Skip to main content

Advertisement

SpringerLink
Log in

Association of lipid parameters and insulin resistance with bone health in South Korean adolescents

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

This study investigated the association between lipid profiles and insulin resistance and bone mineral content (BMC) in Korean adolescents and found that BMC was inversely associated with triglyceride (TG) and homeostasis model assessment of insulin resistance (HOMA-IR). This association did not differ according to obesity status in either boys or girls.

Introduction

To prevent future osteoporosis, it is important to identify factors that affect bone health in adolescents as well as adults. This study aimed to examine the association between lipid profiles and insulin resistance and BMC in Korean adolescents.

Methods

Data from 706 boys and 621 girls, who participated in the Korea National Health and Nutrition Examination Survey from 2008 to 2011, were analyzed. Lipid profiles were measured, and HOMA-IR was calculated to assess insulin resistance. BMC was measured for the total femur, femur neck, and lumbar spine by using whole-body dual-energy X-ray absorptiometry (DXA).

Results

TG level and HOMA-IR were negatively correlated with BMC at all three sites in boys. In girls, TG level showed a negative correlation with BMC at the femur neck and lumbar spine, and HOMA-IR was negatively associated with BMC at the femur neck only. These inverse associations did not differ according to obesity status in either sex. Adjusted means of BMC at the three sites in boys tended to decrease in the higher tertile groups of TG and HOMA-IR, and the adjusted means of BMC for the total femur in girls tended to decrease in the higher tertile groups of TG and HOMA-IR.

Conclusions

BMC was inversely associated with TG and HOMA-IR in Korean adolescents, and this association was more pronounced in boys. This association did not differ according to obesity status in either sex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Jeong TD, Lee W, Choi SE, Kim JS, Kim HK, Bae SJ, Chun S, Min WK (2014) Relationship between serum total cholesterol level and serum biochemical bone turnover markers in healthy pre- and postmenopausal women. Biomed Res Int 2014:398397

    PubMed Central  PubMed  Google Scholar 

  2. Lloyd T, Eggli DF (1992) Measurement of bone mineral content and bone density in healthy twelve-year-old white females. J Nucl Med 33:1143–1145

    CAS  PubMed  Google Scholar 

  3. Heaney RP (2003) Bone mineral content, not bone mineral density, is the correct bone measure for growth studies. Am J Clin Nutr 78:350–351, author reply 351–352

    CAS  PubMed  Google Scholar 

  4. Chiarelli F, Marcovecchio ML (2008) Insulin resistance and obesity in childhood. Eur J Endocrinol 159(Suppl 1):S67–74

    Article  CAS  PubMed  Google Scholar 

  5. Clark EM, Ness AR, Tobias JH (2006) Adipose tissue stimulates bone growth in prepubertal children. J Clin Endocrinol Metab 91:2534–2541

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Timpson NJ, Sayers A, Davey-Smith G, Tobias JH (2009) How does body fat influence bone mass in childhood? A Mendelian randomization approach. J Bone Miner Res 24:522–533

    Article  PubMed Central  PubMed  Google Scholar 

  7. Montalcini T, Emanuele V, Ceravolo R, Gorgone G, Sesti G, Perticone F, Pujia A (2004) Relation of low bone mineral density and carotid atherosclerosis in postmenopausal women. Am J Cardiol 94:266–269

    Article  PubMed  Google Scholar 

  8. de Almeida Pereira Coutinho M, Bandeira E, de Almeida JM, Godoi ET, Vasconcelos G, Bandeira F (2013) Low bone mass is associated with increased carotid Intima media thickness in Men with type 2 diabetes mellitus. Clin Med Insights Endocrinol Diabetes 6:1–6

    Article  PubMed Central  PubMed  Google Scholar 

  9. Lee HT, Shin J, Min SY, Lim YH, Kim KS, KimSG KJH, Lim HK (2015) Relationship between bone mineral density and a 10-year risk for coronary artery disease in a healthy Korean population: the Korea National Health and Nutrition Examination Survey 2008–2010. Coron Artery Dis 26:66–71

