adulthood indicate that children with high cholesterol levels have a substantially greater risk of having elevated adult levels than the general population, but many of these children will have adult levels that do not require individual intervention. Consequently, a population-based approach to modification of risk factors and behaviors including fat, saturated fat, and cholesterol intakes and smoking habits in children and adolescents is important for the prevention of elevated serum lipids and reducing cardiovascular risk in adulthood. The PDAY study further supports the modification of risk factors beginning in adolescence to slow the development of early atherosclerotic lesions [2]. In four cross-sectional community-based studies conducted over 11 years (1979 through 1990), Frank et al. found that as cholesterol knowledge improved, so did the dietary behavior and blood cholesterol levels of 12- to 24-year-olds [29]. These data show the importance of continued national monitoring of children’s and adolescents’ mean serum total cholesterol levels and other risk factors to support the population-based approach outlined by the NCEP Expert Panel on Blood Cholesterol Levels in Children and Adolescents [4]. The NCEP also recommended that lipid cut points be applied to the screening of children who have a family history of premature cardiovascular disease or parental hypercholesteremia [4]. Although self-reported family history data were collected for children in NHANES III, data were not collected that allowed for a precise classification according to NCEP guidelines. Many of the precursors to cardiovascular disease begin in childhood which implies that the key to a healthy

SERUM LIPIDS AMONG U.S. CHILDREN AND ADOLESCENTS

adult population begins with primary prevention. The results of this investigation provide the scientific community, clinicians, and policy makers with a comprehensive picture of the lipid distribution among children and adolescents in the United States. These data can be used as a reference for the U.S. population for comparison to other studies, to measure and track progress in the health of American children, and to plan intervention and education programs for the prevention of cardiovascular disease. ACKNOWLEDGMENTS The authors thank Dr. Paul Bachorik at The Johns Hopkins University School of Medicine and Dr. Christopher Sempos at the National Heart, Lung, and Blood Institute, National Institutes of Health, for their helpful comments on the manuscript. REFERENCES 1. Strong JP. The natural history of atherosclerosis in childhood. In: Williams CL, Wynder EL, editors. Hyperlipidemia in childhood and the development of atherosclerosis. New York: New York Academy of Sciences, 1991:9–15. 2. McGill HC, McMahan CA, Malcom GT, Oalmann MC, Strong JP. Effects of serum lipoproteins and smoking on atherosclerosis in young men and women. The PDAY Research Group. Pathobiological Determinants of Atherosclerosis in Youth. Arterioscler Thromb Vasc Biol 1997;17:95–106. 3. Newman WP, Freedman DS, Voors AW, Gard PD, Srinivasan SR, Cresanta JL, et al. Relation of serum lipoprotein levels and systolic blood pressure to early atherosclerosis: The Bogalusa Heart Study. N Engl J Med 1986;314:138–44. 4. U.S. Department of Health and Human Services. Report of the Expert Panel on Blood Cholesterol Levels in Children and Adolescents. Washington, DC: U.S. Govt. Printing Office, 1991; DHHS Publication No. (PHS) 91-2732. 5. Johnson CL, Rifkind BM, Sempos CT, Carroll MD, Bachorik PS, Briefel RR, et al. Declining serum total cholesterol levels among U.S. adults: the National Health and Nutrition Examination Surveys. JAMA 1993;269:3002–8. 6. National Center for Health Statistics. Health, United States, 1996–97 and Injury Chartbook. Hyattsville, MD:1997; DHHS Publication No. (PHS) 97-1232. 7. National Center for Health Statistics. Plan and operation of the health examination survey of youths 12–17 years of age. Vital Health Stat 1 1974(8). 8. National Center for Health Statistics. Plan and operation of the health and nutrition examination survey, 1971–74. Vital Health Stat 1 1973(10). 9. U.S. Department of Health and Human Services. National Center for Health Statistics. Third National Health and Nutrition Examination Survey, 1988–94, Reference manuals and reports (CDROM). Hyattsville, MD: Centers for Disease Control and Prevention, 1996. 10. Friedewald WT, Levy RI Fredrickson DS. Estimation of the concentration of low density lipoprotein cholesterol in plasma without use of the preparative ultracentrifuge. Clin Chem 1972; 18:499–502. 11. National Cholesterol Education Program. Summary of the Second Report of the National Cholesterol Education Program

