Skip to main content
SpringerLink
Log in

Adiposity and bone microarchitecture in the GLOW study

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

Low body mass index (BMI) is an established risk factor for fractures in postmenopausal women but the interaction of obesity with bone microarchitecture is not fully understood. In this study, obesity was associated with more favourable bone microarchitecture parameters but not after parameters were normalised for body weight.

Introduction

To examine bone microarchitecture in relation to fat mass and examine both areal bone mineral density (aBMD) and microarchitecture in relation to BMI categories in the UK arm of the Global Longitudinal Study of Osteoporosis in Women.

Methods

Four hundred and ninety-one women completed questionnaires detailing medical history; underwent anthropometric assessment; high-resolution peripheral quantitative computed tomography (HRpQCT) scans of the radius and tibia and DXA scans of whole body, proximal femur and lumbar spine. Fat mass index (FMI) residuals (independent of lean mass index) were derived. Linear regression was used to examine HRpQCT and DXA aBMD parameters according to BMI category (unadjusted) and HRpQCT parameters in relation to FMI residuals (with and without adjustment for anthropometric, demographic and lifestyle covariates).

Results

Mean (SD) age was 70.9 (5.4) years; 35.0% were overweight, 14.5% class 1 obese and 7.7% class 2/3 obese. There were significant increasing trends according to BMI category in aBMD of whole body, hip, femoral neck and lumbar spine (p ≤ 0.001); cortical area (p < 0.001), thickness (p < 0.001) and volumetric density (p < 0.03), and trabecular number (p < 0.001), volumetric density (p < 0.04) and separation (p < 0.001 for decreasing trend) at the radius and tibia. When normalised for body weight, all HRpQCT and DXA aBMD parameters decreased as BMI increased (p < 0.001). FMI residuals were associated with bone size and trabecular architecture at the radius and tibia, and tibial cortical microarchitecture.

Conclusion

Significant trends in HRpQCT parameters suggested favourable bone microarchitecture at the radius and tibia with increasing BMI but these were not proportionate to increased weight.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. (1993) Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis. In: The American Journal of Medicine. pp 646–650

  2. Hernlund E, Svedbom A, Ivergård M et al (2013) Osteoporosis in the European Union: medical management, epidemiology and economic burden: a report prepared in collaboration with the International Osteoporosis Foundation (IOF) and the European Federation of Pharmaceutical Industry Associations (EFPIA). Arch Osteoporos 8. https://doi.org/10.1007/s11657-013-0136-1

  3. Reginster JY, Burlet N (2006) Osteoporosis: a still increasing prevalence. Bone 38:4–9. https://doi.org/10.1016/j.bone.2005.11.024

    Article  Google Scholar 

  4. US Department of Health and Human Services (2004) Bone health and osteoporosis: a report of the Surgeon General. US Heal Hum Serv 32:219–228. https://doi.org/10.2165/00002018-200932030-00004

    Article  Google Scholar 

  5. Van Staa TP, Dennison EM, Leufkens HGM, Cooper C (2001) Epidemiology of fractures in England and Wales. Bone 29:517–522. https://doi.org/10.1016/S8756-3282(01)00614-7

    Article  PubMed  Google Scholar 

  6. Burge R, Dawson-Hughes B, Solomon DH et al (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J Bone Miner Res. https://doi.org/10.1359/jbmr.061113

  7. De Laet C, Kanis JA, Odén A et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int 16:1330–1338. https://doi.org/10.1007/s00198-005-1863-y

    Article  PubMed  Google Scholar 

  8. Compston JE, Watts NB, Chapurlat R et al (2011) Obesity is not protective against fracture in postmenopausal women: Glow. Am J Med. https://doi.org/10.1016/j.amjmed.2011.06.013

  9. Beck TJ, Petit MA, Wu G et al (2009) Does obesity really make the femur stronger? BMD, geometry, and fracture incidence in the women’s health initiative-observational study. J Bone Miner Res. https://doi.org/10.1359/jbmr.090307

