Bone-inspired microarchitectures achieve enhanced fatigue life

Abstract

Microarchitectured materials achieve superior mechanical properties through geometry rather than composition. Although ultralightweight microarchitectured materials can have high stiffness and strength, application to durable devices will require sufficient service life under cyclic loading. Naturally occurring materials provide useful models for high-performance materials. Here, we show that in cancellous bone, a naturally occurring lightweight microarchitectured material, resistance to fatigue failure is sensitive to a microarchitectural trait that has negligible effects on stiffness and strength-the proportion of material oriented transverse to applied loads. Using models generated with additive manufacturing, we show that small increases in the thickness of elements oriented transverse to loading can increase fatigue life by 10 to 100 times, far exceeding what is expected from the associated change in density. Transversely oriented struts enhance resistance to fatigue by acting as sacrificial elements. We show that this mechanism is also present in synthetic microlattice structures, where fatigue life can be altered by 5 to 9 times with only negligible changes in density and stiffness. The effects of microstructure on fatigue life in cancellous bone and lattice structures are described empirically by normalizing stress in traditional stress vs. life (S-N) curves by √ψ, where ψ is the proportion of material oriented transverse to load. The mechanical performance of cancellous bone and microarchitectured materials is enhanced by aligning structural elements with expected loading; our findings demonstrate that this strategy comes at the cost of reduced fatigue life, with consequences to the use of microarchitectured materials in durable devices and to human health in the context of osteoporosis.

Keywords: additive manufacturing; bone; microarchitecture; microarchitectured materials; osteoporosis.

Fig. 1.

Microarchitecture influences fatigue damage accumulation in cancellous bone. (A) The creep fatigue curve of cancellous bone is shown with the three phases of fatigue loading indicated. Cyclic compressive loading of cancellous bone was stopped at different points along the creep fatigue curve (data points) to determine patterns of damage accumulation (fatigue life was estimated as in ref. 21). (Inset) Cyclic loading waveform is shown. The 3D images of cancellous bone with (B) green indicating damage, (C) plate-like and rod-like struts, and (D) strut orientation relative to anatomical position (longitudinal, oblique, and transverse). (E) The amount of damage in cancellous bone (damage volume fraction, DV/BV) was correlated with maximum applied strain, but specimens with thicker rod-like trabeculae experienced less damage accumulation (R² = 0.76, P < 0.01). Error bars indicate the SDs as determined from the linear mixed effects model. (F) Early in fatigue life, strut failure occurs primarily in transversely oriented rod-like struts; final mechanical failure is characterized by widespread failure of longitudinally oriented plate-like struts.

Fig. 2.

Models of cancellous bone generated using additive manufacturing show that fatigue life is sensitive to small changes in microarchitecture. (A) Digital images of human vertebral cancellous bone were edited and printed into (B) high-resolution 3D models. Increases in the thickness rod-like struts had small effects on (C) density and (D) stiffness (Young’s modulus in first cycle of loading) yet resulted in (E) increases in fatigue life by as much as 2 orders of magnitude. (Lines connect samples derived from the same bone specimen; 2 magnitudes of normalized cyclic stress are shown. Scatter is a result of variations in microstructure among the 5 bone samples.) (F) A microcomputed tomography image of a 3D-printed sample of cancellous bone after fatigue loading to failure. A radioopaque dye penetrant indicated regions of accumulated damage. (Inset) Magnified view. (G) The amount of damage (damage volume fraction, DV/BV) generated by fatigue loading to failure was reduced in 3D-printed specimens with greater thickness of rod-like struts.

Fig. 3.

Transverse volume influences fatigue life in repeating cellular solids. (A) Images of the bone-inspired microstructure and an octet truss are shown. (Scale bar: 5 mm.) (B) The fatigue life of microarchitectured materials printed as designed or with rod-like struts thickened (colored) is shown. Thickening transverse struts increases fatigue life, while thickening vertically oriented struts reduces fatigue life (specific stiffness, E₀/ρ is also shown). (C) Fatigue life of the lattice structures is related to the inelastic dissipation energy per unit work determined from finite element models. (D) Fatigue life for 3D-printed specimens at different applied cyclic loading (σ/E₀, noted in microstrains) is shown with lines indicating regression model fits (Eq. 2) (R² = 0.82). Symbols indicate bone (●), bone-like microstructure (▲), and octets (♦).