Interfacial Strength of Cement Lines in Human Cortical Bone

In human cortical bone, cement lines (or reversal lines) separate osteons from the interstitial bone tissue, which consists of remnants of primary lamellar bone or fragments of remodeled osteons. There have been experimental evidences of the cement line involvement in the failure process of bone such as fatigue and damage. However, there are almost no experimental data on interfacial properties of cement lines in human cortical bone. The objective of this study is to design and assemble a precision and computer controlled osteon pushout microtesting system, and to experimentally determine the interfacial strength of cement lines in human cortical bone by performing osteon pushout tests. Thirty specimens were prepared from humeral diaphyses of four human subjects. Twenty specimens were tested under the condition of a small hole in the supporting plate, in which the cement line debonding occurred. The cement line interfacial strength ranged from 5.38 MPa to 10.85 MPa with an average of 7.31±1.73 MPa. On the other hand, ten specimens were tested under the condition of a large hole in the supporting plate, in which the shear failure inside osteons was observed. The specimens tested under the condition of the large hole resulted in an average shear strength of 73.71±15.06 MPa, ranging from 45.97 MPa to 93.74 MPa. Therefore, our results suggest that the cement line interface between osteon and interstitial bone tissue is weaker than that between bone tissue lamellae.     

Micromechanics fracture in osteonal cortical bone: a study of the interactions between microcrack propagation, microstructure and the material properties

A two-dimensional micromechanical fibre reinforced composite materials model for osteonal cortical bone is presented. The interstitial bone is modelled as a matrix, the osteons are modelled as fibres, and the cement line is presented as interface tissue. The interaction between osteons and microcracks is evaluated by linear elastic fracture mechanics theory, followed by a determination of the stress intensity factor at the vicinity of the microcrack tips. The results indicate that bone microstructural heterogeneity greatly influences fracture parameters. Furthermore, microstructural morphology and loading conditions affect growth trajectories, the microcrack propagation trajectory deviates from the osteon under tensile loading, and osteon penetration is observed under compressive loads.     

Micromechanics modeling of Haversian cortical bone properties.

A finite-element micromechanics model for Haversian cortical bone tissue has been developed and studied. The model is an extension of two-dimensional micromechanics techniques for fiber-reinforced composite materials. Haversian systems, or secondary osteons, are considered to be the fiber component, and interstitial lamellar bone the matrix material. The cement line is included as an 'interphase' component along the fiber/matrix interface. The model assumes a regular repeatable spacing of the longitudinally aligned continuous fibers and is, therefore, restricted to approximating Haversian cortical bone in its present form. Haversian porosity is modeled explicitly by incorporating a hollow fiber to represent the Haversian canal. Solutions have been obtained by applying uniform macroscopic stresses to the boundaries of the repeating unit cell model. Macroscopic mechanical property predictions correspond reasonably well with the experimental data for cortical bone, but are necessarily dependent on the input properties for each constituent, which are not well established. The predicted variation in the elastic modulus with porosity is not as sensitive as that observed experimentally. Stresses within the constituents can also be modeled with this method and are demonstrated to deviate from the macroscopic applied stress levels.     

Crack propagation in cortical bone is affected by the characteristics of the cement line: a parameter study using an XFEM interface damage model

Bulk properties of cortical bone have been well characterized experimentally, and potent toughening mechanisms, e.g., crack deflections, have been identified at the microscale. However, it is currently difficult to experimentally measure local damage properties and isolate their effect on the tissue fracture resistance. Instead, computer models can be used to analyze the impact of local characteristics and structures, but material parameters required in computer models are not well established. The aim of this study was therefore to identify the material parameters that are important for crack propagation in cortical bone and to elucidate what parameters need to be better defined experimentally. A comprehensive material parameter study was performed using an XFEM interface damage model in 2D to simulate crack propagation around an osteon at the microscale. The importance of 14 factors (material parameters) on four different outcome criteria (maximum force, fracture energy, crack length and crack trajectory) was evaluated using ANOVA for three different osteon orientations. The results identified factors related to the cement line to influence the crack propagation, where the interface strength was important for the ability to deflect cracks. Crack deflection was also favored by low interface stiffness. However, the cement line properties are not well determined experimentally and need to be better characterized. The matrix and osteon stiffness had no or low impact on the crack pattern. Furthermore, the results illustrated how reduced matrix toughness promoted crack penetration of the cement line. This effect is highly relevant for the understanding of the influence of aging on crack propagation and fracture resistance in cortical bone.