    Article  PubMed  Google Scholar 

  10. Tankò LB, Bagger YZ, Christiansen C (2003) Low bone mineral density in the hip as a marker of advanced atherosclerosis in elderly women. Calcif Tissue Int 73:15–20

    Article  PubMed  Google Scholar 

  11. Koshiyama H, Wada Y, Nakamura Y (2001) Hypercholesterolemia as a possible risk factor for osteopenia in type 2 diabetes mellitus. Arch Intern Med 161:1678

    Article  CAS  PubMed  Google Scholar 

  12. Adami S, Braga V, Zamboni M, Gatti D, Rossini M, Bakri J, Battaglia E (2004) Relationship between lipids and bone mass in 2 cohorts of healthy women and men. Calcif Tissue Int 74:136–142

    Article  CAS  PubMed  Google Scholar 

  13. Solomon DH, Avorn J, Canning CF, Wang PS (2005) Lipid levels and bone mineral density. Am J Med 118:1414

    Article  Google Scholar 

  14. Barrett-Connor E, Kritz-Silverstein D (1996) Does hyperinsulinemia preserve bone? Diabetes Care 19:1388–1392

    Article  CAS  PubMed  Google Scholar 

  15. Abrahamsen B, Rohold A, Henriksen JE, Beck-Nielsen H (2000) Correlations between insulin sensitivity and bone mineral density in non-diabetic men. Diabet Med 17:124–129

    Article  CAS  PubMed  Google Scholar 

  16. Dennison EM, Syddall HE, Aihie Sayer A, Craighead S, Phillips DI, Cooper C (2004) Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire Cohort Study: evidence for an indirect effect of insulin resistance? Diabetologia 47:1963–1968

    Article  CAS  PubMed  Google Scholar 

  17. Birkeland KI, Hanssen KF, Torjesen PA, Vaaler S (1993) Level of sex hormone-binding globulin is positively correlated with insulin sensitivity in men with type 2 diabetes. J Clin Endocrinol Metab 76:275–278

    CAS  PubMed  Google Scholar 

  18. Faulhaber GA, Premaor MO, Moser Filho HL, Silla LM, Furlanetto TW (2009) Low bone mineral density is associated with insulin resistance in bone marrow transplant subjects. Bone Marrow Transplant 43:953–957

    Article  CAS  PubMed  Google Scholar 

  19. Koroglu BK, Kiris F, Ersoy IH, Sutcu R, Yildiz M, Aksu O, Ermis F, Ersoy S, Tamer MN (2011) Relation of leptin, adiponectin and insulin resistance to bone mineral density in type 2 diabetic postmenopausal women. Endokrynol Pol 62:429–435

    CAS  PubMed  Google Scholar 

  20. Lawlor DA, Sattar N, Sayers A, Tobias JH (2012) The association of fasting insulin, glucose, and lipids with bone mass in adolescents: findings from a cross-sectional study. J Clin Endocrinol Metab 97:2068–2076

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Expert Panel on Detection, Evauation, and Treatment of High Blood Cholesterol in Adults (2001) Executive summary of the third report of the national cholesterol education, and treatment of high blood cholesterol in adults (adult treatment panel III). JAMA 285:2486–2497

    Article  Google Scholar 

  22. Moon JS, Lee SY, Nam CM, Choi JM, Choe BK, Seo JW, Oh K, Jang MJ, Hwang SS, Yoo MH, Kim YT, Lee CG (2008) 2007 Korean National Growth Charts: review of developmental process and an outlook. Korean J Pediatr 51:1–25

    Article  Google Scholar 

  23. Korea Centers for Disease Control and Prevention (KCDC). Korea National Health and Nutrition Examination Survey. https://knhanes.cdc.go.kr/knhanes/index.do. Accessed 1 August 2015.

