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Ethnic and sex differences in bone marrow adipose tissue and bone mineral density relationship

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Abstract

Summary

The relationship between bone marrow adipose tissue and bone mineral density is different between African Americans and Caucasians as well as between men and women. This suggests that the mechanisms that regulate the differentiation and proliferation of bone marrow stromal cells may differ in these populations.

Introduction

It has long been established that there are ethnic and sex differences in bone mineral density (BMD) and fracture risk. Recent studies suggest that bone marrow adipose tissue (BMAT) may play a role in the pathogenesis of osteoporosis. It is unknown whether ethnic and sex differences exist in the relationship between BMAT and BMD.

Methods

Pelvic BMAT was evaluated in 455 healthy African American and Caucasian men and women (age 18–88 years) using whole-body T1-weighted magnetic resonance imaging. BMD was measured using whole-body dual-energy X-ray absorptiometry.

Results

A negative correlation was observed between pelvic BMAT and total body BMD or pelvic BMD (r = −0.533, −0.576, respectively; P < 0.001). In multiple regression analyses with BMD as the dependent variable, ethnicity significantly entered the regression models as either an individual term or an interaction with BMAT. Menopausal status significantly entered the regression model with total body BMD as the dependent variable. African Americans had higher total body BMD than Caucasians for the same amount of BMAT, and the ethnic difference for pelvic BMD was greater in those participants with a higher BMAT. Men and premenopausal women had higher total body BMD levels than postmenopausal women for the same amount of BMAT.

Conclusions

An inverse relationship exists between BMAT and BMD in African American and Caucasian men and women. The observed ethnic and sex differences between BMAT and BMD in the present study suggest the possibility that the mechanisms regulating the differentiation and proliferation of bone marrow stromal cells may differ in these populations.

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References

  1. Farmer ME, White LR, Brody JA, Bailey KR (1984) Race and sex differences in hip fracture incidence. Am J Public Health 74:1374–1380

    Article  PubMed  CAS  Google Scholar 

  2. Kellie SE, Brody JA (1990) Sex-specific and race-specific hip fracture rates. Am J Public Health 80:326–328

    Article  PubMed  CAS  Google Scholar 

  3. Ettinger B, Sidney S, Cummings SR, Libanati C, Bikle DD, Tekawa IS, Tolan K, Steiger P (1997) Racial differences in bone density between young adult Black and White subjects persist after adjustment for anthropometric, lifestyle, and biochemical differences. J Clin Endocrinol Metab 82:429–434

    Article  PubMed  CAS  Google Scholar 

  4. Barrett-Connor E, Siris ES, Wehren LE, Miller PD, Abbott TA, Berger ML, Santora AC, Sherwood LM (2005) Osteoporosis and fracture risk in women of different ethnic groups. J Bone Miner Res 20:185–194

    Article  PubMed  Google Scholar 

  5. Nieves JW, Formica C, Ruffing J, Zion M, Garrett P, Lindsay R, Cosman F (2005) Males have larger skeletal size and bone mass than females, despite comparable body size. J Bone Miner Res 20:529–535

    Article  PubMed  Google Scholar 

  6. Beresford JN, Bennett JH, Devlin C, Leboy PS, Owen ME (1992) Evidence for an inverse relationship between the differentiation of adipocytic and osteogenic cells in rat marrow stromal cell cultures. J Cell Sci 102:341–351

    PubMed  CAS  Google Scholar 

  7. Shih TT, Chang CJ, Hsu CY, Wei SY, Su KC, Chung HW (2004) Correlation of bone marrow lipid water content with bone mineral density on the lumbar spine. Spine 29:2844–2850

    Article  PubMed  Google Scholar 

  8. Wehrli FW, Hopkins JA, Hwang SN, Song HK, Snyder PJ, Haddad JG (2000) Cross-sectional study of osteopenia with quantitative MR imaging and bone densitometry. Radiology 217:527–538

