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Fluid flow in the osteocyte mechanical environment: a fluid–structure interaction approach

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Abstract

Osteocytes are believed to be the primary sensor of mechanical stimuli in bone, which orchestrate osteoblasts and osteoclasts to adapt bone structure and composition to meet physiological loading demands. Experimental studies to quantify the mechanical environment surrounding bone cells are challenging, and as such, computational and theoretical approaches have modelled either the solid or fluid environment of osteocytes to predict how these cells are stimulated in vivo. Osteocytes are an elastic cellular structure that deforms in response to the external fluid flow imposed by mechanical loading. This represents a most challenging multi-physics problem in which fluid and solid domains interact, and as such, no previous study has accounted for this complex behaviour. The objective of this study is to employ fluid–structure interaction (FSI) modelling to investigate the complex mechanical environment of osteocytes in vivo. Fluorescent staining of osteocytes was performed in order to visualise their native environment and develop geometrically accurate models of the osteocyte in vivo. By simulating loading levels representative of vigorous physiological activity (\(3,000\,\upmu \upvarepsilon \) compression and 300 Pa pressure gradient), we predict average interstitial fluid velocities \((\sim 60.5\,\upmu \text{ m/s })\) and average maximum shear stresses \((\sim 11\, \text{ Pa })\) surrounding osteocytes in vivo. Interestingly, these values occur in the canaliculi around the osteocyte cell processes and are within the range of stimuli known to stimulate osteogenic responses by osteoblastic cells in vitro. Significantly our results suggest that the greatest mechanical stimulation of the osteocyte occurs in the cell processes, which, cell culture studies have indicated, is the most mechanosensitive area of the cell. These are the first computational FSI models to simulate the complex multi-physics mechanical environment of osteocyte in vivo and provide a deeper understanding of bone mechanobiology.

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Acknowledgments

The authors would like to acknowledge funding from the Irish Research Council for Science, Engineering and Technology (IRCSET), under the EMBARK program (S. W. V.), the European Research Council (ERC) under grant number 258992 (BONEMECHBIO) and the Irish Centre for High-End Computing (ICHEC).

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  1. Biomechanics Research Centre (BMEC), Mechanical and Biomedical Engineering, College of Engineering and Informatics, National University of Ireland, Galway, Ireland

    Stefaan W. Verbruggen, Ted J. Vaughan & Laoise M. McNamara

  2. Department of Mechanical and Biomedical Engineering, National University of Ireland, Galway, Ireland

    Laoise M. McNamara

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  1. Stefaan W. Verbruggen
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  3. Laoise M. McNamara
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Correspondence to Laoise M. McNamara.

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Verbruggen, S.W., Vaughan, T.J. & McNamara, L.M. Fluid flow in the osteocyte mechanical environment: a fluid–structure interaction approach. Biomech Model Mechanobiol 13, 85–97 (2014). https://doi.org/10.1007/s10237-013-0487-y

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