Calcified Tissue International

, Volume 86, Issue 5, pp 350–358 | Cite as

Negative Association between Metabolic Syndrome and Bone Mineral Density in Koreans, Especially in Men

  • Ha Young Kim
  • Jae Won ChoeEmail author
  • Hong Kyu Kim
  • Sung Jin Bae
  • Beom Jun Kim
  • Seung Hun Lee
  • Jung-Min Koh
  • Ki Ok Han
  • Hyoung Moo Park
  • Ghi Su Kim


Cardiovascular disease and osteoporosis are thought to share common risk factors, and metabolic syndrome (MS) is composed of major risk factors for cardiovascular disease. This study was performed to investigate the relationships between specific MS components and bone mineral density (BMD). BMD was measured at the femoral neck of Korean men aged 40 years or more (n = 1,780) and postmenopausal women (n = 1,108) using dual-energy X-ray absorptiometry. We identified subjects with MS as defined by two criteria, International Diabetes Federation (IDF) and American Heart Association/National Heart, Lung, and Blood Institute (AHA/NHLBI). Body fat and lean mass were measured via bioimpedance analysis. The prevalence of MS was 19.8% and 7.7% in men and 20.8% and 11.6% in postmenopausal women according to the AHA/NHLBI definition and the IDF definition, respectively. After multivariate adjustment, femoral neck BMD was significantly lower in subjects with MS regardless of diagnostic criteria. BMD decreased as the number of MS components increased (P < 0.001 for trends in both sexes). Among MS components, waist circumference was the most important factor in this negative association. When multiple linear regression models were applied to each 5-kg weight stratum to test for a linear trend, waist circumference and fat mass were negatively associated with BMD and lean mass was positively associated with BMD in men but not in women. MS was associated with a lower BMD in Korean men and postmenopausal women, suggesting that visceral fat may lead to bone loss, especially in men.


Bone mineral density Metabolic syndrome Visceral fat 



This work was supported by funding from Novartis as well as grants from the Korea Healthcare Technology R&D Project and the Ministry for Health, Welfare, and Family Affairs, Republic of Korea (project A080256).


