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Contribution of Mineral to Bone Structural Behavior and Tissue Mechanical Properties

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Abstract

Bone geometry and tissue material properties jointly govern whole-bone structural behavior. While the role of geometry in structural behavior is well characterized, the contribution of the tissue material properties is less clear, partially due to the multiple tissue constituents and hierarchical levels at which these properties can be characterized. Our objective was to elucidate the contribution of the mineral phase to bone mechanical properties across multiple length scales, from the tissue material level to the structural level. Vitamin D and calcium deficiency in 6-week-old male rats was employed as a model of reduced mineral content with minimal collagen changes. The structural properties of the humeri were measured in three-point bending and related to the mineral content and geometry from microcomputed tomography. Whole-cortex and local bone tissue properties were examined with infrared (IR) spectroscopy, Raman spectroscopy, and nanoindentation to understand the role of altered mineral content on the constituent material behavior. Structural stiffness (−47%) and strength (−50%) were reduced in vitamin D-deficient (−D) humeri relative to controls. Moment of inertia (−38%), tissue mineral density (TMD, −9%), periosteal mineralization (−28%), and IR mineral:matrix ratio (−19%) were reduced in −D cortices. Thus, both decreased tissue mineral content and changes in cortical geometry contributed to impaired skeletal load-bearing function. In fact, 97% of the variability in humeral strength was explained by moment of inertia, TMD, and IR mineral:matrix ratio. The strong relationships between structural properties and cortical material composition demonstrate a critical role of the microscale material behavior in skeletal load-bearing performance.

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Acknowledgment

We thank Dr. Stephen Doty and Jeanane Diouri for assistance with tissue processing and histology, Dr. Jacqueline Cole for assistance with mechanical testing and statistical analyses, Dr. Sylvia Christakos for advice on the study design, Hayat Taleb for X-ray diffraction and infrared spectroscopic analyses, and Dr. Junghyun Cho and Andy Zhang for help with nanoindentation. Funding was provided by the Cornell Center for Materials Research (NSF DMR 0520404), the National Institutes of Health (R01 AR053571, P30 AR046121), and the American Association of University Women Educational Foundation (Selected Professions Fellowship).

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Authors and Affiliations

  1. Sibley School of Mechanical and Aerospace Engineering, Cornell University, 219 Upson Hall, Ithaca, NY, 14853, USA

    Eve Donnelly & Marjolein C. H. van der Meulen

  2. Department of Biomedical Engineering, Cornell University, Ithaca, NY, USA

    Dan X. Chen

  3. Musculoskeletal Integrity Program, Hospital for Special Surgery, New York, NY, USA

    Adele L. Boskey & Marjolein C. H. van der Meulen

  4. Department of Biochemistry, Weill Medical College of Cornell University, New York, NY, USA

    Adele L. Boskey

  5. Graduate Program in Physiology, Biophysics, and Systems Biology, Weill Medical College of Cornell University, New York, NY, USA

    Adele L. Boskey

  6. Department of Materials Science and Engineering, Cornell University, Ithaca, NY, USA

    Shefford P. Baker

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  1. Eve Donnelly
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  2. Dan X. Chen
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  3. Adele L. Boskey
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  4. Shefford P. Baker
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  5. Marjolein C. H. van der Meulen
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Correspondence to Marjolein C. H. van der Meulen.

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The first two authors contributed equally to this study.

The authors have stated that they have no conflict of interest.

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Donnelly, E., Chen, D.X., Boskey, A.L. et al. Contribution of Mineral to Bone Structural Behavior and Tissue Mechanical Properties. Calcif Tissue Int 87, 450–460 (2010). https://doi.org/10.1007/s00223-010-9404-x

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