  10. Prieto-Alhambra D, Premaor MO, Fina Avilés F et al (2012) The association between fracture and obesity is site-dependent: A population-based study in postmenopausal women. J Bone Miner Res. https://doi.org/10.1002/jbmr.1466

  11. Premaor MO, Pilbrow L, Tonkin C et al (2010) Obesity and fractures in postmenopausal women. J Bone Miner Res. https://doi.org/10.1359/jbmr.091004

  12. Gnudi S, Sitta E, Lisi L (2009) Relationship of body mass index with main limb fragility fractures in postmenopausal women. J Bone Miner Metab. https://doi.org/10.1007/s00774-009-0056-8

  13. Sornay-Rendu E, Boutroy S, Vilayphiou N et al (2013) In obese postmenopausal women, bone microarchitecture and strength are not commensurate to greater body weight: The OS des femmes de Lyon (OFELY) study. J Bone Miner Res. https://doi.org/10.1002/jbmr.1880

  14. Friedman AW (2006) Important determinants of bone strength: beyond bone mineral density. J Clin Rheumatol 12:70–77. https://doi.org/10.1353/psg.2006.0122

    Article  PubMed  Google Scholar 

  15. Pollock NK, Laing EM, Baile CA et al (2007) Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr. https://doi.org/10.1093/ajcn/86.5.1530

  16. Farr JN, Chen Z, Lisse JR et al (2010) Relationship of total body fat mass to weight-bearing bone volumetric density, geometry, and strength in young girls. Bone. https://doi.org/10.1016/j.bone.2009.12.033

  17. Edwards MH, Ward KA, Ntani G et al (2015) Lean mass and fat mass have differing associations with bone microarchitecture assessed by high resolution peripheral quantitative computed tomography in men and women from the Hertfordshire Cohort Study. Bone. https://doi.org/10.1016/j.bone.2015.07.013

  18. Gibbs JC, Giangregorio LM, Wong AKO et al (2017) Appendicular and whole body lean mass outcomes are associated with finite element analysis-derived bone strength at the distal radius and tibia in adults aged 40 years and older. Bone. https://doi.org/10.1016/j.bone.2017.06.006

  19. Evans AL, Paggiosi MA, Eastell R, Walsh JS (2015) Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J Bone Miner Res 30:920–928. https://doi.org/10.1002/jbmr.2407

    Article  PubMed  Google Scholar 

  20. Hooven FH, Adachi JD, Adami S et al (2009) The Global Longitudinal Study of Osteoporosis in Women (GLOW): Rationale and study design. Osteoporos Int. https://doi.org/10.1007/s00198-009-0958-2

  21. Pialat JB, Burghardt AJ, Sode M, Link TM, Majumdar S (2012) Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone 50:111–118. https://doi.org/10.1016/j.bone.2011.10.003

    Article  CAS  PubMed  Google Scholar 

  22. Burghardt AJ, Kazakia GJ, Ramachandran S, Link TM, Majumdar S (2010) Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J Bone Miner Res 25:983–993. https://doi.org/10.1359/jbmr.091104

    Article  PubMed  Google Scholar 

  23. Morin S, Leslie WD (2009) High bone mineral density is associated with high body mass index. Osteoporos Int 20:1267–1271. https://doi.org/10.1007/s00198-008-0797-6

    Article  CAS  PubMed  Google Scholar 

  24. Pesonen J, Sirola J, Tuppurainen M, Jurvelin J, Alhava E, Honkanen R, Kr H (2005) High bone mineral density among perimenopausal women. Osteoporos Int 16:1899–1906. https://doi.org/10.1007/s00198-005-1958-5

    Article  PubMed  Google Scholar 

  25. Nielson CM, Bouxsein ML, Freitas SS, Ensrud KE, Orwoll ES, for the Osteoporotic Fractures in Men (MrOS) Research Group (2009) Trochanteric soft tissue thickness and hip fracture in older men. J Clin Endocrinol Metab 94:491–496. https://doi.org/10.1210/jc.2008-1640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sukumar D, Schlussel Y, Riedt CS, Gordon C, Stahl T, Shapses SA (2011) Obesity alters cortical and trabecular bone density and geometry in women. Osteoporos Int 22:635–645. https://doi.org/10.1007/s00198-010-1305-3

