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Osteocalcin and measures of adiposity: a systematic review and meta-analysis of observational studies

Archives of Osteoporosis volume 15, Article number: 145 (2020) Cite this article

Abstract

Summary

Osteocalcin, the osteoblast-derived protein, has been shown to be modulated in patients with problematic glucose metabolism. Our systematic review and meta-analysis found that in humans, higher blood osteocalcin level is associated with lower body indices of fat.

Purpose/introduction

Osteocalcin (OC) was found to be inversely correlated with measures of glucose and energy metabolism, with some groups suggesting the undercarboxylated form (ucOC) to be metabolically active, although the link is not clear, especially in humans. Given obesity is a major risk factor for metabolic disorders, we aimed to assess the correlation between OC and two measures of body weight: body mass index (BMI) and percentage body fat (%BF).

Methods

MEDLINE and EMBASE were searched to identify observational studies in adult populations that reported the crude correlation coefficients (r) between OC and BMI and %BF. Pool r were obtained using random-effects models.

Results

Fifty-one publications were included in this analysis. Both total OC (TOC) (pooled r = − 0.151, 95% CI – 0.17, − 0.130; I2 = 52%) and ucOC (pooled r = − 0.060, 95% CI – 0.103, − 0.016; I2 = 54%) were inversely correlated with BMI. The pooled r between TOC and BMI in Caucasian-and-other-regions (r = − 0.187) were stronger than those in Asian populations (r = − 0.126; intra-group p = 0.002; R2 = 0.21). The mean/median BMI of the reported cohort was the major contributor to between-study heterogeneity in correlation between TOC/ucOC and BMI (R2 = 0.28 and 0.77, respectively). Both TOC and ucOC were also inversely correlated with %BF (TOC: pooled r = − 0.185, 95% CI – 0.257 to − 0.112; ucOC: pooled r = − 0.181, 95% CI – 0.258 to − 0.101).

Conclusion

Higher OC and ucOC were correlated with lower BMI and %BF. The inverse correlations between TOC/ucOC and BMI appear to be affected by ethnicity and obesity status.

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References

  1. Lian JB, Gundberg CM (1988) Osteocalcin: biochemical considerations and clinical applications. Clin Orthop Relat Res 226:267–291

    Article  CAS  Google Scholar 

  2. Brennan-Speranza TC, Conigrave AD (2015) Osteocalcin: an osteoblast-derived polypeptide hormone that modulates whole body energy metabolism. Calcif Tissue Int 96(1):1–10

    Article  CAS  PubMed  Google Scholar 

  3. Hauschka PV, Lian JB, Cole DE, Gundberg CM (1989) Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone. Physiol Rev 69(3):990–1047

    Article  CAS  PubMed  Google Scholar 

  4. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130(3):456–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ferron M, McKee MD, Levine RL, Ducy P, Karsenty G (2012) Intermittent injections of osteocalcin improve glucose metabolism and prevent type 2 diabetes in mice. Bone 50(2):568–575

    Article  CAS  PubMed  Google Scholar 

  6. Ferron M, Hinoi E, Karsenty G, Ducy P (2008) Osteocalcin differentially regulates β cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci 105(13):5266–5270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Booth SL, Centi A, Smith SR, Gundberg C (2013) The role of osteocalcin in human glucose metabolism: marker or mediator? Nat Rev Endocrinol 9(1):43–55

    Article  CAS  PubMed  Google Scholar 

  8. Desbois C, Hogue DA, Karsenty G (1994) The mouse osteocalcin gene cluster contains three genes with two separate spatial and temporal patterns of expression. J Biol Chem 269(2):1183–1190

    Article  CAS  PubMed  Google Scholar 

  9. Celeste AJ, Rosen V, Buecker JL, Kriz R, Wang EA, Wozney JM (1986) Isolation of the human gene for bone gla protein utilizing mouse and rat cDNA clones. EMBO J 5(8):1885–1890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Lambert LJ et al (2016) Increased trabecular bone and improved biomechanics in an osteocalcin-null rat model created by CRISPR/Cas9 technology. Dis Model Mech 9(10):1169–1179

