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Microstructural heterogeneity of the collagenous network in the loaded and unloaded periodontal ligament and its biomechanical implications

Zhong, Jingxiao ; Pierantoni, Maria LU orcid ; Weinkamer, Richard ; Brumfeld, Vlad ; Zheng, Keke ; Chen, Junning ; Swain, Michael V. ; Weiner, Steve and Li, Qing (2021) In Journal of Structural Biology 213(3).
Abstract

The periodontal ligament (PDL) is a highly heterogeneous fibrous connective tissue and plays a critical role in distributing occlusal forces and regulating tissue remodeling. Its mechanical properties are largely determined by the extracellular matrix, comprising a collagenous fiber network interacting with the capillary system as well as interstitial fluid containing proteoglycans. While the phase-contrast micro-CT technique has portrayed the 3D microscopic heterogeneity of PDL, the topological parameters of its network, which is crucial to understanding the multiscale constitutive behavior of this tissue, has not been characterized quantitatively. This study aimed to provide new understanding of such microscopic heterogeneity of the... (More)

The periodontal ligament (PDL) is a highly heterogeneous fibrous connective tissue and plays a critical role in distributing occlusal forces and regulating tissue remodeling. Its mechanical properties are largely determined by the extracellular matrix, comprising a collagenous fiber network interacting with the capillary system as well as interstitial fluid containing proteoglycans. While the phase-contrast micro-CT technique has portrayed the 3D microscopic heterogeneity of PDL, the topological parameters of its network, which is crucial to understanding the multiscale constitutive behavior of this tissue, has not been characterized quantitatively. This study aimed to provide new understanding of such microscopic heterogeneity of the PDL with quantifications at both tissue and collagen network levels in a spatial manner, by combining phase-contrast micro-CT imaging and a purpose-built image processing algorithm for fiber analysis. Both variations within a PDL and among the PDL with different shapes, i.e. round-shaped and kidney-shaped PDLs, are described in terms of tissue thickness, fiber distribution, local fiber densities, and fiber orientation (namely azimuthal and elevation angles). Furthermore, the tissue and collagen fiber network responses to mechanical loading were evaluated in a similar manner. A 3D helical alignment pattern was observed in the fiber network, which appears to regulate and adapt a screw-like tooth motion under occlusion. The microstructural heterogeneity quantified here allows development of sample-specific constitutive models to characterize the PDL's functional and pathological loading responses, thereby providing a new multiscale framework for advancing our knowledge of this complex limited mobility soft-hard tissue interface.

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author
; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Fast-Fourier transform, Fibrous network quantification, Loading response, Phase-contrast micro-CT, Soft tissue heterogeneity
in
Journal of Structural Biology
volume
213
issue
3
article number
107772
publisher
Elsevier
external identifiers
  • scopus:85111519343
  • pmid:34311076
ISSN
1047-8477
DOI
10.1016/j.jsb.2021.107772
language
English
LU publication?
yes
id
24841d33-a8b8-47a9-a671-03d4cafc8d22
date added to LUP
2021-08-24 13:25:21
date last changed
2024-06-01 14:26:52
@article{24841d33-a8b8-47a9-a671-03d4cafc8d22,
  abstract     = {{<p>The periodontal ligament (PDL) is a highly heterogeneous fibrous connective tissue and plays a critical role in distributing occlusal forces and regulating tissue remodeling. Its mechanical properties are largely determined by the extracellular matrix, comprising a collagenous fiber network interacting with the capillary system as well as interstitial fluid containing proteoglycans. While the phase-contrast micro-CT technique has portrayed the 3D microscopic heterogeneity of PDL, the topological parameters of its network, which is crucial to understanding the multiscale constitutive behavior of this tissue, has not been characterized quantitatively. This study aimed to provide new understanding of such microscopic heterogeneity of the PDL with quantifications at both tissue and collagen network levels in a spatial manner, by combining phase-contrast micro-CT imaging and a purpose-built image processing algorithm for fiber analysis. Both variations within a PDL and among the PDL with different shapes, i.e. round-shaped and kidney-shaped PDLs, are described in terms of tissue thickness, fiber distribution, local fiber densities, and fiber orientation (namely azimuthal and elevation angles). Furthermore, the tissue and collagen fiber network responses to mechanical loading were evaluated in a similar manner. A 3D helical alignment pattern was observed in the fiber network, which appears to regulate and adapt a screw-like tooth motion under occlusion. The microstructural heterogeneity quantified here allows development of sample-specific constitutive models to characterize the PDL's functional and pathological loading responses, thereby providing a new multiscale framework for advancing our knowledge of this complex limited mobility soft-hard tissue interface.</p>}},
  author       = {{Zhong, Jingxiao and Pierantoni, Maria and Weinkamer, Richard and Brumfeld, Vlad and Zheng, Keke and Chen, Junning and Swain, Michael V. and Weiner, Steve and Li, Qing}},
  issn         = {{1047-8477}},
  keywords     = {{Fast-Fourier transform; Fibrous network quantification; Loading response; Phase-contrast micro-CT; Soft tissue heterogeneity}},
  language     = {{eng}},
  number       = {{3}},
  publisher    = {{Elsevier}},
  series       = {{Journal of Structural Biology}},
  title        = {{Microstructural heterogeneity of the collagenous network in the loaded and unloaded periodontal ligament and its biomechanical implications}},
  url          = {{http://dx.doi.org/10.1016/j.jsb.2021.107772}},
  doi          = {{10.1016/j.jsb.2021.107772}},
  volume       = {{213}},
  year         = {{2021}},
}