     

The role of the lamellar interface during torsional yielding of human cortical bone

Fragility fractures are a result of alterations in bone quantity, tissue properties, applied loads, or a combination of these factors. The current study addresses the contribution of cortical bone tissue properties to skeletal fragility by characterizing the shear damage accumulation processes which occur during torsional yielding in normal bone. Samples of human femoral cortical bone were loaded in torsion and damaged at a post-yield twist level. The number of microcracks within osteons, interstitial tissue, and along cement lines were assessed using basic fuchsin staining. Damage density measures (number of cracks/mm2) were correlated with stiffness degradation and changes in relaxation. Damaged samples exhibited a wide variation in total microcrack density, ranging from 1.1 to 43.3 cracks/mm2 with a mean density of 19.7 +/- 9.8 cracks/mm2. Lamellar interface cracks comprised more than 75% of the total damage, indicating that the lamellar interface is weak in shear and is a principal site of shear damage accumulation. Damage density was positively correlated with secant stiffness degradation, but only explained 22% of the variability in degradation. In contrast, damage density was uncorrelated with the changes in relaxation, indicating that a simple crack counting measure such as microcrack density was not an appropriate measure of relaxation degradation. Finally, a nonuniform microcrack density distribution was observed, suggesting that internal shear stresses were redistributed within the torsion samples during post-yield loading. The results suggested that the lamellar interface in human cortical bone plays an important role in torsional yielding by keeping cracks physically isolated from each other and delaying microcrack coalescence in order to postpone the inevitable formation of the fatal crack.     

Geometric determinants to cement line debonding and osteonal lamellae failure in osteon pushout tests

Cement lines are the boundaries between secondary osteons and the surrounding interstitial bone matrix in cortical bone. The interfacial properties of cement lines have been determined by osteon pushout tests. However, distinctively different material properties were obtained when osteon pushout tests were performed under different test geometries. In the present study, an axisymmetric two-dimensional finite element model was used to simulate an osteon pushout test using the test geometry of actual experiments. The results indicated that shear failure within the osteonal lamellae would occur when the osteon pushout test was performed under the condition of a thick specimen and large supporting hole. On the other hand, cement line debonding occurred when the osteon pushout test was performed using a thin specimen and small supporting hole. The finite element results were consistent with previous experiments of osteon pushout tests under different test geometries. Furthermore, the finite-element results suggest that a smoothly curved punch would most likely cause debonding at the cement line instead of osteonal lamellae.     

The effect of cement creep and cement fatigue damage on the micromechanics of the cement–bone interface

The cement–bone interface provides fixation for the cement mantle within the bone. The cement–bone interface is affected by fatigue loading in terms of fatigue damage or microcracks and creep, both mostly in the cement. This study investigates how fatigue damage and cement creep separately affect the mechanical response of the cement–bone interface at various load levels in terms of plastic displacement and crack formation. Two FEA models were created, which were based on micro-computed tomography data of two physical cement–bone interface specimens. These models were subjected to tensile fatigue loads with four different magnitudes. Three deformation modes of the cement were considered: ‘only creep’, ‘only damage’ or ‘creep and damage’. The interfacial plastic deformation, the crack reduction as a result of creep and the interfacial stresses in the bone were monitored. The results demonstrate that, although some models failed early, the majority of plastic displacement was caused by fatigue damage, rather than cement creep. However, cement creep does decrease the crack formation in the cement up to 20%. Finally, while cement creep hardly influences the stress levels in the bone, fatigue damage of the cement considerably increases the stress levels in the bone. We conclude that at low load levels the plastic displacement is mainly caused by creep. At moderate to high load levels, however, the plastic displacement is dominated by fatigue damage and is hardly affected by creep, although creep reduced the number of cracks in moderate to high load region.     

