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Cushion Mechanism of Goat Hoof Bulb Tissues

Cushion Mechanism of Goat Hoof Bulb Tissues Hindawi Applied Bionics and Biomechanics Volume 2019, Article ID 3021576, 11 pages https://doi.org/10.1155/2019/3021576 Research Article 1 1 1 2 2 1 Weijun Tian , Hai Liu , Qi Zhang , Bo Su, Wei Xu , and Qian Cong Key Laboratory of Bionic Engineering (Ministry of Education, China), Jilin University, Changchun 130022, China China North-Vehicle Research, Fengtai District, Beijing 100072, China Correspondence should be addressed to Qian Cong; congqian@jlu.edu.cn Received 21 April 2019; Revised 9 September 2019; Accepted 3 October 2019; Published 6 November 2019 Academic Editor: Craig P. McGowan Copyright © 2019 Weijun Tian et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The hoof bulb sections of white goats were observed via scanning electron microscopy and stereomicroscopy in order to explore the cushion mechanism in the bulb tissue microstructures of hoofed animals. The hoof bulbs consisted of multilayer tissues, including an epidermal layer, a dermal layer, and subcutaneous tissues from outside to inside. A bionic model based on hoof bulb tissue composite structures was built with a normal model as the control. The microcosmic mechanics of the bulb tissues was analyzed via the finite element method. Simulations showed that when the bionic model was impacted by the top plates at the speed of 1-10 m/s, stress was concentrated in the epidermal layer and uniformly distributed in the dermal layer and dermal papillae, which effectively reduced the impact onto the ground. The cornified epidermal layer can resist the instant impact onto the ground, while the dermal papillae embedded in the dermal layer can store, release, and dissipate the impulsive energy, and the three parts synergically act in the cushion. 1. Introduction camels consist of several layers, including the sole (cornified pad), common coverings, digital cushions, and yellow bed The feet of animals consist of numerous bones, muscles, lig- [6]. The broad and fat pads connecting the toes prevent aments, and joints and are the major part of weight bearing camels from sinking into the loose sand and allow them to and motion. Feet mainly function as cushion and support walk or run nonstop in deserts [2]. Their unique limbs make and show unique functions and characteristics during the African elephants the terrestrial organism that can support activities of animals owing to the special tissue structures the heaviest weight. In addition to other morphological and biomechanical properties [1]. characteristics, the feet of African elephants are equipped During the moving process, feet are the only part where with large pads, which can bear, store, or absorb machinery force and are critical in force allocation [7]. The foot pads of animals make contact with the ground, and due to the sud- den variation of forces upon the contact, the instant force is African elephants are mainly composed of sheet-like or several times larger than the weight [2, 3]. The percussive bunch-like fiber connective tissues, forming large gaps waves induced by the ground reaction are transferred from among metacarpals, metatarsal bones, and phalanges, and the feet through the limbs and to the trunk and then through the gaps are filled with lipid tissues, and the inner of foot the backbones to the brain. In the natural surroundings, these pads consist of collagens and web-like elastic fibers [8]. animals usually go through a lot of uneven ground, which Histologically, the claws and foot pads are separated by the produces the large impact to the animal’s body. Excessively soft honeycomb-like bodies built by closed partitions or large impact will severely damage the body and brain of ani- the collagen-strengthened elastic dissepiments and are filled mals [4]. The reason these animals adapt to the uneven with lipid (lipid tissue) cells [2, 9, 10]. Foot pads are excellent ground is largely the protection of their foot structure. weight-bearing biostructures and depend on the closed cells The foot pads and claws are a great design of nature and filled with liquids or lipid tissues to cushion the large distor- are the protective and bearing structures of feet. The feet of tion. During deformation, the amount of such structural camels are like tires filled with lipids [5]. The foot pad of response is nonlinear [11]. During the past decades, many 2 Applied Bionics and Biomechanics From the remaining 2 goats, the hoofs were cut off, and biomechanical studies have been conducted on animal claws and foot pads but are focused on the mechanical properties. the hoof capsules, which can be easily contaminated on the In particular, for hoofed animals, much research is focused surface, were pretreated. The hoof capsules were first washed on the material structures, mechanical performances, and with deionized water, then dust-removed, naturally dried, friction performance of horse hoofs [12–14]. and washed with acetone and anhydrous ethanol to remove The relationship between horse hoof wall composite the surface oil stains and other contaminants. After that, structures and functions were investigated via morphological the hoofs were dissected to acquire the hoof capsules, which and mechanical studies [15, 16]. Morphological studies were cleaned and frozen for use. The complete hoof capsules showed that the sizes, shape, and helical intermediate fila- were taken out of the refrigerator, and after thawing and soft- ments of horse hoof walls can guide the growing direction ening, were washed with clean water and wiped with dry of hoof wall cracks, so as to inhibit the inward and upward towels. Then, the hoof capsules were cut off with scalpels. crack expansion mechanisms [17–19]. Sections about 5 mm wide, 5 mm high, and in the bulb wall White goats, also called domestic goats, are the most thickness were extracted and placed onto glass slides, which numerous and widely distributed. With strong adaptability were put in a cool place for natural drying. After that, the sec- and surviving ability, they can survive under harsh cliff con- tions were stuck via electric plating adhesion onto a sample ditions. The living environment makes white goats extremely table, which was placed in vacuum film deposition equip- agile and strong. During foraging, they have to leap among ment for gold spraying for 30 s, followed by observation cliffs. To avoid chase by natural enemies, they have to be fast under an EVO 18 scanning electron microscope (SEM, Carl and continuously jump down from dozens of meters high. Zeiss Microscopy GmbH, Jena, Germany). Goat and blue sheep are cloven-hoofed animals, and the 2.2. Microscopic Observation hoofs play important roles in its locomotion [20]. Goats have a rough soft and flexible pad on the bottom of their two-toed 2.2.1. SEM. The hoof bulb tissues were observed with SEM. hoofs, and it is a shock absorber that also generates a friction The microstructures (Figure 2(a)) show that the longitudinal force due to its texture [21]. The rear end of the hoof is wide sections of hoof bulb tissues can be divided into two layers. and roughly spherical, and the outside of the toe is higher The upper layer consists of many honeycomb-like inclined than the inside, so that the soil can be consolidated below fine tube structures. As shown in Figure 3, the parameters the hoofs [22]. All these actions cannot be made by other ani- of the tubed were measured and evaluated, which would be mals of similar body form. In this study targeted at white used in the simulation. The tubes are separated at a distance goats, the unprocessed hoof bulb tissues were observed under of 140-250 μm (Figure 3(a)), the diameters are 80-110 μm scanning electron microscopy (SEM). Then, the bulb tissues (Figure 3(b)), the inclined angle is about 57 (Figure 3(c)), were stained and histologically tested under microscopy. and the layer thickness is about 1.3 mm (Figure 3(d)). Finally, the biomechanical functions of the bulb tissue micro- The epidermal layer is