Molecular origin of viscoelasticity in mineralized collagen fibrils

TL;DR

This study uses molecular dynamics to explore how mineralization and hydration affect the viscoelastic properties of collagen fibrils, revealing water's role in energy dissipation and mechanical behavior at the molecular level.

Contribution

It provides the first systematic molecular-level analysis of mineralization and hydration effects on collagen fibril viscoelasticity using dynamic simulations.

Findings

Increased mineralization raises dynamic moduli, especially at low strains.

Water presence softens elastic response but increases viscosity, notably at high frequencies.

Water drastically reduces relaxation times, enhancing energy dissipation during transient loads.

Abstract

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.