  24. Oh JY, Yang YJ, Kim BS, Kang JH (2007) Validity and reliability of Korean version of International Physical Activity Questionnaire (IPAQ) short form. J Korean Acad Fam Med 28:532–541

    Google Scholar 

  25. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502

    CAS  PubMed  Google Scholar 

  26. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419

    Article  CAS  PubMed  Google Scholar 

  27. Joo NS, Dawson-Hughes B, Yeum KJ (2013) 25-Hydroxyvitamin D, calcium intake, and bone mineral content in adolescents and young adults: analysis of the fourth and fifth Korea National Health and Nutrition Examination Survey (KNHANES IV-2, 3, 2008–2009 and V-1, 2010). J Clin Endocrinol Metab 98:3627–3636

    Article  CAS  PubMed  Google Scholar 

  28. Rosen CJ, Klibanski A (2009) Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. Am J Med 122:409–414

    Article  CAS  PubMed  Google Scholar 

  29. Yoo HJ, Park MS, Yang SJ, Kim TN, Lim KI, Kang HJ, Song W, Baik SH, Choi DS, Choi KM (2012) The differential relationship between fat mass and bone mineral density by gender and menopausal status. J Bone Miner Metab 30:47–53

    Article  PubMed  Google Scholar 

  30. Holecki M, Wiecek A (2010) Relationship between body fat mass and bone metabolism. Pol Arch Med Wewn 120:361–367

    CAS  PubMed  Google Scholar 

  31. Tintut Y, Morony S, Demer LL (2004) Hyperlipidemia promotes osteoclastic potential of bone marrow cells ex vivo. Arterioscler Thromb Vasc Biol 24:e6–10

    Article  CAS  PubMed  Google Scholar 

  32. Poli A, Bruschi F, Cesana B, Rossi M, Paoletti R, Crosignani PG (2003) Plasma low-density lipoprotein cholesterol and bone mass densitometry in postmenopausal women. Obstet Gynecol 102:922–926

    Article  CAS  PubMed  Google Scholar 

  33. Kato M, Patel MS, Levasseur R, Lobov I, Chang BH, Glass DA 2nd, Hartmann C, Li L, Hwang TH, Brayton CF, Lang RA, Karsenty G, Chan L (2002) Cbfa1-independent decrease in osteoblast proliferation, osteopenia, and persistent embryonic eye vascularization in mice deficient in Lrp5, a Wnt coreceptor. J Cell Biol 157:303–314

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Mani A, Radhakrishnan J, Wang H, Mani A, Mani MA, Nelson-Williams C, Carew KS, Mane S, Najmabadi H, Wu D, Lifton RP (2007) LRP6 mutation in a family with early coronary disease and metabolic risk factors. Science 315:1278–1282

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Lee NK, Karsenty G (2008) Reciprocal regulation of bone and energy metabolism. Trends Endocrinol Metab 19:161–166

    Article  CAS  PubMed  Google Scholar 

  36. Pollock NK, Bernard PJ, Gower BA, Gundberg CM, Wenger K, Misra S, Bassali RW, Davis CL (2011) Lower uncarboxylated osteocalcin concentrations in children with prediabetes is associated with beta-cell function. J Clin Endocrinol Metab 96:E1092–1099

    Article  PubMed Central  PubMed  Google Scholar 

  37. Roodman GD (1993) Role of cytokines in the regulation of bone resorption. Calcif Tissue Int 53(Suppl 1):S94–98

    Article  CAS  PubMed  Google Scholar 

  38. Yamaguchi T, Sugimoto T, Yano S, Yamauchi M, Sowa H, Chen Q, Chilhara K (2002) Plasma lipids and osteoporosis in postmenopausal women. Endocr J 49:211–217

    Article  CAS  PubMed  Google Scholar 

  39. Shin D, Kim S, Kim KH, Lee K, Park SM (2014) Association between insulin resistance and bone mass in men. J Clin Endocrinol Metab 99:988–995

    CAS  PubMed  Google Scholar 

  40. Brownbill RA, Ilich JZ (2006) Lipid profile and bone paradox: higher serum lipids are associated with higher bone mineral density in postmenopausal women. J Womens Health 15:261–270

