Advertisement

Calcified Tissue International

, Volume 87, Issue 3, pp 218–225 | Cite as

Relationship Between Visceral Adiposity and Bone Mineral Density in Korean Adults

  • Han Seok Choi
  • Kwang Joon Kim
  • Kyoung Min Kim
  • Nam Wook Hur
  • Yumie Rhee
  • Dae Suk Han
  • Eun Jig Lee
  • Sung-Kil LimEmail author
Article

Abstract

The objective of the study was to investigate the relationship between visceral and subcutaneous adiposity measured by computed tomography and bone mineral density (BMD) and to identify the metabolic factors associated with BMD. We studied 461 subjects recruited from the health-care center at Severance Hospital, Yonsei University College of Medicine. Multivariate regression analyses were conducted to examine the cross-sectional associations between body composition-related or metabolic parameters and BMD. After adjusting for body weight and other confounders, visceral fat area had an inverse association with BMD in men (β = −0.133, P = 0.049 for lumbar spine; β = −0.135, P = 0.037 for femoral neck; β = −0.179, P = 0.005 for total hip) and women (β = −0.424, P < 0.001 for lumbar spine; β = −0.302, P = 0.005 for femoral neck; β = −0.274, P = 0.014 for total hip). However, the subcutaneous fat area showed no statistically significant relationship with BMD at most sites. Among the metabolic parameters, HDL cholesterol was positively associated with BMD, while LDL cholesterol was negatively associated with BMD in men. In women, total and LDL cholesterol were negatively associated with BMD at the lumbar spine. We conclude that visceral adiposity is inversely associated with BMD after adjusting for confounders and that metabolic factors may partly contribute to this inverse relation.

Keywords

Obesity Bone mineral density Visceral adiposity Subcutaneous adiposity Metabolic factor 

Notes

Acknowledgements

This work was supported by a Science Research Center grant to the Bone Metabolism Research Center (2009-0063265) funded by the Korean Ministry of Education, Science and Technology. This work was also supported by the Brain Korea 21 Project for Medical Science, Yonsei University. We thank Dane Grace for editing the manuscript.

