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nacre with several other natural materials. 5 The plot shows these materials are surprisingly tough, considering their low density, high strength, and stiffness. These properties result from a hybrid, hierarchical design built by self-assembly from the molecular level up, resulting in anisotropic, hierarchical architectures. Bone is about 65 wt% hydroxyapatite (Ca10(PO4)6(OH)2) embedded in an organic matrix of type I collagen. Two main forms exist: cortical (or compact) and cancellous (or trabecular). At the microstructural level, osteons compose cortical bone and consist of dense (5–10 percent porosity), concentrically oriented lamellar sheets surrounding small vascular channels and lacuna spaces ~10–50 μm in diameter. Lamellar sheets, 3–7 μm thick, have a “twisted plywood” architecture with fibers oriented at various angles.6 Each fiber is composed of several mineralized collagen fibrils ~150 nm in diameter and 5–10 μm long. Each fibril consists of tropocollagen proteins and periodically spaced hydroxyapatite minerals with a characteristic periodicity of 67 nm. Figure 2(a) shows how the microstructure of cortical bone consists of layers (or lamellae) of aligned fibers that are oriented in successive rotations of ~30°.7–9 Cancellous bone, on the other hand, has a cellular structure (75–85 percent porosity) of trabecular struts surrounding large pores 100–500 μm wide. Although morphologically similar to cortical bone at the submicrometer level, cancellous bone contains flat lamellar sheets, rather than cylindrical osteons. Mechanical loading mediates the growth of both bone types (i.e., bone grows in response to stress), which yields varying mechanical properties depending on location, age, sex, and physiology. Compared with bone, nacre exhibits superior mechanical properties, primarily because it lacks porosity. Nacre is ~95 wt% crystalline aragonite (CaCO3) platelets embedded in an organic matrix of chitin and proteins.10 The inorganicplatelets and organic-matrix structure resembles a “brick-and-mortar” structure, with stacked aragonite “bricks” ~0.5 μm thick by 8–10 μm wide “mortared” by organic layers 20–50 nm thick (Figure 2(b)).10 Mineral bridges 25–55 nm in diameter connect the platelets.11 This organization of successive layers is a consequence of the nucleation and growth of aragonite crystals, leading to the formation of tiles aligned about the c-axis.12 The platelets have a characteristic surface roughness caused by asperities ~50 nm wide and 30 nm high.13 However, the platelets are not discrete tiles dispersed in Modulus (GPa) Toughness (kJ/m2) Figure 1. Ashby plot comparing toughness and modulus. Bone and nacre are tough materials despite their low density.5 a continuous organic matrix. Similar to bone, the organic and inorganic constituents are continuous, interpenetrating phases that grow concurrently. 12 Additional growth bands of organic layers ~20 μm thick, corresponding to periods of growth interruption, separate mesolayers ~300 μm wide.12 Several mechanisms across various length scales contribute to the excellent strength and toughness of bone and nacre. In cortical bone, extrinsic toughening occurs behind the crack tip at length scales >1 μm,4,14 including crack deflection and twisting around osteons, uncracked-ligament bridging, collagen-fibril bridging, and constrained microcracking. Intrinsic toughening mechanisms in bone occur ahead of the crack tip at length scales <1 μm4,14 and include hidden length sacrificial bonding, microcracking, fibrillar sliding, and molecular uncoiling. In nacre, the brick-and-mortar structure deflects crack propagation, leading to failure via delamination, tile pullout, or tile fracture.15,16 As stress accumulates, the organic matrix dissipates energy, acting as a tough, viscoelastic glue.13,17 The mineral bridges resist intertile shearing (tile pullout) and tensile failure (tile fracture), acting as reinforcing struts to give nacre its strength and stiffness. The surface asperities prevent excessive sliding between adjacent platelets, further protecting nacre from fracture by delamination or tile pullout.13,17 Other toughening mechanisms in nacre include platelet interlocks (waviness) as well as rotation, sliding, and organic bridging between nanograins.15,16 On a more fundamental level, the microstructural anisotropy found in cortical bone and nacre provides these materials their high mechanical properties (Table 1). The high, yet anisotropic, compressive strengths relate directly to the American Ceramic Society Bulletin, Vol. 93, No. 5 | www.ceramics.org 19 Credit: Porter; UCSD Figure 2. Compressive strengths reflect microstructural anisotropies. (a) Cortical bone has a “twisted plywood” lamellar microstructure. (b) Abalone nacre microstructure follows a “brick-and-mortar” morphology.8,9 Credit: Porter; UCSD


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