Calcified Tissue International

, Volume 87, Issue 1, pp 36–43 | Cite as

Adiponectin and Peak Bone Mass in Men: A Cross-Sectional, Population-Based Study

  • M. Frost
  • B. Abrahamsen
  • T. L. Nielsen
  • J. Frystyk
  • A. Flyvbjerg
  • C. Hagen
  • M. Andersen
  • K. Brixen
Article

Abstract

Adiponectin, a protein classically known to be secreted by adipocytes, is also secreted by bone-forming cells. Results of previous studies have been contradictory as to whether serum adiponectin and bone mineral density (BMD) are associated. The aim of this study was to investigate a possible association between serum adiponectin and BMD in young, healthy men at a time of peak bone mass. BMD in the femoral neck, total hip, and lumbar spine were measured in this population-based cross-sectional study of 700 men aged 20–29 years participating in the Odense Androgen Study. Magnetic resonance imaging of femoral cortical thickness and bone marrow size was performed in a subsample of 363 participants. The associations between serum adiponectin and various bone measures were investigated by means of regression analyses with adjustment for potential confounding variables. An inverse association was found between serum adiponectin and total hip BMD and a direct between adiponectin and femoral bone marrow size (r = −0.092; P = 0.036 and r = 0.164; P = 0.003, respectively). Femoral muscle size may, at least in part, explain the association between adiponectin and total hip BMD. Serum adiponectin was inversely associated with total hip BMD in men at the time of peak bone mass, but this association may be explained by factors related to muscle size and function. The observed association between adiponectin and femoral bone marrow size was retained even after adjustment for potential covariates.