References

  1. 1.
    Wardlaw GM (1996) Putting body weight and osteoporosis into perspective. Am J Clin Nutr 63:433S–436SPubMedGoogle Scholar
  2. 2.
    Edelstein SL, Barrett-Connor E (1993) Relation between body size and bone mineral density in elderly men and women. Am J Epidemiol 138:160–169PubMedGoogle Scholar
  3. 3.
    Kameda T, Mano H, Yuasa T, Mori Y, Miyazawa K, Shiokawa M, Nakamaru Y, Hiroi E, Hiura K, Kameda A, Yang NN, Hakeda Y, Kumegawa M (1997) Estrogen inhibits bone resorption by directly inducing apoptosis of the bone-resorbing osteoclasts. J Exp Med 186:489–495CrossRefPubMedGoogle Scholar
  4. 4.
    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
  5. 5.
    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
  6. 6.
    Zhao LJ, Jiang H, Papasian CJ, Maulik D, Drees B, Hamilton J, Deng HW (2008) Correlation of obesity and osteoporosis: effect of fat mass on the determination of osteoporosis. J Bone Miner Res 23:17–29CrossRefPubMedGoogle Scholar
  7. 7.
    Wajchenberg BL (2000) Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev 21:697–738CrossRefPubMedGoogle Scholar
  8. 8.
    Heiss CJ, Sanborn CF, Nichols DL, Bonnick SL, Alford BB (1995) Associations of body fat distribution, circulating sex hormones, and bone density in postmenopausal women. J Clin Endocrinol Metab 80:1591–1596CrossRefPubMedGoogle Scholar
  9. 9.
    Blaauw R, Albertse EC, Hough S (1996) Body fat distribution as a risk factor for osteoporosis. S Afr Med J 86:1081–1084PubMedGoogle Scholar
  10. 10.
    Douchi T, Yamamoto S, Oki T, Maruta K, Kuwahata R, Nagata Y (2000) Relationship between body fat distribution and bone mineral density in premenopausal Japanese women. Obstet Gynecol 95:722–725CrossRefPubMedGoogle Scholar
  11. 11.
    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
  12. 12.
    Warming L, Ravn P, Christiansen C (2003) Visceral fat is more important than peripheral fat for endometrial thickness and bone mass in healthy postmenopausal women. Am J Obstet Gynecol 188:349–353CrossRefPubMedGoogle Scholar
  13. 13.
    Bonora E, Micciolo R, Ghiatas AA, Lancaster JL, Alyassin A, Muggeo M, DeFronzo RA (1995) Is it possible to derive a reliable estimate of human visceral and subcutaneous abdominal adipose tissue from simple anthropometric measurements? Metabolism 44:1617–1625Google Scholar
  14. 14.
    Clasey JL, Bouchard C, Teates CD, Riblett JE, Thorner MO, Hartman ML, Weltman A (1999) The use of anthropometric and dual-energy X-ray absorptiometry (DXA) measures to estimate total abdominal and abdominal visceral fat in men and women. Obes Res 7:256–264PubMedGoogle Scholar
  15. 15.
    Snijder MB, Visser M, Dekker JM, Seidell JC, Fuerst T, Tylavsky F, Cauley J, Lang T, Nevitt M, Harris TB (2002) The prediction of visceral fat by dual-energy X-ray absorptiometry in the elderly: a comparison with computed tomography and anthropometry. Int J Obes Relat Metab Disord 26:984–993CrossRefPubMedGoogle Scholar
  16. 16.
    Lukaski HC, Bolonchuk WW, Hall CB, Siders WA (1986) Validation of tetrapolar bioelectrical impedance method to assess human body composition. J Appl Physiol 60:1327–1332PubMedGoogle Scholar
  17. 17.
    Maurin AC, Chavassieux PM, Frappart L, Delmas PD, Serre CM, Meunier PJ (2000) Influence of mature adipocytes on osteoblast proliferation in human primary cocultures. Bone 26:485–489CrossRefPubMedGoogle Scholar
  18. 18.
    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
  19. 19.
    Krishnan V, Bryant HU, Macdougald OA (2006) Regulation of bone mass by Wnt signaling. J Clin Invest 116:1202–1209CrossRefPubMedGoogle Scholar
  20. 20.
    Yamaguchi T, Sugimoto T, Yano S, Yamauchi M, Sowa H, Chen Q, Chihara K (2002) Plasma lipids and osteoporosis in postmenopausal women. Endocr J 49:211–217CrossRefPubMedGoogle Scholar
  21. 21.
    Parhami F, Morrow AD, Balucan J, Leitinger N, Watson AD, Tintut Y, Berliner JA, Demer LL (1997) Lipid oxidation products have opposite effects on calcifying vascular cell and bone cell differentiation. A possible explanation for the paradox of arterial calcification in osteoporotic patients. Arterioscler Thromb Vasc Biol 17:680–687PubMedGoogle Scholar