Improvement of mechanical properties of acrylic bone cement by fiber reinforcement

Acrylic bone cement is significantly weaker and less stiff than compact bone. Bone cement is also weaker in tension than in compression. This limits its use in orthopaedics to areas where tensile stresses are minimum. We have attempted to improve the mechanical properties of PMMA by reinforcing it with metal wires, and graphite and aramid fibers. Normal, carbon fiber reinforced and aramid fiber reinforced bone cement specimens were tested in compression. Addition of a small percentage (1-2% by weight for carbon and up to 6% for aramid) of these fibers improved the mechanical properties significantly. Due to the improved mechanical properties of fiber reinforced bone cement, its clinical use may reduce the incidence of cement fracture and thus loosening of the prosthesis.     

Osteonal effects on elastic modulus and fatigue life in equine bone

We hypothesized that recently formed, incompletely mineralized, and thus, relatively deformable osteons in the equine third metacarpus enhance in vitro load-controlled fatigue life in two ways. Macroscopically, there is a compliance effect, because reduced tissue elastic modulus diminishes the stress required to reach a given strain. Microscopically, there is a cement line effect, in which new osteons and their cement lines more effectively serve as barriers to crack propagation. We studied 18 4 x 10 x 100 mm beams from the medial, lateral, and dorsal cortices of metacarpal bones from 6 thoroughbred racehorses. Following load-controlled fatigue testing to fracture in 4 point bending, a transverse, 100 microm thick, basic fuchsin-stained cross-section was taken from the load-bearing region. The number and diameter of all intact (and thus recently formed/compliant) secondary osteons in a 3.8 x 3.8 mm region in the center of the section were determined. The associated area fraction and cement line length of intact osteons were calculated, and the relationships between these variables, elastic modulus (E), and the logarithm of fatigue life (logN(F)) were analyzed. As expected, logN(F) was negatively correlated with E, which was in turn negatively correlated with intact osteon area fraction and density. (LogN(F))/E increased in proportion to intact osteon density and nonlinearly with cement line density (mm/mm(2)). These results support the hypothesis that remodeling extends load-controlled fatigue life both through the creation of osteonal barriers to microdamage propagation and modulus reduction.     

Age-related properties at the microscale affect crack propagation in cortical bone

The increased risk for fracture with age is associated not only with reduced bone mass but also with impaired bone quality. At the microscale, bone quality is related to porosity, microstructural organization, accumulated microdamage and intrinsic material properties. However, the link between these characteristics and fracture behavior is still missing. Bone tissue has a complex structure and as age-related compositional and structural changes occur at all hierarchical length scales it is difficult to experimentally identify and discriminate the effect of each mechanism. The aim of this study was therefore to use computational models to analyze how microscale characteristics in terms of porosity, intrinsic toughness properties and microstructural organization affect the mechanical behavior of cortical bone. Tensile tests were simulated using realistic microstructural geometries based on microscopy images of human cortical bone. Crack propagation was modelled using the extended finite element method where cement lines surrounding osteons were modelled with an interface damage law to capture crack deflections along osteon boundaries. Both increased porosity and impaired material integrity resulted in straighter crack paths with cracks penetrating osteons, similar to what is seen experimentally for old cortical bone. However, only the latter predicted a more brittle failure behavior. Furthermore, the local porosity influenced the crack path more than the macroscopic porosity. In conclusion, age-related changes in cortical bone affect the crack path and the mechanical response. However, increased porosity alone was not driving damage in old bone, but instead impaired tissue integrity was required to capture brittle failure in aging bone.     

