In vivo bone strain and finite element modeling of a rhesus macaque mandible during mastication

doi:10.1016/J.ZOOL.2017.08.010

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In vivo bone strain and finite element modeling of a rhesus macaque mandible during mastication

Journal Article•DOI•

In vivo bone strain and finite element modeling of a rhesus macaque mandible during mastication

Olga Panagiotopoulou¹, Olga Panagiotopoulou², Jose Iriarte-Diaz³, Simon Wilshin⁴, Paul C. Dechow⁵, Andrea B. Taylor⁶, Hyab Mehari Abraha², Sharifah F. Aljunid, Callum F. Ross⁷ - Show less +5 more•Institutions (7)

Monash University, Clayton campus¹, University of Queensland², University of Illinois at Urbana–Champaign³, Royal Veterinary College⁴, Texas A&M University⁵, Touro University California⁶, University of Chicago⁷

01 Sep 2017-Zoology (Elsevier)-Vol. 124, pp 13-29

TL;DR: A subject-specific FEM of a rhesus macaque mandible was constructed, loaded and validated using in vivo data from the same animal, and the relative strain magnitudes were similar to those recorded in vivo for all strain locations.

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About: This article is published in Zoology.The article was published on 2017-09-01 and is currently open access. It has received 26 citations till now.

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Journal Article•DOI•

Finite element analysis of individual taenioglossan radular teeth (Mollusca).

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Wencke Krings¹, Jordi Marcé-Nogué², Jordi Marcé-Nogué³, Jordi Marcé-Nogué⁴, Hasan Karabacak¹, Matthias Glaubrecht¹, Stanislav N. Gorb⁵ - Show less +3 more•Institutions (5)

University of Hamburg¹, State University of New York System², Autonomous University of Barcelona³, Rovira i Virgili University⁴, University of Kiel⁵

25 Aug 2020-Acta Biomaterialia

TL;DR: For the first time, a quantitative approach is used, Finite-Element-Analysis (FEA), to test hypotheses regarding the function of particular taenioglossan tooth types, and it is posited that the central and lateral teeth are best suitable for scratching substrate loosening ingesta, whereas the marginals are best suited for gathering food particles.

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26 citations

Journal Article•DOI•

The use of extruded finite-element models as a novel alternative to tomography-based models: a case study using early mammal jaws.

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Nuria Melisa Morales-García¹, Thomas D. Burgess¹, Jennifer J. Hill², Pamela G. Gill³, Emily J. Rayfield¹ - Show less +1 more•Institutions (3)

University of Bristol¹, Smithsonian Institution², American Museum of Natural History³

24 Dec 2019-Journal of the Royal Society Interface

TL;DR: Extruded FE models constitute a viable alternative to the use of tomography-based 3D models, particularly in relatively flat bones, in Morganucodon and Kuehneotherium.

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Abstract: Finite-element (FE) analysis has been used in palaeobiology to assess the mechanical performance of the jaw. It uses two types of models: tomography-based three-dimensional (3D) models (very accura...

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24 citations

Cites methods from "In vivo bone strain and finite elem..."

...Interface 16:(2)0190674 2 mandible of an ostrich [8], and in macaque mandibles using in vitro data [29], as well as combined in vivo and ex vivo data [30]....
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Journal Article•DOI•

The Mechanical Effect of the Periodontal Ligament on Bone Strain Regimes in a Validated Finite Element Model of a Macaque Mandible.

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Hyab Mehari Abraha¹, Jose Iriarte-Diaz², Callum F. Ross³, Andrea B. Taylor⁴, Olga Panagiotopoulou¹ - Show less +1 more•Institutions (4)

Monash University, Clayton campus¹, Sewanee: The University of the South², University of Chicago³, Touro University California⁴

30 Oct 2019-Frontiers in Bioengineering and Biotechnology

TL;DR: The findings suggest that the mechanical importance of the PDL in FEMs of the mandible during chewing is dependent on the scope of the hypotheses being tested, and whether researchers are comparing strain gradients across species/taxa or if researchers are concerned with absolute strain values, sensitivity analysis is required.