    Article  CAS  Google Scholar 

  41. Sivas F, Alemdaroglu E, Elverici E, Kuluğ T, Ozoran K (2009) Serum lipid profile: its relationship with osteoporotic vertebrae fractures and bone mineral density in Turkish postmenopausal women. Rheumatol Int 29:885–890

    Article  CAS  PubMed  Google Scholar 

  42. Orozco P (2004) Atherogenic lipid profile and elevated lipoprotein (a) are associated with lower bone mineral density in early postmenopausal overweight women. Eur J Epidemiol 19:1105–1112

    Article  CAS  PubMed  Google Scholar 

  43. Cui LH, Shin MH, Chung EK, Lee YH, Kweon SS, Park KS, Choi JS (2005) Association between bone mineral densities and serum lipid profiles of pre- and post-menopausal rural women in South Korea. Osteoporos Int 16:1975–1981

    Article  CAS  PubMed  Google Scholar 

  44. Kim YH, Nam GE, Cho KH, Choi YS, Kim SM, Han BD, Han KD, Lee KS, Park CH, Kim DH (2013) Low bone mineral density is associated with dyslipidemia in South Korean men: the 2008–2010 Korean National Health and Nutrition Examination Survey. Endocr J 60:1179–1189

    Article  CAS  PubMed  Google Scholar 

  45. Wu LY, Yang TC, Kuo SW, Hsiao CF, Hung YJ, Hsieh HC, Tseng HC, Hsieh AT, Chen TW, Chang JB, Pei D (2003) Correlation between bone mineral density and plasma lipids in Taiwan. Endocr Res 29:317–325

    Article  CAS  PubMed  Google Scholar 

  46. Kuk JL, Lee S, Heymsfield SB, Ross R (2005) Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Epidemiol 144:335–345

    Google Scholar 

  47. Langer C, Gansz B, Goepfert C, Engel T, Uehara Y, von Dehn G, Jansen H, Assmass G, von Eckardstein A (2002) Testosterone up-regulates scavenger receptor BI and stimulates cholesterol efflux from macrophages. Biochem Biophys Res Commun 296:1051–1057

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We sincerely thank the participants of the 2008–2011 Korea National Health and Nutrition Examination Survey.

Funding information

This work was not supported by any funding.

Compliance with ethical guidelines

ᅟ

Conflicts of interest

None

Author information

Author notes

    Authors and Affiliations

    1. Department of Family Medicine, Korea University Ansan Hospital, College of Medicine, Korea University, 516 Gojan-dong, Danwon-gu, Ansan-si, Gyeonggi-do, 425-707, South Korea

      S.-W. Park, G.-E. Nam, D.-W. Jung, S.-J. Yoon, J.-S. Choi, J.-E. Lee, J.-E. Sang, Y.-J. Yoon & D.-H. Kim

    2. Department of Biostatistics, Catholic University College of Medicine, Seoul, 137-701, South Korea

      K. Han & Y.-G. Park

    Authors
    1. S.-W. Park
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. G.-E. Nam
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. D.-W. Jung
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. S.-J. Yoon
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. K. Han
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Y.-G. Park
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. J.-S. Choi
      View author publications

      You can also search for this author in PubMed Google Scholar

    8. J.-E. Lee
      View author publications

      You can also search for this author in PubMed Google Scholar

    9. J.-E. Sang
      View author publications

      You can also search for this author in PubMed Google Scholar

    10. Y.-J. Yoon
      View author publications

      You can also search for this author in PubMed Google Scholar

    11. D.-H. Kim
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to G.-E. Nam or D.-H. Kim.

    Additional information

    G.-E. Nam and D.-H. Kim contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Park, SW., Nam, GE., Jung, DW. et al. Association of lipid parameters and insulin resistance with bone health in South Korean adolescents. Osteoporos Int 27, 635–642 (2016). https://doi.org/10.1007/s00198-015-3306-8

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00198-015-3306-8

    Keywords

    Search

    Navigation