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Smith C, Voisin S, al Saedi A, Phu S, Brennan-Speranza T, Parker L, Eynon N, Hiam D, Yan X, Scott D, Blekkenhorst LC, Lewis JR, Seeman E, Byrnes E, Flicker L, Duque G, Yeap BB, Levinger I (2020) Osteocalcin and its forms across the lifespan in adult men. Bone 130:115085

    Article  CAS  PubMed  Google Scholar 

  12. Moriishi T, Ozasa R, Ishimoto T, Nakano T, Hasegawa T, Miyazaki T, Liu W, Fukuyama R, Wang Y, Komori H, Qin X, Amizuka N, Komori T (2020) Osteocalcin is necessary for the alignment of apatite crystallites, but not glucose metabolism, testosterone synthesis, or muscle mass. PLoS Genet 16(5):e1008586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Sims N et al (1997) Human and murine osteocalcin gene expression: conserved tissue restricted expression and divergent responses to 1,25-dihydroxyvitamin D sub(3) in vivo. Mol Endocrinol 11(11):1695–1708

    Article  CAS  PubMed  Google Scholar 

  14. Lian JB, Shalhoub V, Aslam F, Frenkel B, Green J, Hamrah M, Stein GS, Stein JL (1997) Species-specific glucocorticoid and 1,25-dihydroxyvitamin D responsiveness in mouse MC3T3-E1 osteoblasts: dexamethasone inhibits osteoblast differentiation and vitamin D down-regulates osteocalcin gene expression. Endocrinology 138(5):2117–2127

    Article  CAS  PubMed  Google Scholar 

  15. Zhang R, Ducy P, Karsenty G (1997) 1,25-Dihydroxyvitamin D3 inhibits osteocalcin expression in mouse through an indirect mechanism. J Biol Chem 272(1):110–116

    Article  CAS  PubMed  Google Scholar 

  16. Clemens TL, Tang H, Maeda S, Kesterson RA, Demayo F, Pike JW, Gundberg CM (1997) Analysis of osteocalcin expression in transgenic mice reveals a species difference in vitamin D regulation of mouse and human osteocalcin genes. J Bone Miner Res 12(10):1570–1576

    Article  CAS  PubMed  Google Scholar 

  17. Liu DM, Guo XZ, Tong HJ, Tao B, Sun LH, Zhao HY, Ning G, Liu JM (2015) Association between osteocalcin and glucose metabolism: a meta-analysis. Osteoporos Int 26(12):2823–2833

    Article  CAS  PubMed  Google Scholar 

  18. Kunutsor SK, Apekey TA, Laukkanen JA (2015) Association of serum total osteocalcin with type 2 diabetes and intermediate metabolic phenotypes: systematic review and meta-analysis of observational evidence. Eur J Epidemiol 30(8):599–614

    Article  CAS  PubMed  Google Scholar 

  19. Liu C et al (2015) Association between serum total osteocalcin level and type 2 diabetes mellitus: a systematic review and meta-analysis. Horm Metab Res 47(11):813–819

    Article  CAS  PubMed  Google Scholar 

  20. Hygum K, Starup-Linde J, Harsløf T, Vestergaard P, Langdahl BL (2017) Mechanisms in endocrinology: diabetes mellitus, a state of low bone turnover – a systematic review and meta-analysis. Eur J Endocrinol 176(3):R137–R157

    Article  CAS  PubMed  Google Scholar 

  21. Millar SA, Patel H, Anderson SI, England TJ, O’Sullivan SE (2017) Osteocalcin, vascular calcification, and atherosclerosis: a systematic review and meta-analysis. Front Endocrinol 8:183