    Article  CAS  PubMed  Google Scholar 

  27. Mitrou P, Lambadiari V, Maratou E et al (2011) Skeletal muscle insulin resistance in morbid obesity: The role of interleukin-6 and leptin. Exp Clin Endocrinol Diabetes. https://doi.org/10.1055/s-0030-1269846

  28. Thomas T, Burguera B (2002) Is leptin the link between fat and bone mass? J Bone Miner Res. https://doi.org/10.1359/jbmr.2002.17.9.1563

  29. Kawai M, Devlin MJ, Rosen CJ (2009) Fat targets for skeletal health. Nat Rev Rheumatol 5(7):365–372

  30. Gomez R, Lago F, Gomez-Reino J et al (2009) Adipokines in the skeleton: Influence on cartilage function and joint degenerative diseases. J Mol Endocrinol 43(1):11–18

  31. Gómez-Ambrosi J, Rodríguez A, Catalán V, Frühbeck G (2008) The bone-adipose axis in obesity and weight loss. Obes Surg 18(9):1134–1143

  32. Schett G (2011) Effects of inflammatory and anti-inflammatory cytokines on the bone. Eur J Clin Invest 41(12):1361–1366

  33. Wellen KE, Hotamisligil GS (2005) Inflammation, stress, and diabetes. J Clin Invest 115(5):1111–1119

  34. Fain JN, Madan AK, Hiler ML et al (2004) Comparison of the release of adipokines by adipose tissue, adipose tissue matrix, and adipocytes from visceral and subcutaneous abdominal adipose tissues of obese humans. Endocrinology. https://doi.org/10.1210/en.2003-1336

  35. Fain JN (2006) Release of interleukins and other inflammatory cytokines by human adipose tissue is enhanced in obesity and primarily due to the nonfat cells. Vitam Horm

  36. Perneger TV (1998) What’s wrong with Bonferroni adjustments. Br Med J 316:1236–1238

    Article  CAS  Google Scholar 

Download references

Availability of data and material

Not applicable.

Funding

We thank the Arthritis Research UK for their support: Arthritis Research UK grant number 20380.

Author information

Authors and Affiliations

  1. MRC Lifecourse Epidemiology Unit, University of Southampton, Southampton, UK

    A.E. Litwic, L.D. Westbury, K. Ward, C. Cooper & E.M. Dennison

  2. Department of Nephrology, Transplantology and Internal Medicine, Medical University of Gdańsk, Gdańsk, Poland

    A.E. Litwic

  3. NIHR Southampton Biomedical Research Centre, University of Southampton and University Hospital Southampton NHS Foundation Trust, Southampton, UK

    C. Cooper

  4. NIHR Oxford Biomedical Research Centre, University of Oxford, Oxford, UK

    C. Cooper

  5. Victoria University of Wellington, Wellington, New Zealand

    E.M. Dennison

Authors
  1. A.E. Litwic
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L.D. Westbury
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Ward
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. C. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E.M. Dennison
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E.M. Dennison.

Ethics declarations

Conflicts of interest

A.E. Litwic, L.D. Westbury and K.A. Ward declare that they have no conflict of interest. C Cooper reports personal fees (outside the submitted work) from Amgen, Danone, Eli Lilly, GSK, Kyowa Kirin, Medtronic, Merck, Nestle, Novartis, Pfizer, Roche, Servier, Shire, Takeda and UCB. EM Dennison reports personal fees (outside the submitted work) from Pfizer Healthcare and UCB.

Ethics approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Code availability

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Litwic, A., Westbury, L., Ward, K. et al. Adiposity and bone microarchitecture in the GLOW study. Osteoporos Int 32, 689–698 (2021). https://doi.org/10.1007/s00198-020-05603-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-020-05603-w

Keywords

Search

Navigation