fully cornified (the very hard and structures were simulated with the finite element method cornified layer in contact with the ground (together with (FEM), and the cushion mechanism of hoof bulb tissues nails)), and the relatively smooth and even cornified epider- was elaborated. mis grows in a cascaded way and contains cracks. The layers are arranged in parallel and the plys are connected tightly 2. Materials and Methods (the cornified epidermis layer in Figure 2(d) is superimposed from tissue structure sheets). No defects or holes were found 2.1. Ethical Declaration. This study was approved by the (Figure 2(d)). Review Board of Jilin University (Changchun, China). In total, 6 adult and healthy white goats without limita- 2.2.2. Histologic Examination. The stereo microscope showed tion to gender (20:0±0:5kg) were bought from a farmer that the hoof bulb tissues of white goats were divided from in the suburb area of Changchun. The goats were anesthe- down to top into the epidermal layer (①), dermal layer tized and killed via carotid bleeding. From 4 of the goats, (②), dermal papillae (④), and subcutaneous connective tis- the hoof capsules and flesh hoofs were collected. Then, bulb sues (③) (Figure 4(b)). The epidermal layer was fully kerati- tissues of 1 cm were cut off (Figure 1) and fixed in 4% para- nized (Figure 4(c)), which thickened the hoof bottom. This formaldehyde for 1 week. After that, the bulb tissues were structure helps to protect the hoof capsules and avoids put into a softening solution (75 mL of 60% ethanol and microbial invasion and, when abrasion from the environ- 25 mL of glycerol) for 1 month. The softened bulb tissues ment is intensified, can effectively minimize injuries to the were dehydrated in an ethanol gradient, then treated in a hoofs [23]. Abundant fat lobules were found in the bulb tis- dimethylbenzene solution until transparency, immersed in sues, and each lobule contained numerous fat cells and was wax, and embedded in an MNT cool-hot embedder (SLEE, surrounded mainly by loose connective tissues and contained Germany) into paraffin bulks. The bulks were cut by a abundant collagenous fibers, elastic fibers, and arteriovenous CUT5062 segment device (SLEE) into continuous tissue tallies (Figure 4(a)). slices (5 μm), which were then spread in a water bath at 40 2.3. Finite Element Method (FEM) Modeling and Simulation. C, sticked, and roasted in a roasting machine. After stain- ing with hematoxylin-eosin (HE), Weigert-VG, and Sacpic, An FEM model based on the hoof bulb tissue microstructure the slices were observed under a right-above fluorescence was built and used to study the biomechanical functions of microscope (Axio Imager A2, Zeiss). this composite structure. A composite microstructured Applied Bionics and Biomechanics 3 (a) (b) Figure 1: Hoof bulb tissues. (a) The location of the slices on the goat hoof and (b) the prepared goat hoof slices. (a) (b) (c) (d) Figure 2: SEM images of hoof bulb tissues. (a) Longitudinal sections of bulb tissues; (b) longitudinal sections of the dermal layer; (c) cross- sections of the dermal layer; (d) cross-section of the epidermal layer. bionic model was established with the 1/250 hoof bulb tissues all the layers of the bionic model was built and ground on the as the prototype. This bionic model consisted of three parts: FEM software ABAQUS. Through dynamic simulation and analysis on ABAQUS, the walking or running of white goats the cube with inner inclined fine tubes, the inclined cylinder, and the cube with one arc surface, which represented the der- was simulated as well as the process of hoof capsule bulbs mal layer (Figure 5(b)), dermal papillae (Figure 5(c)), and contacting the ground. The organism soft tissues are usually epidermal layer (Figure 5(d)), respectively. For the dermal manifested as nonuniform, anisotropic, pseudoincompressi- papilla model, the tube space was set as 160 μm, diameter ble, and nonlinear-plastic-viscoelastic materials [24]. To sim- was 80 mm, incline angle was 50 plify the complex models, researchers have idealized the foot , and layer thickness was 1.3 mm. A rectangular plate was connected to the top of the bottom tissues as homogeneous and isotropic linear elastic bionic model and was called the top plate (①) (Figure 5(a)), materials [25]. The material properties of different parts of which represents the goat body with mass and velocity. In the hoof bulb tissues as well as the elements of FEM division the simulating process, the top plate acts as the dynamic body [26–28] are shown in Table 1. The material properties of the normal model are shown in Table 2. The mesh size of FEM inducing crash to the model, simulating the actual crash com- ing from the goat body to goat hoofs. Another rectangular was set as 0.02 mm. plate was fixed at the lower part of the bionic model to simu- When the mass or sizes of the object differed, the object late the hard ground (②) (Figure 5(a)). A 3D model involving with a smaller mass to contact surface area ratio is less 4 Applied Bionics and Biomechanics (a) (b) (c) (d) Figure 3: The measurement of the tubes by SEM: (a) the tube spacing (b) the diameter (c) the inclined angle, and (d) the thickness. (a) (b) (c) Figure 4: Histological images of hoof bulbs: (a) subcutaneous connective tissues, (b) longitudinal sections of bulb tissues, and (c) epidermis layer. ①: epidermal layer; ②: dermal layer; ③: subcutaneous connective tissues; ④: dermal papillae. affected by impulsive stress, because when the object crashes to the top plate velocity becoming zero. M is the mass of the unto the ground under the same velocity conditions, the con- top plate, P represents the impulse of the model under the crash of the top plate. With the same initial velocity, usually, clusion above will be obtained by the following formula: we consider ðV − V Þ/t as the constant between the bionic 1 2 model and the normal model. The smaller the mass to con- ΔP = F ⋅ t = M ⋅ V − V , V =0, ð1Þ ðÞ 1 2 2 tact surface area ratio (M/S) is, the smaller the impulsive stress P is. The bionic model for simulation was a small part V − V F M V − V 1 2 1 2 ð2Þ F = M ⋅ , P = = ⋅ : of the real hoof bulb tissues, the mass of the top plate is much t S S t smaller compared to the actual goat body mass. According to In the formula, V represents the initial velocity exerted formula (2), when M is smaller, the stress is smaller so that on the top plate and t is the time from the beginning of crash the simulating comparing result is not obvious enough. To Applied Bionics and Biomechanics 5 (a) (b) (c) (d) (e) Figure 5: (a) Hoof bulb tissue assembly model, (b) dermal layer model, (c) dermal papilla model, (d) epidermal layer model, and (e) normal model. ①: top plate; ②: ground supporting plate. consisted of two layers, including the dermal layer and the Table 1: Material properties and element types of the FEM model. epidermal layer (Figure 5(e)). For both the bionic model Young’s and the normal model, the elastic modulus, Poisson’s ratio, Name Element modulus Poisson’s and density all differed among different layers, but these E (MPa) models were composed of homogeneous, isotropic, and lin- ear elastic materials. In the two models, the same initial Epidermal layer 3-D tetrahedrons 113.8 0.38 velocity and restraint were loaded and then the outputs Dermal layer 3-D tetrahedrons 7.0 0.45 were compared. Dermal papillae 3-D tetrahedrons 0.6 0.495 206 × 10 Top plate 3-D tetrahedrons 0.3 3. FEM Result and Analysis Ground supporting 3-D tetrahedrons 206 × 10 0.3 plate The process of the goat hoof bulbs contacting the ground was simulated on ABAQUS. As shown in Figure 6, in the simulat- ing process, the instantaneous initial velocity is exerted on Table 2: Material properties and types of the normal model. the top plate firstly. Then, the top plate transfers the energy to the simulating model. So the stress first occurs on the Young’s top plate. With the simulating process ongoing, the other Name Element modulus Poisson’s parts of the simulating model will have stress and stain corre- E (MPa) sponding to the impact