Journal of Bone and Mineral Metabolism

, Volume 31, Issue 5, pp 571–578 | Cite as

The association between bone mineral density and metabolic syndrome: a Korean population-based study

  • Hoon Kim
  • Han Jin Oh
  • Hoon Choi
  • Woong Hwan Choi
  • Sung-Kil Lim
  • Jung Gu Kim
Original Article


This study was conducted to investigate the association between the metabolic syndrome (MS), which includes a cluster of major risk factors for cardiovascular diseases, and bone mineral density (BMD) from a population-based study. This cross-sectional study was based on a nationwide representative survey data from the Korean National Health and Nutrition Examination Survey (KNHANES) 2008. A total of 3,207 subjects were included from the KNHANES 2008 and composed of men (mean age 48.4 years), premenopausal women (mean age 36.5 years) and postmenopausal women (mean age 64.8 years). The MS was identified according to the new criteria from a joint scientific statement endorsed by major organizations including the National Heart, Lung, and Blood Institute. The mean age of study participants was significantly different according to MS status (58.2 years in the MS group vs. 45.7 years in the non-MS group, P < 0.001). The association between MS and BMD at the lumbar spine and proximal femur was analyzed with adjustment for potential confounders. Although the adjusted BMD at all skeletal sites was not significantly different between participants with and without MS, an increased number of MS components was associated with low adjusted femoral neck (FN) BMD only in men (P = 0.01). After adjusting confounding factors, the triglyceride component of MS was related to low FN BMD in men, but to high BMD at all of the skeletal sites measured in postmenopausal women. The glucose component of MS showed an association with high adjusted BMD at total hip in men. Men with MS had significantly higher odds for pooled osteopenia and osteoporosis (odds ratio: 1.49, 95 % confidence interval: 1.04–2.14). In conclusion, low BMD is associated with MS in Korean men, and the association between the MS component and the BMD is different according to gender.