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Abstract: The primary anatomical function of the periodontal ligament (PDL) is to attach teeth to their sockets. However, theoretical and constitutive mechanical models have proposed that during mastication the PDL redistributes local occlusal loads and reduces the jaw’s resistance to torsional deformations. These hypotheses imply that accurately modelling the PDL’s material properties and geometry in finite element analysis (FEA) is a prerequisite to obtaining precise strain and deformation data. Yet, many finite element studies of the human and non-human primate masticatory apparatus exclude the PDL or model it with simplicity, in part due to limitations in µCT/CT scan resolution and material property assignment. Previous studies testing the sensitivity of finite element models (FEMs) to the PDL have yielded contradictory results, however a major limitation of these studies is that FEMs were not validated against in vivo bone strain data. Hence, this study uses a validated and subject specific FEM to assess the effect of the PDL on strain and deformation regimes in the lower jaw of a rhesus macaque (Macaca mulatta) during simulated unilateral post-canine chewing. Our findings demonstrate that the presence of the PDL does influence local and global surface strain magnitudes (principal and shear) in the jaw. However, the PDL’s effect is limited (diff. ~200-300µe) in areas away from the alveoli. Our results also show that varying the PDL’s Young’s Modulus within the range of published values (0.07-1750 MPa) has very little effect on global surface strains. These findings suggest that the mechanical importance of the PDL in FE models of the mandible during chewing is dependent on the scope of the hypotheses being tested. If researchers are comparing strain gradients across species/taxa, the PDL may be excluded with minimal effect on results, but, if researchers are concerned with absolute strain values, sensitivity analysis is required.

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22 citations

Cites background or methods from "In vivo bone strain and finite elem..."

...As the PDL itself cannot be visualized in CT, its geometry was demarcated as a continuous, non-uniform space between the tooth root and alveolar bone (spanning 3–6 voxels), and was segmented using a combination of manual and automatic methods (Panagiotopoulou et al., 2017)....
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...The details of capturing model geometry, segmentation, and material property assignment for the cortical bone, trabecular tissue, teeth and PDL are described in full elsewhere (Panagiotopoulou et al., 2017)....
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...To test our hypotheses we used a previously published FEM of a rhesus macaque mandible (Panagiotopoulou et al., 2017) and validated our FEMs against in vivo bone strain data....
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...Briefly, all muscle-force vectors were derived from a combination of in vivo raw EMG signals collected when the animal was chewing on nuts and ex vivo muscle physiological crosssectional area (PCSA) analysis to estimate the maximum force potential of each muscle (Panagiotopoulou et al., 2017)....
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...Bone screws were implanted in the mandible to measure three dimensional (3D) rigid body kinematics of the mandible during the post-canine unilateral chewing modeled in this study (Iriarte-Diaz et al., 2011; Ross et al., 2012; Panagiotopoulou et al., 2017)....
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Journal Article•DOI•

Glucocorticoids cause mandibular bone fragility and suppress osteocyte perilacunar-canalicular remodeling.

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A. Sean Alemi¹, Courtney M. Mazur¹, Courtney M. Mazur², Tristan W. Fowler¹, Jonathon J. Woo¹, P. Daniel Knott¹, Tamara Alliston¹, Tamara Alliston² - Show less +4 more•Institutions (2)

University of California, San Francisco¹, University of California, Berkeley²

03 Oct 2018-Bone reports

TL;DR: Osteocyte PLR in the neural crest-derived mandible is susceptible to glucocorticoids, just as it is in the mesodermally-derived femur, highlighting the need to further study PLR as a target of drugs, and radiation in mandibular osteonecrosis.

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Abstract: Osteocytes support dynamic, cell-intrinsic resorption and deposition of bone matrix through a process called perilacunar/canalicular remodeling (PLR). In long bones, PLR depends on MMP13 and is tightly regulated by PTH, sclerostin, TGFβ, and glucocorticoids. However, PLR is regulated differently in the cochlea, suggesting a mechanism that is anatomically distinct. Unlike long bones, the mandible derives from neural crest and exhibits unique susceptibility to medication and radiation induced osteonecrosis. Therefore, we sought to determine if PLR in the mandible is suppressed by glucocorticoids, as it is in long bone. Hemimandibles were collected from mice subcutaneously implanted with prednisolone or vehicle containing pellets for 7, 21, or 55 days (n = 8/group) for radiographic and histological analyses. Within 21 days, micro-computed tomography revealed a glucocorticoid-dependent reduction in bone volume/total volume and trabecular thickness and a significant decrease in bone mineral density after 55 days. Within 7 days, glucocorticoids strongly and persistently repressed osteocytic expression of the key PLR enzyme MMP13 in both trabecular and cortical bone of the mandible. Cathepsin K expression was significantly reduced only after 55 days of glucocorticoid treatment, at which point histological analysis revealed a glucocorticoid-dependent reduction in the lacunocanalicular surface area. In addition to reducing bone mass and suppressing PLR, glucocorticoids also reduced the stiffness of mandibular bone in flexural tests. Thus, osteocyte PLR in the neural crest-derived mandible is susceptible to glucocorticoids, just as it is in the mesodermally-derived femur, highlighting the need to further study PLR as a target of drugs, and radiation in mandibular osteonecrosis.

