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

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Abstract

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.

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References

  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 89:4246–4253

    Article  CAS  PubMed  Google Scholar 

  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 159:589–595

    Article  PubMed  Google Scholar 

  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 20:1912–1920

    Article  PubMed  Google Scholar 

  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 24:2023–2031

    Article  CAS  PubMed  Google Scholar 

  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 87:666–674

    Article  CAS  PubMed  Google Scholar 

  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 91:3908–3915

    Article  CAS  PubMed  Google Scholar 

  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 93:1952–1958

    Article  CAS  PubMed  Google Scholar 

  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 282:27285–27297

    Article  CAS  PubMed  Google Scholar 

  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 92:4161–4164

    Article  CAS  PubMed  Google Scholar 

  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 17:426–432

    Article  CAS  PubMed  Google Scholar 

  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 18:1337–1344

    Article  Google Scholar 

  12. Hwang DK, Choi HJ (2010) The relationship between low bone mass and metabolic syndrome in Korean women. Osteoporos Int 21:425–431

    Article  PubMed  Google Scholar 

  13. Fujimoto WY (1996) Overview of non-insulin-dependent diabetes mellitus (NIDDM) in different population groups. Diabet Med 13:S7–S10

    Article  CAS  PubMed  Google Scholar 

  14. Abate N, Chandalia M (2003) The impact of ethnicity on type 2 diabetes. J Diabetes Complications 17:39–58

    Article  PubMed  Google Scholar 

  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 112:2735–2752

    Article  PubMed  Google Scholar 

  16. Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366:1059–1062

    Article  PubMed  Google Scholar 

  17. Jukka AS (2003) Body composition assessment with segmental multifrequency bioimpedance method. J Sports Sci Med 2(suppl 3):1–29

    Google Scholar 

  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 30:380–391

    Article  CAS  PubMed  Google Scholar 

  19. Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW (2007) Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 92:1640–1646

    Article  CAS  PubMed  Google Scholar 

  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 83:146–154

    CAS  PubMed  Google Scholar 

  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–E751

    CAS  PubMed  Google Scholar 

  22. Berg AH, Scherer PE (2005) Adipose tissue, inflammation, and cardiovascular disease. Circ Res 96:939–949

    Article  CAS  PubMed  Google Scholar 

  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 257:88–91

    Article  CAS  PubMed  Google Scholar 

  24. Manolagas SC, Jilka RL (1995) Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med 332:305–311

    Article  CAS  PubMed  Google Scholar 

  25. Nanes MS (2003) Tumor necrosis factor-alpha: molecular and cellular mechanisms in skeletal pathology. Gene 321:1–15

    Article  CAS  PubMed  Google Scholar 

  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 319:516–518

    Article  CAS  PubMed  Google Scholar 

  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 63:466–470

    Article  CAS  PubMed  Google Scholar 

  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 77:1648–1653

    Article  CAS  PubMed  Google Scholar 

  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 86:2032–2042

    Article  CAS  PubMed  Google Scholar 

  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 81:1330–1334

    CAS  PubMed  Google Scholar 

  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 144:335–345

    CAS  PubMed  Google Scholar 

  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 58:463–467

    CAS  PubMed  Google Scholar 

  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 33:384–389

    Article  CAS  PubMed  Google Scholar 

  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 25:165–171

    Article  PubMed  Google Scholar 

  35. Blaauw R, Albertse EC, Hough S (1996) Body fat distribution as a risk factor for osteoporosis. S Afr Med J 86:1081–1084

    CAS  PubMed  Google Scholar 

  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 18:784–790

    Article  CAS  PubMed  Google Scholar 

  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 44:739–746

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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).

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Correspondence to Jae Won Choe.

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Kim, H.Y., Choe, J.W., Kim, H.K. et al. Negative Association between Metabolic Syndrome and Bone Mineral Density in Koreans, Especially in Men. Calcif Tissue Int 86, 350–358 (2010). https://doi.org/10.1007/s00223-010-9347-2

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  • DOI: https://doi.org/10.1007/s00223-010-9347-2

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