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Osteoporosis International

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01-04-2013 | Short Communication

Cold-activated brown adipose tissue is an independent predictor of higher bone mineral density in women

Authors: P. Lee, R. J. Brychta, M. T. Collins, J. Linderman, S. Smith, P. Herscovitch, C. Millo, K. Y. Chen, F. S. Celi

Published in: Osteoporosis International | Issue 4/2013

Abstract

Summary

In animals, defective brown adipogenesis leads to bone loss. Whether brown adipose tissue (BAT) mass relates to bone mineral density (BMD) in humans is unclear. We determined the relationship between BAT mass and BMD by cold-stimulated positron-emission tomography (PET) and dual-energy X-ray absorptiometry (DXA) in healthy volunteers. Higher BAT mass was associated with higher BMD in healthy women, but not in men, independent of age and body composition.

Introduction

Contrary to the traditional belief that BAT is present only in infants, recent studies revealed significant depots of BAT present in adult humans. In animals, defective brown adipogenesis leads to bone loss. While white adipose tissue mass is a known determinant of BMD in humans, the relationship between BAT and BMD in humans is unclear. We thus examined the relationship between BAT and BMD in healthy adults.

Methods

BAT volume (ml) and activity (standard uptake value) were determined by ¹⁸F-fluorodeoxyglucose PET after overnight mild cold exposure at 19 °C, and BMD was determined by DXA.

Results

Among 24 healthy adults (age 28 ± 1 years, F = 10), BAT volumes were 82.4 ± 99.5 ml in women and 49.7 ± 54.5 ml in men. Women manifested significantly higher BAT activity, by 9.4 ± 8.1 % (p = 0.03), than men. BAT volume correlated positively with total and spine BMD (r ² = 0.40 and 0.49, respectively, p < 0.02) in women and remained a significant predictor after adjustment for age, fat, and lean body mass (p < 0.05). Total and spine BMD were higher in women who harbored visually detectable BAT on PET images than those without by 11 ± 2 % (p = 0.02) and 22 ± 2 % (p < 0.01), respectively. No associations were observed between BAT parameters and BMD in men.

Conclusions

This study demonstrated higher BMD among healthy women with more abundant BAT, independent of age and other body compositional parameters. This was not observed in men. The data suggest that brown adipogenesis may be physiologically related to modulation of bone density.

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Nedergaard J, Bengtsson T, Cannon B (2007) Unexpected evidence for active brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 293:E444–E452PubMedCrossRef

Feldmann HM, Golozoubova V, Cannon B, Nedergaard J (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab 9:203–209PubMedCrossRef

Saito M, Okamatsu-Ogura Y, Matsushita M et al (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58:1526–1531PubMedCrossRef

van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, Schrauwen P, Teule GJ (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500–1508PubMedCrossRef

Lee P, Zhao JT, Swarbrick MM, Gracie G, Bova R, Greenfield JR, Freund J, Ho KK (2011) High prevalence of brown adipose tissue in adult humans. J Clin Endocrinol Metab 96:2450–2455PubMedCrossRef

Lee P, Greenfield JR, Ho KK, Fulham MJ (2010) A critical appraisal of the prevalence and metabolic significance of brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 299:E601–E606PubMedCrossRef

Salamone LM, Glynn N, Black D, Epstein RS, Palermo L, Meilahn E, Kuller LH, Cauley JA (1995) Body composition and bone mineral density in premenopausal and early perimenopausal women. J Bone Miner Res 10:1762–1768PubMedCrossRef

Albala C, Yanez M, Devoto E, Sostin C, Zeballos L, Santos JL (1996) Obesity as a protective factor for postmenopausal osteoporosis. Int J Obes Relat Metab Disord 20:1027–1032PubMed

Reid IR, Plank LD, Evans MC (1992) Fat mass is an important determinant of whole body bone density in premenopausal women but not in men. J Clin Endocrinol Metab 75:779–782PubMedCrossRef

10.

Janicka A, Wren TA, Sanchez MM, Dorey F, Kim PS, Mittelman SD, Gilsanz V (2007) Fat mass is not beneficial to bone in adolescents and young adults. J Clin Endocrinol Metab 92:143–147PubMedCrossRef

11.

Gilsanz V, Chalfant J, Mo AO, Lee DC, Dorey FJ, Mittelman SD (2009) Reciprocal relations of subcutaneous and visceral fat to bone structure and strength. J Clin Endocrinol Metab 94:3387–3393PubMedCrossRef

12.

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 95:1247–1255PubMedCrossRef

13.

Motyl KJ, Raetz M, Tekalur SA, Schwartz RC, McCabe LR (2011) CCAAT/enhancer binding protein beta-deficiency enhances type 1 diabetic bone phenotype by increasing marrow adiposity and bone resorption. Am J Physiol Regul Integr Comp Physiol 300:R1250–R1260PubMedCrossRef

14.

Carmona MC, Hondares E, Rodriguez de la Concepcion ML, Rodriguez-Sureda V, Peinado-Onsurbe J, Poli V, Iglesias R, Villarroya F, Giralt M (2005) Defective thermoregulation, impaired lipid metabolism, but preserved adrenergic induction of gene expression in brown fat of mice lacking C/EBPbeta. Biochem J 389:47–56PubMedCrossRef

15.

Zanotti S, Stadmeyer L, Smerdel-Ramoya A, Durant D, Canalis E (2009) Misexpression of CCAAT/enhancer binding protein beta causes osteopenia. J Endocrinol 201:263–274PubMedCrossRef

16.

Motyl KJ, Rosen CJ (2011) Temperatures rising: brown fat and bone. Discov Med 11:179–185PubMed

17.

Bredella MA, Fazeli PK, Freedman LM, Calder G, Lee H, Rosen CJ, Klibanski A (2012) Young women with cold-activated brown adipose tissue have higher bone mineral density and lower Pref-1 than women without brown adipose tissue: a study in women with anorexia nervosa, women recovered from anorexia nervosa, and normal-weight women. J Clin Endocrinol Metab 97:E584–E590PubMedCrossRef

18.

Krings A, Rahman S, Huang S, Lu Y, Czernik PJ, Lecka-Czernik B (2012) Bone marrow fat has brown adipose tissue characteristics, which are attenuated with aging and diabetes. Bone 50:546–552PubMedCrossRef

19.

Olmsted-Davis E, Gannon FH, Ozen M et al (2007) Hypoxic adipocytes pattern early heterotopic bone formation. Am J Pathol 170:620–632PubMedCrossRef

20.

Zhang H, Schulz TJ, Espinoza DO, Huang TL, Emanuelli B, Kristiansen K, Tseng YH (2010) Cross talk between insulin and bone morphogenetic protein signaling systems in brown adipogenesis. Mol Cell Biol 30:4224–4233PubMedCrossRef

Title: Cold-activated brown adipose tissue is an independent predictor of higher bone mineral density in women
Authors: P. Lee
R. J. Brychta
M. T. Collins
J. Linderman
S. Smith
P. Herscovitch
C. Millo
K. Y. Chen
F. S. Celi
Publication date: 01-04-2013
Publisher: Springer-Verlag
Published in: Osteoporosis International / Issue 4/2013
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI: https://doi.org/10.1007/s00198-012-2110-y

At a glance: The STEP trials

Springer Medicine

Cold-activated brown adipose tissue is an independent predictor of higher bone mineral density in women

Abstract

Summary

Introduction

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Summary

Introduction

Methods

Results

Conclusions

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