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Journal of Atherosclerosis and Thrombosis logoLink to Journal of Atherosclerosis and Thrombosis
. 2016 Dec 1;23(12):1334–1344. doi: 10.5551/jat.35634

Reference Values for The Triglyceride to High-Density Lipoprotein Cholesterol Ratio and Non-High-Density Lipoprotein Cholesterol in Korean Children and Adolescents: The Korean National Health and Nutrition Examination Surveys 2007–2013

Young Suk Shim 1, Joon Woo Baek 1, Min Jae Kang 1, Yeon Jeong Oh 1, Seung Yang 1, Il Tae Hwang 1,✉
PMCID: PMC5221496  PMID: 27373984

Abstract

Aim: Cholesterol levels vary throughout childhood and adolescence. The aim of the present study was to evaluate and identify age- and gender-specific reference values for serum lipid concentrations including non-high-density lipoprotein cholesterol (non-HDL-C) and the triglyceride to HDL-C ratio (TG/HDL-C ratio) in apparently healthy Korean children and adolescents.

Methods: A total of 6197 participants aged 10 to 19 years old from the 2007–2013 Korean National Health and Nutrition Examination Survey were analyzed. Serum lipid concentrations were evaluated according to age and gender.

Results: The overall mean concentration of non-HDL-C was 105.5 ± 25.6 mg/dL, with a significant gender difference: 103.3 ± 26.1 mg/dL in boys and 107.9 ± 24.7 mg/dL in girls (p = 0.028). The median values of non-HDL-C concentrations in boys and girls, respectively, were 111 and 112 mg/dL in the 10-year-old age group, 95 and 103 mg/dL in the 15-year-old age group, and 109 and 103 mg/dL in the 19-year-old age group. The overall mean TG/HDL-C ratio was 1.74 ± 1.22, and there were no significant gender differences: 1.77 ± 1.25 in boys and 1.72 ± 1.22 in girls (p = 0.183). The median values of the TG/HDL-C ratio in boys and girls were 1.16 and 1.00 in the 10-year-olds, 1.54 and 0.95 in the 15-year-olds, and 1.74 and 0.84 in the 19-year-olds, respectively.

Conclusions: Age- and gender-specific reference values for non-HDL-C and for the TG/HDL-C ratio in children and adolescents could provide valuable information for individualized interpretations of lipid profiles and interventions as well as for strategies to prevent and manage childhood and adolescent dyslipidemia.

Keywords: Triglyceride to high-density lipoprotein cholesterol ratio, Non-high-density lipoprotein cholesterol, Dyslipidemia, Children, Adolescents

See editorial vol. 23: 1311–1312

Introduction

The morbidity and mortality because of atherosclerotic cardiovascular disease (CVD) has become the leading cause of death in Korea, accounting for approximately 25% of all deaths1); furthermore, the age of CVD onset now tends to be younger than in previous decades2). Atherosclerosis can begin in childhood, and its development has been related to cardiovascular risk factors, including dyslipidemia3). Early recognition of the risk factors and age-specific interventions are both important in preventing CVD in adulthood. However, the cholesterol levels of children and adolescents have attracted little interest.

Recently, non-conventional lipid profiles have been suggested to be predictors of cardiovascular events. These predictors include the concentrations of non-high-density lipoprotein cholesterol (non-HDL-C) and the triglyceride (TG) to HDL-C ratio (TG/HDL-C ratio). Non-HDL-C, defined as the total cholesterol minus the high-density lipoprotein cholesterol (HDL-C), includes all atherogenic cholesterols, such as low-density lipoprotein (LDL), lipoprotein (a), intermediate-density lipoprotein (IDL), and very-low-density lipoprotein (VLDL) remnants4). In the National Cholesterol Education Program-Adult Treatment Panel III (NCEP-ATP III), non-HDL-C concentrations have been restricted to being a secondary goal in patients with high triglyceride concentrations of ≥200 mg/dL, whereas low-density lipoprotein cholesterol (LDL-C) concentrations are used as a primary therapeutic target5). However, recent studies have demonstrated that non-HDL-C can be used as an accurate predictor of cardiovascular disease6). The TG/HDL-C ratio has been suggested as a measure to identify overweight individuals with insulin resistance7, 8). In recent studies, the TG/HDL-C ratio was found to be associated with cardiovascular mortality9). It is well established that cholesterol levels vary by nation and ethnicity10). Therefore, caution should be used in the application of reference values from other nations and ethnicities in the Korean population. However, there are scarce reports on the distribution of non-HDL-C and of the TG/HDL-C ratio in Korean children and adolescents.

