World Journal of Pediatrics

, Volume 14, Issue 5, pp 461–469 | Cite as

Associations of non-high-density lipoprotein cholesterol with metabolic syndrome and its components in Korean children and adolescents: the Korea National Health and Nutrition Examination Surveys 2008–2014

  • Yong Min Kim
  • So Hyun Kim
  • Young Suk ShimEmail author
Original Article



In this study, we aimed to investigate the relationship between single-gender Korean references for non-high-density lipoprotein cholesterol (non-HDL-C) and metabolic syndrome (MetS) in childhood.


A total of 5742 Korean children aged 10–18 years who participated in a national survey were included. The subjects were classified into three groups based on single-gender non-HDL-C levels as follows: < 120 mg/dL (desirable), ≥ 120 and < 150 mg/dL (borderline high), and ≥ 150 mg/dL (high).


Males in the borderline high non-HDL-C group had odds ratios (ORs) of 2.86 (95% confidence interval, 2.30–3.56) for elevated triglycerides (TG), 1.73 (1.08–1.79) for reduced high-density lipoprotein cholesterol (HDL-C) and 1.73 (1.08–2.78) for MetS compared with males in the desirable non-HDL-C group after adjusting for covariates. Males in the high non-HDL-C group had ORs of 1.65 (1.14–2.41) for elevated blood pressure (BP), 6.21 (4.27–9.05) for elevated TG, and 3.29 (1.49–7.26) for MetS compared with males in the desirable non-HDL-C group. Females in the borderline high non-HDL-C group had ORs of 3.03 (2.43–3.76) for elevated TG, 1.63 (1.13–2.35) for reduced HDL-C, and 4.53 (2.47–8.31) for MetS compared with females in the desirable non-HDL-C group. Females in the high non-HDL-C group had ORs of 1.43 (1.00–2.04) for elevated BP, 6.36 (4.45–9.08) for elevated TG, and 7.64 (3.65–15.96) for MetS compared with females in the desirable non-HDL-C group.


Our results suggest that, in a Korean population, a non-HDL-C level of 120 mg/dL for males and 150 mg/dL for females is the threshold between borderline high and high risk for MetS.


Adolescents Cardiovascular risk Children Metabolic syndrome Non-high-density lipoprotein cholesterol 


Author contributions

All authors were involved in drafting the article and critically revising it for important intellectual content, and all authors approved the final version to be submitted for publication. YSS has full access to all of the data pertaining to the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. YMK, SHK, and YSS participated in the writing of the paper. YMK and YSS participated in the research design. YSS provided expert advice regarding the statistical design. YSS participated in the analysis and interpretation of the data. YMK, SHK, and YSS participated in the data collection.


No funding was received in the current study.

Compliance with ethical standards

Ethical approval

All procedures in studies involving human participants were performed in accordance with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Conflict of interest

Authors declare no conflict of interest.


