The morphology of the interfacial tissue between bighorn sheep horn and bony horncore increases contact surface to enhance strength and facilitate load transfer from the horn to the horncore.

The horns of bighorn sheep rams are permanent cranial appendages used for high energy head-to-head impacts during interspecific combat. The horns attach to the underlying bony horncore by a layer of interfacial tissue that facilitates load transfer between the impacted horn and underlying horncore, which has been shown to absorb substantial energy during head impact. However, the morphology and mechanical properties of the interfacial tissue were previously unknown. Histomorphometry was used to quantify the interfacial tissue composition and morphology and lap-shear testing was used to quantify its mechanical properties. Histological analyses revealed the interfacial tissue is a complex network of collagen and keratin fibers, with collagen being the most abundant protein. Sharpey's fibers provide strong attachment between the interfacial tissue and horncore bone. The inner horn surface displayed microscopic porosity and branching digitations which increased the contact surface with the interfacial tissue by approximately 3-fold. Horn-horncore samples tested by lap-shear loading failed primarily at the horn surface, and the interfacial tissue displayed non-linear strain hardening behavior similar to other soft tissues. The elastic properties of the interfacial tissue (i.e., low- and high-strain shear moduli) were comparable to previously measured values for the equine laminar junction. The interfacial tissue contact surface was positively correlated with the interfacial tissue shear strength (1.23 ± 0.21 MPa), high-strain shear modulus (4.5 ± 0.7 MPa), and strain energy density (0.38 ± 0.07 MJ/m3). STATEMENT OF SIGNIFICANCE: The bony horncore in bighorn sheep rams absorbs energy to reduce brain cavity accelerations and mitigate brain injury during head butting. The interfacial zone between the horn and horncore transfers energy from the impacted horn to the energy absorbing horncore but has been largely neglected in previous models of bighorn sheep ramming since interfacial tissue properties were previously unknown. This study quantified the morphology and mechanical properties of the horn-horncore interfacial tissue to better understand structure-property relationships that contribute to energy transfer during ramming. Results from this study will improve models of bighorn sheep ramming used to study mechanisms of brain injury mitigation and may inspire novel materials and structures for brain injury prevention in humans.

Structure-property relationships of velar bone tissue from the energy absorbing horncore of bighorn sheep rams.

Velar bone is the material that fills the horncore of bighorn sheep rams. The architectural dimensions of velar bone are orders of magnitude larger than trabecular bone, and velae are more sail-like compared to strut-like trabeculae. Velar bone is important for energy absorption and reduction of brain cavity accelerations during high energy head impacts, but velar bone material properties were previously unknown. It was hypothesized that velar bone tissue would have properties that are beneficial for increased energy absorption at the material level. Solid velar bone beams were tested using dynamic mechanical analysis and three-point bending to quantify mechanical properties. Additionally, the porosity, osteon population density, and mineral content of the solid velar sails were quantified. The velar bone damping factor (∼0.03 - 0.06) and modulus of toughness (3.9 ± 0.4 MJ/m3) were lower than other mammalian cortical bone tissues. The solid bony sails have a bending modulus (8.6 ± 0.5 GPa) that lies within the range of bending moduli values previously reported for individual trabecular struts and cortical bone tissue. The solid velar bone sails had porosity (6.7 ± 0.9 %) and bone mineral content (66 ± 1 %) in the range of cortical bone values. Interestingly, velar sails contained osteons, which are rarely found in trabecular struts. The velar bone osteon population density (5.8 ± 0.9 osteons/mm2) is in the low end of the range of values reported for cortical bone in other mammals. STATEMENT OF SIGNIFICANCE: Bighorn sheep rams sustain high energy head impacts during intraspecific combat without overt signs of brain injury. Previous studies have shown that the bony horncore plays a critical role in energy absorption and reduction of brain cavity accelerations post impact, which has implications for concussion prevention in humans. However, the material properties of the horncore velar bone were previously unknown. This study quantified the material properties and structure-property relationships of the horncore velar bone at the tissue level. Results from this study will improve our understanding of how bighorn sheep mitigate brain injury during head-to-head impacts and may inspire the design of novel materials for energy absorption applications (i.e., helmets materials that reduce concussion occurrence in humans).

How the geometry and mechanics of bighorn sheep horns mitigate the effects of impact and reduce the head injury criterion.

Male bighorn sheep (Ovis canadensis) participate in seasonal ramming bouts that can last for hours, yet they do not appear to suffer significant brain injury. Previous work has shown that the keratin-rich horn and boney horncore may play an important role in mitigating brain injury by reducing brain cavity accelerations through energy dissipating elastic mechanisms. However, the extent to which specific horn shapes (such as the tapered spiral of bighorn sheep) may reduce accelerations post-impact remains unclear. Thus, the goals of this work were to (a) quantify bighorn sheep horn shape, particularly the cross-sectional areal properties related to bending that largely dictate post-impact deformations, and (b) investigate the effects of different tapered horn shapes on reducing post-impact accelerations in an impact model with finite element analysis. Cross-sectional areal properties indicate bighorn sheep horns have a medial-lateral bending preference at the horn tip (p= 0.006), which is likely to dissipate energy through medial-lateral horn tip oscillations after impact. Finite element modeling showed bighorn sheep native horn geometry reduced the head injury criterion (HIC15) by 48% compared to horns with cross-sections rotated by 90° to have a cranial-caudal bending preference, and by 125% compared to a circular tapered spiral model. These results suggest that the tapered spiral horn shape of bighorn sheep is advantageous for dissipating energy through elastic mechanisms following an impact. These findings can be used to broadly inform the design of improved safety equipment and impact systems.