In the present study, we aimed to evaluate and identify age- and gender-specific reference values for serum lipids, including total cholesterol (TC), HDL-C, TG, LDL-C, non-HDL-C and the TG/HDL-C ratio, in a apparently healthy population of Korean children and adolescents.

Methods

Subjects

Data from the Korean National Health and Nutrition Examination Survey (KNHANES) from 2007–2013 were used. The KNHANES, a cross-sectional, nationally representative and population-based surveillance system, has been conducted annually since 1998 to evaluate the health and nutritional status of the civilian, non-institutionalized population of the Republic of Korea11). The survey is conducted by the Division of Chronic Disease Surveillance at the Korean Centers for Disease Control and Prevention. This survey, a nationally representative study, uses a stratified, multistage probability sampling design to select household units. The participants complete questionnaires that include a health interview survey, a health behavior survey, and a nutrition survey. All participants also undergo a health examination survey that includes fasting glucose, fasting insulin and fasting lipid profiles.

A total of 6,213 subjects had measures for TC, HDL-C, and TG and were 10 to 19 years old in the 2007–2013 KNHANES. Participants who had type 1 or 2 diabetes mellitus (DM) or thyroid disease were excluded from this study. Additionally, we excluded subjects receiving current medication for hyperlipidemia. Current medication for hyperlipidemia was defined as the administration of a drug for more than 20 days each month. Because LDL-C was determined using Friedewald's equation (LDL-C= total cholesterol − HDL-C − TG/5), which cannot be used when the triglyceride concentration is ≥400 mg/dL12), the participants with serum TG concentrations ≥400 mg/dL were also excluded. A final sample of 6,197 participants (3,260 males, 2,937 females) was available for analysis.

Anthropometric and Laboratory Measurements

The anthropometric data collected included height, weight, body mass index (BMI), waist circumference and blood pressure. BMI was determined by the weight in kilograms divided by the square of the height in meters (kg/m2). Blood samples were obtained from all subjects after ≥8 h of fasting. The collected specimens were centrifuged, frozen at −70°C and transported to a central laboratory (Seoul Medical Science Institute, Seoul, Korea before 2008 and NeoDIN Medical Institute, Seoul, Korea since 2008), where they were measured within 24 h. In 2007, the serum TC, HDL-C, and TG concentrations were measured enzymatically using ADIVIA1650 (Siemens/USA) with commercial reagents (Siemens/USA). After 2008, serum lipid concentrations, including total cholesterol (Pureauto S CHO-N; Daiichi, Tokyo, Japan), HDL-C (Cholestest N HDL; Daiichi), and triglycerides (Pureauto S TG-N; Daiichi), were analyzed by an enzymatic method using an automated analyzer (Hitachi Automatic Analyzer 7600, Hitachi). LDL-C concentrations were determined using Friedewald's formula. Non-HDL-C was calculated as: TC–HDL-C. Because the domestic laboratory which used to determine HDL-C changed in 2008, and the respective institutes used different analyzing methods and devices, some differences existed in the HDL-C results. Commutable frozen serum samples were prepared and sent to the Lipid Reference Laboratory at the Centers for Disease Control and Prevention in the USA. These data were compared with those from the two domestic laboratory institutes, and a conversion equation to adjust for the differences was formulated to obtain the true HDL-C value. The total coefficient of variation (CVs) for total cholesterol was 1.0%–2.8%. The total CV for HDL-C was 0.9%–3.2%, and the total CV for triglycerides was 0.9%–3.1%.

Definition

The presence of type 1 or 2 DM and thyroid disease and the current use of medications for hyperlipidemia were assessed using the responses to the questionnaire that the respective subjects had provided during the health interview. Dyslipidemia was defined by the following measures: 1) hyper-TC concentration (TC ≥200 mg/dL), hypo-HDL-C concentration (HDL-C < 40 mg/dL), hyper-TG concentration (TG ≥130 mg/dL), hyper-LDL-C (LDL-C ≥130 mg/dL), and hyper-non-HDL-C (non-HDL-C ≥145 mg/dL)5, 13).

