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Quantifying intracortical bone microstructure: a critical appraisal of 2D and 3D approaches for assessing vascular canals and osteocyte lacunae

Quantifying intracortical bone microstructure: a critical appraisal of 2D and 3D approaches for assessing vascular canals and osteocyte lacunae
Quantifying intracortical bone microstructure: a critical appraisal of 2D and 3D approaches for assessing vascular canals and osteocyte lacunae
Describing and quantifying vascular canal orientation and volume of osteocyte lacunae in bone is important in studies of bone growth, mechanics, health and disease. It is also an important element in analysing fossil bone in palaeohistology, key to understanding the growth, life, and death of extinct animals. Often, bone microstructure is studied using two-dimensional (2D) sections, and three-dimensional (3D) shape and orientation of structures are estimated by modelling the structures using idealised geometries based on information from their cross sections. However, these methods rely on structures meeting strict geometric assumptions. Recently, 3D methods have been proposed which could provide a more accurate and robust approach to bone histology, but these have not been tested in direct comparison with their 2D counterparts in terms of accuracy and sensitivity to deviations from model assumptions. We compared 2D and 3D methodologies for estimating key microstructural traits using a combination of experimental and idealised test datasets. We generated populations of cylinders (canals) and ellipsoids (osteocyte lacunae), varying the cross-sectional aspect ratios of cylinders and orientation of ellipsoids to test sensitivity to deviations from cylindricality and longitudinal orientation, respectively. Using published methods, based on 2D sections and 3D datasets, we estimated cylinder orientation and ellipsoid volume. We applied the same methods to six CT datasets of duck cortical bone, using the full volumes for 3D measurements and single CT slices to represent 2D sections. Using in silico test datasets that did deviate from ideal cylinders and ellipsoids resulted in inaccurate estimates of cylinder or canal orientation, and reduced accuracy in estimates of ellipsoid and lacunar volume. These results highlight the importance of using appropriate 3D imaging and quantitative methods for quantifying volume and orientation of 3D structures and offer approaches to significantly enhance our understanding of bone physiology based on accurate measures for bone microstructures.
X-ray CT, bone, fossil, histology, image analysis, osteocyte, vascular canal
0021-8782
653-668
Williams, Katherine Anne
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Gostling, Neil J.
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Steer, Joshua
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Oreffo, Richard
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Schneider, Philipp
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Williams, Katherine Anne
bf87a040-9a95-4c4e-a078-d289404b7523
Gostling, Neil J.
4840aa40-cb6c-4112-a0b9-694a869523fc
Steer, Joshua
19fab79c-1991-4762-85da-abda7ce82ab1
Oreffo, Richard
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Schneider, Philipp
a810f925-4808-44e4-8a4a-a51586f9d7ad

Williams, Katherine Anne, Gostling, Neil J., Steer, Joshua, Oreffo, Richard and Schneider, Philipp (2021) Quantifying intracortical bone microstructure: a critical appraisal of 2D and 3D approaches for assessing vascular canals and osteocyte lacunae. Journal of Anatomy, 238 (3), 653-668. (doi:10.1111/joa.13325).

Record type: Article

Abstract

Describing and quantifying vascular canal orientation and volume of osteocyte lacunae in bone is important in studies of bone growth, mechanics, health and disease. It is also an important element in analysing fossil bone in palaeohistology, key to understanding the growth, life, and death of extinct animals. Often, bone microstructure is studied using two-dimensional (2D) sections, and three-dimensional (3D) shape and orientation of structures are estimated by modelling the structures using idealised geometries based on information from their cross sections. However, these methods rely on structures meeting strict geometric assumptions. Recently, 3D methods have been proposed which could provide a more accurate and robust approach to bone histology, but these have not been tested in direct comparison with their 2D counterparts in terms of accuracy and sensitivity to deviations from model assumptions. We compared 2D and 3D methodologies for estimating key microstructural traits using a combination of experimental and idealised test datasets. We generated populations of cylinders (canals) and ellipsoids (osteocyte lacunae), varying the cross-sectional aspect ratios of cylinders and orientation of ellipsoids to test sensitivity to deviations from cylindricality and longitudinal orientation, respectively. Using published methods, based on 2D sections and 3D datasets, we estimated cylinder orientation and ellipsoid volume. We applied the same methods to six CT datasets of duck cortical bone, using the full volumes for 3D measurements and single CT slices to represent 2D sections. Using in silico test datasets that did deviate from ideal cylinders and ellipsoids resulted in inaccurate estimates of cylinder or canal orientation, and reduced accuracy in estimates of ellipsoid and lacunar volume. These results highlight the importance of using appropriate 3D imaging and quantitative methods for quantifying volume and orientation of 3D structures and offer approaches to significantly enhance our understanding of bone physiology based on accurate measures for bone microstructures.