    Article  Google Scholar 

  22. Schwartz AV, Schafer AL, Grey A, Vittinghoff E, Palermo L, Lui LYL, Wallace RB, Cummings SR, Black DM, Bauer DC, Reid IR (2013) Effects of antiresorptive therapies on glucose metabolism: results from the FIT, HORIZON-PFT, and FREEDOM trials. J Bone Miner Res 28(6):1348–1354

    Article  CAS  PubMed  Google Scholar 

  23. Shea MK, Dawson-Hughes B, Gundberg CM, Booth SL (2017) Reducing undercarboxylated osteocalcin with vitamin K supplementation does not promote lean tissue loss or fat gain over 3 years in older women and men: a randomized controlled trial. J Bone Miner Res 32(2):243–249

    Article  CAS  PubMed  Google Scholar 

  24. Lewis JR, Brennan-Speranza TC, Levinger I, Byrnes E, Lim EM, Blekkenhorst LC, Sim M, Hodgson JM, Zhu K, Lim WH, Adams LA, Prince RL (2019) Effects of calcium supplementation on circulating osteocalcin and glycated haemoglobin in older women. Osteoporos Int 30:2065–2072

    Article  CAS  PubMed  Google Scholar 

  25. Sun Q, van Dam RM, Spiegelman D, Heymsfield SB, Willett WC, Hu FB (2010) Comparison of dual-energy X-ray absorptiometric and anthropometric measures of adiposity in relation to adiposity-related biologic factors. Am J Epidemiol 172(12):1442–1454

    Article  PubMed  PubMed Central  Google Scholar 

  26. Gallagher D, Heymsfield SB, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y (2000) Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr 72(3):694–701

    Article  CAS  PubMed  Google Scholar 

  27. Kindblom JM et al (2009) Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. [Erratum appears in J Bone Miner Res. 2010 Dec;25(12):2527]. J Bone Miner Res 24(5):785–791

    Article  CAS  PubMed  Google Scholar 

  28. Hwang YC, Jee JH, Jeong IK, Ahn KJ, Chung HY, Lee MK (2012) Circulating osteocalcin level is not associated with incident type 2 diabetes in middle-aged male subjects: mean 8.4-year retrospective follow-up study. Diabetes Care 35(9):1919–1924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lee SW, Jo HH, Kim MR, Kim JH, You YO (2015) Association between osteocalcin and metabolic syndrome in postmenopausal women. Arch Gynecol Obstet 292(3):673–681

    Article  CAS  PubMed  Google Scholar 

  30. Knapen MHJ, Schurgers LJ, Shearer MJ, Newman P, Theuwissen E, Vermeer C (2012) Association of vitamin K status with adiponectin and body composition in healthy subjects: uncarboxylated osteocalcin is not associated with fat mass and body weight. Br J Nutr 108(6):1017–1024

    Article  CAS  PubMed  Google Scholar 

  31. Kanazawa I, Yamaguchi T, Yamauchi M, Yamamoto M, Kurioka S, Yano S, Sugimoto T (2011) Serum undercarboxylated osteocalcin was inversely associated with plasma glucose level and fat mass in type 2 diabetes mellitus. Osteoporos Int 22(1):187–194

    Article  CAS  PubMed  Google Scholar 

  32. Kord-Varkaneh H, Djafarian K, khorshidi M, Shab-Bidar S (2017) Association between serum osteocalcin and body mass index: a systematic review and meta-analysis. Endocrine 58(1):24–32

    Article  CAS  PubMed  Google Scholar 

  33. Stroup DF et al (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15):2008–2012

    Article  CAS  PubMed  Google Scholar 

  34. Basurto-Acevedo L et al (2018) Relationship between bone remodeling and metabolism in the elderly. Rev Med Inst Mex Seguro Soc 56(S1):6–11

    Google Scholar 

  35. Elmaataoui A, Elmachtani Idrissi S, Dami A, Bouhsain S, Chabraoui L, Ouzzif Z (2014) Association between bone turnover markers, bone mineral density and vitamin D in Moroccan postmenopausal women. Pathol Biol 62(1):49–54

