Mechanical basis of bone strength: influence of bone material, bone structure and muscle action

Abstract

This review summarises current understanding of how bone is sculpted through adaptive processes, designed to meet the mechanical challenges it faces in everyday life and athletic pursuits, serving as an update for clinicians, researchers and physical therapists. Bone's ability to resist fracture under the large muscle and locomotory forces it experiences during movement and in falls or collisions is dependent on its established mechanical properties, determined by bone's complex and multidimensional material and structural organisation. At all levels, bone is highly adaptive to habitual loading, regulating its structure according to components of its loading regime and mechanical environment, inclusive of strain magnitude, rate, frequency, distribution and deformation mode. Indeed, the greatest forces habitually applied to bone arise from muscular contractions, and the past two decades have seen substantial advances in our understanding of how these forces shape bone throughout life. Herein, we also highlight the limitations of in vivo methods to assess and understand bone collagen, and bone mineral at the material or tissue level. The inability to easily measure or closely regulate applied strain in humans is identified, limiting the translation of animal studies to human populations, and our exploration of how components of mechanical loading regimes influence mechanoadaptation.

Figure 1

Stress-strain, force-deformation curve demonstrating elastic and plastic regions, and ultimate strength (adapted from[95,99-101]).

Figure 2

Stress-strain characteristics of macroscopic tissue (adapted from[95,118]). Cortical bone is stiffer with a high resistance to stress and low resistance to strain [2% yield]. Trabecular bone is porous with a low resistance to stress and high resistance to strain [50% yield].

Figure 3

Mechanostat Theory: Modeling and remodeling effects on bone strength and mass. DW= disuse window; AW= adapted window; MOW = mild overload window; POW= pathologic overload window; MES= minimum effective strain (r= remodeling, m= modeling, p= microdamage), Fx= fracture strain (adapted from[69,127,131]).

Figure 4

Osteogenic relationship between strain magnitude and strain frequency: Low magnitude, low frequency activities and high magnitude, high frequency activities may lead to maladaptation due to insufficient (resorptive) or excessive (stress reaction) stimuli.

Figure 5

The relationship between daily loading cycles (magnitude, rate and frequency) and subsequent bone adaptation (reprinted with permission from[71]). Bone is maintained (red line), formed (superior portion) or resorbed (inferior portion) using a variety of different strain environments.

Figure 6

Bone mass of rats (•) and turkeys (Δ). Anabolic effect of mechanical loading saturates as the number of loading cycle’s increases, with limited benefit above ~40 cycles per day (reprinted with permission from[153]).

Figure 7

Bone formation (rBFR/BS) of rat tibia after applying loads in 4 bouts of 90-cycles every second day, with various rest provided between bouts; ~4 to 8 hours appears optimal (reprinted with permission from[164]).

Figure 8

A schematic representation of various loading modes applied to bone in isolation.

Figure 9

Deterioration of thickness, connectivity and porosity for trabecular (A and B) and cortical (C and D) bone (adapted from[260,261]).

Figure 10

Definitions of mineral density at the material, compartment and whole-bone levels (reprinted with permission from[280]). Mineralisation and porosity differ between trabecular (A and B) and cortical (C and D) regions. Mass is equal (grey areas); however volume differs (areas encased by black lines).

Figure 11

Cross-sectional moment of inertia (CSMI) of a long bone (adapted from[298]); where CSMI increases as the cortex widens (R₁= inner radius; R₂= outer radius), spreading mass (cortical wall thickness) further from the neutral axis.

Figure 12

The effect of changes in cortex diameter on bone strength under compression and bending without any change in areal density (adapted from[22]); a limitation of aBMD when assessing the mechanical competence of bone.

Figure 13

Variations in bone size and shape between age-matched, recreational (left) and elite (right) male athletes illustrating variations in cortical thickness, shape and alignment.

Figure 14

Fatigue curve (adapted from[95]): The relationship between load, repetition and injury onset (left), with cortical bone and trabecular bone stress-strain properties super-imposed (right). A positive shift in the fatigue-curve demonstrates the benefit of increasing bone strength; a more resilient bone able to handle more stress prior to strain.

Figure 15

A pathophysiological overview of overuse and fatigue fractures (adapted from[416,417]).