The associations between body fat distribution and bone mineral density in the Oxford Biobank: a cross sectional study

ABSTRACT Background Body composition is associated with bone mineral density (BMD), but the precise associations between body fat distribution and BMD remain unclear. The regional adipose tissue depots have different metabolic profiles. We hypothesized that they would have independent associations with BMD. Research Design and Methods We used data from 4,900 healthy individuals aged 30–50 years old from the Oxford Biobank to analyze associations between regional fat mass, lean mass and total BMD. Results Total lean mass was strongly positively associated with BMD. An increase in total BMD was observed with increasing mass of all the fat depots, as measured either by anthropometry or DXA, when accounting for lean mass. However, on adjustment for both total fat mass and lean mass, fat depot specific associations emerged. Increased android and visceral adipose tissue mass in men, and increased visceral adipose tissue mass in women, were associated with lower BMD. Conclusions Fat distribution alters the association between adiposity and BMD.

[1]  Yuezhong Ren,et al.  The impact of a high fat diet on bones: potential mechanisms. , 2021, Food & function.

[2]  Bo Hu,et al.  Relationships between anthropometric adiposity indexes and bone mineral density in a cross-sectional Chinese study. , 2020, The spine journal : official journal of the North American Spine Society.

[3]  Wei Liu,et al.  Effects of Laparoscopic Sleeve Gastrectomy on Bone Mineral Density and Bone Metabolism in Chinese Patients with Obesity , 2020, Diabetes, metabolic syndrome and obesity : targets and therapy.

[4]  Chunli Song,et al.  Short‐term caloric restriction induced bone loss in both axial and appendicular bones by increasing adiponectin , 2020, Annals of the New York Academy of Sciences.

[5]  P. Pietschmann,et al.  Osteoporosis and Sarcopenia Increase Frailty Syndrome in the Elderly , 2019, Front. Endocrinol..

[6]  F. Magkos,et al.  The epidemiology of obesity. , 2019, Metabolism: clinical and experimental.

[7]  Atul Gupta,et al.  The underlying pathophysiology and therapeutic approaches for osteoporosis , 2018, Medicinal research reviews.

[8]  C. Fall,et al.  Comparison of regional fat measurements by dual-energy X-ray absorptiometry and conventional anthropometry and their association with markers of diabetes and cardiovascular disease risk , 2017, International Journal of Obesity.

[9]  F. Karpe,et al.  Cohort Profile Cohort Profile : The Oxford Biobank , 2018 .

[10]  Anthony J Bishara,et al.  Confidence intervals for correlations when data are not normal , 2017, Behavior research methods.

[11]  D. Kiel,et al.  Visceral Adipose Tissue Is Associated With Bone Microarchitecture in the Framingham Osteoporosis Study , 2017, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[12]  J. Reginster,et al.  Osteoporosis and sarcopenia: two diseases or one? , 2015, Current opinion in clinical nutrition and metabolic care.

[13]  K. Zhu,et al.  Associations between body mass index, lean and fat body mass and bone mineral density in middle-aged Australians: The Busselton Healthy Ageing Study. , 2015, Bone.

[14]  F. Mauvais-Jarvis,et al.  The role of androgens in metabolism, obesity, and diabetes in males and females , 2015, Obesity.

[15]  M. McCarthy,et al.  LRP5 Regulates Human Body Fat Distribution by Modulating Adipose Progenitor Biology in a Dose- and Depot-Specific Fashion , 2015, Cell metabolism.

[16]  F. Karpe,et al.  Biology of upper-body and lower-body adipose tissue—link to whole-body phenotypes , 2015, Nature Reviews Endocrinology.

[17]  H. Nam,et al.  Sex-related differences in the association between waist circumference and bone mineral density in a Korean population , 2014, BMC Musculoskeletal Disorders.

[18]  Yuwei Wu,et al.  Central adiponectin administration reveals new regulatory mechanisms of bone metabolism in mice. , 2014, American journal of physiology. Endocrinology and metabolism.

[19]  J. Cornish,et al.  Cytokines and Hormones That Contribute to the Positive Association between Fat and Bone , 2014, Front. Endocrinol..

[20]  P. Xue,et al.  Associations between fat distribution and volumetric bone mineral density in Chinese adults , 2014, Endocrine.

[21]  S. Norris,et al.  The association between body composition, 25(OH)D, and PTH and bone mineral density in black African and Asian Indian population groups. , 2014, The Journal of clinical endocrinology and metabolism.

[22]  Y. Wang,et al.  Relationship of body composition with bone mineral density in northern Chinese men by body mass index levels , 2014, Journal of Endocrinological Investigation.

[23]  E. Tai,et al.  Associations between ethnicity, body composition, and bone mineral density in a Southeast Asian population. , 2013, The Journal of clinical endocrinology and metabolism.

[24]  N. Tandon,et al.  Relationship of body fat and its distribution with bone mineral density in Indian population. , 2013, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[25]  Binsheng Zhao,et al.  Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. , 2013, The Journal of clinical endocrinology and metabolism.

[26]  D. Christofaro,et al.  The relationship between visceral fat thickness and bone mineral density in sedentary obese children and adolescents , 2013, BMC Pediatrics.

[27]  Seongwon Cha,et al.  Bone Mineral Density-Associated Polymorphisms Are Associated with Obesity-Related Traits in Korean Adults in a Sex-Dependent Manner , 2012, PloS one.