    PubMed  CAS  Google Scholar 

  9. Griffith JF, Yeung DK, Antonio GE, Lee FK, Hong AW, Wong SY, Lau EM, Leung PC (2005) Vertebral bone mineral density, marrow perfusion, and fat content in healthy men and men with osteoporosis: dynamic contrast-enhanced MR imaging and MR spectroscopy. Radiology 236:945–951

    Article  PubMed  Google Scholar 

  10. Di Iorgi N, Rosol M, Mittelman SD, Gilsanz V (2008) Reciprocal relation between marrow adiposity and the amount of bone in the axial and appendicular skeleton of young adults. J Clin Endocrinol Metab 93:2281–2286

    Article  PubMed  Google Scholar 

  11. Shen W, Chen J, Punyanitya M, Shapses S, Heshka S, Heymsfield SB (2007) MRI-measured bone marrow adipose tissue is inversely related to DXA-measured bone mineral in Caucasian women. Osteoporos Int 18:641–647

    Article  PubMed  CAS  Google Scholar 

  12. Quarto R, Thomas D, Liang CT (1995) Bone progenitor cell deficits and the age-associated decline in bone repair capacity. Calcif Tissue Int 56:123–129

    Article  PubMed  CAS  Google Scholar 

  13. Mullender MG, van der Meer DD, Huiskes R, Lips P (1996) Osteocyte density changes in aging and osteoporosis. Bone 18:109–113

    Article  PubMed  CAS  Google Scholar 

  14. Rickard DJ, Kassem M, Hefferan TE, Sarkar G, Spelsberg TC, Riggs BL (1996) Isolation and characterization of osteoblast precursor cells from human bone marrow. J Bone Miner Res 11:312–324

    Article  PubMed  CAS  Google Scholar 

  15. Rosen CJ, Bouxsein ML (2006) Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2:35–43

    Article  PubMed  CAS  Google Scholar 

  16. Kawai M, Devlin MJ, Rosen CJ (2009) Fat targets for skeletal health. Nat Rev Rheumatol 5:365–372

    Article  PubMed  Google Scholar 

  17. Duque G, Li W, Adams M, Xu S, Phipps R (2010) Effects of risedronate on bone marrow adipocytes in postmenopausal women. Osteoporos Int

  18. Luu YK, Capilla E, Rosen CJ, Gilsanz V, Pessin JE, Judex S, Rubin CT (2009) Mechanical stimulation of mesenchymal stem cell proliferation and differentiation promotes osteogenesis while preventing dietary-induced obesity. J Bone Miner Res 24:50–61

    Article  PubMed  CAS  Google Scholar 

  19. Sen B, Xie Z, Case N, Styner M, Rubin CT, Rubin J (2011) Mechanical signal influence on mesenchymal stem cell fate is enhanced by incorporation of refractory periods into the loading regimen. J Biomech 44:593–599

    Article  PubMed  Google Scholar 

  20. Vande Berg BC, Malghem J, Lecouvet FE, Maldague B (1998) Magnetic resonance imaging of normal bone marrow. Eur Radiol 8:1327–1334

    Article  PubMed  CAS  Google Scholar 

  21. Bosy-Westphal A, Later W, Schautz B, Lagerpusch M, Goele K, Heller M, Gluer CC, Muller MJ (2011) Impact of intra- and extra-osseous soft tissue composition on changes in bone mineral density with weight loss and regain. Obesity (Silver Spring) 19:1503–1510

    Article  Google Scholar 

  22. Abate N, Burns D, Peshock RM, Garg A, Grundy SM (1994) Estimation of adipose tissue mass by magnetic resonance imaging: validation against dissection in human cadavers. J Lipid Res 35:1490–1496

    PubMed  CAS  Google Scholar 

  23. Mitsiopoulos N, Baumgartner RN, Heymsfield SB, Lyons W, Gallagher D, Ross R (1998) Cadaver validation of skeletal muscle measurement by magnetic resonance imaging and computerized tomography. J Appl Physiol 85:115–122