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20 citations

Cites background from "In vivo bone strain and finite elem..."

...This heterogeneity may help mandibular bone accommodate the diverse forces encountered during mastication (Panagiotopoulou et al., 2017)....
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Journal Article•DOI•

Why ruminating ungulates chew sloppily: Biomechanics discern a phylogenetic pattern

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Zupeng Zhou¹, Daniela E. Winkler², Josep Fortuny³, Thomas M. Kaiser⁴, Jordi Marcé-Nogué⁴, Jordi Marcé-Nogué³ - Show less +2 more•Institutions (4)

Guilin University of Electronic Technology¹, University of Mainz², Autonomous University of Barcelona³, University of Hamburg⁴

17 Apr 2019-PLOS ONE

TL;DR: Three-dimensional finite element analysis is used to assess the biomechanical performance of mandibles in eleven ungulate taxa with well-established but distinct dietary preferences and finds that mandibular morphologies reflect the masticatory demands of specific ingesta within the orders Artiodactyla and PerissodactylA.

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Abstract: There is considerable debate regarding whether mandibular morphology in ungulates primarily reflects phylogenetic affinities or adaptation to specific diet. In an effort to help resolve this debate, we use three-dimensional finite element analysis (FEA) to assess the biomechanical performance of mandibles in eleven ungulate taxa with well-established but distinct dietary preferences. We found notable differences in the magnitude and the distribution of von Mises stress between Artiodactyla and Perissodactyla, with the latter displaying lower overall stress values. Additionally, within the order Artiodactyla the suborders Ruminantia and Tylopoda showed further distinctive stress patterns. Our data suggest that a strong phylogenetic signal can be detected in biomechanical performance of the ungulate mandible. In general, Perissodactyla have stiffer mandibles than Artiodactyla. This difference is more evident between Perissodactyla and ruminant species. Perissodactyla likely rely more heavily on thoroughly chewing their food upon initial ingestion, which demands higher bite forces and greater stress resistance, while ruminants shift comminution to a later state (rumination) where less mechanical effort is required by the jaw to obtain sufficient disintegration. We therefore suggest that ruminants can afford to chew sloppily regardless of ingesta, while hindgut fermenters cannot. Additionally, our data support a secondary degree of adaptation towards specific diet. We find that mandibular morphologies reflect the masticatory demands of specific ingesta within the orders Artiodactyla and Perissodactyla. Of particular note, stress patterns in the white rhinoceros (C. simum) look more like those of a general grazer than like other rhinoceros' taxa. Similarly, the camelids (Tylopoda) appear to occupy an intermediate position in the stress patterns, which reflects the more ancestral ruminating system of the Tylopoda.

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20 citations

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Journal Article•DOI•

CircStat: A Matlab Toolbox for Circular Statistics

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Philipp Berens¹•Institutions (1)

Max Planck Society¹

23 Sep 2009-Journal of Statistical Software

TL;DR: The CircStat toolbox for MATLAB is implemented which provides methods for the descriptive and inferential statistical analysis of directional data and analyzes a dataset from neurophysiology to demonstrate the capabilities of the Circstat toolbox.

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Abstract: Directional data is ubiquitious in science. Due to its circular nature such data cannot be analyzed with commonly used statistical techniques. Despite the rapid development of specialized methods for directional statistics over the last fifty years, there is only little software available that makes such methods easy to use for practioners. Most importantly, one of the most commonly used programming languages in biosciences, MATLAB, is currently not supporting directional statistics. To remedy this situation, we have implemented the CircStat toolbox for MATLAB which provides methods for the descriptive and inferential statistical analysis of directional data. We cover the statistical background of the available methods and describe how to apply them to data. Finally, we analyze a dataset from neurophysiology to demonstrate the capabilities of the CircStat toolbox.