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JANAT-2020-0037_accepted_version_combined - Accepted Manuscript
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Accepted/In Press date: 10 September 2020
e-pub ahead of print date: 8 October 2020
Published date: March 2021
Additional Information: Funding Information: This work is funded by the Institute for Life Sciences at the University of Southampton and the Faculty of Engineering and Physical Sciences at the University of Southampton through its Engineering and Physical Sciences Research Council (EPSRC) Doctoral Training Partnership support. Additional support by the UK Regenerative Medicine Platform Acellular / Smart Materials ? 3D Architecture (MR/R015651/1) to RO is acknowledged. Technical support at beamline I13-2 of Diamond Light Source was provided by Andrew Bodey and Shashidhara Marathe, and additional assistance during experiments at beamline I13-2 was provided by Harry Rossides, Roxanna Ramnarine Sanchez, Alisha Sharma, Erik Meilak and Christian Laurent. The authors would also like to thank the two anonymous reviewers of this paper for their kind words and very constructive comments, which have helped us to improve this publication significantly. All data supporting this study are openly available from the University of Southampton repository at https://doi.org/10.5258/SOTON/D1198. Funding Information: This work is funded by the Institute for Life Sciences at the University of Southampton and the Faculty of Engineering and Physical Sciences at the University of Southampton through its Engineering and Physical Sciences Research Council (EPSRC) Doctoral Training Partnership support. Additional support by the UK Regenerative Medicine Platform Acellular / Smart Materials – 3D Architecture (MR/R015651/1) to RO is acknowledged. Technical support at beamline I13‐2 of Diamond Light Source was provided by Andrew Bodey and Shashidhara Marathe, and additional assistance during experiments at beamline I13‐2 was provided by Harry Rossides, Roxanna Ramnarine Sanchez, Alisha Sharma, Erik Meilak and Christian Laurent. The authors would also like to thank the two anonymous reviewers of this paper for their kind words and very constructive comments, which have helped us to improve this publication significantly. All data supporting this study are openly available from the University of Southampton repository at https://doi.org/10.5258/SOTON/D1198 . Publisher Copyright: © 2020 The Authors. Journal of Anatomy published by John Wiley & Sons Ltd on behalf of Anatomical Society
Keywords: X-ray CT, bone, fossil, histology, image analysis, osteocyte, vascular canal

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Local EPrints ID: 444070
URI: http://eprints.soton.ac.uk/id/eprint/444070
ISSN: 0021-8782
PURE UUID: 9ae7d11d-d09d-4745-8795-c57a5def22f5
ORCID for Katherine Anne Williams: ORCID iD orcid.org/0000-0001-6827-9261
ORCID for Neil J. Gostling: ORCID iD orcid.org/0000-0002-5960-7769
ORCID for Joshua Steer: ORCID iD orcid.org/0000-0002-6288-1347
ORCID for Richard Oreffo: ORCID iD orcid.org/0000-0001-5995-6726
ORCID for Philipp Schneider: ORCID iD orcid.org/0000-0001-7499-3576

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Date deposited: 24 Sep 2020 16:31
Last modified: 22 Oct 2022 04:01

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Author: Katherine Anne Williams ORCID iD
Author: Joshua Steer ORCID iD
Author: Richard Oreffo ORCID iD

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