  22. 22.
    Vashishth D, Gibson GJ, Khoury JI, Schaffler MB, Kimura J, Fyhrie DP (2001) Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone 28:195–201CrossRefPubMedGoogle Scholar
  23. 23.
    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
  24. 24.
    Zillikens MC, Uitterlinden AG, van Leeuwen JP, Berends AL, Henneman P, van Dijk KW, Oostra BA, van Duijn CM, Pols HA, Rivadeneira F (2010) The role of body mass index, insulin, and adiponectin in the relation between fat distribution and bone mineral density. Calcif Tissue Int 86:116–125CrossRefPubMedGoogle Scholar
  25. 25.
    Russell M, Mendes N, Miller KK, Rosen CJ, Lee H, Klibanski A, Misra M (2010) Visceral fat is a negative predictor of bone density measures in obese adolescent girls. J Clin Endocrinol Metab 95:1247–1255CrossRefPubMedGoogle Scholar
  26. 26.
    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 74:136–142CrossRefPubMedGoogle Scholar
  27. 27.
    Feig DI, Kang DH, Johnson RJ (2008) Uric acid and cardiovascular risk. N Engl J Med 359:1811–1821CrossRefPubMedGoogle Scholar
  28. 28.
    Fang J, Alderman MH (2000) Serum uric acid and cardiovascular mortality the NHANES I epidemiologic follow-up study, 1971–1992. National Health and Nutrition Examination Survey. JAMA 283:2404–2410CrossRefPubMedGoogle Scholar
  29. 29.
    Nieto FJ, Iribarren C, Gross MD, Comstock GW, Cutler RG (2000) Uric acid and serum antioxidant capacity: a reaction to atherosclerosis? Atherosclerosis 148:131–139Google Scholar
  30. 30.
    McTernan PG, Anderson LA, Anwar AJ, Eggo MC, Crocker J, Barnett AH, Stewart PM, Kumar S (2002) Glucocorticoid regulation of p450 aromatase activity in human adipose tissue: gender and site differences. J Clin Endocrinol Metab 87:1327–1336CrossRefPubMedGoogle Scholar
  31. 31.
    Zhao H, Tian Z, Hao J, Chen B (2005) Extragonadal aromatization increases with time after ovariectomy in rats. Reprod Biol Endocrinol 3:6CrossRefPubMedGoogle Scholar
  32. 32.
    Chiodini I, Tauchmanova L, Torlontano M, Battista C, Guglielmi G, Cammisa M, Colao A, Carnevale V, Rossi R, Di Lembo S, Trischitta V, Scillitani A (2002) Bone involvement in eugonadal male patients with adrenal incidentaloma and subclinical hypercortisolism. J Clin Endocrinol Metab 87:5491–5494CrossRefPubMedGoogle Scholar
  33. 33.
    Peeke PM, Chrousos GP (1995) Hypercortisolism and obesity. Ann N Y Acad Sci 771:665–676CrossRefPubMedGoogle Scholar
  34. 34.
    Hypponen E, Boucher BJ, Berry DJ, Power C (2008) 25-Hydroxyvitamin D, IGF-1, and metabolic syndrome at 45 years of age: a cross-sectional study in the 1958 British birth cohort. Diabetes 57:298–305CrossRefPubMedGoogle Scholar
  35. 35.
    Lu L, Yu Z, Pan A, Hu FB, Franco OH, Li H, Li X, Yang X, Chen Y, Lin X (2009) Plasma 25-hydroxyvitamin D concentration and metabolic syndrome among middle-aged and elderly Chinese individuals. Diabetes Care 32:1278–1283CrossRefPubMedGoogle Scholar
  36. 36.
    Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G (2000) Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 100:197–207CrossRefPubMedGoogle Scholar
  37. 37.
    Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, Armstrong D, Ducy P, Karsenty G (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111:305–317CrossRefPubMedGoogle Scholar
  38. 38.
    Burguera B, Hofbauer LC, Thomas T, Gori F, Evans GL, Khosla S, Riggs BL, Turner RT (2001) Leptin reduces ovariectomy-induced bone loss in rats. Endocrinology 142:3546–3553CrossRefPubMedGoogle Scholar
  39. 39.
    Shinoda Y, Yamaguchi M, Ogata N, Akune T, Kubota N, Yamauchi T, Terauchi Y, Kadowaki T, Takeuchi Y, Fukumoto S, Ikeda T, Hoshi K, Chung UI, Nakamura K, Kawaguchi H (2006) Regulation of bone formation by adiponectin through autocrine/paracrine and endocrine pathways. J Cell Biochem 99:196–208CrossRefPubMedGoogle Scholar
  40. 40.
    Yamauchi M, Sugimoto T, Yamaguchi T, Nakaoka D, Kanzawa M, Yano S, Ozuru R, Sugishita T, Chihara K (2001) Plasma leptin concentrations are associated with bone mineral density and the presence of vertebral fractures in postmenopausal women. Clin Endocrinol (Oxf) 55:341–347CrossRefGoogle Scholar
