Structure-Function Relationships: Defining the Design Criteria

(funded by NIH U01 EB016422) 5-12

Scientific illustration of biologic tendon to bone attachment structures
Figure 2: At the millimeter length scale (left), tendon attaches to bone over a large footprint area. At the micrometer length scale (middle), gradients exist in mineral content and orientation, and tissues interdigitate across wavy interfaces. At the nanometer length scale (right), mineral accumulates in collagen fibril gap spaces and on surfaces to stiffen the fibrils.

We have demonstrated that the enthesis is a functionally graded material with regard to its cell phenotypes, extracellular matrix composition, structural organization, and mechanical properties. A number of mechanisms across multiple spatial scales combine to produce a robust mechanical attachment between the two materials (Figure 2). At the nanometer length scale, mineral crystals accumulate on collagen fibrils to stiffen them, but only after a percolated network of mineral forms.7,11,12 The particular arrangement of the mineral crystals relative to the collagen fibril gap channels and outer surfaces dictates their stiffening effects. At the micrometer length scale, the concentration of mineral, the interdigitation of mineralized and unmineralized tissues, and a compliant zone serve to balance strength and toughness of the attachment.7,12-14 For example, although interdigitation leads to a small decrease in attachment strength, it also leads to a dramatic increase in attachment toughness.13 Similarly, a surprising and counter-intuitive compliant zone between tendon and bone, measured experimentally5, serves to reduce stress concentrations at the enthesis and further toughen the attachment.9 At the millimeter length scale, the tendon splays at the attachment to reduce stress concentrations6 and the attachment footprint area scales to normalize stress15. Understanding these mechanisms of load transfer provides the design criteria for effective attachment of tendon to bone.