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2,557 citations

"In vivo bone strain and finite elem..." refers methods in this paper

...All EMG and strain data were exported from Vicon as C3D files, imported into MatLab (Mathworks, Natick, MA, USA) using the Biomechanical ToolKit (BTK) (Barre and Armand, 2014) and analyzed by J.I.-D. using custom scripts in Matlab....
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...Maximum gape events were automatically identified using a custom Matlab script, but we manually selected only those events that represented rhythmic chewing....
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...Kinematic data were processed in Matlab using customized scripts based on the KineMat toolbox kit (http://isbweb.org/software/ movanal/kinemat/) and the BTK toolbox....
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...To compare FEM data to the strain gauge data, all the out-of-plane components of the strain tensor (i.e., εzz, εxz, εyz) were set to zero and principal strains—the eigenvalues and eigenvectors of the rotated strain tensors—at the gauge sites were calculated using a custom-written Matlab script (see Ross et al., 2011 for details)....
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...The orientation of the principal strains was analyzed using the circular statistics toolbox, CirscStat for Matlab (Berens, 2009)....
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Journal Article•DOI•

The elastic and ultimate properties of compact bone tissue

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Donald T. Reilly¹, Albert H. Burstein¹•Institutions (1)

Case Western Reserve University¹

01 Jan 1975-Journal of Biomechanics

TL;DR: The use of a tranversely isotropic model is tested for the elastic behavior of bovine and human bone and the five independent constants of this model are determined.

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1,448 citations

"In vivo bone strain and finite elem..." refers background in this paper

...because strain magnitudes are related to fracture probability (Burstein et al., 1972; Reilly and Burstein, 1975) and because strains activate adaptive bone remodeling, repair and modeling in response to load (Frost, 1987; Forwood and Turner, 1995; Turner, 1998)....
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...…to be an important design criterion for biological structures because strain magnitudes are related to fracture probability (Burstein et al., 1972; Reilly and Burstein, 1975) and because strains activate adaptive bone remodeling, repair and modeling in response to load (Frost, 1987; Forwood and…...
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Book•

Bones: Structure and Mechanics

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John D. Currey

30 Jun 2002

TL;DR: Copiously illustrated, engagingly written, and assuming little in the way of prior knowledge or mathematical background, Bones is both an ideal introduction to the field and also a reference sure to be frequently consulted by practicing researchers.

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Abstract: This is a comprehensive and accessible overview of what is known about the structure and mechanics of bone, bones, and teeth. In it, John Currey incorporates critical new concepts and findings from the two decades of research since the publication of his highly regarded The Mechanical Adaptations of Bones. Crucially, Currey shows how bone structure and bone's mechanical properties are intimately bound up with each other and how the mechanical properties of the material interact with the structure of whole bones to produce an adapted structure. For bone tissue, the book discusses stiffness, strength, viscoelasticity, fatigue, and fracture mechanics properties. For whole bones, subjects dealt with include buckling, the optimum hollowness of long bones, impact fracture, and properties of cancellous bone. The effects of mineralization on stiffness and toughness and the role of microcracking in the fracture process receive particular attention. As a zoologist, Currey views bone and bones as solutions to the design problems that vertebrates have faced during their evolution and throughout the book considers what bones have been adapted to do. He covers the full range of bones and bony tissues, as well as dentin and enamel, and uses both human and non-human examples. Copiously illustrated, engagingly written, and assuming little in the way of prior knowledge or mathematical background, Bones is both an ideal introduction to the field and also a reference sure to be frequently consulted by practicing researchers.

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1,298 citations

"In vivo bone strain and finite elem..." refers background in this paper

...An alternative approach, and the one adopted here, models subcortical bone as a single solid (called ‘trabecular tissue’) and assigns it an E-value lower than that of cortical bone in accordance with the principle that, due to its increased porosity, subcortical tissue has an E-value 20–30% lower than that of cortical bone (Cowin, 2001; Currey, 2002)....
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...…subcortical bone as a single solid (called ‘trabecular tissue’) and assigns it an E-value lower than that of cortical bone in accordance with the principle that, due to its increased porosity, subcortical tissue has an E-value 20–30% lower than that of cortical bone (Cowin, 2001; Currey, 2002)....
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Book•DOI•

Bone mechanics handbook

[...]

