Bone indentation recovery time correlates with bond reforming time

Despite centuries of work, dating back to Galileo1, the molecular basis of bone's toughness and strength remains largely a mystery. A great deal is known about bone microsctructure2,3,4,5 and the microcracks6,7 that are precursors to its fracture, but little is known about the basic mechanism for dissipating the energy of an impact to keep the bone from fracturing. Bone is a nanocomposite of hydroxyapatite crystals and an organic matrix. Because rigid crystals such as the hydroxyapatite crystals cannot dissipate much energy, the organic matrix, which is mainly collagen, must be involved. A reduction in the number of collagen cross links has been associated with reduced bone strength8,9,10 and collagen is molecularly elongated (‘pulled’) when bovine tendon is strained11. Using an atomic force microscope12,13,14,15,16, a molecular mechanistic origin for the remarkable toughness of another biocomposite material, abalone nacre, has been found12. Here we report that bone, like abalone nacre, contains polymers with ‘sacrificial bonds’ that both protect the polymer backbone and dissipate energy. The time needed for these sacrificial bonds to reform after pulling correlates with the time needed for bone to recover its toughness as measured by atomic force microscope indentation testing. We suggest that the sacrificial bonds found within or between collagen molecules may be partially responsible for the toughness of bone.