from the top plate,. so that the top Epidermal layer 3-D tetrahedrons 113.8 0.38 plate’s stress will change constantly during the whole simula- Dermal layer 3-D tetrahedrons 7.0 0.45 tion (Figure 6). The bionic model and the normal model were separately fixed onto the supporting plates on the ground, Top plate 3-D tetrahedrons 206 × 10 0.3 and the top plates were assigned with the initial impact veloc- Ground supporting 3-D tetrahedrons 206 × 10 0.3 ity of 1-10 m/s, and the models outputted the impact force plate onto the supporting plates (ground reaction), displacement of the upper surface of the dermal layer, and the inner stress of the models (Figure 6). improve the simulation veracity to the actual situation, we set the initial velocity of the top plate in the FEM simulation 3.1. Ground Reaction. During the motion of a goat, the reac- tion when the hoof bulbs contact the ground is one of the as 1-10 m/s, which is larger than the velocity when the goat foot touched the ground; the actual crashing velocity of a important indices to measure the biomechanical perfor- goat is about 0.69 m/s-0.9 m/s according to our experiment mance of hoof bulb tissues. As shown on the reaction-time curves (Figure 7(a)), the reaction from the supporting plates high speed photography videos. This makes the simulating result more obvious. As shown in Figure 6, stress first occurs of the two models changed with time in a typical single peak mode, indicating the ground impact during the contact at the top plate, which indicates that the top plate is the moving plate. between the hoof bulbs, and the ground impact gradually intensified and then weakened. The ground contact time of To study the cushion mechanism of goat hoof bulbs, a the bionic model was longer than that of the normal model normal model was needed in addition to the bionic model. −5 −5 In the normal model, the dermal papillae and the dermal (3×10 vs. 2:5×10 s), and the ratio of the peak reaction layer were considered as one body, and thus, this model only of the bionic model to the normal model was 0.85 (0.072 6 Applied Bionics and Biomechanics Figure 6: The simulation process of the bionic model. 0.10 1.6 1.4 0.08 1.2 1.0 0.06 0.8 0.04 0.6 0.4 0.02 0.2 0.00 0.0 –6 –5 –5 –5 –5 –5 –5 5.0×10 1.0×10 1.5×10 2.0×10 2.5×10 3.0×10 3.5×10 0 2 4 6 8 10 Time (s) Velocity (m/s) Normal model Normal model Bionic model Bionic model (a) (b) 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0 2 4 6 8 10 Velocity (m/s) Normal model Bionic model (c) Figure 7: (a) Ground reactions from the bionic model and the normal model when the top plates were loaded with the velocity of 1 m/s; (b) peak ground reactions from the two models under the loaded velocity of 1 to 10 m/s; (c) ratio of reaction peak of the bionic model to the normal model under the loaded velocity of 1 to 10 m/s. vs. 0.084 N). As the loading velocity on the top plates rose, the model to the normal model declined from 0.85 to 0.62, and peak reaction from the two models both linearly increased the changing rate decreased (Figure 7(c)). and the increasing rate was larger in the normal model (Figure 7(b)). As the loading velocity on the top plates rose 3.2. Displacement of the Upper Surface. The goat hoof bulb from 1 to 10 m/s, the ratio of peak reaction from the bionic hypodermic tissues are rich in fat tissues and elastic tissues, Ground reaction force (N) Rate of max ground reaction force Max ground reaction force (N) Applied Bionics and Biomechanics 7 0.040 0.08 0.035 0.07 0.030 0.06 0.025 0.05 0.020 0.04 0.015 0.03 0.010 0.02 0.005 0.01 0.000 0.00 0 24 6 810 0.00000 0.00001 0.00002 0.00003 Velocity (m/s) Time (s) Bionic model Bionic model Normal model Normal model (a) (b) Figure 8: (a) Displacement on the upper surface of the bionic model and the normal model at the loading velocity of 5 m/s; (b) peak displacement on the two models at different loading velocities. (Figure 9(a)). During the impact onto the ground, when which largely reduce the pressures upon contact with the ground and can scatter various external forces imposed on the ground reaction maximized, the stress on the epidermal the hoofs during the walking process. The deformation of layer from the down to the top first increased and then hoof bulbs is another key indicator of biomechanical perfor- decreased in both models (Figures 9(a)–9(c)). When the mances of hoof bulb tissues. During the FEM analysis, since loading velocity was 1 m/s, the stress-node curves of the the volumetric change rate of models can be hardly com- two models nearly overlapped, as the stress both increased puted, the displacement of the upper surface was used to from 1.5 to 2.755 and then slowly declined to 0.25 MPa, characterize the deformed amount of hoof bulb tissues. indicating that at low-velocity impact, the stress magnitude When the loading rate on the top plates was 5 m/s, the and distribution on the epidermal layer were identical maximum displacement on the upper surface of the bionic between the two models (Figure 9(b)). When the loading model and the normal model was 0.36 and 0.30 mm, respec- velocity was 10 m/s, the stress of the normal model rose tively, and the displacement-time curves were both typical of from 2.5 to 7.5 and then declined to 5.5 MPa, while that the single peak mode. At the early stage upon the impact in the bionic model first increased from 2.25 to 5.25 and −5 onto the supporting plates (5× 10 s), the displacements then slowly declined to 2.5 MPa, indicating the stress distri- butions on the epidermal layers were identical between the of the two models were nearly the same, but with the two models (Figure 9(c)). As the loading velocity rose, the prolonging of time, the difference of displacement between the two models gradually enlarged and finally stabilized at stresses at the lower parts were identical between the two models, but at the upper nodes, the stress differences 0.09 mm (Figure 8(a)). As the loading velocity on the top plates increased, the maximum displacements of both between models were enlarged (Figures 9(b) and 9(c)). As the loading velocity on the top plates rose from 1 to models increased and the difference between the two models 10 m/s, the ratio of peak epidermal stress from the bionic was unchanged. model to the normal model increased from 1.0 to 1.45 (Figure 9(d)). 3.3. Internal Stress Distribution in the Epidermal Layer Model. Since only the epidermal layers were completely the same in the two models, when the ground reaction during 3.4. Stress Distributions inside the Bionic Model. The goat the contact with the ground maximized, the stress magni- hoof bulb tissues consist of dermal papillae, the dermal layer, tudes and distributions on the central axis of the epidermal and the epidermal layer. The epidermal layer is fully cornified and mainly functions to thicken the hoof bottom. When the layers both differed between the two models. Along the cen- tral axis of the epidermal layer, 17 grid nodes were marked environmental abrasion is intensified, the epidermal layer from down to top to extract the stresses (Figure 9(a)). can effectively minimize the injuries to the hoofs. Dermal Clearly, when the ground reaction maximized, the papillae enlarge the connection area between the epidermis stress was concentrated on the epidermal layer, which and the derma, which contributes to the firm connection mainly occurred in the lower part of the epidermal layer between the two. Displacement (mm) Displacement (mm) 8 Applied Bionics and Biomechanics 3.0 2.5 S, Mises (avg: 75%) +7.302e+00 2.0 +6.703e+00 +6.104e+00 +5.505e+00 1.5 +4.906e+00 +4.307e+00 +3.708e+00 1.0 +3.109e+00 +2.510e+00 +1.912e+00 0.5 +1.313e+00 +7.139e+00 +1.150e–01 0.0 024 68 10 12 14 16 18 Number of nodes Normal model Bionic model (a) (b) 8 9 3 3 02 46 8 10 12 02468 10 12 14 16 18 Velocity (m/s) Number of nodes Normal model Normal model Bionic model Bionic model (c) (d) Figure 9: (a) Stress nephogram on the longitudinal section of the epidermal layer; stresses at different nodes when the loading speed onto the top plates was (b) 1 m/s or (c) 10 