Statistics

The data were analyzed using SPSS for Windows version 21 (IBM SPSS Inc., Chicago, IL, USA). The serum concentrations of TC, HDL-C, TG, LDL-C, and non-HDL-C and the TG/HDL-C ratio were analyzed according to age and gender for each age group and are presented as the mean ± standard deviation (SD) and percentiles (5th, 10th, 25th, 50th, 75th, 90th, 95th). P values less than 0.05 were considered statistically significant. Data are reported as the mean ± SD for the continuous variables.

Results

Clinical Characteristics of the Study Population

The clinical characteristics of the subjects are presented in Table 1. The boys had a significantly greater mean height (163.79 cm vs. 156.98 cm in girls, p < 0.001), weight (56.92 kg vs. 50.02 kg, p < 0.001) waist circumference (71.32 cm vs. 66.96 cm, p < 0.001), BMI (20.89 kg/m2 vs. 20.13 kg/m2, p < 0.001), systolic blood pressure (108.29 mmHg vs. 103.45 mmHg, p < 0.001) and diastolic pressure (66.84 mmHg vs. 65.61 mmHg, p < 0.001) than girls. The mean age was higher in the girls than in the boys (14.20 years old vs. 14.02 years old, respectively, p = 0.011).

Table 1. Clinical characteristics of the study population (n = 6197).

Total Boys Girls P
Number 6207 3260 2937
Age (years) 14.1 ± 2.8 14.0 ± 2.7 14.2 ± 2.8   0.011
Height (cm) 160.6 ± 11.4 163.8 ± 12.7 157.0 ± 8.4 <0.001
Weight (kg) 53.7 ± 13.9 56.9 ± 15.5 50.0 ± 10.8 <0.001
Waist circumference (cm) 69.3 ± 9.7 71.3 ± 10.5 67.0 ± 8.2 <0.001
Body mass index (kg/m2) 20.5 20.9 ± 3.8 20.1 ± 3.3 <0.001
Systolic blood pressure (mmHg) 106.0 ± 10.5 108.3 ± 10.9 103.5 ± 9.4 <0.001
Diastolic blood pressure (mmHg) 66.3 ± 9.3 66.9 ± 9.9 65.6 ± 8.5 <0.001
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Age-specific Reference Values for Serum Lipid Concentrations According to Age and Gender

Table 2 shows the mean, standard deviation, median, and percentile values for the serum lipid levels according to age and gender.

Table 2. Means, standard deviations, medians and percentiles for serum lipid profiles, non-HDL-C and TG/HDL-C ratios by age and gender among Korean children and adolescents (n = 6197).