    PubMed  CAS  Google Scholar 

  24. Albu JB, Kovera AJ, Allen L, Wainwright M, Berk E, Raja-Khan N, Janumala I, Burkey B, Heshka S, Gallagher D (2005) Independent association of insulin resistance with larger amounts of intermuscular adipose tissue and a greater acute insulin response to glucose in African American than in white nondiabetic women. Am J Clin Nutr 82:1210–1217

    PubMed  CAS  Google Scholar 

  25. Brambilla P, Bedogni G, Moreno LA, Goran MI, Gutin B, Fox KR, Peters DM, Barbeau P, De Simone M, Pietrobelli A (2006) Crossvalidation of anthropometry against magnetic resonance imaging for the assessment of visceral and subcutaneous adipose tissue in children. Int J Obes (Lond) 30:23–30

    Article  CAS  Google Scholar 

  26. Janssen I, Ross R (1999) Effects of sex on the change in visceral, subcutaneous adipose tissue and skeletal muscle in response to weight loss. Int J Obes Relat Metab Disord 23:1035–1046

    Article  PubMed  CAS  Google Scholar 

  27. Ross R, Leger L, Morris D, Jd G, Guardo R (1992) Quantification of adipose tissue by MRI: relationship with anthropometric variables. J Appl Physiol 72:787–795

    PubMed  CAS  Google Scholar 

  28. Owens S, Litaker M, Allison J, Riggs S, Ferguson M, Gutin B (1999) Prediction of visceral adipose tissue from simple anthropometric measurements in youths with obesity. Obes Res 7:16–22

    PubMed  CAS  Google Scholar 

  29. Grunfeld C, Rimland D, Gibert CL, Powderly WG, Sidney S, Shlipak MG, Bacchetti P, Scherzer R, Haffner S, Heymsfield SB (2007) Association of upper trunk and visceral adipose tissue volume with insulin resistance in control and HIV-infected subjects in the FRAM study. J Acquir Immune Defic Syndr 46:283–290

    Article  PubMed  Google Scholar 

  30. Demerath EW, Sun SS, Rogers N et al (2007) Anatomical patterning of visceral adipose tissue: race, sex, and age variation. Obesity (Silver Spring) 15:2984–2993

    Article  Google Scholar 

  31. Xiang QS (2006) Two-point water–fat imaging with partially-opposed-phase (POP) acquisition: an asymmetric Dixon method. Magn Reson Med 56:572–584

    Article  PubMed  Google Scholar 

  32. Costa DN, Pedrosa I, McKenzie C, Reeder SB, Rofsky NM (2008) Body MRI using IDEAL. AJR Am J Roentgenol 190:1076–1084

    Article  PubMed  Google Scholar 

  33. Meisamy S, Hines CD, Hamilton G, Sirlin CB, McKenzie CA, Yu H, Brittain JH, Reeder SB (2011) Quantification of hepatic steatosis with T1-independent, T2-corrected MR imaging with spectral modeling of fat: blinded comparison with MR spectroscopy. Radiology 258:767–775

    Article  PubMed  Google Scholar 

  34. Russell-Aulet M, Wang J, Thornton J, Pierson RNJ (1991) Comparison of dual-photon absorptiometry systems for total-body bone and soft tissue measurements: dual-energy X-rays versus gadolinium 153. J Bone Miner Res 6:411–415

    Article  PubMed  CAS  Google Scholar 

  35. Wu CH, Heshka S, Wang J, Pierson RN Jr, Heymsfield SB, Laferrere B, Wang Z, Albu JB, Pi-Sunyer X, Gallagher D (2007) Truncal fat in relation to total body fat: influences of age, sex, ethnicity and fatness. Int J Obes (Lond) 31:1384–1391

