Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Techniques and Methods

Improved femoral micro-architecture in adult male individuals with overweight: fracture resistance due to regional specificities

International Journal of Obesity (2023)Cite this article

Subjects

Abstract

Background

It is still unclear whether femoral fracture risk is positively or negatively altered in individuals with overweight. Considering the lack of studies including men with overweight, this study aimed to analyze regional specificities in mechano-structural femoral properties (femoral neck and intertrochanteric region) in adult male cadavers with overweight compared to their normal-weight age-matched counterparts.

Methods

Ex-vivo osteodensitometry, micro-computed tomography, and Vickers micro-indentation testing were performed on femoral samples taken from 30 adult male cadavers, divided into the group with overweight (BMI between 25 and 30 kg/m2; n = 14; age:55 ± 16 years) and control group (BMI between 18.5 and 25 kg/m2; n = 16; age:51 ± 18 years).

Results

Better quality of trabecular and cortical microstructure in the inferomedial (higher trabecular bone volume fraction, trabecular thickness, and cortical thickness, coupled with reduced cortical pore diameter, p < 0.05) and superolateral femoral neck (higher trabecular number and tendency to lower cortical porosity, p = 0.043, p = 0.053, respectively) was noted in men with overweight compared to controls. Additionally, the intertrochanteric region of men with overweight had more numerous and denser trabeculae, coupled with a thicker and less porous cortex (p < 0.05). Still, substantial overweight-induced change in femoral osteodensitometry parameters and Vickers micro-hardness was not demonstrated in assessed femoral subregions (p > 0.05).

Conclusions

Despite the absence of significant changes in femoral osteodensitometry, individuals with overweight had better trabecular and cortical femoral micro-architecture implying higher femoral fracture resistance. However, the microhardness was not significantly favorable in the individuals who were overweight, indicating the necessity for further research.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The methodological steps used to assess femoral mechano-structure in individuals with overweight.
Fig. 2: The comparison of the representative femoral micro-architectural parameters between individuals with overweight and their age-matched normal-weight counterparts.
Fig. 3: The region-specific percentage of the difference between the group with overweight and control group in representative micro-architectural parameters.

Data availability

Data generated during this study are available from the corresponding author (MD) upon justified request.

References

  1. Palermo A, Tuccinardi D, Defeudis G, Watanabe M, D’Onofrio L, Lauria AP, et al. BMI and BMD: The potential interplay between obesity and bone fragility. Int J Environ Res Public Health. 2016;13:544.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Hebebrand J, Holm JC, Woodward E, Baker JL, Blaak E, Durrer Schutz D, et al. A proposal of the European association for the study of obesity to Improve the ICD-11 diagnostic criteria for obesity based on the three dimensions etiology, degree of adiposity and health risk. Obes Facts. 2017;10:284–307.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Shapses SA, Pop LC, Wang Y. Obesity is a concern for bone health with aging. Nutr Res. 2017;39:1–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Anandacoomarasamy A, Caterson I, Sambrook P, Fransen M, March L. The impact of obesity on the musculoskeletal system. Int J Obes. 2008;32:211–22.

    Article  CAS  Google Scholar 

  5. Cawsey S, Padwal R, Sharma AM, Wang X, Li S, Siminoski K. Women with severe obesity and relatively low bone mineral density have increased fracture risk. Osteoporos Int. 2014;26:103–11.

    Article  PubMed  Google Scholar 

  6. Tang X, Liu G, Kang J, Hou Y, Jiang F, Yuan W, et al. Obesity and risk of hip fracture in adults: a meta-analysis of prospective cohort studies. PLoS One. 2013;8:6–12.

    Google Scholar 

  7. Prieto-Alhambra D, Premaor MO, Fina Avilés F, Hermosilla E, Martinez-Laguna D, Carbonell-Abella C, et al. The association between fracture and obesity is site-dependent: A population-based study in postmenopausal women. J Bone Miner Res. 2012;27:294–300.

    Article  PubMed  Google Scholar 

  8. Premaor MO, Compston JE, Fina Avilés F, Pagès-Castellà A, Nogués X, Díez-Pérez A, et al. The association between fracture site and obesity in men: a population-based cohort study. J Bone Miner Res. 2013;28:1771–7.

    Article  PubMed  Google Scholar 

  9. Premaor MO, Ensrud K, Lui L, Parker RA, Cauley J, Hillier TA, et al. Risk factors for nonvertebral fracture in obese older women. J Clin Endocrinol Metab. 2011;96:2414–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Li X, Gong X, Jiang W. Abdominal obesity and risk of hip fracture: a meta-analysis of prospective studies. Osteoporos Int. 2017;28:2747–57.

    Article  CAS  PubMed  Google Scholar 

  11. Greco EA, Fornari R, Rossi F, Santiemma V, Prossomariti G, Annoscia C, et al. Is obesity protective for osteoporosis? Evaluation of bone mineral density in individuals with high body mass index. Int J Clin Pract. 2010;64:817–20.