Surface pretreatment for prolonged survival of cemented tibial prosthesis components: full- vs. surface-cementation technique]

Aseptic loosening of tibial components due to degradation of the interface between bone cement and metallic tibial shaft component is still a persistent problem, particularly for surface-cemented tibial components. The surface cementation technique has important clinical meaning in case of revision and for avoidance of stress shielding. This study was done to prove crack formation in the bone cement near the metallic surface when this is not coated. We propose a newly developed coating process by SiOx-PVD layering to avoid crack formation. A biomechanical model for a vibration fatigue test was done to prove that crack formation can be significantly reduced in the case of coated surfaces. It was found that coated tibial components showed a highly significant reduction of cement cracking near the metal/bone cement interface (p < 0.01) and a significant reduction of gap formation in the metal-to-bone cement interface (p < 0.05). Coating dramatically reduces hydrolytic- and stress-related crack formation at the prosthesis metal/bone cement interface. This leads to a more homogenous load transfer into the cement mantle which should reduce the frequency of loosening in the metal/bone cement/bone interfaces. With surface coating of the tibial component it should become possible that surface-cemented TKAs reveal similar loosening rates as TKAs both surface- and stem-cemented. This would be an important clinical advantage since it is believed that surface cementing reduces metaphyseal bone loss in the case of revision and stress shielding for a better bone health.     

Secondary osteon size and collagen/lamellar organization (“osteon morphotypes”) are not coupled,but potentially adapt independently for local strain mode or magnitude

In bone, matrix slippage that occurs at cement lines of secondary osteons during loading is an important toughening mechanism. Toughness can also be enhanced by modifications in osteon cross-sectional size (diameter) for specific load environments; for example, smaller osteons in more highly strained “compression” regions vs. larger osteons in less strained “tension” regions. Additional osteon characteristics that enhance toughness are distinctive variations in collagen/lamellar organization (i.e., “osteon morphotypes”). Interactions might exist between osteon diameter and morphotype that represent adaptations for resisting deleterious shear stresses that occur at the cement line. This may be why osteons often have a peripheral ring (or “hoop”) of highly oblique/transverse collagen. We hypothesized that well developed/distinct “hoops” are compensatory adaptations in cases where increased osteon diameter is mechanically advantageous (e.g., larger osteons in “tension” regions would have well developed/distinct “hoops” in order to resist deleterious consequences of co-existing localized shear stresses). We tested this hypothesis by determining if there are correlations between osteon diameters and strongly hooped morphotypes in “tension”, “compression”, and “neutral axis” regions of femora (chimpanzees, humans), radii (horse, sheep) and calcanei (horse, deer). The results reject the hypothesis—larger osteons are not associated with well developed/distinct “hoops”, even in “tension regions” where the effect was expected to be obvious. Although osteon diameter and morphotype are not coupled, osteon diameters seem to be associated with increased strain magnitudes in some cases, but this is inconsistent. By contrast, osteon morphotypes are more strongly correlated with the distribution of tension and compression.     

The effect of moisture absorption on the fatigue crack propagation resistance of acrylic bone cement.

In vivo, bone cement is subject to cyclic loading in a fluid environment. However, little is known about the effect of moisture absorption on the fatigue crack propagation resistance of bone cement. The effect of moisture absorption at 37 degrees C on the fatigue crack propagation resistance of a common bone cement (Endurance, DePuy, Orthopaedics, Inc.) was examined. Preliminary fracture toughness tests were conducted on disk-shaped, vacuum-mixed cement specimens (compact tension type) that were cyclically pre-cracked. Plain-strain fracture toughness K(IC) (MPa square root(m)) was determined. To study the effect of moisture absorption four treatment groups, with different soaking periods in Ringer's at 37 degrees C, of Endurance cement were tested. The specimens weights prior to and following soaking showed a significant increase in mean weight for specimens soaked for 8 and 12 weeks. Linear regression analysis of log(da/dN) vs. log (deltaK) was conducted on the combined data in each fatigue test group. Soaking bone cement in Ringer's at 37 degrees C for 8 and 12 weeks lead to an improvement in fatigue crack propagation resistance, that may be related to water sorption that increases polymer chain mobility, with enhanced crack tip blunting. It may be more physiologically relevant to conduct in vitro studies of fatigue and fracture toughness of bone cements following storage in a fluid environment.     