m/s; (d) peak internal stress on the epidermal layer in both models at different loading speeds. With FEM, the process of hoof bulbs impacting the 4. Discussion ground was simulated. The peak stress and stress nephograms of dermal papillae, the dermal layer, and the epidermal layer SEM and histological observation showed the goat hoof bulb at different impacting velocities were detected (Figure 10). tissues mainly consist of an epidermal layer, a dermal layer, When the ground reaction peaked, the internal stress and hypodermic connective tissues. The epidermal layer is distributions in the dermal papillae and the dermal layer fully cornified and is the hardest part of hoof bulb tissues of the bionic model were both uniform (Figures 10(a) and and mainly functions to thicken the hoof bottom and directly 10(b)). When the loading velocity on the top plates rose contacts with the ground. During motion, when the impact from 1 to 10 m/s, the peak stress increased from 0.038 to between the hoofs and the ground was aggravated and the 0.474 MPa in the dermal papillae, from 0.29 to 2.58 MPa environmental wear was intensified, the injuries to the hoofs at the dermal layer, and from 2.66 to 5.6 MPa at the epider- can be effectively decreased. The dermal layer is rich in fat tis- mal layer. As the loading velocity increased, the changing sues and elastic fibers, which largely reduce the pressures rate of the internal peak stress in the dermal papillae of upon contact with the ground and can scatter the various the bionic model was unchanged, that in the dermal layer external forces imposed onto the hoofs during the walking gradually increased, but that in the epidermal layer gradu- process and thus are critical in preventing damage to the ally declined. hoofs. Dermal papillae enlarge the connection area between Mises stress (MPa) Mises max stress (MPa) Mises stress (MPa) Applied Bionics and Biomechanics 9 U, magnitude +3.270e–02 +3.117e–02 +2.964e–02 +2.811e–02 +2.658e–02 +2.505e–02 +2.352e–02 +2.199e–02 +2.046e–02 +1.893e–02 +1.740e–02 1 +1.587e–02 +1.434e–02 02 4 68 10 Velocity (m/s) Epidermal layer Corium layer Dermal papillae (a) (b) (c) Figure 10: (a) Cross-sectional stress nephogram at the dermal layer of the bionic model; (b) longitudinal-section stress nephogram at the dermal layer of the bionic model; (c) peak internal stresses of dermal papillae, dermal layer, and epidermal layer at different loading velocities. the epidermis and the derma, which contributes to the firm related to the different living surroundings of goats and connection between the two. The dermal papillae are regu- horses: the horse usually runs on the prairie and the crash larly buried in the dermal layer at the inclining angle of 57 , condition to the hoof is the soil, whereas for the goat, the and the dermal papillae of hoof bulb tissues are much longer crash condition is usually the rock, which is harder than soil, and more regularly distributed than those in the skin. so that the goat may need more cushion capacity on their FEM showed the bionic model based on the dermal layer hoofs, and the goat hoofs having better cushion capacity than microstructures can well reduce the ground reaction, and this horse hoofs result from the differences in the tubules’ ability within a certain range was gradually strengthened inclined angle, density, and diameter. with the increment of loading velocity. This was because As the collision speed increased, the three layer structures the epidermal layer, the dermal layer, and dermal papillae of hoof bulb tissues showed different biomechanical charac- were different in structures and material properties and can teristics. As the speed rose, the impact onto the bulb tissues synergistically act to weaken the ground impact. During the was intensified accordingly, but the peak inner stresses of collision process, the epidermal layer experienced small the epidermal layer, dermal layer, and dermal papillae deformation and internal stress concentration and thus increased at different rates. The increasing rate of internal undertook a large portion of the impact. The dermal layer peak stress declined at the epidermal layer, rose at the dermal is very soft and can absorb the impulsive force by generating layer, and was unchanged in the dermal papillae. It indicated very large deformation. The dermal papillae regularly that the special microstructure layer can automatically adjust arranged at the inclination angle of 50 are very soft and the impact absorption ratios among different layers during can effectively reduce the transfer of impact from the epider- the different ground impacts. During low-speed collision, mal layer to the dermal layer and also disperse the impact in the hoof bulbs are affected by low ground impact; the epider- the dermal layer, which avoids the stress concentration and mal layer including the cuticle layer is thick and hard enough, thereby prevents the dermal layer from being destroyed. so it can suffer from the stress and protect the inner part of Based on the foot cushion property research on other animals the hoof from being damaged. So the epidermal layer under- like the cat’s paw, the impact to the ground is usually reduced takes the majority of the impact. As the collision speed by the material characteristics of fat [29, 30], whereas the increases, the collision and friction between the epidermal cushion mechanism of the goat hoof is determined by the layer and the ground are aggravated, which will further dam- composite structure and inclined holes, not only the mate- age the epidermal layer, so the epidermal layer suffers from a rials. This composite structure with holes can produce more smaller portion of the impact (as shown in Figure 10(c)) to obvious cushion capacity by the coupling methodology (mul- protect itself from being damaged. It indicates that when tilayer structure and hole structure). According to some the impact between the hoofs and the ground was aggra- researches about the horse hoofs, the tubules also exist at vated and the environmental wear was intensified, the inju- the inner hoof wall. The inclined angle of the tubules is differ- ries to the hoofs can be effectively decreased because of the ent between the left and the right foot, arranging from 86.47 lower damage of the epidermal layer. This special micro- to 104.85 ; the tubule spacing ranges from 0.36 to 0.53 mm; structure has excellent cushion ability to effectively reduce and the diameters are about 0.2 mm [31, 32]. The inclined the ground impact onto the trunk and prevents animals angle of the goat hoof inner wall is about 57 , which is smaller from being damaged by high-strength movement, such as than the horse. And the tubes of the goat hoof wall are sepa- running and jumping. rated at a distance of 0.14 mm-0.25 mm with 0.08-0.11 mm diameter; the separated distance and diameter are all smaller 4.1. Study Limitation. According to results of the FEM simu- than those of the horse. We consider that the difference is lation, the study emphasizes the cushion mechanism of the Mises max stress (MPa) 10 Applied Bionics and Biomechanics goat hoof bulb tissue structure and the model is established Acknowledgments with three structures with different material properties. The authors gratefully acknowledge the support of the But the material of each bionic structure is set as homoge- National Natural Science Foundation of China (Grant Nos. neous and isotropic linear elastic materials. The pressure 91748211, 51305157) and the project of the 13th Five-Year distribution may be different compared to the model with Common Technology (Grant No. 41412040101). nonuniform, anisotropic, pseudoincompressible, nonlinear- plastic-viscoelastic materials. The model in this study just dis- cusses the results of a homogeneous and isotropic linear elastic References material model. Further, we can research about the non- uniform, anisotropic, pseudoincompressible, and nonlinear- [1] Z. 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Cushion Mechanism of Goat Hoof Bulb Tissues