Age n Mean SD Percentile
 　 Age n Mean SD Percentile
5 10 25 50 75 90 95 5 10 25 50 75 90 95
Boys Girls
Total cholesterol (mg/dL) Total cholesterol (mg/dL)
10 354 167.9 24.4 134 139 151 165 181 202 213 10 315 167.6 26.0 129 135 148 166 184 200 219
11 376 163.7 25.8 125 133 145 163 183 197 208 11 332 161.9 23.7 126 131 145 161 178 192 202
12 401 157.7 29.1 116 126 139 154 172 193 207 12 311 161.1 24.8 124 132 146 160 177 196 209
13 375 151.6 25.0 113 123 135 149 166 183 197 13 327 161.1 25.3 124 131 146 160 173 196 208
14 388 148.2 25.3 108 117 131 147 163 178 190 14 343 161.9 25.2 122 128 144 163 177 195 207
15 332 147.6 26.6 106 115 129 145 166 180 194 15 279 159.1 11.2 123 128 142 157 173 194 207
16 290 150.6 28.1 109 118 133 146 165 186 197 16 278 161.0 26.0 122 129 143 158 177 196 207
17 293 148.7 24.7 113 121 129 146 166 182 192 17 290 161.9 26.7 126 132 142 158 178 199 212
18 260 153.7 27.3 115 123 135 151 169 190 202 18 228 164.6 27.0 124 134 146 162 178 202 217
19 191 159.8 24.7 118 130 143 159 176 190 199 19 234 165.1 26.4 125 133 147 164 181 197 206
Total 3260 155.0 27.0 115 123 137 153 171 190 202 Total 2937 162.6 25.7 124 132 145 161 178 196 209
High-density lipoprotein cholesterol (mg/dL) High-density lipoprotein cholesterol (mg/dL)
10 354 56.7 11.8 39 43 48 55 64 73 79 10 315 54.8 11.3 39 41 47 53 62 70 75
11 376 55.1 11.5 38 41 47 55 62 70 75 11 332 53.5 11.1 36 41 46 52 61 68 74
12 401 53.0 11.2 36 39 45 52 60 69 73 12 311 54.5 10.0 37 41 48 54 61 67 71
13 375 51.6 11.0 35 39 44 50 59 66 70 13 327 53.5 10.4 36 41 47 53 60 66 71
14 388 50.3 10.2 34 37 42 50 57 63 68 14 343 53.4 10.4 38 40 46 53 60 67 71
15 332 48.7 9.6 35 37 42 48 55 61 65 15 279 54.3 11.2 36 40 47 54 62 69 72
16 290 49.1 9.6 35 37 43 49 54 61 67 16 278 54.3 11.4 37 40 46 53 62 68 76
17 293 48.9 9.2 34 37 42 48 55 61 63 17 290 55.4 10.4 39 42 48 55 62 68 72
18 260 50.8 10.0 36 38 44 51 57 64 69 18 228 55.8 12.4 36 40 48 55 65 72 76
19 191 50.3 9.4 36 39 43 49 56 61 68 19 234 58.4 10.5 42 45 51 58 65 71 78
Total 3260 51.7 10.8 36 39 44 51 58 66 71 Total 2937 54.6 11.0 38 41 47 54 62 68 73
Triglyceride (mg/dL) Triglyceride (mg/dL)
10 354 76.7 42.6 31 37 47 65 97 125 168 10 315 89.4 43.9 35 44 59 80 112 146 164
11 376 81.5 51.1 30 36 48 67 96 148 195 11 332 95.1 50.2 38 44 59 83 119 160 192
12 401 81.6 48.3 33 37 50 70 95 140 184 12 311 93.3 45.4 42 47 65 84 110 147 180
13 375 86.3 51.0 33 38 52 73 105 151 197 13 327 87.4 44.5 38 45 58 78 103 132 183
14 388 79.3 43.4 32 38 48 67 97 142 165 14 343 89.0 46.1 38 46 57 77 108 149 189
15 332 83.6 44.9 36 41 55 73 99 142 176 15 279 84.5 47.7 36 44 54 74 103 140 166
16 290 86.7 46.1 36 41 56 78 106 146 178 16 278 79.8 40.4 36 41 54 71 94 130 159
17 293 87.5 47.9 38 42 55 75 103 153 189 17 290 78.0 38.4 33 40 51 69 95 126 158
18 260 86.5 47.0 38 43 54 74 105 143 168 18 228 79.2 36.0 39 43 55 71 94 127 158
19 191 99.0 51.6 42 51 65 87 113 169 207 19 234 80.1 46.3 33 39 51 69 92 130 176
Total 3260 84.1 48.3 34 39 52 72 101 144 180 Total 2937 86.3 45.0 37 44 56 76 104 140 171
Boys Girls
Low-density lipoprotein cholesterol (mg/dL) Low-density lipoprotein cholesterol (mg/dL)
10 354 95.9 21.8 64 71 81 95 109 126 135 10 315 94.9 22.3 59 67 78 94 111 123 134