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(NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel II). JAMA 1993;269:3015–23. 12. Abell LL, Levy BB, Brodie BB, Kendal FE. Simplified method for the estimation of total cholesterol in serum and demonstration of its specificity. J Biol Chem 1952;195:357–66. 13. Bachorik PS to Carroll MD. Johns Hopkins University School of Medicine. Memorandum, January 27, 1992. 14. Shah BV, Barnwell BG, Bieler GS. SUDAAN users manual, Release 7.0. Research Triangle Park, NC: Research Triangle Institute, 1996. 15. Khare M, Mohadjer LK, Ezzati-Rice TM, Waksberg J. An evaluation of nonresponse bias in NHANES III (1988–91). Proceedings of the Section on Survey Research, American Statistical Association, Toronto, Canada, 1994. 16. Levy P S, Hamill PV, Heald F, Rowland M. Total serum cholesterol values of youths 12–17 years, United States. National Center for Health Statistics, Hyattsville, MD: Vital and Health Statistics, Series 11, No. 156, 1976. 17. Abraham S, Johnson CL, Carroll MD. Total serum cholesterol levels of children 4–17 years, United States, 1971–74. National Center for Health Statistics, Hyattsville, MD: Vital and Health Statistics, Series 11, No. 207, 1978. 18. Feinleib M, Johnson C, Ingster L. Trends in blood lipids and related nutrient intakes for US children. In: Filer LJ, Lauer RM, Luepker RV, editors. Prevention of atherosclerosis and hypertension beginning in youth. Philadelphia: Lea and Febiger, 1994: 23–32. 19. Kwiterovich PO. Plasma lipid and lipoprotein levels in childhood. In: Williams CL, Wynder EL, editors. Hyperlipidemia in childhood and the development of atherosclerosis. New York: The New York Academy of Sciences, 1991:90–107. 20. Freedman DS, Newman WP, Tracy RE, Voors AE, Srinivasan SR, Webber LS, et al. Black-white differences in aortic fatty streaks in adolescence and early adulthood: the Bogalusa Heart Study. Circulation 1988;77:856–64. 21. Lauer RM, Lee J, Clarke WR. Factors affecting the relationship between childhood and adult cholesterol levels: The Muscatine Study. Pediatrics 1988;309–318. 22. U.S. Department of Agriculture and US Department of Health and Human Services. 1995 Dietary guidelines for americans. fourth ed. Home and Garden Bulletin No. 232. Washington, DC, 1995. 23. McDowell MA, Briefel RR, Alaimo K, Bischof AM, Caughman CR, Carroll MD, et al. Energy and macronutrient intakes of persons ages 2 months and over in the United States: Third National Health and Nutrition Examination Survey, Phase 1, 1988–91. Advance Data from Vital and Health Statistics, No. 255. Hyattsville, MD: National Center for Health Statistics, 1994. 24. Federation of American Societies for Experimental Biology, Life Sciences Research Office. Prepared for the Interagency Board for Nutrition Monitoring and Related Research. Third Report on Nutrition Monitoring in the United States. Vols. 1 and 2. U.S. Government Printing Office, Washington, DC, 1995. 25. Ernst ND, Sempos CT, Briefel RR, Clark MB. Consistency between US dietary fat intake and serum total cholesterol levels: The National Health and Nutrition Examination Surveys. Am J Clin Nutr. 1997;66(Suppl.):965S–72S. 26. Troiano RP, Flegal KM, Kuczmarski RJ, Campbell SM, Johnson CL. Overweight prevalence and trends for children and adolescents: The National Health and Nutrition Examination Surveys, 1963 to 1991. Arch Pediatr Adolesc Med 1995;149:1085–91.

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Tracking of serum lipids and lipoproteins from childhood to adulthood: The Bogalusa Heart Study. Am J Epidemiol 1991;133: 884–99. 29. Frank E, Winkleby M, Foremann SP, Rockhill B, Farquhar JW. Improvements in cholesterol-related knowledge and behavior and plasma cholesterol levels in youths during the 1980s. Am J Prev Med 1993;9:168–74.