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It’s tough to be strong: Advances in bioinspired structural ceramic-based materials orientation, alignment, and uniformity of the layered microstructures in bone and nacre (Figure 2). Engineering bioinspired materials The natural world provides many examples of cellular structures: trabecular bone, plant stems (e.g., wood), cuttlefish bones, corals, sponges, sea urchin spines, horseshoe crab exoskeletons, feathers, porcupine quills, and bird beak interiors. An interconnected network of struts and plates form the faces of the cell walls in cellular solids. The cells tend to align for maximum mechanical efficiency. Therefore, many cellular solids develop anisotropically as they respond to load orientations. For example, the compressive strength of a trabecular femur head is much higher in the direction of maximum load than in the transverse directions.18 Research shows that the elastic modulus and strength of an open cell porous material are strong functions of density.18 Cellular solids are of interest in the biomedical field as scaffolds for bony (osseointegration) or cellular ingrowth. Therefore, mechanical integrity is important. Emulating the intricate organization of the molecular, nano-, micro-, and macrostructures found in nature may be the key to developing higher performance synthetic materials. Using advanced synthetic materials, such as alumina, zirconia, polymethylmethacrylate (PMMA), and epoxy, rather than nature's relatively weak constituents, such as hydroxyapatite, aragonite (CaCO3), collagen, and chitin, it becomes possible to engineer bioinspired materials with hybrid, hierarchical architectures that outperform their biological counterparts. For example, according to the rule of mixtures, the global mechanical properties (X) of a hybrid composite material depend on the properties (Xi) and fractions (qi) of the individual parts (i): X=-qi Xi. However, most biological materials do not follow the rule of mixtures and exhibit higher than expected mechanical properties.19 For instance, two common modes of failure in plateletreinforced composites are platelet fracture (brittle failure) and platelet pullout (ductile failure).20 Both bone and nacre have optimized interfacial adhesion between the stiff inorganic platelets and ductile organic matrix, such that ductile failure occurs just before brittle failure. This adaptation, combined with structural hierarchy, provides bone and nacre extremely high flaw tolerance and fracture toughness20,21—better than most synthetic materials. Bioinspired ceramic-based materials Drawing inspiration from hard biological materials, many research groups in the past decade have engineered extremely strong, stiff, and tough ceramic-based materials by various nature-inspired processes to produce thin films, porous scaffolds, or bulk composites. Table 1 compares the properties of bone and nacre with selected bioinspired materials, which were selected because they mimic, or draw inspiration from, one or more of the nanostructural or microstructural features that provide bone and nacre their extraordinary mechanical properties. Thin films Inspired by nacre, thin film bottomup fabrication techniques exploit chemical, physical, electrical, or mechanical forces to drive assembly of synthetic building blocks. Methods include layerby layer self-assembly, enzyme- and peptide-mediated synthesis, biomineralization, centrifugation, evaporation or vacuum filtration, solution casting, chemical bath or electrophoretic deposition, ion beam sputtering, and morphosynthesis. Most of these syntheses occur near room temperature and in an aqueous environment. Organic constituents control and regulate size, morphology, orientation, texture, and organization of mineral crystals in biological systems. Langmuir–Blodgett films, reverse micelles, liquid crystals, and self-assembled monolayers (SAMs) have mimicked successfully chemistries of biological proteins that promote nucleation of inorganic crystals. The SAM approach has been most effective for nucleating crystals with controlled orientation and polymorph. SAM molecules have the general formula RSiX3, where R is an organic functional group and X is typically an alkoxide or halide. One end of the SAM molecule attaches to the substrate and the other functional end promotes nucleation of inorganic crystals. Tailoring the functional group allows for deposition of continuous or pattered ceramic thin films.22 Crystalline single-metal oxides can be deposited at temperatures <100°C, making this an attractive method for further development. However, crystalline multiconstituent metal oxides are difficult to produce using this method. Enzymes catalyze chemical reactions such as hydrolysis, reduction–oxidation, and elimination of specific functional groups in living matter. They also can be used for site selective oxide, hydroxide, carbonate, and phosphate deposition at low temperatures. For example, the enzyme silicatein-α promotes biosynthesis of SiO2 in sponges and diatoms and can be isolated and cloned from glass sponges. It also can catalyze nucleation of ceramic films, particles, and nanowires of TiO2, ZrO2, SnO2, and CaTiO3.23 Peptides, proteins, polyamides, and amino acids—acting as a catalyst or template to control the morphology, polymorph, and orientation—induce nucleation of TiO2. Catalyzed hydrolysis of phosphate esters by alkaline phosphatase produces patterned thin films of hydroxyapatite on collagen substrates.24 The above methods produce a thin layer, prompting researchers to pursue other methods to attempt to duplicate the layered microstructure to macrostructure of bone and nacre films. A significant early attempt to develop nacre-like films deposited sequential layers of montmorillonite (MTM) clay platelets and poly(diallydimethylammonium chloride) polyelectrolytes using a surfactantmediated self-assembly approach.25 The films had ultimate tensile strengths up to 109 MPa and Young's moduli up to 13 GPa, similar to the properties of nacre and cortical bone, respectively. A similar layer-by-layer approach fabricated MTM/poly(vinyl alcohol) nanocomposites closely resembling nacre’s brick-and-mortar microstructure and formed optically transparent multilayer composites with an unsurpassed stiffness 20 www.ceramics.org | American Ceramic Society Bulletin, Vol. 93, No. 5


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