  Bone is a stiff and though, hierarchical and continuously evolving material
that optimizes its structure to respond to mechanical stimuli, which also
govern growth and remodeling processes. However, a full understanding of the
underlying mechanisms responsible for the cooperation of bone toughness and
biological functions, with important implications in bone ageing, osteoporosis
and tissue repair, has yet to be achieved. In particular, how micro-damage
nucleation, needed for tissue remodeling, does not evolve into catastrophic
failure in such a stiff material, still remains a partial enigma, cement lines,
interfaces and sacrificial elements alone not providing a definitive answer to
the question. Here, we bring to light a novel stress-based bone toughening
mechanism, calling into play the nearly-symmetrical, chiral and hierarchical
architecture of the osteons, demonstrating that their arrangement
simultaneously gives rise to stress states alternating in sign along the osteon
radius and to localized stress amplifications, both in the tensile and
compressive regimes. This unveils a previously unforeseen synergistic mechanism
allowing micro-damage accumulation without propagating cracks, kindled by the
contrast between crack-opening due to tensile hoop stresses and crack-stopping
due to compressive stresses at the crack tips in adjacent lamellae, which seal
the crack ends conferring toughness to bone well beyond that predicted by
current models. Furthermore, shear stresses occur at the lamellar interfaces,
contributing with fluid flow to mechanically stimulate the osteocytes and to
amplify the bone signalling. These results, obtained through original exact
elastic solutions and confirmed by both FE fracture analyses and experimental
tests on 3D-printed osteon prototypes, contribute with another piece in the
puzzle to making the rational biophysical picture of bone mechanobiology
complete.