    Article  Google Scholar 

  36. Gallagher D, Belmonte D, Deurenberg P, Wang Z, Krasnow N, Pi-Sunyer FX, Heymsfield SB (1998) Organ-tissue mass measurement allows modeling of REE and metabolically active tissue mass. Am J Physiol 275:E249–258

    PubMed  CAS  Google Scholar 

  37. Heymsfield SB, Gallagher D, Kotler DP, Wang Z, Allison DB, Heshka S (2002) Body-size dependence of resting energy expenditure can be attributed to nonenergetic homogeneity of fat-free mass. Am J Physiol Endocrinol Metab 282:E132–138

    PubMed  CAS  Google Scholar 

  38. Shen W, Wang Z, Tang H, Heshka S, Punyanitya M, Zhu S, Lei J, Heymsfield SB (2003) Volume estimates derived in vivo by imaging methods: model comparisons with visible woman as the reference. Obes Res 11:217–225

    Article  PubMed  Google Scholar 

  39. (2004) NIST/SEMATECH e-Handbook of statistical methods. http://www.itl.nist.gov/div898/handbook/eda/section3/eda336.htm Accessed September 29th, 2004

  40. Moerman EJ, Teng K, Lipschitz DA, Lecka-Czernik B (2004) Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: the role of PPAR-gamma2 transcription factor and TGF-beta/BMP signaling pathways. Aging Cell 3:379–389

    Article  PubMed  CAS  Google Scholar 

  41. Schellinger D, Lin CS, Hatipoglu HG, Fertikh D (2001) Potential value of vertebral proton MR spectroscopy in determining bone weakness. AJNR Am J Neuroradiol 22:1620–1627

    PubMed  CAS  Google Scholar 

  42. 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 2:165–171

    Article  PubMed  CAS  Google Scholar 

  43. Fu X, Ma X, Lu H, He W, Wang Z, Zhu S (2011) Associations of fat mass and fat distribution with bone mineral density in pre- and postmenopausal Chinese women. Osteoporos Int 22:113–119

    Article  PubMed  CAS  Google Scholar 

  44. Pouilles JM, Tremollieres F, Ribot C (1993) The effects of menopause on longitudinal bone loss from the spine. Calcif Tissue Int 52:340–343

    Article  PubMed  CAS  Google Scholar 

  45. Riis BJ, Hansen MA, Jensen AM, Overgaard K, Christiansen C (1996) Low bone mass and fast rate of bone loss at menopause: equal risk factors for future fracture: a 15-year follow-up study. Bone 19:9–12

    Article  PubMed  CAS  Google Scholar 

  46. Scane AC, Sutcliffe AM, Francis RM (1993) Osteoporosis in men. Baillieres Clin Rheumatol 7:589–601

    Article  PubMed  CAS  Google Scholar 

  47. Slemenda C, Hui SL, Longcope C, Johnston CC (1987) Sex steroids and bone mass. A study of changes about the time of menopause. J Clin Invest 80:1261–1269

    Article  PubMed  CAS  Google Scholar 

  48. Englund U, Littbrand H, Sondell A, Pettersson U, Bucht G (2005) A 1-year combined weight-bearing training program is beneficial for bone mineral density and neuromuscular function in older women. Osteoporos Int 16:1117–1123

    Article  PubMed  Google Scholar 

  49. Edelstein SL, Barrett-Connor E (1993) Relation between body size and bone mineral density in elderly men and women. Am J Epidemiol 138:160–169

    PubMed  CAS  Google Scholar 

  50. Gilsanz V, Roe TF, Mora S, Costin G, Goodman WG (1991) Changes in vertebral bone density in Black girls and White girls during childhood and puberty. N Engl J Med 325:1597–1600

    Article  PubMed  CAS  Google Scholar 

  51. Araujo AB, Travison TG, Harris SS, Holick MF, Turner AK, McKinlay JB (2007) Race/ethnic differences in bone mineral density in men. Osteoporos Int 18:943–953