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Copyright © 2019 Weijun Tian et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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10.1155/2019/3021576
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Hindawi Applied Bionics and Biomechanics Volume 2019, Article ID 3021576, 11 pages https://doi.org/10.1155/2019/3021576 Research Article 1 1 1 2 2 1 Weijun Tian , Hai Liu , Qi Zhang , Bo Su, Wei Xu , and Qian Cong Key Laboratory of Bionic Engineering (Ministry of Education, China), Jilin University, Changchun 130022, China China North-Vehicle Research, Fengtai District, Beijing 100072, China Correspondence should be addressed to Qian Cong; congqian@jlu.edu.cn Received 21 April 2019; Revised 9 September 2019; Accepted 3 October 2019; Published 6 November 2019 Academic Editor: Craig P. McGowan Copyright © 2019 Weijun Tian et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The hoof bulb sections of white goats were observed via scanning electron microscopy and stereomicroscopy in order to explore the cushion mechanism in the bulb tissue microstructures of hoofed animals. The hoof bulbs consisted of multilayer tissues, including an epidermal layer, a dermal layer, and subcutaneous tissues from outside to inside. A bionic model based on hoof bulb tissue composite structures was built with a normal model as the control. The microcosmic mechanics of the bulb tissues was analyzed via the finite element method. Simulations showed that when the bionic model was impacted by the top plates at the speed of 1-10 m/s, stress was concentrated in the epidermal layer and uniformly distributed in the dermal layer and dermal papillae, which effectively reduced the impact onto the ground. The cornified epidermal layer can resist the instant impact onto the ground, while the dermal papillae embedded in the dermal layer can store, release, and dissipate the impulsive energy, and the three parts synergically act in the cushion. 1. Introduction camels consist of several layers, including the sole (cornified pad), common coverings, digital cushions, and yellow bed The feet of animals consist of numerous bones, muscles, lig- [6]. The broad and fat pads connecting the toes prevent aments, and joints and are the major part of weight bearing camels from sinking into the loose sand and allow them to and motion. Feet mainly function as cushion and support walk or run nonstop in deserts [2]. Their unique limbs make and show unique functions and characteristics during the African elephants the terrestrial organism that can support activities of animals owing to the special tissue structures the heaviest weight. In addition to other morphological and biomechanical properties [1]. characteristics, the feet of African elephants are equipped During the moving process, feet are the only part where with large pads, which can bear, store, or absorb machinery force and are critical in force allocation [7]. The foot pads of animals make contact with the ground, and due to the sud- den variation of forces upon the contact, the instant force is African elephants are mainly composed of sheet-like or several times larger than the weight [2, 3]. The percussive bunch-like fiber connective tissues, forming large gaps waves induced by the ground reaction are transferred from among metacarpals, metatarsal bones, and phalanges, and the feet through the limbs and to the trunk and then through the gaps are filled with lipid tissues, and the inner of foot the backbones to the brain. In the natural surroundings, these pads consist of collagens and web-like elastic fibers [8]. animals usually go through a lot of uneven ground, which Histologically, the claws and foot pads are separated by the produces the large impact to the animal’s body. Excessively soft honeycomb-like bodies built by closed partitions or large impact will severely damage the body and brain of ani- the collagen-strengthened elastic dissepiments and are filled mals [4]. The reason these animals adapt to the uneven with lipid (lipid tissue) cells [2, 9, 10]. Foot pads are excellent ground is largely the protection of their foot structure. weight-bearing biostructures and depend on the closed cells The foot pads and claws are a great design of nature and filled with liquids or lipid tissues to cushion the large distor- are the protective and bearing structures of feet. The feet of tion. During deformation, the amount of such structural camels are like tires filled with lipids [5]. The foot pad of response is nonlinear [11]. During the past decades, many 2 Applied Bionics and Biomechanics From the remaining 2 goats, the hoofs were cut off, and biomechanical studies have been conducted on animal claws and foot pads but are focused on the mechanical properties. the hoof capsules, which can be easily contaminated on the In particular, for hoofed animals, much research is focused surface, were pretreated. The hoof capsules were first washed on the material structures, mechanical performances, and with deionized water, then dust-removed, naturally dried, friction performance of horse hoofs [12–14]. and washed with acetone and anhydrous ethanol to remove The relationship between horse hoof wall composite the surface oil stains and other contaminants. After that, structures and functions were investigated via morphological the hoofs were dissected to acquire the hoof capsules, which and mechanical studies [15, 16]. Morphological studies were cleaned and frozen for use. The complete hoof capsules showed that the sizes, shape, and helical intermediate fila- were taken out of the refrigerator, and after thawing and soft- ments of horse hoof walls can guide the growing direction ening, were washed with clean water and wiped with dry of hoof wall cracks, so as to inhibit the inward and upward towels. Then, the hoof capsules were cut off with scalpels. crack expansion mechanisms [17–19]. Sections about 5 mm wide, 5 mm high, and in the bulb wall White goats, also called domestic goats, are the most thickness were extracted and placed onto glass slides, which numerous and widely distributed. With strong adaptability were put in a cool place for natural drying. After that, the sec- and surviving ability, they can survive under harsh cliff con- tions were stuck via electric plating adhesion onto a sample ditions. The living environment makes white goats extremely table, which was placed in vacuum film deposition equip- agile and strong. During foraging, they have to leap among ment for gold spraying for 30 s, followed by observation cliffs. To avoid chase by natural enemies, they have to be fast under an EVO 18 scanning electron microscope (SEM, Carl and continuously jump down from dozens of meters high. Zeiss Microscopy GmbH, Jena, Germany). Goat and blue sheep are cloven-hoofed animals, and the 2.2. Microscopic Observation hoofs play important roles in its locomotion [20]. Goats have a rough soft and flexible pad on the bottom of their two-toed 2.2.1. SEM. The hoof bulb tissues were observed with SEM. hoofs, and it is a shock absorber that also generates a friction The microstructures (Figure 2(a)) show that the longitudinal force due to its texture [21]. The rear end of the hoof is wide sections of hoof bulb tissues can be divided into two layers. and roughly spherical, and the outside of the toe is higher The upper layer consists of many honeycomb-like inclined than the inside, so that the soil can be consolidated below fine tube structures. As shown in Figure 3, the parameters the hoofs [22]. All these actions cannot be made by other ani- of the tubed were measured and evaluated, which would be mals of similar body form. In this study targeted at white used in the simulation. The tubes are separated at a distance goats, the unprocessed hoof bulb tissues were observed under of 140-250 μm (Figure 3(a)), the diameters are 80-110 μm scanning electron microscopy (SEM). Then, the bulb tissues (Figure 3(b)), the inclined angle is about 57 (Figure 3(c)), were stained and histologically tested under microscopy. and the layer thickness is about 1.3 mm (Figure 