Body mass index Bone mineral density Menopause Metabolic syndrome 


Conflict of interest



  1. 1.
    Kanis JA, Johnell O, Oden A, Johansson H, McCloskey E (2008) FRAX and the assessment of fracture probability in men and women from the UK. Osteoporos Int 19:385–397PubMedCrossRefGoogle Scholar
  2. 2.
    Anagnostis P, Karagiannis A, Kakafika AI, Tziomalos K, Athyros VG, Mikhailidis DP (2009) Atherosclerosis and osteoporosis: age-dependent degenerative processes or related entities? Osteoporos Int 20:197–207PubMedCrossRefGoogle Scholar
  3. 3.
    Farhat GN, Cauley JA (2008) The link between osteoporosis and cardiovascular disease. Clin Cases Miner Bone Metab 5:19–34PubMedGoogle Scholar
  4. 4.
    Yudkin JS, Stehouwer CD, Emeis JJ, Coppack SW (1999) C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 19:972–978PubMedCrossRefGoogle Scholar
  5. 5.
    Roodman GD (1993) Role of cytokines in the regulation of bone resorption. Calcif Tissue Int 53:S94–S98PubMedCrossRefGoogle Scholar
  6. 6.
    Choi SH, An JH, Lim S, Koo BK, Park SE, Chang HJ, Choi SI, Park YJ, Park KS, Jang HC, Shin CS (2009) Lower bone mineral density is associated with higher coronary calcification and coronary plaque burdens by multidetector row coronary computed tomography in pre- and postmenopausal women. Clin Endocrinol (Oxf) 71:644–651CrossRefGoogle Scholar
  7. 7.
    Collins TC, Ewing SK, Diem SJ, Taylor BC, Orwoll ES, Cummings SR, Strotmeyer ES, Ensrud KE (2009) Peripheral arterial disease is associated with higher rates of hip bone loss and increased fracture risk in older men. Circulation 119:2305–2312PubMedCrossRefGoogle Scholar
  8. 8.
    Sumino H, Ichikawa S, Kasama S, Takahashi T, Kumakura H, Takayama Y, Kanda T, Sakamaki T, Kurabayashi M (2006) Elevated arterial stiffness in postmenopausal women with osteoporosis. Maturitas 55:212–218PubMedCrossRefGoogle Scholar
  9. 9.
    Tanko LB, Christiansen C, Cox DA, Geiger MJ, McNabb MA, Cummings SR (2005) Relationship between osteoporosis and cardiovascular disease in postmenopausal women. J Bone Miner Res 20:1912–1920PubMedCrossRefGoogle Scholar
  10. 10.
    Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, Donato KA, Fruchart JC, James WP, Loria CM, Smith SC Jr (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120:1640–1645PubMedCrossRefGoogle Scholar
  11. 11.
    Eckel RH, Alberti KG, Grundy SM, Zimmet PZ (2010) The metabolic syndrome. Lancet 375:181–183PubMedCrossRefGoogle Scholar
  12. 12.
    Hernandez JL, Olmos JM, Pariente E, Martinez J, Valero C, Garcia-Velasco P, Nan D, Llorca J, Gonzalez-Macias J (2010) Metabolic syndrome and bone metabolism: the Camargo Cohort study. Menopause 17:955–961PubMedCrossRefGoogle Scholar
  13. 13.
    Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431PubMedCrossRefGoogle Scholar
  14. 14.
    Jeon YK, Lee JG, Kim SS, Kim BH, Kim SJ, Kim YK, Kim IJ (2011) Association between bone mineral density and metabolic syndrome in pre- and postmenopausal women. Endocr J 58:87–93PubMedCrossRefGoogle Scholar
  15. 15.
    Kim HY, Choe JW, Kim HK, Bae SJ, Kim BJ, Lee SH, Koh JM, Han KO, Park HM, Kim GS (2010) Negative association between metabolic syndrome and bone mineral density in Koreans, especially in men. Calcif Tissue Int 86:350–358PubMedCrossRefGoogle Scholar
  16. 16.
    Kinjo M, Setoguchi S, Solomon DH (2007) Bone mineral density in adults with the metabolic syndrome: analysis in a population-based U.S. sample. J Clin Endocrinol Metab 92:4161–4164PubMedCrossRefGoogle Scholar
  17. 17.
    von Muhlen D, Safii S, Jassal SK, Svartberg J, Barrett-Connor E (2007) Associations between the metabolic syndrome and bone health in older men and women: the Rancho Bernardo Study. Osteoporos Int 18:1337–1344CrossRefGoogle Scholar
  18. 18.
    Choi HS, Oh HJ, Choi H, Choi WH, Kim JG, Kim KM, Kim KJ, Rhee Y, Lim SK (2011) Vitamin D insufficiency in Korea—a greater threat to younger generation: the Korea National Health and Nutrition Examination Survey (KNHANES) 2008. J Clin Endocrinol Metab 96:643–651PubMedCrossRefGoogle Scholar
  19. 19.
    Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366:1059–1062PubMedCrossRefGoogle Scholar
  20. 20.
    Kanis JA, Melton LJ 3rd, Christiansen C, Johnston CC, Khaltaev N (1994) The diagnosis of osteoporosis. J Bone Miner Res 9:1137–1141PubMedCrossRefGoogle Scholar
  21. 21.
    Johnell O, Kanis JA, Oden A, Johansson H, De Laet C, Delmas P, Eisman JA, Fujiwara S, Kroger H, Mellstrom D, Meunier PJ, Melton LJ 3rd, O’Neill T, Pols H, Reeve J, Silman A, Tenenhouse A (2005) Predictive value of BMD for hip and other fractures. J Bone Miner Res 20:1185–1194PubMedCrossRefGoogle Scholar
