Functional Grading of Mineral and Collagen in the Attachment of Tendon to Bone

Abstract

Attachment of dissimilar materials is a major challenge because high levels of localized stress may develop at their interfaces. An effective biologic solution to this problem exists at one of nature's most extreme interfaces: the attachment of tendon (a compliant, structural "soft tissue") to bone (a stiff, structural "hard tissue"). The goal of our study was to develop biomechanical models to describe how the tendon-to-bone insertion derives its mechanical properties. We examined the tendon-to-bone insertion and found two factors that give the tendon-to-bone transition a unique grading in mechanical properties: 1), a gradation in mineral concentration, measured by Raman spectroscopy; and 2), a gradation in collagen fiber orientation, measured by polarized light microscopy. Our measurements motivate a new physiological picture of the tissue that achieves this transition, the tendon-to-bone insertion, as a continuous, functionally graded material. Our biomechanical model suggests that the experimentally observed increase in mineral accumulation within collagen fibers can provide significant stiffening of the partially mineralized fibers, but only for concentrations of mineral above a "percolation threshold" corresponding to formation of a mechanically continuous mineral network within each collagen fiber (e.g., the case of mineral connectivity extending from one end of the fiber to the other). Increasing dispersion in the orientation distribution of collagen fibers from tendon to bone is a second major determinant of tissue stiffness. The combination of these two factors may explain the nonmonotonic variation of stiffness over the length of the tendon-to-bone insertion reported previously. Our models explain how tendon-to-bone attachment is achieved through a functionally graded material composition, and provide targets for tissue engineered surgical interventions and biomimetic material interfaces.

Processing of polycaprolactone and hydroxyapatite to fabricate graded electrospun composites for tendon-bone interface regeneration

“…Since the extruder continuously disperses and distributes the particles during the process, the closeness of actual and experimental loading levels is not surprising. Overall, Figure 2 clearly demonstrates that the linearly and continuously varying nHA concentration was accomplished across the mesh thickness, which is in accordance with the change of mineral concentration observed across the native tendon-bone interface [18].…”

“…In this study, the process was ceased after approximately 8 h, because the thickness obtained within this period would be appropriate for tendon-bone regeneration applications. Tendonbone interface thickness in native tissue is reported to change between 100-200 μm [18]. The presence of nHA mineral particles within the entire mesh was determined from samples obtained from eight different and equally spaced locations.…”

“…Electrospinning these two components, namely PCL and nHA, simultaneously in a feed rate controlled manner would generate spatially graded PCL-nHA composite meshes, which would be very suitable for tendon-bone interface tissue engineering applications. It is accepted and demonstrated [18] that the tendon-bone interface is characterized by continuously changing mineral concentrations across the interface. Therefore, the composite mesh fabricated here could mimic this interface and be potentially utilized for its regeneration/repair.…”

“…For example, an investigation on the supraspinatus tendon-to-bone insertion of Fisher Rat demonstrated that change in mineral content occurs within ~120 μm resolution [18]. Since an abrupt change in material properties between two homogeneous materials generally leads to mechanical failure due to high stress concentrations accumulated at the interface, fabrication of devices with gradients in properties at physiological resolution is a requirement for better mimicking the structures and functions of native tissues.…”

Cartilage-Bone Interface Features, Scaffold and Cell Options for Regeneration

“…Another school of thought for the hierarchical organization of the cartilage-bone interface is the belief of graded change in the composition of ECM components [6][7][8][9]. Although the compartmental organization approach for cartilage-bone interface components has been dominant for years [5,10], recent studies characterizing cartilagebone, as well as tendon-bone, interface at microscopic dimensions found that mineral composition is changing gradually across the interface [4,11,12].…”