Biomimetic Materials by Freeze Casting
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Natural materials, such as bone and abalone nacre, exhibit exceptional mechanical properties, a product of their intricate microstructural organization. Freeze casting is a relatively simple, inexpensive, and adaptable materials processing method to form porous ceramic scaffolds with controllable microstructural features. After infiltration of a second polymeric phase, hybrid ceramic-polymer composites can be fabricated that closely resemble the architecture and mechanical performance of natural bone and nacre. Inspired by the narwhal tusk, magnetic fields applied during freeze casting can be used to further control architectural alignment, resulting in freeze-cast materials with enhanced mechanical properties.
Biomimetic materials are synthetic materials that mimic one or more aspects of the design, function, or properties of natural biological materials.1, 2, 3 Many structural biological materials, such as bone and abalone nacre, have evolved exceptional mechanical properties in spite of the relatively weak material constituents that make up their composition.1, 2, 3 Interestingly, their mechanical properties are highly anisotropic, an adaptation to the nature and magnitude of external tractions.1, 2, 3 These properties are a product of their complex structural organization and architectural hierarchy from the nanoscale to macroscale.1, 2, 3
A variety of materials processing methods, ranging from self-assembly4, 5, 6 and layer-by-layer deposition7,8 to nanolithography9,10 and 3-D printing,11, 12, 13 has been explored to develop synthetic biomimetic materials. Freeze casting is a relatively simple, inexpensive, and adaptable technique to fabricate bulk porous scaffolds and hybrid composites. Deville,14 Gutierrez et al.,15 Qian and Zhang,16 and Li et al.17 provide excellent reviews of general freeze casting topics, including the processing principles, materials, structures, properties, and applications. This article focuses on freeze casting as it relates to different biomimetic materials and processing modifications inspired by nature.
To fabricate hybrid composites, polymers or metals may be infiltrated into the porous ceramic scaffolds.19, 20, 21, 22 Figure 1e shows a schematic of this process. A variety of different polymer infiltration techniques includes polymer melt immersion,23 polymer–solvent evaporation,24, 25, 26, 27, 28 in situ polymerization,19, 20, 21,29, 30, 31, 32 particle centrifugation,33 and chemical vapor deposition.34, 35, 36In situ polymerization is the most popular method used to impregnate porous scaffolds with polymers. In this method, a liquid monomer and catalyst are forced into the pores of a ceramic scaffold under vacuum and subsequently polymerized. Figure 1f–g show micrographs of a porous zirconia scaffold (Fig. 1f) and a hybrid zirconia-epoxy composite (Fig. 1g) synthesized in this manner. Interpenetrating, bi-continuous composites, such as those shown in Fig. 1g, are generally stronger and tougher than composites composed of a polymer matrix containing randomly dispersed ceramic particles.20
There are a variety of potential applications for porous ceramics and hybrid composites fabricated by freeze casting. Biomimetic materials, such as structural composites19, 20, 21, 22,29, 30, 31,37,38 that may be useful as high-performance components in industries ranging from aerospace to automotive manufacturing and potential bone replacements12,13,19,31,39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56, 57, 58, 59 are most encouraging and are the primary focus of this article. Other potential applications for freeze-cast materials with complex shapes and designer microstructures include separation filters, insulators, sensors, electrodes, catalyst supports, fuel cells, and piezoelectric devices.14, 15, 16, 17
Other slurry properties, such as pH, viscosity, eutectic temperature, osmotic pressure, and surface tension, influence the behavior of the freezing vehicle.58,59,61,68,70, 71, 72, 73, 74, 75, 76 Changing these properties is generally accomplished by adding various liquid modifiers. Rheological properties, such as pH and viscosity, show strong correlations to the resulting microstructure and mechanical properties of freeze-cast scaffolds.58 Fu et al.43 and Munch et al.71 used additives, such as dioxane (Fig. 2e), glycerol (Fig. 2f), sucrose, sodium chloride, citric water, or ethanol, to modify the microstructures (e.g., lamellar or cellular), surface roughness (e.g., faceted or dendritic), and interlamellar bridging of freeze-cast scaffolds by changing the eutectic phase diagram of the colloidal suspensions. Our group (UCSD) (unpublished work) is investigating the effects of isopropanol, which results in elongated lamellar pores with periodic surface roughness and thick mineral bridging (Fig. 2g). Pekor et al.72,73 demonstrated that soluble polymers commonly used as plasticizers, such as polyethylene glycol and polyvinyl alcohol, have a significant effect on the degree of constitutional supercooling, which affects pore size and secondary dendrite spacing. Deville et al.77 used zirconium acetate, a salt with unique ice-structuring properties, to limit the incorporation of water molecules into growing ice crystals, resulting in faceted polyhedral structures (Fig. 2h). Several research groups have demonstrated that sacrificial pore-formers, such as polymer beads, sponges or salts, added to the slurry before freezing and removed after lyophilization by heating or dissolving with appropriate solvents create complex pore architectures with varied morphologies (Fig. 2i).56,78, 79, 80, 81, 82
Modifying the freeze conditions is another alternative to control the microstructures of freeze-cast scaffolds. Munch et al.71 showed that patterning the freezing surface can manipulate the long-range ordering of ice lamellae by controlling the initial direction of nucleation. Deville et al.67 and Waschkies et al.83 used double-sided cooling to more precisely control the temperature gradient. Moon et al.,84 Macchetta et al.,49 and Koh et al.85 demonstrated the concept of radial cooling to construct porous ceramics with radial channel alignment (Fig. 2j). Jung et al.44 used sequential solid loading to create titanium scaffolds with a gradient in porosity and pore sizes. Koh et al.86 fabricated dense/porous bilayered ceramics with camphene, by freezing the bottom surface, while exposing the top surface of the slurry to air for controlled solvent evaporation. Zhang et al.87 fabricated dense/porous bilayered ceramics by applying an electric field during freezing (Fig. 2k). Porter et al.88 applied a magnetic field perpendicular to the ice growth direction in a uniaxial freezing device to align lamellar microstructures in two directions: parallel to the freezing direction and the magnetic flux path (Fig. 2l).
