Courtesy of Dr. Ulrich Muller, Linz, Austria
Courtesy of Dr. Ulrich Muller, Linz, Austria

In my previous article, I asked the question “Why are your bones not made of steel?” This was a way to think about the types of structural materials that are found in biological organisms, and to contrast them with those which we have developed for load-bearing purposes in engineering components and structures. I pointed out that natural materials such as bone have mechanical properties which are much inferior to those of engineering materials such as steel or carbon-fibre composites.

In this article I'd like to take the argument a bit further, and ask “How can Nature get away with using such weak materials?” It turns out that Nature has a few tricks up her sleeve, which allow her to make the best of the materials available to her. To put it another way, suppose you were able to make a piece of bone which was identical in composition and microstructure to a natural bone. At the present time we can't do that, because bone has a complex structure involving a series of hierarchical scales from the nano scale upwards: it's just too difficult to manufacture. We can make composites using the same basic building blocks – the crystalline ceramic hydroxyapatite and the natural polymer collagen – but so far the materials which we've made by mixing these together have had very poor mechanical properties. Bu t nanotechnology is advancing all the time and it's certainly conceivable that, at some point in the future, we will be able to perfectly reproduce the material that is bone. Well, the bad news is that even when we can do that, we won't be able to use it to replace bone in the human body. A bone made in this way would fail within a week of normal use.

The reason for this discrepancy is that Nature uses some strategies, some little tricks, which we cannot, and which allow biological materials to be used at higher applied stresses. I'm going to talk about four of these tricks, and in each case I have attempted to quantify the effect which they have in terms of raising the allowable operating stress.

The first of these tricks is pain. How convenient it would be if your car could tell you, “I'm feeling a bit of a twinge in my front suspension arm on the left hand side.” Then off you would go to garage and they would find a fatigue crack. Pain is not pleasant, but it is an excellent way of alerting you to the presence of damage before that damage reaches a critical level. A “stress fracture” is the term doctors give to the sharp pain experienced in a bone after doing too much exercise. It's common in athletes, dancers and racehorses. But, despite the name, it's not a fracture, and that's the point. The pain occurs as a result of a small crack, a few millimetres in length. In all but the very dedicated (and perhaps pharmacologically assisted) sportsman or woman, the amount of pain is so great that you are forced to stop using the limb concerned, giving the bone time to heal up. The engineering equivalent of this is inspection and maintenance, by which we can detect fatigue cracks, wear and other types of damage. The big difference is that we can only inspect periodically – once a year for example – but in biological materials the inspection is happening continuously. This allows Nature to live dangerously, safe in the knowledge that any gradually accumulating damage will be detected before it leads to complete failure.

The second trick is continuous repair. Again this is something rather similar to what we do in engineering structures – we detect sub-critical damage and deal with it – but Nature obtains a great advantage by doing the process continually, rather than periodically. In bone this happens when the damage is about an order of magnitude smaller than that needed to cause the pain signal. Cracks a few hundred microns in length are forming and growing continually as a result of normal daily activities. These cracks are detected and repaired: the repair process takes a week or so and involves special groups of cells, some of which remove regions of damaged bone by dissolving them away, whilst others make new bone to fill the gap. We can observe this process experimentally but what we don't know is how these microscopic cracks are detected in the first place. It's one of the topics which we are researching in my group at the moment. It seems certain that the detecting is being done by cells called osteocytes which live inside the bone, connected together in a continuous network. Other tissues in the body which are capable of repair, such as muscles and tendons, also contain living cells. Tissues which have no resident population of cells, such as tooth enamel, are not self repairing, which is why your dentist keeps busy. Cartilage is an interesting case; it does contain some cells, but not many, and its ability to repair itself is poor; this is a major factor in the development of arthritis, which is essentially the wearing away and deterioration of cartilage.

The above two tricks are available to Nature, but not to us, because biological structures are alive. Or, to be more precise, they contain living cells which create, monitor and regulate the load-bearing materials around them. The other two tricks which I want to talk about are different; they don't rely on the presence of living cells, but they are, nevertheless, tricks which we can't copy.

Trick number three can be stated like this: Nature plans for a high rate of failure in her creations. Something like nine out of every ten birds that are born never live to adulthood. Success in evolutionary terms means the survival of the species, not the individual, so the best strategy for species survival – the best rate of transmission of DNA to the next generation – may involve a considerable amount of wastage at the individual level. For example, it makes sense to have bones which are relatively thin and light, requiring less energy and material for their manufacture, and reducing the energy needed to move the limbs around, even if this means that fractures will occur from time to time. Not all fractures are fatal, but a monkey with a broken leg doesn't do so well in the daily struggle for survival. But then neither would a monkey who had bones that were thicker and heavier than the next monkey. Nature strikes a balance, and the result is a rather high failure rate. Measurements of primates in the wild for example, have shown that each individual bone has a 1–3% probability of failing some time during the individual's life. Contrast this with a failure probability of 10-6, which is typically used in designing engineering structures. Human beings are risk averse; we want to live in houses that will almost never fall down, thank you very much. The business of estimating failure probability, and designing accordingly, is very complex, but the simple fact is that to reduce the failure probability we have to widen the gap between the operating stress and the material's strength, which means using materials in a less than optimal way.