A model of tension and compression cracks with cohesive zone at a bone-cement interface

This paper gives an insight about compression and tension cracks as encountered at a bone-cement interface. Within the context of continuum theory of fracture, an analytical solution is presented for the problem of a bimaterial interface edge crack under uniaxial tension or compression, assuming no tangential slip along the crack faces since cement pedicles penetrate into the cancellous bone several millimeters. Also essential to the solution are cohesive zone effects that account for a strengthening mechanism over the crack faces. The solution provides a methodological framework for quantifying the influence of the cohesive zone on the magnitude of the stress singularity. Mode I crack tip stress intensity factors are calculated at different stages of the loading and unloading phases under uniaxial tension or compression. Finally, an inelastic mechanism is presented that gives theoretical support to explain the formation of interfacial compression cracks, a phenomenon that was not previously appreciated and that arises from the rigid cement being forced into the more compliant cancellous bone.     

Distribution of osteonic and interstitial components in the human femoral shaft with reference to structure, calcification and mechanical properties

This paper analyzes the distribution of osteons and interstitial bone in the femoral compacta according to their structure, degree of calcification and mechanical properties. Three cross sections, 100 microns thick, each located 1 cm from the next, were prepared by grinding from the middle third of a human femoral shaft. Starting from the premise that, in lamellar bone, lamellae whose fiber bundles and crystallites have a longitudinal course withstand loading by tension, whereas those whose fiber bundles and crystallites have a transversal course withstand loading by compression, each osteon and fragment of interstitial bone has been given a number recording the percentage of its surface consisting of lamellae with transversally oriented fiber bundles and crystallites (bright under the polarizing microscope). The degree of calcification of the same structures was determined micro-radiographically. The distribution of both osteons and interstitial bone was assessed using a tungsten grid for reference. The total surface of each bone microstructure, and the percentage of that surface consisting of bright lamellae, were all calculated using a Zeiss Video-plan. Our results confirm the view that the distribution of both osteons and interstitial bone is mainly related to their structure--and hence to their mechanical properties. In addition, bone remodeling seems to be most active in areas capable of supporting tensile stress.     

Osteon interfacial strength and histomorphometry of equine cortical bone

The interfacial strength of secondary osteons from the diaphysis of the Thoroughbred equine third metacarpal was evaluated using the fiber pushout test. The pushout was performed on 300-500 microm sections of 4x4x15 mm bone blocks machined from four anatomic regions of the cortex. Pushout strength was evaluated from proximal to distal location within the diaphysis on four osteon types classified under polarized light on adjacent histologic sections from each block. The shear strength of the interfaces were estimated from shear lag theory. Differences were found in the interfacial strength of osteons based on appearance under polarized light with bright field having the highest interfacial strength (40.3 MPa). The lowest strength was found in the dark field osteons (22.8 MPa). The dorsal region had the highest shear strength and toughness compared to all other regions. The cement line and interlamellar interfaces are similar in strength, but exhibit regional dependence--specifically, the palmar region strength is less (17.5 MPa) than the osteon interlamellar interfaces (30.4 MPa) and osteon type dependent (alternating significantly weaker than other types). Histomorphometry revealed significant regional differences (p<0.0001) in osteon area fraction among the four osteon types as well as differences in the osteon diameter (p=0.01), with dorsal regions having larger osteons (170 microm) than the palmar region (151 microm). Fatigue life and fracture toughness of Haversian bone are reported in the literature to be regionally dependent and are known to be associated with osteon pullout--an osteon interfacial phenomenon. Therefore, the results presented in this study are important to further the understanding of the mechanisms of fragility and damage accumulation in cortical bone.     

