Elastic anisotropy and collagen orientation of osteonal bone are dependenton the mechanical strain distribution

There is evidence that the collagen microarchitecture of bone is influenced by mechanical stresses or strains. We hypothesized that peak functional st rains correlate with the elastic anisotropy and collagen orientation of bon e tissue and that the bone anisotropy might be changed by altering the stra in patterns in canine radii for 12 months. We tested these hypotheses in st udies using nine adult foxhounds. The baseline group (n = 3) had three rose tte strain gauges placed around the midshaft of the radius, and strain dist ributions were measured during walking. The osteotomy group (n = 3) had 2 c m of the ulna surgically removed, and the sham group (n = 3) received a sha m osteotomy. The osteotomy and sham groups were allowed free movement in ca ges with runs for 12 months, after which strain distributions mere measured on the radii during walking. Bone-tissue anisotropy and collagen architect ure were measured in radii from which the in vivo longitudinal strain patte rns had been measured. The collagen birefringence patterns were measured wi th use of a circularly polarized light technique, and the elastic anisotrop y of the bone, mineral, and collagen matrix was evaluated with a novel acou stic microscopy technique. Peak longitudinal strains in the radius correlat ed with the normalized longitudinal structure index (a polarized light meas ure of collagen birefringence) and the tissue anisotropy ratio. The average anisotropy ratio was 1.28 +/- 0.01 in the posterior (compressive) cortex a nd 1.43 +/- 0.01 in the anterior (tensile) cortex (these values are signifi cantly different at p < 0.0001). The ulnar osteotomy changed the strain pat tern on the radius, causing increased tensile strains in the medial cortex by more than 5-fold that were associated with a significant increase in the anisotropy ratio in the bone tissue. The longitudinal structure index was strongly correlated (r = 0.62, p < 0.005) with the anisotropy ratio of demi neralized bone but was not correlated with that of deproteinized bone; this indicates that it reflects collagen fibril orientation in the bone matrix. These results indicate that mechanical strains affect both collagen and mi neral microarchitecture in bone tissue, i.e., tensile strains are associate d with increased tissue anisotropy and compressive strains, with decreased anisotropy.