  22. 22.
    Kanis JA, Johansson H, Johnell O, Oden A, De Laet C, Eisman JA, Pols H, Tenenhouse A (2005) Alcohol intake as a risk factor for fracture. Osteoporos Int 16:737–742PubMedCrossRefGoogle Scholar
  23. 23.
    Kanis JA, Johansson H, Oden A, Johnell O, De Laet C, Eisman JA, McCloskey EV, Mellstrom D, Melton LJ 3rd, Pols HA, Reeve J, Silman AJ, Tenenhouse A (2004) A family history of fracture and fracture risk: a meta-analysis. Bone 35:1029–1037PubMedCrossRefGoogle Scholar
  24. 24.
    Kanis JA, Johnell O, Oden A, Johansson H, De Laet C, Eisman JA, Fujiwara S, Kroger H, McCloskey EV, Mellstrom D, Melton LJ, Pols H, Reeve J, Silman A, Tenenhouse A (2005) Smoking and fracture risk: a meta-analysis. Osteoporos Int 16:155–162PubMedCrossRefGoogle Scholar
  25. 25.
    Barrett-Connor E, Goodman-Gruen D (1998) Gender differences in insulin-like growth factor and bone mineral density association in old age: the Rancho Bernardo Study. J Bone Miner Res 13:1343–1349PubMedCrossRefGoogle Scholar
  26. 26.
    Krall EA, Dawson-Hughes B, Hirst K, Gallagher JC, Sherman SS, Dalsky G (1997) Bone mineral density and biochemical markers of bone turnover in healthy elderly men and women. J Gerontol A Biol Sci Med Sci 52:M61–M67PubMedCrossRefGoogle Scholar
  27. 27.
    Makovey J, Naganathan V, Sambrook P (2005) Gender differences in relationships between body composition components, their distribution and bone mineral density: a cross-sectional opposite sex twin study. Osteoporos Int 16:1495–1505PubMedCrossRefGoogle Scholar
  28. 28.
    Hernandez JL, Olmos JM, Gonzalez-Macias J (2011) Metabolic syndrome, fractures and gender. Maturitas 68:217–223PubMedCrossRefGoogle Scholar
  29. 29.
    Akune T, Ohba S, Kamekura S, Yamaguchi M, Chung UI, Kubota N, Terauchi Y, Harada Y, Azuma Y, Nakamura K, Kadowaki T, Kawaguchi H (2004) PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest 113:846–855PubMedGoogle Scholar
  30. 30.
    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 16:1975–1981PubMedCrossRefGoogle Scholar
  31. 31.
    Meier CR, Schlienger RG, Kraenzlin ME, Schlegel B, Jick H (2000) HMG-CoA reductase inhibitors and the risk of fractures. JAMA 283:3205–3210PubMedCrossRefGoogle Scholar
  32. 32.
    Wang PS, Solomon DH, Mogun H, Avorn J (2000) HMG-CoA reductase inhibitors and the risk of hip fractures in elderly patients. JAMA 283:3211–3216PubMedCrossRefGoogle Scholar
  33. 33.
    Tintut Y, Morony S, Demer LL (2004) Hyperlipidemia promotes osteoclastic potential of bone marrow cells ex vivo. Arterioscler Thromb Vasc Biol 24:e6–e10PubMedCrossRefGoogle Scholar
  34. 34.
    Niemeier A, Niedzielska D, Secer R, Schilling A, Merkel M, Enrich C, Rensen PC, Heeren J (2008) Uptake of postprandial lipoproteins into bone in vivo: impact on osteoblast function. Bone 43:230–237PubMedCrossRefGoogle Scholar
  35. 35.
    Kao WH, Kammerer CM, Schneider JL, Bauer RL, Mitchell BD (2003) Type 2 diabetes is associated with increased bone mineral density in Mexican–American women. Arch Med Res 34:399–406PubMedCrossRefGoogle Scholar
  36. 36.
    Abrahamsen B, Rohold A, Henriksen JE, Beck-Nielsen H (2000) Correlations between insulin sensitivity and bone mineral density in non-diabetic men. Diabet Med 17:124–129PubMedCrossRefGoogle Scholar
  37. 37.
    Barrett-Connor E, Kritz-Silverstein D (1996) Does hyperinsulinemia preserve bone? Diabetes Care 19:1388–1392PubMedCrossRefGoogle Scholar
  38. 38.
    Ahmed LA, Schirmer H, Berntsen GK, Fonnebo V, Joakimsen RM (2006) Features of the metabolic syndrome and the risk of non-vertebral fractures: the Tromso study. Osteoporos Int 17:426–432PubMedCrossRefGoogle Scholar

Copyright information

© The Japanese Society for Bone and Mineral Research and Springer Japan 2013

Authors and Affiliations

  • Hoon Kim
    • 1
  • Han Jin Oh
    • 2
  • Hoon Choi
    • 3
  • Woong Hwan Choi
    • 4
  • Sung-Kil Lim
    • 5
  • Jung Gu Kim
    • 1
  1. 1.Department of Obstetrics and GynecologySeoul National University College of MedicineSeoulKorea
  2. 2.Department of Family MedicineCollege of Medicine, Kwandong UniversityGangneungKorea
  3. 3.Department of Obstetrics and GynecologyInje University Sanggye Paik HospitalSeoulKorea
  4. 4.Department of Internal MedicineCollege of Medicine, Hanyang UniversitySeoulKorea
  5. 5.Department of Internal MedicineYonsei University College of MedicineSeoulKorea

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