Bioinspired energy absorbing material designs using additive manufacturing.

Nature provides many biological materials and structures with exceptional energy absorption capabilities. Few, relatively simple molecular building blocks (e.g., calcium carbonate), which have unremarkable intrinsic mechanical properties individually, are used to produce biopolymer-bioceramic composites with unique hierarchical architectures, thus producing biomaterial-architectures with extraordinary mechanical properties. Several biomaterials have inspired the design and manufacture of novel material architectures to address various engineering problems requiring high energy absorption capabilities. For example, the microarchitecture of seashell nacre has inspired multi-material 3D printed architectures that outperform the energy absorption capabilities of monolithic materials. Using the hierarchical architectural features of biological materials, iterative design approaches using simulation and experimentation are advancing the field of bioinspired material design. However, bioinspired architectures are still challenging to manufacture because of the size scale and architectural hierarchical complexity. Notwithstanding, additive manufacturing technologies are advancing rapidly, continually providing researchers improved abilities to fabricate sophisticated bioinspired, hierarchical designs using multiple materials. This review describes the use of additive manufacturing for producing innovative synthetic materials specifically for energy absorption applications inspired by nacre, conch shell, shrimp shell, horns, hooves, and beetle wings. Potential applications include athletic prosthetics, protective head gear, and automobile crush zones.

Material properties of bighorn sheep (Ovis canadensis) horncore bone with implications for energy absorption during impacts.

Bighorn sheep rams participate in high impact head-butting without overt signs of brain injury, thus providing a naturally occurring animal model for studying brain injury mitigation. Previously published finite element modeling showed that both the horn and bone materials play important roles in reducing brain cavity accelerations during ramming. However, in that study the elastic modulus of bone was assumed to be similar to that of human bone since the modulus of ram bone was unknown. Therefore, the goal of this study was to quantify the mechanical properties, mineral content, porosity, and microstructural organization of horncore cortical bone from juvenile and adult rams. Mineral content and elastic modulus increased with horn size, and porosity decreased. However, modulus of toughness did not change with horn size. This latter finding raises the possibility that the horncore cortical bone has not adapted exceptional toughness despite an extreme loading environment and may function primarily as an interface material between the horn and the porous bone within the horncore. Thus, geometric properties of the horn and horncore, including the porous bone architecture, may be more important for energy absorption during ramming than the horncore cortical bone. Results from this study can be used to improve accuracy of finite element models of bighorn sheep ramming to investigate these possibilities moving forward.

Bioinspired material architectures from bighorn sheep horncore velar bone for impact loading applications.

Rocky Mountain bighorn sheep rams (Ovis canadensis canadensis) routinely conduct intraspecific combat where high energy cranial impacts are experienced. Previous studies have estimated cranial impact forces to be up to 3400 N during ramming, and prior finite element modeling studies showed the bony horncore stores 3 × more strain energy than the horn during impact. In the current study, the architecture of the porous bone within the horncore was quantified, mimicked, analyzed by finite element modeling, fabricated via additive manufacturing, and mechanically tested to determine the suitability of the novel bioinspired material architecture for use in running shoe midsoles. The iterative biomimicking design approach was able to tailor the mechanical behavior of the porous bone mimics. The approach produced 3D printed mimics that performed similarly to ethylene-vinyl acetate shoe materials in quasi-static loading. Furthermore, a quadratic relationship was discovered between impact force and stiffness in the porous bone mimics, which indicates a range of stiffness values that prevents impact force from becoming excessively high. These findings have implications for the design of novel bioinspired material architectures for minimizing impact force.

Differing trabecular bone architecture in dinosaurs and mammals contribute to stiffness and limits on bone strain.

The largest dinosaurs were enormous animals whose body mass placed massive gravitational loads on their skeleton. Previous studies investigated dinosaurian bone strength and biomechanics, but the relationships between dinosaurian trabecular bone architecture and mechanical behavior has not been studied. In this study, trabecular bone samples from the distal femur and proximal tibia of dinosaurs ranging in body mass from 23-8,000 kg were investigated. The trabecular architecture was quantified from micro-computed tomography scans and allometric scaling relationships were used to determine how the trabecular bone architectural indices changed with body mass. Trabecular bone mechanical behavior was investigated by finite element modeling. It was found that dinosaurian trabecular bone volume fraction is positively correlated with body mass similar to what is observed for extant mammalian species, while trabecular spacing, number, and connectivity density in dinosaurs is negatively correlated with body mass, exhibiting opposite behavior from extant mammals. Furthermore, it was found that trabecular bone apparent modulus is positively correlated with body mass in dinosaurian species, while no correlation was observed for mammalian species. Additionally, trabecular bone tensile and compressive principal strains were not correlated with body mass in mammalian or dinosaurian species. Trabecular bone apparent modulus was positively correlated with trabecular spacing in mammals and positively correlated with connectivity density in dinosaurs, but these differential architectural effects on trabecular bone apparent modulus limit average trabecular bone tissue strains to below 3,000 microstrain for estimated high levels of physiological loading in both mammals and dinosaurs.