In natural organic-inorganic composites like bone and nacre, stiff but very brittle mineral crystals are joined by soft but ductile organic materials.17,42 These materials combine both high mechanical strength and toughness at the same time. In this respect, a well-studied system is nacre, which consists of 95% aragonitic CaCO3 polymorph, but is 3000 times more fracture-resistant than pure aragonite.17 Nature applies different structural concepts to achieve stiff and tough materials. These concepts are similar for all biomaterials and are described in this chapter by using bone and nacre as examples.
Many biomaterials contain stiff nanoparticles, such as hydroxyapatite mineral particles in bone, which exhibit a thickness of 2-4 nm.24 The nanometer size of the particles ensures
The soft organic matrix in which the stiff particles are embedded plays a crucial role for the toughness of biomaterials. The molecular mechanistic origin of the toughness is based on the reversible opening of sacrificial bonds upon exerting deformation forces.38,44 The organic fibers elongate under mechanical stress due to a stepwise unfolding of folded domains or opening of loops. The energy stored in the respective fiber is dissipated as heat. This mechanism can occur until all folded domains or loops are pulled open via stretching of hidden lengths of the macromolecules. Further application of forces leads to a breaking of the fibers. Upon stress release before the organic molecules break, the folded domains or loops can reversibly re-form.38 Other sacrificial bonds that contribute to the materials toughness include – using bone as an example – calcium-mediated bonds. The bonds reveal hidden length upon opening and can, for example, be formed between several macromolecules or between macromolecules and mineral particles.44
The aforementioned structural aspects revealed that the major part of the load is carried by the stiff particles, giving rise to the stiffness of the biocomposites, whereas most of the deformation occurs by shearing of the organic matrix in which the particles are embedded.30 A staggered arrangement of anisotropic particles within the organic matrix, as found for example in bone, ensures an optimum combination of mechanical stiffness and toughness, as
9 proposed by Fratzl et al.,43,45,46 provided that a tight binding between organic and inorganic components exists.30
A tight interface between the stiff particles and the soft matrix involving special interface polymers was highlighted as a structural key characteristic by Fratzl et al.30 The load can only be transferred between the particles if the organic matrix acts as amphiphilic glue and the organic molecules remain fixed to the particles under stress (Figure 1.7).
Figure 1.7: Arrangement of mineral particles (dark gray) in organic phase (light gray). The horizontal white lines indicate shearing forces occurring in the organic phase between the stiff particles. In absence of shear, the white lines are horizontal (a), whereas their orientation changes upon applying deformation forces (b). Tensile stress can only be transmitted through the organic matrix when assuming a tight interface between organic and inorganic components.24,30
Breaking the connection between organic and inorganic components will cause a fast drop of the mechanical performance of the materials.30 Amphiphilic polymers, capable of both binding to the inorganic components and forming an organic phase between the stiff particles, are consequently a target for the fabrication of biomimetic composites.
Figure 1.7 also illustrates that the material becomes stiffer the more elongated the particles are.24,45 This phenomenon is attributable to the decreasing distance between the particle layers upon shearing and the resulting increase in aspect ratio, assuming a tight binding, and consequently, a constant contact length between the particles and the organic phase.
The sophisticated hierarchical structuring of biomaterials has an important influence on their outstanding mechanical performance,47 ensuring high flaw tolerance from the nanoscale up to the macroscopic scale.48 Typically, the ability of the microstructure of a material to dissipate deformation energy without crack propagation determines the toughness of the material.49 Hierarchically structured biomaterials are able to prevent crack propagation by applying different mechanisms either via dissipation of energy or shielding of the crack-tip.49,50 Several
10 micro-scale toughening mechanisms were identified in bone (Figure 1.8). As known for polymers, bone is able to dissipate deformation energy without crack propagation via viscoplastic flow or via microcracking, which is the formation of non-connected microcracks.
Crack ligament bridging and crack deflection, which are known to be toughening mechanisms in ceramics, were also observed in bone.49-51 The most important mechanisms for the macroscopic fracture toughness are expected to be crack ligament bridging and crack deflection, which act in bone on the length scale of several micrometers up to several hundreds of micrometers.50
Figure 1.8: Toughening mechanisms in bone: viscoplastic flow (a), microcracking (b), crack bridging (c), and crack deflection (d). The shaded areas indicate the stressed domains close to the crack tip.51
Crack bridging was reported to occur by uncracked ligaments, e.g. in bone by unbroken individual collagen fibers, bridging the gap between both sides of the crack (Figure 1.9a).49,52 Figure 1.9b shows a crack in bone, which is deflected by individual lamellae that surround the central canal in the fundamental functional unit of cortical bone (osteon). The rotating direction of collagen fibrils within the lamellar structure (inset of Figure 1.9b) is of vital importance for the crack deflection mechanism.49,51
Figure 1.9: (a) SEM image of crack bridging in human cortical bone by collagen fibers.52 (b) SEM graph of a crack in an osteon, which is deflected by bone lamellae, forming a zigzag path. The horizontal red lines indicate successive lamellae. The inset illustrates the rotating orientation of collagen fibers within lamellaes.49,51
11 Like for bone, the unique combination of mechanical stiffness and toughness of nacre arises due to contributions of several structural features, including the internal structure of the aragonite platelets,53,54 and their staggered arrangement within the polymer matrix,45,46 as well as interface properties,55-59 such as mineral bridges (see Chapter 1.4.2).58,60 This type of arrangement also renders the whole structure flexible by increasing the deformability of the organic matrix.30