Toughening and mechanosensing in bone: a perfectly balanced mechanism based on competing stresses

Abstract

Bone is a stiff and though, hierarchically organized and continuously evolving material that optimizes its structure across the scales to properly respond to mechanical stimuli, which also govern growth and remodelling processes through a complex cascades of interlaced mechanobiological events. However, a full understanding of the fascinating underlying mechanisms responsible for the cooperation of bone toughness and biological functions, with important implications in bone ageing, osteoporosis and post-trauma repairing processes, has yet to be achieved. In particular, how micro-damage nucleation -which is necessary for tissue remodelling-does not evolve into catastrophic failure in such a stiff material, still remains a partial enigma, given that the presence of cement lines, interfaces and sacrificial elements, which dissipate energy and deviate cracks, alone do not provide a definitive answer to the question. To help solve this challenging problem, here we bring to light a novel stress-based bone toughening mechanism, calling into play the nearly-symmetrical, chiral and hierarchical architecture of the osteon, in which adjacent lamellae are arranged in clockwise and counter-clockwise manners as a result of the different orientation of their components, i.e. collagen fibrils and carbonated hydroxyapatite crystallites. Somewhat counter-intuitively, we demonstrate that this arrangement simultaneously gives rise to stress states that are alternating in sign along the osteon radius and to localized stress amplification phenomena, both in the tensile and compressive regimes. This unveils a previously unforeseen synergistic mechanism allowing micro-damage accumulation without propagating cracks, which is kindled by the contrast between crack-opening due to tensile hoop stresses (required for bone remodelling)