11 376 92.2 22.3 58 65 75 91 107 122 130 11 332 89.5 21.0 54 64 77 89 101 117 127
12 401 88.5 25.2 55 61 73 85 100 119 131 12 311 89.0 21.9 55 63 74 88 101 118 130
13 375 82.7 20.9 52 57 70 80 94 111 120 13 327 90.1 22.8 59 65 77 86 102 117 133
14 388 82.1 22.8 48 56 66 80 96 109 119 14 343 90.6 22.0 58 64 76 89 103 119 130
15 332 82.1 22.2 49 55 66 80 96 112 119 15 279 87.9 22.2 56 64 72 86 100 118 128
16 290 84.1 25.1 47 57 68 82 96 113 129 16 278 90.7 22.8 58 62 74 90 105 122 132
17 293 82.3 22.8 48 55 67 80 98 112 121 17 290 90.9 23.3 59 65 74 88 102 125 139
18 260 85.6 23.3 50 59 69 84 99 116 127 18 228 93.0 23.1 62 66 77 90 107 122 138
19 191 89.6 21.6 54 63 76 89 103 116 125 19 234 90.6 22.8 58 64 76 88 105 117 127
Total 3260 86.5 23.4 52 59 71 84 100 116 126 Total 2937 90.7 22.4 58 64 75 89 104 120 131
Non-high-density lipoprotein cholesterol (mg/dL) Non-high-density lipoprotein cholesterol (mg/dL)
10 354 111.3 23.4 78 84 95 111 124 144 156 10 315 112.8 23.7 76 85 94 112 129 143 153
11 376 108.5 24.8 73 77 90 106 125 143 151 11 332 108.5 23.7 71 79 94 107 121 140 149
12 401 104.8 27.7 67 76 88 99 119 139 156 12 311 107.7 23.7 70 78 91 106 121 141 156
13 375 100.0 24.7 64 71 84 97 113 131 143 13 327 107.6 24.5 72 81 92 104 122 138 154
14 388 98.0 25.4 61 69 81 96 113 128 140 14 343 108.4 23.3 74 80 91 107 123 139 154
15 332 98.8 25.1 62 68 80 96 116 129 143 15 279 104.8 25.6 68 77 87 101 118 139 152
16 290 101.5 28.1 63 69 82 98 114 135 154 16 278 106.7 25.8 69 77 89 104 121 140 155
17 293 99.8 25.7 63 68 82 99 116 134 146 17 290 106.5 25.7 71 78 88 102 120 143 158
18 260 102.9 27.1 65 72 83 101 119 136 150 18 228 108.8 25.8 73 79 91 105 124 143 154
19 191 109.4 25.4 70 78 93 109 126 145 151 19 234 106.6 26.1 71 77 89 103 122 137 155
Total 3260 103.3 26.1 66 73 85 101 119 136 150 Total 2937 107.9 24.7 72 79 91 105 122 140 153
Triglyceride to high-density lipoprotein cholesterol ratio Triglyceride to high-density lipoprotein cholesterol ratio
10 354 1.48 1.05 0.45 0.55 0.79 1.16 1.83 2.75 3.74 10 315 1.78 1.21 0.59 0.73 1.00 1.45 2.22 3.09 4.06
11 376 1.63 1.29 0.51 0.60 0.83 1.21 1.88 3.35 4.20 11 332 1.96 1.38 0.55 0.71 1.06 1.63 2.49 3.55 4.63
12 401 1.69 1.23 0.52 0.62 0.89 1.29 2.06 3.20 4.45 12 311 1.85 1.19 0.66 0.80 1.13 1.59 2.24 3.06 4.00
13 375 1.83 1.36 0.53 0.65 0.95 1.44 2.29 3.37 4.55 13 327 1.76 1.16 0.66 0.76 1.00 1.47 2.10 2.91 4.18
14 388 1.70 1.15 0.59 0.69 0.93 1.35 2.06 3.17 4.11 14 343 1.81 1.24 0.65 0.78 1.00 1.46 2.20 3.16 4.16
15 332 1.83 1.21 0.68 0.80 1.01 1.54 2.24 3.16 4.19 15 279 1.72 1.45 0.63 0.69 0.95 1.34 1.98 2.91 3.92
16 290 1.86 1.13 0.61 0.77 1.05 1.60 2.39 3.27 3.81 16 278 1.61 1.12 0.57 0.68 0.92 1.31 1.87 2.79 4.11
17 293 1.92 1.30 0.68 0.79 1.07 1.55 2.29 3.71 4.40 17 290 1.53 1.03 0.58 0.65 0.84 1.25 1.86 2.71 3.66
18 260 1.83 1.19 0.64 0.78 0.98 1.51 2.27 3.16 4.18 18 228 1.56 0.98 0.56 0.67 0.91 1.26 1.86 2.73 3.79
19 191 2.10 1.32 0.75 0.90 1.19 1.74 2.49 4.02 4.97 19 234 1.47 1.10 0.53 0.63 0.84 1.17 1.63 2.54 3.83
Total 3260 1.77 1.25 0.57 0.68 0.94 1.44 2.17 3.25 4.20 Total 2937 1.72 1.22 0.60 0.71 0.97 1.40 2.04 3.04 4.04
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SD; standard deviation