Mimicking Bone and Nacre
Bone is composed of ~67 wt.% hydroxyapatite (HA) minerals embedded in an organic matrix of type I collagen.91 It exists in two main forms: cortical (or compact) bone and cancellous (or spongy) bone.91 At the microstructural level, cortical bone is composed of osteons (Fig. 3a), which consist of dense (5–10% porosity) concentrically oriented lamellar sheets that surround small vascular channels and lacuna spaces ~10–50 μm in diameter.31,92 Cancellous bone (Fig. 3b), on the other hand, is highly porous (75–85% porosity) and consists of trabecular struts that surround large pores ~100–500 μm in diameter.31,93 Figure 3c shows an artificial scaffold fabricated by freeze casting on a concentrically patterned surface that reflects the natural architecture of an osteon.19 Figure 3d shows an artificial scaffold fabricated by a modified method that combines freeze gel casting and the polymer sponge technique, mimicking the trabecular architecture of cancellous bone.56
Nacre is composed of ~95 wt.% aragonite platelets (or tiles) embedded in an organic matrix of chitin.94 Commonly described as a “brick-and-mortar” structure, the aragonite platelets are “bricks” that are self-assembled and “glued” together by the chitin biopolymer matrix.95 By freeze casting thin alumina platelets, Hunger et al.96 showed that shear flow induced by ice growth aligns platelets with their long dimension parallel to the freezing direction. This resulted in scaffolds with nacre-like microstructures having a higher toughness, yield strength, and Young’s modulus than similar scaffolds composed of spherical particles.96 Excluding the organic matrix, nacre primarily relies on two intrinsic toughening mechanisms: mineral bridges (Fig. 3e) and surface asperities (Fig. 3f).95,97,98 Figure 3g shows a magnified micrograph of a single mineral bridge connecting two adjacent lamellae formed during the sintering stage after freeze casting.20 Figure 3h shows surface roughness asperities fabricated by freeze casting with the addition of sucrose.20 As previously mentioned (refer to Fig. 2), the density and thickness of mineral bridges as well as the surface roughness of lamellar walls can be tailored by changing the slurry properties and freezing conditions.
The organic matrix is, perhaps, the most important toughening mechanism in bone and nacre. For instance, the tensile strength in nacre (perpendicular to the layered structure) is ~4.2 MPa, compared to that of deproteinized nacre having a strength of ~0.33 MPa.99 Even though the organic matrix accounts for only 5 vol.% of nacre, when it is removed the strength of nacre is reduced by ~92%.99 Similarly, the compressive strength and stiffness of cortical bone (as reported for mature bovine femur bone in the longitudinal direction) decreases from ~120 MPa and ~22 GPa, respectively, to ~24 MPa and ~9 GPa when the organic matrix is removed by deproteinization.92 Therefore, it is no wonder several research groups focus on freeze casting and subsequent polymer infiltration to fabricate hybrid inorganic–organic composites.19, 20, 21, 22,29, 30, 31,37,38
Magnetic Freeze Casting
Under a static magnetic field, TiO2-Fe3O4 scaffolds showed homogeneous microstructural organization with enhanced strength and stiffness in directions parallel to the magnetic flux path.88 As seen in Fig. 6d, the strength and stiffness more than doubled (in the magnetic field direction) with the addition of a static magnetic field (Fig. 6e) over identical samples fabricated with no magnetic field (Fig. 6f). The enhanced mechanical properties arise from the directional alignment of pore channels induced by the magnetic field.88 Potential applications for magnetic field aligned freeze casting include: spiral-reinforced structures with exceptional torsional rigidity, structural alignment of high aspect ratio nanoparticles to create “nanobridges” between adjacent lamellae for increased strength and toughness, or local two-dimensional and three-dimensional reinforced structures, such as those described by Erb et al.102
Natural structural materials, such as bone and nacre, are excellent examples of how microstructure and architectural organization across multiple length scales influence mechanical properties. Mimicking the various strengthening and toughening mechanisms observed in nature led to the development of novel lightweight, high-performance materials. Freeze casting is a popular method to fabricate biomimetic materials that emulate the microstructural features of natural biological materials. Intricate microstructural control of porous scaffolds and hybrid composites is possible by altering the slurry properties and freeze conditions during the freeze casting process. Bioinspired applications for freeze casting include hybrid inorganic–organic composites for structural components that mimic nacre, porous ceramic scaffolds for bone replacements that mimic bone, and magnetic field aligned freeze casting for multidirectional alignment inspired by the narwhal tusk.
We are particularly thankful to Dr. A.P. Tomsia for sharing with us the technology for freeze casting at the Lawrence Berkeley National Laboratory. Professor E.A. Olevsky and Dr. Y.-S. Lin conducted systematic experiments at San Diego State University that were helpful in our understanding of the freeze casting process. Dr. E. Novitskaya and Ms. M.I. Lopez contributed their knowledge of the material properties of bone and nacre. Support by the National Science Foundation, Division of Materials Research, Ceramics and Biomaterials Program, 1006931, is gratefully acknowledged.
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