  1. 1.
    Ogden CL, Flegal KM, Carroll MD, Johnson CL. Prevalence and trends in overweight among US children and adolescents, 1999–2000. JAMA. 2002;288:1728–32.CrossRefPubMedCentralPubMedGoogle Scholar
  2. 2.
    Oh KW, Jang MJ, Lee NY, Moon JS, Lee CG, Yoo MH, et al. Prevalence and trends in obesity among Korean children and adolescents in 1997 and 2005. Korean J Pediatr. 2008;51:950–5.CrossRefGoogle Scholar
  3. 3.
    Chen W, Bao W, Begum S, Elkasabany A, Srinivasan SR, Berenson GS. Age-related patterns of the clustering of cardiovascular risk variables of syndrome X from childhood to young adulthood in a population made up of black and white subjects: the Bogalusa Heart Study. Diabetes. 2000;49:1042–8.CrossRefPubMedCentralPubMedGoogle Scholar
  4. 4.
    Ford ES, Giles WH, Mokdad AH. Increasing prevalence of the metabolic syndrome among u.s. Adults. Diabetes Care. 2004;27:2444–9.CrossRefPubMedGoogle Scholar
  5. 5.
    Chen W, Srinivasan SR, Li S, Xu J, Berenson GS. Clustering of long-term trends in metabolic syndrome variables from childhood to adulthood in Blacks and Whites: the Bogalusa Heart Study. Am J Epidemiol. 2007;166:527–33.CrossRefPubMedCentralPubMedGoogle Scholar
  6. 6.
    National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III) final report. Circulation. 2002;106:3143–421.CrossRefGoogle Scholar
  7. 7.
    Cui Y, Blumenthal RS, Flaws JA, Whiteman MK, Langenberg P, Bachorik PS, et al. Non-high-density lipoprotein cholesterol level as a predictor of cardiovascular disease mortality. Arch Intern Med. 2001;161:1413–9.CrossRefPubMedCentralPubMedGoogle Scholar
  8. 8.
    Kilgore M, Muntner P, Woolley JM, Sharma P, Bittner V, Rosenson RS. Discordance between high non-HDL cholesterol and high LDL-cholesterol among US adults. J Clin Lipidol. 2014;8:86–93.CrossRefPubMedCentralPubMedGoogle Scholar
  9. 9.
    Li C, Ford ES, McBride PE, Kwiterovich PO, McCrindle BW, Gidding SS. Non-high-density lipoprotein cholesterol concentration is associated with the metabolic syndrome among US youth aged 12–19 years. J Pediatr. 2011;158:201–7.CrossRefPubMedCentralPubMedGoogle Scholar
  10. 10.
    Shim YS, Baek JW, Kang MJ, Oh YJ, Yang S, Hwang IT. 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. J Atheroscler Thromb. 2016;23:1334–44.CrossRefPubMedCentralPubMedGoogle Scholar
  11. 11.
    Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, et al. Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol. 2014;43:69–77.CrossRefPubMedCentralPubMedGoogle Scholar
  12. 12.
    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.PubMedGoogle Scholar
  13. 13.
    Moon JS, Lee SY, Nam CM, Choi JM, Choe BK, Seo JW, et al. 2007 Korean National Growth Charts: review of developmental process and an outlook. Korean J Pediatr. 2008;51:1–25.CrossRefGoogle Scholar
  14. 14.
    Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.CrossRefPubMedGoogle Scholar
  15. 15.
    Cook S, Weitzman M, Auinger P, Nguyen M, Dietz WH. Prevalence of a metabolic syndrome phenotype in adolescents: findings from the third National Health and Nutrition Examination Survey, 1988–1994. Arch Pediatr Adolesc Med. 2003;157:821–7.CrossRefPubMedCentralPubMedGoogle Scholar
  16. 16.
    Berenson GS, Srinivasan SR, Bao W, Newman WP 3rd, Tracy RE, Wattigney WA. Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The Bogalusa Heart Study. N Engl J Med. 1998;338:1650–6.CrossRefPubMedCentralPubMedGoogle Scholar
  17. 17.
    McMahan CA, Gidding SS, Malcom GT, Tracy RE, Strong JP, McGill HC Jr. Pathobiological determinants of atherosclerosis in youth risk scores are associated with early and advanced atherosclerosis. Pediatrics. 2006;118:1447–55.CrossRefPubMedCentralPubMedGoogle Scholar
  18. 18.
    Chen W, Srinivasan SR, Li S, Xu J, Berenson GS. Metabolic syndrome variables at low levels in childhood are beneficially associated with adulthood cardiovascular risk: the Bogalusa Heart Study. Diabetes Care. 2005;28:126–31.CrossRefPubMedCentralPubMedGoogle Scholar
  19. 19.
    Hirschler V, Maccallini G, Molinari C, Urrutia IM, Castano On Behalf of the San Antonio de Los Cobres Study Group LA. Association between nontraditional risk factors and metabolic syndrome in indigenous Argentinean school children. Diabetes Technol Ther. 2014;16:84–90.CrossRefPubMedCentralPubMedGoogle Scholar
  20. 20.
    Pischon T, Girman CJ, Sacks FM, Rifai N, Stampfer MJ, Rimm EB. Non-high-density lipoprotein cholesterol and apolipoprotein B in the prediction of coronary heart disease in men. Circulation. 2005;112:3375–83.CrossRefPubMedCentralPubMedGoogle Scholar
