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Mechanics of mineralized collagen fibrils upon transient loads

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 Added by Mario Milazzo
 Publication date 2020
  fields Physics
and research's language is English




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Collagen is a key structural protein in the human body, which undergoes mineralization during the formation of hard tissues. Earlier studies have described the mechanical behavior of bone at different scales highlighting material features across hierarchical structures. Here we present a study that aims to understand the mechanical properties of mineralized collagen fibrils upon tensile/compressive transient loads, investigating how the kinetic energy propagates and it is dissipated at the molecular scale, thus filling a gap of knowledge in this area. These specific features are the mechanisms that Nature has developed to passively dissipate stress and prevent structural failures. In addition to the mechanical properties of the mineralized fibrils, we observe distinct nanomechanical behaviors for the two regions (i.e., overlap and gap) of the D-period to highlight the effect of the mineralization. We notice decreasing trends for both wave speeds and Young s moduli over input velocity with a marked strengthening effect in the gap region due to the accumulation of the hydroxyapatite. In contrast, the dissipative behavior is not affected by either loading conditions or the mineral percentage, showing a stronger dampening effect upon faster inputs compatible to the bone behavior at the macroscale. Our results improve the understanding of mineralized collagen composites unveiling the energy dissipative behavior of such materials. This impacts, besides the physiology, the design and characterization of new bioinspired composites for replacement devices (e.g., prostheses for sound transmission or conduction) and for optimized structures able to bear transient loads, e.g., impact, fatigue, in structural applications.



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Bone is mineralized tissue constituting the skeletal system, supporting and protecting body organs and tissues. At the molecular level, mineralized collagen fibril is the basic building block of bone tissue, and hence, understanding bone properties down to fundamental tissue structures enables to better identify the mechanisms of structural failures and damages. While efforts have focused on the study of the micro- and macro-scale viscoelasticity related to bone damage and healing based on creep, mineralized collagen has not been explored on a molecular level. We report a study that aims at systematically exploring the viscoelasticity of collagenous fibrils with different mineralization levels. We investigate the dynamic mechanical response upon cyclic and impulsive loads to observe the viscoelastic phenomena from either shear or extensional strains via molecular dynamics. We perform a sensitivity analysis with several key benchmarks: intrafibrillar mineralization percentage, hydration state, and external load amplitude. Our results show a growth of the dynamic moduli with an increase of mineral percentage, pronounced at low strains. When intrafibrillar water is present, the material softens the elastic component but considerably increases its viscosity, especially at high frequencies. This behaviour is confirmed from the material response upon impulsive loads, in which water drastically reduces the relaxation times throughout the input velocity range by one order of magnitude, with respect to the dehydrated counterparts. We find that upon transient loads, water has a major impact on the mechanics of mineralized fibrillar collagen, being able to improve the capability of the tissue to passively and effectively dissipate energy, especially after fast and high-amplitude external loads.
Collagen is the key protein of connective tissue (i.e., skin, tendons and ligaments, cartilage, among others) accounting for 25% to 35% of the whole-body protein content, and entitled of conferring mechanical stability. This protein is also a fundamental building block of bone due to its excellent mechanical properties together with carbonated hydroxyapatite minerals. While the mechanical resilience and viscoelasticity have been studied both in vitro and in vivo from the molecule to tissue level, wave propagation properties and energy dissipation have not yet been deeply explored, in spite of being crucial to understand the vibration dynamics of collagenous structures (e.g., eardrum, cochlear membranes) upon impulsive loads. By using a bottom-up atomistic modelling approach, here we study a collagen peptide under two distinct impulsive displacement loads, including longitudinal and transversal inputs. Using a one-dimensional string model as a model system, we investigate the roles of hydration and load direction on wave propagation along the collagen peptide and the related energy dissipation. We find that wave transmission and energy-dissipation strongly depend on the loading direction. Also, the hydrated collagen peptide can dissipate five times more energy than dehydrated one. Our work suggests a distinct role of collagen in term of wave transmission of different tissues such as tendon and eardrum. This study can step towards understanding the mechanical behaviour of collagen upon transient loads, impact loading and fatigue, and designing biomimetic and bio-inspired materials to replace specific native tissues such as the tympanic membrane.
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