    Article  CAS  PubMed  Google Scholar 

  36. Yeap BB, Chubb SAP, Flicker L, McCaul KA, Ebeling PR, Beilby JP, Norman PE (2010) Reduced serum total osteocalcin is associated with metabolic syndrome in older men via waist circumference, hyperglycemia, and triglyceride levels. Eur J Endocrinol 163(2):265–272

    Article  CAS  PubMed  Google Scholar 

  37. Yeap BB, Alfonso H, Chubb SAP, Gauci R, Byrnes E, Beilby JP, Ebeling PR, Handelsman DJ, Allan CA, Grossmann M, Norman PE, Flicker L (2015) Higher serum undercarboxylated osteocalcin and other bone turnover markers are associated with reduced diabetes risk and lower estradiol concentrations in older men. J Clin Endocrinol Metab 100(1):63–71

    Article  CAS  PubMed  Google Scholar 

  38. Gundberg CM, Nieman SD, Abrams S, Rosen H (1998) Vitamin K status and bone health: an analysis of methods for determination of undercarboxylated osteocalcin. J Clin Endocrinol Metab 83(9):3258–3266

    CAS  PubMed  Google Scholar 

  39. Aloe AM (2015) Inaccuracy of regression results in replacing bivariate correlations. Res Synth Methods 6(1):21–27

    Article  PubMed  Google Scholar 

  40. Wells G et al The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa Hospital Research Institute. 2015 [cited 2017 10-Jun]; Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp

  41. Downes MJ et al (2016) Development of a critical appraisal tool to assess the quality of cross-sectional studies (AXIS). BMJ Open 6(12)

  42. National Heart, L, B. Institute (2014) Quality assessment tool for observational cohort and cross-sectional studies. National Institutes of Health, Department of Health and Human Services, Bethesda

    Google Scholar 

  43. Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5(1):13

    Article  PubMed  PubMed Central  Google Scholar 

  44. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188

    Article  CAS  PubMed  Google Scholar 

  45. Borenstein M et al (2011) Introduction to meta-analysis. John Wiley & Sons

  46. Higgins JPT et al (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560

    Article  PubMed  PubMed Central  Google Scholar 

  47. Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Zhou BF (2002) Predictive values of body mass index and waist circumference for risk factors of certain related diseases in Chinese adults--study on optimal cut-off points of body mass index and waist circumference in Chinese adults. Biomed Environ Sci 15(1):83–96

    PubMed  Google Scholar 

  49. Liu X, Brock KE, Brennan-Speranza TC (2017) Comment on ‘Association between serum osteocalcin and body mass index: a systematic review and meta-analysis’. Endocrine

  50. Bezerra dos Santos Magalhães K et al (2013) Metabolic syndrome and central fat distribution are related to lower serum osteocalcin concentrations. Ann Nutr Metab 62(3):183–188

    Article  PubMed  CAS  Google Scholar 

  51. Tan A, Gao Y, Yang X, Zhang H, Qin X, Mo L, Peng T, Xia N, Mo Z (2011) Low serum osteocalcin level is a potential marker for metabolic syndrome: results from a Chinese male population survey. Metab Clin Exp 60(8):1186–1192

    Article  CAS  PubMed  Google Scholar 

  52. Liao M, Guo X, Yu X, Pang G, Zhang S, Li J, Tan A, Gao Y, Yang X, Zhang H, Qin X, Mo L, Lu Z, Wu C, Mo Z (2013) Role of metabolic factors in the association between osteocalcin and testosterone in Chinese men. J Clin Endocrinol Metab 98(8):3463–3469

    Article  CAS  PubMed  Google Scholar 

  53. Rejnmark L, Vestergaard P, Mosekilde L (2006) Treatment with beta-blockers, ACE inhibitors, and calcium-channel blockers is associated with a reduced fracture risk: a nationwide case–control study. J Hypertens 24(3):581–589