[28]  L. Melton,et al.  Relationship of sympathetic activity to bone microstructure, turnover, and plasma osteopontin levels in women. , 2012, The Journal of clinical endocrinology and metabolism.

[29]  M. Bouxsein,et al.  Determinants of bone microarchitecture and mechanical properties in obese men. , 2012, The Journal of clinical endocrinology and metabolism.

[30]  F. Karpe,et al.  Marked resistance of femoral adipose tissue blood flow and lipolysis to adrenaline in vivo , 2012, Diabetologia.

[31]  Daniel L. Koller,et al.  Genome-wide meta-analysis identifies 56 bone mineral density loci and reveals 14 loci associated with risk of fracture , 2012, Nature Genetics.

[32]  Sung-il Cho,et al.  The association between fat and lean mass and bone mineral density: the Healthy Twin Study. , 2012, Bone.

[33]  Inês Barroso,et al.  A genome-wide association meta-analysis identifies new childhood obesity loci , 2012, Nature Genetics.

[34]  S. Heymsfield,et al.  Relationship between abdominal fat and bone mineral density in white and African American adults. , 2012, Bone.

[35]  David L. Ergun,et al.  Dual-Energy X-Ray Absorptiometry for Quantification of Visceral Fat , 2012, Obesity.

[36]  G. Schett Effects of inflammatory and anti‐inflammatory cytokines on the bone , 2011, European journal of clinical investigation.

[37]  H. Deng,et al.  The Fat Mass and Obesity Associated Gene, FTO, Is Also Associated with Osteoporosis Phenotypes , 2011, PloS one.

[38]  M. Brotto,et al.  Pge2 Accelerates Myogenesis of C2c12 Myoblasts , 2011 .

[39]  A. Silman,et al.  Characteristics of secondary, primary, and compensated hypogonadism in aging men: evidence from the European Male Ageing Study. , 2010, The Journal of clinical endocrinology and metabolism.

[40]  F. Karpe,et al.  Gluteofemoral body fat as a determinant of metabolic health , 2010, International Journal of Obesity.

[41]  M. Mittleman,et al.  Effects of myostatin deletion in aging mice , 2009, Aging cell.

[42]  H. Frost,et al.  A 2003 update of bone physiology and Wolff's Law for clinicians. , 2009, The Angle orthodontist.

[43]  Marybeth Brown,et al.  Skeletal muscle and bone: effect of sex steroids and aging. , 2008, Advances in physiology education.

[44]  J. Cauley,et al.  Bone Mineral Density Changes during the Menopause Transition in a Multiethnic Cohort of Women , 2008 .

[45]  C. K. Song,et al.  Sympathetic innervation of white adipose tissue and its regulation of fat cell number. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[46]  Patricia Ducy,et al.  Leptin Regulates Bone Formation via the Sympathetic Nervous System , 2002, Cell.

[47]  J. Kaufman,et al.  Estradiol in elderly men , 2002, The aging male : the official journal of the International Society for the Study of the Aging Male.

[48]  E. Poehlman,et al.  Menopause‐Related Changes in Body Fat Distribution , 2000, Annals of the New York Academy of Sciences.

[49]  G G Klee,et al.  Journal of Clinical Endocrinology and Metabolism Printed in U.S.A. Copyright © 1998 by The Endocrine Society Relationship of Serum Sex Steroid Levels and Bone Turnover Markers with Bone Mineral Density in Men and Women: A Key Role for Bioavailable Estroge , 2022 .

[50]  J S Yudkin,et al.  Journal of Clinical Endocrinology and Metabolism Printed in U.S.A. Copyright © 1997 by The Endocrine Society Subcutaneous Adipose Tissue Releases Interleukin-6, But Not Tumor Necrosis Factor-�, in Vivo* , 2022 .

[51]  I. Reid,et al.  Insulin increases histomorphometric indices of bone formation In vivo , 1996, Calcified Tissue International.

[52]  R. Blaauw,et al.  Body fat distribution as a risk factor for osteoporosis. , 1996, South African medical journal = Suid-Afrikaanse tydskrif vir geneeskunde.

[53]  J. Gimble,et al.  Bone morphogenetic proteins inhibit adipocyte differentiation by bone marrow stromal cells , 1995, Journal of cellular biochemistry.

[54]  A. Hofman,et al.  The association between age and bone mineral density in men and women aged 55 years and over: the Rotterdam Study. , 1994, Bone and mineral.

[55]  R. Turner,et al.  Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man , 1985, Diabetologia.

[56]  K. Rubinow Estrogens and Body Weight Regulation in Men. , 2017, Advances in experimental medicine and biology.

[57]  K. Zhu,et al.  Discordance between fat mass index and body mass index is associated with reduced bone mineral density in women but not in men: the Busselton Healthy Ageing Study , 2016, Osteoporosis International.

[58]  Yazeng Huang,et al.  Associations of fat mass and fat distribution with bone mineral density in Chinese obese population. , 2015, Journal of clinical densitometry : the official journal of the International Society for Clinical Densitometry.

[59]  M. Cowie National Institute for Health and Care Excellence. , 2015, European heart journal.

[60]  A. Hofman,et al.  Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam Study. , 2004, Bone.

[61]  T. Douchi,et al.  Relationship of upper body fat distribution to higher regional lean mass and bone mineral density , 2003, Journal of Bone and Mineral Metabolism.

[62]  B. Tarquini,et al.  Evidence for bone mass and body fat distribution relationship in postmenopausal obese women. , 1997, Archives of gerontology and geriatrics.