  41. 41.
    Pasco JA, Henry MJ, Kotowicz MA, Collier GR, Ball MJ, Ugoni AM, Nicholson GC (2001) Serum leptin levels are associated with bone mass in nonobese women. J Clin Endocrinol Metab 86:1884–1887CrossRefPubMedGoogle Scholar
  42. 42.
    Lenchik L, Register TC, Hsu FC, Lohman K, Nicklas BJ, Freedman BI, Langefeld CD, Carr JJ, Bowden DW (2003) Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone 33:646–651CrossRefPubMedGoogle Scholar
  43. 43.
    Araneta MR, von Mühlen D, Barrett-Connor E (2009) Sex differences in the association between adiponectin and BMD, bone loss, and fractures: the Rancho Bernardo study. J Bone Miner Res 24:2016–2022CrossRefPubMedGoogle Scholar
  44. 44.
    Blum M, Harris SS, Must A, Naumova EN, Phillips SM, Rand WM, Dawson-Hughes B (2003) Leptin, body composition and bone mineral density in premenopausal women. Calcif Tissue Int 73:27–32CrossRefPubMedGoogle Scholar
  45. 45.
    Kontogianni MD, Dafni UG, Routsias JG, Skopouli FN (2004) Blood leptin and adiponectin as possible mediators of the relation between fat mass and BMD in perimenopausal women. J Bone Miner Res 19:546–551CrossRefPubMedGoogle Scholar
  46. 46.
    Oh KW, Lee WY, Rhee EJ, Baek KH, Yoon KH, Kang MI, Yun EJ, Park CY, Ihm SH, Choi MG, Yoo HJ, Park SW (2005) The relationship between serum resistin, leptin, adiponectin, ghrelin levels and bone mineral density in middle-aged men. Clin Endocrinol (Oxf) 63:131–138CrossRefGoogle Scholar
  47. 47.
    Gonnelli S, Caffarelli C, Del Santo K, Cadirni A, Guerriero C, Lucani B, Franci B, Nuti R (2008) The relationship of ghrelin and adiponectin with bone mineral density and bone turnover markers in elderly men. Calcif Tissue Int 83:55–60CrossRefPubMedGoogle Scholar
  48. 48.
    Fontana L, Eagon JC, Trujillo ME, Scherer PE, Klein S (2007) Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes 56:1010–1013CrossRefPubMedGoogle Scholar
  49. 49.
    Fuller K, Murphy C, Kirstein B, Fox SW, Chambers TJ (2002) TNFα potently activates osteoclasts, through a direct action independent of and strongly synergistic with RANKL. Endocrinology 143:1108–1118CrossRefPubMedGoogle Scholar
  50. 50.
    White MF (2003) Insulin signaling in health and disease. Science 302:1710–1711CrossRefPubMedGoogle Scholar
  51. 51.
    Nawrocki AR, Scherer PE (2004) The delicate balance between fat and muscle: adipokines in metabolic disease and musculoskeletal inflammation. Curr Opin Pharmacol 4:281–289CrossRefPubMedGoogle Scholar
  52. 52.
    Steppan CM, Wang J, Whiteman EL, Birnbaum MJ, Lazar MA (2005) Activation of SOCS-3 by resistin. Mol Cell Biol 25:1569–1575CrossRefPubMedGoogle Scholar
  53. 53.
    Thrailkill KM, Lumpkin CK Jr, Bunn RC, Kemp SF, Fowlkes JL (2005) Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab 289:E735–E745CrossRefPubMedGoogle Scholar
  54. 54.
    Kawamura N, Kugimiya F, Oshima Y, Ohba S, Ikeda T, Saito T, Shinoda Y, Kawasaki Y, Ogata N, Hoshi K, Akiyama T, Chen WS, Hay N, Tobe K, Kadowaki T, Azuma Y, Tanaka S, Nakamura K, Chung UI, Kawaguchi H (2007) Akt1 in osteoblasts and osteoclasts controls bone remodeling. PLoS ONE 2:e1058CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Han Seok Choi
    • 1
    • 2
  • Kwang Joon Kim
    • 2
    • 3
  • Kyoung Min Kim
    • 2
    • 3
  • Nam Wook Hur
    • 4
  • Yumie Rhee
    • 2
    • 3
  • Dae Suk Han
    • 3
  • Eun Jig Lee
    • 2
    • 3
    • 5
  • Sung-Kil Lim
    • 2
    • 3
    • 5
    Email author
  1. 1.Division of Endocrinology and Metabolism, Department of Internal MedicineDongguk University Ilsan HospitalGoyang-shiKorea
  2. 2.Institute of Endocrine ResearchYonsei University College of MedicineSeoulKorea
  3. 3.Department of Internal MedicineYonsei University College of MedicineSeoulKorea
  4. 4.Department of Preventive MedicineYonsei University College of MedicineSeoulKorea
  5. 5.Brain Korea 21 Project for Medical SciencesYonsei University College of MedicineSeoulKorea

Personalised recommendations