    Article  CAS  PubMed  Google Scholar 

  12. Migliaccio S, Greco EA, Fornari R, Donini LM, Lenzi A. Is obesity in women protective against osteoporosis? Diabetes Metab Syndr Obes Targets Ther. 2011;4:273–82.

    Article  Google Scholar 

  13. Rikkonen T, Sund R, Sirola J, Honkanen R, Poole KES, Kröger H. Obesity is associated with early hip fracture risk in postmenopausal women: a 25-year follow-up. Osteoporos Int. 2021;32:769–77.

    Article  CAS  PubMed  Google Scholar 

  14. Nielson CM, Marshall LM, Adams AL, Leblanc ES, Cawthon PM, Ensrud K, et al. BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res. 2011;26:496–502.

    Article  PubMed  Google Scholar 

  15. Lee JS, Kawakubo K, Sato H, Kobayashi Y, Haruna Y. Relationship between total and regional bone mineral density and menopausal state, body composition and life style factors in overweight Japanese women. Int J Obes. 2001;25:880–6.

    Article  CAS  Google Scholar 

  16. Jadzic J, Mijucic J, Nikolic S, Djuric M, Djonic D. The comparison of age- and sex-specific alteration in pubic bone microstructure: a cross-sectional cadaveric study. Exp Gerontol. 2021;150:111375.

    Article  PubMed  Google Scholar 

  17. Djonic D, Milovanovic P, Nikolic S, Ivovic M, Marinkovic J, Beck T, et al. Inter-sex differences in structural properties of aging femora: implications on differential bone fragility: a cadaver study. J Bone Miner Metab. 2011;29:449–57.

    Article  PubMed  Google Scholar 

  18. Cauley JA. Estrogen and bone health in men and women. Steroids. 2015;99:11–15.

    Article  CAS  PubMed  Google Scholar 

  19. Shanbhogue VV, Støving RK, Frederiksen KH, Hanson S, Brixen K, Gram J, et al. Bone structural changes after gastric bypass surgery evaluated by HR-pQCT: a two-year longitudinal study. Eur J Endocrinol. 2017;176:685–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Yu EW, Thomas BJ, Brown JK, Finkelstein JS. Simulated increases in body fat and errors in bone mineral density measurements by DXA and QCT. J Bone Miner Res. 2012;27:119–24.

    Article  PubMed  Google Scholar 

  21. De Laet C, Kanis JA, Oden A, Johansson H, Johnell O, Delmas PD, et al. Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporos Int. 2005;16:1330–8.

    Article  PubMed  Google Scholar 

  22. Caffarelli C, Alessi C, Nuti R, Gonnelli S. Divergent effects of obesity on fragility fractures. Clin Interv Aging. 2014;9:1629–36.

    PubMed  PubMed Central  Google Scholar 

  23. Link TM, Heilmeier U. Bone quality — beyond bone mineral density. Semin Musculoskelet Radiol. 2016;20:269–78.

    Article  PubMed  Google Scholar 

  24. Evans AL, Paggiosi MA, Eastell R, Walsh JS. Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J Bone Miner Res. 2015;30:920–8.

    Article  PubMed  Google Scholar 

  25. Bredella MA, Lin E, Gerweck AV, Landa MG, Thomas BJ, Torriani M, et al. Determinants of bone microarchitecture and mechanical properties in obese men. J Clin Endocrinol Metab. 2012;97:4115–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Andersen S, Frederiksen KD, Hansen S, Brixen K, Gram J, Støving RK. Bone structure and estimated bone strength in obese patients evaluated by high-resolution peripheral quantitative computed tomography. Calcif Tissue Int. 2014;95:19–28.

    Article  CAS  PubMed  Google Scholar 

  27. Giner M, Montoya MJ, Miranda C, Vázquez MA, Miranda MJ, Pérez-Cano R. Influence of obesity on microarchitecture and biomechanical properties in patients with hip fracture. Rev Osteoporos y Metab Miner. 2017;9:20–6.

    Article  CAS  Google Scholar 

  28. Sornay-Rendu E, Boutroy S, Vilayphiou N, Claustrat B, Chapurlat RD. 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. 2013;28:1679–87.

    Article  CAS  PubMed  Google Scholar 

  29. Folli F, Sabowitz BN, Schwesinger W, Fanti P, Guardado-Mendoza R, Muscogiuri G. Bariatric surgery and bone disease: from clinical perspective to molecular insights. Int J Obes. 2012;36:1373–9.

    Article  CAS  Google Scholar 

  30. Djuric M, Djonic D, Milovanovic P, Nikolic S, Marshall R, Marinkovic J, et al. Region-specific sex-dependent pattern of age-related changes of proximal femoral cancellous bone and its implications on differential bone fragility. Calcif Tissue Int. 2010;86:192–201.