  21. 21.
    Boekholdt SM, Arsenault BJ, Mora S, Pedersen TR, LaRosa JC, Nestel PJ, et al. Association of LDL cholesterol, non-HDL cholesterol, and apolipoprotein B levels with risk of cardiovascular events among patients treated with statins: a meta-analysis. JAMA. 2012;307:1302–9.CrossRefPubMedCentralPubMedGoogle Scholar
  22. 22.
    Frontini MG, Srinivasan SR, Xu JH, Tang R, Bond MG, Berenson G. Utility of non-high-density lipoprotein cholesterol versus other lipoprotein measures in detecting subclinical atherosclerosis in young adults (The Bogalusa Heart Study). Am J Cardiol. 2007;100:64–8.CrossRefPubMedCentralPubMedGoogle Scholar
  23. 23.
    Ramjee V, Sperling LS, Jacobson TA. Non-high-density lipoprotein cholesterol versus apolipoprotein B in cardiovascular risk stratification: do the math. J Am Coll Cardiol. 2011;58:457–63.CrossRefPubMedCentralPubMedGoogle Scholar
  24. 24.
    Expert Panel on Integrated Guidelines for Cardiovascular Health, and Risk Reduction in Children and Adolescents. National Heart, Lung, and Blood Institute. Expert panel on integrated guidelines for cardiovascular health and risk reduction in children and adolescents: summary report. Pediatrics. 2011;128(Suppl 5):S213–56.Google Scholar
  25. 25.
    Dai S, Yang Q, Yuan K, Loustalot F, Fang J, Daniels SR, et al. Non-high-density lipoprotein cholesterol: distribution and prevalence of high serum levels in children and adolescents: united States National Health and Nutrition Examination Surveys, 2005–2010. J Pediatr. 2014;164:247–53.CrossRefPubMedCentralPubMedGoogle Scholar
  26. 26.
    Abe Y, Okada T, Sugiura R, Yamauchi K, Murata M. Reference ranges for the non-high-density lipoprotein cholesterol levels in Japanese children and adolescents. J Atheroscler Thromb. 2015;22:669–75.CrossRefPubMedCentralPubMedGoogle Scholar
  27. 27.
    Ginsberg HN. Insulin resistance and cardiovascular disease. J Clin Invest. 2000;106:453–8.CrossRefPubMedCentralPubMedGoogle Scholar
  28. 28.
    Bonora E, Kiechl S, Willeit J, Oberhollenzer F, Egger G, Targher G, et al. Prevalence of insulin resistance in metabolic disorders: the Bruneck Study. Diabetes. 1998;47:1643–9.CrossRefPubMedCentralPubMedGoogle Scholar
  29. 29.
    Resnick HE, Jones K, Ruotolo G, Jain AK, Henderson J, Lu W, et al. Insulin resistance, the metabolic syndrome, and risk of incident cardiovascular disease in nondiabetic American Indians: the Strong Heart Study. Diabetes Care. 2003;26:861–7.CrossRefPubMedCentralPubMedGoogle Scholar
  30. 30.
    DeFronzo RA, Ferrannini E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care. 1991;14:173–94.CrossRefPubMedGoogle Scholar
  31. 31.
    Dandona P, Aljada A, Bandyopadhyay A. Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol. 2004;25:4–7.CrossRefPubMedCentralPubMedGoogle Scholar
  32. 32.
    Parvanova AI, Trevisan R, Iliev IP, Dimitrov BD, Vedovato M, Tiengo A, et al. Insulin resistance and microalbuminuria: a cross-sectional, case-control study of 158 patients with type 2 diabetes and different degrees of urinary albumin excretion. Diabetes. 2006;55:1456–62.CrossRefPubMedCentralPubMedGoogle Scholar
  33. 33.
    Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation. 2006;113:1888–904.CrossRefPubMedGoogle Scholar
  34. 34.
    Saely CH, Aczel S, Marte T, Langer P, Hoefle G, Drexel H. The metabolic syndrome, insulin resistance, and cardiovascular risk in diabetic and nondiabetic patients. J Clin Endocrinol Metab. 2005;90:5698–703.CrossRefPubMedCentralPubMedGoogle Scholar
  35. 35.
    Kuwabara K, Harada S, Sugiyama D, Kurihara A, Kubota Y, Higashiyama A, et al. Relationship between non-high-density lipoprotein cholesterol and low-density lipoprotein cholesterol in the general population. J Atheroscler Thromb. 2016;23:477–90.CrossRefPubMedCentralPubMedGoogle Scholar
  36. 36.
    de Ferranti SD, Gauvreau K, Ludwig DS, Neufeld EJ, Newburger JW, Rifai N. Prevalence of the metabolic syndrome in American adolescents: findings from the Third National Health and Nutrition Examination Survey. Circulation. 2004;110:2494–7.CrossRefPubMedCentralPubMedGoogle Scholar

Copyright information

© Children's Hospital, Zhejiang University School of Medicine 2018

Authors and Affiliations

  1. 1.Department of Pediatrics, Hallym University Dongtan Sacred Heart HospitalHallym University College of MedicineSeoulRepublic of Korea

Personalised recommendations