TC Concentrations

The overall mean concentration of TC was 158.6 ± 26.7 mg/dL, with a significant gender difference: 155.0 ± 27.0 mg/dL in boys and 162.6 ± 25.7 mg/dL in girls (p < 0.001).

The median TC level was approximately 160 mg/dL in 10- to 11-year-old boys and decreased to approximately 150 mg/dL in 12- to 18-year-old boys. The 95th percentile value was approximately 210 mg/dL in 10- to 12-year-old boys and approximately 200 mg/dL in 13- to 19-year-old boys. In girls, the median value of TC concentration was approximately 160 mg/dL in the 11- to 19-year-old age groups. The 95th percentile concentration was approximately 210 mg/dL in 12- to 19-year-old girls. The prevalence of a TC concentration >200 mg/dL was 5.6% in boys and 8.3% in girls.

HDL-C Concentrations

The overall mean concentration of HDL-C was 53.1 ± 11.0 mg/dL with a significant gender difference: 51.7 ± 10.8 mg/dL in boys and 54.6 ± 10.6 mg/dL in girls (p < 0.001).

In boys, the median concentration of HDL-C was approximately 55 mg/dL in the 10- to 11-year-old groups and decreased to approximately 50 mg/dL in the 12- to 19-year-old groups. The 5th percentile value of HDL-C was approximately 40 mg/dl in 10- to 19-year-old boys. In girls, the median concentration of HDL-C and the 5th percentile level of HDL-C was similar, approximately 55 mg/dL and 40 mg/dL, respectively, in the 10- to 19-year-old age groups. The prevalence of a HDL-C concentration <40 mg/dL was 12.0% in boys and 7.5% in girls.

TG Concentrations

The overall mean concentration of TG was 85.0 ± 46.2 mg/dL, with no significant gender difference: 84.1 ± 48.3 mg/dL in boys and 86.3 ± 45.0 mg/dL in girls (p = 0.057).

In boys, the median value of TG concentration increased gradually from 65 mg/dL in the 10-year-old age group to approximately 75 mg/dL in the 18-yearold age group. Overall, the 95th percentile concentration was approximately 185 mg/dL in the 10- to 19-year-old age groups. In girls, the median TG concentration decreased gradually from 80 mg/dL in the 10-year-old age group to approximately 70 mg/dL in the 19-year-old age group. Overall, the 95th percentile TG was approximately 170 mg/dL in girls of all ages. The prevalence of a TG concentration ≥130 mg/dL was 13.3% in boys and 12.9% in girls.

LDL-C Concentrations

The overall mean concentration of LDL-C was 88.5 ± 23.0 mg/dL, with a significant gender difference: 86.5 ± 23.4 mg/dL in boys and 90.7 ± 22.4 mg/dL in girls (p < 0.001).

In boys, the median concentration of LDL-C was approximately 90 mg/dL in the 10- to 11-yearold age groups and approximately 85 mg/dL in the 12- to 19-year-old age groups. The 95th percentile LDL-C concentration was approximately 130 mg/dL in 10- to 12-year-olds and decreased to approximately 125 mg/dL in 13- to 19-year-olds. In girls, the median value of LDL-C concentration was relatively consistent at approximately 90 mg/dl. The 95th percentile LDL-C concentration was approximately 130 mg/dL in 10- to 19-year-old girls. The prevalence of a LDL-C concentration ≥130 mg/dL was 4.2% in boys and 5.5% in girls.

Non-HDL-C Concentration

The overall mean concentration of non-HDL-C was 105.5 ± 25.6 mg/dL, and there was a significant gender difference: 103.3 ± 26.1 mg/dL in boys and 107.9 ± 24.7 mg/dL in girls (p = 0.028).

In boys, the median value of non-HDL-C concentrations was approximately 110 mg/dL in the 10- to 11-year-old age groups and approximately 100 mg/dL in the 12- to 17-year-old age groups. Finally, the median value of non-HDL-C concentrations was approximately 110 mg/dL in the 18- to 19-year-olds. The 95th percentile non-HDL-C concentration was approximately 150 mg/dL in the 10- to 19-year-old age groups (Fig. 1-A). The curve of the non-HDL-C was U-shaped in boys. In girls, the median non-HDL-C concentration was approximately 110 mg/dL in the 10- to 11-year-old age groups and approximately 105 mg/dL in the 12- to 19-year-old age groups. The 95th percentile concentration of non-HDL-C was relatively consistent, at an approximate level of 150 mg/dL (Fig. 1-B). The prevalence of a non-HDL-C concentration ≥145 mg/dL was 6.5% in boys and 7.8% in girls.

Fig. 1.

Fig. 1.

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Reference percentile curves for non-HDL-C according to age in Korean boys (A) and girls (B) (n = 6,197)

TG/HDL-C Ratio

The overall mean TG/HDL-C ratio was 1.74 ± 1.22, and there was no significant gender difference: 1.77 ± 1.25 in boys and 1.72 ± 1.22 in girls (p = 0.183).