3(d)). Finally, the biomechanical functions of the bulb tissue micro- The epidermal layer is fully cornified (the very hard and structures were simulated with the finite element method cornified layer in contact with the ground (together with (FEM), and the cushion mechanism of hoof bulb tissues nails)), and the relatively smooth and even cornified epider- was elaborated. mis grows in a cascaded way and contains cracks. The layers are arranged in parallel and the plys are connected tightly 2. Materials and Methods (the cornified epidermis layer in Figure 2(d) is superimposed from tissue structure sheets). No defects or holes were found 2.1. Ethical Declaration. This study was approved by the (Figure 2(d)). Review Board of Jilin University (Changchun, China). In total, 6 adult and healthy white goats without limita- 2.2.2. Histologic Examination. The stereo microscope showed tion to gender (20:0±0:5kg) were bought from a farmer that the hoof bulb tissues of white goats were divided from in the suburb area of Changchun. The goats were anesthe- down to top into the epidermal layer (①), dermal layer tized and killed via carotid bleeding. From 4 of the goats, (②), dermal papillae (④), and subcutaneous connective tis- the hoof capsules and flesh hoofs were collected. Then, bulb sues (③) (Figure 4(b)). The epidermal layer was fully kerati- tissues of 1 cm were cut off (Figure 1) and fixed in 4% para- nized (Figure 4(c)), which thickened the hoof bottom. This formaldehyde for 1 week. After that, the bulb tissues were structure helps to protect the hoof capsules and avoids put into a softening solution (75 mL of 60% ethanol and microbial invasion and, when abrasion from the environ- 25 mL of glycerol) for 1 month. The softened bulb tissues ment is intensified, can effectively minimize injuries to the were dehydrated in an ethanol gradient, then treated in a hoofs [23]. Abundant fat lobules were found in the bulb tis- dimethylbenzene solution until transparency, immersed in sues, and each lobule contained numerous fat cells and was wax, and embedded in an MNT cool-hot embedder (SLEE, surrounded mainly by loose connective tissues and contained Germany) into paraffin bulks. The bulks were cut by a abundant collagenous fibers, elastic fibers, and arteriovenous CUT5062 segment device (SLEE) into continuous tissue tallies (Figure 4(a)). slices (5 μm), which were then spread in a water bath at 40 2.3. Finite Element Method (FEM) Modeling and Simulation. C, sticked, and roasted in a roasting machine. After stain- ing with hematoxylin-eosin (HE), Weigert-VG, and Sacpic, An FEM model based on the hoof bulb tissue microstructure the slices were observed under a right-above fluorescence was built and used to study the biomechanical functions of microscope (Axio Imager A2, Zeiss). this composite structure. A composite microstructured Applied Bionics and Biomechanics 3 (a) (b) Figure 1: Hoof bulb tissues. (a) The location of the slices on the goat hoof and (b) the prepared goat hoof slices. (a) (b) (c) (d) Figure 2: SEM images of hoof bulb tissues. (a) Longitudinal sections of bulb tissues; (b) longitudinal sections of the dermal layer; (c) cross- sections of the dermal layer; (d) cross-section of the epidermal layer. bionic model was established with the 1/250 hoof bulb tissues all the layers of the bionic model was built and ground on the as the prototype. This bionic model consisted of three parts: FEM software ABAQUS. Through dynamic simulation and analysis on ABAQUS, the walking or running of white goats the cube with inner inclined fine tubes, the inclined cylinder, and the cube with one arc surface, which represented the der- was simulated as well as the process of hoof capsule bulbs mal layer (Figure 5(b)), dermal papillae (Figure 5(c)), and contacting the ground. The organism soft tissues are usually epidermal layer (Figure 5(d)), respectively. For the dermal manifested as nonuniform, anisotropic, pseudoincompressi- papilla model, the tube space was set as 160 μm, diameter ble, and nonlinear-plastic-viscoelastic materials [24]. To sim- was 80 mm, incline angle was 50 plify the complex models, researchers have idealized the foot , and layer thickness was 1.3 mm. A rectangular plate was connected to the top of the bottom tissues as homogeneous and isotropic linear elastic bionic model and was called the top plate (①) (Figure 5(a)), materials [25]. The material properties of different parts of which represents the goat body with mass and velocity. In the hoof bulb tissues as well as the elements of FEM division the simulating process, the top plate acts as the dynamic body [26–28] are shown in Table 1. The material properties of the normal model are shown in Table 2. The mesh size of FEM inducing crash to the model, simulating the actual crash com- ing from the goat body to goat hoofs. Another rectangular was set as 0.02 mm. plate was fixed at the lower part of the bionic model to simu- When the mass or sizes of the object differed, the object late the hard ground (②) (Figure 5(a)). A 3D model involving with a smaller mass to contact surface area ratio is less 4 Applied Bionics and Biomechanics (a) (b) (c) (d) Figure 3: The measurement of the tubes by SEM: (a) the tube spacing (b) the diameter (c) the inclined angle, and (d) the thickness. (a) (b) (c) Figure 4: Histological images of hoof bulbs: (a) subcutaneous connective tissues, (b) longitudinal sections of bulb tissues, and (c) epidermis layer. ①: epidermal layer; ②: dermal layer; ③: subcutaneous connective tissues; ④: dermal papillae. affected by impulsive stress, because when the object crashes to the top plate velocity becoming zero. M is the mass of the unto the ground under the same velocity conditions, the con- top plate, P represents the impulse of the model under the crash of the top plate. With the same initial velocity, usually, clusion above will be obtained by the following formula: we consider ðV − V Þ/t as the constant between the bionic 1 2 model and the normal model. The smaller the mass to con- ΔP = F ⋅ t = M ⋅ V − V , V =0, ð1Þ ðÞ 1 2 2 tact surface area ratio (M/S) is, the smaller the impulsive stress P is. The bionic model for simulation was a small part V − V F M V − V 1 2 1 2 ð2Þ F = M ⋅ , P = = ⋅ : of the real hoof bulb tissues, the mass of the top plate is much t S S t smaller compared to the actual goat body mass. According to In the formula, V represents the initial velocity exerted formula (2), when M is smaller, the stress is smaller so that on the top plate and t is the time from the beginning of crash the simulating comparing result is not obvious enough. To Applied Bionics and Biomechanics 5 (a) (b) (c) (d) (e) Figure 5: (a) Hoof bulb tissue assembly model, (b) dermal layer model, (c) dermal papilla model, (d) epidermal layer model, and (e) normal model. ①: top plate; ②: ground supporting plate. consisted of two layers, including the dermal layer and the Table 1: Material properties and element types of the FEM model. epidermal layer (Figure 5(e)). For both the bionic model Young’s and the normal model, the elastic modulus, Poisson’s ratio, Name Element modulus Poisson’s and density all differed among different layers, but these E (MPa) models were composed of homogeneous, isotropic, and lin- ear elastic materials. In the two models, the same initial Epidermal layer 3-D tetrahedrons 113.8 0.38 velocity and restraint were loaded and then the outputs Dermal layer 3-D tetrahedrons 7.0 0.45 were compared. Dermal papillae 3-D tetrahedrons 0.6 0.495 206 × 10 Top plate 3-D tetrahedrons 0.3 3. FEM Result and Analysis Ground supporting 3-D tetrahedrons 206 × 10 0.3 plate The process of the goat hoof bulbs contacting the ground was simulated on ABAQUS. As shown in Figure 6, in the simulat- ing process, the instantaneous initial velocity is exerted on Table 2: Material properties and types of the normal model. the top plate firstly. Then, the top plate transfers the energy to the simulating model. So the stress first occurs on the Young’s top plate. With the simulating process ongoing, the other Name Element modulus Poisson’s parts