The fourth and final trick is rather more subtle but, I think, just as important as the other three. It relates to a material's internal structure. Almost all biological materials contain fibres, and as anyone who has worked with fibre composites knows, the orientation of the fibres is the crucial factor as regards mechanical performance. We have become very good at making composites with a wide range of mechanical properties, but we normally do it by arranging the fibres in two dimensions, in flat laminated sheets or helically-wound tubes. Nature goes one better: she can arrange fibres in three dimensions. Combine this with the ability to vary the material's composition and fibre orientation from place to place within a single component and you have a versatile design system such as we can only dream about for engineering structures. Consider for example the cartilage on your knee joint. Only a few millimetres thick, its fibre orientation changes through ninety degrees from the surface (where fibres resist shear loadings) to the interior (where they support the cartilage against compression). Where cartilage meets bone the mineral content gradually increases to avoid an abrupt interface.

A particularly good example of 3D fibre arrangements in action is the joint made where the branch of a tree meets the trunk. In both trunk and branch the wood fibres are highly oriented to provide maximum stiffness and strength along their respective axes. Wood is very anisotropic, being up to ten times stronger in the direction parallel to the fibres, compared to the perpendicular direction. To avoid creating a weak point, the fibres of branch and trunk curve around where the two meet. Something very similar happens at the point where a tendon is attached to a bone. The mineral crystals in the bone change their orientation near the attachment to line up with the muscle forces flowing in through the tendon; fibres from the tendon run through into the bone and become gradually mineralised at the transition. This is all very clever stuff, and we certainly can't replicate this kind of structure with current manufacturing methods, at least not at any reasonable cost. The reason Nature can to do it with apparent ease is because biological structures are built from the bottom up, by assembling molecules one by one, grouping them together into fibres, and so on, up to the macroscopic scale. Fibres from the tree branch flow into the body of the trunk because both branch and trunk have grown by gradual addition of material around their circumferences. Bone is made by first laying down the collagen fibres, which are later hardened by mineral precipitation. There is evidence to show that, even in embryo, the shape and structure of each bone is influenced by the presence of stresses created by muscle action.

How much are these tricks worth? I have tried to estimate the increase in allowable operating stress which results in each case, taking the example of bone. In doing this I've been able to draw on previous work from our lab, and experimental data from many other sources. Much of our understanding of this material has only emerged in the last ten or twenty years, and it's still very incomplete, but at least we have some pretty good estimates of its strength, toughness and, crucially, its high-cycle fatigue properties. Whilst we still don't really understand how it monitors and repairs damage, we can observe and quantify the phenomena involved.

The beneficial effect of pain can be estimated by calculating the time it takes for a millimetre-sized crack to grow to cause a complete fracture; if this time is shorter than a typical engineering inspection period (say one year) then the stress would have to be reduced if we didn't have pain to help us. To consider failure rates we can use a Weibull analysis to describe the scatter in material properties and thus estimate the probability of failure as a function of operating stress. A similar analysis, combined with an estimate of the time for the repair process (and its scatter) allows one to estimate failure times with and without repair. It's more difficult to quantify the effect of 3D fibre arrangement: an upper bound would be the ratio between the material's strength in the best and worst loading directions, e.g. longitudinal and transverse in bone. Combining these various effects creates more errors and so the final result should be treated with circumspection. My answer, for the increase in operating stress which these four effects allow, is a factor of 17, which is pretty enormous.

One can then go on to estimate how much thicker a bone would have to be if it did not have these tricks to fall back on. Given that a typical bone sees a mixture of bending and compression forces, the result is that the cross section (and therefore the weight) would need to increase by about a factor of 10. That's what I meant earlier in this article when I said that, even if we could make the material which is bone, we still wouldn't be able to use it. Without these little tricks of nature, our bodies would effectively become impossible. The science of Biomimetics is based on the idea that we can learn from Nature. This is true, but what the above analysis shows is that we can't simply copy Nature's materials and structures, because some of what Nature does can't be imitated. We should let ourselves be inspired by Nature, but remember that we humans do things differently.

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DOI: 10.1016/S1369-7021(10)70067-5