In boys, the median TG/HDL-C ratio increased gradually from 1.16 in the 10-year-olds to 1.75 in the 19-year-olds. Although the 95th percentile values of the TG/HDL-C ratio varied, they showed an increasing tendency overall (Fig. 2-A). In girls, the median TG/HDL-C ratio decreased gradually from 1.46 in the 10-year-old age group to 1.17 in the 19-year-old age group. The 95th percentile TG/HDL-C ratio decreased gradually from 4.61 in 10-year-old girls to 3.83 in 19-year-old girls (Fig. 2-B).

Fig. 2.

Fig. 2.

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Reference percentile curves for the TG/HDL-C ratio according to age in Korean boys (A) and girls (B) (n = 6,197)

Discussion

In the present study, we identified the reference values of fasting serum lipid profiles including non-HDL-C and TG/HDL-C ratios in Korean children and adolescents from a nationally representative survey. We evaluated the distributions of non-HDL-C and of TG/HDL-C ratios in Korean children and adolescents aged 10 to 19 years. The overall means of the non-HDL-C and of the TG/HDL-C ratio in boys were 103.3 ± 26.1 mg/dL and 1.77 ± 1.25, respectively, and 107.9 ± 24.7 mg/dL and 1.22 ± 0.60 in girls, respectively.

In pediatric fields, measuring non-HDL-C has a distinct advantage because it does not require fasting. The Expert Panel on Integrated Guidelines for Cardiovascular Health and Risk Reduction in Children and Adolescents recommends the use of non-fasting non-HDL-C concentrations as a screening method for dyslipidemia. Several lines of evidence have supported non-HDL-C as a good predictor of CVD risk. In the Pathobiological Determinants of Atherosclerosis in Youth (PDAY) study, adolescents and adults aged 15 to 34 years with high non-HDL-C concentrations were at a significantly high risk for histological progression from fatty streaks to advanced atherosclerotic lesions14). In the Bogalusa Heart Study, non-HDL-C levels were as good as or better than other lipoprotein measurements, including LDL-C level, for identifying subclinical atherosclerosis among young subjects aged 24 to 48 years15). A study of US children and adolescents aged 12 to 19 years demonstrated that non-HDL-C was significantly associated with metabolic syndrome, which is significantly associated with CVD in adulthood16). In a US study of non-HDL-C, youth with non-HDL-C concentrations ≥120 mg/dL and ≥145 mg/dL were at borderline high and high risk of metabolic syndrome, respectively. Therefore, in the Expert Panel on Integrated Guidelines for Cardiovascular Health and Risk Reduction in Children and Adolescents, a non-HDL-C concentration <120 mg/dL, between 120 and 144 mg/dL and ≥145 mg/dL are defined as acceptable, borderline high and high, respectively13). Recently, a study of Japanese children and adolescents aged 9 to 16 years presented reference values for non-fasting non-HDL-C17). In that population, a non-HDL-C concentration ≥122 mg/dL in boys and ≥125 mg/dL in girls were considered borderline high risk (highest 75th percentile), whereas a non-HDL-C concentration of ≥152 mg/dL in boys and ≥159 mg/dL in girls indicated high risk (highest 95th percentile). Another Japanese study reported that obese boys with MetS have elevated non-HDL-C levels and may have a higher risk for the development of atherosclerosis18). In their study, the mean non-HDL-C level in obese boys was 139.0 mg/dl and that in boys with abdominal obesity, pre-MetS (abdominal obesity plus one component of MetS), and MetS were 112.9, 135.4, and 149.0 mg/dl, respectively. However, there have been no available data for non-HDL-C in Korea. In the present study, a non-HDL-C of ≥111 mg/dL in boys and ≥112 mg/dL in girls was the highest 75th percentile, and a non-HDL-C ≥156 mg/dL in boys and ≥158 mg/dL in girls was the highest 95th percentile. The prevalence of a non-HDL-C concentration ≥145 mg/dL was 6.5% in boys and 7.8% in girls. Our results will help clinicians interpret lipid profiles in Korea. Further studies are needed to identify the optimal cutoff points for non-HDL-C concentrations in Korean children and adolescents.