of the simulating model will have stress and stain corre- E (MPa) sponding to the impact from the top plate,. so that the top Epidermal layer 3-D tetrahedrons 113.8 0.38 plate’s stress will change constantly during the whole simula- Dermal layer 3-D tetrahedrons 7.0 0.45 tion (Figure 6). The bionic model and the normal model were separately fixed onto the supporting plates on the ground, Top plate 3-D tetrahedrons 206 × 10 0.3 and the top plates were assigned with the initial impact veloc- Ground supporting 3-D tetrahedrons 206 × 10 0.3 ity of 1-10 m/s, and the models outputted the impact force plate onto the supporting plates (ground reaction), displacement of the upper surface of the dermal layer, and the inner stress of the models (Figure 6). improve the simulation veracity to the actual situation, we set the initial velocity of the top plate in the FEM simulation 3.1. Ground Reaction. During the motion of a goat, the reac- tion when the hoof bulbs contact the ground is one of the as 1-10 m/s, which is larger than the velocity when the goat foot touched the ground; the actual crashing velocity of a important indices to measure the biomechanical perfor- goat is about 0.69 m/s-0.9 m/s according to our experiment mance of hoof bulb tissues. As shown on the reaction-time curves (Figure 7(a)), the reaction from the supporting plates high speed photography videos. This makes the simulating result more obvious. As shown in Figure 6, stress first occurs of the two models changed with time in a typical single peak mode, indicating the ground impact during the contact at the top plate, which indicates that the top plate is the moving plate. between the hoof bulbs, and the ground impact gradually intensified and then weakened. The ground contact time of To study the cushion mechanism of goat hoof bulbs, a the bionic model was longer than that of the normal model normal model was needed in addition to the bionic model. −5 −5 In the normal model, the dermal papillae and the dermal (3×10 vs. 2:5×10 s), and the ratio of the peak reaction layer were considered as one body, and thus, this model only of the bionic model to the normal model was 0.85 (0.072 6 Applied Bionics and Biomechanics Figure 6: The simulation process of the bionic model. 0.10 1.6 1.4 0.08 1.2 1.0 0.06 0.8 0.04 0.6 0.4 0.02 0.2 0.00 0.0 –6 –5 –5 –5 –5 –5 –5 5.0×10 1.0×10 1.5×10 2.0×10 2.5×10 3.0×10 3.5×10 0 2 4 6 8 10 Time (s) Velocity (m/s) Normal model Normal model Bionic model Bionic model (a) (b) 0.9 0.8 0.7 0.6 0.5 0.4 0.3 0.2 0.1 0.0 0 2 4 6 8 10 Velocity (m/s) Normal model Bionic model (c) Figure 7: (a) Ground reactions from the bionic model and the normal model when the top plates were loaded with the velocity of 1 m/s; (b) peak ground reactions from the two models under the loaded velocity of 1 to 10 m/s; (c) ratio of reaction peak of the bionic model to the normal model under the loaded velocity of 1 to 10 m/s. vs. 0.084 N). As the loading velocity on the top plates rose, the model to the normal model declined from 0.85 to 0.62, and peak reaction from the two models both linearly increased the changing rate decreased (Figure 7(c)). and the increasing rate was larger in the normal model (Figure 7(b)). As the loading velocity on the top plates rose 3.2. Displacement of the Upper Surface. The goat hoof bulb from 1 to 10 m/s, the ratio of peak reaction from the bionic hypodermic tissues are rich in fat tissues and elastic tissues, Ground reaction force (N) Rate of max ground reaction force Max ground reaction force (N) Applied Bionics and Biomechanics 7 0.040 0.08 0.035 0.07 0.030 0.06 0.025 0.05 0.020 0.04 0.015 0.03 0.010 0.02 0.005 0.01 0.000 0.00 0 24 6 810 0.00000 0.00001 0.00002 0.00003 Velocity (m/s) Time (s) Bionic model Bionic model Normal model Normal model (a) (b) Figure 8: (a) Displacement on the upper surface of the bionic model and the normal model at the loading velocity of 5 m/s; (b) peak displacement on the two models at different loading velocities. (Figure 9(a)). During the impact onto the ground, when which largely reduce the pressures upon contact with the ground and can scatter various external forces imposed on the ground reaction maximized, the stress on the epidermal the hoofs during the walking process. The deformation of layer from the down to the top first increased and then hoof bulbs is another key indicator of biomechanical perfor- decreased in both models (Figures 9(a)–9(c)). When the mances of hoof bulb tissues. During the FEM analysis, since loading velocity was 1 m/s, the stress-node curves of the the volumetric change rate of models can be hardly com- two models nearly overlapped, as the stress both increased puted, the displacement of the upper surface was used to from 1.5 to 2.755 and then slowly declined to 0.25 MPa, characterize the deformed amount of hoof bulb tissues. indicating that at low-velocity impact, the stress magnitude When the loading rate on the top plates was 5 m/s, the and distribution on the epidermal layer were identical maximum displacement on the upper surface of the bionic between the two models (Figure 9(b)). When the loading model and the normal model was 0.36 and 0.30 mm, respec- velocity was 10 m/s, the stress of the normal model rose tively, and the displacement-time curves were both typical of from 2.5 to 7.5 and then declined to 5.5 MPa, while that the single peak mode. At the early stage upon the impact in the bionic model first increased from 2.25 to 5.25 and −5 onto the supporting plates (5× 10 s), the displacements then slowly declined to 2.5 MPa, indicating the stress distri- butions on the epidermal layers were identical between the of the two models were nearly the same, but with the two models (Figure 9(c)). As the loading velocity rose, the prolonging of time, the difference of displacement between the two models gradually enlarged and finally stabilized at stresses at the lower parts were identical between the two models, but at the upper nodes, the stress differences 0.09 mm (Figure 8(a)). As the loading velocity on the top plates increased, the maximum displacements of both between models were enlarged (Figures 9(b) and 9(c)). As the loading velocity on the top plates rose from 1 to models increased and the difference between the two models 10 m/s, the ratio of peak epidermal stress from the bionic was unchanged. model to the normal model increased from 1.0 to 1.45 (Figure 9(d)). 3.3. Internal Stress Distribution in the Epidermal Layer Model. Since only the epidermal layers were completely the same in the two models, when the ground reaction during 3.4. Stress Distributions inside the Bionic Model. The goat the contact with the ground maximized, the stress magni- hoof bulb tissues consist of dermal papillae, the dermal layer, tudes and distributions on the central axis of the epidermal and the epidermal layer. The epidermal layer is fully cornified and mainly functions to thicken the hoof bottom. When the layers both differed between the two models. Along the cen- tral axis of the epidermal layer, 17 grid nodes were marked environmental abrasion is intensified, the epidermal layer from down to top to extract the stresses (Figure 9(a)). can effectively minimize the injuries to the hoofs. Dermal Clearly, when the ground reaction maximized, the papillae enlarge the connection area between the epidermis stress was concentrated on the epidermal layer, which and the derma, which contributes to the firm connection mainly occurred in the lower part of the epidermal layer between the two. Displacement (mm) Displacement (mm) 8 Applied Bionics and Biomechanics 3.0 2.5 S, Mises (avg: 75%) +7.302e+00 2.0 +6.703e+00 +6.104e+00 +5.505e+00 1.5 +4.906e+00 +4.307e+00 +3.708e+00 1.0 +3.109e+00 +2.510e+00 +1.912e+00 0.5 +1.313e+00 +7.139e+00 +1.150e–01 0.0 024 68 10 12 14 16 18 Number of nodes Normal model Bionic model (a) (b) 8 9 3 3 02 46 8 10 12 02468 10 12 14 16 18 Velocity (m/s) Number of nodes Normal model Normal model Bionic model Bionic model (c) (d) Figure 9: (a) Stress nephogram on the longitudinal section of the epidermal layer; stresses at different