    Article  CAS  PubMed  Google Scholar 

  54. Dobnig H, Piswanger-Sölkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, Maier E, Maritschnegg P, Sieberer C, Fahrleitner-Pammer A (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91(9):3355–3363

    Article  CAS  PubMed  Google Scholar 

  55. Brennan-Speranza TC, Henneicke H, Gasparini SJ, Blankenstein KI, Heinevetter U, Cogger VC, Svistounov D, Zhang Y, Cooney GJ, Buttgereit F, Dunstan CR, Gundberg C, Zhou H, Seibel MJ (2012) Osteoblasts mediate the adverse effects of glucocorticoids on fuel metabolism. J Clin Invest 122(11):4172–4189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Bao Y, Ma X, Yang R, Wang F, Hao Y, Dou J, He H, Jia W (2013) Inverse relationship between serum osteocalcin levels and visceral fat area in Chinese men. J Clin Endocrinol Metab 98(1):345–351

    Article  CAS  PubMed  Google Scholar 

  57. Buday B, Pach FP, Literati-Nagy B, Vitai M, Vecsei Z, Koranyi L (2013) Serum osteocalcin is associated with improved metabolic state via adiponectin in females versus testosterone in males. Gender specific nature of the bone–energy homeostasis axis. Bone 57(1):98–104

    Article  CAS  PubMed  Google Scholar 

  58. Caplan AI (1991) Mesenchymal stem cells. J Orthop Res 9(5):641–650

    Article  CAS  PubMed  Google Scholar 

  59. Berner HS, Lyngstadaas SP, Spahr A, Monjo M, Thommesen L, Drevon CA, Syversen U, Reseland JE (2004) Adiponectin and its receptors are expressed in bone-forming cells. Bone 35(4):842–849

    Article  CAS  PubMed  Google Scholar 

  60. Luo XH, Guo LJ, Yuan LQ, Xie H, Zhou HD, Wu XP, Liao EY (2005) Adiponectin stimulates human osteoblasts proliferation and differentiation via the MAPK signaling pathway. Exp Cell Res 309(1):99–109

    Article  CAS  PubMed  Google Scholar 

  61. Hill HS et al (2014) Carboxylated and uncarboxylated forms of osteocalcin directly modulate the glucose transport system and inflammation in adipocytes. Horm Metab Res 46(05):341–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Yeap BB, Alfonso H, Chubb SAP, Byrnes E, Beilby JP, Ebeling PR, Allan CA, Schultz C, Hankey GJ, Golledge J, Flicker L, Norman PE (2015) Proportion of undercarboxylated osteocalcin and serum P1NP predict incidence of myocardial infarction in older men. J Clin Endocrinol Metab 100(10):3934–3942

    Article  CAS  PubMed  Google Scholar 

  63. Ngarmukos C, Chailurkit LO, Chanprasertyothin S, Hengprasith B, Sritara P, Ongphiphadhanakul B (2012) A reduced serum level of total osteocalcin in men predicts the development of diabetes in a long-term follow-up cohort. Clin Endocrinol 77(1):42–46

    Article  Google Scholar 

  64. Yeap BB, Chubb SAP, Flicker L, McCaul KA, Ebeling PR, Hankey GJ, Beilby JP, Norman PE (2012) Associations of total osteocalcin with all-cause and cardiovascular mortality in older men. The health in men study. Osteoporos Int 23(2):599–606

    Article  CAS  PubMed  Google Scholar 

  65. Cairns JR, Price PA (1994) Direct demonstration that the vitamin k-dependent bone gla protein is incompletely γ-carboxylated in humans. J Bone Miner Res 9(12):1989–1997

    Article  CAS  PubMed  Google Scholar 

  66. Sokoll LJ, O'Brien ME, Camilo ME, Sadowski JA (1995) Undercarboxylated osteocalcin and development of a method to determine vitamin K status. Clin Chem 41(8):1121–1128