Keywords

Adiponectin Peak bone mass Osteoporosis 

References

  1. 1.
    Felson DT, Zhang Y, Hannan MT, Anderson JJ (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res 8:567–573CrossRefPubMedGoogle Scholar
  2. 2.
    De Laet C, Kanis JA, Oden A, Johanson H, Johnell O, Delmas P et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 16:1330–1338CrossRefPubMedGoogle Scholar
  3. 3.
    Ensrud KE, Cauley J, Lipschutz R, Cummings SR (1997) Weight change and fractures in older women. Study of Osteoporotic Fractures Research Group. Arch Intern Med 157:857–863CrossRefPubMedGoogle Scholar
  4. 4.
    Ensrud KE, Fullman RL, Barrett-Connor E, Cauley JA, Stefanick ML, Fink HA et al (2005) Voluntary weight reduction in older men increases hip bone loss: the Osteoporotic Fractures in Men study. J Clin Endocrinol Metab 90:1998–2004CrossRefPubMedGoogle Scholar
  5. 5.
    Forsmo S, Aaen J, Schei B, Langhammer A (2006) What is the influence of weight change on forearm bone mineral density in peri- and postmenopausal women? The Health Study of Nord-Trondelag, Norway. Am J Epidemiol 164:890–897CrossRefPubMedGoogle Scholar
  6. 6.
    Gennari L, Nuti R, Bilezikian JP (2004) Aromatase activity and bone homeostasis in men. J Clin Endocrinol Metab 89:5898–5907CrossRefPubMedGoogle Scholar
  7. 7.
    Reid IR, Evans MC, Cooper GJ, Ames RW, Stapleton J (1993) Circulating insulin levels are related to bone density in normal postmenopausal women. Am J Physiol 265(4 pt 1):E655–E659PubMedGoogle Scholar
  8. 8.
    Abrahamsen B, Rohold A, Henriksen JE, Beck-Nielsen H (2000) Correlations between insulin sensitivity and bone mineral density in non-diabetic men. Diabet Med 17:124–129CrossRefPubMedGoogle Scholar
  9. 9.
    Scherer PE, Williams S, Fogliano M, Baldini G, Lodish HF (1995) A novel serum protein similar to C1q, produced exclusively in adipocytes. J Biol Chem 270:26746–26749CrossRefPubMedGoogle Scholar
  10. 10.
    Weyer C, Funahashi T, Tanaka S, Hotta K, Matsuzawa Y, Pratley RE et al (2001) Hypoadiponectinemia in obesity and type 2 diabetes: close association with insulin resistance and hyperinsulinemia. J Clin Endocrinol Metab 86:1930–1935CrossRefPubMedGoogle Scholar
  11. 11.
    Frederiksen L, Nielsen TL, Wraae K, Hagen C, Frystyk J, Flyvbjerg A et al (2009) Subcutaneous rather than visceral adipose tissue is associated with adiponectin levels and insulin resistance in young men. J Clin Endocrinol Metab 94:4010–4015CrossRefPubMedGoogle Scholar
  12. 12.
    Berner HS, Lyngstadaas SP, Spahr A, Monjo M, Thommesen L, Drevon CA et al (2004) Adiponectin and its receptors are expressed in bone-forming cells. Bone 35:842–849CrossRefPubMedGoogle Scholar
  13. 13.
    Shinoda Y, Yamaguchi M, Ogata N, Akune T, Kubota N, Yamauchi T et al (2006) Regulation of bone formation by adiponectin through autocrine/paracrine and endocrine pathways. J Cell Biochem 99:196–208CrossRefPubMedGoogle Scholar
  14. 14.
    Luo XH, Guo LJ, Yuan LQ, Xie H, Zhou HD, Wu XP et al (2005) Adiponectin stimulates human osteoblasts proliferation and differentiation via the MAPK signaling pathway. Exp Cell Res 309:99–109CrossRefPubMedGoogle Scholar
  15. 15.
    Williams GA, Wang Y, Callon KE, Watson M, Lin JM, Lam JB et al (2009) In vitro and in vivo effects of adiponectin on bone. Endocrinology 150:3603–3610CrossRefPubMedGoogle Scholar
  16. 16.
    Luo XH, Guo LJ, Xie H, Yuan LQ, Wu XP, Zhou HD et al (2006) Adiponectin stimulates RANKL and inhibits OPG expression in human osteoblasts through the MAPK signaling pathway. J Bone Miner Res 21:1648–1656CrossRefPubMedGoogle Scholar
  17. 17.
    Lenchik L, Register TC, Hsu FC, Lohman K, Nicklas BJ, Freedman BI et al (2003) Adiponectin as a novel determinant of bone mineral density and visceral fat. Bone 33:646–651CrossRefPubMedGoogle Scholar
  18. 18.
    Michaelsson K, Lind L, Frystyk J, Flyvbjerg A, Gedeborg R, Berne C et al (2008) Serum adiponectin in elderly men does not correlate with fracture risk. J Clin Endocrinol Metab 93:4041–4047CrossRefPubMedGoogle Scholar
  19. 19.
    Peng XD, Xie H, Zhao Q, Wu XP, Sun ZQ, Liao EY (2008) Relationships between serum adiponectin, leptin, resistin, visfatin levels and bone mineral density, and bone biochemical markers in Chinese men. Clin Chim Acta 387:31–35CrossRefPubMedGoogle Scholar
  20. 20.
    Araneta MR, von Mühlen D, Barrett-Connor E (2009) Sex differences in the association between adiponectin and bone mineral density, bone loss and fractures: the Rancho Bernardo Study. J Bone Miner Res 24:2016–2022Google Scholar
  21. 21.
    Johnell O, Kanis JA, Oden A, Johansson H, De Laet C, Delmas P et al (2005) Predictive value of BMD for hip and other fractures. J Bone Miner Res 20:1185–1194CrossRefPubMedGoogle Scholar
  22. 22.
    Eisman JA, Kelly PJ, Morrison NA, Pocock NA, Yeoman R, Birmingham J et al (1993) Peak bone mass and osteoporosis prevention. Osteoporos Int 3(suppl 1):56–60CrossRefPubMedGoogle Scholar
  23. 23.
    Nielsen TL, Wraae K, Brixen K, Hermann AP, Andersen M, Hagen C (2006) Prevalence of overweight, obesity and physical inactivity in 20- to 29-year-old, Danish men. Relation to sociodemography, physical dysfunction and low socioeconomic status: the Odense Androgen Study. Int J Obes (Lond) 30:805–815CrossRefGoogle Scholar
  24. 24.
    Frystyk J, Tarnow L, Hansen TK, Parving HH, Flyvbjerg A (2005) Increased serum adiponectin levels in type 1 diabetic patients with microvascular complications. Diabetologia 48:1911–1918CrossRefPubMedGoogle Scholar
  25. 25.