nodes when the loading speed onto the top plates was (b) 1 m/s or (c) 10 m/s; (d) peak internal stress on the epidermal layer in both models at different loading speeds. With FEM, the process of hoof bulbs impacting the 4. Discussion ground was simulated. The peak stress and stress nephograms of dermal papillae, the dermal layer, and the epidermal layer SEM and histological observation showed the goat hoof bulb at different impacting velocities were detected (Figure 10). tissues mainly consist of an epidermal layer, a dermal layer, When the ground reaction peaked, the internal stress and hypodermic connective tissues. The epidermal layer is distributions in the dermal papillae and the dermal layer fully cornified and is the hardest part of hoof bulb tissues of the bionic model were both uniform (Figures 10(a) and and mainly functions to thicken the hoof bottom and directly 10(b)). When the loading velocity on the top plates rose contacts with the ground. During motion, when the impact from 1 to 10 m/s, the peak stress increased from 0.038 to between the hoofs and the ground was aggravated and the 0.474 MPa in the dermal papillae, from 0.29 to 2.58 MPa environmental wear was intensified, the injuries to the hoofs at the dermal layer, and from 2.66 to 5.6 MPa at the epider- can be effectively decreased. The dermal layer is rich in fat tis- mal layer. As the loading velocity increased, the changing sues and elastic fibers, which largely reduce the pressures rate of the internal peak stress in the dermal papillae of upon contact with the ground and can scatter the various the bionic model was unchanged, that in the dermal layer external forces imposed onto the hoofs during the walking gradually increased, but that in the epidermal layer gradu- process and thus are critical in preventing damage to the ally declined. hoofs. Dermal papillae enlarge the connection area between Mises stress (MPa) Mises max stress (MPa) Mises stress (MPa) Applied Bionics and Biomechanics 9 U, magnitude +3.270e–02 +3.117e–02 +2.964e–02 +2.811e–02 +2.658e–02 +2.505e–02 +2.352e–02 +2.199e–02 +2.046e–02 +1.893e–02 +1.740e–02 1 +1.587e–02 +1.434e–02 02 4 68 10 Velocity (m/s) Epidermal layer Corium layer Dermal papillae (a) (b) (c) Figure 10: (a) Cross-sectional stress nephogram at the dermal layer of the bionic model; (b) longitudinal-section stress nephogram at the dermal layer of the bionic model; (c) peak internal stresses of dermal papillae, dermal layer, and epidermal layer at different loading velocities. the epidermis and the derma, which contributes to the firm related to the different living surroundings of goats and connection between the two. The dermal papillae are regu- horses: the horse usually runs on the prairie and the crash larly buried in the dermal layer at the inclining angle of 57 , condition to the hoof is the soil, whereas for the goat, the and the dermal papillae of hoof bulb tissues are much longer crash condition is usually the rock, which is harder than soil, and more regularly distributed than those in the skin. so that the goat may need more cushion capacity on their FEM showed the bionic model based on the dermal layer hoofs, and the goat hoofs having better cushion capacity than microstructures can well reduce the ground reaction, and this horse hoofs result from the differences in the tubules’ ability within a certain range was gradually strengthened inclined angle, density, and diameter. with the increment of loading velocity. This was because As the collision speed increased, the three layer structures the epidermal layer, the dermal layer, and dermal papillae of hoof bulb tissues showed different biomechanical charac- were different in structures and material properties and can teristics. As the speed rose, the impact onto the bulb tissues synergistically act to weaken the ground impact. During the was intensified accordingly, but the peak inner stresses of collision process, the epidermal layer experienced small the epidermal layer, dermal layer, and dermal papillae deformation and internal stress concentration and thus increased at different rates. The increasing rate of internal undertook a large portion of the impact. The dermal layer peak stress declined at the epidermal layer, rose at the dermal is very soft and can absorb the impulsive force by generating layer, and was unchanged in the dermal papillae. It indicated very large deformation. The dermal papillae regularly that the special microstructure layer can automatically adjust arranged at the inclination angle of 50 are very soft and the impact absorption ratios among different layers during can effectively reduce the transfer of impact from the epider- the different ground impacts. During low-speed collision, mal layer to the dermal layer and also disperse the impact in the hoof bulbs are affected by low ground impact; the epider- the dermal layer, which avoids the stress concentration and mal layer including the cuticle layer is thick and hard enough, thereby prevents the dermal layer from being destroyed. so it can suffer from the stress and protect the inner part of Based on the foot cushion property research on other animals the hoof from being damaged. So the epidermal layer under- like the cat’s paw, the impact to the ground is usually reduced takes the majority of the impact. As the collision speed by the material characteristics of fat [29, 30], whereas the increases, the collision and friction between the epidermal cushion mechanism of the goat hoof is determined by the layer and the ground are aggravated, which will further dam- composite structure and inclined holes, not only the mate- age the epidermal layer, so the epidermal layer suffers from a rials. This composite structure with holes can produce more smaller portion of the impact (as shown in Figure 10(c)) to obvious cushion capacity by the coupling methodology (mul- protect itself from being damaged. It indicates that when tilayer structure and hole structure). According to some the impact between the hoofs and the ground was aggra- researches about the horse hoofs, the tubules also exist at vated and the environmental wear was intensified, the inju- the inner hoof wall. The inclined angle of the tubules is differ- ries to the hoofs can be effectively decreased because of the ent between the left and the right foot, arranging from 86.47 lower damage of the epidermal layer. This special micro- to 104.85 ; the tubule spacing ranges from 0.36 to 0.53 mm; structure has excellent cushion ability to effectively reduce and the diameters are about 0.2 mm [31, 32]. The inclined the ground impact onto the trunk and prevents animals angle of the goat hoof inner wall is about 57 , which is smaller from being damaged by high-strength movement, such as than the horse. And the tubes of the goat hoof wall are sepa- running and jumping. rated at a distance of 0.14 mm-0.25 mm with 0.08-0.11 mm diameter; the separated distance and diameter are all smaller 4.1. Study Limitation. According to results of the FEM simu- than those of the horse. We consider that the difference is lation, the study emphasizes the cushion mechanism of the Mises max stress (MPa) 10 Applied Bionics and Biomechanics goat hoof bulb tissue structure and the model is established Acknowledgments with three structures with different material properties. The authors gratefully acknowledge the support of the But the material of each bionic structure is set as homoge- National Natural Science Foundation of China (Grant Nos. neous and isotropic linear elastic materials. The pressure 91748211, 51305157) and the project of the 13th Five-Year distribution may be different compared to the model with Common Technology (Grant No. 41412040101). nonuniform, anisotropic, pseudoincompressible, nonlinear- plastic-viscoelastic materials. The model in this study just dis- cusses the results of a homogeneous and isotropic linear elastic References material model. Further, we can research about the non- uniform, anisotropic, pseudoincompressible, and nonlinear- [1] Z. 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