  1. 1.
    Schulz E, Arfai K, Liu X, Sayre J, Gilsanz V (2004) Aortic calcification and the risk of osteoporosis and fractures. J Clin Endocrinol Metab 89:4246–4253CrossRefPubMedGoogle Scholar
  2. 2.
    Samelson EJ, Kiel DP, Broe KE, Zhang Y, Cupples LA, Hannan MT, Wilson PW, Levy D, Williams SA, Vaccarino V (2004) Metacarpal cortical area and risk of coronary heart disease: the Framingham Study. Am J Epidemiol 159:589–595CrossRefPubMedGoogle Scholar
  3. 3.
    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 20:1912–1920CrossRefPubMedGoogle Scholar
  4. 4.
    Szulc P, Samelson EJ, Kiel DP, Delmas PD (2009) Increased bone resorption is associated with increased risk of cardiovascular events in men—the MINOS Study. J Bone Miner Res 24:2023–2031CrossRefPubMedGoogle Scholar
  5. 5.
    Szulc P, Garnero P, Claustrat B, Marchand F, Duboeuf F, Delmas PD (2002) Increased bone resorption in moderate smokers with low body weight: the Minos study. J Clin Endocrinol Metab 87:666–674CrossRefPubMedGoogle Scholar
  6. 6.
    Fink HA, Ewing SK, Ensrud KE, Barrett-Connor E, Taylor BC, Cauley JA, Orwoll ES (2006) Association of testosterone and estradiol deficiency with osteoporosis and rapid bone loss in older men. J Clin Endocrinol Metab 91:3908–3915CrossRefPubMedGoogle Scholar
  7. 7.
    Ding C, Parameswaran V, Udayan R, Burgess J, Jones G (2008) Circulating levels of inflammatory markers predict change in bone mineral density and resorption in older adults: a longitudinal study. J Clin Endocrinol Metab 93:1952–1958CrossRefPubMedGoogle Scholar
  8. 8.
    Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK, Kousteni S, O’Brien CA, Bellido T, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282:27285–27297CrossRefPubMedGoogle Scholar
  9. 9.
    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 92:4161–4164CrossRefPubMedGoogle Scholar
  10. 10.
    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 17:426–432CrossRefPubMedGoogle Scholar
  11. 11.
    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
  12. 12.
    Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431CrossRefPubMedGoogle Scholar
  13. 13.
    Fujimoto WY (1996) Overview of non-insulin-dependent diabetes mellitus (NIDDM) in different population groups. Diabet Med 13:S7–S10CrossRefPubMedGoogle Scholar
  14. 14.
    Abate N, Chandalia M (2003) The impact of ethnicity on type 2 diabetes. J Diabetes Complications 17:39–58CrossRefPubMedGoogle Scholar
  15. 15.
    Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC Jr, Spertus JA, Costa F (2005) Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation 112:2735–2752CrossRefPubMedGoogle Scholar
  16. 16.
    Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366:1059–1062CrossRefPubMedGoogle Scholar
  17. 17.
    Jukka AS (2003) Body composition assessment with segmental multifrequency bioimpedance method. J Sports Sci Med 2(suppl 3):1–29Google Scholar
  18. 18.
    Malavolti M, Mussi C, Poli M, Fantuzzi AL, Salvioli G, Battistini N, Bedogni G (2003) Cross-calibration of eight-polar bioelectrical impedance analysis versus dual-energy X-ray absorptiometry for the assessment of total and appendicular body composition in healthy subjects aged 21–82 years. Ann Hum Biol 30:380–391CrossRefPubMedGoogle Scholar
  19. 19.
    Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW (2007) Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 92:1640–1646CrossRefPubMedGoogle Scholar
  20. 20.
    Hsu YH, Venners SA, Terwedow HA, Feng Y, Niu T, Li Z, Laird N, Brain JD, Cummings SR, Bouxsein ML, Rosen CJ, Xu X (2006) Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr 83:146–154PubMedGoogle Scholar
  21. 21.
    Kern PA, Ranganathan S, Li C, Wood L, Ranganathan G (2001) Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab 280:E745–E751PubMedGoogle Scholar
  22. 22.
    Berg AH, Scherer PE (2005) Adipose tissue, inflammation, and cardiovascular disease. Circ Res 96:939–949CrossRefPubMedGoogle Scholar
  23. 23.
    Jilka RL, Hangoc G, Girasole G, Passeri G, Williams DC, Abrams JS, Boyce B, Broxmeyer H, Manolagas SC (1992) Increased osteoclast development after estrogen loss: mediation by interleukin-6. Science 257:88–91CrossRefPubMedGoogle Scholar
