June 2006

iomimetics, the art and science of transferring biological designs into the realm of human use, is far from a straightforward process. The path from theory to product tends to be so convoluted that only a handful of biomimetic products are commercially viable—Velcro sticks out as a rare success. One of the holy grails of biomimetics is artificial bone, which promises to be both useful and marketable. After all, baby boomers are rapidly losing, breaking,

	Nacre, the tough material of most shells, is made up of layers of calcium carbonate interleaved with layers of organic glue. Photomicrograph © Silvain Deville

and wearing down their natural supply; the demand for replacement bone within their generation alone is high enough that biomimeticists would turn nature inside out to find a solution.

It so happens that nacre, the brick and mortar of most mollusk shells, can take quite a beating, which is why such otherwise defenseless, soft-bodied creatures go to the trouble of making the stuff. Nacre is mainly made of a ceramic, a hard nonmetallic mineral—calcium carbonate in this case. What’s intriguing is that unlike your favorite coffee mug or run-of-the-mill grail, nacre is a ceramic that is unusually tough. Typically the smallest crack in a ceramic object races through the brittle structure to cause a full-blown failure. You may have noticed how seldom you find a mug or a plate that’s nearly, but not completely, broken.

But nacre is not a simple or homogeneous piece of clay. Rather, like my favorite pastry, the napoleon, nacre is made of thin sheets of ceramic interleaved with even thinner sheets of organic glue. Although one ceramic sheet is easy to fracture, the crack stops when it hits the gluey interface, and more energy must be spent to start the crack in the next layer [see photomicrograph right]. Incidentally, those thin sheets are about the same thickness as wavelengths of visible light, which explains why the insides of abalone shells—made of nacre—reflect a rainbow of colors.

As it happens, your skeleton, too, is made up largely of a ceramic: hydroxyapatite. When it’s healthy, it doesn’t shatter nearly as easily as a cup or a bowl either. That is because an organized network of collagen fibers toughens the bone, and a lattice of little struts forms a spongy, energy-dissipating framework for most of your bones. If nacre could be sculpted into the shape of patellas or pelvises, the material might be just what the doctor ordered. Nacre is more similar to bone, and would likely make a better match, than titanium or stainless steel, when a new joint is needed for an aging hip or a demolished elbow.

Unfortunately, although the structure and remarkable properties of nacre have been known for thirty years, the simplicity of the material is deceptive. So far no one has been able to make synthetic nacre. Most attempts have focused on alternating a layer of ceramic with a wash of glue, and repeating that ad nauseum. The process ends up with a nacrelike material, but the thickness of the ceramic layers is hard to control, and it takes thousands of cycles to produce a slab of appreciable heft. More important, the interface between glue and ceramic—so critical in stopping cracks from propagating through a natural shell—has proved extremely hard to copy from nature. Ceramic bone implants currently on the market apparently wear well, but they are more brittle than healthy bone.

Another approach now seems much more promising. Antoni P. Tomsia, a materials scientist at the Lawrence Berkeley National Laboratory in California, and his team have taken advantage of the properties of freezing water to make a finely layered composite that’s amazingly tough. Two such properties, seemingly irrelevant to making bone, led to the new technique for fabricating nacre. First, seawater doesn’t freeze uniformly: pure water crystals segregate themselves from salt and other suspended impurities. Second, the growth of this pure ice can be controlled to produce broad, flat crystals; the crystals naturally organize themselves in such a way that distinct layers of pure water-ice crystals and layers of salt or other particles are formed. The result looks a lot like nacre but on a much larger scale. Tomsia’s team discovered that by increasing the rate at which water freezes, they could make the layering progressively finer.

To make synthetic bone, the team adds granules of hydroxyapatite to the water, then freezes the mixture at a very low temperature. The result is a finely layered composite of ice and mineral. Now they can remove the water by freeze-drying the composite, which leaves a complex, layered structure of hydroxyapatite. The structure has rough surfaces, as does natural nacre. Some hydroxyapatite granules that span the spaces left behind by the sublimated ice add support, and a quick blast of heat—not unlike the firing of clay in a kiln—further strengthens the lattice. Finally, an epoxy is added to the dried block of hydroxyapatite in a vacuum; the epoxy infiltrates the spaces between the plates where the ice used to be and mimics the organic glue layer of nacre [see diagrams and photomicrograph below].

Artificial nacre can be made by freezing a slurry of water and ceramic particles, which forces the particles into distinct layers between growing, self-organizing ice crystals (schematic diagram, a). The pure ice crystals are freeze-dried, leaving vertical voids between pillars of ceramic (b). Glue is then forced into the voids and allowed to harden (c). The final product, shown in this photomicrograph (d), approaches natural nacre in strength and toughness, but the layers of the natural substance are substantially thinner. Photomicrograph © Silvain Deville

One advantage of Tomsia’s system is that the final product closely matches the shape of the freezing container. That makes it possible to mold the blocks according to the bone that must be replaced. Furthermore, since varying the freezing rate can change the thickness of the layers, composites can be formed that have, say, a core that is more dense than its shell. Unfortunately, a practical method of making this material in bulk and molding it to exact specifications has yet to be tested. Tomsia’s group is also working to achieve even thinner layers in their faux nacre.

Nature offers an infinite variety of biological designs, free for the taking. But exploiting nature’s solutions to structural problems requires a team with disparate talents and a large dose of patience. Bone continues to pose a challenge to bioengineers and biomechanists. As Tomsia’s method and other competing products take the stage, I wish them all the time-honored words of good luck: “Break a leg.” And if someday the phrase turns from theatrical encouragement into literal description, I might find myself very grateful to be patched up with the architectural stuff of seashells.

Adam Summers (asummers@uci.edu) is an assistant professor of bioengineering and of ecology and evolutionary biology at the University of California, Irvine.

Copyright © Natural History Magazine, Inc., 2006