Peter Zioupos

Changes in the stiffness, strength, and toughness of human cortical bone with age.

Aging adversely affects the elastic and ultimate properties of human cortical bone as seen in uniaxial tests in quasi static loading, high strain rate impact or fatigue. Little is known about the full effects of aging on toughness and its relationship with strength. In the present article the elastic modulus (E), strength (sigma f), fracture toughness (KC and J-integral), and work of fracture (Wf) were determined in specimens of male human femoral bone aged between 35-92 years. In this way we investigated whether fracture of bone in three situations, allowing various amounts of damage prior to fracture, can provide a better insight into the fracture process and also the relative importance of these experimental methods for assessing the soundness of bone material. We found a steady and significant decrease with age for all these mechanical measures. E fell by 2.3%, from its value of 15.2 GPa at 35 years of age, per decade of later life; sigma f fell similarly from 170 MPa by 3.7%; KC from 6.4 MPa m1/2 by 4.1%; J-integral from 1.2 kJ m-2 by 3%, and the Wf from 3.4 kJ m-2 by 8.7%. In aging bone there was a deterioration in the elastic properties of the material. This reduced the (elastically calculated) critical stress intensity level (KC) required to initiate a macrocrack, or the nonlinear energy associated with the onset of fracture (J). The macrocrack was preceded by less damage, and once created needed less energy to drive through the tissue (Wf).

The role of collagen in the declining mechanical properties of aging human cortical bone.

The importance of the mechanical role of collagen in bone is becoming increasingly more clear as evidence mounts on the detrimental effects of altered collagen on the mechanical properties of bone. We previously examined a set of mechanical properties (material stiffness, strength, and toughness) of human femoral bone (ages 35-92) and found that a gradual deterioration in these properties occurs with age. The present study examines the collagen of the same specimens and relates the collagen properties to the mechanical ones. In the collagen we measured the concentration of stable mature crosslinks, the shrinkage temperature, and the rate of contraction during isometric heating. The changes in the concentration of mature (pyridinium and deoxypyridinium) crosslinks showed no clear relationship to age nor did they correlate with the mechanical properties. The shrinkage temperature declined with age and correlated with a bones toughness. The maximum rate of contraction was strongly correlated with three different measures of tissue toughness, but much less to stiffness and strength. Our results reinforce speculation regarding the toughening role of collagen in bone mechanics and suggest that the fragility of aging bone may be related to collagen changes.

The extent of microcracking and the morphology of microcracks in damaged bone

Strain-induced damage in bovine laminar bone has been examined using laser scanning confocal microscopy (LSCM). The specimens were loaded in a fluorescein solution, which penetrated the newly formed cracks in the specimen. The microcracking, and the larger cracking, induced by strain were very clearly visible. The microcracking occurred diffusely in regions of high strain (stress), but was particularly obvious in the vicinity of large machined stressconcentrators. The microcracking could be shown not to be artefactual, that is, it was produced by strain, and not by specimen preparation. The microcracking interacted with the structure of the bone, often having a wavy appearance related to the histology. Microcracks seemed to be particularly associated with the most highly mineralized parts of the bone. LSCM is a technique holding great promise for the investigation of the initiation and development of damage in mineralized hard tissues, and other translucent materials.

Variations in the Individual Thick Lamellar Properties Within Osteons by Nanoindentation

The nanoindentation method was used to examine variations in the individual thick lamellar properties within completed secondary osteons as a function of distance from the osteonal center (haversian canal). In general, there is a decline in both elastic modulus and hardness from the center of the osteon outward. Because some of the osteons may have a different general trend than others, an analysis of covariance was also carried out. The overall analysis was highly significant for both elastic modulus and hardness. Also, osteon number was significant as a factor, indicating that there was some difference in the overall thick lamellar properties of the different osteons. An unpaired t-test showed statistically significant differences (p = 0.0005 and 0.0004, respectively) between thick lamellar properties obtained from most of the inner two osteonal lamellae (E = 20.8 +/- 1.3 GPa and H = 0.65 +/- 0.06 GPa) and those from outermost two osteonal lamellae (E = 18.8 +/- 1.0 GPa and H = 0.55 +/- 0.05 GPa). In general, lamellar properties from near to the center of the osteon were greater than those from the outermost osteonal lamella. The mechanical properties of osteons are also significantly lower than those of the interstitial bone (p < 0.0001). The ratio (E1/E2) of the elastic moduli of the outermost osteonal lamella (E1) (considered to be the soft part of the osteons) and that of interstitial bone (E2) was approximately 0.7. These results may have important implications for the mechanical contribution of individual osteons to bone biomechanics.

Accumulation of in-vivo fatigue microdamage and its relation to biomechanical properties in ageing human cortical bone.

Bone matrix accumulates microdamage in the form of microcracks as a result of everyday cyclic loading activities. In two very recent studies, which used conventional histological stains and light microscopy techniques, the amount of this in‐vivo microdamage in the cortices of long bones has been shown to increase with age. These articles have suggested that in‐vivo microcracks may have an effect on the material properties of the tissue. However, a precise quantitative relationship between the number of microcracks and the mechanical properties of these same bones has not been produced before, and in particular the way the microcracks may affect the stiffness, the strength or possibly the toughness of the tissue. This article presents an examination of the in‐vivo microdamage in human bones by the use of laser scanning confocal microscopy, which offers better discrimination and allows examination of the cracks in‐situ. Quantification of in‐vivo fatigue microcracks was performed by counting the microcrack numerical density and surface density in specimens for which we have previously derived a full set of mechanical properties as a function of age. It is shown that bone microdamage relates more to the toughness (measured by three different measures) of ageing bone tissue than to its stiffness and strength. The result allows us (i) to re‐evaluate the fragility of ageing human bone and put more emphasis on its energy‐related resistance to fracture than perhaps on its stiffness or strength and also (ii) to understand more fully the causal relationship and interactions between microcracks and tissue toughness.