The TG/HDL-C ratio, a recently introduced lipid profile measure, may be a better predictor of small, dense low-density lipoprotein (LDL)19), an atherogenic lipoprotein particle that strongly predicts coronary heart disease and has been related to an increased risk of CVD20). An elevated TG/HDL-C ratio has been associated with coronary artery disease in adults who underwent cardiac catheterization21). TG/HDL-C was found to be an independent predictor of carotid intima-media thickness progression, which is an independent risk factor for CVD in adults22). In a study of US adolescents and adults aged 10 to 26 years, the TG/HDL-C ratio was found to be an independent predictor of arterial stiffness in adolescents and young adults23). In addition, a large Italian study showed that the TG/HDL-C ratio can be a simple and effective tool to identify children and adolescents with atherogenic dyslipidemia and cardio-metabolic risk24). In that Italian study, individuals with a TG/HDL-C ratio ≥2.2 were at high risk of preclinical signs of organ damage. Another study in the US demonstrated that white children and adolescents with a TG/HDL-C ratio ≥2.27 were at a high risk of insulin resistance25). Insulin resistance is a main mechanism involved in metabolic syndrome, which is a significant risk factor for CVD. Thus individuals with a TG/HDL-C ratio ≥2.27 can be considered at risk for CVD. However, in a study by Ostfeld et al.21), adults with a TG/HDL-C ratio ≥3.5 were significantly associated with CAD. Furthermore, in a study on US adolescents and young adults by Urbina et al.23), individuals with a TG/HDL-C ratio ≥2.7 were at high risk (the highest tertile). There is thus controversy over the cutoff point for cardiovascular risk. There have been few studies on the distribution of the TG/HDL-C ratio in healthy children and adolescents. In this study, the overall mean TG/HDL-C ratio was 1.77 in boys and 1.72 in girls. The highest 75th percentile was 2.39 in boys and 2.49 in girls, and the highest 95th percentile was 4.55 in boys and 4.63 in girls. The highest 75th percentile of the TG/HDL-C ratio in both genders was within the values of 2.2 to 2.7, which were the values associated with a high risk of CVD in children adolescents in this study.

In our study, the trends in TG/HDL-C ratio regarding age differed between boys and girls. The TG/HDL-C ratio tended to increase with age in boys, whereas the trend in TG/HDL-C ratio was decreasing with age in girls. Serum lipids are affected by age, gender, ethnicity, nutritional state, pubertal stage, physical activity, and hormonal status including menstrual cycle for women26–29). Although the study populations in a study by Skinner et al.26) did not fast, the curves of TG regarding age had a slightly increasing trend after the age of 10 in boys but a decreasing trend in girls. On the other hand, the HDL-C curve for age showed a decreasing trend in boys, whereas the HDL-C curve for age showed an increasing trend in girls. A Japanese study found a decreasing trend in HDL-C with age in boys and an increasing trend in HDL-C with age in girls17). Moreover, a previous Korean study showed that the HDL-C concentrations had an increasing trend with age in girls but a decreasing trend in boys30). The TG levels regarding age had an increasing trend in boys and a decreasing trend in girls30). Those results showed a similar pattern in TG and HDL-C concentrations as the present study. Although the direct TG/HDL-C ratio was not estimated in that study, we can postulate that the TG/HDL-C ratio for age would have a similar pattern as the one in our study throughout childhood and adolescence.

The results of this study confirmed previous findings that the distribution of serum lipids vary with age and gender26, 31, 32). This can be related to physiologic changes that indicate hormonal influences and lead to lipid variations. However, current guidelines for lipids and treatment based on fixed cutoff values do not reflect a normal distribution of age and gender. Evaluating lipid profiles against age- and gender-specific curves could be helpful in managing lipid problems in children and adolescents. It is expected that these curves could play a role in preventing over- and under-treatment. From the individual's perspective, proper management of lipids within age- and gender-specific reference values can help delay future cardiovascular events33). From a national perspective, these curves could play a significant role in planning national strategies for the prevention and control of cholesterol in children and adolescents.

There were several limitations to this study. The results were based on cross-sectional data; therefore, we cannot track whether each child followed the pattern of the curves. We were unable to evaluate the associations between the distribution of serum lipids and pubertal stage. There were no available data from previous studies to compare with the present study, and we cannot evaluate the trends in serum lipid concentrations. Further studies are needed to evaluate trends in the distribution of serum lipids with an increased sample size.

Conclusion

This study on the distribution of serum lipid concentrations in Korea demonstrated age- and gender-specific reference values of serum lipid profiles including non-HDL-C and TG/HDL-C ratios in children and adolescents based on a nationally representative survey. These results provide not only more information for individualized interpretation of lipid profiles and interventions but also valuable information for planning strategies to prevent and manage childhood and adolescent dyslipidemia.

Acknowledgement

None.

Conflicts of Interest

The authors declare no conflicts of interest.

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