Fatigue creep damage at the cement–bone interface: An experimental and a micro-mechanical finite element study

The goal of this study was to quantify the micromechanics of the cement–bone interface under tensile fatigue loading using finite element analysis (FEA) and to understand the underlying mechanisms that play a role in the fatigue behavior of this interface. Laboratory cement–bone specimens were subjected to a tensile fatigue load, while local displacements and crack growth on the specimen's surface were monitored. FEA models were created from these specimens based upon micro-computed tomography data. To accurately model interfacial gaps at the interface between the bone and cement, a custom-written erosion algorithm was applied to the bone model. A fatigue load was simulated in the FEA models while monitoring the local displacements and crack propagation. The results showed the FEA models were able to capture the general experimental creep damage behavior and creep stages of the interface. Consistent with the experiments, the majority of the deformation took place at the contact interface. Additionally, the FEA models predicted fatigue crack patterns similar to experimental findings. Experimental surface cracks correlated moderately with FEA surface cracks (r²=0.43), but did not correlate with the simulated crack volume fraction (r²=0.06). Although there was no relationship between experimental surface cracks and experimental creep damage displacement (r²=0.07), there was a strong relationship between the FEA crack volume fraction and the FEA creep damage displacement (r²=0.76). This study shows the additional value of FEA of the cement–bone interface relative to experimental studies and can therefore be used to optimize its mechanical properties.     

The system of bony canals as the basis for the angioarchitectonics of bones]

The spatial interrelationships of osteon canals were studied in corrosion preparations with the help of rastral electron microscopy. The structure of microvessels, their belonging to a definite link of the microcirculatory bed, the interaction of vessels and their position with respect to the osseous matrix were studied in bone sections impregnated with silver nitrate after V. V. Kuprijanov. Haversian canals in the compact substance of the bone are longitudinally oriented, can duplicate and form a single system of canals. The neighbouring canals of osteons might be bound by means of Volkmann's canals. The investigation of the Haversian canals in serial sections has shown that the diameter of the same canals of osteons can change at different levels, the diameter of the osteons themselves remaining unchanged. This seems to speak of uneven development of osteons in their different parts. In the Haversian canal there are one-two or occasionally three vessels having all three links of the morphocirculatory bed. The course and ramification of the vessel are identical to the shape of the osteon canal which includes them. The vessels are closely connected with the bony matrix by means of connective tissue bundles directed from the canal wall to the vessel wall. These bundles appear to serve as a peculiar anchor or amortizing apparatus and its elasticity might be a factor of a change of the shape and direction of the canal vessels in the bone development process.     

Anisotropy of age-related toughness loss in human cortical bone: a finite element study

A mechanistic understanding of the role of bone quality on fracture processes is essential for determining the underlying causes of age-related changes in the mechanical response of the human bone. In this study, a previously developed cohesive finite element model was used to investigate the effects of age-related changes and the orientation of crack growth on the toughening behavior of human cortical bone. The change in the anisotropy of toughening mechanisms with age was also studied. Finite element method (FEM) simulations showed that the initiation toughness decreased by 3% and 8%/decade for transverse and longitudinal crack growth, respectively. In contrast, fracture resistance curve slope for transverse and longitudinal crack growth decreased by 2% and 3%/decade, respectively. Initiation fracture toughness values were higher for the transverse than for the longitudinal for a given age. On the other hand, propagation fracture toughness values were higher for longitudinal than for transverse crack growth for a given age. With respect to age, the toughness ratio for crack initiation decreased by 6%/decade, but that for propagation showed almost no change (less than 1%). In light of these findings, an analytical model evaluating the crack arresting feature of cement lines, is proposed to explain the factors that determine crack penetration into osteons or its deflection by cement lines.     

Microscopic fracture aspects of impact tested human bones

The fracture aspects of impact twisted human femurs and tibias have been studied in their wet condition. The main tool used to correlate fracture behaviour with bone structure was the scanning electron microscope. Supplementary data were obtained from macroscopic fracture pattern analyses and stress coat experiments on slowly tested dried bone. The interest of the data reported concerns two major points. Firstly the analysis of the fractographic results leads to the conclusion that the fracture has presumably been initiated by shearing parallel with the torsion axis. The fracture propagates along so called spiral and oblique fracture lines. Secondly, the correlation of the macroscopic fracture pattern with microscopic fracture aspects indicates that the fracture is initiated along the cement lines, which can be considered as the weak matrix in an osteon-cement lining composite. The fracture propagates along the cement lines as well as through osteons and lamellae. Throughout the impact fracture surfaces ductile and brittle fracture aspects were observed, although the brittle fracture mode was predominant during propagation.