    Article  CAS  PubMed  Google Scholar 

  31. Jadzic J, Milovanovic P, Cvetkovic D, Ivovic M, Tomanovic N, Bracanovic M, et al. Mechano-structural alteration in proximal femora of individuals with alcoholic liver disease: implications for increased bone fragility. Bone. 2021;150:116020.

    Article  CAS  PubMed  Google Scholar 

  32. Beck TJ. Hip structural analysis (HSA) program. Cent Dis Control Prev. 2002;43:1–10.

    Google Scholar 

  33. Orwoll ES, Marshall LM, Nielson CM, Cummings SR, Lapidus J, Cauley JA, et al. Finite element analysis of the proximal femur and hip fracture risk in older men. J Bone Miner Res. 2009;24:475–83.

    Article  PubMed  Google Scholar 

  34. Ruiz Wills C, Olivares AL, Tassani S, Ceresa M, Zimmer V, González Ballester MA, et al. 3D patient-specific finite element models of the proximal femur based on DXA towards the classification of fracture and non-fracture cases. Bone. 2019;121:89–99.

    Article  PubMed  Google Scholar 

  35. Miura M, Nakamura J, Matsuura Y, Wako Y, Suzuki T, Hagiwara S, et al. Prediction of fracture load and stiffness of the proximal femur by CT-based specimen specific finite element analysis: cadaveric validation study. BMC Musculoskelet Disord. 2017;18:1–8.

    Article  Google Scholar 

  36. Ito M, Nishida A, Koga A, Ikeda S, Shiraishi A, Uetani M, et al. Contribution of trabecular and cortical components to the mechanical properties of bone and their regulating parameters. Bone. 2002;31:351–8.

    Article  CAS  PubMed  Google Scholar 

  37. Boivin G, Bala Y, Doublier A, Farlay D, Ste-Marie LG, Meunier PJ, et al. The role of mineralization and organic matrix in the microhardness of bone tissue from controls and osteoporotic patients. Bone. 2008;43:532–8.

    Article  CAS  PubMed  Google Scholar 

  38. Dall’Ara E, Öhman C, Baleani M, Viceconti M. The effect of tissue condition and applied load on Vickers hardness of human trabecular bone. J Biomech. 2007;40:3267–70.

    Article  PubMed  Google Scholar 

  39. Cohen A, Dempster DW, Recker RR, Lappe JM, Zhou H, Zwahlen A, et al. Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab. 2013;98:2562–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Ng AlvinC, Melton LJ, Atkinson EJ, Achenbach SJ, Holets MF, Peterson JM, et al. Relationship of adiposity to bone volumetric density and microstructure in men and women across the adult lifespan. Bone. 2013;55:119–25.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Franco-Trepat E, Guillán-Fresco M, Alonso-Pérez A, Jorge-Mora A, Francisco V, Gualillo O, et al. Visfatin connection: present and future in osteoarthritis and osteoporosis. J Clin Med. 2019;8:1178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Tanna N, Patel K, Moore AE, Dulnoan D, Edwards S, Hampson G. The relationship between circulating adiponectin, leptin and vaspin with bone mineral density (BMD), arterial calcification and stiffness: a cross-sectional study in post-menopausal women. J Endocrinol Investig. 2017;40:1345–53.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study received financial support from the Science Fund of the Republic of Serbia (IDEAS program, grant no. 7749444, BoFraM project) and the Ministry of Science of the Republic of Serbia (grant no. 200110 and 451–03–1524/2023–04/18). The Authors thank Dr. Miomira Ivovic for her valuable help during DXA scanning.

Author information

Authors and Affiliations

  1. Center of Bone Biology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia

    Jelena Jadzic, Uros Andjelic, Petar Milovanovic, Danijela Djonic & Marija Djuric

  2. Institute of Forensic Medicine, Faculty of Medicine, University of Belgrade, Belgrade, Serbia

    Vladimir Zivkovic & Slobodan Nikolic

Authors
  1. Jelena Jadzic
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Uros Andjelic
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Petar Milovanovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Vladimir Zivkovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Slobodan Nikolic
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Danijela Djonic
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marija Djuric
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

JJ, PM and MD conceptualized the study and used methodology. VZ and SN carried out sample collection. JJ and UA conducted data acquisition and wrote the original draft. All authors interpreted the results and provided review and editing of the manuscript. MD was responsible for project administration and funding acquisition. All authors approved the submitted version of the manuscript.

Corresponding author

Correspondence to Marija Djuric.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval

The Ethics Committee of the Faculty of Medicine, University of Belgrade confirmed that our study complied with relevant national and international standards based on the Declaration of Helsinki principles (approval no. 1322/VII-17). The Institutional Ethics Committee waived the informed consent requirement for collecting the samples included in the study.

Additional information

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jadzic, J., Andjelic, U., Milovanovic, P. et al. Improved femoral micro-architecture in adult male individuals with overweight: fracture resistance due to regional specificities. Int J Obes (2023). https://doi.org/10.1038/s41366-023-01389-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41366-023-01389-z

Search

Advanced search

Quick links