    Article  PubMed  CAS  Google Scholar 

  52. Tracy JK, Meyer WA, Flores RH, Wilson PD, Hochberg MC (2005) Racial differences in rate of decline in bone mass in older men: the Baltimore men’s osteoporosis study. J Bone Miner Res 20:1228–1234

    Article  PubMed  Google Scholar 

  53. Sheu Y, Cauley JA, Wheeler VW, Patrick AL, Bunker CH, Ensrud KE, Orwoll ES, Zmuda JM (2011) Age-related decline in bone density among ethnically diverse older men. Osteoporos Int 22:599–605

    Article  PubMed  CAS  Google Scholar 

  54. 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 94:3387–3393

    Article  PubMed  CAS  Google Scholar 

  55. Katzmarzyk PT, Barreira TV, Harrington DM, Staiano AE, Heymsfield SB, Gimble JM (2011) Relationship between abdominal fat and bone mineral density in White and African American adults. Bone. Epubdate: 2011 May 10

  56. Lu H, Fu X, Ma X, Wu Z, He W, Wang Z, Allison DB, Heymsfield SB, Zhu S (2011) Relationships of percent body fat and percent trunk fat with bone mineral density among Chinese, Black, and White subjects. Osteoporos Int. Epub date: 2011 Jan 19

  57. Bredella MA, Torriani M, Ghomi RH, Thomas BJ, Brick DJ, Gerweck AV, Rosen CJ, Klibanski A, Miller KK (2011) Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity (Silver Spring) 19:49–53

    Article  CAS  Google Scholar 

  58. Hangartner TN, Johnston CC (1990) Influence of fat on bone measurements with dual-energy absorptiometry. Bone Miner 9:71–81

    Article  PubMed  CAS  Google Scholar 

  59. Bolotin HH, Sievanen H, Grashuis JL (2003) Patient-specific DXA bone mineral density inaccuracies: quantitative effects of nonuniform extraosseous fat distributions. J Bone Miner Res 18:1020–1027

    Article  PubMed  CAS  Google Scholar 

  60. Somjen D, Katzburg S, Kohen F, Gayer B, Posner GH, Yoles I, Livne E (2011) The effects of native and synthetic estrogenic compounds as well as vitamin D less-calcemic analogs on adipocytes content in rat bone marrow. J Endocrinol Invest 34:106–110

    PubMed  CAS  Google Scholar 

  61. Looker AC (2005) Body fat and vitamin D status in Black versus White women. J Clin Endocrinol Metab 90:635–640

    Article  PubMed  CAS  Google Scholar 

  62. Cauley JA, Danielson ME, Boudreau R, et al. (2011) Serum 25 hydroxyvitamin (OH)D and clinical fracture risk in a multiethnic cohort of women: the Women’s Health Initiative (WHI). J Bone Miner Res. Epub date: 2011 Jun 29

  63. (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: report of a WHO study group. In. World Health Organization, Geneva, Switzerland

  64. Lang T, Augat P, Majumdar S, Ouyang X, Genant HK (1998) Noninvasive assessment of bone density and structure using computed tomography and magnetic resonance. Bone 22:149S–153S

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The project described was supported by Award Number R21DK082937 from the National Institute of Diabetes, Digestive and Kidney Diseases. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institute of Diabetes, Digestive and Kidney Diseases or the National Institutes of Health.

The project was also supported by the National Institutes of Health Grants R01 DK40414, R01 DK42618 and P30 DK26687, R29-AG14715, F32-AG05679, M01 RR00645 and UL1 RR024156.

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Shen, W., Chen, J., Gantz, M. et al. Ethnic and sex differences in bone marrow adipose tissue and bone mineral density relationship. Osteoporos Int 23, 2293–2301 (2012). https://doi.org/10.1007/s00198-011-1873-x

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