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The Role of Water Compartments in the Material Properties of Cortical Bone

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Abstract

Comprising ~20 % of the volume, water is a key determinant of the mechanical behavior of cortical bone. It essentially exists in two general compartments: within pores and bound to the matrix. The amount of pore water—residing in the vascular-lacunar-canalicular space—primarily reflects intracortical porosity (i.e., open spaces within the matrix largely due to Haversian canals and resorption sites) and as such is inversely proportional to most mechanical properties of bone. Movement of water according to pressure gradients generated during dynamic loading likely confers hydraulic stiffening to the bone as well. Nonetheless, bound water is a primary contributor to the mechanical behavior of bone in that it is responsible for giving collagen the ability to confer ductility or plasticity to bone (i.e., allows deformation to continue once permanent damage begins to form in the matrix) and decreases with age along with fracture resistance. Thus, dehydration by air-drying or by solvents with less hydrogen bonding capacity causes bone to become brittle, but interestingly, it also increases stiffness and strength across the hierarchical levels of organization. Despite the importance of matrix hydration to fracture resistance, little is known about why bound water decreases with age in hydrated human bone. Using 1H nuclear magnetic resonance (NMR), both bound and pore water concentrations in bone can be measured ex vivo because the proton relaxation times differ between the two water compartments, giving rise to two distinct signals. There are also emerging techniques to measure bound and pore water in vivo with magnetic resonance imaging (MRI). The NMR/MRI-derived bound water concentration is positively correlated with both the strength and toughness of hydrated bone and may become a useful clinical marker of fracture risk.

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Acknowledgements and Funding

Our work investigating the role of water in bone is made possible by funding from The National Institute of Arthritis and Musculoskeletal and Skin Diseases and The National Institute of Biomedical Imaging and Bioengineering of the National Institutes of Health (NIH) under award nos. AR063157 and EB014308, respectively. Additional support is provided by a Biomedical Laboratory Research and Development grant 1I01BX001018 from the VA Office of Research and Development. We thank the Musculoskeletal Tissue Foundation (Edison, NJ) and the Vanderbilt Donor Program (Nashville, TN) for providing cadaveric bone. We thank Mary Kate Manhard for providing the images of bound water and pore water from the tibia of a subject.

Conflict of interest

Dr. Nyman and Dr. Does have a patent entitled "System and Method for Determining Mechanical Properties of Bone Structures". This patent involves measurements of bound and pore water. Dr. Granke’s salary is supported by AR063157, but otherwise has no conflicts related to the present research.

Human and Animal Rights and Informed Consent

The imaging of subjects followed a protocol approved by the Institutional Review Board at Vanderbilt University. The use of animals followed a protocol approved by the Institutional Animal Care and Use Committee at Vanderbilt University.

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Authors and Affiliations

  1. Department of Orthopaedic Surgery & Rehabilitation, Vanderbilt University Medical Center, Nashville, TN, 37232, USA

    Mathilde Granke & Jeffry S. Nyman

  2. Center for Bone Biology, Vanderbilt University Medical Center, Nashville, TN, 37232, USA

    Mathilde Granke & Jeffry S. Nyman

  3. Department of Biomedical Engineering, Vanderbilt University, Nashville, TN, 37232, USA

    Mark D. Does & Jeffry S. Nyman

  4. Institute of Imaging Science, Vanderbilt University, Nashville, TN, 37232, USA

    Mark D. Does

  5. Department of Radiology and Radiological Sciences, Vanderbilt University, Nashville, TN, 37232, USA

    Mark D. Does

  6. Department of Electrical Engineering, Vanderbilt University, Nashville, TN, 37232, USA

    Mark D. Does

  7. Department of Veterans Affairs, Tennessee Valley Healthcare System, Nashville, TN, 37212, USA

    Jeffry S. Nyman

  8. Vanderbilt Orthopaedic Institute, Medical Center East, South Tower, Suite 4200, Nashville, TN, 37232, USA

    Jeffry S. Nyman

Authors
  1. Mathilde Granke
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  2. Mark D. Does
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  3. Jeffry S. Nyman
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Corresponding author

Correspondence to Jeffry S. Nyman.

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Granke, M., Does, M.D. & Nyman, J.S. The Role of Water Compartments in the Material Properties of Cortical Bone. Calcif Tissue Int 97, 292–307 (2015). https://doi.org/10.1007/s00223-015-9977-5

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  • DOI: https://doi.org/10.1007/s00223-015-9977-5

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