  24. 24.
    Manolagas SC, Jilka RL (1995) Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med 332:305–311CrossRefPubMedGoogle Scholar
  25. 25.
    Nanes MS (2003) Tumor necrosis factor-alpha: molecular and cellular mechanisms in skeletal pathology. Gene 321:1–15CrossRefPubMedGoogle Scholar
  26. 26.
    Bertolini DR, Nedwin GE, Bringman TS, Smith DD, Mundy GR (1986) Stimulation of bone resorption and inhibition of bone formation in vitro by human tumour necrosis factors. Nature 319:516–518CrossRefPubMedGoogle Scholar
  27. 27.
    Salamone LM, Whiteside T, Friberg D, Epstein RS, Kuller LH, Cauley JA (1998) Cytokine production and bone mineral density at the lumbar spine and femoral neck in premenopausal women. Calcif Tissue Int 63:466–470CrossRefPubMedGoogle Scholar
  28. 28.
    Cohen-Solal ME, Graulet AM, Denne MA, Gueris J, Baylink D, de Vernejoul MC (1993) Peripheral monocyte culture supernatants of menopausal women can induce bone resorption: involvement of cytokines. J Clin Endocrinol Metab 77:1648–1653CrossRefPubMedGoogle Scholar
  29. 29.
    Scheidt-Nave C, Bismar H, Leidig-Bruckner G, Woitge H, Seibel MJ, Ziegler R, Pfeilschifter J (2001) Serum interleukin 6 is a major predictor of bone loss in women specific to the first decade past menopause. J Clin Endocrinol Metab 86:2032–2042CrossRefPubMedGoogle Scholar
  30. 30.
    Kuk JL, Lee S, Heymsfield SB, Ross R (2005) Waist circumference and abdominal adipose tissue distribution: influence of age and sex. Am J Clin Nutr 81:1330–1334PubMedGoogle Scholar
  31. 31.
    Schreiner PJ, Terry JG, Evans GW, Hinson WH, Crouse JR 3rd, Heiss G (1996) Sex-specific associations of magnetic resonance imaging-derived intra-abdominal and subcutaneous fat areas with conventional anthropometric indices. The Atherosclerosis Risk in Communities Study. Am J Epidemiol 144:335–345PubMedGoogle Scholar
  32. 32.
    Lemieux S, Prud’homme D, Bouchard C, Tremblay A, Despres JP (1993) Sex differences in the relation of visceral adipose tissue accumulation to total body fatness. Am J Clin Nutr 58:463–467PubMedGoogle Scholar
  33. 33.
    Jankowska EA, Rogucka E, Medras M (2001) Are general obesity and visceral adiposity in men linked to reduced bone mineral content resulting from normal ageing? A population-based study. Andrologia 33:384–389CrossRefPubMedGoogle Scholar
  34. 34.
    Cui LH, Shin MH, Kweon SS, Park KS, Lee YH, Chung EK, Nam HS, Choi JS (2007) Relative contribution of body composition to bone mineral density at different sites in men and women of South Korea. J Bone Miner Metab 25:165–171CrossRefPubMedGoogle Scholar
  35. 35.
    Blaauw R, Albertse EC, Hough S (1996) Body fat distribution as a risk factor for osteoporosis. S Afr Med J 86:1081–1084PubMedGoogle Scholar
  36. 36.
    Hanley DA, Brown JP, Tenenhouse A, Olszynski WP, Ioannidis G, Berger C, Prior JC, Pickard L, Murray TM, Anastassiades T, Kirkland S, Joyce C, Joseph L, Papaioannou A, Jackson SA, Poliquin S, Adachi JD (2003) Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: cross-sectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res 18:784–790CrossRefPubMedGoogle Scholar
  37. 37.
    Enzi G, Gasparo M, Biondetti PR, Fiore D, Semisa M, Zurlo F (1986) Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr 44:739–746PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Ha Young Kim
    • 1
  • Jae Won Choe
    • 2
    Email author
  • Hong Kyu Kim
    • 2
  • Sung Jin Bae
    • 2
  • Beom Jun Kim
    • 3
  • Seung Hun Lee
    • 3
  • Jung-Min Koh
    • 3
  • Ki Ok Han
    • 4
  • Hyoung Moo Park
    • 5
  • Ghi Su Kim
    • 3
  1. 1.Division of Endocrinology and MetabolismUniversity of Wonkwang College of Medicine, Sanbon Medical CenterGunpoKorea
  2. 2.Health Promotion CenterUniversity of Ulsan College of Medicine, Asan Medical CenterSeoulKorea
  3. 3.Division of Endocrinology and MetabolismUniversity of Ulsan College of Medicine, Asan Medical CenterSeoulKorea
  4. 4.Department of MedicineUniversity of Kwandong College of Medicine, Cheil General Hospital and Women’s Healthcare CenterSeoulKorea
  5. 5.Department of Obstetrics and GynecologyUniversity of Chung-Ang College of MedicineSeoulKorea

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