    Frystyk J, Dinesen B, Orskov H (1995) Non-competitive time-resolved immunofluorometric assays for determination of human insulin-like growth factor I and II. Growth Regul 5:169–176PubMedGoogle Scholar
  26. 26.
    Nielsen TL, Hagen C, Wraae K, Brixen K, Petersen PH, Haug E et al (2007) Visceral and subcutaneous adipose tissue assessed by magnetic resonance imaging in relation to circulating androgens, sex hormone–binding globulin, and luteinizing hormone in young men. J Clin Endocrinol Metab 92:2696–2705CrossRefPubMedGoogle Scholar
  27. 27.
    Jurimae J, Rembel K, Jurimae T, Rehand M (2005) Adiponectin is associated with bone mineral density in perimenopausal women. Horm Metab Res 37:297–302CrossRefPubMedGoogle Scholar
  28. 28.
    Jurimae J, Jurimae T (2007) Adiponectin is a predictor of bone mineral density in middle-aged premenopausal women. Osteoporos Int 18:1253–1259CrossRefPubMedGoogle Scholar
  29. 29.
    Misra M, Miller KK, Cord J, Prabhakaran R, Herzog DB, Goldstein M et al (2007) Relationships between serum adipokines, insulin levels, and bone density in girls with anorexia nervosa. J Clin Endocrinol Metab 92:2046–2052CrossRefPubMedGoogle Scholar
  30. 30.
    Richards JB, Valdes AM, Burling K, Perks UC, Spector TD (2007) Serum adiponectin and bone mineral density in women. J Clin Endocrinol Metab 92:1517–1523CrossRefPubMedGoogle Scholar
  31. 31.
    Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Yano S, Sugimoto T (2009) Relationships between serum adiponectin levels versus bone mineral density, bone metabolic markers, and vertebral fractures in type 2 diabetes mellitus. Eur J Endocrinol 160:265–273CrossRefPubMedGoogle Scholar
  32. 32.
    Oh KW, Lee WY, Rhee EJ, Baek KH, Yoon KH, Kang MI et al (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
  33. 33.
    Ferrari S, Rizzoli R, Chaponnier C, Gabbiani G, Bonjour JP (1993) Parathyroid hormone-related protein increases cAMP production in mammary epithelial cells. Am J Physiol 264(3 pt 1):E471–E475PubMedGoogle Scholar
  34. 34.
    Jurimae J, Jurimae T (2007) Plasma adiponectin concentration in healthy pre- and postmenopausal women: relationship with body composition, bone mineral, and metabolic variables. Am J Physiol Endocrinol Metab 293:E42–E47CrossRefPubMedGoogle Scholar
  35. 35.
    Zillikens MC, Uitterlinden AG, van Leeuwen JP, Berends AL, Henneman P, van Dijk KW et al (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
  36. 36.
    Riggs BL, Khosla S, Melton LJ III (1998) A unitary model for involutional osteoporosis: estrogen deficiency causes both type I and type II osteoporosis in postmenopausal women and contributes to bone loss in aging men. J Bone Miner Res 13:763–773CrossRefPubMedGoogle Scholar
  37. 37.
    Jensen LB, Vestergaard P, Hermann AP, Gram J, Eiken P, Abrahamsen B et al (2003) Hormone replacement therapy dissociates fat mass and bone mass, and tends to reduce weight gain in early postmenopausal women: a randomized controlled 5-year clinical trial of the Danish Osteoporosis Prevention Study. J Bone Miner Res 18:333–342CrossRefPubMedGoogle Scholar
  38. 38.
    Yatagai T, Nagasaka S, Taniguchi A, Fukushima M, Nakamura T, Kuroe A et al (2003) Hypoadiponectinemia is associated with visceral fat accumulation and insulin resistance in Japanese men with type 2 diabetes mellitus. Metabolism 52:1274–1278CrossRefPubMedGoogle Scholar
  39. 39.
    Yokota T, Meka CS, Medina KL, Igarashi H, Comp PC, Takahashi M et al (2002) Paracrine regulation of fat cell formation in bone marrow cultures via adiponectin and prostaglandins. J Clin Invest 109:1303–1310PubMedGoogle Scholar
  40. 40.
    Justesen J, Stenderup K, Ebbesen EN, Mosekilde L, Steiniche T, Kassem M (2001) Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology 2:165–171CrossRefPubMedGoogle Scholar
  41. 41.
    Okazaki R, Inoue D, Shibata M, Saika M, Kido S, Ooka H et al (2002) Estrogen promotes early osteoblast differentiation and inhibits adipocyte differentiation in mouse bone marrow stromal cell lines that express estrogen receptor (ER) alpha or beta. Endocrinology 143:2349–2356CrossRefPubMedGoogle Scholar
  42. 42.
    Lee HW, Kim SY, Kim AY, Lee EJ, Choi JY, Kim JB (2009) Adiponectin stimulates osteoblast differentiation through induction of COX2 in mesenchymal progenitor cells. Stem Cells 27:2254–2262CrossRefPubMedGoogle Scholar
  43. 43.
    Kanazawa I, Yamaguchi T, Sugimoto T (2009) Baseline serum total adiponectin level is positively associated with changes in bone mineral density after 1-year treatment of type 2 diabetes mellitus. MetabolismGoogle Scholar
  44. 44.
    Sodi R, Hazell MJ, Durham BH, Rees C, Ranganath LR, Fraser WD (2009) The circulating concentration and ratio of total and high molecular weight adiponectin in post-menopausal women with and without osteoporosis and its association with body mass index and biochemical markers of bone metabolism. Clin Biochem 42(13–14):1375–1380CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • M. Frost
    • 1
  • B. Abrahamsen
    • 2
  • T. L. Nielsen
    • 1
  • J. Frystyk
    • 3
  • A. Flyvbjerg
    • 3
  • C. Hagen
    • 4
  • M. Andersen
    • 1
  • K. Brixen
    • 1
  1. 1.Department of EndocrinologyOdense University HospitalOdense CDenmark
  2. 2.Department of Internal MedicineGentofte County HospitalCopenhagenDenmark
  3. 3.Department of Endocrinology and Internal MedicineAarhus University HospitalAarhusDenmark
  4. 4.Department of EndocrinologyBispebjerg HospitalCopenhagenDenmark

Personalised recommendations