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Tomography-Based Quantification of Regional Differences in Cortical Bone Surface Remodeling and Mechano-Response

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Abstract

Bone has an adaptive capacity to maintain structural integrity. However, there seems to be a heterogeneous cortical (re)modeling response to loading at different regions within the same bone, which may lead to inconsistent findings since most studies analyze only one region. It remains unclear if the local mechanical environment is responsible for this heterogeneous response and whether both formation and resorption are affected. Thus, we compared the formation and resorptive response to in vivo loading and the strain environment at two commonly analyzed regions in the mouse tibia, the mid-diaphysis and proximal metaphysis. We quantified cortical surface (re)modeling by tracking changes between geometrically aligned consecutive in vivo micro-tomography images (time lapse 15 days). We investigated the local mechanical strain environment using finite element analyses. The relationship between mechanical stimuli and surface (re)modeling was examined by sub-dividing the mid-diaphysis and proximal metaphysis into 32 sub-regions. In response to loading, metaphyseal cortical bone (re)modeled predominantly at the periosteal surface, whereas diaphyseal (re)modeling was more pronounced at the endocortical surface. Furthermore, different set points and slopes of the relationship between engendered strains and remodeling response were found for the endosteal and periosteal surfaces at the metaphyseal and diaphyseal regions. Resorption was correlated with strain at the endocortical, but not the periosteal surfaces, whereas, formation correlated with strain at all surfaces, except at the metaphyseal periosteal surface. Therefore, besides mechanical stimuli, other non-mechanical factors are likely driving regional differences in adaptation. Studies investigating adaptation to loading or other treatments should consider region-specific (re)modeling differences.

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Acknowledgements

The authors would like to thank Marta Aido and Tobias Thiele for helping with the animal experiments and Mario Thiele for assistance with the µCT imaging. We thank Steffen Prohaska and Hans-Christian Hege from Zuse Institute for use of ZibAMIRA software. This study was partially supported by the German Research Foundation (Deutsche Forschungsgemeinschaft; WI 3761/4-1, CH1123/4-1, DU 298/21-1), the German Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung: TP5/DIMEOs), the Shriners Hospitals for Children, and the Réseau de recherche en santé buccodentaire et osseuse recruitment aid program.

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Authors and Affiliations

  1. Julius Wolff Institute, Charité - Universitätsmedizin Berlin, Berlin, Germany

    Annette I. Birkhold, Hajar Razi, Georg N. Duda, Sara Checa & Bettina M. Willie

  2. Continuum Biomechanics and Mechanobiology Research Group, Institute of Applied Mechanics, University of Stuttgart, Stuttgart, Germany

    Annette I. Birkhold

  3. Max Planck Institute of Colloids and Interfaces, Potsdam, Germany

    Hajar Razi

  4. Department of Pediatric Surgery, McGill University, Research Centre, Shriners Hospital for Children-Canada, 1003 Decarie Blvd, Montreal, H4A 0A9, Canada

    Bettina M. Willie

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  1. Annette I. Birkhold
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  5. Bettina M. Willie
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Correspondence to Bettina M. Willie.

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Annette I. Birkhold, Hajar Razi, Georg N. Duda, Sara Checa, and Bettina M. Willie have no conflicts of interest.

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Animal studies were performed in accordance with an ethical animal use protocol approved by the local legal representative (LAGeSo Berlin, G0333/09).

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Birkhold, A.I., Razi, H., Duda, G.N. et al. Tomography-Based Quantification of Regional Differences in Cortical Bone Surface Remodeling and Mechano-Response. Calcif Tissue Int 100, 255–270 (2017). https://doi.org/10.1007/s00223-016-0217-4

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