Bone is generally considered a biomimetic model. Indeed, among bio logical materials, bone is a promising candidate. It is a lightweight structural material, which provides support to a wide class of animal bodies. It has a great com- bination of mechanical properties, which make it very attractive for research studies. In particular, bone has a remarkable fracture toughness, which far exceeds that of its basic constituents (i.e. collagen and HAP). Its fracture behavior and its significant toughness make bone an interesting material not only from a medical point of view but also from an engineering one, since it can be used as a model for the design of new tough composite materials.
Bone can be considered, as a first approximation, a ceramic–polymer composite consisting of collagenous matrix, reinforced with mineral platelets, mainly composed of calcium and phosphorus in the form of HAP crystals. Collagen and HAP are considered the basic building blocks of bone: HAP, the brittle and stiff part, providing stiffness and strength and mainly responsible for carrying out the load, and collagen fibers, con- ferring flexibility to bone, and the possibility of dissipating energy under large mechanical deformation. Bone has a complex hierarchical struc- ture, with various organization levels, spanning from the atomistic to the
macroscale. At each level, it is possible to distinguish a specific structure, with characteristic features and dimensions, optimized to meet specific functions. Thanks to this hierarchical system, the resulting properties of bone are far superior to those of the individual building blocks. Figure 5.2 gives an overview of bone multiscale structure, from nano- to macroscale.
At subnanoscale, we recognize the basic building blocks, collagen, and HAP, which form, during the mineralization process, the mineralized col- lagen fibrils (MCFs). Such fibrils show a staggered configuration, with some gap regions, which are filled by HAP crystals during bone formation [70–73]. In Figure 5.3, a schematic representation of bone building blocks and their staggered arrangement is given.
These MCFs are highly conserved building blocks of bone, univer- sally present in all bony tissues [74–77]. At nano- to micro-scale, they are assembled into fibrils arrays, held together by a protein phase, conferring additional dissipative functions, with different fibril array patterns, similar to composite laminates. At microscale, the fibril arrays form the lamellae (between 3 and 7 μm thick), which are arranged to build cylindrical fea- tures (with a diameter up to 200–300 μm and a length of 1–2 cm), called
Figure 5.2 Multiscale structure of bone: (a) bone structure at macroscale, where it is possible to distinguish the cortical or hard tissue from the trabecular or spongy one.
(b) Microstructure of cortical bone, also known as Haversian structure, where it is possible to recognize the characteristic cylindrical feature (i.e. osteon). (c) Circumferential lamellae. (d) Collagen fiber bundles. (e) Collagen mineralized fibrils. (f) Single
tropocollagen molecule surrounded by HAP nanocrystals. The picture shown in (b) was taken by means of an optical microscope, pictures represented in (c–e) were taken by means of an SEM after an FIB cutting, and figure (f) is from atomistic simulations of collagen–HAP system. Reprinted with permission from [17].
10 mm 100 m 1 m 800 nm 500 nm 1 nm
(a) (b) (c) (d) (e) (f)
Figure 5.3 Schematic representation of bone building blocks, collagen fibrils, and HAP, placed into a staggered configuration.
Hydroxyapatite
Collagen
osteons. The latter are representative of the Haversian system, a charac- teristic microstructure of cortical bone. Osteons are made of concentric lamellae and an internal vascular canal (~50–90 μm in diameter) and interspersed into a matrix made of other lamellae, called interstitial lamel- lae. The outer boundaries of osteons are then surrounded by the so-called
“cement lines”, about 1–5 μm thick, which result from the remodeling pro- cess. At a larger scale, bone structure is not as highly conserved as at the nanostructural level, but starts to differentiate, in trabecular (also known as spongy or cancellous) and cortical (or compact) bone. The two bone types show different structures (i.e. higher porosity in spongy bone), and con- sequently different mechanical properties, being intended to perform dif- ferent functions in the body. Cortical bone can also show a woven-fibered structure. In this case, it is known as woven cortical bone and is the only type of bony tissue that can be formed ex novo. Haversian bone, instead, also known as secondary bone, originates from the remodeling process, so it cannot be formed ex novo. Woven bone is often found in young grow- ing skeletons, or in adult skeletons in cases of trauma or disease, forming around bone fracture sites. It is essentially an SOS response by the body to place a mechanically stiff structure within a needy area in a relatively short period of time. For these reasons, it is the most disorganized type of bone tissue, without an osteon structural organization, nor a lamellar one [78].
In the presented case studies, the research focus is on the microstruc- tural level, where the main toughening mechanisms occur [23–25, 79, 80].
For all the case studies, we borrow inspiration from bone, and in particu- lar cortical bone, for the design of novel composites. Indeed, the purpose of these studies is not to investigate the entire hierarchical structure of bone from the atomic level and up, but focusing on the Haversian struc- ture and on the microstructural toughening mechanisms, such as crack deflection. The latter is favored by the osteons, characteristic microstruc- tural features, and results in a major increase in the overall bone frac- ture toughness [80]. Osteons are secondary structures, resulting from the stress-induced remodeling process. They have a cylindrical shape, con- sisting of circumferential lamellae to build a circular-to-elliptical cross section, and are interspersed into an interstitial matrix made of lamellae with an apparently random distribution. Their geometry and their prop- erties, different from the matrix (i.e. the osteon–matrix stiffness ratio is about 0.64) [81], induce stress delocalization, reducing the local stresses at the crack tip, and causing crack shielding. Moreover, additional energy dissipation is given by the presence of microcracks, in all bone tissue and in particular, in the osteon outer boundaries, called cement lines [80]. The Haversian structure, which have a crucial role in determining the overall
fracture toughness of the bone tissue, is a secondary structure, which originates from the remodeling process and represents a body response and adaptation to local needs and functions (load bearing capability and self-healing) [82]. This structure is representative of many animals—in particular animals subjected to stresses coming from gravity force (e.g.
human, equine, ovine, and bovine species)—and the osteon density and distribution is correlated to the stress distribution [82]. Indeed, other species, not subjected to stresses coming from the gravity force, such as fishes, are instead characterized by a more lamellar organization [83].
Besides the role of microstructural features in enhancing fracture tough- ness, additional energy dissipation contributing to increase toughness arises from the bone heterogeneity, which confers bone different proper- ties than a uniform material [84]. The heterogeneity is typical of biologi- cal materials and may be reproduced in biologically inspired composites thanks to innovative multi-material technology.