Ageing Human Bone: Factors Affecting its Biomechanical Properties and the Role of Collagen

The incidence of fractures increases with age. This is partly due to extraosseous factors and partly to the increased fragility of the bone material itself. Ageing adversely affects the “quality” of human bone material, its elastic and ultimate properties. The hypothesis here is that these effects are caused by factors such as architectural changes, compositional changes, physicochemical changes, changes at the micromechanical level, and the degree of prior in vivo microdamage. Examination of the extent of the secondary osteonal area, the porosity level, the calcium content, the mineral/wet weight fraction, the dry density, the condition of the collagen and its content in mature x-links, the elasticity of osteonal and interstitial lamellae at the microscopic level and the numericaland surface-density of the in vivo fatigue microcracks has been undertaken. The findings show that some factors simply affect the stiffness and the strength of bone, while others soley affect its toughness. We discuss the implications of these findings in the context of the composite nature of the ageing bone material matrix.

Effect of formaldehyde fixation on some mechanical properties of bovine bone.

The risk of infection of investigators working on the biomechanics of human bone from a variety of modern pathogens including the human immunodeficiency virus or the hepatitis B virus has increased recently. New safety procedures are needed to reduce that risk. The procedure we follow in our laboratory employs brief (< 3 h) fixation in formaldehyde, and we report here the effects it has on some mechanical properties of bovine bone. Results in quasistatic loading tests were almost unaffected by our fixation protocol, but a significant decrease in impact strength was found. These results indicate that there may be some interaction between fixation and strain rate dependent effects and, therefore, some caution is needed when using common biomechanical measurement methods on fixed bone material.

The Effect of Strain Rate on the Mechanical Properties of Human Cortical Bone

Bone mechanical properties are typically evaluated at relatively low strain rates. However, the strain rate related to traumatic failure is likely to be orders of magnitude higher and this higher strain rate is likely to affect the mechanical properties. Previous work reporting on the effect of strain rate on the mechanical properties of bone predominantly used nonhuman bone. In the work reported here, the effect of strain rate on the tensile and compressive properties of human bone was investigated. Human femoral cortical bone was tested longitudinally at strain rates ranging between 0.14-29.1 s(-1) in compression and 0.08-17 s(-1) in tension. Youngs modulus generally increased, across this strain rate range, for both tension and compression. Strength and strain (at maximum load) increased slightly in compression and decreased (for strain rates beyond 1 s(-1)) in tension. Stress and strain at yield decreased (for strain rates beyond 1 s(-1)) for both tension and compression. In general, there seemed to be a relatively simple linear relationship between yield properties and strain rate, but the relationships between postyield properties and strain rate were more complicated and indicated that strain rate has a stronger effect on postyield deformation than on initiation of yielding. The behavior seen in compression is broadly in agreement with past literature, while the behavior observed in tension may be explained by a ductile to brittle transition of bone at moderate to high strain rates.

The accumulation of fatigue microdamage in human cortical bone of two different ages in vitro

OBJECTIVE To analyse the development of damage during fatigue cycling of human bone. DESIGN Changes in compliance and the cycles to failure were monitored in cortical bone samples subjected to oscillating stress in vitro. BACKGROUND Previous studies produced mainly the relationship between the applied stress and the final cycles to failure (sigma-N(f)plots). However, cyclic stressing increases the compliance of the bone continuously, and causes a progressive mechanical/structural degradation. Recording this accumulation of damage allows one to know how close bone is to the point of failure; more importantly, it allows a more comprehensive modelling of fatigue processes in cortical bone. METHODS The occurrence of material damage was continuously monitored during the tests. The 20 specimens came from two female subjects, 27 and 56 years old. The range of the cyclic stresses was 58-130 MPa. RESULTS The damage was quantified with a graphical and an empirical/numerical method, and we have also microscopically observed the generation of internal microcracks. The range of cycles to failure was from 1 to 210,000. CONCLUSIONS It was observed that (i) the older tissue showed a lower fatigue strength than the younger one, (ii) both tissues sustained similar damage levels prior to failure, and (iii) they both showed a continuous accumulation of damage during the tests, the course of which depended on the level of stress.

Mechanical properties of nacre and highly mineralized bone

We compared the mechanical properties of ‘ordinary’ bovine bone, the highly mineralized bone of the rostrum of the whale Mesoplodon densirostris, and mother of pearl (nacre) of the pearl oyster Pinctada margaritifera. The rostrum and the nacre are similar in having very little organic material. However, the rostral bone is much weaker and more brittle than nacre, which in these properties is close to ordinary bone. The ability of nacre to outperform rostral bone is the result of its extremely well–ordered microstructure, with organic material forming a nearly continuous jacket round all the tiny aragonite plates, a design well adapted to produce toughness. In contrast, in the rostrum the organic material, mainly collagen, is poorly organized and discontinuous, allowing the mineral to join up to form, in effect, a brittle stony material.