Stephen C. Cowin

15 Mar 2001

TL;DR: Basic Biology Integrated Bone Tissue Physiology: Anatomy and Physiology (Jee) Cell Biology of Bone (Majeska) Molecular Biology Techniques to Measure Skeletal Gene Expression (Young and Dieudonne) and Creating Transgenic Mice to Study Skeletal Function ( young and Xu).

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Abstract: Basic Biology Integrated Bone Tissue Physiology: Anatomy and Physiology (Jee) Cell Biology of Bone (Majeska) Molecular Biology Techniques to Measure Skeletal Gene Expression (Young and Dieudonne) Creating Transgenic Mice to Study Skeletal Function (Young and Xu) Bone Mineralization (Boskey) Techniques from Mechanics and Imaging Mechanics of Materials (Cowin) Experimental Techniques for Bone Mechanics (Turner and Burr) In Vivo Measurement of Bone Deformations Using Strain Gages (Fritton and Rubin) Imaging of Bone Structure (Ruegsegger) Mechanical and Architectural Properties of Bone Mechanical Properties of Cortical Bone and Cancellous Bone Tissue (Guo) Viscoelastic Properties of Cortical Bone (Lakes) Composite Models of Bone Properties (Lucchinetti) Dense Bone Tissue as a Molecular Composite (Lucchinetti) Quantification of Cancellous Bone Architecture (Odgaard) Elastic Constants of Cancellous Bone (von Rietbergen and Huiskes) Strength of Trabecular Bone (Keaveny) Observations of Damage in Bone (Jepsen, Davy, and Akkus) Bone Damage Mechanics (Davy and Jepsen) Ontogenic Changes in Compact Bone Material Properties (Currey) Mechanical Effects of Postmortem Changes, Preservation, and Allograft Bone Treatments (Martin and Sharkey) Flow of Fluids in Bone Blood Flow in Bone (Winet) Interstitial Fluid Flow (Knothe-Tate) Bone Poroelasticity (Cowin) Streaming Potentials in Bone (Pollack) The Intrinsic Permeability of Cancellous Bone (Arramon and Nauman) Bone Adaptation Pathophysiology of Functional Adaptation of Bone in Remodeling and Repair In Vivo (Goodship and Cunningham) Devices and Techniques for in Vitro Mechanical Stimulation of Bone Cells (Brown) Experiments on Cell Mechanosensitivity (Burger) Mechanosensory Mechanisms in Bone (Cowin and Moss) The False Premise of Wolff's Law (Cowin) Bone Modeling and Remodeling: Theories and Computation (Hart) Mechanics of Bone Regeneration (Prendergast and van der Meulen) Clinically Related Issues Applications of Bone Mechanics (Villarraga and Ford) Noninvasive Measurement of Bone Integrity (Kaufman and Siffert) Bone Prostheses and Implants (Prendergast) Design and Manufacture of Bone Replacement Scaffolds (Hollister, Chu, Halloran, and Feinberg)

...read moreread less

1,120 citations

"In vivo bone strain and finite elem..." refers background in this paper

...An alternative approach, and the one adopted here, models subcortical bone as a single solid (called ‘trabecular tissue’) and assigns it an E-value lower than that of cortical bone in accordance with the principle that, due to its increased porosity, subcortical tissue has an E-value 20–30% lower than that of cortical bone (Cowin, 2001; Currey, 2002)....
[...]
...…subcortical bone as a single solid (called ‘trabecular tissue’) and assigns it an E-value lower than that of cortical bone in accordance with the principle that, due to its increased porosity, subcortical tissue has an E-value 20–30% lower than that of cortical bone (Cowin, 2001; Currey, 2002)....
[...]

Journal Article•DOI•

Young's modulus of trabecular and cortical bone material: ultrasonic and microtensile measurements.

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Jae Young Rho¹, Richard B. Ashman, Charles H. Turner²•Institutions (2)

State University of New York System¹, Indiana University – Purdue University Indianapolis²

01 Feb 1993-Journal of Biomechanics

TL;DR: The results suggest that when considered mechanically, cortical and trabecular bone are not the same material.

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1,109 citations

"In vivo bone strain and finite elem..." refers background in this paper

...However, constraints on image resolution mean that defining the geometry of the individual trabeculae in the subcortex can be problematic, as CT/μCT cannot accurately capture the fine details of the trabeculae within the subcortex (Rho et al., 1993; Dechow and Hylander, 2000; Rapoff et al., 2008)....
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