    Article  CAS  PubMed  Google Scholar 

  67. Ivaska KK, Hentunen TA, Vääräniemi J, Ylipahkala H, Pettersson K, Väänänen HK (2004) Release of intact and fragmented osteocalcin molecules from bone matrix during bone resorption in vitro. J Biol Chem 279(18):18361–18369

    Article  CAS  PubMed  Google Scholar 

  68. Garnero P, Sornay-Rendu E, Chapuy MC, Delmas PD (1996) Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis. J Bone Miner Res 11(3):337–349

    Article  CAS  PubMed  Google Scholar 

  69. Sayinalp S, Gedik O, Koray Z (1995) Increasing serum osteocalcin after glycemic control in diabetic men. Calcif Tissue Int 57(6):422–425

    Article  CAS  PubMed  Google Scholar 

  70. Deurenberg P, Yap M, Van Staveren WA (1998) Body mass index and percent body fat: a meta analysis among different ethnic groups. Int J Obes Relat Metab Disord 22(12)

  71. Lim U, Ernst T, Buchthal SD, Latch M, Albright CL, Wilkens LR, Kolonel LN, Murphy SP, Chang L, Novotny R, le Marchand L (2011) Asian women have greater abdominal and visceral adiposity than Caucasian women with similar body mass index. Nutr Diabetes 1:e6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Author notes

  1. Kaye E. Brock and Tara C. Brennan-Speranza co-senior authorship

Authors and Affiliations

  1. Department of Physiology, School of Medical Sciences, Faculty of Medicine and Health, The University of Sydney, Sydney, Australia

    Xiaoying Liu, Julia Mathers, Melissa Cameron, Kaye E. Brock & Tara C. Brennan-Speranza

  2. School of Public Health, Faculty of Medicine and Health, The University of Sydney, Sydney, NSW, 2006, Australia

    Yihui Liu & Tara C. Brennan-Speranza

  3. Institute for Health and Sport (IHES), Victoria University, Melbourne, Australia

    Itamar Levinger

  4. Australian Institute for Musculoskeletal Science (AIMSS), Department of Medicine-Western Health, Melbourne Medical School, The University of Melbourne, Melbourne, Australia

    Itamar Levinger

  5. Medical School, University of Western Australia, Perth, Australia

    Bu B. Yeap & Joshua R. Lewis

  6. Department of Endocrinology and Diabetes, Fiona Stanley Hospital, Perth, Australia

    Bu B. Yeap

  7. Centre for Kidney Research, Children’s Hospital at Westmead, School of Public Health, Sydney Medical School, The University of Sydney, Sydney, Australia

    Joshua R. Lewis

  8. School of Medical and Health Sciences, Edith Cowan University, Joondalup, WA, Australia

    Joshua R. Lewis

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  1. Xiaoying Liu
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Contributions

Study design: XL, TBS, KB and JL. Literature search: XL and JL. Data collection: XL and YL. Data analysis: XL and KB. Data interpretation: XL, TBS, KB, IL, BBY, and JL. Manuscript drafting: XL, JM, KB, and TBS. Critical revision: TBS, JL, MC, IL, and BBY. All authors had final approval of the submitted manuscript.

Corresponding author

Correspondence to Tara C. Brennan-Speranza.

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Conflict of interest

Xiaoying Liu, Yihui Liu, Julia Mathers, Melissa Cameron, Itamar Levinger, Bu Yeap, Joshua Lewis, Kaye Brock, and Tara Brennan-Speranza declare that they have no conflict of interest. The salary of JL is supported by a National Health and Medical Research Council (NHMRC) of Australia Career Development Fellowship (ID 1107474).

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Liu, X., Liu, Y., Mathers, J. et al. Osteocalcin and measures of adiposity: a systematic review and meta-analysis of observational studies. Arch Osteoporos 15, 145 (2020). https://doi.org/10.1007/s11657-020-00812-6

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Keywords

  • Osteocalcin
  • Body mass index
  • Adiposity
  • Body fat percentage