The Role of Mineral in the Storage of Elastic Energy in Turkey Tendons

Abstract

Mammals elastically store energy in leg and foot tendons during locomotion. In the turkey, much of the force generated by the gastrocnemius muscle is stored as elastic energy during tendon deformation and not within the muscle. During growth, avian tendons mineralize in the portions distal to the muscle and show increased tensile strength and modulus as a result. The purpose of this study was to evaluate the viscoelastic behavior of turkey tendons and self-assembled collagen fiber models to determine the molecular basis for tendon deformation. The stress-strain behavior of tendons and self-assembled collagen fibers was broken into elastic and viscous components. The elastic component was found to be to a first approximation independent of source of the collagen and to depend only on the extent of cross-linking. In the absence of cross-links the elastic component of the stress was found to be negligible for self-assembled type I collagen fibers. In the presence of cross-links the behavior approached that found for mineralized turkey tendons. The elastic constant for turkey tendon was shown to be between 5 and 7.75 GPa while it was about 6.43 GPa for self-assembled collagen fibers aged for 6 months at 22 degrees C. The viscous component for mineralized turkey tendons was about the same as that of self-assembled collagen fibers aged for 6 months, a result suggesting that addition of mineral does not alter the viscous properties of tendon. It is concluded that elastic energy storage in tendons involves direct stretching of the collagen triple-helix, nonhelical ends, and cross-links between the molecules and is unaffected by mineralization. Furthermore, it is hypothesized that mineralization of turkey tendons is an efficient means of preserving elastic energy storage while providing for increased load-bearing ability required for locomotion of adult birds.

Mechanical Implications of the Domain Structure of Fiber-Forming Collagens: Comparison of the Molecular and Fibrillar Flexibilities of the α1-Chains Found in Types I–III Collagen

“…Results of these studies suggest that the elastic modulus for types I and II collagen appears to be between 7 and 8 GPa in tendon, in the superficial zone of articular cartilage and in self-assembled type I collagen fibers (Silver et al, 2000(Silver et al, 2a-c, 2002. The value of the elastic modulus for collagens in dermis and cardiovascular tissue is somewhat lower due to differences in molecular packing and composition (Silver et al, 2000b(Silver et al, , 2001b. The value for the elastic modulus measured for dermis (4 MPa) is lower, due to the higher tilt angle and a different cross-link pattern (Silver et al, 2001a).…”

“…The value for the elastic modulus measured for dermis (4 MPa) is lower, due to the higher tilt angle and a different cross-link pattern (Silver et al, 2001a). The high value of the elastic modulus for tendon, mineralized tendon and superficial zone of articular cartilage suggests that the physiologic role of fibrilforming collagens in many extracellular matrices may be to promote the storage of elastic energy during tensile deformation (Silver et al, 2000a(Silver et al, , 2000b(Silver et al, , 2001a. It has recently been proposed that mineralization is an efficient means for increasing elastic energy storage and transmission in developing turkey tendons (Silver et al, 2000b;2001a).…”

Micromechanical bending of single collagen fibrils using atomic force microscopy

“…The Young's moduli are comparable to those of dry collagen (1-8 GPa) presented in literature. [14][15][16][17] After cross-linking with glutaraldehyde, an average Young's modulus value of 14.7 6 2.7 GPa from Eq. (3) or 3.8 6 0.8 GPa from Eq.…”

“…With macro-tensile testing, the data presented in the literature on the modulus of elasticity (Young's modulus) of dry collagen tissue and collagen fibers range from 1 to 8 GPa. [14][15][16][17] Based on Xray diffraction studies, Puxkandl et al reported that the overall strain of the tendon was always larger than the strain in the individual fibrils. 18 In addition, Sasaki and Odajima 19,20 reported different values of Young's modulus by testing collagen molecules, fibrils and tendons.…”

Biomimetic Collagen Nanofibrous Materials for Bone Tissue Engineering

“…Many researchers focused on the relationship between the fine structure of the periodic banding pattern of type I collagen, the onset and progression of mineralization and elastic strain energy storage during tensile deformation of the protein. [29][30][31] Their works have led to biomechanical considerations of elastic energy storage in collagen and the molecular basis for elastic and viscous deformation, as well as for energy storage of collagen. [32] It is proposed that tensile deformation of collagen involves stretching of the flexible regions in its hole and overlap zones that are opened to provide possible binding sites for calcium and phosphate ions involved in mineralization.…”